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Properties of temporomandibular joint nociceptors in normal and inflamed tissue

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Title:
Properties of temporomandibular joint nociceptors in normal and inflamed tissue
Creator:
Loughner, Barry Allen, 1943-
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English
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xi, 130 leaves : ill. ; 29 cm.

Subjects

Subjects / Keywords:
Asymptotes ( jstor )
Capsules ( jstor )
Jaw ( jstor )
Knee joint ( jstor )
Nerves ( jstor )
Nociceptors ( jstor )
Pain ( jstor )
Reactivity ( jstor )
Temporomandibular joint ( jstor )
Velocity ( jstor )
Department of Oral Biology thesis Ph.D ( mesh )
Dissertations, Academic -- College of Dentistry -- Department of Oral Biology -- UF ( mesh )
Nociceptors -- physiology ( mesh )
Temporomandibular Joint -- physiology ( mesh )
Genre:
bibliography ( marcgt )
theses ( marcgt )
non-fiction ( marcgt )

Notes

Thesis:
Thesis (Ph. D.)--University of Florida, 1992.
Bibliography:
Includes bibliographical references (leaves 118-129).
Additional Physical Form:
Also available online.
General Note:
Typescript.
General Note:
Vita.
Statement of Responsibility:
by Barry Loughner.

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University of Florida
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University of Florida
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Copyright [name of dissertation author]. Permission granted to the University of Florida to digitize, archive and distribute this item for non-profit research and educational purposes. Any reuse of this item in excess of fair use or other copyright exemptions requires permission of the copyright holder.
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27245086 ( OCLC )
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RK470 .L68 1992 ( lcc )

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PROPERTIES OF TEMPOROMANDIBULAR JOINT NOCICEPTORS
IN NORMAL AND INFLAMED TISSUE













BY


BARRY LOUGHNER


A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL
OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT
OF THE REQUIREMENTS FOR THE DEGREE OF
DOCTOR OF PHILOSOPHY


UNIVERSITY OF FLORIDA


1992




























I dedicate this work to my daughter, Carina Beth.














ACKNOWLEDGEMENTS


I thank Dr. Brian Cooper, Ph.D., for his technical guidance in the research

involved in this dissertation. I thank Ms. Martha Oberdorfer for her technical assistance. I

thank Dr. Parker Mahan, D.D.S., Ph.D., and Dr. Arnold S. Bleiweis, Ph.D. for their

strategic guidance. I thank Dr. Robert Bates, D.D.S., M.S. for his administrative

assistance.













TABLE OF CONTENTS


LIST OF TABLES ...........................................................................

LIST OF FIGURES .........................................................................

KEY TO SYMBOLS ........................................................................

ABSTRACT ...................................................................................

CHAPTERS

1 INTRODUCTION .............................................................

2 METHODS ......................................................................
Subjects ......................................................................
Exposure of the TMJ and Trigeminal Ganglion .......................
Recording Procedures .....................................................
Characterization of TMJ Afferents .......................................
Statistics ................................................................... *
Experimental Inflammation ................................................

3 RESULTS ......................................................................
Identification of TMJ Nociceptors ......................................
Characterization of TMJ Nociceptors in Normal Tissue ..............
Properties of TMJ Nociceptors in Inflamed Tissue .....................
Experiment I: Properties of units in the Previously Inflamed TMJ...
Experiment II: Properties of Units in the Acutely Inflamed TMJ .....

4 DISCUSSION ..................................................................
Sensitization of TMJ Nociceptors ........................................
Factors Contributing to Sensitization .....................................

APPENDICES

A DEVELOPMENT AND MAINTENANCE OF TMJ PAIN ..............

B PSYCHOPHYSICS OF TMJ DISORDERS ................................

C NEUROANATOMY OF THE TMJ .........................................

D CENTRAL REPRESENTATION OF TMJ AFFERENTS ................

E TRIGEMINAL GANGLION ..................................................

F GROSS ANATOMY ...........................................................








G SUMMARY TABLES OF TMJ REACTIVITY .................. 90

LIST OF REFERENCES ......................................................... 118

BIOGRAPHICAL SKETCH .................................................... 130














LIST OF TABLES


Table 3-1

Table 3-2


Table 3-3

Table 3-4



Table 3-5

Table G-l 1

Table G-2

Table G-3

Table G-4


Table G-5

Table G-6

Table G-7

Table G-8

Table G-9

Table G-10


Table G-1 I


Table G-12


Table G-13


TMJ force/movement relationships in the vertical plane......................

Properties on nociceptors that demonstrate vertical plane or horizontal
plane reactivity ..................................................................

Mean values of properties of TMJ nociceptors ...............................

Qualitative improvements in reactivity for nociceptors that were
characterized in normal tissue and then tested again subsequent to
carrageenan injection ...........................................................

Changes in reactivity for 8 units after exposure to saline ..................

Reactivity in vertical plane (normal tissue) ..................................

Reactivity in horizontal plane (normal tissue), left lateral ................

Reactivity in horizontal plane (normal tissue), right lateral ................

Reactivity in the vertical plane in previously inflamed tissue. Reactivity
in horizontal plane in previously inflamed tissue, left lateral ..............

TMJ nociceptor reactivity in normal tissue, vertical plane ................

TMJ nociceptor reactivity in normal tissue, horizontal plane ..............

TMJ nociceptor reactivity in previously inflamed tissue ...................

TMJ nociceptor reactivity in acutely inflamed tissue .......................

TMJ nociceptor reactivity in saline injected tissue .........................

Effect of canrrageenan in acutely inflamed tissue reactivity in the vertical
plane, unit #1 ....................................................................

Effect of carrageenan in acutely inflamed tissue reactivity in the vertical
plane, unit #2 ....................................................................

Effect of carrageenan in acutely inflamed tissue reactivity in the vertical
plane, unit #3 ....................................................................

Effect of carrageenan in acutely inflamed tissue reactivity in the vertical
plane, unit #4 ....................................................................


25


28

37



46

51

91

92

93


94

95

96

97

98

99


100


101


102


103








Table G-14


Table G-15


Table G-16


Table G-17


Table G-18


Table G-19


Table G-20


Table G-21

Table G-22

Table G-23

Table G-24

Table G-25

Table G-26

Table G-27


Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal
plane, unit #1 .................................................................... 104

Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal
plane, unit #2 ................................................................... 105

Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal
plane, unit #3 ................................................................... 106

Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal
plane, unit #4 .................................................................... 107

Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal
plane, unit #5 .................................................................... 108

Effect of can-rrageenan in acutely inflamed tissue reactivity in the horizontal
plane, unit #6 .................................................................... 109
Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal
plane, unit #7 .................................................................... 110

Effect of saline reactivity in the horizontal plane, unit #1 ................... I11

Effect of saline reactivity in the horizontal plane, unit #2 ................... 112

Effect of saline reactivity in the horizontal plane, unit #3 ................... 113

Effect of saline reactivity in the horizontal plane, unit #4 ................... 114

Effect of saline reactivity in the horizontal plane, unit #6 ................... 115

Effect of saline reactivity in the horizontal plane, unit #7 ................... 116

Effect of saline reactivity in the horizontal plane, unit #8 ................... 117








LIST OF FIGURES

Figure 2-1 Mandibular movements were produced by a hand held probe ............ 8

Figure 2-2 Dynamic and static test series for force, displacement and velocity ...... 10

Figure 2-3 Demonstration of sensitization as a shift of stimulus-response functions.. 14

Figure 3-1 Receptive field distribution in the lateral and posterior capsule of the
temporomandibular joint for normal tissue .................................. 18

Figure 3-2 Receptive field distribution in the lateral and posterior capsule of
the temporomandibular joint for previously inflamed tissue, acutely
inflamed tissue and saline control tissue ...................................... 20

Figure 3-3 Relationships between applied force and vertical plane movements of
the m andible ................................................................ 23-24

Figure 3-4 Dynamic reactivity in normal tissue .......................................... 30

Figure 3-5 Dynamic reactivity in previously inflamed tissue ......................... 33

Figure 3-6 Averaged dynamic response functions of nociceptors fitted in normal
and previously inflamed tissue ................................................ 41

Figure 3-8 Reactivity of nociceptors exposed to saline ................ ................ 43

Figure 3-9 Comparison between pre-inflamed and post-inflamed reactivity in
scatter plot forms ......................................................... 48-49

Figure F-l Schematic diagram of the human temporomandibular joint. Sagittal and
frontal views .................................................................... 87














KEY TO SYMBOLS

* Vertical plane or previously inflamed tisue.

A Horizontal plane or acutely inflamed tissue.

+ Saline control tissue.














Abstract of Dissertation Presented to the Graduate School
of the University of Florida in Partial Fulfillment of the
Requirements for the Degree of Doctor of Philosophy

PROPERTIES OF TEMPOROMANDIBULAR JOINT NOCICEPTORS
IN NORMAL AND INFLAMED TISSUE

By

Barry Loughner

May, 1992



Chairman: Parker Mahan, D.D.S., Ph.D.
Cochairman: Brian Cooper, Ph.D.
Major Department: Oral Biology


Mechanical response properties of nociceptors of the goat temporomandibular joint

(TMJ) were characterized by unit recordings from the trigeminal ganglion. Populations of

afferents were sampled in normal tissue and in tissue previously inflamed (PI) with

carrageenan for at least 6 hours prior to testing. In other experiments, nociceptors were

characterized in normal tissue and then retested for up to 3 hrs subsequent to exposure to

carrageenan (AI). To produce mandibular movement in the vertical and horizontal planes,

dynamic and static forces were applied to the mandibular pole. Stimuli were quantified by

force and angular displacement transducers. Receptive fields were small, single spots (2-3

mm) and located on the lateral or posterior capsule of the TMJ. Conduction velocities were

shown to be in the group III and IV range. Stimulus-interval data was best described by

power functions. Assessment of force-movement relationships indicated that capsular

nociceptors responded exclusively to intense forces that produce extreme displacements of

the mandible.









In normal tissue, 24 of 36 nociceptors transduced dynamically applied stimuli

(mean activation threshold for dynamic force = 15.9 + 11.3 N and for force velocity =

17.3 + 18.9 N/s). Relatively fewer units transduced static force (8/36) or position

(1/36).

In PI conditions, tests revealed enhanced reactivity for dynamically applied

stimuli. Mean power functions for dynamic tests in PI conditions (LnISI = -1.3 LnF +

7.3) had steeper slopes compared to those in normal tissue (LnISI = -1.1 LnF + 5.4)

and were shifted graphically to regions indicating greater reactivity (below and to the

left of those in normal tissue). These shifts were suggestive of sensitization.

In AI conditions, 8 of 11 nociceptors acquired either dynamic or static coding

ability. Acquired coding ability also appeared in nociceptors (n = 2) that were without

transducing capacity in normal tissue. Acquired reactivity for vertical plane movement

was also seen for those nociceptors (n = 3) that were reactive only to movement in the

horizontal plane in normal tissue. Acquisition of coding ability following carrageenan-

induced inflammation suggested afferent sensitization.













CHAPTER 1


INTRODUCTION



The temporomandibular joint (TMJ) is the site of a number of disorders that burden

the health care system and extract a large cost in human suffering (Helkimo, 1979; Solberg,

1987). Afferent groups presumed to mediate TMJ pain are likely to play a role in a variety

of TMJ disorders. Many theories have been proposed to explain TMJ pain and dysfunction

(Deboever, 1973; Dubner et al., 1978, Yemm, 1979). These theories propose both intra-

and extra-articular origins of TMJ pain. Intra-articular theories argue that pressure or

tension on articular tissues results in TMJ pain. Extra-articular theories propose that

muscles or other contiguous structures refer pain to the TMJ (see Appendix A).

Fundamental to an evaluation of intra-articular theories is an understanding of the response

properties of TMJ nociceptors.

Our understanding of nociceptors innervating articular tissues has been advanced in

recent years (Schaible and Schmidt, 1983a, b, 1988b; Guilbaud et al., 1985; Birrell et al.,

1990). Most detailed information concerning the response properties of joint nociceptors

has come from studies of the cat knee and rat ankle joint. While there is considerable

information regarding the neuroanatomy of the TMJ (see Appendix C), little is known

about the physiology of nociceptors of the temporomandibular joint.

Early studies examining properties of afferents innervating the cat knee joint

reported activation of slowly conducting, myelinated fibers only by forceful rotational

movements beyond the physiological range of motion (Burgess and Clark, 1969; Clark and

Burgess, 1975). In contrast, Schaible and Schmidt (1983b) identified populations of









small fibers that were activated by passive movement of the knee joint, both within and

beyond the normal range of motion. These afferents were categorized into four populations

on the basis of their response range. Afferents of populations I and II responded to

innocuous joint movement in the normal range of motion, but population II responded best

to forceful rotation. Population III units were activated exclusively by forceful movement

and population IV had no response to movement. Based on movement sensitivity,

afferents that responded within the normal range of motion were not considered

nociceptors, while those that respond beyond the normal range were nociceptors.

Subsequent studies by Schaible and Schmidt (1985, 1988b) concentrated on populations

HIII and IV. However, despite the importance of range for classifying afferents, distinctions

between normal and non-normal ranges have been ancedotal. Quantification of the

relationship between range of motion and afferent activity is still pending.

There are no studies that have examined properties of TMJ nociceptors. Previous

reports have examined the discharge characteristics of afferent traffic in the

auriculotemporal nerve that may contribute to position sense and control of mandibular

movement (Kawamura et al., 1967; Klineberg et al, 1970, 1971; Kawamura and Abe,

1974; Lund and Matthews, 1981). While TMJ nociceptors may have properties similar to

those described for cat knee joint, there are considerable functional and anatomical

differences between these two joints that indicate that properties of TMJ nociceptors should

be determined (see Appendices C and F).

Changes in the properties of TMJ nociceptors (sensitization) may account for some

of the symptoms of TMJ dysfunction. These symptoms include pain during mandibular

movement, pain on local joint palpation, and tonic pain. Changes in nociceptor properties

are likely to be necessary to the development of these forms of pain. As pain on movement

is a primary symptom of TMJ dysfunction, a precise determination of the relationship

between movement and afferent discharges is valuable. Quantification of force and

movement also permits more direct specifications of movements which are outside the









normal range of motion, and identification of afferents that respond specifically in these

ranges.

Sensitization of TMJ receptors may be an important defense mechanism that

protects the joint from excessive movement which may cause injury. The TMJ is often the

site of inflammations associated with various forms of TMJ dysfunction (e.g. arthritis and

synovitis). An understanding of how inflammation may modify TMJ afferent function

would reveal the form and range of TMJ afferent sensitization and lead to a better

understanding of both etiology and treatment.

Sensitization of nociceptors has been documented in the cat knee joint (Coggeshall

et al., 1983; Schaible and Schmidt, 1985, 1988b; Grigg et al., 1986) and in the rat ankle

joint (Guilbaud et al., 1985) following chemically-induced acute or chronic arthritis. Acute

arthritis in the cat knee joint, induced by carrageenan and kaolin, produced changes in the

discharge properties in joint afferents. These changes include an increase in the proportion

of small fibers that could be activated by innocuous joint movement, recruited units, and

the appearance of spontaneous activity. Studies of sensitization of TMJ nociceptors may

provide uniquely important information regarding short and long term changes occurring in

TMJ afferents following local trauma, arthritis or chronic disc displacement.

In the following experiments, we examined properties of TMJ nociceptors in both

normal and inflamed tissue of the goat. The goat is an excellent model for TMJ physiology

because of functional and structural similarities to humans including range of motion and

innervation of the auriculotemporal nerve. (See Appendices C and F).














CHAPTER 2


METHODS



Subjects


Experiments were performed on 59 goats, ages 6- 12 months and weighing 30 60

lbs. All goats were kept in pens at the veterinary hospital. Goat health was monitored and

maintained by animal care technicians, veterinary staff and faculty. All procedures were

approved by an internal review board (protocol 7136).


Exposure of the TMJ and Trigeminal Ganglion


Rompun (3 mg/kg) and Ketamine (11 mg/kg) were given as preanesthetics.

Anesthesia was induced with a-chloralose (7.5 mg/ml) via a lactated ringers drip. If

necessary, pentabarbitol was periodically administered intravenously to maintain deep

anesthesia. Goats were artificially respirated at a rate of 10-20 breaths per minute. Blood

pressure, body temperature and end-tidal CO2 were continuously monitored and maintained

within physiological limits. At the conclusion of each experiment, the goats were

euthanized with saturated KCL.

To expose the right TMJ, the skin was removed from the lateral posterior aspect of

the face. The parotid gland, pinna and the zygomaticoauricularis muscles were removed to

access the posterior portion of the TMJ capsule. The styloid process and associated

muscular and ligamentous attachments were clipped off at the sphenoid bone. The origin of









the sternomastoid and caudal digastric muscles were excised from the mastoid process and

jugular process of the occiput, respectively. The sphenomandibular ligament and fatty

tissues were removed. Care was taken to preserve the microvasculature of the TMJ

capsule. The exposed capsular tissue was kept moist by repeated applications of

physiological saline.

Several nerves were cut distal to the trigeminal ganglion in order to avoid recording

activity other than TMJ afferents. The buccinator nerve was severed as it passed the

anterior border of the masseter muscle. The masseteric nerve was cut as it entered the deep

and superficial masseter muscle. The posterior trunk of the mandibular nerve was cut distal

to the branching of the auriculotemporal nerve. As a consequence, afferents of the lingual,

inferior alveolar and mylohyoid nerves were eliminated.

The trigeminal ganglion was accessed via its position caudal to the foramen ovale.

Removal of the thin, lateral plate of bone of the tympanic bulla and the tympanic plate

exposed the ossicles of the middle ear and internal surface of the tympanic membrane.

Removal of the inferior aspect of the greater wing of the sphenoid and the inferior aspect of

the petrous bone exposed the caudal surface of the trigeminal ganglion. Access to the

ganglion is improved by removing the sphenomandibular ligament and fatty tissue in the

infratemporal fossa.



Recording Procedures


Extracellular recordings were made by penetration of the trigeminal ganglion with

tungsten microelectrodes (Microprobe, Inc.) until unit potentials were evoked by passive

jaw movement. Most units were found in the posterior region of the trigeminal ganglion.

(See Appendix E). Receptive fields were then identified on the lateral or posterior capsule

of the TMJ. Amplified output was led to and monitored by a digital oscilloscope and an

audio speaker. Data was digitized and stored on video tape (Vetter Instruments, Model No.









3000A). Data were recovered from tape for analysis with an RC computerscope (RC

Electronics) or captured on a line by a thermal printer (Astromed, Dash IV).

After a unit was characterized, the conduction velocity was determined by

measuring the latency of responses to suprathreshold electrical stimulation applied to the

receptive field on the TMJ capsule. Electrical stimulation was performed with a Grass S88

stimulator and isolated, constant current unit. Square-wave pulses of 0.2 to 2 msec

duration were applied with monopolar electrodes. Conduction distance was estimated in

situ.



Characterization of TMJ Afferents



Once an afferent was isolated, passive jaw movements were used to determine

which type of movement was preferred (preferred movements were those which produced
,
the most vigorous response). Jaw movements included: 1) vertical jaw movements from

the closed to the open position. Afferent responses to vertical jaw movements were termed

"vertical plane reactivity" (VP); 2) lateral jaw movements from the closed to extreme lateral

position. Afferent responses to the lateral jaw movements were termed "horizontal plane

reactivity" (HP).

A force probe was used to produce jaw movement. The probe consisted of an axial

force transducer (Entran Instruments, Model ELF TC500-20) embedded in a plexiglass

rod. The transducer monitored forces used to move the jaw in the vertical or horizontal

plane. The probe was applied to fixed points of a bit which was mounted to the incisal

teeth of the mandible at the midline. Force and jaw movement were recorded on video tape

along with afferent activity. Jaw movement was monitored by an angular displacement

transducer (ADT, Trans-Tek Model # 604-001) mounted above the right TMJ (Figure 2-1).

Using the probe, both dynamic and static forces were applied to the mandible (Figure 2-2).

















































Figure 2-1.


Mandibular movements were produced by a hand held probe. Force
applied to the mandible was quantified by a force transducer. Vertical
plane mandibular movement was quantified by an angular displacement
transducer mounted above the right TMJ and attached to the mandibular
pole by a slide assembly. Vertical plane movement of the mandible was
produced by applying force at point A on the jaw movement apparatus.
Horizontal plane movement was produced by applying force at point B.
Afferent recordings were made following exposure and penetration of the
trigeminal ganglion proximal to the foramen ovale.




































Oscilloscope






















































Figure 2-2. Dynamic and static test series for force, displacement and velocity. A)
Dynamic test series. Sawtooth patterns of successively increasing
velocities. B) Static test series. Stepwise pattern of successively
increasing force and displacement.

















TEST FOR DYNAMIC REACTIVITY


UNITS


FORCE (N)


DISPLACEMENT (d"g)


i1 I a -


TIME


TEST FOR STATIC REACTIVITY


UNITS









FORCE (N)







DISPLACEMENT (d"g)


I II i1 H


TIME









Isolated units were characterized by two series of jaw manipulations. The first

series consisted of five tests of reactivity to dynamic force. The first, at a low velocity,

was followed by jaw movements of progressively higher velocities. The range of

velocities was approximately 0.3 to 250.0 N/sec. The second series consisted of five

stepwise, static force applications. Each step was maintained for approximately 2 seconds.

Forces up to 120 N were applied.

To confirm that jaw movement activated afferents of the TMJ capsule, receptive

fields on the capsule were identified and characterized for each case. Thresholds for

activation of mechanosensitive afferents on the capsule of the TMJ were determined by the

bending force of von Frey filaments (monofilament nylon) of different stiffnesses. The

method of limits was used to determine threshold. Nylon probes were applied to the

capsular field until the minimum force required to activate the afferent was determined. In

some cases, no receptive field could be found. This group of cases was treated separately

from afferents with identified receptive fields.



Statistics


Nociceptors were defined as those afferents that responded preferentially to

extremes of jaw movement. Relationships between force applied and jaw movement were

assessed to determine whether the afferents reacted at movement extremes. Force-

movement data was plotted for all units (n = 10) that responded preferentially to vertical

jaw movement and produced significant functions. Momentary relationships between

force, jaw movement and unit activity were determined. Force-interspike interval,

movement-interspike interval and velocity-interspike interval records were fit to linear,

logarithmic, exponential or power functions using simple linear regression (Statistical

Analysis System, SAS). The best fits were determined by comparison of coefficients of

determination.









For analysis of static reactivity, regression data were "segmented and balanced." A

segment (or step) of force was added to the regression model until the coefficient of

determination was maximal. The regression was "balanced" by using only six scores for

each stepwise force segment This procedure avoids weighting the regression differentially

at higher steps, where more scores typically bias the regression. These procedures were

not possible on tests of dynamic force reactivity. Therefore, for dynamic force or

movement tests, all spike intervals were used until a minimum interval was obtained.

Several characteristics of regression lines were subjected to analysis. These

included force-activation thresholds, movement-activation thresholds, force-frequency

asymptotes, movement-frequency asymptotes, mean response intervals, slopes and

intercepts. Force-activation thresholds (FAT) and movement-activation thresholds (MAT)

were defined as the instantaneous force or degree of movement at the first response

interval. Force-frequency asymptotes (FFA) and movement-frequency asymptotes (MFA)

were defined as the force or movement at which the frequency response was maximal (i.e.,

minimum response interval). The FAT or MAT paired with the FFA or FMA were used as

the lower and upper boundary values to plot functions derived from regressions. The mean

response interval (MRI) was calculated from the regression equation by using the mean

force or movement value calculated from the boundary values (FAT + FFA/2 or MAT +

MFA/2). Force-frequency thresholds and movement-frequency thresholds (FFTs and

MFTs) were determined for each unit that was tested for static reactivity. The FFT1' and

MFT were defined as the minimum force or movement which would maintain a sustained

discharge of the afferent. Slopes, intercepts and coefficients of determination were

generated only from significant regressions. Unit reactivity that could not be described by

significant functions were called "non-coding" or "non-transducing" afferents.

"Sensitization" refers to the enhanced excitability ofTMJ afferents that may occur

following carrageenan-induced inflammation. Enhanced excitability is reflected

quantitatively as changes in response properties of TMJ afferents in normal and in inflamed









tissue. Sensitization was assessed qualitatively by comparisons of functions fit to units in

normal and inflamed tissues.

Shifts of stimulus-response coding functions were used as an indication of

enhanced reactivity. Significant functions generated from responses of afferents in

inflamed tissue that were located graphically below and/or to the left of functions fit in

normal tissue were suggestive of sensitization (See Figure 2-3). Significant functions that

were acquired in inflamed tissue but not expressed in normal tissue also were considered to

represent sensitization. Sensitization was assessed quantitatively by statistical comparisons

of function characteristics generated from stimulus tests on units in normal and inflamed

conditions. Function characteristics (slope, intercept, thresholds, asymptotic activity,

coefficients of determination and mean interval) were compared in normal and inflamed

conditions using a one-way ANOVA (Li, 1967) for between subject and t-tests for within

subject's comparisons. Only significant functions contributed to the analysis.


Experimental Inflammation


Inflammation of the TMJ was induced by injection of 200 l of 2% carrageenan

(Sigma Chem.). In some cases, units were characterized in normal tissue and then exposed

to carrageenan. If the receptive field was located on the lateral side of the capsule,

carrageenan was dropped directly onto the receptive field as well as injected into the area of

the receptive field. If the receptive field was located on the posterior side of the capsule,

carrageenan was injected into the area of the receptive field. The remainder of the

carrageenan was injected into the superior joint space. Subsequent testing was performed

after at least 30 minutes and continued for up to 3 hours. In other cases, units characterized

in normal tissue were treated with saline. The injection of saline and subsequent retests

were identical to those used with carrageenan. In other cases, response properties of

separate populations of TMJ afferents were examined only in normal or pre-inflamed


















DEMONSTRATION OF SENSITIZATION
SHIFT OF STIMULUS-RESPONSE CODING FUNCTION
6 Ln interval (nsec)

5

4

3

2


0 . . L . i . . . . . .
0 1 2 3 45

Ln Force O-ewtonrs)
-v Fuiction A -*- Function B
















Figure 2-3. Demonstration of sensitization as a shift of stimulus-response
functions. Shifts of significant stimulus-response functions to graphic
zones of enhanced reactivity (below and to the left) suggests
sensitization. For downward shifts, each point on line B represents a
higher rate of discharge (shorter interval) at an equivalent force. For
leftward shifts, reactivity appears at forces which previously were
ineffective.





15


tissue. In this instance, inflammation was induced at least 6 hours before recording began.

Carrageenan (2%, 200 p.1l) was injected into the lateral and posterior aspects of the TMJ

capsule as well as the superior joint space.













CHAPTER 3


RESULTS


Identification of TMJ Nociceptors


Receptive fields for units with VP or HP reactivity were found on the lateral and

posterior capsule of the TMJ (Figures 3-1 and 3-2). The mean von Frey thresholds for VP

and HP units were 27 39 g and 15 + 20 g, respectively. The receptive fields of these

units were single, small spots (approximately 2-3 mm). In some cases, receptive fields

could not be identified. It is possible that the receptive fields of these units were located on

the medial capsule, posterior attachment tissues or peripheral portions of the articular disc.

Alternatively, it is possible that units without identified receptive fields were not of TMJ

origin but, instead, of muscular origin (lateral pterygoid or temporalis muscles).

Conduction velocities were determined to be in the group III and IV fiber range (0.4 to 8.5

m/s). Due to the inaccessibility of many of the receptive fields, conduction velocities could

only be obtained for 30% of the units (19 of 63 units).

The response characteristics of TMJ afferents were examined. Mechanical

reactivity to jaw movement was determined using both dynamically and statically applied

forces. In order to distinguish between joint afferents acting as proprioceptors from those

acting as nociceptors,we searched for afferents with a preference for intense stimuli. It was

predicted that TMJ nociceptors would respond in the noxious range of mandibular motion,

where the noxious range of motion was defined as that passive mandibular motion where

the mandible encounters considerable resistance imposed by constraints of soft tissue.



















































Figure 3-1.


Receptive field (RF) distribution in the lateral and posterior capsule of the
TMJ for normal tissue. A) Distribution of RFs in the lateral capsule. B)
Distribution of RFs in the posterior capsule. RFs (n=36) of afferents in
A) and B) responded to either vertical plane (.) or horizontal plane (A)
movement of the mandible. POST, posterior, ANT, Anterior, MED,
medial; LAT, lateral.







A




POST







B


MED


LAT


















































Figure 3-2. Receptive field (RF) distribution in the lateral and posterior capsule of the
TMJ for previously inflamed tissue (-), acutely inflamed tissue (A&) and
saline control tissue (+). A) Lateral capsule. B) Posterior capsule.
POST, posterior, ANT, anterior;, MED, Medial; LAT, lateral.







A





POST







B


MED


LAT









Therefore, relationships between applied force and jaw movement were examined to

determine the noxious range and compare it with afferent discharge properties.

Due to physical constraints of the preparation, force-movement relationships could

only be examined for VP units. Characterization of force-movement relationships in the

vertical plane revealed a biphasic relationship between applied force and mandibular

movement (Figure 3-3). Linear force-movement relationships gave way to exponential

force-movement relationships when the mandible reached an extreme of opening. It is

likely that this exponential phase corresponds to the noxious range. Force-movement

curves of VP units (n = 10) were best described by power functions (Table 3-1). Power

functions were the best fit in 10 of 10 cases (R2 = 0.92 + 0.06). The functional range of

VP units may be graphically assessed by observing activation thresholds plotted on force-

movement curves. As can be seen in Figure 3-3, nearly all afferents began to respond in

the transition zone between the linear and exponential phases of the curves. This can be

examined statistically by examining the functions fit below the point of activation. For the

10 cases in which power functions were fit, activation threshold occurred during portions

of the curves which were exponentially accelerating (6/10 cases, R2 = 0.86 + 0.17). In 4

cases, activation thresholds occurred in portions of the curve in which force was increasing

linearly (R2 = 0.88 0.19). The activation thesholds of these 4 units occurred at forces

approaching the power phase of the curve. The observed preference for high forces (mean

activation threshold for force = 20.6 + 11.0 N; mean frequency asymptote = 49.6 + 20.7

N) at extremes of the range of motion (mean activation threshold at 13.7 + 5.4; mean

frequency asymptote = 20.4 + 5.9) suggested that these TMJ afferents were nociceptors.


Characterization of TMJ Nociceptors in Normal Tissue


Units were classified according to their preferred movement plane. Preferred

movement was defined as that plane of motion in which mandibular excursion evokes the




















































Figure 3-3. Relationships between applied force and vertical plane movements of the
mandible. Ten biphasic curves indicated that low forces were sufficient to
open the jaw through most of its range of motion. High forces produce
minimal degrees of opening where the joint encounters considerable
resistance from soft tissue. In each case, the TMJ nociceptor begins to
respond at the point indicated by the arrow.










TMJ FORCEIMOVEMENT RELATIONSHIPS: VERTICAL PLANE

D


0 20 40 60 sO 100 120 140
FORCE (Newtons)
-,- TEST --- TEST -*- TEST -0- TEST
1 2 3 4






B


0 15 30 45 80 75 0O 105 120 135 150
FORCE (Newtmn)
=m TEST-,,- TESTm-m TESTm TEST-*" TEST
1 2 3 4 6






C


is OVEMENT (dear***)

12







N042090H


0 10 20 30 40 so50


sO


FORCE (N*wtons)
,,, TEST ,* TESTM, TnEST-- TESTmA* TEST
1 2 3 4 5






E


0 15 30 45 s0 75 90 10S 120 135 150
FORCE (Newton )
-A- TEST.- TEST-*- TEST-U- TEST-- TEST
1 2 3 4 5


0 10 20 30 40 50 0 5 10 15 20 25 30 35
FORCE (Newton.) FORCE (Newton<)
a-A TEST E-*- TEST-- TEST-@- TEST-- TEST -A- TEST TEST E
1 2 3 4 5 1 2 3


40 45


:Sq













TMJ FORCE/MOVEMENT RELATIONSHIPS: VERTICAL PLANE



I


0 10 20 30 40 so50 60 70 80

FORCE (Nowtons)
-As TEST -*- TEST -*- TEST -m- TEST
1 2 3 4


0 10 20 30 40 SO 80


FORCE (Newtons)
"A- TEST TEST
1 2


I OVEMENT fdeorees) MOVEMENT (decrees)


25

20



10

___ _St
092791K 101691F
S . . . . . . . . . . . . . . . . . . . . . . . . . .
0 10 20 30 40 50 60 70 0 10 20 30 40 so50 so

FORCE (Newtons) FORCE (Newton.)
-Am TEST -- TEST -*- TEST U-- TEST -A- TEST -0- TEST
1 2 3 4 1 2


Figure 3.3. (cont'd)


* TEST
3









Table 3-1
Force/Movement Relationships in the Vertical Plane


2
FILE FUNCTION FULL RANGE LOW RANGE R P

042090H POW LnI = 0.69 LnF + 4.8 0.93 0.0001
042090H LIN I = 0.15 F + 1.8 0.90 0.0001
042090H POW Lnl = 0.8 LnF + 0.89 0.96 0.0001
042090H LIN I = 0.2F + 0.87 0.95 0.0001
110990E POW Lnl = 0.8 LnF + 2.1 0.97 0.0001
110990E LIN I = 0.6 F + 2.3 0.96 0.0001
110990E POW LnI = 1.1 LnF + 0.15 0.92 0.0001
110990E LIN I = 1.0 + 0.19 0.97 0.0001
111490D1 POW LnI = 0.4 LnF + 1.1 0.91 0.0001
111490D1 LIN 1=0.IF+ 8.5 0.87 0.0001
111490D1 POW LnI = 1.7 LnF+ 2.2 0.92 0.0001 1
111490D1 LIN I = 1.0F+ 4.2 0.86 0.0001
111490D2 POW LnI = 1.3 LnF + 1.2 0.91 0.0001
111490D2 LIN I = 0.7F+ 0.22 0.87 0.0001
111490D2 POW LnI = 2.3 LnF + 3.5 0.94 0.0001
111490D2 LIN I= 1.4F + 7.4 0.97 0.0001
022791A POW LnI = 0.3 LnF + 2..2 0.93 0.0001
022791A LIN I = 0.77F + 11.0 0.79 0.0001
022791A POW LnI = 0.15 LnF +2.0 0.80 0.04
022791A LIN I = 1.8F + 5.9 0.97 0.0001
032891X POW LnI =0.37 LnF + 1.1 0.99 0.0001
032891X LIN I = 0.23F + 3.7 0.88 0.0001
032891X POW LnI = 0.4 LnF + 0.01 0.98 0.0001
032891X LIN I = 0.55F + 2.3 0.88 0.0001
080591 IC POW Lnl = 0.34 LnF + 1.9 0.87 0.0001
080591C LIN I = 0.28F + 12.0 0.77 0.0001
080591C POW LnI = 0.46 LnF + 1.8 0.57 0.0003
080591C ULIN I = 1.5 F + 5.3 0.61 0.0001
091691A POW LnI = 0.54 LnF + 1.3 0.87 0.0001
091691A LIN I = 0.42F+ 9.0 0.83 0.0001
091691A POW LnI = 0.64 LnF + 1.2 0.52 0.01
091691A LIN I = 2.3 F + 1.3 0.37 0.04
092791K POW LnI = 0.48 LnF + 1.4 0.96 0.0001
092791K LIN I = 0.37 F + 8.6 0.88 0.0001
092791K POW LnI = 0.59 LnF + 1.3 0.90 0.0001
092791K LIN I = .97F + 4.1 0.88 0.0001
101891F POW LnI = 0.5 LnF + 1.3 0.83 0.0001
101891F LIN I = 0.29F + 11.0 0.73 0.0001
101891F POW LnI = 0.74 LnF + 1.0 0.86 0.0001
101891F LIN I = 0.9 F + 5.6 0.64 0.0001

Note: POW, power; LIN, linear.









strongest response from an afferent. Thirty-six afferents with receptive fields in the TMJ

capsule were activated by either vertical plane (VP or opening) or horizontal plane (HP or

lateral displacement) motion. Eighteen afferents responded preferentially to movement in

the vertical plane and 18 responded best to movement in the horizontal plane. A few units

were activated by right lateral displacement (n = 5) or protrusive (n = 2) movement but

most TMJ afferents responded preferentially to either opening (VP) or left lateral

displacement (HP).

Once preferred movement was determined, tests of dynamic and static reactivity

were conducted. Relationships between force, position or movement and response interval

were quantified. The responses of TMJ nociceptors were quantified by regressions fit

between instantaneous dynamic force, force velocity, movement, static force or position

and instantaneous interspike interval.

As it was not clear which function would best describe TMJ afferents, linear,

power, logarithmic and exponential models were explored. By comparison of the relative

proportions of variance accounted for by each model, it was determined that power

functions accounted for the greatest percentage of variance (mean R2 = 0.46 + 0.26; n = 71

cases). Power functions were best fits compared to other functions for both dynamic

(26/59 cases) and static tests (10/12 cases). Power functions were second best fits in 20

out of 59 cases for dynamic tests and 1 out of 12 cases for static tests. Linear functions

were superior in 7 cases, logarithmic in 12 cases and exponential in 16 cases. Since power

functions were the best or second best fit in 46 of 71 cases (mean R2 = 0.45 .30), power

functions were used to represent the data in normal tissue. In inflamed tissue (both PI and

AI), power functions accounted for the greatest percentage of variance in 101 of 146 cases

(mean R2 = 0.50 + 0.21).

TMJ nociceptors could be found which transduced (or coded) all aspects of force,

movement or position, and many transduced more than one variable. "Code" indicates that









a unit's reactivity was proportional to force or some other stimulus variable and that the

relationship could be described by a significant power function.

The great majority of TMJ nociceptors (n = 24) coded dynamic aspects of force

applied to the mandible, and relatively few coded for static aspects of these stimuli.

Twenty-three of 36 units that responded to either VP or HP jaw movement coded for

dynamic force (mean activation threshold = 20.1 17.5 N) and 15 of 36 units coded for

force velocity (mean activation threshold = 15.5 + 20.5 N/s; Table 3-2). In contrast, only

8 of 36 units coded for static force (mean activation threshold 17.8 + 18.3 N), while 5 of

35 units coded jaw movement (mean activation thresholds of 11.0" + 4.0, and only 1 of

36 units coded for jaw position. In some cases, unit reactivity could be described by more

than one function. Twelve of 23 units that could be fit to dynamic force were also

significantly fit to force velocity. Six of these 12 units were significantly fit to force

velocity, and 6 of these 12 units were significantly fit to static force as well. Ten of 36 units

could not be fit to any function. Fourteen additional units had jaw movement reactivity but

no receptive field could be found.

Mean functions were generated from individually fitted functions by pooling

slopes, intercepts and boundary values. Functions presented in Figure 3-4 represent the

principle transducing properties of TMJ afferents: dynamic force and force velocity.



Properties of TMJ Nociceptors in Inflamed Tissue



The response properties of afferents were examined in capsular tissue that was

previously inflamed (PI) by carrageenan. In these experiments, TMJ tissues were exposed

to carrageenan for at least 6 hours prior to testing. In other experiments, afferents were

tested in normal tissue and then tested again after an acute injection of carrageenan or

saline. Afferent reactivity was examined for up to 3 hours subsequent to exposure to

carrageenan.










TABLE 3-2


TMJ NOCICEPTOR REACTIVITY IN NORMAL TISSUE
with RF (n=36) without RF (n=14)
Test Conditions
code (n=25) no code (n=10) code (n=--9) no code (n=5)


Dynamic Force 23 12 6 6



Force Velocity 15 19 4 8



Movement 5 10 2 3


Static Force 8 23 1 4



Static Position 14 0
1 14 0 4


Conduction 0.4 to 7.5 0.5 to 1.5
mrn/sec m/sec
Velocity (n =6) (n = 3)
Post-test
Spontaneous 3 0 0 0

Activity

Note: Receptive fields (RF) in the TMJ capsule were identified for 36 units. Twenty-five
units with RFs coded for one or more of the stimuli. Most units (n = 23) with an
RE on the TMJ capsule coded for dynamic force. Fourteen additional units had
either VP or HP reactivity but an RF could not be found. "Code" indicates that a
unit's reactivity could be described by a significant power function. Of the 36
afferents with RFs in the TMJ capsule, 3 units demonstrated spontaneous
activity after dynamic or static testing. Five units with RFs in the TMJ capsule
responded preferentially to right lateral displacement. Most of these units (3 of
5 cases) coded dynamic force. Appendix G contains descriptive statistics for
these units.














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Experiment 1: Properties of Units in the
Previously Inflamed TMJ


In the PI condition, transduction of the dynamic aspects of stimulus force was best

described by power functions. Power functions were the best fit compared to other

functions (7 of 13 cases; R2 = 0.33 0.25) and were best or second best fit in 9 of 13

cases. Therefore, exposure to carrageenan did not modify the nature of functions which

described afferent activity. Individually fitted power functions generated during dynamic

and static response testing in inflamed tissue are illustrated in Figure 3-5.

Comparison of units in normal and inflamed tissue (see Figure 3-6) suggested

improved reactivity for units that responded preferentially to movement in the vertical

plane. Increased reactivity to dynamic stimuli was particularly prominent. In normal

tissue, 11 of 18 units with RFs on the TMJ capsule coded for dynamic force or velocity;

while proportionally more units (5/5) transduced dynamic force or velocity in the PI

condition. Mean functions for dynamic force in inflamed and noninflamed conditions were

calculated by averaging slopes and intercepts of individual functions (LnI = -1.3LnF + 7.3,

(n = 25); LnI = 1.1 LnF + 5.4, (n = 6)] for inflamed and noninflamed, respectively). The

mean functions for all VP and HP units fitted during dynamic testing in normal and

inflamed tissue suggested improvement of dynamic reactivity (Figure 3-6). The shifts of

the mean function for units in PI condition to a graphic position below the mean function

for normal tissue was suggestive of sensitization to dynamic forces.

Mean functions were also calculated for afferents transducing force velocity. A

shift of the mean function of PI units that coded for force velocity [Lnl = -0.7 LnF + 3.5,

(n = 6)] was also observed in comparison to the mean functions in normal tissue [LnI = -

0.38 LnF + 4.7, (n = 16)]. These functions are illustrated in Figure 3-6. A shift of the

mean function for afferents in inflamed tissue below and to the left of the mean function for

normal tissue also suggested sensitization to velocity of applied forces.



















































Figure 3-5.


Dynamic reactivity in previously inflamed tissue. Power functions best
described the relationship between instantaneous dynamic force and force
velocity with instantaneous response interval in the vertical or horizontal
plane. A) Six of 7 units transduced dynamic force (mean slope = -1.1 +
0.5; range = 7.6 + 10.2 to 33.3 + 32.1 N; mean R2= 0.24 + 0.16). B)
Six of 7 units transduced force velocity (mean slope = -0.7 0.8; range =
4.8 + 4.5 to 40.2 + 22.2 N/s; mean R2 = 0.33 + 0.28).











REACTIVITY IN PREVIOUSLY INFLAMED TISSUE:
DYNAMIC FORCE
Ln Interval (msec)


5 .N



3

2

1
0 U I | *
-1.5 0.0 1.5 3.0 4.5 6.0

Ln FORCE (Newtons)
-V- T7 -*- E1 -m- J1 -*- E3 -A- T1 -+- 02



REACTIVITY IN PREVIOUSLY INFLAMED TISSUE;
FORCE VELOCITY
SLn Interval (msec)
6

5
~A

4

3

2

1


-1 0 1 2 3 4 5 6

Ln Velocity (Newtons/sec)
-+- B2 -A- T7 -0- El -- J1 -A- E3 -- T1

















































Figure 3-6.


Averaged dynamic response functions of nociceptors fitted in normal and
previously inflamed tissue (PI). A) Mean function for dynamic force
fitted in PI tissue (mean interval = 29.9 + 7.9 msec) falls below the mean
dynamic force function fitted in normal tissue (mean interval = 44.7 +
16.5 msec) suggesting sensitization. B) Mean function for force velocity
in PI tissue (mean interval = 22.2 + 3.3 msec; mean activation threshold =
17.3 + 18.9 N/s) falls below and to the left of mean force velocity
function fitted in normal tissue (mean interval = 7.4 + 4.8 msec; mean
activation threshold = 4.8 + 4.5 N/s) suggesting enhanced reactivity
(sensitization)











CHANGES IN REACTIVITY TO DYNAMIC FORCE
FOLLOWING CARRAGEENAN INFLAMMATION
Ln Interval (msec)
6

5

4


3N
3------*^---

1---------

1 I ---------------------


-V-- N (n=25)


Ln Force (Newtons)
-*- INF (n=6)


CHANGES IN REACTIVITY TO FORCE VELOCITY
FOLLOWING CARRAGEENAN INFLAMMATION
Ln Interval (msec)
6

5

4
3 ,







5 -,-------------- I p -- I ----------


-Tv- N (n=16)


2 3

Ln Velocity (Newtons/sec)
9- INF (n=6)









Statistical comparisons between function characteristics in normal and inflamed

tissues confirmed that dynamic reactivity improved in inflamed tissues (See Table 3-3).

This was manifested as changes in activation threshold, frequency asymptotes and function

intercepts. The mean activation threshold (8.3 13.2 N) for units in inflamed tissue (n =

4) that responded best to jaw opening and transduced dynamic force was significantly

lowered relative to the mean activation threshold (24.1 + 11.2 N) for VP units (n = 10) in

normal tissue (F = 5.36, df = 13, p < 0.04). For those same units, the mean intercept in

inflamed tissue (5.0 + 3.0) was significantly decreased relative to the mean intercept in

normal tissue (9.0 + 3.1). Similar changes were observed for afferents that transduced

force velocity. The mean frequency asymptote (37.5 23.6 N/s) for these units was

significantly less than the mean frequency asymptote (148.0 + 79.6 N/s) for units (n = 8),

in normal tissue (F = 8.89, df = 12, p < 0.01). The mean force-frequency asymptote (40.2

+ 22.2 N/s) for PI units (n = 6) that coded for force velocity in both VP and HP jaw

movements were significantly less than the mean force-frequency asymptote (156.5 + 83.1

N/s) for VP and HP units (n = 15) in normal tissue (F = 9.57, df = 21, p < 0.01).

The changes we have observed in dynamic reactivity of TMJ nociceptors are

suggestive of sensitization. However, experiments of this type (PI tissue) are subject to

sampling errors. The best form of evidence for nociceptor sensitization comes from

observations of single affferents making transitions from the normal to the sensitized state,

following acute injections of pro-inflammatory substances.


Experiment II: Promperties of Units in the
Acutely Inflamed TMJ


The findings of enhanced dynamic reactivity observed in populations of afferents

sampled from normal and subacutely inflamed TMJ tissues were complemented by

observations made on units in which testing was performed before and after carrageenan-



















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induced inflammation (acutely inflamed or AI). Outcomes of experiments using PI

methods suggested that individually characterized afferents would manifiest improved

dynamic reactivity.

Observations of quantitative shifts in force interval functions were confirmed, and

additional qualitative changes were observed. Eleven units were characterized in normal

tissue and then retested 1-3 h after exposure to carrageenan. Four units responded

preferentially to VP jaw movement and 7 responded best to HP movement For 9 units that

transduced stimulus intensity in both normal and inflamed tissue, 6 demonstrated enhanced

reactivity for dynamic force (Figure 3-7). Four of these 6 units had post-inflammatory

functions that shifted below the pre-inflammatory function. One of these also showed

leftward shift. Three of 6 units that demonstrated enhanced dynamic force reactivity

showed a leftward function shift relative to pre-inflammatory functions but failed to shift

below the control case. Mean function characteristics for these nociceptors are presented in

Table 3-3.

Experiments were performed to determine whether changes in AI reactivity

occurred as a result of carrageenan or other causes, such as repeated stimulation. In these

control experiments, saline (100 ill) was injected into the area of the RF and into the TMJ

capsule. Reactivity was examined in 8 units after exposure to saline. Five of 8 units

transduced dynamic force in both the pre- and post-saline conditions. While quantitative

changes in reactivity were small following saline injections, there was some indication that

repeated testing could produce qualitative changes in reactivity similar to those observed

following carrageenan injection (See Figure 3-8).

Following saline injection, mean activation threshold was reduced from 14.1 +

15.0 N in pre-saline condition to 11.5 + 7.5 N. These changes were relatively small

compared to changes observed following carrageenan (11.2 + 9.9 to 5.1 + 3.7 N).

Statistical comparisons indicated that the mean changes in activation threshold was

significantly less in saline than carrageenan treated cases (T = -2.2; DF = 15; p = 0.04)).




















































Figure 3-7.


Demonstration of sensitization (enhanced reactivity). Six of 11 units
were characterized in normal tissue and then tested again after acutely
inflamed (AI) with carrageenan. Power functions generated from
retesting in acutely inflamed tissue were positioned below and/or to the
left of power functions fitted on normal tissue. N, normal, Min,
inflamed; HR, inflamed.





















REACTIVITY IN VERTICAL PLANE: NORMAL TO INFLAMED
DYNAMIC FORCE: UNIT #1

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REACTIVITY IN VERTICAL PLANE: NORMAL TO INFLAMED
DYNAMIC FORCE: UNIT #3






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REACTIVITY IN HORIZONTAL PLANE: NORMAL TO INFLAMED
DYNAMIC FORCE: UNIT #2

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REACTIVITY IN HORIZONTAL PLANE: NORMAL TO INFLAMED
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DYNAMIC FORCE: UNIT #4
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REACTIVITY IN HORIZONTAL PLANE: NORMAL TO INFLAMED
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Figure 3-8.


Reactivity of nociceptors exposed to saline. Five units transduced
dynamic force in both the pre- and post-saline conditions. A) and B)
demonstrate quantative changes in dynamic force reactivity. C), D) and
E) show no enhanced reactivity.

















A
REACTIVITY IN HORIZONTAL PLANE: SALINE CONTROL
DYNAMIC FORCE: LEFT LATERAL UNIT #3

: n Wa *lr4W-----------






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B
REACTIVITY IN HORIZONTAL PLANE: SALINE CONTROL
DYNAMIC FORCE: LEFT LATERAL UNIT #6





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C
REACTIVITY IN HORIZONTAL PLANE: SALINE CONTROL
DYNAMIC FORCE: LEFT LATERAL UNIT #2
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REACTIVITY IN HORIZONTAL PLANE: SALINE CONTROL
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REACTIVITY IN HORIZONTAL PLANE: SALINE CONTROL
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Therefore while shifts in activation threshold could occur following repeated testing, the

changes that followed carrageenan injection were significantly greater.

In experiment I, it was determined that most TMJ nociceptors transduced dynamic

force and velocity, but few transduced either static force, movement or position.

Following acute exposure to carrageenan, qualitative changes in coding capacities were

noted; that is, afferents coded for stimulus features not previously transduced.

Qualitative improvements were observed for most units for either dynamically or

statically applied stimuli. Eight of 11 nociceptors acquired either dynamic or static coding

ability (Table 3-4). Four of 4 units that preferred VP jaw movement and transduced

dynamic force in normal tissue acquired the ability to transduce force velocity (n = 2), static

force (n = 1) or jaw position (n = 1) in inflamed tissue. Two of 5 AI units that preferred

HP movement and transduced dynamic force in normal tissue also acquired the ability to

transduce static force. Acquired coding also appeared in nociceptors that were without

transducing capacity in normal tissue. Two of 7 AI units that preferred HP movement

acquired the capacity to transduce both dynamic and static force. Other changes appeared

as de novo reactivity. Three of 7 units that had only HP jaw movement initially acquired

similar reactivity for VP movement (dynamic force). Six units demonstrated spontaneous

activity after stimulus testing.

The finding that a large proportion (8/11) of nociceptors acquired coding ability

after exposure of carrageenan suggested a qualitative form of sensitization. The nature of

these qualitative changes can be best appreciated by comparing scatter plots representing

comparisons between pre-inflamed and post-inflamed reactivity. Two types of trends (shift

and rotation) were observed. Shift indicates a movement of a scatter of points into graphic

zones of greater sensitivity. Rotation indicates the development of a significant slope

associated with the scatter field of points. Of the 9 of 11 nociceptors that acquired coding

ability, all 9 showed shifts and/or rotation. Figure 3-9 illustrates significant functions of

units that demonstrated shifts and units that demonstrated rotation of scatter point fields.





45




Table 3-4.

EFFECT OF CARRAGEENAN ON TRANSDUCING CAPACITY

Qualitative improvements in reactivity for nociceptors that were
characterized in normal tissue and then tested again subsequent to
carrageenan injection. Eight of 11 nociceptors acquired either dynamic or
static coding ability. Coding ability was also acquired for nociceptors (n =
2) that had no transducing capacity in normal tissue. Three units that
responded to horizontal plane movement acquired vertical plane reactivity in
acutely inflamed tissue. Six units demonstrated spontaneous activity after
stimulus testing in acutely inflamed tissue.



UNIT PLANE PRE-INFLAMED POST-INFLAMED CODING OTHER POST-TEST
SHIFT MOVEMENT SPONTAN.
____________________________ACTIVITY

1 VP DYNAMIC FORCE DYNAMIC FORCE YES YES
FORCE VELOCITY
MOVEMENT MOVEMENT
STATIC FORCE STATIC FORCE
POSITION POSITION

2 VP DYNAMIC FORCE DYNAMIC FORCE YES
STATIC FORCE YES


3 VP DYNAMIC FORCE DYNAMIC FORCE
FORCE VELOCITY YES NOW
STATIC FORCE STATIC FORCE

4 VP DYNAMIC FORCE DYNAMIC FORCE
FORCE VELOCITY
MOVEMENT MOVEMENT WE
POSITION YES


Note: VP, vertical plane











Table 3-4 (cont'd).


UNIT PLANE PRE-INFLAMED POST-INFLAMED CODING OTHER POST-TEST
SHIFT MOVEMENT SPONTAN.
ACTIVITY

5 HP DYNAMIC FORCE YES
FORCE VELOCITY YES YES
STATIC FORCE YES ____________

6 HP DYNAMIC FORCE DYNAMIC FORCE
FORCE VELOCITY FORCE VELOCITY
STATIC FORCE YES YES


7 HP DYNAMIC FORCE DYNAMIC FORCE OPEN: CODE N3NE
FORCE VELOCITY FORCE VELOCITY OPEN: CODE
STATIC FORCE YES OPEN: NON-CODE


8 HP DYNAMIC FORCE DYNAMIC FORCE YES
FORCECVELOCITY FORCE VELOCITY
STATIC FORCE STATIC FORCE

9 HP DYNAMIC FORCE DYNAMIC FORCE OPEN: CODE YES


10 HP DYNAMIC FORCE DYNAMIC FORCE
STATIC FORCE STATIC FORCE
NOWE

11 HP DYNAMIC FORCE YES OPEN: NON-CODE
FORCE VELOCITY YES OPEN: NON-CODE
STATIC FORCE YES OPEN:NON-CODE N3NE


Note: HP, horizontal plane














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Of the 9 units exhibiting rotation, 4 also shifted. It was possible that shift was a more

mature form of sensitization that followed rotation. In units which were examined over

several hours, 2 of 2 units that exhibited rotations subsequently manifested shifts of their

scatter plot field (See Figure 3-9).

Control tests indicted that qualitative changes could also be observed after saline

injection. In 1 of 8 cases, a qualitative improvement was observed in dynamic coding

capacity (Table 3-5). Thus, improved dynamic reactivity is possible as the result of saline

injection. However, the tendency towards acquired coding appeared to be greater for

carrageenan-induced inflammation (8 of 11 cases).

In summary, experiments were performed to characterize the response properties of

presumed nociceptors in normal and inflamed capsular tissue of the TMJ. Most TMJ

afferents preferred either movement in the horizontal or vertical plane. Their reactivity

functions were best described by power functions fit between dynamic force, force velocity

and response interval. In normal tissue, TMJ afferents had properties of nociceptors, in

that the activation threshold was at the extreme range of jaw movement, either in the

exponential portion or in the transition zone between the linear and exponential force-

movement curves that described jaw movement. It was predicted that TMJ nociceptors

would sensitize following exposure to carrageenan. To test this, populations of afferents

were sampled in previouslyly inflamed tissue and their responses compared to those of

afferent populations in normal tissue. Improved reactivity was observed, especially

reactivity to dynamic stimuli (dynamic force and force velocity). To avoid sampling errors

that could have biased these observations, units were characterized in acutely inflamed

tissue after being characterized in normal tissue. These afferents manifested similar

quantitative improvements in dynamic reactivity. Additionally, qualitative improvements of

coding capacity were observed. Acquisition of coding capacity following acute

inflammation suggested afferent sensitization.











TABLE 3-5
EFFECT OF SANE ON TRANSDUCING CAPACITY
UNIT PLANE PRE-CODING POST-CODING CODIN OTHER POST-TEST
SHIFT MOVEMENT SPONTAN.
ACTIVITY

I I-lP DYNAMIC FORCE DYNAMIC FORCE
FORCE VELOCITY FORCE VELOCITY NONE
STATIC FORCE STATIC FORCE


2 HP DYNAMIC FORCE DYNAMIC FORCE
FORCE VELOCITY YES NONE
STATIC FORCE STATIC FORCE


3 HP DYNAMIC FORCE DYNAMIC FORCE
STATIC FORCE STATIC FORCE NONE


4 HP DYNAMIC FORCE
FORCE VELOCITY
MOVEMENT NONE
STATIC FORCE
POSITION


5 HP NON-CODING NON-CODING NOE




6 HP DYNAMIC FORCE DYNAMIC FORCE
NONE



7 HP DYNAMIC FORCE DYNAMIC FORCE
STATIC FORCE STATIC FORCE NONE




8 liHP STATIC FORCE STATIC FORCE NONE


Note: Changes in reactivity for 8 units after exposure to saline. One of 8 units acquired coding ability
for force velocity. HP, horizontal plane.













CHAPTER 4


DISCUSSION



Afferents were isolated from the trigeminal ganglion and efforts were made to

determine whether they had nociceptive properties. Tests included quantification of

response range, identification of relevant stimulus variables and the tendency to sensitize.

Afferents that are nociceptors should transduce noxious stimuli (Sherrington, 1947), while

other joint afferents (proprioceptors) would be expected to be most reactive in the normal

range of motion, be bidirectionallly sensitive, and exhibit spontaneous activity (Burke et

aL, 1988; Macefield et al., 1990, Dorm et al., 1991).

The relationship between applied force and mandibular movement was examined to

determine the "noxious range" and compare it with the threshold of afferents. The noxious

range is likely to correspond to that portion of the force/jaw movement relationship where

forces increased exponentially with jaw movement. TMJ afferents were activated at or near

the beginning of the exponential phase and their firing became asymptotic in the exponential

phase. Thus, a preference for high forces (mean activation threshold = 20.6 + 1 1.ON) at

extremes of the mandibular range of motion (mean activation threshold = 13.7 5.4; mean

frequency asymptote = 49.6 + 20.7 N) suggested that these TMJ afferents were

nociceptors.

In contrast, a small group of units (n = 3) had responses to both jaw opening and

closing. Their properties are distinct from populations of afferents which may be important

in signalling tissue damage. Their activation thresholds (1.1 + 0.9 N) and range of

reactivity (1.1 0.9 to 10.4 + 4.1 N) are considerably different from that of nociceptors

described above, and respond chiefly to innocuous joint movement within the physiological









range of motion. Afferents with similar properties have been observed in the cat knee joint

(Dom, et al., 1991). In this study, large diameter afferents (Group II) responded

exclusively in the normal range of motion, were directionally sensitive, and demonstrated

no resting activity. Whereas activity in nociceptors is likely to contribute to joint pain,

these low threshold afferents may contribute to proprioception or sensations of pressure

(Burke et al., 1988; Macefield et al., 1990; see Appendix B).

In other laboratories, recordings have been made from group III and IV joint

afferents innervating the cat knee (Burgess and Clark, 1969; Clark, 1975; Schaible and

Schmidt, 1983b). Schaible and Schmidt (1983b) divided their joint afferents into 4

subgroups which were differentiated, in part, by their qualitative response to movement.

They defined nociceptors as those afferents that responded through, beyond or exclusively

beyond the normal range of joint motion. These afferents had a steep rise in discharge

frequency during forceful rotational movements, similar to those described previously

(Burgess and Clark, .1969; Coggeshall et al., 1983). These observations compare

favorably with ours, in that intense mechanical stimulation is needed to achieve a maximum

response. It is difficult to make detailed comparisons between the response properties of

afferents described by Schaible and Schmidt and others with those in our experiments, as

no attempt was made by them to quantify the properties of afferents other than local

pressure thresholds. Our experiments represent the first quantification of nociceptor

reactivity across a range of suprathreshold stimuli with verification of the relationship

between movement, response minima and maxima.

Early experiments created some confusion as to the basic properties of joint

afferents. Studies that have examined the activity of mechanoreceptors supplying cat joint

tissues (Burgess and Clark, 1969; Clark and Burgess, 1975; Rossi and Grigg, 1982)

primarily emphasized proprioception, and addressed the questions as to whether position

sense is coded by joint or muscle afferent fibers. They determined that joint afferents are

only responsive at the extremes of the movement range, seemingly ruling out any useful









role in proprioception and clouding the functional distinction between free nerve endings

(nociceptors) and well recognized encapsulated Golgi and Ruffini type end organs which

are found throughout the capsule (Thilander, 1961; Ishibashi, 1966). Yet, others have

reported that many afferents respond within the normal range movement (Klineberg et al.,

1971; Lund and Matthews, 1981; Schaible and Schmidt, 1983b; Dom et al., 1991).

Microneurographic studies appear to have resolved this confusion in favor of the findings

of Schmidt and company. These studies have examined the behavior of neuronal

populations that signal joint position and mechanosensibility in humans. Burke et al.,

(1988) recorded responses of joint, muscle and cutaneous mechanoreceptors associated

with finger joints to position and movement. Whereas most responded at the limits of joint

rotation, a few afferents responded within the normal range. It is unclear whether the

former group could code for pain, as pain was never induced by the movements, but the

latter group appears to be appropriate for proprioceptive function. The relatively small

population (3 of 16 cases) that provided a proprioceptive code was not dissimilar to our

own (3 of 36 cases). Microstimulation of similar groups of joint afferents innervating

finger joints indicated that innocuous sensations of movement or deep pressure were

evoked (Macefield, et al., 1990). Thus, a proprioceptive role for joint afferents seems to

be confirmed, although they may represent a small portion of the afferent population.


Sensitization of TMJ Nociceptors


Nociceptors in all preparations will sensitize following exposure to extreme heat

(Burgess and Perl, 1967; Beck et al., 1974; Fitzgerald and Lynn, 1977; Campbell et al.,

1979), mechanical forces (Reeh et al., 1987) or proinflammatory substances (Schaible and

Schmidt, 1988a; Berberich et al., 1988; Cooper et al., 1991), and these are reflected as

changes in central reactivity (Neugebauer and Schaible, 1990; see Appendix D). Sensitized

nociceptors in skin, muscles and joints have enhanced reactivity to thermal, mechanical









and/or chemical stimuli. In our experiments, where afferents were sampled from

previously inflamed capsular tissue or where characterized afferents were retested in acutely

inflamed tissue, a variety of forms of sensitization was found. These changes included a

significant decrease in mean activation threshold, shifts in stimulus response functions and

qualitative forms of sensitization. Additional changes were observed for afferents in the PI

condition (frequency asymptote and intercept) that were not replicated in the AI condition.

Recent experiments on cat knee joint nociceptors (Schaible and Schmidt, 1988b)

have also produced evidence of changes in reactivity following carrageenan injection. Over

half of the units that were classified as nociceptors in normal tissue responded to innocuous

joint movements in the normal range of motion after inflammation. In effect, such

enhanced reactivity, from extremes of movement to the normal range of motion indicates a

decreased activation threshold. In our experiments, decreases in activation threshold were

observed following carrageenean-induced inflammation. These decreased activation

thresholds fell within the linear phase of force-movement relationship.

In our study, qualitative forms of sensitization were also observed. These appeared

both in carrageenan treated nociceptors (8 of 11 cases), and infrequently in saline treated

controls (1/8). The nature of these qualitative changes can be best appreciated by

comparing scatter plots representing comparisons between preinflamed and postinflamed

reactivity. It is important to examine scatter plots because the acquisition of transducing

ability could have represented a distorted outcome. For example, outliers could have

rendered functions insignificant where they were otherwise significant. However,

examination of plots following carrageenan showed new relationships between force and

response interval and shifts to greater reactivity.

Two types of trends were observed: rotation and shift. Rotational trends were

indicated by a change in slopes which suggested increased proportional reactivity. A shift

to the left represented a decrease in activation threshold that was seen consistently in AI and

PI conditions for units with extant coding capacity. The shifts that were observed, were









less likely to be related to the development of qualitative changes than rotation. Rotation

represents a new functional reactivity in the form of a proportional response to imposed

forces. The basis of the qualitative changes could be either receptor based metabolic

alteration secondary to the generation of proinflammatory substances, or could result from

improved mechanical coupling between the receptor and the applied force.

Edema is a major component of inflammation that may impact on mechanical

coupling. Afferent terminals of small fibers that are located in the area of inflammation are

subject to an altered physical environment as a consequence of fluid extravasation. What

effect local changes from edema may have in the responsiveness of joint receptors is

unclear. In other preparations, edema may act to enhance or deter afferent responsiveness,

the direction of the effect being dependent on tissue properties that are peculiar to each site

(Cooper et al, 1990).

Acquisition of transducing capacity could be similar to observations of recruited

activity described by other laboratories. This "recruitment" of afferents was observed in

the cat knee joint preparation (Schaible and Schmidt, 1985, 1988b) and also in cutaneous

preparations (Handwerker et al., 1991). A distinction between our observations and those

of Schaible and Schmidt is that our sensitized afferents all have some pre-existing

reactivity. We did not observe recruitment as silent units which "wake up." Given this,

recruited activity and acquired coding may be distinct forms of sensitization. Our failure to

observe recruitment may be due to methodological constraints of our preparation. In our

experiments, extracellular recordings of neural activity in the trigeminal ganglion limits the

number of neurons that could be recorded at any site. Very few cell bodies are in the

functional range of the microelectrode. On the other hand, in teased fiber preparations such

as those used by Schaible, Schmidt and Handwerker, electrodes have essentially zero

impedance, therefore many more afferents can be recorded from simultaneously. This

makes it more likely for recruitment to be observed.









Factors Contributing to Sensitization



Mechanical sensitization of joint afferents, following inflammation, is likely to be

due to the production and release of endogenous substances. Injection of carrageenan

produces a rapid inflammation that has been characterized in a number of behavioral and

physiological preparations (Vinegar et al., 1987). Various factors may contribute to

sensitization of joint afferents during carrageenan-induced inflammation, including both

edema and the formation and release of algesics.

Changes in the response properties of joint afferents during inflammation have been

attributed to the actions of bradykinin, prostaglandins, and serotonin. These mediators

may alter mechanical responsivity of afferents, modify chemical responsivity, activate

afferents or a combination of the three. Changes in reactivity of small fibers in inflamed

tissue to bradykinin have been observed (Kanaka et al., 1985; He et al., 1990; Grubb et

al., 1991). Bradykinin activates most group III and IV units that responded to passive joint

movement. Bradykinin also activates afferents otherwise classified as "silent" (Heppleman

et al., 1987).

Joint afferents can also be activated by prostaglandin (E or I). Prostaglandins E1 or

E2 activated small afferents which responded to passive joint movement (Heppleman et al.,

1985; Schaible and Schmidt, 1988a), and modified mechanical responses of these

afferents. Following exposure to PGE2, most group III and some group IV units showed

enhanced joint movement reactivity and responded within the normal range of motion.

These PGE2-evoked increases in unit responsiveness paralleled those observed during

acute arthritis (Schaible and Schmidt, 1985, 1988a). Similar properties have been

prescribed for PGI2, and it has been suggested that PGI2 may be the dominant PG in joint

afferent sensitization (Birrell et al., 1991; McQueen et al., 1991).

Interactions between pro-inflammatory mediators are also likely to be important, but

they have not been determined in much detail. Prostaglandin E1 (Schaible, 1983) and









prostaglandin E2 (Grubb et al., 1991) have been shown to sensitize joint nociceptors to

bradykinin. This may impact both on movement sensitive and tonic forms of joint pain.

Serotonin is also important in nociceptor sensitization. The effect of 5-HT on

response characteristics of small afferent fibers have been studied in normal and inflamed

cat knee joints (Heppelman et al., 1987) and rat ankle joints (Birrell et al., 1990; Grubb et

al., 1988). Most group III and IV fibers that showed reactivity to cat knee movement were

also activated by 5-HT. Units recorded from normal rat ankle joints were excited by 5-HT

and showed enhanced activity in arthritic joints.

The consequences of carrageenan injections are very complex, and have not been

determined for joints specifically (Vinegar et al., 1987). One sequence of events that

occurs in skin, during the initial stage of inflammation (0-60 min) suggests a divergence

from mechanisms proposed for sensitization of joint afferents. Immediately after injection

of carrageenan, small amounts are absorbed by mast cells. The cytotoxic action of

carrageenan initiates the arachidonate metabolic cascade and mast cell degranulation.

Endoperoxides and serotonin are released. The endoperoxides are not believed to be

prostaglandins but are believed to be reactive intermediates, and bradykinin is not believed

to play a role. This stands in contrast to studies directly implicating bradykinin, PGE's and

PGI2 in afferent sensitization and at the very least implicates that additional factors may

play a role in carrageenan inflammation. The role of 5-HT in carrageenan induced arthritis

is also unclear. While 5-HT is released by carrageenan in rats, it is unlikely to be directly

released in other species due to the absence of 5-HT in mast cells. Serotonin may be more

important when vascular damage occurs (Zeller et al, 1983; Garcia-Leme, 1989). This

may, in fact, be more relevant to TMJ dysfunction.

Clearly, reactivity to a host of algesics is shared by most small diameter afferents

innervating joint tissue. Bradykinin, prostaglandins and perhaps 5-HT may play a role in

afferent sensitization in inflamed joints. However, in each instance, it is not clear what is

meant by normal range of motion and it is not clear to what extent shifts produced by





59



bradykinin, PGE2 or serotonin are the basis for changes produced with carrageenan or

other proinflammatory substances. The lack of detail in this respect is partly due to the

absence of quantification of stimulus and response variables. Quantification of neural

activity in respect to threshold, range and salient stimulus features (static or dynamic

reactivity) should permit a fuller evaluation of role played by these substances and others in

modification of joint nociceptor reactivity.














APPENDIX A


DEVELOPMENT AND MAINTENANCE OF TMJ PAIN


Many theories have been advanced to account for the production of TMJ pains.

(For reviews, see Deboever, 1973; Dubner et al., 1978, Yemm, 1979). TMJ dysfunction

may account not only for pain in the joint itself, but also for pain arising from associated

facial structures.


Intra-articular Origins of TMJ Pain


1) Pressure Theory

Pressure theories have been the most prevalent explanations for the production of

TMJ pain. These theories suggest that disruption of the normal articular mechanics may

impose abnormal pressures on structures of the TMJ. Costen (1934) postulated that facial

pain associated with the TMJ was a consequence of pressure on the auriculotemporal nerve

brought about by impaction of the condyle against the tympanic plate. Anatomically, this

theory is untenable since the auriculotemporal nerve ramifies before reaching the TMJ. The

articular branches of the auriculotemporal nerve arise at the medialposterior aspect of the

neck of the condyle and ascend into the soft tissue of the joint inferior to the tympanic plate.

The auriculotemporal nerve is vulnerable to pressure at its proximal course. The

auriculotemporal nerve arises from the posterior trunk of the mandibular nerve along the

medial surface of the lower belly of the lateral pterygoid muscle. Entrapment of the

auriculotemporal nerve in the lateral pterygoid muscle has been demonstrated in 5% of









cadaver specimens (Loughner et al., 1990). Pressure in the form of compression by a

hyperactive lateral pterygoid muscle may produce pain and/or paresthesia. Furthermore,

patients with an internal derangement of the TMJ often have accompanying spasticity of the

lateral pterygoid muscle.

Pressure on the posterior attachment tissues by the condyle could also cause TMJ

pain (Sicher, 1955). Posterior displacement of the condyle or spastic contracture of the

superior belly of the lateral pterygoid muscle may result in anterior displacement of the

disc. As a consequence, the posterior attachment tissues are positioned where forces

generated during mastication may produce local pressure on these highly vascularized and

innervated tissues.

Local joint pressure may activate mechanoreceptive nociceptors in connective tissue

such as the posterior attachment tissues. Inflammation could result from trauma due to a

sudden, intense impact or from repeated pressure. Endogenous algesics released in the

zone of inflammation may sensitize joint nociceptors by decreasing threshold and

increasing response to mechanical stimuli (Heppelman et al., 1985).

A common procedure thought to discern anterior displacement of the disc is the

impact-loading test. Manual loading applied in an anterior-superior direction at the

posterior portion of the body of the mandible impacts the condyle into the articular fossa.

If pain is evoked, it is thought that the disc is displaced and the condyle is impacting onto

the posterior attachment tissues. However, disc displacement may exist without impact

loading pain. This is assessed by imaging techniques, such as arthrography or magnetic

resonsance imaging. Therefore, direct pressure on the disc or posterior attachment tissues

is not sufficient to explain TMJ pain in all cases.

A corollary notion related to Sicher's theory was advanced by Frost (1968) to

explain some patterns of joint pain. Frost hypothesized that bone pain may be evoked by

the pressure of two articulating, irregular, joint surfaces in the absence of an intact

interposing disc. Presumably, the irregular bony surfaces represent osteoarthritic changes.









Other investigators (Kreutziger and Mahan, 1975) have included arthroses of bony

structures as causative factors in TMJ pain. Besides the degenerative processes that may

occur in the bony anatomy of the TMJ, degenerative changes of the villi of the synovium

have been claimed to be causally related to TMJ pain (Olson, 1969). Supposedly,

disruption of the secretary function of the villi can disturb proper nutrition and lubrication

of the TMJ resulting in TMJ dysfunction.

2) Tension Theory
Tension theories of TMJ pain can be divided into static and dynamic. Static state

involves a resting position of the mandible. Dynamic state involves active or passive jaw

movement Anteriormedial displacement of the disc may generate static tension on the

posterior and lateral aspects of the capsule (Dubner et al., 1978) where the greatest member

of mechanoreceptors are located (Zimny, 1988). It is possible that resting tension will

produce prolonged discharge in TMJ nociceptors. If the anteriormedial displacement of the

"disc is advanced, there is a release of the disc attachment at the lateral pole of the condyle

which untethers the disc from the lateral aspect of the TMJ. In this case, the posterior

attachment tissues are vulnerable to tension from a disc displacement during static

conditions.

Patients suffering from pain in the TMJ often demonstrate symptoms of capsulitis;

this included pain on local palpation or pain during small movements within the normal

range of motion. Inflammatory processes in the TMJ may initiate or potentiate TMJ pain

(Dubner et al., 1978). Dynamic theories propose that pain is produced during jaw

movement by excitation of functionally distinct types of mechanoreceptors in the capsule

and posterior attachment tissues. Activation may be enhanced by capsulitis. Zimmy

(1988) advanced a conceptual model of TMJ pain during jaw movement. As the condyle

rotates and translates freely through intermediate degrees of angle, the capsule and posterior

attachment tissues are deformed. Such deformation is normally insufficient to excite

mechanoreceptors. As the condyle approaches its border movement, the capsule and









posterior attachment tissues become taut. Mechanoreceptors in the capsule and posterior

attachment tissues are activated by the resultant tension. Thus, these mechanoreceptors

appear to act as detectors that sense the safe limits of joint movement. Supposedly, jaw

movement beyond safe limits can represent real or potential tissue damaging stimuli. If

these mechanoreceptors are nociceptors, they may be sensitized following capsulitis so that

small movements in the functional range of motion produce pain. Clark and Burgess

(1975) suggested that large, myelinated afferents signal the pressure felt as the extremes of

joint movement are reached. These investigators demonstrated that slowly adapting

receptors in the capsule were excited only at extremes of flexion and extension of the knee

joint of the cat (Burgess and Clark, 1969). On the other hand, Schaible and Schmidt

(1983b) attribute a similar detection role for small fibers which are active only at the

borders of the joint movement.

Following capsulitis, the tension required to produce activation of nociceptors

might be greatly reduced. Animals studies in the cat knee joint (Schaible and Schmidt,

1988b) and rat ankle joint (Guilbaud, 1988) have demonstrated increased responsiveness

of group III and IV afferents to innocuous mechanical stimulation after induction of acute

inflammation. The relationship between nociceptor discharge and capsular tension is yet to

be demonstrated.

The reactivity of mechanoreceptors in the capsule of the cat knee have been used to

assess tension produced by joint movement (Grigg and Hoffman, 1989; Hoffman and

Grigg, 1989). The frequency of neurons with receptive fields in the posterior capsule

showed a linear relationship with tension applied (knee extension) at the area of the

receptive field. The posterior joint capsule was minimally loaded even during

hyperextension movements.








Extra-articular Theories of TMJ pain



Distinct theories of the origin of extra-articular pain have arisen, and include the

myofascial pain theory and referred pain theory.

1) Myofascial Pain Theory

The myofascial pain theory postulates chronic hyperactivity in head and neck

musculature as a causative agent in extra-articular pain. The myofascial pain theory

suggests that the chronicity of muscle pain is due to the "trigger point" (Travell, 1976).

The trigger point is defined as a localized area of chronic inflammation of fibrous

connective tissue in muscle. Histological examination of biopsy material from trigger

points in patients suffering from interstitial myofibrositis reveal degranulated mast cells and

platelet clots (Awad, 1973). The author proposes a hypothesis suggesting that trauma-

induced extravasation of platelets leads to release of 5-HT which subsequently results in

edema and vasoconstriction. The release of such endogenous algesics in muscle may play

a role in the pain and tenderness associated with trigger points. For example, activation of

group IV afferent neurons in cat muscle have been demonstrated by close arterial injection

of bradykinin, 5-HT or histamine (Mense and Schmidt, 1974). Serotonin may also

sensitize mucosal nociceptors to mechanical stimuli (Friedman et al., 1988; Cooper et aL,

1991).

Muscle pain and the reduction of pain free jaw movement are frequent complaints of

patients with facial pain. The limitation of jaw movement may involve the modulation of

the reflex control of masticatory muscles (Klineberg, 1971; Dubner et al., 1978).

Greenfield and Wyke (1966) studied the role of TMJ afferents in reflexes that modify the

activity of muscles of mastication. The experimental procedure involved detaching all the

supra- and infra-mandibular muscles at their insertions from one half of the cat mandible.

Movement of the ipsilateral half of the mandible resulted in activation or inhibition of









dissected muscles. Similar responses were produced in the detatched muscles by direct

tension on the capsule after condylectomy.

Jaw movement has been shown to modulate the firing pattern of alpha motoneurons

in the trigeminal motor nucleus in cats (Kawamura et al., 1967). These investigators

demonstrated changes in the discharge rate of motor neurons of the masseter muscle in

response to passive rotation of the ipsilateral condyle. Rotating the condyle to an open

position evoked an increase in firing pattern of masseter motoneurons. A closed position

evoked a decrease in firing pattern.

Abe and Kawamura (1973) recorded efferent discharges from branches of the

mandibular nerve which innervate the masseter and digastric muscles. Ipsilateral condylar

rotation to an open position inhibited alpha-motor units in the masseteric nerve. Local

mechanical stimulation of the posterior part of the TMJ capsule inhibited the discharge

pattern of masseteric neurons and facilitated motor fibers innervating the digastric muscle.

It is not surprising that afferent activity from mechanoreceptors in the TMJ modulate

efferent activity in masticatory muscles in order to coordinate jaw movement. The presence

of chronic activation of TMJ afferents may induce chronic reflex activation of facial

musculature. Chronic activation may produce muscle pain that limits movement.

Clinically, bruxism has been associated with muscle hyperactivity and TMJ

dysfunction. Bruxism is defined as a nonfunctional voluntary or involuntary mandibular

activity featuring habitual grinding or clenching of the teeth (Kawamura, 1980). Chronic,

repetitive mandibular movement seen in bruxism is thought to deliver excessive reaction

forces to the TMJ which could produce local inflammatory changes. Putative causes of

bruxism include occlusal stress, CNS and hereditary factors.

2) Referred pain theory

Pain may be referred to the TMJ from other head and neck regions (Bell, 1969).

Travell (1976) suggested that continuous hyperactivity of muscles from the head and neck

may refer pain to the TMJ. The explanations for the origin of referred pain have largely









ruled out nerve branching in the periphery as a source of referred pain. The convergence

theory of referred pain invokes a central locus of action in the superficial layers of the

medullary dorsal horn. Noxious input from different sources converge on transmission

cells responding to noxious input (for review, see Fields, 1987). Pain may be mistakenly

mislocated to an area distant from the site of origin due to expectation or previous

experience with pain in the referred site.

In most cases, TMJ pain is not restricted to the joint but is also associated with

extra-articular regions. The most common areas are ipsilateral eyeball, superciliary ridge,

deep masseter muscle, and angle of mandible (Mahan and Ailing, 1991). The

craniovertebral junction and upper neck are other referral sites of TMJ pain (Schellhas et

al., 1989).













APPENDIX B


PSYCHOPHYSICS OF TMJ DISORDERS



Pain and mandibular dysfunction are two.common manifestations of TMJ

disorders. Pain can occur when the mandible is at rest or during function. Disordered

movement of the mandible is a sign of mandibular dysfunction (i.e. the inability to

masticate properly). Patients suffering from TMJ disorders often complain of pain while

chewing. Whether mandibular dysfuntion is directly or indirectly due to TMJ disorder or

due uniquely to pain that results from jaw movement is unclear.
Chewing efficiency, jaw movement, biting force and perception of jaw position are

quantifiable features of mastication. A review of the literature reveals studies which have

been directed at investigating the relationship between TMJ disorders and mastication.

There has been little psychophysical experimentation involved in quantifying pain

associated with mandibular dysfunction. Even though most of these studies pertain to

treatment efficacy, understanding the relationship between TMJ disorders and mastication

may be valuable in understanding the relationship between pain and TMJ disorders.


Chewing Efficiency


Typically, the clinical appraisal of individual's chewing efficiency is limited to a

subjective report provided by the patient. Early investigators (Christiansen, 1922;

Dahlberg, 1942) developed the technique of using a series of sieves with different mesh

sizes and test materials for chewing in order to estimate chewing efficiency. A simple









method that can be used clinically to assess chewing efficiency was developed by Loos

(1963) and modified by Carlsson and Helkimo (1972). Test material is chewed for 10, 20

or 40 seconds.

Masticated test materials are then measured in millimeters. Chewing efficiency is rated

according to the size of the material and number of seconds of chewing.

A more elaborate, standardized measure of chewing efficiency, called the

Coefficient of Masticatory Performance, was developed by Manly and Braley (1950). The

Coefficient of Masticatory Performance was defined as the percentage of chewed peanuts

that pass through a 10-mesh screen sieve after being subjected to 20 masticatory strokes.

Rominger and Rugh (1986), utilizing this test, compared the chewing performance of a

group of patients with TMJ dysfunction to a group of normal controls. The patient group

had significantly lower coefficient scores than the normal control group. Lemke et al.

(1987) investigated the level of masticatory efficiency of post-TMJ surgical patients several

years after treatment. These investigators found that the post-surgery group had

significantly lower chewing efficiency scores than a group of non-treated non-

dysfunctional patients.

Taken together, these studies indicate a negative relationship between chewing

efficiency and TMJ disorders. Whether the inability to chew efficiently is due to the TMJ

pain or associated muscular pain is uncertain.


Jaw Movement



The sensory apparatus of the TMJ is thought to play a role in the synchronizing

mechanisms involved with the control of jaw movement (Sicher, 1955). The influences of

TMJ afferents on functional jaw movements has been studied in both normal subjects and

patients suffering from TMJ disorders. In normal subjects, Posselt and Thilander (1965)

anesthetized the lateral part of the TMJ capsule. They observed an increase in lateral









movement and maximum opening. The authors suggested that the lateral ligament may be

associated with a protective mechanism during extreme opening. Klineberg (1980) also

anesthetized the TMJs of normal subjects and observed an increase in size of the envelope

of function (range of motion), and suggested that mechanoreceptors of the TMJ play a

modulatory role in motor control of the mandible.

One measure of jaw movement is maximum range of motion (ROM). The

measurement is made for opening, lateral and protrusive excursions. An assessment of

ROM for normal subjects has been reported by Posselt (1968). For normal subjects (adult

males) maximum opening averages 50-60 mm; hinge opening, 20-25 mm; lateral excursion

from midline, 10 mm; and protrusive excursion, 10 mm. Anaesthesization of the lateral

capusle of the TMJ increased hinge opening and protrusion by 10-15% (Posselt and

Thilander, 1965). For patients suffering from TMJ disorders, ROM is generally limited

compared to normal subjects. Helkimo (1974) devised a pain-dysfunction index which

rates severity of mandibular function in regard to pain report for jaw movement and TMJ

palpation. This index was modified by Zarb and Carlsson (1988). Normal ROM was >39

mm for opening and >6 mm for lateral excursions. For patients, ROM was 30-39 mm for

opening and 4-6 mm for lateral excursions. Patients with this amount of impairment

reported pain during at least one jaw movement and pain on palpation of the TMJ's. For

other patients, ROM was <30 mm for opening and <4 mm for lateral excursions. Patients

with this amount of impairment reported during 2 or more jaw movements and pain on

palpation of the TMJ's.

Many clinicians observe a decrease in ROM for patients suffering from TMJ

disorders. These patients are often hesitant to open their mouth maximally because of real

or expected pain. As a result, a measure of ROM may result in a value less than the patient

is actually capable of producing. Therefore, other components of mastication may be more

likely to be reliable measures of jaw function. Moreover, the movements of the mandible









that are made during mastication are well within the border movements of the mandible as

defined by the ROM (Okeson, 1989).


Jaw Position



One feature of mandibular function is the ability to control the position of the

mandible within the limits of one's maximum ROM. An important question in the literature

dealing with proprioception is whether position sense is signalled by joint or muscle

afferents. Part of the literature implicates joint afferents (For reviews see Rose and

Mountcastle, 1959; Skoglund, 1973; Dubner et al., 1978); another part of the literature

implicates muscle afferents (for review, see Burgess et al., 1982). It is reasonable to

explain joint position sense in terms of both joint and muscle afferent input.

Jaw position sense has been studied in both normal subjects and patients suffering

from TMJ disorders. Thilander (1961) assessed perception of mandibular position before

and after unilateral or bilateral anesthetization of the TMJ in normal subjects. The results

showed that subjects had more difficulty returning to an initial jaw position, following

anesthetization. Larsson and Thilander (1964) explored the relationship between position

sense and local mechanical pressure applied to the TMJ in normal subjects. The authors

found that position sense was not influenced by local pressure. When the local pressure

was reported to be painful, again position sense was not affected. However, when the

joint was locally anesthetized, jaw position sense deteriorated. If then, local pressure was

applied to the joint during the course of anesthesia, position sense returned to normal

levels. Presumably, local pressure recruited muscle afferents. Input from muscle

mechanoreceptors may have provided the sensory feedback necessary to restore position

sense. The authors reported that ansethetization of the TMJ was performed by infiltration

into the skin and tissues lateral to the capsule. This technique may have not anesthetized

the TMJ completely.








Interdental thickness discrimination is one method that has been used to analyze the

position sense of the mandible. Interdental thickness discrimination is the ability to detect

differences in the thickness of test materials placed between opposing teeth. Caffese et al.,

(1973) studied the possible influence of TMJ receptors in tactile occlusal perception by

assessing minimal thickness detection between opposing teeth before and after

anesthetization of the TMJ. These authors found significant differences in threshold

detection in the anesthetized joint compared to the normal joint. On the other hand, Siirila

and Laine (1972) obtained different results from their study of interdental thickness

discrimination. Anesthetization of TMJ did not significantly diminish subjects' ability to

detect differences in thickness between teeth at various degrees of mouth opening.

Morimoto and Kawamura (1978) obtained similar results and suggested that the muscle

spindles in the muscles of mastication are mainly responsible for size discrimination.

If mechanoreceptors of the TMJ play a role in jaw position sense, their influence

maybe modulated by TMJ disorders. Ransjo and Thilander (1963) studied position sense

of the mandible in patients with TMJ disorders which were thought to be of myogenic

origin or due to functional malocclusion. The authors assumed that functional

malocclusion caused impairment of TMJ receptors. Position sense was found to be poorer

for the malocclusion group compared to the normal group. Position sense of the myogenic

group was normal. Amelioration of TMJ symptoms after treatment was accompanied by

improvement in the perception of jaw position. This study is in accord with the previous

work of Thilander (1961) suggesting that TMJ mechanoreceptors play a major role in the

ability to perceive position sense of the mandible.

A more recent study by van Willigen et al., (1986) investigated perception of jaw

position in subjects with symptoms of TMJ disorders. They found that all subjects with

craniomandibular dysfunction demonstrated greater mismatches of jaw position compared

with normal subjects. On the other hand, other studies present contrasting evidence

(Christensen and Troest, 1975; Morimoto and Kawamura, 1978; Broekhuijsen and van









Willigen, 1983; van der Berghe et al., 1987). Morimoto and Kawamura (1978) tested

interdental thickness discrimination in 8 patients with unilateral or bilateral mandibular

condyles that were either surgically mobilized or removed. The authors failed to observe

any lessened capacity to discriminate thickness. These authors concluded that TMJ

receptors were not essential to size discrimination ability.

Broekhuijsen and van Willigen (1983) studied position sense of the mandible in

normal subjects before and after injection of the TMJ capsule bilaterally with local

anesthetic. Perception of mandibular position was unaffected by anesthetization of the

TMJs. Van den Berghe et al., (1987) assessed position sense of the mandible in patients

suffering from TMJ disorders before and after treatment. Patients' abilities to determine

jaw position were unchanged after successful treatment.

The relative unimportance of joint afferents in assessing position and movement is

noted for a variety of joints. In the human knee joint, injection of local anesthetic into the

joint does not deteriorate the subjects' ability to detect passive angular displacements of five

degrees (Clark et al, 1979). Moreover, total joint replacement of the hip produces little

impairment of sensations associated with joint movement (Grigg et al, 1973).

In summary, the ability to control the position of the jaw is an important aspect of

mandibular function. Position sense has been studied in both normal subjects and patients

suffering from TMJ disorders. The preponderance of the evidence suggests that sensory

input from the TMJ contributes little information in controlling the position of the mandible.


Bite Force


Different parameters of bite force, such as maximum bite force, submaximal bite

force and bite force discrimination have been investigated in an effort to assess mandibular

function.








Maximum Bite Force

The maximum bite force is the measure of the greatest force which an individual can

produce by biting on an instrument containing a force transducer. The maximal level of

bite force that an individual is capable of producing is rarely required or utilized during

chewing. Therefore, the relevance of maximum bite force as a measure of mandibular

function is uncertain. Also, a measure of maximum bite force may result in a value less

than an individual is capable or willing to produce. Clark et al., (1984) reported that the

maximum bite force of normal subjects is limited by pain tolerance. Patients suffering from

TMJ disorder may be incapable of producing maximum bite force due to the direct effect of

mandibular dysfunction or unwillingness to bite normally due to the indirect effect of pain.

Such may be the case in several studies that assessed maximum bite force in patients

suffering from TMJ disorders (Helkimo et al., 1975; Sheikolelam et al., 1982). Helkimo

et al. (1975) reported that maximum bite force was lower in a patient group with TMJ

disorders than for a control group. Patients' level of maximum bite force increased

following treatment. Sheikolelam et al., (1982) observed that maximum bite force was

significantly less for their patients with TMJ disorders than for normal controls.


Submaximal Bite Force

One important component of the normal chewing cycle is the individual's ability to

produce and control relatively low levels of biting force. Submaximal bite force is the

measure of different levels of biting force below maximum bite force. It seems reasonable

to suggest that impaired mandibular function may result in impairment of the ability to

control submaximal bite force. Several studies have investigated submaximal bite force in

patients with mandibular dysfunction (Helkimo et al., 1975; Agerberg, 1988). Bite force

was registered with different types of bite beams incorporating a force transducer. A

common feature of patient populations was pain in the TMJ. These studies reported that









patients had lower values for submaximal bite force (3-25 kg) compared to control subjects

(5-50 kg).

Bite Force Discrimination


In order for an individual to control the different levels of bite force, he/she must be

able to discriminate differences in the intensity of their own biting force. The role of TMJ

mechanoreceptors in bite force discrimination has been investigated in normal subjects

(Williams et al., 1984; Williams et al., 1989). Bite force was assessed before, during and

after anesthetization of the TMJ by auriculotemporal nerve block (Williams et al., 1984) or

infiltration into the superior joint cavity (Williams et al., 1989). These studies suggest that

the TMJ mechanoreceptors do not appear to be responsible for discrimination of bite force.

In summary, maximum bite force, submaximal bite force and bite force

discrimination are three commonly used measures of mandibular function. Studies

assessing maximum and submaximal bite force indicate that patients suffering from TMJ

disorders have decreased bite force strength. The ability to discriminate bite force levels

has not been studied in patients having TMJ disorders. Neither maximum bite force,

submaximal bite force nor bite force discrimination measures have provided clear

information on the relationship between TMJ sensory input and mandibular function.













APPENDIX C


NEUROANATOMY OF THE TMJ


Until Thilander's (1961) comprehensive, anatomical and histological study of the

innervation of the human TMJ, research on innervation of the TMJ involved macroscopic

studies. Riidinger (1857) observed that the auriculotemporal nerve coursed to the posterior

aspect of the joint where three or four articular branches entered the capsule. The anterior

aspect of the capsule received one or two twigs derived from the masseteric and deep

temporal nerves. Textbooks describing the TMJ generally accepted Riidinger's findings.

Moreover, other anatomists (Guerrier and Bolonyi, 1948; Baumann, 1951; Hromada,

1960) are in agreement with the neural topography described by Riidinger but for the

possible exception of the contribution of the facial nerve.

Some sensory fibers travel in the facial nerve, which is otherwise devoted to motor

function. These afferent fibers constitute about 15% of the total nerve fiber population

(Foley, 1960). Guerrier and Bolonyi (1948) reported that branches of the facial nerve

always terminated in the lateral surface of the TMJ. Hromada (1960) stated that a twig

from the facial nerve passed into the lateral aspect of the capsule in about half of his

dissected specimens. On the other hand, Thilander (1961) reported that, immediately

lateral to the capsule, a twig from the facial nerves courses in an anterior direction but does

not ramify into the joint. Kerr (1962) also reported that afferents of the facial nerve

terminate only in the dermatomes of Cl and C2 in the cat. Our observations (unpublished)

suggest that the facial nerve does not innervate the TMJ of the human. However, the facial









nerve was seen to communicate with the auriculotemporal nerve distal to the TMJ.

In contrast to the innervation of the human TMJ, the facial nerve of the goat

communicates with the auriculotemporal nerve proximal to the articular branches. The

functional implications of this topography are unclear. Some afferents from the TMJ may

travel centrally in the facial nerve or afferents in the facial nerve travel in the

auriculotemporal nerve.

Thilander (1961) reported that the auriculotemporal nerve is the major sensory

nerve of the TMJ. The branches from the auriculotemporal nerve innervate the posterior,

medial, and lateral aspect of the anterior capsule. These branches enter the inferior aspect

of the capsule along the neck of the condyle. This observation is not in accord with

Rudinger (1857) who reported that the articular branches of the auriculotemporal nerve

passed between the condyle and the pars tympanica. However, a recent study (Loughner et

al., 1990) confirms Thilander's report. In this laboratory, macroscopic dissections of the

TMJ of the goat (unpublished) show a similar course of the auriculotemporal nerve and

distribution of articular branches.

According to Hilton's Law (1879), nerves that innervate the muscles that move a

particular joint also contribute to innervation of the joint. Surprisingly, that contribution is

only about 30% of the total TMJ innervation (Thilander, 1961). Twigs from the masseteric

nerve innervate parts of the anterior capsule and anterior aspect of the medial capsule. The

posterior deep temporal nerve innervate the lateral anterior aspect of the capsule. The

auriculotemporal nerve supplies the remaining 70% of the TMJ.

Thilander (1961) estimated that the human TMJ is innervated by an average of 1500

peripheral afferent fibers. The auriculotemporal nerve contributes two thirds of the total

amount The greatest number of the articular fibers have a diameter between 1 and 2 gm

and probably terminate as free endings in the capsule, posterior attachment tissues and

adventitia of blood vessels associated with the joint. Other afferent fibers, though fewer in

number, and ranging from 6 to 11 m, terminate in complex neural endings.









The posterior attachment tissues contain a rich plexus of nerve fibers from the

auriculotemporal nerve. Hall et al., (1985) identified and quantified the types of nerve

fibers in the posterior attachment tissues. The authors found that the majority of axons

were unmyelinated. The lateral portion of the posterior attachment tissues contain

significantly higher percentage of unmyelinated fibers. Other investigators (Weinmann and

Sicher, 1951; Sicher, 1955) have reported abundant innervation in association with blood

vessels in the loose connective tissue between the posteror border of the articular disc and

the capsule.

A few nerve fibers have been observed in the synovial membrane of the human

TMJ (Thilander, 1961; Ishibashi, 1966). Ishibashi, (1974) found free nerve endings and

glomerular endings beneath the superficial cell layer of the synovial membrane located on

the posterior aspect of the TMJ. Bemrnick (1962) described encapsulated end bulbs in the

synovial folds in the TMJ of the rat. These observations appear to contradict those who

believe that the synovial tissue serves no sensory function (Olson, 1969). Although the

nerve endings in the synovial membrane have been reported to be closely associated with

blood vessels (Hagen-Torn, 1882; Davis, 1945), unmyelinated nerve fibers have been

described in the synovium separated from blood vessels (Kellgren and Samuel, 1950;

Rossie, 1950). Kawamura et al. (1967) found Golgi-type endings in the synovial tissue

layer of the TMJ of the cat but not in the synovial membrane itself. Whether the synovial

membrane is innervated or not, the justapositon of afferent fibers allows sensibility in the

territory of the synovium.

As reported by Thilander (1961), the articular disc contained no nerve endings.

However, other investigators (Ishibashi, 1966; Schmid, 1969; Zimny and St. Onge, 1987)

described articular nerves innervating the periphery of the disc in the human TMJ. Similar

results were reported in the monkey (Keller and Moffet, 1968), in the rat (Bemick, 1962)

and in the mouse (Frommer and Monroe, 1966). These studies are consistent with

histological studies of fetal material. Kitamura (1974) reported that, in the 5th month in









utero, nerve fibers were observed in the disc; further development was accompanied by a

reduction in disc innervation. Corroboration of the influence of growth on disc innervation

came from Hromada (1960), who observed free nerve endings in the disc of various

animals; at older ages such endings were limited to the periphery of the disc. By

comparison, the nerve supply to the meniscus of the human knee remains unclear (For

review see Zimny, 1988). The most recent study (Albright and Zimny, 1987) reports that

free and complex nerve endings were observed in outer and middle one-third of the

meniscus; whereas, no innervation was found in the inner one-third.

Innervation of the TMJ of the monkey and cat resemble that of the human joint

(Franks, 1965; Keller and Moffett, 1968). Branches from the deep temporal and

masseteric nerves supply the anterior capsule, and the articular branches of the

auriculotemporal nerve supply the TMJ posteriorly. Preliminary macrodissection of the

nerves innervating the TMJ of one goat was performed in this laboratory. The

auriculotemporal nerve gave off three articular branches along the posterior aspect of the

neck of the condyle. The articular branches ascended into the fatty and fibrous articular

tissue. The termination of the temporal branch of the auriculotemporal nerve appeared in

the facial skin inferior to the zygomatic arch. The masseteric nerve was observed to arise

from the anterior trunk of the mandibular nerve, course lateral along the anterior border of

the capsule of the TMJ and terminate in the superficial and deep masseter muscle. Twigs

from the masseteric nerve appeared to enter the anteriorlateral aspect of the capsule.

Tissues surrounding articulations possess fewer types of receptors than muscle or

cutaneous tissue. Thilander (1961) described four types of neural endings in the human

TMJ: Ruffini-like receptors, modified Pacinian endings, Golgi tendon organs and free

nerve endings. Ishibashi (1966) also reported the presence of free nerve endings and

complex terminal expansions in the human TMJ. Keller and Moffett (1968) reported free

and complex nerve endings in the TMJ of monkeys. Many investigators have identified








free and complex nerve endings in the TMJ of the cat (Kawamura and Majima, 1964;

Greenfield and Wyke, 1966; Kawamura et al., 1967; Wyke, 1967; Klineberg, 1971).

The three types of complicated nerve endings were sparsely distributed compared to

the free nerve endings. The most common complex ending is the Ruffini ending. Ruffini-

like endings were encountered in the lateral and posteriorlateral aspect of the capsule in

humans (Thilander, 1961). Griffin and Harris (1975) described a thinly unencapsulated

corpuscle located close to the periosteum of the neck of the condyle and in the lateral and

medial aspects of the capsule fat pads. These receptors may have been similar to the

Ruffini endings described by Klineberg (1971) in the TMJ of the cat. The Ruffini-type,

low theshold mechanoreceptors were once thought to signal joint position (Boyd and

Roberts, 1953; Boyd, 1954; Cohen, 1955; Skoglund, 1956, 1973). However, other

investigators (Burgess and Clark, 1969; McCall et al., 1974; Clark and Burgess, 1975;

Clark, 1975; Grigg, 1975; Grigg and Greenspan, 1977) have shown that Ruffini endings

are seldom active at intermediate positions of the cat knee joint. They are responsive to

extremes of joint movement. Consequently, these receptors are unlikely the peripheral

neural substrate that code for position sense. Instead, Ruffini endings appear to signal the

torque produced when the joint is extended and/or rotated at the limit of the range of

motion. (Grigg et al., 1982a).

Pacinian endings were found in the lateral aspect of the capsule (Thilander, 1961).

Paciniform-type end organs in cats have a similar distribution as Ruffini endings but less

dense (Kawamura et al., 1967; Klineberg, 1971). Golgi tendon organs were located in the

temporomandibular ligament and anterior capsule (Thilander, 1961; Griffin et al., 1965).

In the anterior capsule, the Golgi end organ was in series with the extrafusal fibers of the

lateral pterygoid muscle and tendon fasciculi of the capsular tissue or the fibrous tissue of

the pes menisci. In the temporomandibular ligament the Golgi end organ was thought to be

in series with fibers of the deep masseter muscle. Both Paciniform endings and Golgi

tendon organs are thought to respond like comparable endings found in cutaneous and









muscle tissue (Willis and Coggeshall, 1978). However, Grigg et al., (1982b) showed that

in the cat knee, Golgi tendon organs responded to local pressure applied perpendicular to

the capsule but not to tension applied parallel to the capsule.

Free nerve endings are the most abundant receptor in the capsule of the human

TMJ. Presumably, free nerve endings derived from myelinated afferents subserve fast pain

sensibility and nociceptive somatic reflexes; free nerve endings derived from unmyelinated

nerve fibers may subserve slow pain sensibility or innervate vascular elements. Free

ending receptor specializations have yet to be defined. In sympathectomized cats, sensory

nonmedullated plexuses have been found in the inner layers of the fibrous capsule, adjacent

synovial tissues and adventitia of blood vessels in the knee joint of cat (Samuel, 1952).

Free endings have been described in the joint capsule, joint ligaments and periarticular fat

pads (Greenfield and Wyke, 1966). Similar results have been reported by Freeman and

Wyke (1967). Free endings characteristic of group III and IV afferents have been

described in the Archilles tendon of the cat as well (Andres et al., 1980). Some of these

free endings may be nociceptors.

Although there are great variations in the morphology of the TMJ between species,

the innervation of the TMJ is quite similar (Kawamura, 1980). The distribution and

appearance of receptors may vary with age and species (Polacek, 1966), but the types of

receptors are consonant across species including human.

In summary, the mammalian TMJ contains four types of receptors (for review see

Skoglund, 1973; Zimny, 1988). The Ruffini and Paciniform mechanoreceptors are

innervated by medium-sized (AB) myelinated fibers, the Golgi tendon organ by large (Aa)

myelinated fibers and the free endings by fine myelinated and unmyelinated afferents.













APPENDIX D


CENTRAL REPRESENTATION OF TMJ AFFERENTS


The central distribution of TMJ afferents has been studied in the trigeminal nuclear

complex. The main sensory nuclei and the dorsal part of the rostral spinal nucleus were

found to contain neurons responsive to isolated condylar movement or pressure applied to

the joint capsule of the cat (Kawamura aand Majima, 1964; Kawamura et al., 1967). The

authors reported simple, qualitative findings describing three types of responses to

ipsilateral condylar rotation (rapidly adapting, slowly adapting and on-off types) and two

types of responses to mechanical stimulation (rapidly adapting and slowly adapting types).

In addition, response patterns of neurons in the trigeminal motor nucleus were recorded

during condylar movements or mechanical stimulation of the joint capsule. As with

responses from the sensory nuclei, no quantification of activity was attempted. Procaine

infiltration into the joint capsule abolished neural responses. Another qualitative study

reported unit activity found in the trigeminal main sensory nucleus and nucleus oralis of the

cat that responded to jaw rotation or pressure applied to the ipsilateral TMJ (Sessle and

Greenwood, 1976). One of these units was antidromically activated from the thalamus.

Other direct projections from the superficial layers of the medullary dorsal horn to the

thalamus have been demonstrated anatomically (Craig and Burton, 1981) and

electrophysiologically (Dostrovsky and Broton, 1985).

The caudal aspects of the trigeminal nucleus complex were found to contain

neurons that are driven by electrical, mechanical, and algesic chemical stimuli applied to the

TMJ (Broton and Sessle, 1988). Neurons in the subnucleus caudalis were first classified









on the basis of their responsiveness to mechanical stimulation to the skin: low-threshold

mechanoreceptors (LTM), wide dynamic range (WDR) or nociceptive specified (NS).

WDR and NS neurons responded maximally to algesic chemical and intense mechanical

stimulation applied to the joint. TMJ stimulation consisted of local probing or extreme jaw

opening. The majority of single units with TMJ input received convergent input from

cutaneous afferents. Kojima (1990) also found convergence patterns of afferent input from

the TMJ and muscle in the subnucleus caudalis. Most of the units tested were responsive

to mechanical and thermal stimulation of both the TMJ and the masseter muscle.

Extensive convergence of cutaneous and muscle inputs on second-order neurons

that respond to articular movement have been described in the cat knee (Schaible et al.,

1986). In some neurons, maximal responses to joint movement occurred with forced

extension, inward rotation or outward rotation. Other neurons were excited only by

noxious movement. Joint movement was considered noxious if the movement was made

forceably. No quantification of forces was attempted. This report compares favorably

with the effects of TMJ stimulation in neurons in the medullary dorsal horn (Broton and

Sessle, 1988), in that most second order neurons that respond to noxious joint simulation

also receive convergent input from skin and/or muscle. Such central convergence may be

important in explaining the tenderness of skin and/or muscles near the joint that are often

observed clinically when the joint is painful.

Changes in responsiveness in spinal neurons have been investigated during the

development of acute arthritis in the cat knee jont (Neugebauer and Schaible, 1990). All

neurons tested with joint input showed enhanced responsiveness to joint flexion after

induction of inflammation.

Other electrophysiological experiments performed in polyarthritic rats demonstrated

nociceptive inputs from chronically inflamed joints to the ventrobasal thalmus (Guilbaud et

al., 1980; Gautron and Guilbaud, 1982), intralaminar and medial thalamus (Kayser and

Guilbaud, 1984; Dostrovsky and Guilbaud, 1990), and somatosensory cortex (Lamour et





83



al., 1983). One consistent feature of the neuronal reactivity seen in all of these studies is

the increase responsiveness of central neurons to non-noxious stimulation of the inflamed

joints. The central mechanisms which might contribute to changes in responsiveness of

central neurons in arthritic rats is still in question. The alterations in discharge behavior

seen in CNS neurons is likely due, in part, to the changes in responsiveness of joint

receptors due to inflammatory processes.













APPENDIX E


TRIGEMINAL GANGLION


The trigeminal ganglion is situated near the apex of the petrous bone in the middle

cranial fossa. It lies in Meckel's cave near the cavernous sinus and internal carotid artery.

The sensory root portiono major) enters the pons in association with the motor root portiono

minor), which courses dorsomedially, and terminates in the trigeminal nuclear complex.

Sensory input from the face enters the trigeminal ganglion via the opthalamic,

maxillary and mandibular division of the trigeminal nerve. The cell bodies of these afferent

fibers are segregated into discrete clusters (Jerge, 1964; Kerr, 1962).

Retrograph transport of HRP injected into the cat TMJ showed that sensory

neurons originate in the trigeminal ganglion (Romfh et al., 1979; Capra, 1987). Whether

all of the cell bodies of afferent neurons innervating the TMJ are located in the trigeminal

ganglion remains unanswered. There is evidence suggesting that the peripheral spinal

neurons innervate the TMJ. Widenfalk and Wiberg (1990) injected HRP into the TMJ of

rats. Labeled cells were observed ipsilaterally in the second to fifth dorsal root ganglion.

In addition, there is evidence suggesting that the mesencephalic nucleus contains cell bodies

of neurons that terminate in the TMJ. In a preliminary communication, Limwongee (1986)

reported injection of HRP into the TMJ of rat, cat and monkey. He found labeled neurons

in the mesencephalic nucleus at the level of the caudal pons. On the other hand, Corbin

(1940) ablated the mesencephalic nucleus and examined histologically the auriculotemporal

nerve. He found no degenerated fibers. In addition, Chen and Turner (1987) injected









HRP into the TMJ and insertion of the lateral pterygoid muscle of rats. They found no

central projection to the mesencephalic nucleus.


Somatotopy


There is general agreement that the trigeminal ganglion in cats is somatopically

represented from a medial to lateral direction (Beaudreau and Jerge, 1968; Zucker and

Welker, 1969; Kerr and Lysak, 1964; Darian-Smith et al., 1965; Marfurt, 1981). The

ophthalmic division lies anteriomedially, the mandibular division lies posteriolaterally and

the maxillary division is situated in an intermediate position. Overlap between divisions

has been reported (Marfurt, 1981; Henry et al., 1986). Romfh et al., (1979) and Capra

(1987) reported that injection of HRP into the capsular tissues of the TMJ in the cat resulted

in a restricted distribution of label in the posteriolateral position of the trigeminal ganglion.

Very few labeled cells were found in the most dorsal or in the most ventral areas of the

mandibular division of the trigeminal ganglion. The majority of labeled cells is found

throughout the intermediate zone in the posteriolateral part of the ganglion.

Electrophysiological studies in cats (Capra and Gaitpon, 1981) and in rabbits (Lund and

Matthews, 1981; Appenteng et al., 1982) confirmed that TMJ afferents were located in the

posteriolateral region of the trigeminal ganglion.

In addition to the mediolateral somatotopy, studies suggest a dorsoventral

somatotopic organization (Kerr and Lysak, 1964; Marfurt, 1981; Capra, 1987).

Representation of oral and perioral structures appear ventral in the ganglion. Areas remote

from the mouth lie in the dorsum of the ganglion.













APPENDIX F


GROSS ANATOMY


The TMJ in mammals is a ginglymus-arthroidal joint, i.e., a hinge joint capable of

gliding movement (Figure F- 1). The craniomandibular articulation involves the condyle of

the mandible juxtaposed with the articular surface of the squamous portion of the temporal

bone. Interposed between the condyle and the articular fossa is an articular disk dividing

the articular space into upper and lower compartments.

The periarticular soft tissue consists of fibrous capsule, posterior attachment

tissues, synovial membrane and accessory ligaments. Except for the synovial membrane,

these tissues serve to limit the range of motion of the joint and to maintain a packed position

(Sicher, 1960; Rocabado, 1983). A packed position is the condyle-disc-fossa relationship

which juxtaposes these TMJ elements at rest and during mandibular movements. The joint

capsule is loose and composed of dense connective tissue with a collagenous matrix richly

supplied with blood vessels and nerves. The dense connective tissue of the capsule is

located primarily on the lateral and medial aspect of the joint and intimately associated with

the temporomandibular and sphenomandibular ligaments, respectively. The anterior

capsule arises from the suture line between the greater wing of the sphenoid bone and the

temporal bone. It inserts on the anteriorlateral aspect of the condylar neck. The loose

connective tissue of the capsule encompasses the joint posteriorly. It arises from the tragal

cartilage laterally and tympanic plate medially. The posterior capsule, as a meshwork of

unorganized collagen fiber, inserts and blends in with the posterior periosteum of the

condylar neck and upper capsule of the parotid gland.









SAGITTAL VIEW


FRONTAL VIEW


1. Articular Surface of Glenoid Fossa 15. Auriculotemporal Nerve
2. Superior Cavitt 16. Blood Vessels
3. Disc (Stippled Area) 17. Posterior Deep Temporal Nerve
4. Capsule 18. Squamo-Sphenoidal Suture
5. Articular Surface of Condyle 19. Parotid Gland
6. Synovial Membrane 20. Sphenomandibular Ligament
7. Squamo-Tympanic Suture
8. Spine of the Sphenoid
9. Vascular Knee of Meniscus
10. Pes Meniscus
11. Superior Belly ofLat. Pterygoid
12. Inferior Belly ofLat. Pterygoid
13. Superior Stratum of Bilaminar Zone of Meniscus
14. Inferior Stratum of Bilaminar Zone of Meniscus

Figure F-I
Schematic diagram of the human temporomandibular joint. Sagittal and
frontal views.









The dense connective tissue of the capsule reinforces the lateral position of the TMJ

and is incorporated into the temporomandibular ligament. Horizontal fibers of the

temporomandibular ligament restrict posterior displacement of the condyle and oblique

fibers tend to limit lateral and inferior displacement (Sicher, 1960; Griffin and Malor,

1974). The posterior attachment tissues consists of collagenous and elastic connective

tissues which extend from the posterior border of the disc to the tympanic plate.

Macroscopic dissections of the goat TMJ were performed in this laboratory. The

articular surface of the condyle is oval in shape, its longer dimension is concave

mediolateral and the shorter dimension is convex anterioposterior. The articular disc is

ovoid, biconcave, and divides the joint into two synovial cavities. The fibrous capsule is

moderately loose which allows for extensive lateral translation of the condyle. The capsule

surrounds the joint, with the exception of the anteriomedial portions, where the lateral

pterygoid muscle attaches to the neck of the condyle. With four exceptions the gross

anatomy of the goat TMJ is similar to the human. First, the lateral aspect of the posterior

attachment tissue extends posteriorly beyond the postglenoid process and attaches to the

inferior surface of the zygomatic process of the temporal bone. This anatomical variation is

associated with the lateralization of the bony articulation of the TMJ beyond the cranial

base. Second, the articular surface of the glenoid fossa is slightly convex in all directions,

rather than concave. To accommodate this convexity the condyle is appropriately concave

along the mediallateral axis. Third, there is no articular eminence. Finally, the lateral

pterygoid muscle attaches to the anteriormedial aspect of the neck of the condyle in a

manner similar to the human, but it does not appear to attach to the disc.


Comparative Anatomy


According to the classification of Turnbull (1970), goats are section I herbivors

while humans are section III omnivores. The TMJ of the goat has been used as an animal









model for oral surgery procedures because the anatomy and biomechanics are similar to the

human TMJ (Bifano et al., 1990).

First, for the vertebrate chewing apparatus, the range of motion is generally

confined to those movements necessary for dealing with a particular diet. Due to a coarse

diet of vegetation, ruminants possess a greater range of mandibular movement than do

carnivores. The excursive movements include hinging, lateral translation, slight protrusion

and mediolateral shift. Hinge opening and lateral translational movements are required for

forceful grinding. The lateral pterygoid muscle is the prime mover of the mandible during

lateral translational movements. The lateral excursion, initiated by contraction of either one

of the lateral pterygoid muscles, is a prerequisite to an effective grinding stroke. Both the

goat and human possess a well-developed, lateral pterygoid muscle.

Second, the elevated position of the condyle of the mandible relative to the occlusal

plane benefits the operation of the masseter and medial pterygoid muscles. They function

synergistically to provide powerful bite force needed for grinding activity.

Third, the condyle is convex anteriorposteriorly, which allows some translation

along a convex articular surface of the fossa. Such anteriorposterior translation represents

a common denominator between the TMJ of non-camivorous mammals and the human

joints. In contrast, carnivores have a deep concave articular fossa that allows only hinge

movement and prevents dislocation during seizure of prey.




Full Text
73
Maximum Bite Force
The maxmum bite force is the measure of the greatest force which an individual can
produce by biting on an instrument containing a force transducer. The maximal level of
bite force that an individual is capable of producing is rarely required or utilized during
chewing. Therefore, the relevance of maximum bite force as a measure of mandibular
function is uncertain. Also, a measure of maximum bite force may result in a value less
than an individual is capable or willing to produce. Clark et al., (1984) reported that the
maximum bite force of normal subjects is limited by pain tolerance. Patients suffering from
TMJ disorder may be incapable of producing maximum bite force due to the direct effect of
mandibular dysfunction or unwillingness to bite normally due to the indirect effect of pain.
Such may be the case in several studies that assessed maximum bite force in patients
suffering from TMJ disorders (Helkimo et ah, 1975; Sheikolelam et ah, 1982). Helkimo
et ah (1975) reported that maximum bite force was lower in a patient group with TMJ
disorders than for a control group. Patients' level of maximum bite force increased
following treatment. Sheikolelam et al., (1982) observed that maximum bite force was
significantly less for their patients with TMJ disorders than for normal controls.
Submaximal Bite Force
One important component of the normal chewing cycle is the individuals ability to
produce and control relatively low levels of biting force. Submaximal bite force is the
measure of different levels of biting force below maximum bite force. It seems reasonable
to suggest that impaired mandibular function may result in impairment of the ability to
control submaximal bite force. Several studies have investigated submaximal bite force in
patients with mandibular dysfunction (Helkimo et ah, 1975; Agerberg, 1988). Bite force
was registered with different types of bite beams incorporating a force transducer. A
common feature of patient populations was pain in the TMJ. These studies reported that


Abstract of Dissertation Presented to the Graduate School
of the University of Florida in Partial Fulfillment of the
Requirements for the Degree of Doctor of Philosophy
PROPERTIES OF TEMPOROMANDIBULAR JOINT NOCICEPTORS
IN NORMAL AND INFLAMED TISSUE
By
Barry Loughner
May, 1992
Chairman: Parker Mahan, D.D.S., Ph.D.
Cochairman: Brian Cooper, Ph.D.
Major Department: Oral Biology
Mechanical response properties of nociceptors of the goat temporomandibular joint
(TMJ) were characterized by unit recordings from the trigeminal ganglion. Populations of
afferents were sampled in normal tissue and in tissue previously inflamed (PI) with
carrageenan for at least 6 hours prior to testing. In other experiments, nociceptors were
characterized in normal tissue and then retested for up to 3 hrs subsequent to exposure to
carrageenan (AI). To produce mandibular movement in the vertical and horizontal planes,
dynamic and static forces were applied to the mandibular pole. Stimuli were quantified by
force and angular displacement transducers. Receptive fields were small, single spots (2-3
mm) and located on the lateral or posterior capsule of the TMJ. Conduction velocities were
shown to be in the group III and IV range. Stimulus-interval data was best described by
power functions. Assessment of force-movement relationships indicated that capsular
nociceptors responded exclusively to intense forces that produce extreme displacements of
the mandible.
x


99
TABLE G-9
TMJ NOCICEPTOR REACTIVITY
IN SALINE INJECTED TISSUE
Test Conditions
with RF (n=8)
code(n=7)
acquired coding (n=l)
Dynamic Force
6
0
Force Velocity
2
1
Movement
0
0
Static Force
6
0
Position
0
0
Conduction
Velocity
0.5-8.5
m/sec
(n=2)

Post-test
Spontaneous
Activity

0


Ill
TABLE G-21
FFFFrT OF S At INF
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #1
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
4.3N
6.4N
2.1N
Freq. Asymptote
26N
35N
9.0N
Mean Rate
2.5
3.2
0.7
Slope
-2.1
-0.74
-1.36
Freq. Thres.



2
R
0.77
0.27
-0.50
Force Velocity
Act. Thres.
7.ON
5.0N/S
-2.0N
Freq. Asymptote
122N
154N/s
13N/s
Mean Rate
2.0
2.6
0.6
Slope
-0.57
-0.21
-0.36
Freq. Thres.



2
R
0.42
0.31
-0.11
Static Force
Act. Thres.
7.IN
2.8N
-4.3N
Freq. Asymptote
27 N
29N
2.0N
Mean Rate
2.9
2.9
0.0
Slope
-1.5
-.72
-0.78
Freq Thres.
7.ON
1.4N
-5.6N
2
R
0.60
0.68
0.08


115
TABLE G-25
ppppOT OF SAI INF
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #6
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
46N
25N
-21N
Freq. Asymptote
71N
59N
-12N
Mean Rate
5.5
4.2
-1.3
Slope
-1.7
-1.2
-0.05
Freq. Thres.



2
R
0.37
0.43
-0.06


78
tero, nerve fibers were observed in the disc; further development was accompanied by a
reduction in disc innervation. Corroboration of the influence of growth on disc innervation
came from Hromada (1960), who observed free nerve endings in the disc of various
animals; at older ages such endings were limited to the periphery of the disc. By
comparison, the nerve supply to the meniscus of the human knee remains unclear (For
review see Zimny, 1988). The most recent study (Albright and Zimny, 1987) reports that
free and complex nerve endings were observed in outer and middle one-third of the
meniscus; whereas, no innervation was found in the inner one-third.
Innervation of the TMJ of the monkey and cat resemble that of the human joint
(Franks, 1965; Keller and Moffett, 1968). Branches from the deep temporal and
masseteric nerves supply the anterior capsule, and the articular branches of the
auriculotemporal nerve supply the TMJ posteriorly. Preliminary macrodissection of the
nerves innervating the TMJ of one goat was performed in this laboratory. The
auriculotemporal nerve gave off three articular branches along the posterior aspect of the
neck of the condyle. The articular branches ascended into the fatty and fibrous articular
tissue. The termination of the temporal branch of the auriculotemporal nerve appeared in
the facial skin inferior to the zygomatic arch. The masseteric nerve was observed to arise
from the anterior trunk of the mandibular nerve, course lateral along the anterior border of
the capsule of the TMJ and terminate in the superficial and deep masseter muscle. Twigs
from the masseteric nerve appeared to enter the anteriorlateral aspect of the capsule.
Tissues surrounding articulations possess fewer types of receptors than muscle or
cutaneous tissue. Thilander (1961) described four types of neural endings in the human
TMJ: Ruffini-like receptors, modified Pacinian endings, Golgi tendon organs and free
nerve endings. Ishibashi (1966) also reported the presence of free nerve endings and
complex terminal expansions in the human TMJ. Keller and Moffett (1968) reported free
and complex nerve endings in the TMJ of monkeys. Many investigators have identified


128
Skoglund S (1956). Anatomical and physiological studies of knee joint innervation in the
cat. Acta Physiol Scand (Supplement 36) 124: 1-101.
Skoglund S. (1973). Joint receptors and kinaesthesis. In: Handbook of Sensory
Physiology. A Iggo (ed), Vol II, Somatosensory System. Springer-Verlag, Berlin,
p. 111-136.
Solberg, WK (1987). Epidemiological findings of importance to management of
temporomandibular disorders. In: Perspectives in Temporomandibular Disorders.
GT Clark and WK Solbert (eds). Quintessence Publishing Co, Chicago, p. 27-44.
ThilanderB (1961). Innervation of temporomandibular joint capsule in man. Trans R
School Dent Umea 2: 1-67.
Travell J (1976). Myofascial trigger points: clinical view. In: Advances in Pain Research
and Therapy. JJ Bonica and D Albe-Fessard (eds), Raven, New York, p. 919-
926.
Turnbull WD (1970). Mammalian masticatory apparatus. Fieldiana. Geology. Vol 18,
No 2 (Field Museum of Natural History, Chicago).
van den Berghe L, de Boever JA, Brockhuijsen ML and van Willigen JD (1987). On the
perception of the preferred jaw position in patients with symptoms of
temporomandibular disorders. J Craniomand Pract 5: 344-350.
van Willigen JD, Broekhuijsen ML, de Bont LGM and van der Kuijl B (1986). On the
perception of jaw position and bite force by subjects with craniomandibular
disorders. J Craniomand Pract 4: 128-133.
Vinegar R, Truax JF, Selph JH, Johnston PR, Venable AL and McKenzie KK (1987).
Pathway to carrageenan-induced inflammation in the hind limb of the rat.
Federation Proc 46: 118-126.
Weinmann JP and Sicher H (1951). Histophysiology of the temporomandibular jont. In:
The Temporomandibular Joint. BG Samat (ed), Thomas, Springfield, p. 71-75.
Widenfalk B and Wiberg M (1990). Origin of sympathetic and sensory innervation of the
temporo-mandibular joint. A retrograde axonal tracing study in the rat.
Neuroscience Letters 109: 30-35.
Williams WN, Henry MA and Mahan PE (1989). The effect of experimental anesthetization
of temporomandibular joint superior cavity on bite force discrimination. J
Craniomand Pract 7: 194-199.
Williams WN, LaPointe LL, Mahan PE and Cornell CE (1984). The influence of TMJ and
central incisors impairment on bite force discrimination. J Craniomand Pract 2: 119-
124.
Willis WD and Coggeshall RE (1978). Sensory Mechanisms of the Spinal Cord. Chapter
2. Plenum Press, New York, p. 9-51.
Yemm R (1979). Neurophysiologic studies of temporomandibular joint dysfunction. In:
Temporomandibular Joint Function and Dysfunction. GA Zarb and CE Carlsson
(eds), Mosby, St Louis, p. 215-237.


Figure 3-6. Averaged dynamic response functions of nociceptors fitted in normal and
previously inflamed tissue (PI). A) Mean function for dynamic force
fitted in PI tissue (mean interval = 29.9 7.9 msec) falls below the mean
dynamic force function fitted in normal tissue (mean interval = 44.7
16.5 msec) suggesting sensitization. B) Mean function for force velocity
in PI tissue (mean interval = 22.2 3.3 msec; mean activation threshold =
17.3 18.9 N/s) falls below and to the left of mean force velocity
function fitted in normal tissue (mean interval = 7.4 + 4.8 msec; mean
activation threshold = 4.8 + 4.5 N/s) suggesting enhanced reactivity
(sensitization)


36
Statistical comparisons between function characteristics in normal and inflamed
tissues confirmed that dynamic reactivity improved in inflamed tissues (See Table 3-3).
This was manifested as changes in activation threshold, frequency asymptotes and function
intercepts. The mean activation threshold (8.3 13.2 N) for units in inflamed tissue (n =
4) that responded best to jaw opening and transduced dynamic force was significantly
lowered relative to the mean activation threshold (24.1 + 11.2 N) for VP units (n = 10) in
normal tissue (F = 5.36, df = 13, p < 0.04). For those same units, the mean intercept in
inflamed tissue (5.0 + 3.0) was significantly decreased relative to the mean intercept in
normal tissue (9.0 3.1). Similar changes were observed for afferents that transduced
force velocity. The mean frequency asymptote (37.5 + 23.6 N/s) for these units was
significantly less than the mean frequency asymptote (148.0 79.6 N/s) for units (n = 8),
in normal tissue (F = 8.89, df = 12, p < 0.01). The mean force-frequency asymptote (40.2
+ 22.2 N/s) for PI units (n = 6) that coded for force velocity in both VP and HP jaw
movements were significantly less than the mean force-frequency asymptote (156.5 83.1
N/s) for VP and HP units (n = 15) in normal tissue (F = 9.57, df = 21, p < 0.01).
The changes we have observed in dynamic reactivity of TMJ nociceptors are
suggestive of sensitization. However, experiments of this type (PI tissue) are subject to
sampling errors. The best form of evidence for nociceptor sensitization comes from
observations of single affferents making transitions from the normal to the sensitized state,
following acute injections of pro-inflammatory substances.
Experiment II: Properties of Units in the
Acutely Inflamed TMJ
The findings of enhanced dynamic reactivity observed in populations of afferents
sampled from normal and subacutely inflamed TMJ tissues were complemented by
observations made on units in which testing was performed before and after carrageenan-


15
tissue. In this instance, inflammation was induced at least 6 hours before recording began.
Carrageenan (2%, 200 jil) was injected into the lateral and posterior aspects of the TMJ
capsule as well as the superior joint space.


101
TABLE G-11
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE VERTICAL PLANE
UNIT #2
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
6.0N
27 N
21N
Freq. Asymptote
33N
66N
33N
Mean Rate
4.8
3.0
-1.8
Slope
-0.44
-0.46
0.01
Freq. Thres.



2
R
0.42
0.11
-0.31
Movement
Act. Thres.
8.0
23*
15*
Freq. Asymptote
24
28
4.0*
Mean Rate
4.1
7.3
3.2
Slope
-0.8
-2.5
1.7
Freq. Thres.



Z
R
0.48
0.19
-0.29
Static Force
Act. Thres.
25N
Freq. Asymptote

59N

Mean Rate
.
3.6
Slope
.
-1.5

Freq Thres.

12.0

2
R
.
0.62
.


28
TABLE 3-2
TMJ NOCICEPTOR REACTIVITY IN NORMAL TISSUE
Test Conditions
with RF (n=36)
without RF (n=14)
code (n=25)
no code (n=10)
code (n=9)
no code (n=5)
Dynamic Force
23
12
6
6
Force Velocity
15
19
4
8
Movement
5
10
2
3
Static Force
8
23
1
4
Static Position
1
14
0
4
Conduction
Velocity
0.4 to 7.5
m/sec
(n = 6)
0.5 to 1.5
m/sec
(n = 3)


Post-test
Spontaneous
Activity
3
0
0
0
Note: Receptive fields (RF) in the TMJ capsule were identified for 36 units. Twenty-five
units with RFs coded for one or more of the stimuli. Most units (n = 23) with an
RF on the TMJ capsule coded for dynamic force. Fourteen additional units had
either VP or HP reactivity but an RF could not be found. "Code" indicates that a
unit's reactivity could be described by a significant power function. Of the 36
afferents with RFs in the TMJ capsule, 3 units demonstrated spontaneous
activity after dynamic or static testing. Five units with RF's in the TMJ capsule
responded preferentially to right lateral displacement. Most of these units ( 3 of
5 cases) coded dynamic force. Appendix G contains descriptive statistics for
these units.


55
and/or chemical stimuli. In our experiments, where afferents were sampled from
previously inflamed capsular tissue or where characterized afferents were retested in acutely
inflamed tissue, a variety of forms of sensitization was found. These changes included a
significant decrease in mean activation threshold, shifts in stimulus response functions and
qualitative forms of sensitization. Additional changes were observed for afferents in the PI
condition (frequency asymptote and intercept) that were not replicated in the AI condition.
Recent experiments on cat knee joint nociceptors (Schaible and Schmidt, 1988b)
have also produced evidence of changes in reactivity following carrageenan injection. Over
half of the units that were classified as nociceptors in normal tissue responded to innocuous
joint movements in the normal range of motion after inflammation. In effect, such
enhanced reactivity, from extremes of movement to the normal range of motion indicates a
decreased activation threshold. In our experiments, decreases in activation threshold were
observed following carrageenean-induced inflammation. These decreased activation
thresholds fell within the linear phase of force-movement relationship.
In our study, qualitative forms of sensitization were also observed. These appeared
both in carrageenan treated nociceptors (8 of 11 cases), and infrequently in saline treated
controls (1/8). The nature of these qualitative changes can be best appreciated by
comparing scatter plots representing comparisons between preinflamed and postinflamed
reactivity. It is important to examine scatter plots because the acquisition of transducing
ability could have represented a distorted outcome. For example, outliers could have
rendered functions insignificant where they were otherwise significant. However,
examination of plots following carrageenan showed new relationships between force and
response interval and shifts to greater reactivity.
Two types of trends were observed: rotation and shift. Rotational trends were
indicated by a change in slopes which suggested increased proportional reactivity. A shift
to the left represented a decrease in activation threshold that was seen consistently in AI and
PI conditions for units with extant coding capacity. The shifts that were observed, were


113
TABLE G-23
FFFFCT OF SAT INF
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #3
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
13N
15N
2.0N
Freq. Asymptote
49N
28N
-21N
Mean Rate
3.5
3.5
0.0
Slope
-0.74
-0.83
0.09
Freq. Thres.



2
R
0.45
0.28
-0.11
Static Force
Act. Thres.
1 IN
7.ON
-4.0N
Freq. Asymptote
38N
41N
3.0N
Mean Rate
3.75
3.71
-0.04
Slope
-0.53
-0.48
-0.05
Freq. Thres.
8.ON
6.ON
-2.0N
2
R
0.36
0.28
-0.08


A
D
REACTIVITY IN VERTICAL PLANE: NORMAL TO INFLAMED REACTIVITY IN HORIZONTAL PLANE: NORMAL TO INFLAMED
DYNAMIC FORCE: UNIT #1 DYNAMIC FORCE: UNIT #2
Ln Foro* fr'towior*)
Ln Fore* t^*wton*)
N 1 KR 3 l-R
1 FR 2 FR
B
E
REACTIVITY IN VERTICAL PLANE: NORMAL TO INFLAMED REACTIVITY IN HORIZONTAL PLANE: NORMAL TO INFLAMED
DYNAMIC FORCE: UNIT #3 DYNAMIC FORCE: UNIT #5
Ln Fore* Ln Fore* 1 HR
2-5 HR
c
F
REACTIVITY IN VERTICAL PLANE: NORMAL TO INFLAMED REACTIVITY IN HORIZONTAL PLANE: NORMAL TO INFLAMED
DYNAMIC FORCE: UNIT #4 DYNAMIC FORCE: UNIT #6
Ln Fore* f'tewtora)
Ln Fore* f'fewtont)
T- N
- 90
2 FR
V- N
- 1 FR


APPENDIX F
GROSS ANATOMY
The TMJ in mammals is a ginglymus-arthroidal joint, i.e., a hinge joint capable of
gliding movement (Figure F-l). The craniomandibular articulation involves the condyle of
the mandible juxtaposed with the articular surface of the squamous portion of the temporal
bone. Interposed between the condyle and the articular fossa is an articular disk dividing
the articular space into upper and lower compartments.
The periarticular soft tissue consists of fibrous capsule, posterior attachment
tissues, synovial membrane and accessory ligaments. Except for the synovial membrane,
these tissues serve to limit the range of motion of the joint and to maintain a packed position
(Sicher, 1960; Rocabado, 1983). A packed position is the condyle-disc-fossa relationship
which juxtaposes these TMJ elements at rest and during mandibular movements. The joint
capsule is loose and composed of dense connective tissue with a collagenous matrix richly
supplied with blood vessels and nerves. The dense connective tissue of the capsule is
located primarily on the lateral and medial aspect of the joint and intimately associated with
the temporomandibular and sphenomandibular ligaments, respectively. The anterior
capsule arises from the suture line between the greater wing of the sphenoid bone and the
temporal bone. It inserts on the anteriorlateral aspect of the condylar neck. The loose
connective tissue of the capsule encompasses the joint posteriorly. It arises from the tragal
cartilage laterally and tympanic plate medially. The posterior capsule, as a meshwork of
unorganized collagen fiber, inserts and blends in with the posterior periosteum of the
condylar neck and upper capsule of the parotid gland.
86


LIST OF FIGURES
Figure 2-1 Mandibular movements were produced by a hand held probe 8
Figure 2-2 Dynamic and static test series for force, displacement and velocity 10
Figure 2-3 Demonstration of sensitization as a shift of stimulus-response functions.. 14
Figure 3-1 Receptive field distribution in the lateral and posterior capsule of the
temporomandibular joint for normal tissue 18
Figure 3-2 Receptive field distribution in the lateral and posterior capsule of
the temporomandibular joint for previously inflamed tissue, acutely
inflamed tissue and saline control tissue 20
Figure 3-3 Relationships between applied force and vertical plane movements of
the mandible 23-24
Figure 3-4 Dynamic reactivity in normal tissue 30
Figure 3-5 Dynamic reactivity in previously inflamed tissue 33
Figure 3-6 Averaged dynamic response functions of nociceptors fitted in normal
and previously inflamed tissue 41
Figure 3-8 Reactivity of nociceptors exposed to saline 43
Figre 3-9 Comparison between pre-inflamed and post-inflamed reactivity in
scatter plot forms 48-49
Figure F-l Schematic diagram of the human temporomandibular joint. Sagittal and
frontal views 87
viii


43
A B
REACTIVITY IN HORIZONTAL PLANE: SALINE CONTROL REACTIVITY IN HORIZONTAL PLANE: SALINE CONTROL
DYNAMIC FORCE: LEFT LATERAL UNIT #3 DYNAMIC FORCE: LEFT LATERAL UNIT #6
Ln Foro* t'tewton*J
Ln Fore* r*wlon*J
S1H
C D
REACTIVITY IN HORIZONTAL PLANE: SALINE CONROL REACTIVITY IN HORIZONTAL PLANE: SALINE CONTROL
DYNAMIC FORCE: LEFT LATERAL UNIT #2 DYNAMIC FORCE: LEFT LATERAL UNIT #7
E
REACTIVITY IN HORIZONTAL PLANE: SALINE CONTROL
DYNAMIC FORCE: RIGHT LATERAL UNIT #1
0 1 2 3 4 5
Ln Foro O't*wton*>
n
- S1h#3
- S2K3


74
patients had lower values for submaximal bite force (3-25 kg) compared to control subjects
(5-50 kg).
Bite Force Discrimination
In order for an individual to control the different levels of bite force, he/she must be
able to discriminate differences in the intensity of their own biting force. The role of TMJ
mechanoreceptors in bite force discrimination has been investigated in normal subjects
(Williams et al., 1984; Williams et al., 1989). Bite force was assessed before, during and
after anesthetization of the TMJ by auriculotemporal nerve block (Williams et al., 1984) or
infiltration into the superior joint cavity (Williams et al., 1989). These studies suggest that
the TMJ mechanoreceptors do not appear to be responsible for discrimination of bite force.
In summary, maximum bite force, submaximal bite force and bite force
discrimination are three commonly used measures of mandibular function. Studies
assessing maximum and submaximal bite force indicate that patients suffering from TMJ
disorders have decreased bite force strength. The ability to discriminate bite force levels
has not been studied in patients having TMJ disorders. Neither maximum bite force,
submaximal bite force nor bite force discrimination measures have provided clear
information on the relationship between TMJ sensory input and mandibular function.


Figure 3-5. Dynamic reactivity in previously inflamed tissue. Power functions best
described the relationship between instantaneous dynamic force and force
velocity with instantaneous response interval in the vertical or horizontal
plane. A) Six of 7 units transduced dynamic force (mean slope = -1.1
0.5; range = 7.6 10.2 to 33.3 32.1 N; mean R2 = 0.24 0.16). B)
Six of 7 units transduced force velocity (mean slope = -0.7 0.8; range =
4.8 4.5 to 40.2 22.2 N/s; mean R2 = 0.33 0.28).


I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
Parker MahanfChairman
Distinguished Service Professor
of Oral Biology
I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
Brian Cooper, Cochairman
Assistant Professor of Neuroscience
I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a;
dissertation for the degree of Doctor of Philosophy.
'Charles Viei
Professor


57
Factors Contributing to Sensitization
Mechanical sensitization of joint afferents, following inflammation, is likely to be
due to the production and release of endogenous substances. Injection of carrageenan
produces a rapid inflammation that has been characterized in a number of behavioral and
physiological preparations (Vinegar et al., 1987). Various factors may contribute to
sensitization of joint afferents during carrageenan-induced inflammation, including both
edema and the formation and release of algesics.
Changes in the response properties of joint afferents during inflammation have been
attributed to the actions of bradykinin, prostaglandins, and serotonin. These mediators
may alter mechanical responsivity of afferents, modify chemical responsivity, activate
afferents or a combination of the three. Changes in reactivity of small fibers in inflamed
tissue to bradykinin have been observed (Kanaka et al., 1985; He et al., 1990; Grubb et
al., 1991). Bradykinin activates most group III and IV units that responded to passive joint
movement. Bradykinin also activates afferents otherwise classified as "silent" (Heppleman
et al., 1987).
Joint afferents can also be activated by prostaglandin (E or I). Prostaglandins Ei or
E2 activated small afferents which responded to passive joint movement (Heppleman et al.,
1985; Schaible and Schmidt, 1988a), and modified mechanical responses of these
afferents. Following exposure to PGE2, most group III and some group IV units showed
enhanced joint movement reactivity and responded within the normal range of motion.
These PGE2-evoked increases in unit responsiveness paralleled those observed during
acute arthritis (Schaible and Schmidt, 1985, 1988a). Similar properties have been
prescribed for PGI2, and it has been suggested that PGI2 may be the dominant PG in joint
afferent sensitization ( Birrell et al., 1991; McQueen et al., 1991).
Interactions between pro-inflammatory mediators are also likely to be important, but
they have not been determined in much detail. Prostaglandin Ej (Schaible, 1983) and


ACKNOWLEDGEMENTS
I thank Dr. Brian Cooper, Ph.D., for his technical guidance in the research
involved in this dissertation. I thank Ms. Martha Oberdorfer for her technical assistance. I
thank Dr. Parker Mahan, D.D.S., Ph.D., and Dr. Arnold S. Bleiweis, Ph.D. for their
strategic guidance. I thank Dr. Robert Bates, D.D.S., M.S. for his administrative
assistance.


27
a unit's reactivity was proportional to force or some other stimulus variable and that the
relationship could be described by a significant power function.
The great majority of TMJ nociceptors (n = 24) coded dynamic aspects of force
applied to the mandible, and relatively few coded for static aspects of these stimuli.
Twenty-three of 36 units that responded to either VP or HP jaw movement coded for
dynamic force (mean activation threshold = 20.1 17.5 N) and 15 of 36 units coded for
force velocity (mean activation threshold = 15.5 20.5 N/s; Table 3-2). In contrast, only
8 of 36 units coded for static force (mean activation threshold 17.8 18.3 N), while 5 of
35 units coded jaw movement (mean activation thresholds of 11.0 4.0, and only 1 of
36 units coded for jaw position. In some cases, unit reactivity could be described by more
than one function. Twelve of 23 units that could be fit to dynamic force were also
significantly fit to force velocity. Six of these 12 units were significantly fit to force
velocity, and 6 of these 12 units were signficantly fit to static force as well. Ten of 36 units
could not be fit to any function. Fourteen additional units had jaw movement reactivity but
no receptive field could be found.
Mean functions were generated from individually fitted functions by pooling
slopes, intercepts and boundary values. Functions presented in Figure 3-4 represent the
principle transducing properties of TMJ afferents: dynamic force and force velocity.
Properties of TMJ Nociceptors in Inflamed Tissue
The response properties of afferents were examined in capsular tissue that was
previously inflamed (PI) by carrageenan. In these experiments, TMJ tissues were exposed
to carrageenan for at least 6 hours prior to testing. In other experiments, afferents were
tested in normal tissue and then tested again after an acute injection of carrageenan or
saline. Afferent reactivity was examined for up to 3 hours subsequent to exposure to
carrageenan.


85
HRP into the TMJ and insertion of the lateral pterygoid muscle of rats. They found no
central projection to the mesencephalic nucleus.
Somatotopv
There is general agreement that the trigeminal ganglion in cats is somatopically
represented from a medial to lateral direction (Beaudreau and Jerge, 1968; Zucker and
Welker, 1969; Kerr and Lysak, 1964; Darian-Smith et al., 1965; Marfurt, 1981). The
ophthalmic division lies anteriomedially, the mandibular division lies posteriolaterally and
the maxillary division is situated in an intermediate position. Overlap between divisions
has been reported (Marfurt, 1981; Henry et al., 1986). Romfh et al., (1979) and Capra
(1987) reported that injection of HRP into the capsular tissues of the TMJ in the cat resulted
in a restricted distribution of label in the posteriolateral position of the trigeminal ganglion.
Very few labeled cells were found in the most dorsal or in the most ventral areas of the
mandibular division of the trigeminal ganglion. The majority of labeled cells is found
throughout the intermediate zone in the posteriolateral part of the ganglion.
Electrophysiological studies in cats (Capra and Gaitpon, 1981) and in rabbits (Lund and
Matthews, 1981; Appenteng et al., 1982) confirmed that TMJ afferents were located in the
posteriolateral region of the trigeminal ganglion.
In addition to the mediolateral somatotopy studies suggest a dorsoventral
somatotopic organization (Kerr and Lysak, 1964; Marfurt, 1981; Capra, 1987).
Representation of oral and perioral structures appear ventral in the ganglion. Areas remote
from the mouth lie in the dorsum of the ganglion.


25
Table 3-1
Force/Movement Relationships in the Vertical Plane
FILE
FUNCTION
FULL RANGE
LOW RANGE
2
R
P
042090H
POW
Lnl = 0.69 LnF + 4.8
0.93
0.0001
042090H
LIN
I = 0.15 F+ 1.8
0.90
0.0001
042090H
POW
Lnl = 0.8 LnF + 0.89
0.96
0.0001
042090H
LIN
I = 0.2F + 0.87
0.95
0.0001
110990E
POW
Lnl = 0.8 LnF + 2.1
0.97
0.0001
1I0990E
LIN
I = 0.6 F + 2.3
0.96
0.0001
110990E
POW
Lnl = 1.1 LnF + 0.15
0.92
0.0001
110990E
LIN
I = 1.0 + 0.19
0.97
0.0001
111490D1
POW
Lnl = 0.4 LnF + 1.1
0.91
0.0001
111490D1
LIN
I = 0.1F + 8.5
0.87
0.0001
111490D1
POW
Lnl = 1.7 LnF+ 2.2
0.92
0.0001
111490D1
LIN
I = 1.0F + 4.2
0.86
0.0001
111490D2
POW
Lnl = 1.3 LnF + 1.2
0.91
0.0001
111490D2
LIN
I = 0.7F+ 0.22
0.87
0.0001
111490D2
POW
Lnl = 2.3 LnF + 3.5
0.94
0.0001
111490D2
LIN
1= 1.4F + 7.4
0.97
0.0001
022791A
POW
Lnl = 0.3 LnF + 2..2
0.93
0.0001
022791A
LIN
I = 0.77F + 11.0
0.79
0.0001
022791A
POW
Lnl = 0.15 LnF +2.0
0.80
0.04
022791A
LIN
1= 1.8F + 5.9
0.97
0.0001
03289IX
POW
Lnl = 0.37 LnF + 1.1
0.99
0.0001
03289IX
LIN
I = 0.23F + 3.7
0.88
0.0001
03289IX
POW
Lnl = 0.4 LnF + 0.01
0.98
0.0001
03289IX
LIN
I = 0.55F + 2.3
0.88
0.0001
080591C
POW
Lnl = 0.34 LnF + 1.9
0.87
0.0001
080591C
LIN
I = 0.28F + 12.0
0.77
0.0001
080591C
POW
Lnl = 0.46 LnF + 1.8
0.57
0.0003
080591C
LIN
1= 1.5 F +5.3
0.61
0.0001
091691A
POW
Lnl = 0.54 LnF + 1.3
0.87
0.0001
091691A
LIN
I = 0.42F + 9.0
0.83
0.0001
091691A
POW
Lnl = 0.64 LnF + 1.2
0.52
0.01
091691A
LIN
I = 2.3 F+ 1.3
0.37
0.04
09279 IK
POW
Lnl = 0.48 LnF + 1.4
0.96
0.0001
09279 IK
LIN
I = 0.37 F + 8.6
0.88
0.0001
09279IK
POW
Lnl = 0.59 LnF + 1.3
0.90
0.0001
09279IK
LIN
1 = .97F + 4.1
0.88
0.0001
101891F
POW
Lnl = 0.5 LnF + 1.3
0.83
0.0001
101891F
LIN
I = 0.29F + 11.0
0.73
0.0001
101891F
POW
Lnl = 0.74 LnF + 1.0
0.86
0.0001
101891F
LIN
I = 0.9 F + 5.6
0.64
0.0001
Note: POW, power, LIN, linear.


6
3000A). Data were recovered from tape for analysis with an RC computerscope (RC
Electronics) or captured on a line by a thermal printer (Astromed, Dash IV).
After a unit was characterized, the conduction velocity was determined by
measuring the latency of responses to suprathreshold electrical stimulation applied to the
receptive field on the TMJ capsule. Electrical stimulation was performed with a Grass S88
stimulator and isolated, constant current unit. Square-wave pulses of 0.2 to 2 msec
duration were applied with monopolar electrodes. Conduction distance was estimated in
situ.
Characterization of TMJ Afferents
Once an afferent was isolated, passive jaw movements were used to determine
which type of movement was preferred (preferred movements were those which produced
*
the most vigorous response). Jaw movements included: 1) vertical jaw movements from
the closed to the open position. Afferent responses to vertical jaw movements were termed
"vertical plane reactivity" (VP); 2) lateral jaw movements from the closed to extreme lateral
position. Afferent responses to the lateral jaw movements were termed "horizontal plane
reactivity" (HP).
A force probe was used to produce jaw movement. The probe consisted of an axial
force transducer (Entran Instruments, Model ELF TC500-20) embedded in a plexiglass
rod. The transducer monitored forces used to move the jaw in the vertical or horizontal
plane. The probe was applied to fixed points of a bit which was mounted to the incisal
teeth of the mandible at the midline. Force and jaw movement were recorded on video tape
along with afferent activity. Jaw movement was monitored by an angular displacement
transducer (ADT, Trans-Tek Model # 604-001) mounted above the right TMJ (Figure 2-1).
Using the probe, both dynamic and static forces were applied to the mandible (Figure 2-2).


Figure 3-7. Demonstration of sensitization (enhanced reactivity). Six of 11 units
were characterized in normal tissue and then tested again after acutely
inflamed (AI) with carrageenan. Power functions generated from
retesting in acutely inflamed tissue were positioned below and/or to the
left of power functions fitted on normal tissue. N, normal, Min,
inflamed; HR, inflamed.


A
REACTIVITY IN VERTICAL PLANE: NORMAL TO INFLAMED
FORCE VELOCITY: UNIT #1
0 1 2 3 4 5 6
Ln Velocity (Newtons/sec)
o n 2m* 2 m-+- 3m* 3 m
B
REACTIVITY IN VERTICAL PLANE: NORMAL TO INFLAMED
FORCE VELOCITY: UNIT #3
Ln Velocity (Newtons/sec)
O N 1 HR 1 HR
C
REACTIVITY IN HORIZONTAL PLANE: NORMAL TO INFLAMED
STATIC FORCE: UNIT #2
0 1 2 3 4 5 6
Ln Force (Newtons)
O N 2 m 2 m
D
REACTIVITY IN HORIZONTAL PLANE; NORMAL TO INFLAMED
STATIC FORCE: UNIT #7
Ln Force (Newtons)
O n
1 l-R
1 HR


46
Table 3-4 (cont'd).
UNIT
PLANE
PRE-INFLAMED
POST-INFLAMED
CODING
SHIFT
OTHER
MOVEMENT
POST-TEST
SPONTAN.
ACTIVITY
5
HP
DYNAMIC FORCE
YES
FORCE VELOCITY
YES
YES
STATIC FORCE
YES
6
HP
DYNAMIC FORCE
DYNAMIC FORCE
FORCE VELOCITY
FORCE VELOCITY
STATIC FORCE
YES

YES
7
HP
DYNAMIC FORCE
DYNAMIC FORCE
OPEN: CODE
NO\E
FORCE VELOCITY
FORCE VELOCITY
OPEN: CODE
STATIC FORCE
YES
OPEN: NON-CODE
8
HP
DYNAMIC FORCE
DYNAMIC FORCE
YES
FORCE VELOCITY
FORCE VELOCITY


STATIC FORCE
STATIC FORCE
9
HP
DYNAMIC FORCE
DYNAMIC FORCE

OPEN: CODE
YES
1 0
HP
DYNAMIC FORCE
DYNAMIC FORCE
STATIC FORCE
STATIC FORCE


NOME
1 1
HP
DYNAMIC FORCE
YES
OPEN: NON-CODE

FORCE VELOCITY
YES
OPEN: NON-CODE
STATIC FORCE
YES
OPEN: NON-CODE
NONE
Note: HP, horizontal plane


69
movement and maximum opening. The authors suggested that the lateral ligament may be
associated with a protective mechanism during extreme opening. Klineberg (1980) also
anesthetized the TMJs of normal subjects and observed an increase in size of the envelope
of function (range of motion), and suggested that mechanoreceptors of the TMJ play a
modulatory role in motor control of the mandible.
One measure of jaw movement is maximum range of motion (ROM). The
measurement is made for opening, lateral and protrusive excursions. An assessment of
ROM for normal subjects has been reported by Posselt (1968). For normal subjects (adult
males) maximum opening averages 50-60 mm; hinge opening, 20-25 mm; lateral excursion
from midline, 10 mm; and protrusive excursion, 10 mm. Anaesthesization of the lateral
capusle of the TMJ increased hinge opening and protrusion by 10-15% (Posselt and
Thilander, 1965). For patients suffering from TMJ disorders, ROM is generally limited
compared to normal subjects. Helkimo (1974) devised a pain-dysfunction index which
rates severity of mandibular function in regard to pain report for jaw movement and TMJ
palpation. This index was modified by Zarb and Carlsson (1988). Normal ROM was >39
mm for opening and >6 mm for lateral excursions. For patients, ROM was 30-39 mm for
opening and 4-6 mm for lateral excursions. Patients with this amount of impairment
reported pain during at least one jaw movement and pain on palpation of the TMJ's. For
other patients, ROM was <30 mm for opening and <4 mm for lateral excursions. Patients
with this amount of impairment reported during 2 or more jaw movements and pain on
palpation of the TMJ's.
Many clinicians observe a decrease in ROM for patients suffering from TMJ
disorders. These patients are often hesitant to open their mouth maximally because of real
or expected pain. As a result, a measure of ROM may result in a value less than the patient
is actually capable of producing. Therefore, other components of mastication may be more
likely to be reliable measures of jaw function. Moreover, the movements of the mandible


Note: DF, dynamic force; FV, force velocity; M, movement; SF, static force; P, position; ^ct. Thres., activation
threshold; Freq. Asym., frequency asymptote; Freq. Thres., frequency threshold; R coefficient of
determination; MRI, mean response interval (natural log value).


44
Therefore while shifts in activation threshold could occur following repeated testing, the
changes that followed carrageenan injection were significantly greater.
In experiment I, it was determined that most TMJ nociceptors transduced dynamic
force and velocity, but few transduced either static force, movement or position.
Following acute exposure to carrageenan, qualitative changes in coding capacities were
noted; that is, afferents coded for stimulus features not previously transduced.
Qualitative improvements were observed for most units for either dynamically or
statically applied stimuli. Eight of 11 nociceptors acquired either dynamic or static coding
ability (Table 3-4). Four of 4 units that preferred VP jaw movement and transduced
dynamic force in normal tissue acquired the ability to transduce force velocity (n = 2), static
force (n = 1) or jaw position (n = 1) in inflamed tissue. Two of 5 AI units that preferred
HP movement and transduced dynamic force in normal tissue also acquired the ability to
transduce static force. Acquired coding also appeared in nociceptors that were without
transducing capacity in normal tissue. Two of 7 AI units that preferred HP movement
acquired the capacity to transduce both dynamic and static force. Other changes appeared
as de novo reactivity. Three of 7 units that had only HP jaw movement initially acquired
similar reactivity for VP movement (dynamic force). Six units demonstrated spontaneous
activity after stimulus testing.
The finding that a large proportion (8/11) of nociceptors acquired coding ability
after exposure of carrageenan suggested a qualitative form of sensitization. The nature of
these qualitative changes can be best appreciated by comparing scatter plots representing
comparisons between pre-inflamed and post-inflamed reactivity. Two types of trends (shift
and rotation) were observed. Shift indicates a movement of a scatter of points into graphic
zones of greater sensitivity. Rotation indicates the development of a significant slope
associated with the scatter field of points. Of the 9 of 11 nociceptors that acquired coding
ability, all 9 showed shifts and/or rotation. Figure 3-9 illustrates significant functions of
units that demonstrated shifts and units that demonstrated rotation of scatter point fields.


14
DEMONSTRATION OF SENSITIZATION
SHIFT OF STIMULUS-RESPONSE CODING FUNCTION
0 1 2 3 4 5
Ln Force (Newtons)
V Function A Function B
Figure 2-3. Demonstration of sensitization as a shift of stimulus-response
functions. Shifts of significant stimulus-response functions to graphic
zones of enhanced reactivity (below and to the left) suggests
sensitization. For downward shifts, each point on line B represents a
higher rate of discharge (shorter interval) at an equivalent force. For
leftward shifts, reactivity appears at forces which previously were
ineffective.


23
TMJ FORCE/MOVEMENT RELATIONSHIPS: VERTICAL PLANE
A D
TEST
1
FORCE (N*wton*)
TEST -- TEST
2 3
TEST
4
1 2 3 4 5
B
E
FORCE (Newton*)
-4- TEST-4- TEST-4- TEST-- TEST-4- TEST
1 2 3 4 5
FORCE (Newton*)
-4- TEST-4- TEST-- TEST-- TEST-4- TEST
1 2 3 4 5
c
F
FORCE (Newton*)
-4- TEST-4- TEST-4- TEST-- TEST -4- TEST
1 2 3 4 5
FORCE (Newton*)
4- TEST
1
TEST
2
- TEST
3


63
posterior attachment tissues become taut. Mechanoreceptors in the capsule and posterior
attachment tissues are activated by the resultant tension. Thus, these mechanoreceptors
appear to act as detectors that sense the safe limits of joint movement. Supposedly, jaw
movement beyond safe limits can represent real or potential tissue damaging stimuli. If
these mechanoreceptors are nociceptors, they may be sensitized following capsulitis so that
small movements in the functional range of motion produce pain. Clark and Burgess
(1975) suggested that large, myelinated afferents signal the pressure felt as the extremes of
joint movement are reached. These investigators demonstrated that slowly adapting
receptors in the capsule were excited only at extremes of flexion and extension of the knee
joint of the cat (Burgess and Clark, 1969). On the other hand, Schaible and Schmidt
(1983b) attribute a similar detection role for small fibers which are active only at the
borders of the joint movement.
Following capsulitis, the tension required to produce activation of nociceptors
might be greatly reduced. Animals studies in the cat knee joint (Schaible and Schmidt,
1988b) and rat ankle joint (Guilbaud, 1988) have demonstrated increased responsiveness
of group III and IV afferents to innocuous mechanical stimulation after induction of acute
inflammation The relationship between nociceptor discharge and capsular tension is yet to
be demonstrated.
The reactivity of mechanoreceptors in the capsule of the cat knee have been used to
assess tension produced by joint movement (Grigg and Hoffman, 1989; Hoffman and
Grigg, 1989). The frequency of neurons with receptive fields in the posterior capsule
showed a linear relationship with tension applied (knee extension) at the area of the
receptive field. The posterior joint capsule was minimally loaded even during
hyperextension movements.


83
al., 1983). One consistent feature of the neuronal reactivity seen in all of these studies is
the increase responsiveness of central neurons to non-noxious stimulation of the inflamed
joints. The central mechanisms which might contribute to changes in responsiveness of
central neurons in arthritic rats is still in question. The alterations in discharge behavior
seen in CNS neurons is likely due, in part, to the changes in responsiveness of joint
receptors due to inflammatory processes.


88
The dense connective tissue of the capsule reinforces the lateral position of the TMJ
and is incorporated into the temporomandibular ligament. Horizontal fibers of the
temporomandibular ligament restrict posterior displacement of the condyle and oblique
fibers tend to limit lateral and inferior displacement (Sicher, 1960; Griffin and Malor,
1974). The posterior attachment tissues consists of collagenous and elastic connective
tissues which extend from the posterior border of the disc to the tympanic plate.
Macroscopic dissections of the goat TMJ were performed in this laboratory. The
articular surface of the condyle is oval in shape, its longer dimension is concave
mediolateral and the shorter dimension is convex anterioposterior. The articular disc is
ovoid, biconcave, and divides the joint into two synovial cavities. The fibrous capsule is
moderately loose which allows for extensive lateral translation of the condyle. The capsule
surrounds the joint, with the exception of the anteriomedial portions, where the lateral
pterygoid muscle attaches to the neck of the condyle. With four exceptions the gross
anatomy of the goat TMJ is similar to the human. First, the lateral aspect of the posterior
attachment tissue extends posteriorly beyond the postglenoid process and attaches to the
inferior surface of the zygomatic process of the temporal bone. This anatomical variation is
associated with the lateralization of the bony articulation of the TMJ beyond the cranial
base. Second, the articular surface of the glenoid fossa is slightly convex in all directions,
rather than concave. To accommodate this convexity the condyle is appropriately concave
along the mediallateral axis. Third, there is no articular eminence. Finally, the lateral
pterygoid muscle attaches to the anteriormedial aspect of the neck of the condyle in a
manner similar to the human, but it does not appear to attach to the disc.
Comparative Anatomy
According to the classification of Turnbull (1970), goats are section II herbivors
while humans are section III omnivores. The TMJ of the goat has been used as an animal


APPENDIX D
CENTRAL REPRESENTATION OF TMJ AFFERENTS
The central distribution of TMJ afferents has been studied in the trigeminal nuclear
complex. The main sensory nuclei and the dorsal part of the rostral spinal nucleus were
found to contain neurons responsive to isolated condylar movement or pressure applied to
the joint capsule of the cat (Kawamura aand Majima, 1964; Kawamura et al., 1967). The
authors reported simple, qualitative findings describing three types of responses to
ipsilateral condylar rotation (rapidly adapting, slowly adapting and on-off types) and two
types of responses to mechanical stimulation (rapidly adapting and slowly adapting types).
In addition, response patterns of neurons in the trigeminal motor nucleus were recorded
during condylar movements or mechanical stimulation of the joint capsule. As with
responses from the sensory nuclei, no quantification of activity was attempted. Procaine
infiltration into the joint capsule abolished neural responses. Another qualitative study
reported unit activity found in the trigeminal main sensory nucleus and nucleus oralis of the
cat that responded to jaw rotation or pressure applied to the ipsilateral TMJ (Sessle and
Greenwood, 1976). One of these units was antidromically activated from the thalamus.
Other direct projections from the superficial layers of the medullary dorsal horn to the
thalamus have been demonstrated anatomically (Craig and Burton, 1981) and
electrophysiologically (Dostrovsky and Broton, 1985).
The caudal aspects of the trigeminal nucleus complex were found to contain
neurons that are driven by electrical, mechanical, and algesic chemical stimuli applied to the
TMJ (Broton and Sessle, 1988). Neurons in the subnucleus caudalis were first classified
81


77
The posterior attachment tissues contain a rich plexus of nerve fibers from the
auriculotemporal nerve. Hall et al., (1985) identified and quantified the types of nerve
fibers in the posterior attachment tissues. The authors found that the majority of axons
were unmyelinated. The lateral portion of the posterior attachment tissues contain
significantly higher percentage of unmyelinated fibers. Other investigators (Weinmann and
Sicher, 1951; Sicher, 1955) have reported abundant innervation in association with blood
vessels in the loose connective tissue between the posteror border of the articular disc and
the capsule.
A few nerve fibers have been observed in the synovial membrane of the human
TMJ (Thilander, 1961; Ishibashi, 1966). Ishibashi, (1974) found free nerve endings and
glomerular endings beneath the superficial cell layer of the synovial membrane located on
the posterior aspect of the TMJ. Bemick (1962) described encapsulated end bulbs in the
synovial folds in the TMJ of the rat. These observations appear to contradict those who
believe that the synovial tissue serves no sensory function (Olson, 1969). Although the
nerve endings in the synovial membrane have been reported to be closely associated with
blood vessels (Hagen-Torn, 1882; Davis, 1945), unmyelinated nerve fibers have been
described in the synovium separated from blood vessels (Kellgren and Samuel, 1950;
Rossie, 1950). Kawamura et al. (1967) found Golgi-type endings in the synovial tissue
layer of the TMJ of the cat but not in the synovial membrane itself. Whether the synovial
membrane is innervated or not, the justapositon of afferent fibers allows sensibility in the
territory of the synovium.
As reported by Thilander (1961), the articular disc contained no nerve endings.
However, other investigators (Ishibashi, 1966; Schmid, 1969; Zimny and St. Onge, 1987)
described articular nerves innervating the periphery of the disc in the human TMJ. Similar
results were reported in the monkey (Keller and Moffet, 1968), in the rat (Bernick, 1962)
and in the mouse (Frommer and Monroe, 1966). These studies are consistent with
histological studies of fetal material. Kitamura (1974) reported that, in the 5th month in


112
TABLE G-22
FFFFrT OF SAI INF
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #2
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
6.9N
7.ON
0.1N
Freq. Asymptote
48N
46
-2.0N
Mean Rate
3.6
3.5
-0.1
Slope
-0.35
-0.62
0.27
Freq. Thres.



2
R
0.20
0.59
0.39
Static Force
Act. Thres.
20N
11N
-9.0N
Freq. Asymptote
49N
60N
1 IN
Mean Rate
4.0
3.1
-0.9
Slope
-1.4
-0.99
-0.42
Freq. Thres.

9.0N
-5.0N
2
R
0.66
0.52
-0.14
Force Velocity
Act. Thres.
13N/s
Freq. Asymptote
179N/9
Mean Rate
3.3
Slope
-0.4
Freq Thres.
2

R
0.63


TABLE OF CONTENTS
LIST OF TABLES vi
LIST OF FIGURES via
KEY TO SYMBOLS ix
ABSTRACT x
CHAPTERS
1 INTRODUCTION 1
2 METHODS 4
Subjects 4
Exposure of the TMJ and Trigeminal Ganglion 4
Recording Procedures 5
Characterization of TMJ Afferents 6
Statistics 11
Experimental Inflammation 13
3 RESULTS 16
Identification of TMJ Nociceptors 16
Characterization of TMJ Nociceptors in Normal Tissue 21
Properties of TMJ Nociceptors in Inflamed Tissue 27
Experiment I: Properties of units in the Previously Inflamed TMJ ... 31
Experiment II: Properties of Units in the Acutely Inflamed TMJ 36
4 DISCUSSION 52
Sensitization of TMJ Nociceptors 54
Factors Contributing to Sensitization 57
APPENDICES
A DEVELOPMENT AND MAINTENANCE OF TMJ PAIN 60
B PSYCHOPHYSICS OF TMJ DISORDERS 67
C NEUROANATOMY OF THE TMJ 75
D CENTRAL REPRESENTATION OF TMJ AFFERENTS 81
E TRIGEMINAL GANGLION 84
F GROSS ANATOMY 86
IV


3
normal range of motion, and identification of afferents that respond specifically in these
ranges.
Sensitization of TMJ receptors may be an important defense mechanism that
protects the joint from excessive movement which may cause injury. The TMJ is often the
site of inflammations associated with various forms of TMJ dysfunction (e.g. arthritis and
synovitis). An understanding of how inflammation may modify TMJ afferent function
would reveal the form and range of TMJ afferent sensitization and lead to a better
understanding of both etiology and treatment.
Sensitization of nociceptors has been documented in the cat knee joint (Coggeshall
et al., 1983; Schaible and Schmidt, 1985, 1988b; Grigg et al., 1986) and in the rat ankle
joint (Guilbaud et al., 1985) following chemically-induced acute or chronic arthritis. Acute
arthritis in the cat knee joint, induced by carrageenan and kaolin, produced changes in the
discharge properties in joint afferents. These changes include an increase in the proportion
of small fibers that could be activated by innocuous joint movement, recruited units, and
the appearance of spontaneous activity. Studies of sensitization of TMJ nociceptors may
provide uniquely important information regarding short and long term changes occurring in
TMJ afferents following local trauma, arthritis or chronic disc displacement.
In the following experiments, we examined properties of TMJ nociceptors in both
normal and inflamed tissue of the goat. The goat is an excellent model for TMJ physiology
because of functional and structural similarities to humans including range of motion and
innervation of the auriculotemporal nerve. (See Appendices C and F).


10
A
UNITS
FORCE (N)
DISPLACEMENT (dog)
B
UNrrs
FORCE (N)
DISPLACEMENT (deg)
TEST FOR DYNAMIC REACTIVITY
I 1 W ft ft
TEST FOR STATIC REACTIVITY
1 H H ih
20-1
IS-
to-
*'
30
20-
10
TIME


124
Jerge CR (1964). The neurologic mechanism underlying cyclic jaw movements. J Prosth
Dent 14: 667-681.
Kanaka R, Schaible H-G and Schmidt RF (1985). Activation of fine articular afferent units
by bradykinin. Brain Res 327: 81-90.
Kawamura Y (1980). Neurophysiology. In: The Temporomandibular Joint. A Biological
Basis for Clinical Practice. BG Sarnat and DM Laskin (eds), Charles Thomas,
Springfield, Illinois, p. 114-126.
Kawamura Y and Abe K (1974). Role of sensory information from temporomandibular
joint. Bull Tokyo Med Dent Univ 21 (Suppl) 78-82.
Kawamura Y and MajimaT (1964). Temporomandibular joint's sensory mechanisms
controlling activities of jaw muscles. J Dent Res 43: 150.
Kawamura Y, Majima T and Kato I (1967). Physiological role of deep mechanoreceptors
in temporomandibular joint capsule. J Osaka Univ Dent Sch 7: 63-76.
Kayser V and Guilbaud G (1984). Further evidence for changes in the responsiveness of
somatosensory neurons in arthritic rats: a study in the posterior intralaminar region
of the thalmus. Brain Res 323: 144-147.
Keller JH and Moffet BC (1968). Nerve endings in the temporomandibular joint of the
rhesus macaque. Anat Rec 160: 587-594.
Kerr FWL (1962). Correlated light and electron microscopic observations on the normal
trigeminal gangion and sensory root in man. J Neurosurg (Suppl) 26: 132-137.
Kerr FWL and Lysak WR (1964). Somatotopic organization of trigeminal ganglion
neurons. Arch Neurol 11: 593-602.
Kitamura H (1974). Development of the Temporomandibular Joint Innervation. Bull
Tokyo Med Dent Univ 21 (Suppl): 83-85.
Klineberg I (1971). Structure and function of temporomandibular joint innervation. Am
Roy Coll Surg 49: 268-288.
Klineberg I (1980). Influence of temporomandibular articular mechanoreceptors on
functional jaw movements. J Oral Rehab 7: 307-317.
Klineberg I, Greenfield BE and Wyke BD (1970). Afferent discharges from
temporomandibular articular mechanoreceptors. Arch Oral Biol 15: 935-952.
Klineberg I, Greenfield BE and Wyke BD (1971). Afferent from discharges from
temporomandibular articular mechanoreceptors: an experimental analysis of their
behavorial characteristics in the cat. Arch Oral Biol 16: 1463-1479.
Kojima Y (1990). Convergence patterns of afferent information from the
temporomandibular joint and masseter muscle in the trigeminal subnucleus caudalis.
Brain Research Bulletin 24: 609-616.


109
TABLE G-19
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #6
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
27 N
ION
-17N
Freq. Asymptote
58N
34N
-24N
Mean Rate
3.5
2.9
-0.6
Slope
-0.88
-0.34
0.54
Freq. Thres.



2
R
0.30
0.28
-0.02
Static Force
Act. Thres.
35N
6.0N
-29N
Freq. Asymptote
41N
48N
7.ON
Mean Rate
7.9
4.6
-3.3
Slope
-1.5
-0.3
-1.2
Freq. Thres.
4.0N
5.ON
1.0N
2
R
0.90
0.38
-0.52


53
range of motion. Afferents with similar properties have been observed in the cat knee joint
(Dom, et al., 1991). In this study, large diameter afferents (Group II) responded
exclusively in the normal range of motion, were directionally sensitive, and demonstrated
no resting activity. Whereas activity in nociceptors is likely to contribute to joint pain,
these low threshold afferents may contribute to proprioception or sensations of pressure
(Burke et al., 1988; Macefield et al., 1990; see Appendix B).
In other laboratories, recordings have been made from group III and IV joint
afferents innervating the cat knee (Burgess and Clark, 1969; Clark, 1975; Schaible and
Schmidt, 1983b). Schaible and Schmidt (1983b) divided their joint afferents into 4
subgroups which were differentiated, in part, by their qualitative response to movement.
They defined nociceptors as those afferents that responded through, beyond or exclusively
beyond the normal range of joint motion. These afferents had a steep rise in discharge
frequency during forceful rotational movements, similar to those described previously
(Burgess and Clark, 1969; Coggeshall et al., 1983). These observations compare
favorably with ours, in that intense mechanical stimulation is needed to achieve a maximum
response. It is difficult to make detailed comparisons between the response properties of
afferents described by Schaible and Schmidt and others with those in our experiments, as
no attempt was made by them to quantify the properties of afferents other than local
pressure thresholds. Our experiments represent the first quantification of nociceptor
reactivity across a range of suprathreshold stimuli with verification of the relationship
between movement, response minima and maxima.
Early experiments created some confusion as to the basic properties of joint
afferents. Studies that have examined the activity of mechanoreceptors supplying cat joint
tissues (Burgess and Clark, 1969; Clark and Burgess, 1975; Rossi and Grigg, 1982)
primarily emphasized proprioception, and addressed the questions as to whether position
sense is coded by joint or muscle afferent fibers. They determined that joint afferents are
only responsive at the extremes of the movement range, seemingly ruling out any useful


71
Interdental thickness discrimination is one method that has been used to analyze the
position sense of the mandible. Interdental thickness discrimination is the ability to detect
differences in the thickness of test materials placed between opposing teeth. Caffese et al.,
(1973) studied the possible influence of TMJ receptors in tactile occlusal perception by
assessing minimal thickness detection between opposing teeth before and after
anesthetization of the TMJ. These authors found significant differences in threshold
detection in the anesthetized joint compared to the normal joint. On the other hand, Siirila
and Laine (1972) obtained different results from their study of interdental thickness
discrimination. Anesthetization of TMJ did not significantly diminish subjects ability to
detect differences in thickness between teeth at various degrees of mouth opening.
Morimoto and Kawamura (1978) obtained similar results and suggested that the muscle
spindles in the muscles of mastication are mainly responsible for size discrimination.
If mechanoreceptors of the TMJ play a role in jaw position sense, their influence
maybe modulated by TMJ disorders. Ransjo and Thilander (1963) studied position sense
of the mandible in patients with TMJ disorders which were thought to be of myogenic
origin or due to functional malocclusion. The authors assumed that functional
malocclusion caused impairment of TMJ receptors. Position sense was found to be poorer
for the malocclusion group compared to the normal group. Position sense of the myogenic
group was normal. Amelioration of TMJ symptoms after treatment was accompanied by
improvement in the perception of jaw position. This study is in accord with the previous
work of Thilander (1961) suggesting that TMJ mechanoreceptors play a major role in the
ability to perceive position sense of the mandible.
A more recent study by van Willigen et al., (1986) investigated perception of jaw
position in subjects with symptoms of TMJ disorders. They found that all subjects with
craniomandibular dysfunction demonstrated greater mismatches of jaw position compared
with normal subjects. On the other hand, other studies present contrasting evidence
(Christensen and Troest, 1975; Morimoto and Kawamura, 1978; Broekhuijsen and van


31
Experiment!: Properties of Units in the
Previously Inflamed TMJ
In the PI condition, transduction of the dynamic aspects of stimulus force was best
described by power functions. Power functions were the best fit compared to other
functions (7 of 13 cases; R2 = 0.33 0.25) and were best or second best fit in 9 of 13
cases. Therefore, exposure to carrageenan did not modify the nature of functions which
described afferent activity. Individually fitted power functions generated during dynamic
and static response testing in inflamed tissue are illustrated in Figure 3-5.
Comparison of units in normal and inflamed tissue (see Figure 3-6) suggested
improved reactivity for units that responded preferentially to movement in the vertical
plane. Increased reactivity to dynamic stimuli was particularly prominent. In normal
tissue, 11 of 18 units with RFs on the TMJ capsule coded for dynamic force or velocity;
while proportionally more units (5/5) transduced dynamic force or velocity in the PI
condition. Mean functions for dynamic force in inflamed and noninflamed conditions were
calculated by averaging slopes and intercepts of individual functions (Lnl = -1.3LnF + 7.3,
(n = 25); Lnl = 1.1 LnF + 5.4, (n = 6)] for inflamed and noninflamed, respectively). The
mean functions for all VP and HP units fitted during dynamic testing in normal and
inflamed tissue suggested improvement of dynamic reactivity (Figure 3-6). The shifts of
the mean function for units in PI condition to a graphic position below the mean function
for normal tissue was suggestive of sensitization to dynamic forces.
Mean functions were also calculated for afferents transducing force velocity. A
shift of the mean function of PI units that coded for force velocity [Lnl = -0.7 LnF + 3.5,
(n = 6)] was also observed in comparison to the mean functions in normal tissue [Lnl = -
0.38 LnF + 4.7, (n = 16)]. These functions are illustrated in Figure 3-6. A shift of the
mean function for afferents in inflamed tissue below and to the left of the mean function for
normal tissue also suggested sensitization to velocity of applied forces.


110
TABLE G-20
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #7
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
7.9N
Freq. Asymptote
30N
Mean Rate
4.8
Slope
-1.04
Freq. Thres.


2
R
.
0.58
Movement
Act. Thres.
l.ON/s
Freq. Asymptote
40N/s
Mean Rate
4.6
Slope
-0.32
Freq. Thres.
2

R
0.40
Force Velocity
Act. Thres.
3.IN
Freq. Asymptote
4.3N
Mean Rate
8.3
Slope
-2.7
Freq Thres.
2
3.IN
R
.
0.47


56
less likely to be related to the development of qualitative changes than rotation. Rotation
represents a new functional reactivity in the form of a proportional response to imposed
forces. The basis of the qualitative changes could be either receptor based metabolic
alteration secondary to the generation of proinflammatory substances, or could result from
improved mechanical coupling between the receptor and the applied force.
Edema is a major component of inflammation that may impact on mechanical
coupling. Afferent terminals of small fibers that are located in the area of inflammation are
subject to an altered physical environment as a consequence of fluid extravasation. What
effect local changes from edema may have in the responsiveness of joint receptors is
unclear. In other preparations, edema may act to enhance or deter afferent responsiveness,
the direction of the effect being dependent on tissue properties that are peculiar to each site
(Cooper et al, 1990).
Acquisition of transducing capacity could be similar to observations of recruited
activity described by other laboratories. This "recruitment" of afferents was observed in
the cat knee joint preparation (Schaible and Schmidt, 1985, 1988b) and also in cutaneous
preparations (Handwerker et al., 1991). A distinction between our observations and those
of Schaible and Schmidt is that our sensitized afferents all have some pre-existing
reactivity. We did not observe recruitment as silent units which "wake up." Given this,
recruited activity and acquired coding may be distinct forms of sensitization. Our failure to
observe recruitment may be due to methodological constraints of our preparation. In our
experiments, extracellular recordings of neural activity in the trigeminal ganglion limits the
number of neurons that could be recorded at any site. Very few cell bodies are in the
functional range of the microelectrode. On the other hand, in teased fiber preparations such
as those used by Schaible, Schmidt and Handwerker, electrodes have essentially zero
impedance, therefore many more afferents can be recorded from simultaneously. This
makes it more likely for recruitment to be observed.


LIST OF TABLES
Table 3-1 TMJ force/movement relationships in the vertical plane 25
Table 3-2 Properties on nociceptors that demonstrate vertical plane or horizontal
plane reactivity 28
Table 3-3 Mean values of properties of TMJ nociceptors 37
Table 3-4 Qualitative improvements in reactivity for nociceptors that were
characterized in normal tissue and then tested again subsequent to
carrageenan injection 46
Table 3-5 Changes in reactivity for 8 units after exposure to saline 51
Table G-l Reactivity in vertical plane (normal tissue) 91
Table G-2 Reactivity in horizontal plane (normal tissue), left lateral 92
Table G-3 Reactivity in horizontal plane (normal tissue), right lateral 93
Table G-4 Reactivity in the vertical plane in previously inflamed tissue. Reactivity
in horizontal plane in previously inflamed tissue, left lateral 94
Table G-5 TMJ nociceptor reactivity in normal tissue, vertical plane 95
Table G-6 TMJ nociceptor reactivity in normal tissue, horizontal plane 96
Table G-7 TMJ nociceptor reactivity in previously inflamed tissue 97
Table G-8 TMJ nociceptor reactivity in acutely inflamed tissue 98
Table G-9 TMJ nociceptor reactivity in saline injected tissue 99
Table G-10 Effect of carrageenan in acutely inflamed tissue reactivity in the vertical
plane, unit #1 100
Table G-l 1 Effect of carrageenan in acutely inflamed tissue reactivity in the vertical
plane, unit #2 101
Table G-l2 Effect of carrageenan in acutely inflamed tissue reactivity in the vertical
plane, unit #3 102
Table G-13 Effect of carrageenan in acutely inflamed tissue reactivity in the vertical
plane, unit #4 103
vi


65
dissected muscles. Similar responses were produced in the detatched muscles by direct
tension on the capsule after condylectomy.
Jaw movement has been shown to modulate the firing pattern of alpha motoneurons
in the trigeminal motor nucleus in cats (Kawamura et al., 1967). These investigators
demonstrated changes in the discharge rate of motor neurons of the masseter muscle in
response to passive rotation of the ipsilateral condyle. Rotating the condyle to an open
position evoked an increase in firing pattern of masseter motoneurons. A closed position
evoked a decrease in firing pattern.
Abe and Kawamura (1973) recorded efferent discharges from branches of the
mandibular nerve which innervate the masseter and digastric muscles. Ipsilateral condylar
rotation to an open position inhibited alpha-motor units in the masseteric nerve. Local
mechanical stimulation of the posterior part of the TMJ capsule inhibited the discharge
pattern of masseteric neurons and facilitated motor fibers innervating the digastric muscle.
It is not surprising that afferent activity from mechanoreceptors in the TMJ modulate
efferent activity in masticatory muscles in order to coordinate jaw movement. The presence
of chronic activation of TMJ afferents may induce chronic reflex activation of facial
musculature. Chronic activation may produce muscle pain that limits movement.
Clinically, bruxism has been associated with muscle hyperactivity and TMJ
dysfunction. Bruxism is defined as a nonfunctional voluntary or involuntary mandibular
activity featuring habitual grinding or clenching of the teeth (Kawamura, 1980). Chronic,
repetitive mandibular movement seen in bruxism is thought to deliver excessive reaction
forces to the TMJ which could produce local inflammatory changes. Putative causes of
bruxism include occlusal stress, CNS and hereditary factors.
2) Referred pain theory
Pain may be referred to the TMJ from other head and neck regions (Bell, 1969).
Travell (1976) suggested that continuous hyperactivity of muscles from the head and neck
may refer pain to the TMJ. The explanations for the origin of referred pain have largely


82
on the basis of their responsiveness to mechanical stimulation to the skin: low-threshold
mechanoreceptors (LTM), wide dynamic range (WDR) or nociceptive specified (NS).
WDR and NS neurons responded maximally to algesic chemical and intense mechanical
stimulation applied to the joint. TMJ stimulation consisted of local probing or extreme jaw
opening. The majority of single units with TMJ input received convergent input from
cutaneous afferents. Kojima (1990) also found convergence patterns of afferent input from
the TMJ and muscle in the subnucleus caudalis. Most of the units tested were responsive
to mechanical and thermal stimulation of both the TMJ and the masseter muscle.
Extensive convergence of cutaneous and muscle inputs on second-order neurons
that respond to articular movement have been described in the cat knee (Schaible et al.,
1986). In some neurons, maximal responses to joint movement occurred with forced
extension, inward rotation or outward rotation. Other neurons were excited only by
noxious movement. Joint movement was considered noxious if the movement was made
forceably. No quantification of forces was attempted. This report compares favorably
with the effects of TMJ stimulation in neurons in the medullary dorsal horn (Broton and
Sessle, 1988), in that most second order neurons that respond to noxious joint simulation
also receive convergent input from skin and/or muscle. Such central convergence may be
important in explaining the tenderness of skin and/or muscles near the joint that are often
observed clinically when the joint is painful.
Changes in responsiveness in spinal neurons have been investigated during the
development of acute arthritis in the cat knee jont (Neugebauer and Schaible, 1990). All
neurons tested with joint input showed enhanced responsiveness to joint flexion after
induction of inflammation.
Other electrophysiological experiments performed in polyarthritic rats demonstrated
nociceptive inputs from chronically inflamed joints to the ventrobasal thalmus (Guilbaud et
al., 1980; Gautron and Guilbaud, 1982), intralaminar and medial thalamus (Kayser and
Guilbaud, 1984; Dostrovsky and Guilbaud, 1990), and somatosensory cortex (Lamour et


Figure 2-1. Mandibular movements were produced by a hand held probe. Force
applied to the mandible was quantified by a force transducer. Vertical
plane mandibular movement was quantified by an angular displacement
transducer mounted above the right TMJ and attached to the mandibular
pole by a slide assembly. Vertical plane movement of the mandible was
produced by applying force at point A on the jaw movement apparatus.
Horizontal plane movement was produced by applying force at point B.
Afferent recordings were made following exposure and penetration of the
trigeminal ganglion proximal to the foramen ovale.


Figure 3-9. Comparison between pre-inflamed and post-inflamed reactivity in scatter plot forms. Two types of trends are
displayed (rotation and shift). A,B,C and D) Units manifesting both rotation and shift to the left of scatter field.
E,F,G.and H) Units manifesting rotation. Functions fit to scatter plots indicate significant transduction capacity was
acquired. N, normal or pre-inflamed case; HR, hours afer carrageenan injection; M, minutes after carrageenan
injection.


Table G-14 Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal
plane, unit #1 104
Table G-15 Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal
plane, unit #2 105
Table G-16 Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal
plane, unit #3 106
Table G-17 Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal
plane, unit #4 107
Table G-18 Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal
plane, unit #5 108
Table G-19 Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal
plane, unit #6 109
Table G-20 Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal
plane, unit #7 110
Table G-21 Effect of saline reactivity in the horizontal plane, unit #1 111
Table G-22 Effect of saline reactivity in the horizontal plane, unit #2 112
Table G-23 Effect of saline reactivity in the horizontal plane, unit #3 113
Table G-24 Effect of saline reactivity in the horizontal plane, unit #4 114
Table G-25 Effect of saline reactivity in the horizontal plane, unit #6 115
Table G-26 Effect of saline reactivity in the horizontal plane, unit #7 116
Table G-27 Effect of saline reactivity in the horizontal plane, unit #8 117
vu


Figure 2-2. Dynamic and static test series for force, displacement and velocity. A)
Dynamic test series. Sawtooth patterns of successively increasing
velocities. B) Static test series. Stepwise pattern of successively
increasing force and displacement.


121
Deboever JA (1973). Functional disturbances of the temporomandibular joints. Oral Sri
Rev 1: 100-117.
Dorn T, Schaible H-G and Schmidt RF (1991). Response properties of thick myelinated
group II afferents in the medial articular nerve of normal and inflamed knee joints of
the cat. Som and Mot Res 8: 127-136.
Dostrovsky JO and Broton JG (1985). Antidromic activation of neurons in the medullary
dorsal horn from stimulation in nucleus submedius. Society of Neuroscience
Abstracts 11: 411.
Dostrovsky JO and Guilbaud G (1990). Nociceptive responses in medial thalamus of the
normal and arthritic rat. Pain 40: 93-104.
Dubner R, Sessle BJ and Storey AT (1978). The Neural Basis of Oral and Facial
Function. Plenum, New York, p. 147-174.
Fields HL (1987). Pain. McGraw-Hill, New York, p. 79-99.
Fitzgerald M and Lynn D (1977). The sensitization of high threshold mechanoreceptors
with myelinatde axons by repeated heating. J Physiol (Lond) 265: 549-563.
Foley JO (1960). A quantitative study of the functional components of the facial nerve.
Am J Anat 107: 237-244.
Franks AS (1965). De beheersing van de bewegingen in het koakgewricht. Nederl T
Tandheelk 72: 605.
Freeman MAR and Wyke B (1967). The innervation of the knee joint: An anatomical and
histological study in the cat. J Anat 101: 505-532.
Friedman R, Cooper BY, Ahlquist ML and Loughner BA (1988). Sensitization of high
threshold mechanoreceptors in the oral cavity of the goat. Society of Neuroscience
Abstracts 14: 562.
Frommer J and Monroe CW (1966). The morphology and distribution of nerve fibers and
endings associated with the mandibular joint of the mouse. J Dent Res 45:1762-
1766.
Frost HM (1968). Musculoskeletal pain. In: Facial Pain. CC Ailing (ed), Lea and
Febiger, Philadelphia, p. 153-173.
Garcia-Leme, J (1989). Hormones and Inflammation. CRC Press Inc, Boca Raton,
Florida, p. 61-64.
Gautron M and Guilbaud G (1982). Somatic responses of ventrobasal thalamic neurons in
polyarthritic rats. Brain Res 237: 459-471.
Greenfield BE and Wyke B (1966). Reflex innervation of the temporomandibular joint.
Nature (Lond) 211: 940-941.
Griffin CJ and Harris R (1975). Innervation of the temporomandibular joint. Aust Dent J
20: 78-85.


117
TABLE G-27
FFFFrT OF SAT INF
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #8
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
7.0N
5.ON
-2.0N
Freq. Asymptote
48N
56N
8.ON
Mean Rate
3.3
3.2
-0.1
Slope
-0.78
-0.86
0.08
Freq. Thres.



2
R
0.37
0.73
0.36


5
the stemomastoid and caudal digastric muscles were excised from the mastoid process and
jugular process of the occiput, respectively. The sphenomandibular ligament and fatty
tissues were removed. Care was taken to preserve the microvasculature of the TMJ
capsule. The exposed capsular tissue was kept moist by repeated applications of
physiological saline.
Several nerves were cut distal to the trigeminal ganglion in order to avoid recording
activity other than TMJ afferents. The buccinator nerve was severed as it passed the
anterior border of the masseter muscle. The masseteric nerve was cut as it entered the deep
and superficial masseter muscle. The posterior trunk of the mandibular nerve was cut distal
to the branching of the auriculotemporal nerve. As a consequence, afferents of the lingual,
inferior alveolar and mylohyoid nerves were eliminated.
The trigeminal ganglion was accessed via its position caudal to the foramen ovale.
Removal of the thin, lateral plate of bone of the tympanic bulla and the tympanic plate
exposed the ossicles of the middle ear and internal surface of the tympanic membrane.
Removal of the inferior aspect of the greater wing of the sphenoid and the inferior aspect of
the petrous bone exposed the caudal surace of the trigeminal ganglion. Access to the
ganglion is improved by removing the sphenomandibular ligament and fatty tissue in the
infratemporal fossa.
Recording Procedures
Extracellular recordings were made by penetration of the trigeminal ganglion with
tungsten microelectrodes (Microprobe, Inc.) until unit potentials were evoked by passive
jaw movement. Most units were found in the posterior region of the trigeminal ganglion.
(See Appendix E). Receptive fields were then identified on the lateral or posterior capsule
of the TMJ. Amplified output was led to and monitored by a digital oscilloscope and an
audio speaker. Data was digitized and stored on video tape (Vetter Instruments, Model No.


26
strongest response from an afferent. Thirty-six afferents with receptive fields in the TMJ
capsule were activated by either vertical plane (VP or opening) or horizontal plane (HP or
lateral displacement) motion. Eighteen afferents responded preferentially to movement in
the vertical plane and 18 responded best to movement in the horizontal plane. A few units
were activated by right lateral displacement (n = 5) or protrusive (n = 2) movement but
most TMJ afferents responded preferentially to either opening (VP) or left lateral
displacement (HP).
Once preferred movement was determined, tests of dynamic and static reactivity
were conducted. Relationships between force, position or movement and response interval
were quantified. The responses of TMJ nociceptors were quantified by regressions fit
between instantaneous dynamic force, force velocity, movement, static force or position
and instantaneous interspike interval.
As it was not clear which function would best describe TMJ afferents, linear,
power, logarithmic and exponential models were explored. By comparison of the relative
proportions of variance accounted for by each model, it was determined that power
functions accounted for the greatest percentage of variance (mean R2 = 0.46 + 0.26; n = 71
cases). Power functions were best fits compared to other functions for both dynamic
(26/59 cases) and static tests (10/12 cases). Power functions were second best fits in 20
out of 59 cases for dynamic tests and 1 out of 12 cases for static tests. Linear functions
were superior in 7 cases, logarithmic in 12 cases and exponential in 16 cases. Since power
functions were the best or second best fit in 46 of 71 cases (mean R2 = 0.45 .30), power
functions were used to represent the data in normal tissue. In inflamed tissue (both PI and
AI), power functions accounted for the greatest percentage of variance in 101 of 146 cases
(mean R2 = 0.50 0.21).
TMJ nociceptors could be found which transduced (or coded) all aspects of force,
movement or position, and many transduced more than one variable. "Code" indicates that


35
A CHANGES IN REACTIVITY TO DYNAMIC FORCE
FOLLOWING CARRAGEENAN INFLAMMATION
0 1 2 3 4 5
Ln Force (Newtons)
N (n=25) INF (n=6)
B CHANGES IN REACTIVITY TO FORCE VELOCITY
FOLLOWING CARRAGEENAN INFLAMMATION
0 12 3 4 5
Ln Velocity (Newtons/sec)
n (n= 16) INF (n=6)


Figure 3-8. Reactivity of nociceptors exposed to saline. Five units transduced
dynamic force in both the pre- and post-saline conditions. A) and B)
demonstrate quantative changes in dynamic force reactivity. C), D) and
E) show no enhanced reactivity.


104
TABLE G-14
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #1
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
Freq. Asymptote
Mean Rate
Slope
Freq. Thres.
2
R
1.4N
34N
4.1
-0.6
0.45
Force Velocity
Act. Thres.
Freq. Asymptote
Mean Rate
Slope
Freq. Thres.
3.0N/S
132N/s
3.9
-0.08
z
R
0.12
Static Force
Act. Thres.
10.7N
Freq. Asymptote
29N
Mean Rate
Slope
Freq Thres.
2
R
4.6
-0.97
2.8N
0.37


129
Zarb GA and Carlsson GE (1988). Examination and differential diagnosis of occlusal
problems. In: A Textbook of Occlusion. HD Mohl, GA Zarb, GE Carlsson and
JO Rugh (eds), Quintessence, Chicago, p. 185-207.
Zeller J, Wussbarth E, Baruth B, Mielke H and Deicher H (1983). Serotonin content of
platelets in inflammatory rheumatic diseases. Correlation with clinical activity.
Arthritis Rheum 26: 532-540.
Zimny ML (1988). Mechanoreceptors in articular tissue. Am J Anat 182: 16-32.
Zimny ML and St. Onge M (1987). Mechanoreceptors in the temporomandibular articular
disk. J Dent Res 66: 237.
Zucker E and Welker WI (1969). Coding of somata sensory input by vibrissae neurons in
the rats trigeminal ganglion. Brain Res 12: 138-156.


123
Hall MB, Parker T, Cherry J and Ballinger WE (1985). Innervation of the bilaminar zone
in human temporomandibular joints. In: Case Reports and Outline, 67th Annual
Meeting and Scientific Sessions. AAOMS, Washington DC, p. 77.
Handwerker HO, Anton and Rech PW (1987). Discharge patterns of afferent cutaneous
nerve fibers from the rat's tail during prolonged noxious mechanical stimulation.
Exp. Brain Res 66: 421-431.
Handwerker HO, Kilo S and Rech PW (1991). Unresponsive afferent nerve fibers in the
sural nerve of the rat. J Physiol 435: 229-242.
He X, Schepelmann K, Schaible H-G and Schmidt RF (1990). Capsaicin inhibits
reponses of fine afferents from the knee joint of the cat to mechanical and chemical
stimuli. Brain Research, 530: 147-150.
Helkimo E, Carlson GE and Carmeli Y (1975). Bite force in patients with functional
disturbances of the masticatory system. J Oral Rehab 2: 397-406.
Helkimo M (1974). Studies of function and dysfunction of the masticatory system. II.
Index for anammestic and clinical dysfunctiona and occlusal state. Sved Dent J 67:
101-121.
Helkimo M (1979). Epidemiological surveys of dysfunction of the masticatory system.
In: Temporomandibular Joint Function and Dysfunction. GA Zarb and C
Carlsson (eds) Mosby, St. Louis, p. 175.
Henry ML, Johnson L, Mahan PE and Westrum L (1986). Somatotopic organization of
dental structures within the feline V ganglion. J Dent Res (Suppl) 64: 210.
Heppelman B, Herbert MK, Schaible H-G and Schmidt RG (1987). Morphological and
physiological characteristics of the innervation of cat's normal and arthritic knee
joint. In: Effects of Injury on Trigeminal and Spinal Somatosensory Systems. LM
Pubols and BJ Sessle (eds). Alan Liss Inc, New York, p. 19-27.
Heppleman B, Schaible H-G and Schmidt RF (1985). Effects of prostaglandins Ei and E2
on the mechanosensitivity of group III afferents from normal and inflamed cat knee
joints. In: Advances in Pain Research and Therapy. HF Fields, R Dubner and F
Cervero (eds), Raven Press, New York, p. 91-101.
Hilton J (1879). In: Jacobson WHA. Rest and pain. Butterworth and Company, New
York, p. 96.
Hoffman AH and Grigg P (1989). Measurement of joint capsule tissue loading in the cat
knee using calibrated mechanoreceptors. J Biomechanics 22: 787-791.
Hromada J (1960). Beitrag zur Kenutnis der Entwicklung und der Variabilitat der
Lamellenkorperchen in der Gelenkkapsel und im periartikulren Gewebe beim
meschlichen Fetus. Acta Anat 40: 27-40.
Ishibashi K (1966). Studies in innervation of human mandibular joint. Jap J Oral Biol 8:
46-57.
Ishibashi K (1974). Innervation of human temporomandibular joint in adult. Bull Tokyo
Med Dent Univ 21 (Suppl): 86-88.


33
REACTIVITY IN PREVIOUSLY INFLAMED TISSUE:
DYNAMIC FORCE
-1.5 0.0 1.5 3.0 4.5 6.0
Ln FORCE (Newtons)
-T- T7 E1 J1 E3 -4- T1 + 02
REACTIVITY IN PREVIOUSLY INFLAMED TISSUE;
FORCE VELOCITY
-1 0 1 2 3 4 5 6
Ln Velocity (Newtons/sec)
- + B2 -A- T7 -O E1 + J1 -a- E3 T1


TABLE G-l
REACTIVITY IN VERTICAL PLANE
NORMAL TISSUE
FILE
FUNCTION
TEST
FREQ.
THRES
ACT.
THRES
FREQ.
ASYM.
MRI
2
R
RF
(gr)
CV
(m/sec)
1
021691E
E3
Lnl = -1.2LnF
+
7.6
DF
14N
30N
4.3
0.56
3.6
0.7
1
021691E
E3
Lnl = -1.4LnF
+
8.4
M
14*
26'
4.9
0.59
3.6
0.7
2
040690S
S3
Lnl = -3.4LnF
+
11.2
DF
15N
19N
6.5
0.25
28.0
0.4
2
040690S
S3
Lnl = -0.37LnF +
2.9
FV
6 N/s
91 N/s
1.3
0.26
28.0
0.4
2
040690S!
S3
Lnl = -1.8LnF
+
5.5
M
T
10'
3.5
0.20
28.0
0.4
2
040690T
T3
Lnl = -5.0LnF
+
1.0
SF
7.ON
9N
15N
6.0
0.73
28.0
0.4
2
040690T!
T3
Lnl = -5.8 LnF +
17.0
P
10
10
16'
6.6
0.73
28.0
0.4
3
041390K
K7
Lnl = -l.lLnF
+
5.5
DF
13N
31N
2.3
0.10
5.4
3
041390N
N7
Lnl = -0.6LnF
+
4.8
FV
2N/s
90N/s
2.1
0.10
5.4
4
042090H
H6
Lnl = -3.0LnF
+
16.0
DF
.
41N
62N
6.9
0.64
76.0
4
042090H!
H6
Lnl = -5.0LnF
+
16.0
M
8
10
13.0
0.64
76.0
5
102690D
D1
Lnl = -0.8LnF
+
7.0
DF
32N
122N
3.4
0.29
5.4
5
102690D
D1
Lnl = -0.6LnF
+
6.4
FV
42N/s
218N/s
3.3
0.30
5.4
6
110990E
E2
Lnl = -2.7LnF
+
11.0
DF
20N
24N
7.3
0.53
3.6
6
110990E
E2
Lnl = l.lLnF
+
7.7
FV
45 N/s
129N/S
2.8
0.76
3.6
6
110990D
D2
Lnl = -0.9LnF
+
7.0
SF
8.ON
30N
65N
3.8
0.66
3.6
.
6
110990E!
E2
Lnl = -6.6LnF
+
19.0
M
10'
12'
14.0
0.73
3.6
.
7
111490E
E2
Lnl = -1.3LnF
+
8.1
DF
30N
88N
2.8
0.54
29.0
7
111490E
E2
Lnl = -0.3LnF
+
4.6
FV
29 N/s
296N/S
2.9
0.25
29.0
7
111490F
F2
Lnl = -0.44LnF
+
5.7
SF
27N
58N
96N
4.1
0.86
20.0
8
111490L
L3
Lnl = -l.lLnF
+
7.5
DF
.
25N
77N
3.2
0.73
5.4
8
111490L
L3
Lnl = -0.22LnF
+
4.0
FV
11 N/s
142N/S
2.9
0.20
5.4
8
111490J!
J3
Lnl = -6.2LnF
+ 21.0
M
15'
22'
9.0
0.31
5.4
.
9
121490A
A1
Lnl = -1.3LnF
+
9.6
DF
38N
113N
4.0
0.68
12.5
10
030791A
A1
Lnl = -0.9LnF
+
7.2
FV
lON/s
48N/s
6.3
0.50
5.4
11
032091G
G3
Lnl = -0.7LnF
+
6.5
DF
12N
36N
4.3
0.40
5.4
7.5
11
032091G
G3
r
3
M
II
1
p
-J
r
3
T1
+
4.8
FV

6N/s
170N/S
3.9
0.19
5.4
7.5


58
prostaglandin E2 (Grubb et al., 1991) have been shown to sensitize joint nociceptors to
bradykinin. This may impact both on movement sensitive and tonic forms of joint pain.
Serotonin is also important in nociceptor sensitization. The effect of 5-HT on
response characteristics of small afferent fibers have been studied in normal and inflamed
cat knee joints (Heppelman et al., 1987) and rat ankle joints (Birrell et al., 1990; Grubb et
al., 1988). Most group III and IV fibers that showed reactivity to cat knee movement were
also activated by 5-HT. Units recorded from normal rat ankle joints were excited by 5-HT
and showed enhanced activity in arthritic joints.
The consequences of carrageenan injections are very complex, and have not been
determined for joints specifically (Vinegar et al., 1987). One sequence of events that
occurs in skin, during the initial stage of inflammation (0-60 min) suggests a divergence
from mechanisms proposed for sensitization of joint afferents. Immediately after injection
of carrageenan, small amounts are absorbed by mast cells. The cytotoxic action of
carrageenan initiates the arachidonate metabolic cascade and mast cell degranulation.
Endoperoxides and serotonin are released. The endoperoxides are not believed to be
prostaglandins but are believed to be reactive intermediates, and bradykinin is not believed
to play a role. This stands in contrast to studies directly implicating bradykinin, PGE's and
PGI2 in afferent sensitization and at the very least implicates that additional factors may
play a role in carrageenan inflammation. The role of 5-HT in carrageenan induced arthritis
is also unclear. While 5-HT is released by carrageenan in rats, it is unlikely to be directly
released in other species due to the absence of 5-HT in mast cells. Serotonin may be more
important when vascular damage occurs (Zeller et al, 1983; Garcia-Leme, 1989). This
may, in fact, be more relevant to TMJ dysfunction.
Clearly, reactivity to a host of algesics is shared by most small diameter afferents
innervating joint tissue. Bradykinin, prostaglandins and perhaps 5-HT may play a role in
afferent sensitization in inflamed joints. However, in each instance, it is not clear what is
meant by normal range of motion and it is not clear to what extent shifts produced by


70
that are made during mastication are well within the border movements of the mandible as
defined by the ROM (Okeson, 1989).
Jaw Position
One feature of mandibular function is the ability to control the position of the
mandible within the limits of one's maximum ROM. An important question in the literature
dealing with proprioception is whether position sense is signalled by joint or muscle
afferents. Part of the literature implicates joint afferents (For reviews see Rose and
Mountcastle, 1959; Skoglund, 1973; Dubner et al., 1978); another part of the literature
implicates muscle afferents (for review, see Burgess et al., 1982). It is reasonable to
explain joint position sense in terms of both joint and muscle afferent input.
Jaw position sense has been studied in both normal subjects and patients suffering
from TMJ disorders. Thilander (1961) assessed perception of mandibular position before
and after unilateral or bilateral anesthetization of the TMJ in normal subjects. The results
showed that subjects had more difficulty returning to an initial jaw position, following
anesthetization. Larsson and Thilander (1964) explored the relationship between position
sense and local mechanical pressure applied to the TMJ in normal subjects. The authors
found that position sense was not influenced by local pressure. When the local pressure
was reported to be painful, again position sense was not affected. However, when the
joint was locally anesthetized, jaw position sense deteriorated. If then, local pressure was
applied to the joint during the course of anesthesia, position sense returned to normal
levels. Presumably, local pressure recruited muscle afferents. Input from muscle
mechanoreceptors may have provided the sensory feedback necessary to restore position
sense. The authors reported that ansethetization of the TMJ was performed by infiltration
into the skin and tissues lateral to the capsule. This technique may have not anesthetized
the TMJ completely.


KEY TO SYMBOLS
Vertical plane or previously inflamed tisue.
A Horizontal plane or acutely inflamed tissue.
+ Saline control tissue.
IX


116
TABLE G-26
PPPPPX ("\p CAT TVfp
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #7
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
7.4N
1 IN
3.6N
Freq. Asymptote
59N
68N
9.0N
Mean Rate
3.6
3.8
0.2
Slope
-0.54
-0.27
-0.27
Freq. Thres.



2
R
0.32
0.20
-0.12
Static Force
Act. Thres.
11N
8.6N
-2.4N
Freq. Asymptote
60N
60N
0.0N
Mean Rate
3.3
3.9
0.6
Slope
-1.30
-0.53
-0.77
Freq. Thres.
5.ON
6.0N
1.0N
2
R
0.77
0.60
-0.17


In normal tissue, 24 of 36 nociceptors transduced dynamically applied stimuli
(mean activation threshold for dynamic force = 15.9 11.3 N and for force velocity =
17.3 + 18.9 N/s). Relatively fewer units transduced static force (8/36) or position
(1/36).
In PI conditions, tests revealed enhanced reactivity for dynamically applied
stimuli. Mean power functions for dynamic tests in PI conditions (LnISI = -1.3 LnF +
7.3) had steeper slopes compared to those in normal tissue (LnISI = -1.1 LnF + 5.4)
and were shifted graphically to regions indicating greater reactivity (below and to the
left of those in normal tissue). These shifts were suggestive of sensitization.
In AI conditions, 8 of 11 nociceptors acquired either dynamic or static coding
ability. Acquired coding ability also appeared in nociceptors (n = 2) that were without
transducing capacity in normal tissue. Acquired reactivity for vertical plane movement
was also seen for those nociceptors (n = 3) that were reactive only to movement in the
. *
horizontal plane in normal tissue. Acquisition of coding ability following carrageenan-
induced inflammation suggested afferent sensitization.
xi


APPENDIX G
SUMMARY TABLES OF TMJ REACTIVITY
90


125
Kreutziger KL and Mahan PE (1975). Temporomandibular degenerative joint disease.
Part I. Anatomy, pathophysiology and clinical description. Oral Surg Oral Med
Oral Pathol 40: 165-182.
Lamour Y, Guilbaud G and Wilier JC (1983). Altered properties and laminar distribution
of neuronal responses to peripheral stimulation in the Sm I cortex of the arthritic rat.
Brain Res 273: 183-187.
Larsson LE and Thilander B (1964). Mandibular positioning. The effect of pressure on the
joint capsule. Acta Neurol Scand 40: 131-143.
Lemke R, Dolwick MF, Hogan B and Rugh JO (1987). Masticatory efficiency of post-
TMJ surgery patients. LADR Abstracts 66:118.
Li JCR (1969). Statistical Inference. Edwards Brothers, Ann Arbor, Michigan.
Limwongee V (1986). Cell body location of trigeminal sensory neuron innervating the
temporomandibular joint in rat, cat and monkey. Society of Neuroscience Abtracts
12: 333.
Loos S (1963). A simple test of masticatory function. Int Dent J 13: 615-616.
Loughner B, Larkin LH and Mahan PE (1990). Nerve entrapment in the lateral pterygoid
muscle. Oral Surg Oral Med Oral Path 69: 299-306.
Lund JP and Matthews B (1981). Responses of temporomandibular joint afferents
recorded in the gasserion ganglion of the rabbit to passive movements of the
mandible. In: Oral-Facial Sensory and Motor Functions. Y Kawamura and R
Dubner (eds), Quintessence, Chicago, p. 153-160.
Macefield G, Gandevia SC and Burke D (1990). Perceptual responses to microstimulation
of single afferents innervating joints, muscles and skin of the human hand. J
Physiol 429: 113-129.
Mahan PE and Ailing CC (1991). Facial Pain. 3rd edition Lea and Febiger, Philadelphia.
Manly RS and Braley LC (1950). Masticatory Performance and Efficiency. J Dent Res
29: 448-462.
Marfurt CF (1981). The somatotopic organization of the cat trigeminal ganglia as
determined by the horseradish peroxidase technique. Anat Rec 201: 105-118.
McCall WD, Farias MC, Williams WJ and Bement SL (1974). Static and dynamic
responses of slowly adapting joint receptors. Brain Res 70: 221-243.
McQueen DS, Iggo A, Birrell GJ and Grubb BD (1991). Effects of paracentamol and
aspirin on neural activity of joint mechanoreceptors in adjuvant arthritis. Br J
Pharmacol 104: 178-182.
Mense S and Schmidt RF (1974). Activation of group IV afferent units from muscle by
algesic agents. Brain Res 72: 305-310.


11
Isolated units were characterized by two series of jaw manipulations. The first
series consisted of five tests of reactivity to dynamic force. The first, at a low velocity,
was followed by jaw movements of progressively higher velocities. The range of
velocities was approximately 0.3 to 250.0 N/sec. The second series consisted of five
stepwise, static force applications. Each step was maintained for approximately 2 seconds.
Forces up to 120 N were applied.
To confirm that jaw movement activated afferents of the TMJ capsule, receptive
fields on the capsule were identified and characterized for each case. Thresholds for
activation of mechanosensitive afferents on the capsule of the TMJ were determined by the
bending force of von Frey filaments (monofilament nylon) of different stiffnesses. The
method of limits was used to determine threshold. Nylon probes were applied to the
capsular field until the minimum force required to activate the afferent was determined. In
some cases, no receptive field could be found. This group of cases was treated separately
from afferents with identified receptive fields.
Statistics
Nociceptors were defined as those afferents that responded preferentially to
extremes of jaw movement. Relationships between force applied and jaw movement were
assessed to determine whether the afferents reacted at movement extremes. Force-
movement data was plotted for all units (n = 10) that responded preferentially to vertical
jaw movement and produced significant functions. Momentary relationships between
force, jaw movement and unit activity were determined. Force-interspike interval,
movement-interspike interval and velocity-interspike interval records were fit to linear,
logarithmic, exponential or power functions using simple linear regression (Statistical
Analysis System, SAS). The best fits were determined by comparison of coefficients of
determination.


103
TABLE G-13
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE VERTICAL PLANE
UNIT #4
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
17N
49N
32N
Freq. Asymptote
7.5N
23N
15.5N
Mean Rate
3.8
3.7
-1.1
Slope
-0.6
-1.0
0.4
Freq. Thres.



2
R
0.33
0.52
0.19
Movement
Act. Thres.
18
ir
-7.0*
Freq. Asymptote
29*
20
-9.0*
Mean Rate
5.3
4.2
-1.1
Slope
-2.1
-1.7
-0.4
Freq. Thres.


.
L
R
0.32
0.66
0.34
Position
Act. Thres.
20
Freq. Asymptote
29
Mean Rate
7.7
Slope
-3.3
Freq. Thres.
2
-14.7'
R

0.65
Force Velocity
Act. Thres.
2.2N/S
Freq. Asymptote
23.5N/S
.
Mean Rate
3.2
.
Slope
-0.12

Freq Thres.
2


R
0.11



102
TABLE G-12
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE VERTICAL PLANE
UNIT #3
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
26N
40.7N
14.7N
Freq. Asymptote
50N
76N
26N
Mean Rate
4.4
2.8
-1.6
Slope
-2.7
-1.17
-1.5
Freq. Thres.



2
R
0.50
0.10
-0.40
Movement
Act. Thres.
21"
24"
3.0
Freq. Asymptote
26
25.5
-0.5
Mean Rate
14
22
8.0
Slope
-7.0
-7.9
0.9
Freq. Thres.
24"
26
20
2
R
0.40
0.90
0.50
Force Velocity
Act. Thres.
Freq. Asymptote
20.0N/S
285N/S
Mean Rate
Slope
Freq Thres.
2
R
1.9
-0.4
0.13


TABLE G-4
REACTIVITY IN THE VERTICAL PLANE
IN PREVIOUSLY INFLAMED TISSUE
FILE
FUNCTION
TEST
FREQ.
THRES
ACT.
THRES
FREQ.
ASYM
2
R
MRI
(m/sec)
RF
(gr)
cv
(m/sec)
1
021089B2
B2
Lnl = -0.29LnF+ 3.3
FV
9.0N/S
60N/S
0.11
2.2
15.0
2
021089T
T7
Lnl = -0.49LnF+ 3.0
DF
1.0N
4.ON
0.10
2.5
15.0
2
021089T
T7
Lnl = -0.5LnF + 3.3
FV
0.8N/S
26N/s
0.26
2.7
15.0
3
021089EE
Ell
Lnl = -1.6LnF + 2.5
DF
0.35N
1.0N
0.19
3.2
15.0
3
021089EE
Ell
Lnl = -2.4LnF + 3.2
FV
0.4N/S
3.3N/S
0.85
0.6
15.0
4
021089JJ
J13
Lnl = -1.8LnF + 5.4
DF
4.0N
8.ON
0.11
2.9
15.0
4
021089JJ
J13
Lnl = -0.5LnF + 3.2
FV
0.8N/S
58N/s
0.41
1.2
15.0
5
041091E
E3
Lnl = -l.lLnF + 9.1
DF
28N
67 N
0.50
5.1
5.0
5
041091E
E3
Lnl = -0.26LnF+ 5.2
FV
lON/s
40N/s
0.20
4.3
5.0
5
041091E!
E3
Lnl = -6.6LnM + 24.0
M
17
20
0.46
17.0
5.0
5
041091F
F3
Lnl = -0.68LnF+ 6.3
SF
3.ON
4.0N
19N
0.44
4.5
5.0
5
041091F!
F3
Lnl = -2.0 LnP + 10.0
P
v
10
17
0.42
6.1
5.0
REACTIVITY IN HORIZONTAL PLANE
IN PREVIOUSLY INFLAMED TISSUE
LEFT LATERAL
FILE
FUNCTION
TEST
FREQ.
THRES
ACT.
THRES
FREQ.
ASYM.
2
R
MRI
(m/sec)
RF
(gr)
CV
(m/sec)
1
033090T
T15
Lnl = -0.2 LnF + 3.0
FV
7.5N/S
54N/s
2.2
0.12
125.0
0.67
1
033090U
U15
Lnl =-1.9LnF + 9.6
SF
9. IN
9.IN
32N
3.7
0.28
125.0
0.67
1
033090TS
T15
Lnl = -0.84LnF+ 6.6
DF
19N
55N
3.6
0.20
125.0
0.67
2
0509910
02
Lnl = -0.59LnF+ 5.9
DF

18N
65N
3.6
0.36
5.5



122
Griffin CJ and Malor R (1974). An analysis of controlled mandibular movement. Monogr
Oral Sci Physiol, Karger, Basel, Vol 4, p. 151-169.
Griffin CJ, Sharpe CJ and Gee E (1965). Inhibition of the linguo-mandibular reflex. I.
Golgi type organs at the pes menisci. Aust Dent J 10: 376-379.
Grigg P (1975). Mechanical factors influencing response of joint afferent neurons from cat
knee. J Neurophysiol 38: 1473-1484.
Grigg P, Finerman GA and Riley LH (1973). Joint-position sense after total hip
replacement. J Bone Joint Surg 55A: 1016-25.
Grigg P and Greenspan BJ (1977). Response of primate joint afferent neurons to
mechanical stimulation of knee joint. J Neurophysiol 40: 1-8.
Grigg P and Hoffman AH (1989). Calibrating joint capsule mechanoreceptors as in vivo
soft tissue load cells. J Biomechanic 22: 781-785.
Grigg P, Hoffman AH and Fogarty KE (1982a). Properties of Golgi-Mazzoni afferents in
cat knee joint capsule, as revealed by mechanical studies of isolated joint capsule. J
Neurophysiol 47: 31-40.
Grigg P, Hoffman AH and Fogarty KE (1982b). Properties of Ruffini afferents revaled by
stress analysis of isolated sections of cat knee capsule. J Neurophysiol 47: 41-57.
Grigg P, Schaible H-G and Schmidt RF (1986). Mechanical sensitivity of Group III and
IV afferents from posterior articular nerve in normal and inflamed cat knee. J
Neurophysiol 55: 635-643.
Grubb BD, Birrell GJ, McQueen DS and Iggo, A (1991). The role of PGE in the
sensitization of mechanoreceptors in normal and inflamed ankle joints of the rat.
Exp Brain Res 84: 383-392.
Grubb BD, McQueen DS, Iggo A, Birrell GJ and Dutia MB (1988). A study of 5-HT-
receptors associated with afferent nerves located in normal and inflamed rat ankle
jonts. Agents and Actions 25: 216-218.
Guerrier Y and Bolonyi F (1948). Linnervation de larticulation temporo-maxillaire. Ann
- doto-laryng 65: 109.
Guilbaud G (1988). Peripheral and central electrophysiological mechanisms of joint and
muscle pain. In: Proceedings of the Vth World Congress on Pain. R Dubner, GF
Gebhart and MR Bond (eds), Elsevier, New York, p. 201-215.
Guilbaud G, Iggo A and Tegner R (1985). Sensory receptors in ankle joint capsules of
normal and arthritic rats. Exp Brain Res 58: 29-40.
Guilbaud G, Peschanski M, Gautron M and Binder D (1980). Neurons responding to
noxious stimulation in VB complex and caudal adjacent regions in the thalamus of
the rat. Pain 8: 303-318.
Hagen-Torn O (1882). Entivicklung und Bau der Synovialmembranen. Arch mikrosk
Anat 21: 591.


80
muscle tissue (Willis and Coggeshall, 1978). However, Grigg et al., (1982b) showed that
in the cat knee, Golgi tendon organs responded to local pressure applied perpendicular to
the capsule but not to tension applied parallel to the capsule.
Free nerve endings are the most abundant receptor in the capsule of the human
TMJ. Presumably, free nerve endings derived from myelinated afferents subserve fast pain
sensibility and nociceptive somatic reflexes; free nerve endings derived from unmyelinated
nerve fibers may subserve slow pain sensibility or innervate vascular elements. Free
ending receptor specializations have yet to be defined. In sympathectomized cats, sensory
nonmedullated plexuses have been found in the inner layers of the fibrous capsule, adjacent
synovial tissues and adventitia of blood vessels in the knee joint of cat (Samuel, 1952).
Free endings have been described in the joint capsule, joint ligaments and periarticular fat
pads (Greenfield and Wyke, 1966). Similar results have been reported by Freeman and
Wyke (1967). Free endings characteristic of group III and IV afferents have been
described in the Archilles tendon of the cat as well (Andres et al., 1980). Some of these
free endings may be nociceptors.
Although there are great variations in the morphology of the TMJ between species,
the innervation of the TMJ is quite similar (Kawamura, 1980). The distribution and
appearance of receptors may vary with age and species (Polacek, 1966), but the types of
receptors are consonant across species including human.
In summary, the mammalian TMJ contains four types of receptors (for review see
Skoglund, 1973; Zimny, 1988). The Ruffini and Paciniform mechanoreceptors are
innervated by medium-sized (Ab) myelinated fibers, the Golgi tendon organ by large (Aa)
myelinated fibers and the free endings by fine myelinated and unmyelinated afferents.


68
method that can be used clinically to assess chewing efficiency was developed by Loos
(1963) and modified by Carlsson and Helkimo (1972). Test material is chewed for 10, 20
or 40 seconds.
Masticated test materials are then measured in millimeters. Chewing efficiency is rated
according to the size of the material and number of seconds of chewing.
A more elaborate, standardized measure of chewing efficiency, called the
Coefficient of Masticatory Performance, was developed by Manly and Braley (1950). The
Coefficient of Masticatory Performance was defined as the percentage of chewed peanuts
that pass through a 10-mesh screen sieve after being subjected to 20 masticatory strokes.
Rominger and Rugh (1986), utilizing this test, compared the chewing performance of a
group of patients with TMJ dysfunction to a group of normal controls. The patient group
had significantly lower coefficient scores than the normal control group. Lemke et al.
(1987) investigated the level of masticatory efficiency of post-TMJ surgical patients several
years after treatment. These investigators found that the post-surgery group had
significantly lower chewing efficiency scores than a group of non-treated non-
dysfunctional patients.
Taken together, these studies indicate a negative relationship between chewing
efficiency and TMJ disorders. Whether the inability to chew efficiently is due to the TMJ
pain or associated muscular pain is uncertain.
Jaw Movement
The sensory apparatus of the TMJ is thought to play a role in the synchronizing
mechanisms involved with the control of jaw movement (Sicher, 1955). The influences of
TMJ afferents on functional jaw movements has been studied in both normal subjects and
patients suffering from TMJ disorders. In normal subjects, Posselt and Thilander (1965)
anesthetized the lateral part of the TMJ capsule. They observed an increase in lateral


UNIVERSITY OF FLORIDA
3 1262 08554 7213


114
TABLE G-24
EFFECT OF SALINE
REACTIVITY IN THE VERTICAL PLANE
UNIT #4
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
Freq. Asymptote
Mean Rate
Slope
Freq. Thres.
2
R
5.7N
54N
3.2
-0.55
0.53
Force Velocity
Act. Thres.
11N
Freq. Asymptote
257N
Mean Rate
3.1
Slope
-0.3
Freq. Thres.
2

R
0.51
Movement
Act. Thres.
9.9
Freq. Asymptote
25
Mean Rate
3.9
Slope
-1.5
Freq. Thres.
2

R
0.58
Static Force
Act. Thres.
6.4N
Freq. Asymptote
50N
Mean Rate
3.4
Slope
-0.8
Freq Thres.
3.ON
2
R
0.65
Position
Act. Thres.
Freq. Asymptote
Mean Rate
Slope
Freq Thres.
2
R
15
25
5.6
-0.32
9.0
0.62


TABLE G-3
REACTIVITY IN HORIZONTAL PLANE
NORMAL TISSUE
RIGHT LATERAL
FILE
FUNCTION
TEST
FREQ.
THRES
ACT.
THRES
FREQ.
ASYM
MRI
2
R
RF
(gr)
CV
(msec)
1
031391B
B2
Lnl = -0.59LnF + 5.3
DF
8.ON
19N
3.9
0.33
5.5
2
041091A
A2
Lnl = -2.1LnF + 8.3
DF

9.ON
12N
6.0
0.91
5.5
3
042491G2
G3
Lnl = -2.2LnF +10.4
SF
12N
14N
26N
5.0
0.38
5.5
4
0424911
14
Lnl = -2.0LnF + 7.8
DF
.
4.0N
17N
2.7
0.70
5.5
4
0424911
14
Lnl = -0.3LnF + 3.4
FV
2.0N
50N/s
2.2
0.26
5.5
4
042491J
14
Lnl = -4.0LnF +13.0
SF
5.ON
9.ON
14N
6.6
0.97
5.5


I dedicate this work to my daughter, Carina Beth.


79
free and complex nerve endings in the TMJ of the cat (Kawamura and Majima, 1964;
Greenfield and Wyke, 1966; Kawamura et al., 1967; Wyke, 1967; Klineberg, 1971).
The three types of complicated nerve endings were sparsely distributed compared to
the free nerve endings. The most common complex ending is the Ruffini ending. Ruffini-
like endings were encountered in the lateral and posteriorlateral aspect of the capsule in
humans (Thilander, 1961). Griffin and Harris (1975) described a thinly unencapsulated
corpuscle located close to the periosteum of the neck of the condyle and in the lateral and
medial aspects of the capsule fat pads. These receptors may have been similar to the
Ruffini endings described by Klineberg (1971) in the TMJ of the cat. The Ruffini-type,
low theshold mechanoreceptors were once thought to signal joint position (Boyd and
Roberts, 1953; Boyd, 1954; Cohen, 1955; Skoglund, 1956, 1973). However, other
investigators (Burgess and Clark, 1969; McCall et al., 1974; Clark and Burgess, 1975;
Clark, 1975; Grigg, 1975; Grigg and Greenspan, 1977) have shown that Ruffini endings
are seldom active at intermediate positions of the cat knee joint. They are responsive to
extremes of joint movement. Consequently, these receptors are unlikely the peripheral
neural substrate that code for position sense. Instead, Ruffini endings appear to signal the
torque produced when the joint is extended and/or rotated at the limit of the range of
motion. (Grigg et al., 1982a).
Pacinian endings were found in the lateral aspect of the capsule (Thilander, 1961).
Paciniform-type end organs in cats have a similar distribution as Ruffini endings but less
dense (Kawamura et al., 1967; Klineberg, 1971). Golgi tendon organs were located in the
temporomandibular ligament and anterior capsule (Thilander, 1961; Griffin et al., 1965).
In the anterior capsule, the Golgi end organ was in series with the extrafusal fibers of the
lateral pterygoid muscle and tendon fasciculi of the capsular tissue or the fibrous tissue of
the pes menisci. In the temporomandibular ligament the Golgi end organ was thought to be
in series with fibers of the deep masseter muscle. Both Paciniform endings and Golgi
tendon organs are thought to respond like comparable endings found in cutaneous and


APPENDIX C
NEUROANATOMY OF THE TMJ
Until Thilanders (1961) comprehensive, anatomical and histological study of the
innervation of the human TMJ, research on innervation of the TMJ involved macroscopic
studies. Riidinger (1857) observed that the auriculotemporal nerve coursed to the posterior
aspect of the joint where three or four articular branches entered the capsule. The anterior
aspect of the capsule received one or two twigs derived from the masseteric and deep
temporal nerves. Textbooks describing the TMJ generally accepted Riidingers findings.
Moreover, other anatomists (Guerrier and Bolonyi, 1948; Baumann, 1951; Hromada,
1960) are in agreement with the neural topography described by Riidinger but for the
possible exception of the contribution of the facial nerve.
Some sensory fibers travel in the facial nerve, which is otherwise devoted to motor
function. These afferent fibers constitute about 15% of the total nerve fiber population
(Foley, 1960). Guerrier and Bolonyi (1948) reported that branches of the facial nerve
always terminated in the lateral surface of the TMJ. Hromada (1960) stated that a twig
from the facial nerve passed into the lateral aspect of the capsule in about half of his
dissected specimens. On the other hand, Thilander (1961) reported that, immediately
lateral to the capsule, a twig from the facial nerves courses in an anterior direction but does
not ramify into the joint. Kerr (1962) also reported that afferents of the facial nerve
terminate only in the dermatomes of Cl and C2 in the cat. Our observations (unpublished)
suggest that the facial nerve does not innervate the TMJ of the human. However, the facial
75


76
nerve was seen to communicate with the auriculotemporal nerve distal to the TMJ.
In contrast to the innervation of the human TMJ, the facial nerve of the goat
communicates with the auriculotemporal nerve proximal to the articular branches. The
functional implications of this topography are unclear. Some afferents from the TMJ may
travel centrally in the facial nerve or afferents in the facial nerve travel in the
auriculotemporal nerve.
Thilander (1961) reported that the auriculotemporal nerve is the major sensory
nerve of the TMJ. The branches from the auriculotemporal nerve innervate the posterior,
medial, and lateral aspect of the anterior capsule. These branches enter the inferior aspect
of the capsule along the neck of the condyle. This observation is not in accord with
Rudinger (1857) who reported that the articular branches of the auriculotemporal nerve
passed between the condyle and the pars tympanica. However, a recent study (Loughner et
al., 1990) confirms Thilander's report. In this laboratory, macroscopic dissections of the
TMJ of the goat (unpublished) show a similar course of the auriculotemporal nerve and
distribution of articular branches.
According to Hilton's Law (1879), nerves that innervate the muscles that move a
particular joint also contribute to innervation of the joint. Surprisingly, that contribution is
only about 30% of the total TMJ innervation (Thilander, 1961). Twigs from the masseteric
nerve innervate parts of the anterior capsule and anterior aspect of the medial capsule. The
posterior deep temporal nerve innervate the lateral anterior aspect of the capsule. The
auriculotemporal nerve supplies the remaining 70% of the TMJ.
Thilander (1961) estimated that the human TMJ is innervated by an average of 1500
peripheral afferent fibers. The auriculotemporal nerve contributes two thirds of the total
amount. The greatest number of the articular fibers have a diameter between 1 and 2 |xm
and probably terminate as free endings in the capsule, posterior attachment tissues and
adventitia of blood vessels associated with the joint. Other afferent fibers, though fewer in
number, and ranging from 6 to 11 (im, terminate in complex neural endings.


I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
This dissertation was submitted to the Graduate Faculty of the College of Medicine
and to the Graduate School and was accepted as partial fulfillment of the requirements for
the degree of Doctor of Philosophy.
May 1992
Dean, College of Medicine
Dean, Graduate School


96
TABLE G-6
TMJ NOCICEPTOR REACTIVITY IN NORMAL TISSUE
HORIZONTAL PLANE
Test Conditions
with RF (n=18)
without RF (n-9)
code(n=14)
no code(n=3)
code (n=l)
no code (n=4)
Dynamic Force
13
4
0
3
Force Velocity
7
9
0
3
Static Force
5
11
0
0
Conduction
Velocity
2.5 to 3.3
m/sec
(n=2)
0.5
m/sec
(n=l)


Post-test
Spontaneous
Activity
1
0
0
0


TABLE G-2
REACTIVITY IN HORIZONTAL PLANE
NORMAL TISSUE
LEFT LATERAL
FILE
FUNCTION
TEST
FREQ.
THRES
ACT.
THRES
FREQ.
ASYM.
MRI
2
R
RF
(gr)
CV
(m/sec)
1
021690A
A1
Lnl =
-1.4LnF +
5.1
SF
3.ON
3.ON
30N
0.5
~0W
8.5
4
2
110990A
A1
Lnl =
-0.4LnF +
5.0
DF
30N
100N
3.3
0.10
15.0
4
3
121990A
A1
Lnl =
-l.OLnF +
5.0
DF
4
6.0N
15N
2.8
0.27
8.5
4
3
121990A
A1
Lnl =
-0.3LnF +
3.4
FV
4
l.ON/s
35N/s
2.3
0.32
8.5
4
011691A
A1
Lnl =
-0.7LnF +
4.8
DF
.
8.ON
33N
2.6
0.40
5.5
2.5
4
011691A
A1
Lnl =
-0.2LnF +
3.8
FV
4
25N/s
267N/s
2.7
0.17
5.5
2.5
4
011691B
B1
Lnl =
-1.8LnF +
8.7
SF
6.0N
16N
42N
2.8
0.97
5.5
2.5
5
011691C
C2
Lnl =
-0.7LnF +
4.8
DF
4
6.0N
34N
2.4
0.77
76.0
4
5
011691C
C2
Lnl =
-0.34LnF +
4.4
FV
4
62N/S
305N/s
2.5
0.34
76.0
4
5
011691D
D2
Lnl =
-1.2LnF +
6.3
SF
4.5N
ION
19N
3.7
0.95
76.0
6
012391A
A2
Lnl =
-0.5LnF +
4.7
DF
4
9.5N
56N
2.8
0.31
29.0
6
012391A
A2
Lnl =
-0.1 LnF +
3.4
FV
4
7.0N/S
119N/s
2.9
0.10
29.0
7
022091A
A1
Lnl =
-1.3LnF +
7.0
DF
4
7.ON
31N
2.9
0.75
15.0
7
022091A
A1
Lnl =
-0.3LnF +
4.7
FV
4
2.0N/S
134 N/s
3.2
0.50
15.0
7
02209IB
B1
Lnl =
-1.4LnF +
8.4
SF
6.ON
12N
38N
3.8
0.64
15.0
8
031391A
A1
Lnl =
-3.0LnF +
14.0
DF
4
18N
34N
3.4
0.73
3.6
9
031391D
D3
Lnl =
-0.42LnF +
5.7
DF
4
5.ON
43N
4.2
0.23
5.5
9
031391D
D3
Lnl =
-0.16LnF +
4.9
FV
4
6.0N/S
171 N/s
4.1
0.16
5.5
10
03209ID
D2
Lnl =
-0.38LnF +
4.6
DF
5.ON
20N
3.6
0.17
3.6
10
03209IE
E2
Lnl =
-0.36LnF +
5.0
SF
2.ON
4.0N
35N
3.8
0.28
3.6
11
032891J
J4
Lnl =
-0.8LnF +
6.9
DF
4
ION
25N
4.7
0.32
5.5
11
032891J
J4
Lnl *
-0.2LnF +
5.0
FV
#
6.0N/S
133N/S
4.0
0.29
5.5
12
042491A
A1
Lnl =
-0.7LnF +
5.3
DF
4
6.0N
19N
3.5
0.60
29.0
13
072691A
A1
Lnl =
-0.78LnF +
5.5
DF
4
13N
40N
2.9
0.19
5.5
14
092791H
H
Lnl =
-0.49LnF +
3.9
DF

3.0N
31N
2.3
0.27
3.6


CHAPTER 3
RESULTS
Identification of TMJ Nociceptors
Receptive fields for units with VP or HP reactivity were found on the lateral and
posterior capsule of the TMJ (Figures 3-1 and 3-2). The mean von Frey thresholds for VP
and HP units were 27 39 g and 15 20 g, respectively. The receptive fields of these
units were single, small spots (approximately 2-3 mm). In some cases, receptive fields
could not be identified. It is possible that the receptive fields of these units were located on
the medial capsule, posterior attachment tissues or peripheral portions of the articular disc.
Alternatively, it is possible that units without identified receptive fields were not of TMJ
origin but, instead, of muscular origin (lateral pterygoid or temporalis muscles).
Conduction velocities were determined to be in the group III and IV fiber range (0.4 to 8.5
m/s). Due to the inaccessibility of many of the receptive fields, conduction velocities could
only be obtained for 30% of the units (19 of 63 units).
The response characteristics of TMJ afferents were examined. Mechanical
reactivity to jaw movement was determined using both dynamically and statically applied
forces. In order to distinguish between joint afferents acting as proprioceptors from those
acting as nociceptors,we searched for afferents with a preference for intense stimuli. It was
predicted that TMJ nociceptors would respond in the noxious range of mandibular motion,
where the noxious range of motion was defined as that passive mandibular motion where
the mandible encounters considerable resistance imposed by constraints of soft tissue.
16


119
Birrell GJ, McQueen DS, Iggo A and Grubb BD (1991). PGl2-induced activation and
sensitization of articular mechanoreceptors. Neuroscience Letters, 124: 5-8.
Boyd IA (1954). The histological structure of the receptors in the knee joint of the cat
correlated with their physiological response. J Physiol (Lond) 124: 476-488.
Boyd IA and Roberts TDM (1953). Proprioceptive discharges from stretch-receptors in the
knee joint of the cat. J Physiol (Lond) 122: 38-58.
Broekhuijsen ML and van Willigen JD. (1983). Factors influencing jaw position sense in
man. Arch Oral Biol 28: 387-391.
Broton JG and Sessle BJ (1988). Reflex excitation of masticatory muscles induced by
algesic chemicals applied to the temporomandibular joint of the cat. Arch Oral Biol
33: 741-747.
Broton JG, Hu JW and Sessle BJ (1988). Effects of temporomandibular joint stimulation
on nociceptive and nonnociceptive neurons of the cats trigeminal subnucleus
caudalis (Medullary dorsal hom). J Neurophysiol 59: 1575-1589.
Burgess PR and Clark FJ (1969). Characteristics of knee joint receptors in the cat. J
Physiol (Lond) 203: 317-335.
Burgess PR and Perl EF (1967). Myelinated afferent fibers responding specifically to
noxious stimulation of the skin. J Physiol (Lond) 190: 541-562.
Burgess PR, Wei JY, Clark FJ and Simon J (1982). Signaling of kinesthetic information
by peripheral sensory receptors. Ann Rev Neurosci 5: 171-187.
Burke D, Gandevia SC and Macefield G (1988). Responses to passive movement of
receptors in joint, skin and muscle of the human head. J Physiol 402: 347-361.
Caffese RG, Carraro JJ and Albano EA (1973). Influence of temporomandibular joint
receptors on tactile occlusal perception. J Periodont Res 8:400-403.
Campbell JN, Meyer RA and LaMotte RH (1979). Sensitization of myelinated nociceptive
afferents that innervate monkey hand. J Neurophysiol 42: 1669-1679.
Capra HF (1987). Localization and central projections of primary afferent neurons that
innervate the temporomandibular joint in cats. Somatosensory Research 4: 201-
213.
Capra NF and Gatipon GB (1981). Unit activity of trigeminal ganglion neurons recorded
during jaw opening and closing. Society of Neuroscience Abstracts 6: 674.
Carlsson GE and Helkimo M (1972). Funktionell undersokning av tuggapparaten. In:
Holst Nordish klinisk odontologi 8-1-1-21, Forlaget for Faglitteratur, Copenhagen.
Chen TT and Turner DF (1987). Sensory innervation of the temporomandibular joint. J
Dent Res Abstracts 66: 1044.
Christensen LV and Troest T (1975). Clinical kinesthetic experiments on the lateral
pterygoid muscle and temporomandibular joint in man. Scand J Dent Res 83: 238-
244.


127
Schaible HG (1983). Sensitization by prostaglandin E¡. Naunyn-Schmiedebergs Arch
Pharmacol (Suppl) 352: R98.
Schaible HG and Schmidt RF (1983a). Activation of groups III and IV sensory units in
medial articular nerve by local mechanical stimulation of knee joint. J Neurophysiol
49: 35-44.
Schaible HG and Schmidt RF (1983b). Responses of fine medial articular nerve afferents
to passive movement of knee joint. J Neurophysiol 49: 1118-1126.
Schaible HG and Schmidt RF (1984). Mechanosensibility of joint receptors with fine
afferent fibers. Exp Brain Res (Suppl 9), p. 284-297.
Schaible HG and Schmidt RF (1985). Effects of an experimental arthritis in the sensory
properties of fine articular afferent units. J Neurophys 54: 1109-1122.
Schaible HG, Schmidt RF and Willis WD (1986). Responses of spinal cord neurons to
stimulation of articular afferent fibers in the cat. J Physiol 372: 575-593.
Schaible HG and Schmidt RF (1988a). Excitation and sensitization of fine articular
afferents from cat's knee joint by prostaglandin E2. J Physiol 403: 91-104.
Schaible HG and Schmidt RF (1988b). Direct observations of the sensitization of articular
afferents during an experimental arthritis. In: Proceedings of the Vth World
Congress of Pain. R Dubner, GF Gebhart, MR Bond (eds), Elsevier, New York,
p. 44-50.
Schellhas KP, Wilkes CH and Baker CC (1989). Facial pain, headache and
temporomandibular joint inflammation. Headache 29: 228-231.
Schmid F (1969). On the nerve distribution of the temporomandibular joint capsule. Oral
Surg Oral Med Oral Path 28: 63-65.
Sessle BJ and Greenwood IF (1976). Inputs to trigeminal brainstem neurons from facial,
oral, tooth, and pharyngolaryngeal tissues. I. Responses to innocuous and
noxious stimuli. Brain Res 117: 211-226.
Sicher H (1955). Structural and functional basis for disorders of the temporomandibular
articulation. J Oral Surg 13: 275-279.
Sicher H (1960). Oral anatomy. 3rd edition, Mosby, St. Louis, p. 166-168.
Siirila HA and Laine P (1972). Sensory thresholds in discriminating differences in
thickness between the teeth by different degrees of mouth opening. Proc Finn Dent
Soc 68: 134-139.
Sheikoleham A, Mller E and Lous I (1982). Postural and maximal activity in elevators of
mandible before and after treatment of functional disorders. Scand J Dent Res 90:
37-46.
Sherrington CS (1947). The Integrative Action of the Nervous System. Yale Univesity
Press, New Haven, Connecticut p. 228.


8


13
tissue. Sensitization was assessed qualitatively by comparisons of functions fit to units in
normal and inflamed tissues.
Shifts of stimulus-response coding functions were used as an indication of
enhanced reactivity. Significant functions generated from responses of afferents in
inflamed tissue that were located graphically below and/or to the left of functions fit in
normal tissue were suggestive of sensitization (See Figure 2-3). Significant functions that
were acquired in inflamed tissue but not expressed in normal tissue also were considered to
represent sensitization. Sensitization was assessed quantitatively by statistical comparisons
of function characteristics generated from stimulus tests on units in normal and inflamed
conditions. Function characteristics (slope, intercept, thresholds, asymptotic activity,
coefficients of determination and mean interval) were compared in normal and inflamed
conditions using a one-way ANOVA (Li, 1967) for between subject and t-tests for within
subject's comparisons. Only significant functions contributed to the analysis.
Experimental Inflammation
Inflammation of the TMJ was induced by injection of 200 p.1 of 2% carrageenan
(Sigma Chem.). In some cases, units were characterized in normal tissue and then exposed
to carrageenan. If the receptive field was located on the lateral side of the capsule,
carrageenan was dropped directly onto the receptive field as well as injected into the area of
the receptive field. If the receptive field was located on the posterior side of the capsule,
carrageenan was injected into the area of the receptive field. The remainder of the
carrageenan was injected into the superior joint space. Subsequent testing was performed
after at least 30 minutes and continued for up to 3 hours. In other cases, units characterized
in normal tissue were treated with saline. The injection of saline and subsequent retests
were identical to those used with carrageenan. In other cases, response properties of
separate populations of TMJ afferents were examined only in normal or pre-inflamed


61
cadaver specimens (Loughner et al., 1990). Pressure in the form of compression by a
hyperactive lateral pterygoid muscle may produce pain and/or paresthesia. Furthermore,
patients with an internal derangement of the TMJ often have accompanying spasticity of the
lateral pterygoid muscle.
Pressure on the posterior attachment tissues by the condyle could also cause TMJ
pain (Sicher, 1955). Posterior displacement of the condyle or spastic contracture of the
superior belly of the lateral pterygoid muscle may result in anterior displacement of the
disc. As a consequence, the posterior attachment tissues are positioned where forces
generated during mastication may produce local pressure on these highly vascularized and
innervated tissues.
Local joint pressure may activate mechanoreceptive nociceptors in connective tissue
such as the posterior attachment tissues. Inflammation could result from trauma due to a
sudden, intense impact or from repeated pressure. Endogenous algesics released in the
zone of inflammation may sensitize joint nociceptors by decreasing threshold and
increasing response to mechanical stimuli (Heppelman et al., 1985).
A common procedure thought to discern anterior displacement of the disc is the
impact-loading test. Manual loading applied in an anterior-superior direction at the
posterior portion of the body of the mandible impacts the condyle into the articular fossa.
If pain is evoked, it is thought that the disc is displaced and the condyle is impacting onto
the posterior attachment tissues. However, disc displacement may exist without impact
loading pain. This is assessed by imaging techniques, such as arthrography or magnetic
resonsance imaging. Therefore, direct pressure on the disc or posterior attachment tissues
is not sufficient to explain TMJ pain in all cases.
A corollary notion related to Sichers theory was advanced by Frost (1968) to
explain some patterns of joint pain. Frost hypothesized that bone pain may be evoked by
the pressure of two articulating, irregular, joint surfaces in the absence of an intact
interposing disc. Presumably, the irregular bony surfaces represent osteoarthritic changes.


72
Willigen, 1983; van der Berghe et al., 1987). Morimoto and Kawamura (1978) tested
interdental thickness discrimination in 8 patients with unilateral or bilateral mandibular
condyles that were either surgically mobilized or removed. The authors failed to observe
any lessened capacity to discriminate thickness. These authors concluded that TMJ
receptors were not essential to size discrimination ability.
Broekhuijsen and van Willigen (1983) studied position sense of the mandible in
normal subjects before and after injection of the TMJ capsule bilaterally with local
anesthetic. Perception of mandibular position was unaffected by anesthetization of the
TMJs. Van den Berghe et al., (1987) assessed position sense of the mandible in patients
suffering from TMJ disorders before and after treatment. Patients' abilities to determine
jaw position were unchanged after successful treatment.
The relative unimportance of joint afferents in assessing position and movement is
noted for a variety of joints. In the human knee joint, injection of local anesthetic into the
joint does not deteriorate the subjects ability to detect passive angular displacements of five
degrees (Clark et al, 1979). Moreover, total joint replacement of the hip produces little
impairment of sensations associated with joint movement (Grigg et al, 1973).
In summary, the ability to control the position of the jaw is an important aspect of
mandibular function. Position sense has been studied in both normal subjects and patients
suffering from TMJ disorders. The preponderance of the evidence suggests that sensory
input from the TMJ contributes little information in controlling the position of the mandible.
Bite Force
Different parameters of bite force, such as maximum bite force, submaximal bite
force and bite force discrimination have been investigated in an effort to assess mandibular
function.


62
Other investigators (Kreutziger and Mahan, 1975) have included arthroses of bony
structures as causative factors in TMJ pain. Besides the degenerative processes that may
occur in the bony anatomy of the TMJ, degenerative changes of the villi of the synovium
have been claimed to be causally related to TMJ pain (Olson, 1969). Supposedly,
disruption of the secretory function of the villi can disturb proper nutrition and lubrication
of the TMJ resulting in TMJ dysfunction.
2) Tension Theory
Tension theories of TMJ pain can be divided into static and dynamic. Static state
involves a resting position of the mandible. Dynamic state involves active or passive jaw
movement. Anteriormedial displacement of the disc may generate static tension on the
posterior and lateral aspects of the capsule (Dubner et al., 1978) where the greatest member
of mechanoreceptors are located (Zimny, 1988). It is possible that resting tension will
produce prolonged discharge in TMJ nociceptors. If the anteriormedial displacement of the
disc is advanced, there is a release of the disc attachment at the lateral pole of the condyle
which untethers the disc from the lateral aspect of the TMJ. In this case, the posterior
attachment tissues are vulnerable to tension from a disc displacement during static
conditions.
Patients suffering from pain in the TMJ often demonstrate symptoms of capsulitis;
this included pain on local palpation or pain during small movements within the normal
range of motion. Inflammatory processes in the TMJ may initiate or potentiate TMJ pain
(Dubner et al., 1978). Dynamic theories propose that pain is produced during jaw
movement by excitation of functionally distinct types of mechanoreceptors in the capsule
and posterior attachment tissues. Activation may be enhanced by capsulitis. Zimmy
(1988) advanced a conceptual model of TMJ pain during jaw movement. As the condyle
rotates and translates freely through intermediate degrees of angle, the capsule and posterior
attachment tissues are deformed. Such deformation is normally insufficient to excite
mechanoreceptors. As the condyle approaches its border movement, the capsule and


Figure 3-4. Dynamic reactivity in normal tissue. Power functions best described the relationship between instantaneous dynamic
force and force velocity with instantaneous response interval for afferents responding to mandibular movement in the
vertical plane (VP) and horizontal plane (HP). A) Ten of 18 VP units transduced dynamic force (mean slope = -1.3 +
0.2; range = 17.0 33.5 to 48.5 22.0 N; mean R2 = 0.46 0.21). These units were activated at a mean opening of
11.2 4.4. The range of activity of each nociceptor was defined as the smallest force or movement required to
produce the minimum response frequency to the force of movement that produced the highest response frequency. B)
Eight of 18 VP units transduced force velocity (mean slope = -0.6 + 0.2; range = 17.5 19.5 to 157.0 86.0 N/s;
mean R2 = 0.30 0.18). C) Thirteen of 18 HP units transduced dynamic force (mean slope = -0.9 0.7; range = 9.7
7.3 to 37.0 + 22.8 N; mean R2 = 0.39 0.24). D) Seven of 18 HP units transduced force velocity (mean slope = -
0.39 0.24; range = 7.9 + 16.9 to 166.0 92.2 N/s; mean R2 = 0.27 0.14).


59
bradykinin, PGE2 or serotonin are the basis for changes produced with carrageenan or
other proinflammatory substances. The lack of detail in this respect is partly due to the
absence of quantification of stimulus and response variables. Quantification of neural
activity in respect to threshold, range and salient stimulus features (static or dynamic
reactivity) should permit a fuller evaluation of role played by these substances and others in
modification of joint nociceptor reactivity.


126
Morimoto T and Kawamura Y. (1978). Interdental thickness discrimination and position
sense of the mandible. In: Oral Physiology and Occlusion. JH Perryman (ed),
Pergaman, New York, p. 149-169.
Neugebauer V and Schaible H-G (1990). Evidence for a central component in the
sensitization of spinal neurons with joint input during development of acute arthritis
in cats knee. J Neurophysiol 64: 299-311.
Okeson JP (1989). Management of temporomandibular disorders and occlusion. 2nd
edition,Mosby, St Louis, p. 87-104.
Olson A (1969). Temporomandibular joint function and functional disturbances. Dent
Clinics North Am 13: 643-648.
Polacek P (1966). Receptors of the joints: Their structure, variability and classification.
Acta Facultat Med Universitat Brunensis 23: 1-107.
Posselt U and Thilander B (1965). Influence of the innervation of the temporo-mandibular
capsule on mandibular border movements. Acta Odont Scand 23: 601-613.
Posselt V (1968). Physiology of occlusion and rehabilitation. 2nd edition, Blackwell,
Oxford.
Ransjo K and Thilander B. (1963). Perception of mandibular position in cases of
temporomandibular joint disorders. Odontolgiska Foreningens Tidskrift 71: 134-
144.
Reeh PW, Bayer L, Kocher L and Handwerker HO (1987). Sensitization of nociceptive
cutaneous nerve fibers from the rat's tail by noxious mechanical stimulation. Exp
Brain Res 65: 505-512.
Rocabado M (1983). Arthrokinematics of the temporomandibular joint. Dent Clin North
Am 27: 573-594.
Rominger JW and Rugh JD (1986). Comparison of masticatory performance of TMJ
dysfunction subjects and controls. J Dent Res 29: 448-462.
Romfh JH, Capra NF and Gatipon GB (1979). The trigeminal nerve and the
temporomandibular joint of the cat: a horseradish peroxidase study. Exp Neurol
65: 99-106.
Rose JE and Mountcastle VB (1959). Touch and kinesthesia. In: Handbook of Physiology.
J Field (ed), Amer Physiol Soc, Wash DC, vol 1, p. 387-429.
Rossi A and Grigg P (1982). Characteristics of hip joint mechanoreceptors in the cat. J
Neurophysiol 27: 573-594.
Rossie F (1950). Sur linnervation fine de la capsule articularie. Acta Anat 10: 161-232.
RiidingerN (1857). Die Gelenknerven des menschlichen. Korpers, Erlangen.
Samuel EP (1952). The autonomic and somatic innervation of the articular capsule. Anat
Rec 113:53-70.


E
REACTIVITY IN VERTICAL PLANE: NORMAL TO INFLAMED
STATIC FORCE: UNIT #2
Ln Velocity (Newtons/sec)
O N 1 hfl 1 HR
F
REACTIVITY IN HORIZONTAL PLANE: SALINE CONTROL
FORCE VELOCITY:LEFT LATERAL UNIT #2
0 1 2 3 4 5 6
Ln Velocity (Newtons/sec)
O N 1 HR 1 HR
Figure 3-9. (cont'd)
G
REACTIVITY IN HORIZONTAL PLANE: NORMAL TO INFLAMED
STATIC FORCE: UNIT #1
Ln Force (Newtons)
O N 1 HR 1 HR
-P.
VO
6
5
4
3
2
1
0
0 1 2 3 4 5 6
Ln Force (Newtons)
O N 30 M 30 M-t-- 1 HR + 1 HR
H
REACTIVITY IN HORIZONTAL PLANE: NORMAL TO INFLAMED
STATIC FORCE: UNIT #3


87
1. Articular Surface of Glenoid Fossa
2. Superior Cavitt
3. Disc (Stippled Area)
4. Capsule
5. Articular Surface of Condyle
6. Synovial Membrane
7. Squamo-Tympanic Suture
8. Spine of the Sphenoid
9. Vascular Knee of Meniscus
10. Pes Meniscus
11. Superior Belly of Lat. Pterygoid
12. Inferior Belly of Lat. Pterygoid
13. Superior Stratum of Bilaminar Zone of Meniscus
14. Inferior Stratum of Bilaminar Zone of Meniscus
Figure F-l
Schematic diagram of the human temporomandibular joint. Sagittal and
frontal views.
15. Auriculotemporal Nerve
16. BloodVessels
17. Posterior Deep Temporal Nerve
18. Squamo-Sphenoidal Suture
19. Parotid Gland
20. Sphenomandibular Ligament


64
Extra-articular Theories of TMJ pain
Distinct theories of the origin of extra-articular pain have arisen, and include the
myofascial pain theory and referred pain theory.
1) Myofascial Pain Theory
The myofascial pain theory postulates chronic hyperactivity in head and neck
musculature as a causative agent in extra-articular pain. The myofascial pain theory
suggests that the chronicity of muscle pain is due to the "trigger point" (Travell, 1976).
The trigger point is defined as a localized area of chronic inflammation of fibrous
connective tissue in muscle. Histological examination of biopsy material from trigger
points in patients suffering from interstitial myofibrositis reveal degranulated mast cells and
platelet clots (Awad, 1973). The author proposes a hypothesis suggesting that trauma-
induced extravasation of platelets leads to release of 5-HT which subsequently results in
edema and vasoconstriction. The release of such endogenous algesics in muscle may play
a role in the pain and tenderness associated with trigger points. For example, activation of
group IV afferent neurons in cat muscle have been demonstrated by close arterial injection
of bradykinin, 5-HT or histamine (Mense and Schmidt, 1974). Serotonin may also
sensitize mucosal nociceptors to mechanical stimuli (Friedman et al., 1988; Cooper et al.,
1991).
Muscle pain and the reduction of pain free jaw movement are frequent complaints of
patients with facial pain. The limitation of jaw movement may involve the modulation of
the reflex control of masticatory muscles (Klineberg, 1971; Dubner et al., 1978).
Greenfield and Wyke (1966) studied the role of TMJ afferents in reflexes that modify the
activity of muscles of mastication. The experimental procedure involved detaching all the
supra- and infra-mandibular muscles at their insertions from one half of the cat mandible.
Movement of the ipsilateral half of the mandible resulted in activation or inhibition of


LIST OF REFERENCES
Abe K and Kawamura Y (1973). A study on inhibition of masseteric a-motor fibre
discharges by mechanical stimulation of the temporomandibular joint in the cat.
Arch Oral Biol 18: 301-304.
Agerberg G (1988). Bite force after temporomandibular joint surgery. Int J Oral
Maxillofac Surg 17: 177-180.
Albright D and Zimny ML (1987). Mechanoreceptors in the human medial meniscus. Anat
Rec (Abstract) 218: 6A-7A.
Andres KH, von Diiring M, Janig W and Schmidt RF (1980). Sensory innervation of the
Achilles tendon by group III and IV afferent fibers. Anat Embryol 172:145-156.
Appenteng K, Lund JP and Sequin JJ (1982). Behavior of cutaneous mechanoreceptors
recorded in mandibular division of gasserian ganglion of the rabbit during
movements of lower jaw. J Neurophysiol 47: 151-166.
Awad EA (1973). Interstitial myofibrositis: Hypothesis of the mechanism. Arch Phys
Med Rehabil 54: 449-453.
Baumann JA (1951). Contribution letude de l'innervation de 1articulation
temporomaxillaire. Compt rend Assoc Anat 38: 120.
Beaudeau DE and Jerge CR (1968). Somatotopic representation into the gasserian
ganglion of tactile peripheral fields in the cat. Arch Oral Biol 131: 247-256.
Beck PW, Handwerker HO and Zimmerman M (1974). Nervous outflow from the cat's
foot during noxious radiant heat stimulation. Brain Res 67: 373-386.
Bell WE (1969). Nonsurgical management of pain-dysfunction syndrome. J Am Dent
Assoc 79: 161-170.
Berberich P, Hoheisel V and Mense S (1988). Effects of a carragenan-induced myositis on
the discharge properties of group III and IV muscle receptors in the cat. J
Neurophysiol 59: 1395-14$).
Bemick S (1962). The vascular and nerve supply to the temporomandibular joint of the
rat. Oral Surg Oral Med Oral Path 15: 488-498.
Bifano CA, Grellner T, Houston G, Farr SC, Ehler WJ, Cissik JH and Chastain M
(1990). Cryogenically preserved adult and juvenile goat mandibular condylar
transplantation. Oral Surg Oral Med Oral Pathol 69: 291-298.
Birrell GJ, McQueen DS, Iggo A, and Grubb BD (1990). The effects of 5-HT on articular
sensory receptors in normal and arthritic rats. Br J Pharmacol 101: 715-721.
118


12
For analysis of static reactivity, regression data were "segmented and balanced." A
segment ^or step) of force was added to the regression model until the coefficient of
determination was maximal. The regression was "balanced" by using only six scores for
each stepwise force segment. This procedure avoids weighting the regression differentially
at higher steps, where more scores typically bias the regression. These procedures were
not possible on tests of dynamic force reactivity. Therefore, for dynamic force or
movement tests, all spike intervals were used until a minimum interval was obtained.
Several characteristics of regression lines were subjected to analysis. These
included force-activation thresholds, movement-activation thresholds, force-frequency
asymptotes, movement-frequency asymptotes, mean response intervals, slopes and
intercepts. Force-activation thresholds (FAT) and movement-activation thresholds (MAT)
were defined as the instantaneous force or degree of movement at the first response
interval. Force-frequency asymptotes (FFA) and movement-frequency asymptotes (MFA)
were defined as the force or movement at which the frequency response was maximal (i.e.,
minimum response interval). The FAT or MAT paired with the FFA or FMA were used as
the lower and upper boundary values to plot functions derived from regressions. The mean
response interval (MRI) was calculated from the regression equation by using the mean
force or movement value calculated from the boundary values (FAT + FFA/2 or MAT +
MFA/2). Force-frequency thresholds and movement-frequency thresholds (FFTs and
MFTs) were determined for each unit that was tested for static reactivity. The FFT and
MFT were defined as the minimum force or movement which would maintain a sustained
discharge of the afferent. Slopes, intercepts and coefficients of determination were
generated only from significant regressions. Unit reactivity that could not be described by
significant functions were called "non-coding" or "non-transducing" afferents.
"Sensitization" refers to the enhanced excitability of TMJ afferents that may occur
following carrageenan-induced inflammation. Enhanced excitability is reflected
quantitatively as changes in response properties of TMJ afferents in normal and in inflamed


20
B
MED


Figure 3-2. Receptive field (RF) distribution in the lateral and posterior capsule of the
TMJ for previously inflamed tissue (), acutely inflamed tissue (a) and
saline control tissue (+). A) Lateral capsule. B) Posterior capsule.
POST, posterior, ANT, anterior, MED, Medial; LAT, lateral.


Figure 3-1. Receptive field (RF) distribution in the lateral and posterior capsule of the
TMJ for normal tissue. A) Distribution of RFs in the lateral capsule. B)
Distribution of RFs in the posterior capsule. RFs (n=36) of afferents in
A) and B) responded to either vertical plane (.) or horizontal plane (A)
movement of the mandible. POST, posterior, ANT, Anterior, MED,
medial; LAT, lateral.


CHAPTER 1
INTRODUCTION
The temporomandibular joint (TMJ) is the site of a number of disorders that burden
the health care system and extract a large cost in human suffering (Helkimo, 1979; Solberg,
1987). Afferent groups presumed to mediate TMJ pain are likely to play a role in a variety
of TMJ disorders. Many theories have been proposed to explain TMJ pain and dysfunction
(Deboever, 1973; Dubner et al., 1978, Yemm, 1979). These theories propose both intra-
and extra-articular origins of TMJ pain. Intra-articular theories argue that pressure or
tension on articular tissues results in TMJ pain. Extra-articular theories propose that
muscles or other contiguous structures refer pain to the TMJ (see Appendix A).
Fundamental to an evaluation of intra-articular theories is an understanding of the response
properties of TMJ nociceptors.
Our understanding of nociceptors innervating articular tissues has been advanced in
recent years (Schaible and Schmidt, 1983a, b, 1988b; Guilbaud et al., 1985; Birrell et al.,
1990). Most detailed information concerning the response properties of joint nociceptors
has come from studies of the cat knee and rat ankle joint. While there is considerable
information regarding the neuroanatomy of the TMJ (see Appendix C), little is known
about the physiology of nociceptors of the temporomandibular joint.
Early studies examining properties of afferents innervating the cat knee joint
reported activation of slowly conducting, myelinated fibers only by forceful rotational
movements beyond the physiological range of motion (Burgess and Clark, 1969; Clark and
Burgess, 1975). In contrast, Schaible and Schmidt (1983b) identified populations of
1


CHAPTER 2
METHODS
Subjects
Experiments were performed on 59 goats, ages 6-12 months and weighing 30-60
lbs. All goats were kept in pens at the veterinary hospital. Goat health was monitored and
maintained by animal care technicians, veterinary staff and faculty. All procedures were
approved by an internal review board (protocol 7136).
Exposure of the TMJ and Trigeminal Ganglion
Rompun (3 mg/kg) and Ketamine (11 mg/kg) were given as preanesthetics.
Anesthesia was induced with a-chloralose (7.5 mg/ml) via a lactated ringers drip. If
necessary, pentabarbitol was periodically administered intravenously to maintain deep
anesthesia. Goats were artifically respirated at a rate of 10-20 breaths per minute. Blood
pressure, body temperature and end-tidal CO2 were continuously monitored and maintained
within physiological limits. At the conclusion of each experiment, the goats were
euthanized with saturated KCL.
To expose the right TMJ, the skin was removed from the lateral posterior aspect of
the face. The parotid gland, pinna and the zygomaticoauricularis muscles were removed to
access the posterior portion of the TMJ capsule. The styloid process and associated
muscular and ligamentous attachments were clipped off at the sphenoid bone. The origin of
4


105
TABLE G-15
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #2
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
2.7N
1.3N
-1.4N
Freq. Asymptote
30N
32N
2.0N
Mean Rate
2.0
3.4
0.5
Slope
-1.1
-0.5
-0.6
Freq. Thres.



2
R
0.63
0.49
-0.14
Force Velocity
Act. Thres.
lN/s
1.6N/S
0.6N/S
Freq. Asymptote
286N/S
185N/S
-lOlN/s
Mean Rate
2.5
3.5
1.0
Slope
-0.26
-0.17
-0.09
Freq. Thres.



L
R
0.30
0.29
-0.01
Static Force
Act. Thres.
Freq. Asymptote
Mean Rate
Slope
Freq Thres.
2
R
3.2N
30N
4.2
-0.6
2.1N
0.63


PROPERTIES OF TEMPOROMANDIBULAR JOINT NOCICEPTORS
IN NORMAL AND INFLAMED TISSUE
BY
BARRY LOUGHNER
A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL
OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT
OF THE REQUIREMENTS FOR THE DEGREE OF
DOCTOR OF PHILOSOPHY
UNIVERSITY OF FLORIDA

I dedicate this work to my daughter, Carina Beth.

ACKNOWLEDGEMENTS
I thank Dr. Brian Cooper, Ph.D., for his technical guidance in the research
involved in this dissertation. I thank Ms. Martha Oberdorfer for her technical assistance. I
thank Dr. Parker Mahan, D.D.S., Ph.D., and Dr. Arnold S. Bleiweis, Ph.D. for their
strategic guidance. I thank Dr. Robert Bates, D.D.S., M.S. for his administrative
assistance.

TABLE OF CONTENTS
LIST OF TABLES vi
LIST OF FIGURES via
KEY TO SYMBOLS ix
ABSTRACT x
CHAPTERS
1 INTRODUCTION 1
2 METHODS 4
Subjects 4
Exposure of the TMJ and Trigeminal Ganglion 4
Recording Procedures 5
Characterization of TMJ Afferents 6
Statistics 11
Experimental Inflammation 13
3 RESULTS 16
Identification of TMJ Nociceptors 16
Characterization of TMJ Nociceptors in Normal Tissue 21
Properties of TMJ Nociceptors in Inflamed Tissue 27
Experiment I: Properties of units in the Previously Inflamed TMJ ... 31
Experiment II: Properties of Units in the Acutely Inflamed TMJ 36
4 DISCUSSION 52
Sensitization of TMJ Nociceptors 54
Factors Contributing to Sensitization 57
APPENDICES
A DEVELOPMENT AND MAINTENANCE OF TMJ PAIN 60
B PSYCHOPHYSICS OF TMJ DISORDERS 67
C NEUROANATOMY OF THE TMJ 75
D CENTRAL REPRESENTATION OF TMJ AFFERENTS 81
E TRIGEMINAL GANGLION 84
F GROSS ANATOMY 86
IV

G SUMMARY TABLES OF TMJ REACTIVITY 90
LIST OF REFERENCES 118
BIOGRAPHICAL SKETCH 130
v

LIST OF TABLES
Table 3-1 TMJ force/movement relationships in the vertical plane 25
Table 3-2 Properties on nociceptors that demonstrate vertical plane or horizontal
plane reactivity 28
Table 3-3 Mean values of properties of TMJ nociceptors 37
Table 3-4 Qualitative improvements in reactivity for nociceptors that were
characterized in normal tissue and then tested again subsequent to
carrageenan injection 46
Table 3-5 Changes in reactivity for 8 units after exposure to saline 51
Table G-l Reactivity in vertical plane (normal tissue) 91
Table G-2 Reactivity in horizontal plane (normal tissue), left lateral 92
Table G-3 Reactivity in horizontal plane (normal tissue), right lateral 93
Table G-4 Reactivity in the vertical plane in previously inflamed tissue. Reactivity
in horizontal plane in previously inflamed tissue, left lateral 94
Table G-5 TMJ nociceptor reactivity in normal tissue, vertical plane 95
Table G-6 TMJ nociceptor reactivity in normal tissue, horizontal plane 96
Table G-7 TMJ nociceptor reactivity in previously inflamed tissue 97
Table G-8 TMJ nociceptor reactivity in acutely inflamed tissue 98
Table G-9 TMJ nociceptor reactivity in saline injected tissue 99
Table G-10 Effect of carrageenan in acutely inflamed tissue reactivity in the vertical
plane, unit #1 100
Table G-l 1 Effect of carrageenan in acutely inflamed tissue reactivity in the vertical
plane, unit #2 101
Table G-l2 Effect of carrageenan in acutely inflamed tissue reactivity in the vertical
plane, unit #3 102
Table G-13 Effect of carrageenan in acutely inflamed tissue reactivity in the vertical
plane, unit #4 103
vi

Table G-14 Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal
plane, unit #1 104
Table G-15 Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal
plane, unit #2 105
Table G-16 Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal
plane, unit #3 106
Table G-17 Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal
plane, unit #4 107
Table G-18 Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal
plane, unit #5 108
Table G-19 Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal
plane, unit #6 109
Table G-20 Effect of carrageenan in acutely inflamed tissue reactivity in the horizontal
plane, unit #7 110
Table G-21 Effect of saline reactivity in the horizontal plane, unit #1 111
Table G-22 Effect of saline reactivity in the horizontal plane, unit #2 112
Table G-23 Effect of saline reactivity in the horizontal plane, unit #3 113
Table G-24 Effect of saline reactivity in the horizontal plane, unit #4 114
Table G-25 Effect of saline reactivity in the horizontal plane, unit #6 115
Table G-26 Effect of saline reactivity in the horizontal plane, unit #7 116
Table G-27 Effect of saline reactivity in the horizontal plane, unit #8 117
vu

LIST OF FIGURES
Figure 2-1 Mandibular movements were produced by a hand held probe 8
Figure 2-2 Dynamic and static test series for force, displacement and velocity 10
Figure 2-3 Demonstration of sensitization as a shift of stimulus-response functions.. 14
Figure 3-1 Receptive field distribution in the lateral and posterior capsule of the
temporomandibular joint for normal tissue 18
Figure 3-2 Receptive field distribution in the lateral and posterior capsule of
the temporomandibular joint for previously inflamed tissue, acutely
inflamed tissue and saline control tissue 20
Figure 3-3 Relationships between applied force and vertical plane movements of
the mandible 23-24
Figure 3-4 Dynamic reactivity in normal tissue 30
Figure 3-5 Dynamic reactivity in previously inflamed tissue 33
Figure 3-6 Averaged dynamic response functions of nociceptors fitted in normal
and previously inflamed tissue 41
Figure 3-8 Reactivity of nociceptors exposed to saline 43
Figre 3-9 Comparison between pre-inflamed and post-inflamed reactivity in
scatter plot forms 48-49
Figure F-l Schematic diagram of the human temporomandibular joint. Sagittal and
frontal views 87
viii

KEY TO SYMBOLS
Vertical plane or previously inflamed tisue.
A Horizontal plane or acutely inflamed tissue.
+ Saline control tissue.
IX

Abstract of Dissertation Presented to the Graduate School
of the University of Florida in Partial Fulfillment of the
Requirements for the Degree of Doctor of Philosophy
PROPERTIES OF TEMPOROMANDIBULAR JOINT NOCICEPTORS
IN NORMAL AND INFLAMED TISSUE
By
Barry Loughner
May, 1992
Chairman: Parker Mahan, D.D.S., Ph.D.
Cochairman: Brian Cooper, Ph.D.
Major Department: Oral Biology
Mechanical response properties of nociceptors of the goat temporomandibular joint
(TMJ) were characterized by unit recordings from the trigeminal ganglion. Populations of
afferents were sampled in normal tissue and in tissue previously inflamed (PI) with
carrageenan for at least 6 hours prior to testing. In other experiments, nociceptors were
characterized in normal tissue and then retested for up to 3 hrs subsequent to exposure to
carrageenan (AI). To produce mandibular movement in the vertical and horizontal planes,
dynamic and static forces were applied to the mandibular pole. Stimuli were quantified by
force and angular displacement transducers. Receptive fields were small, single spots (2-3
mm) and located on the lateral or posterior capsule of the TMJ. Conduction velocities were
shown to be in the group III and IV range. Stimulus-interval data was best described by
power functions. Assessment of force-movement relationships indicated that capsular
nociceptors responded exclusively to intense forces that produce extreme displacements of
the mandible.
x

In normal tissue, 24 of 36 nociceptors transduced dynamically applied stimuli
(mean activation threshold for dynamic force = 15.9 11.3 N and for force velocity =
17.3 + 18.9 N/s). Relatively fewer units transduced static force (8/36) or position
(1/36).
In PI conditions, tests revealed enhanced reactivity for dynamically applied
stimuli. Mean power functions for dynamic tests in PI conditions (LnISI = -1.3 LnF +
7.3) had steeper slopes compared to those in normal tissue (LnISI = -1.1 LnF + 5.4)
and were shifted graphically to regions indicating greater reactivity (below and to the
left of those in normal tissue). These shifts were suggestive of sensitization.
In AI conditions, 8 of 11 nociceptors acquired either dynamic or static coding
ability. Acquired coding ability also appeared in nociceptors (n = 2) that were without
transducing capacity in normal tissue. Acquired reactivity for vertical plane movement
was also seen for those nociceptors (n = 3) that were reactive only to movement in the
. *
horizontal plane in normal tissue. Acquisition of coding ability following carrageenan-
induced inflammation suggested afferent sensitization.
xi

CHAPTER 1
INTRODUCTION
The temporomandibular joint (TMJ) is the site of a number of disorders that burden
the health care system and extract a large cost in human suffering (Helkimo, 1979; Solberg,
1987). Afferent groups presumed to mediate TMJ pain are likely to play a role in a variety
of TMJ disorders. Many theories have been proposed to explain TMJ pain and dysfunction
(Deboever, 1973; Dubner et al., 1978, Yemm, 1979). These theories propose both intra-
and extra-articular origins of TMJ pain. Intra-articular theories argue that pressure or
tension on articular tissues results in TMJ pain. Extra-articular theories propose that
muscles or other contiguous structures refer pain to the TMJ (see Appendix A).
Fundamental to an evaluation of intra-articular theories is an understanding of the response
properties of TMJ nociceptors.
Our understanding of nociceptors innervating articular tissues has been advanced in
recent years (Schaible and Schmidt, 1983a, b, 1988b; Guilbaud et al., 1985; Birrell et al.,
1990). Most detailed information concerning the response properties of joint nociceptors
has come from studies of the cat knee and rat ankle joint. While there is considerable
information regarding the neuroanatomy of the TMJ (see Appendix C), little is known
about the physiology of nociceptors of the temporomandibular joint.
Early studies examining properties of afferents innervating the cat knee joint
reported activation of slowly conducting, myelinated fibers only by forceful rotational
movements beyond the physiological range of motion (Burgess and Clark, 1969; Clark and
Burgess, 1975). In contrast, Schaible and Schmidt (1983b) identified populations of
1

2
small fibers that were activated by passive movement of the knee joint, both within and
beyond the normal range of motion. These afferents were categorized into four populations
on the basis of their response range. Afferents of populations I and II responded to
innocuous joint movement in the normal range of motion, but population II responded best
to forceful rotation. Population III units were activated exclusively by forceful movement
and population IV had no response to movement. Based on movement sensitivity,
afferents that responded within the normal range of motion were not considered
nociceptors, while those that respond beyond the normal range were nociceptors.
Subsequent studies by Schaible and Schmidt (1985, 1988b) concentrated on populations
III and IV. However, despite the importance of range for classifying afferents, distinctions
between normal and non-normal ranges have been ancedotal. Quantification of the
relationship between range of motion and afferent activity is still pending.
There are no studies that have examined properties of TMJ nociceptors. Previous
reports have examined the discharge characteristics of afferent traffic in the
auriculotemporal nerve that may contribute to position sense and control of mandibular
movement (Kawamura et al., 1967; Klineberg et al, 1970, 1971; Kawamura and Abe,
1974; Lund and Matthews, 1981). While TMJ nociceptors may have properties similar to
those described for cat knee joint, there are considerable functional and anatomical
differences between these two joints that indicate that properties of TMJ nociceptors should
be determined (see Appendices C and F).
Changes in the properties of TMJ nociceptors (sensitization) may account for some
of the symptoms of TMJ dysfunction. These symptoms include pain during mandibular
movement, pain on local joint palpation, and tonic pain. Changes in nociceptor properties
are likely to be necessary to the development of these forms of pain. As pain on movement
is a primary symptom of TMJ dysfunction, a precise determination of the relationship
between movement and afferent discharges is valuable. Quantification of force and
movement also permits more direct specifications of movements which are outside the

3
normal range of motion, and identification of afferents that respond specifically in these
ranges.
Sensitization of TMJ receptors may be an important defense mechanism that
protects the joint from excessive movement which may cause injury. The TMJ is often the
site of inflammations associated with various forms of TMJ dysfunction (e.g. arthritis and
synovitis). An understanding of how inflammation may modify TMJ afferent function
would reveal the form and range of TMJ afferent sensitization and lead to a better
understanding of both etiology and treatment.
Sensitization of nociceptors has been documented in the cat knee joint (Coggeshall
et al., 1983; Schaible and Schmidt, 1985, 1988b; Grigg et al., 1986) and in the rat ankle
joint (Guilbaud et al., 1985) following chemically-induced acute or chronic arthritis. Acute
arthritis in the cat knee joint, induced by carrageenan and kaolin, produced changes in the
discharge properties in joint afferents. These changes include an increase in the proportion
of small fibers that could be activated by innocuous joint movement, recruited units, and
the appearance of spontaneous activity. Studies of sensitization of TMJ nociceptors may
provide uniquely important information regarding short and long term changes occurring in
TMJ afferents following local trauma, arthritis or chronic disc displacement.
In the following experiments, we examined properties of TMJ nociceptors in both
normal and inflamed tissue of the goat. The goat is an excellent model for TMJ physiology
because of functional and structural similarities to humans including range of motion and
innervation of the auriculotemporal nerve. (See Appendices C and F).

CHAPTER 2
METHODS
Subjects
Experiments were performed on 59 goats, ages 6-12 months and weighing 30-60
lbs. All goats were kept in pens at the veterinary hospital. Goat health was monitored and
maintained by animal care technicians, veterinary staff and faculty. All procedures were
approved by an internal review board (protocol 7136).
Exposure of the TMJ and Trigeminal Ganglion
Rompun (3 mg/kg) and Ketamine (11 mg/kg) were given as preanesthetics.
Anesthesia was induced with a-chloralose (7.5 mg/ml) via a lactated ringers drip. If
necessary, pentabarbitol was periodically administered intravenously to maintain deep
anesthesia. Goats were artifically respirated at a rate of 10-20 breaths per minute. Blood
pressure, body temperature and end-tidal CO2 were continuously monitored and maintained
within physiological limits. At the conclusion of each experiment, the goats were
euthanized with saturated KCL.
To expose the right TMJ, the skin was removed from the lateral posterior aspect of
the face. The parotid gland, pinna and the zygomaticoauricularis muscles were removed to
access the posterior portion of the TMJ capsule. The styloid process and associated
muscular and ligamentous attachments were clipped off at the sphenoid bone. The origin of
4

5
the stemomastoid and caudal digastric muscles were excised from the mastoid process and
jugular process of the occiput, respectively. The sphenomandibular ligament and fatty
tissues were removed. Care was taken to preserve the microvasculature of the TMJ
capsule. The exposed capsular tissue was kept moist by repeated applications of
physiological saline.
Several nerves were cut distal to the trigeminal ganglion in order to avoid recording
activity other than TMJ afferents. The buccinator nerve was severed as it passed the
anterior border of the masseter muscle. The masseteric nerve was cut as it entered the deep
and superficial masseter muscle. The posterior trunk of the mandibular nerve was cut distal
to the branching of the auriculotemporal nerve. As a consequence, afferents of the lingual,
inferior alveolar and mylohyoid nerves were eliminated.
The trigeminal ganglion was accessed via its position caudal to the foramen ovale.
Removal of the thin, lateral plate of bone of the tympanic bulla and the tympanic plate
exposed the ossicles of the middle ear and internal surface of the tympanic membrane.
Removal of the inferior aspect of the greater wing of the sphenoid and the inferior aspect of
the petrous bone exposed the caudal surace of the trigeminal ganglion. Access to the
ganglion is improved by removing the sphenomandibular ligament and fatty tissue in the
infratemporal fossa.
Recording Procedures
Extracellular recordings were made by penetration of the trigeminal ganglion with
tungsten microelectrodes (Microprobe, Inc.) until unit potentials were evoked by passive
jaw movement. Most units were found in the posterior region of the trigeminal ganglion.
(See Appendix E). Receptive fields were then identified on the lateral or posterior capsule
of the TMJ. Amplified output was led to and monitored by a digital oscilloscope and an
audio speaker. Data was digitized and stored on video tape (Vetter Instruments, Model No.

6
3000A). Data were recovered from tape for analysis with an RC computerscope (RC
Electronics) or captured on a line by a thermal printer (Astromed, Dash IV).
After a unit was characterized, the conduction velocity was determined by
measuring the latency of responses to suprathreshold electrical stimulation applied to the
receptive field on the TMJ capsule. Electrical stimulation was performed with a Grass S88
stimulator and isolated, constant current unit. Square-wave pulses of 0.2 to 2 msec
duration were applied with monopolar electrodes. Conduction distance was estimated in
situ.
Characterization of TMJ Afferents
Once an afferent was isolated, passive jaw movements were used to determine
which type of movement was preferred (preferred movements were those which produced
*
the most vigorous response). Jaw movements included: 1) vertical jaw movements from
the closed to the open position. Afferent responses to vertical jaw movements were termed
"vertical plane reactivity" (VP); 2) lateral jaw movements from the closed to extreme lateral
position. Afferent responses to the lateral jaw movements were termed "horizontal plane
reactivity" (HP).
A force probe was used to produce jaw movement. The probe consisted of an axial
force transducer (Entran Instruments, Model ELF TC500-20) embedded in a plexiglass
rod. The transducer monitored forces used to move the jaw in the vertical or horizontal
plane. The probe was applied to fixed points of a bit which was mounted to the incisal
teeth of the mandible at the midline. Force and jaw movement were recorded on video tape
along with afferent activity. Jaw movement was monitored by an angular displacement
transducer (ADT, Trans-Tek Model # 604-001) mounted above the right TMJ (Figure 2-1).
Using the probe, both dynamic and static forces were applied to the mandible (Figure 2-2).

Figure 2-1. Mandibular movements were produced by a hand held probe. Force
applied to the mandible was quantified by a force transducer. Vertical
plane mandibular movement was quantified by an angular displacement
transducer mounted above the right TMJ and attached to the mandibular
pole by a slide assembly. Vertical plane movement of the mandible was
produced by applying force at point A on the jaw movement apparatus.
Horizontal plane movement was produced by applying force at point B.
Afferent recordings were made following exposure and penetration of the
trigeminal ganglion proximal to the foramen ovale.

8

Figure 2-2. Dynamic and static test series for force, displacement and velocity. A)
Dynamic test series. Sawtooth patterns of successively increasing
velocities. B) Static test series. Stepwise pattern of successively
increasing force and displacement.

10
A
UNITS
FORCE (N)
DISPLACEMENT (dog)
B
UNrrs
FORCE (N)
DISPLACEMENT (deg)
TEST FOR DYNAMIC REACTIVITY
I 1 W ft ft
TEST FOR STATIC REACTIVITY
1 H H ih
20-1
IS-
to-
*'
30
20-
10
TIME

11
Isolated units were characterized by two series of jaw manipulations. The first
series consisted of five tests of reactivity to dynamic force. The first, at a low velocity,
was followed by jaw movements of progressively higher velocities. The range of
velocities was approximately 0.3 to 250.0 N/sec. The second series consisted of five
stepwise, static force applications. Each step was maintained for approximately 2 seconds.
Forces up to 120 N were applied.
To confirm that jaw movement activated afferents of the TMJ capsule, receptive
fields on the capsule were identified and characterized for each case. Thresholds for
activation of mechanosensitive afferents on the capsule of the TMJ were determined by the
bending force of von Frey filaments (monofilament nylon) of different stiffnesses. The
method of limits was used to determine threshold. Nylon probes were applied to the
capsular field until the minimum force required to activate the afferent was determined. In
some cases, no receptive field could be found. This group of cases was treated separately
from afferents with identified receptive fields.
Statistics
Nociceptors were defined as those afferents that responded preferentially to
extremes of jaw movement. Relationships between force applied and jaw movement were
assessed to determine whether the afferents reacted at movement extremes. Force-
movement data was plotted for all units (n = 10) that responded preferentially to vertical
jaw movement and produced significant functions. Momentary relationships between
force, jaw movement and unit activity were determined. Force-interspike interval,
movement-interspike interval and velocity-interspike interval records were fit to linear,
logarithmic, exponential or power functions using simple linear regression (Statistical
Analysis System, SAS). The best fits were determined by comparison of coefficients of
determination.

12
For analysis of static reactivity, regression data were "segmented and balanced." A
segment ^or step) of force was added to the regression model until the coefficient of
determination was maximal. The regression was "balanced" by using only six scores for
each stepwise force segment. This procedure avoids weighting the regression differentially
at higher steps, where more scores typically bias the regression. These procedures were
not possible on tests of dynamic force reactivity. Therefore, for dynamic force or
movement tests, all spike intervals were used until a minimum interval was obtained.
Several characteristics of regression lines were subjected to analysis. These
included force-activation thresholds, movement-activation thresholds, force-frequency
asymptotes, movement-frequency asymptotes, mean response intervals, slopes and
intercepts. Force-activation thresholds (FAT) and movement-activation thresholds (MAT)
were defined as the instantaneous force or degree of movement at the first response
interval. Force-frequency asymptotes (FFA) and movement-frequency asymptotes (MFA)
were defined as the force or movement at which the frequency response was maximal (i.e.,
minimum response interval). The FAT or MAT paired with the FFA or FMA were used as
the lower and upper boundary values to plot functions derived from regressions. The mean
response interval (MRI) was calculated from the regression equation by using the mean
force or movement value calculated from the boundary values (FAT + FFA/2 or MAT +
MFA/2). Force-frequency thresholds and movement-frequency thresholds (FFTs and
MFTs) were determined for each unit that was tested for static reactivity. The FFT and
MFT were defined as the minimum force or movement which would maintain a sustained
discharge of the afferent. Slopes, intercepts and coefficients of determination were
generated only from significant regressions. Unit reactivity that could not be described by
significant functions were called "non-coding" or "non-transducing" afferents.
"Sensitization" refers to the enhanced excitability of TMJ afferents that may occur
following carrageenan-induced inflammation. Enhanced excitability is reflected
quantitatively as changes in response properties of TMJ afferents in normal and in inflamed

13
tissue. Sensitization was assessed qualitatively by comparisons of functions fit to units in
normal and inflamed tissues.
Shifts of stimulus-response coding functions were used as an indication of
enhanced reactivity. Significant functions generated from responses of afferents in
inflamed tissue that were located graphically below and/or to the left of functions fit in
normal tissue were suggestive of sensitization (See Figure 2-3). Significant functions that
were acquired in inflamed tissue but not expressed in normal tissue also were considered to
represent sensitization. Sensitization was assessed quantitatively by statistical comparisons
of function characteristics generated from stimulus tests on units in normal and inflamed
conditions. Function characteristics (slope, intercept, thresholds, asymptotic activity,
coefficients of determination and mean interval) were compared in normal and inflamed
conditions using a one-way ANOVA (Li, 1967) for between subject and t-tests for within
subject's comparisons. Only significant functions contributed to the analysis.
Experimental Inflammation
Inflammation of the TMJ was induced by injection of 200 p.1 of 2% carrageenan
(Sigma Chem.). In some cases, units were characterized in normal tissue and then exposed
to carrageenan. If the receptive field was located on the lateral side of the capsule,
carrageenan was dropped directly onto the receptive field as well as injected into the area of
the receptive field. If the receptive field was located on the posterior side of the capsule,
carrageenan was injected into the area of the receptive field. The remainder of the
carrageenan was injected into the superior joint space. Subsequent testing was performed
after at least 30 minutes and continued for up to 3 hours. In other cases, units characterized
in normal tissue were treated with saline. The injection of saline and subsequent retests
were identical to those used with carrageenan. In other cases, response properties of
separate populations of TMJ afferents were examined only in normal or pre-inflamed

14
DEMONSTRATION OF SENSITIZATION
SHIFT OF STIMULUS-RESPONSE CODING FUNCTION
0 1 2 3 4 5
Ln Force (Newtons)
V Function A Function B
Figure 2-3. Demonstration of sensitization as a shift of stimulus-response
functions. Shifts of significant stimulus-response functions to graphic
zones of enhanced reactivity (below and to the left) suggests
sensitization. For downward shifts, each point on line B represents a
higher rate of discharge (shorter interval) at an equivalent force. For
leftward shifts, reactivity appears at forces which previously were
ineffective.

15
tissue. In this instance, inflammation was induced at least 6 hours before recording began.
Carrageenan (2%, 200 jil) was injected into the lateral and posterior aspects of the TMJ
capsule as well as the superior joint space.

CHAPTER 3
RESULTS
Identification of TMJ Nociceptors
Receptive fields for units with VP or HP reactivity were found on the lateral and
posterior capsule of the TMJ (Figures 3-1 and 3-2). The mean von Frey thresholds for VP
and HP units were 27 39 g and 15 20 g, respectively. The receptive fields of these
units were single, small spots (approximately 2-3 mm). In some cases, receptive fields
could not be identified. It is possible that the receptive fields of these units were located on
the medial capsule, posterior attachment tissues or peripheral portions of the articular disc.
Alternatively, it is possible that units without identified receptive fields were not of TMJ
origin but, instead, of muscular origin (lateral pterygoid or temporalis muscles).
Conduction velocities were determined to be in the group III and IV fiber range (0.4 to 8.5
m/s). Due to the inaccessibility of many of the receptive fields, conduction velocities could
only be obtained for 30% of the units (19 of 63 units).
The response characteristics of TMJ afferents were examined. Mechanical
reactivity to jaw movement was determined using both dynamically and statically applied
forces. In order to distinguish between joint afferents acting as proprioceptors from those
acting as nociceptors,we searched for afferents with a preference for intense stimuli. It was
predicted that TMJ nociceptors would respond in the noxious range of mandibular motion,
where the noxious range of motion was defined as that passive mandibular motion where
the mandible encounters considerable resistance imposed by constraints of soft tissue.
16

Figure 3-1. Receptive field (RF) distribution in the lateral and posterior capsule of the
TMJ for normal tissue. A) Distribution of RFs in the lateral capsule. B)
Distribution of RFs in the posterior capsule. RFs (n=36) of afferents in
A) and B) responded to either vertical plane (.) or horizontal plane (A)
movement of the mandible. POST, posterior, ANT, Anterior, MED,
medial; LAT, lateral.

A
POST
B
MED

Figure 3-2. Receptive field (RF) distribution in the lateral and posterior capsule of the
TMJ for previously inflamed tissue (), acutely inflamed tissue (a) and
saline control tissue (+). A) Lateral capsule. B) Posterior capsule.
POST, posterior, ANT, anterior, MED, Medial; LAT, lateral.

20
B
MED

21
Therefore, relationships between applied force and jaw movement were examined to
determine the noxious range and compare it with afferent discharge properties.
Due to physical constraints of the preparation, force-movement relationships could
only be examined for VP units. Characterization of force-movement relationships in the
vertical plane revealed a biphasic relationship between applied force and mandibular
movement (Figure 3-3). Linear force-movement relationships gave way to exponential
force-movement relationships when the mandible reached an extreme of opening. It is
likely that this exponential phase corresponds to the noxious range. Force-movement
curves of VP units (n = 10) were best described by power functions (Table 3-1). Power
functions were the best fit in 10 of 10 cases (R2 = 0.92 0.06). The functional range of
VP units may be graphically assessed by observing activation thresholds plotted on force-
movement curves. As can be seen in Figure 3-3, nearly all afferents began to respond in
the transition zone between the linear and exponential phases of the curves. This can be
examined statistically by examining the functions fit below the point of activation. For the
10 cases in which power functions were fit, activation threshold occurred during portions
of the curves which were exponentially accelerating (6/10 cases, R2 = 0.86 + 0.17). In 4
cases, activation thresholds occurred in portions of the curve in which force was increasing
linearly (R2 = 0.88 0.19). The activation thesholds of these 4 units occurred at forces
approaching the power phase of the curve. The observed preference for high forces (mean
activation threshold for force = 20.6 11.0 N; mean frequency asymptote = 49.6 + 20.7
N) at extremes of the range of motion (mean activation threshold at 13.7 5.4; mean
frequency asymptote = 20.4 5.9) suggested that these TMJ afferents were nociceptors.
Characterization of TMJ Nociceptors in Normal Tissue
Units were classified according to their preferred movement plane. Preferred
movement was defined as that plane of motion in which mandibular excursion evokes the

Figure 3-3. Relationships between applied force and vertical plane movements of the
mandible. Ten biphasic curves indicated that low forces were sufficient to
open the jaw through most of its range of motion. High forces produce
minimal degrees of opening where the joint encounters considerable
resistance from soft tissue. In each case, the TMJ nociceptor begins to
respond at the point indicated by the arrow.

23
TMJ FORCE/MOVEMENT RELATIONSHIPS: VERTICAL PLANE
A D
TEST
1
FORCE (N*wton*)
TEST -- TEST
2 3
TEST
4
1 2 3 4 5
B
E
FORCE (Newton*)
-4- TEST-4- TEST-4- TEST-- TEST-4- TEST
1 2 3 4 5
FORCE (Newton*)
-4- TEST-4- TEST-- TEST-- TEST-4- TEST
1 2 3 4 5
c
F
FORCE (Newton*)
-4- TEST-4- TEST-4- TEST-- TEST -4- TEST
1 2 3 4 5
FORCE (Newton*)
4- TEST
1
TEST
2
- TEST
3

24
TMJ FORCE/MOVEMENT RELATIONSHIPS: VERTICAL PLANE
Figure 3.3. (contd)

25
Table 3-1
Force/Movement Relationships in the Vertical Plane
FILE
FUNCTION
FULL RANGE
LOW RANGE
2
R
P
042090H
POW
Lnl = 0.69 LnF + 4.8
0.93
0.0001
042090H
LIN
I = 0.15 F+ 1.8
0.90
0.0001
042090H
POW
Lnl = 0.8 LnF + 0.89
0.96
0.0001
042090H
LIN
I = 0.2F + 0.87
0.95
0.0001
110990E
POW
Lnl = 0.8 LnF + 2.1
0.97
0.0001
1I0990E
LIN
I = 0.6 F + 2.3
0.96
0.0001
110990E
POW
Lnl = 1.1 LnF + 0.15
0.92
0.0001
110990E
LIN
I = 1.0 + 0.19
0.97
0.0001
111490D1
POW
Lnl = 0.4 LnF + 1.1
0.91
0.0001
111490D1
LIN
I = 0.1F + 8.5
0.87
0.0001
111490D1
POW
Lnl = 1.7 LnF+ 2.2
0.92
0.0001
111490D1
LIN
I = 1.0F + 4.2
0.86
0.0001
111490D2
POW
Lnl = 1.3 LnF + 1.2
0.91
0.0001
111490D2
LIN
I = 0.7F+ 0.22
0.87
0.0001
111490D2
POW
Lnl = 2.3 LnF + 3.5
0.94
0.0001
111490D2
LIN
1= 1.4F + 7.4
0.97
0.0001
022791A
POW
Lnl = 0.3 LnF + 2..2
0.93
0.0001
022791A
LIN
I = 0.77F + 11.0
0.79
0.0001
022791A
POW
Lnl = 0.15 LnF +2.0
0.80
0.04
022791A
LIN
1= 1.8F + 5.9
0.97
0.0001
03289IX
POW
Lnl = 0.37 LnF + 1.1
0.99
0.0001
03289IX
LIN
I = 0.23F + 3.7
0.88
0.0001
03289IX
POW
Lnl = 0.4 LnF + 0.01
0.98
0.0001
03289IX
LIN
I = 0.55F + 2.3
0.88
0.0001
080591C
POW
Lnl = 0.34 LnF + 1.9
0.87
0.0001
080591C
LIN
I = 0.28F + 12.0
0.77
0.0001
080591C
POW
Lnl = 0.46 LnF + 1.8
0.57
0.0003
080591C
LIN
1= 1.5 F +5.3
0.61
0.0001
091691A
POW
Lnl = 0.54 LnF + 1.3
0.87
0.0001
091691A
LIN
I = 0.42F + 9.0
0.83
0.0001
091691A
POW
Lnl = 0.64 LnF + 1.2
0.52
0.01
091691A
LIN
I = 2.3 F+ 1.3
0.37
0.04
09279 IK
POW
Lnl = 0.48 LnF + 1.4
0.96
0.0001
09279 IK
LIN
I = 0.37 F + 8.6
0.88
0.0001
09279IK
POW
Lnl = 0.59 LnF + 1.3
0.90
0.0001
09279IK
LIN
1 = .97F + 4.1
0.88
0.0001
101891F
POW
Lnl = 0.5 LnF + 1.3
0.83
0.0001
101891F
LIN
I = 0.29F + 11.0
0.73
0.0001
101891F
POW
Lnl = 0.74 LnF + 1.0
0.86
0.0001
101891F
LIN
I = 0.9 F + 5.6
0.64
0.0001
Note: POW, power, LIN, linear.

26
strongest response from an afferent. Thirty-six afferents with receptive fields in the TMJ
capsule were activated by either vertical plane (VP or opening) or horizontal plane (HP or
lateral displacement) motion. Eighteen afferents responded preferentially to movement in
the vertical plane and 18 responded best to movement in the horizontal plane. A few units
were activated by right lateral displacement (n = 5) or protrusive (n = 2) movement but
most TMJ afferents responded preferentially to either opening (VP) or left lateral
displacement (HP).
Once preferred movement was determined, tests of dynamic and static reactivity
were conducted. Relationships between force, position or movement and response interval
were quantified. The responses of TMJ nociceptors were quantified by regressions fit
between instantaneous dynamic force, force velocity, movement, static force or position
and instantaneous interspike interval.
As it was not clear which function would best describe TMJ afferents, linear,
power, logarithmic and exponential models were explored. By comparison of the relative
proportions of variance accounted for by each model, it was determined that power
functions accounted for the greatest percentage of variance (mean R2 = 0.46 + 0.26; n = 71
cases). Power functions were best fits compared to other functions for both dynamic
(26/59 cases) and static tests (10/12 cases). Power functions were second best fits in 20
out of 59 cases for dynamic tests and 1 out of 12 cases for static tests. Linear functions
were superior in 7 cases, logarithmic in 12 cases and exponential in 16 cases. Since power
functions were the best or second best fit in 46 of 71 cases (mean R2 = 0.45 .30), power
functions were used to represent the data in normal tissue. In inflamed tissue (both PI and
AI), power functions accounted for the greatest percentage of variance in 101 of 146 cases
(mean R2 = 0.50 0.21).
TMJ nociceptors could be found which transduced (or coded) all aspects of force,
movement or position, and many transduced more than one variable. "Code" indicates that

27
a unit's reactivity was proportional to force or some other stimulus variable and that the
relationship could be described by a significant power function.
The great majority of TMJ nociceptors (n = 24) coded dynamic aspects of force
applied to the mandible, and relatively few coded for static aspects of these stimuli.
Twenty-three of 36 units that responded to either VP or HP jaw movement coded for
dynamic force (mean activation threshold = 20.1 17.5 N) and 15 of 36 units coded for
force velocity (mean activation threshold = 15.5 20.5 N/s; Table 3-2). In contrast, only
8 of 36 units coded for static force (mean activation threshold 17.8 18.3 N), while 5 of
35 units coded jaw movement (mean activation thresholds of 11.0 4.0, and only 1 of
36 units coded for jaw position. In some cases, unit reactivity could be described by more
than one function. Twelve of 23 units that could be fit to dynamic force were also
significantly fit to force velocity. Six of these 12 units were significantly fit to force
velocity, and 6 of these 12 units were signficantly fit to static force as well. Ten of 36 units
could not be fit to any function. Fourteen additional units had jaw movement reactivity but
no receptive field could be found.
Mean functions were generated from individually fitted functions by pooling
slopes, intercepts and boundary values. Functions presented in Figure 3-4 represent the
principle transducing properties of TMJ afferents: dynamic force and force velocity.
Properties of TMJ Nociceptors in Inflamed Tissue
The response properties of afferents were examined in capsular tissue that was
previously inflamed (PI) by carrageenan. In these experiments, TMJ tissues were exposed
to carrageenan for at least 6 hours prior to testing. In other experiments, afferents were
tested in normal tissue and then tested again after an acute injection of carrageenan or
saline. Afferent reactivity was examined for up to 3 hours subsequent to exposure to
carrageenan.

28
TABLE 3-2
TMJ NOCICEPTOR REACTIVITY IN NORMAL TISSUE
Test Conditions
with RF (n=36)
without RF (n=14)
code (n=25)
no code (n=10)
code (n=9)
no code (n=5)
Dynamic Force
23
12
6
6
Force Velocity
15
19
4
8
Movement
5
10
2
3
Static Force
8
23
1
4
Static Position
1
14
0
4
Conduction
Velocity
0.4 to 7.5
m/sec
(n = 6)
0.5 to 1.5
m/sec
(n = 3)


Post-test
Spontaneous
Activity
3
0
0
0
Note: Receptive fields (RF) in the TMJ capsule were identified for 36 units. Twenty-five
units with RFs coded for one or more of the stimuli. Most units (n = 23) with an
RF on the TMJ capsule coded for dynamic force. Fourteen additional units had
either VP or HP reactivity but an RF could not be found. "Code" indicates that a
unit's reactivity could be described by a significant power function. Of the 36
afferents with RFs in the TMJ capsule, 3 units demonstrated spontaneous
activity after dynamic or static testing. Five units with RF's in the TMJ capsule
responded preferentially to right lateral displacement. Most of these units ( 3 of
5 cases) coded dynamic force. Appendix G contains descriptive statistics for
these units.

Figure 3-4. Dynamic reactivity in normal tissue. Power functions best described the relationship between instantaneous dynamic
force and force velocity with instantaneous response interval for afferents responding to mandibular movement in the
vertical plane (VP) and horizontal plane (HP). A) Ten of 18 VP units transduced dynamic force (mean slope = -1.3 +
0.2; range = 17.0 33.5 to 48.5 22.0 N; mean R2 = 0.46 0.21). These units were activated at a mean opening of
11.2 4.4. The range of activity of each nociceptor was defined as the smallest force or movement required to
produce the minimum response frequency to the force of movement that produced the highest response frequency. B)
Eight of 18 VP units transduced force velocity (mean slope = -0.6 + 0.2; range = 17.5 19.5 to 157.0 86.0 N/s;
mean R2 = 0.30 0.18). C) Thirteen of 18 HP units transduced dynamic force (mean slope = -0.9 0.7; range = 9.7
7.3 to 37.0 + 22.8 N; mean R2 = 0.39 0.24). D) Seven of 18 HP units transduced force velocity (mean slope = -
0.39 0.24; range = 7.9 + 16.9 to 166.0 92.2 N/s; mean R2 = 0.27 0.14).

A REACTIVITY IN THE VERTICAL PLANE:
DYNAMIC FORCE
0 1 2 3 4 5 6
Ln FORCE (Newtons)
-A- D1 E2 E2 L3 A1
-7- S3 -O- K7 -O- H6 -O- E3 -O- G3
C REACTIVITY IN THE VERTICAL PLANE:
FORCE VELOCITY
-2 -1 0 1 2 3 4 5 6
Ln VELOCITY (Newtons/sec)
-A- D1 E2 L3 A1
-7- S3 -o- N7 -O- G3 -O- G3
B
REACTIVITY IN THE HORIZONTAL PLANE:
DYNAMIC FORCE
0 1 2 3 4 5 6
Ln FORCE (Newtons)
-A- A1 A1 A1 C2 A A1
-A- D -O- J4 -O- A1 D3 A1 + A1
D REACTIVITY IN THE HORIZONTAL PLANE:
FORCE VELOCITY
-2 -1 0 1 2 3 4 5 6
Ln VELOCITY (Newtons/sec)
-A- A1 A1 C2 A2
A1 D3 -V- J4
LO
O

31
Experiment!: Properties of Units in the
Previously Inflamed TMJ
In the PI condition, transduction of the dynamic aspects of stimulus force was best
described by power functions. Power functions were the best fit compared to other
functions (7 of 13 cases; R2 = 0.33 0.25) and were best or second best fit in 9 of 13
cases. Therefore, exposure to carrageenan did not modify the nature of functions which
described afferent activity. Individually fitted power functions generated during dynamic
and static response testing in inflamed tissue are illustrated in Figure 3-5.
Comparison of units in normal and inflamed tissue (see Figure 3-6) suggested
improved reactivity for units that responded preferentially to movement in the vertical
plane. Increased reactivity to dynamic stimuli was particularly prominent. In normal
tissue, 11 of 18 units with RFs on the TMJ capsule coded for dynamic force or velocity;
while proportionally more units (5/5) transduced dynamic force or velocity in the PI
condition. Mean functions for dynamic force in inflamed and noninflamed conditions were
calculated by averaging slopes and intercepts of individual functions (Lnl = -1.3LnF + 7.3,
(n = 25); Lnl = 1.1 LnF + 5.4, (n = 6)] for inflamed and noninflamed, respectively). The
mean functions for all VP and HP units fitted during dynamic testing in normal and
inflamed tissue suggested improvement of dynamic reactivity (Figure 3-6). The shifts of
the mean function for units in PI condition to a graphic position below the mean function
for normal tissue was suggestive of sensitization to dynamic forces.
Mean functions were also calculated for afferents transducing force velocity. A
shift of the mean function of PI units that coded for force velocity [Lnl = -0.7 LnF + 3.5,
(n = 6)] was also observed in comparison to the mean functions in normal tissue [Lnl = -
0.38 LnF + 4.7, (n = 16)]. These functions are illustrated in Figure 3-6. A shift of the
mean function for afferents in inflamed tissue below and to the left of the mean function for
normal tissue also suggested sensitization to velocity of applied forces.

Figure 3-5. Dynamic reactivity in previously inflamed tissue. Power functions best
described the relationship between instantaneous dynamic force and force
velocity with instantaneous response interval in the vertical or horizontal
plane. A) Six of 7 units transduced dynamic force (mean slope = -1.1
0.5; range = 7.6 10.2 to 33.3 32.1 N; mean R2 = 0.24 0.16). B)
Six of 7 units transduced force velocity (mean slope = -0.7 0.8; range =
4.8 4.5 to 40.2 22.2 N/s; mean R2 = 0.33 0.28).

33
REACTIVITY IN PREVIOUSLY INFLAMED TISSUE:
DYNAMIC FORCE
-1.5 0.0 1.5 3.0 4.5 6.0
Ln FORCE (Newtons)
-T- T7 E1 J1 E3 -4- T1 + 02
REACTIVITY IN PREVIOUSLY INFLAMED TISSUE;
FORCE VELOCITY
-1 0 1 2 3 4 5 6
Ln Velocity (Newtons/sec)
- + B2 -A- T7 -O E1 + J1 -a- E3 T1

Figure 3-6. Averaged dynamic response functions of nociceptors fitted in normal and
previously inflamed tissue (PI). A) Mean function for dynamic force
fitted in PI tissue (mean interval = 29.9 7.9 msec) falls below the mean
dynamic force function fitted in normal tissue (mean interval = 44.7
16.5 msec) suggesting sensitization. B) Mean function for force velocity
in PI tissue (mean interval = 22.2 3.3 msec; mean activation threshold =
17.3 18.9 N/s) falls below and to the left of mean force velocity
function fitted in normal tissue (mean interval = 7.4 + 4.8 msec; mean
activation threshold = 4.8 + 4.5 N/s) suggesting enhanced reactivity
(sensitization)

35
A CHANGES IN REACTIVITY TO DYNAMIC FORCE
FOLLOWING CARRAGEENAN INFLAMMATION
0 1 2 3 4 5
Ln Force (Newtons)
N (n=25) INF (n=6)
B CHANGES IN REACTIVITY TO FORCE VELOCITY
FOLLOWING CARRAGEENAN INFLAMMATION
0 12 3 4 5
Ln Velocity (Newtons/sec)
n (n= 16) INF (n=6)

36
Statistical comparisons between function characteristics in normal and inflamed
tissues confirmed that dynamic reactivity improved in inflamed tissues (See Table 3-3).
This was manifested as changes in activation threshold, frequency asymptotes and function
intercepts. The mean activation threshold (8.3 13.2 N) for units in inflamed tissue (n =
4) that responded best to jaw opening and transduced dynamic force was significantly
lowered relative to the mean activation threshold (24.1 + 11.2 N) for VP units (n = 10) in
normal tissue (F = 5.36, df = 13, p < 0.04). For those same units, the mean intercept in
inflamed tissue (5.0 + 3.0) was significantly decreased relative to the mean intercept in
normal tissue (9.0 3.1). Similar changes were observed for afferents that transduced
force velocity. The mean frequency asymptote (37.5 + 23.6 N/s) for these units was
significantly less than the mean frequency asymptote (148.0 79.6 N/s) for units (n = 8),
in normal tissue (F = 8.89, df = 12, p < 0.01). The mean force-frequency asymptote (40.2
+ 22.2 N/s) for PI units (n = 6) that coded for force velocity in both VP and HP jaw
movements were significantly less than the mean force-frequency asymptote (156.5 83.1
N/s) for VP and HP units (n = 15) in normal tissue (F = 9.57, df = 21, p < 0.01).
The changes we have observed in dynamic reactivity of TMJ nociceptors are
suggestive of sensitization. However, experiments of this type (PI tissue) are subject to
sampling errors. The best form of evidence for nociceptor sensitization comes from
observations of single affferents making transitions from the normal to the sensitized state,
following acute injections of pro-inflammatory substances.
Experiment II: Properties of Units in the
Acutely Inflamed TMJ
The findings of enhanced dynamic reactivity observed in populations of afferents
sampled from normal and subacutely inflamed TMJ tissues were complemented by
observations made on units in which testing was performed before and after carrageenan-

TABLE 3-3. Mean values of properties of TMJ nociceptors.
A. NORMAL TISSUE
Test
n
Slope
Intercept
Act.
Thres.
Freq.
Asym.
Freg.
Thres.
2
R
MRI
DF
23
-1.2 + 0.9
7.3 3.1
15.9 11.3
47.0 31.5
0.42 0.22
3.71.4
FV
15
-0.4 + 0.3
4.8 1.4
17.3 18.9
156.5 83.0
0.30 0.18
3.11.1
M
5
-4.2 + 2.4
14.0 6.7
10.8 3.6
16.0 7.5
0.49 0.23
9.94.8
SF
8
-1.6 + 1.5
5.9 2.4
17.7 18.3
42.5 26.5
7.9 + 7.9
0.75 0.23
3.6 1.5
P
1
-5.8
17
10
16
10
0.73
6.6
B. PREVIOUSLY INFLAMED TISSUE
Test
n
Slope
Intercept
Act.
Thres.
Freq.
Asym.
Freg.
Thres.
2
R
MRI
DF
6
-1.1 +0.5
5.42.4
7.6 10.2
33.3 32-1
0.24 0.16
3.50.9
FV
6
-0.7 +0.8
3.50.8
4.8 4.5
40.2 22-2

0.33 0.78
2.2 1.3
M
1
-6.6
24
17
20

0.46
17
SF
2
-1.3 +0.9
7.92.3
6.5 3.6
25.5 9-2
6.1 + 4.3
0.36 0.11
4.1 0.6
P
1
-2.0
10.0
10
17
7
0.42
6.1
C. A or
fELY INFLAMED 1
"ISSUE
Test
Cond
n
Slope
Intercept
Act.
Thres.
Freq.
Asym.
Freg.
Thres.
2
R
MRI
DF
Pre
9
-1.3 +1.4
7.4
4.1
12.9 + 9.0
41.4 +
13.3
0.43 0.23
4.3 +
2.1
DF
Post
9
-0.9 +0.6
5.5
1.4
11.4 +13.5
41.3
24.9
0.38 0.20
3.2 +
0.5
FV
Pre
2
-0.2 +0.06
4.4
0.5'
14.0 + 18.4
252.0 114.6
#
0.39 0.07
3.0 +
0.1
FV
Post
2
-0.7 +0.7
5.6
3.3
9.0 + 5.7
167.0 +
16.9
0.48 0.30
3.0 +
0.1
M
Pre
3
-3.3 +3.3
13.8
9.9
15.7 + 6.8
26.3 +
2.5
#
0.40 0.08
7.8 +
5.4
M
Post
3
-4.0 +3.4
15.8
10.7
19.3 + 7.2
24.5 +
4.1
0.58 0.36
11.1 +
9.5
SF
Pre
3
-1.0 +0.6
7.4
2.0
20.3 + 14.0
33.0 +
13.9
8.2+ 3.7
0.54 0.34
5.5 +
2.1
SF
Post
3
-0.8 +0.6
6.4
2.2
8.5 + 8.4
43.3 +
11.7
5.2+ 3.7
0.58 0.15
4.5 +
0.7
P
Pre
1
-1.1
7.1
10.5
16
10
0.35
5.2
P
Post
1
-1.2
6.8
3.4
22
2.7
0.79
3.3

Note: DF, dynamic force; FV, force velocity; M, movement; SF, static force; P, position; ^ct. Thres., activation
threshold; Freq. Asym., frequency asymptote; Freq. Thres., frequency threshold; R coefficient of
determination; MRI, mean response interval (natural log value).

39
induced inflammation (acutely inflamed or AI). Outcomes of experiments using PI
methods suggested that individually characterized afferents would manifiest improved
dynamic reactivity.
Observations of quantitative shifts in force interval functions were confirmed, and
additional qualitative changes were observed. Eleven units were characterized in normal
tissue and then retested 1-3 h after exposure to carrageenan. Four units responded
preferentially to VP jaw movement and 7 responded best to HP movement. For 9 units that
transduced stimulus intensity in both normal and inflamed tissue, 6 demonstrated enhanced
reactivity for dynamic force (Figure 3-7). Four of these 6 units had post-inflammatory
functions that shifted below the pre-inflammatory function. One of these also showed
leftward shift. Three of 6 units that demonstrated enhanced dynamic force reactivity
showed a leftward function shift relative to pre-inflammatory functions but failed to shift
below the control case. Mean function characteristics for these nociceptors are presented in
Table 3-3.
Experiments were performed to determine whether changes in AI reactivity
occurred as a result of carrageenan or other causes, such as repeated stimulation. In these
control experiments, saline (100 |il) was injected into the area of the RF and into the TMJ
capsule. Reactivity was examined in 8 units after exposure to saline. Five of 8 units
transduced dynamic force in both the pre- and post-saline conditions. While quantitative
changes in reactivity were small following saline injections, there was some indication that
repeated testing could produce qualitative changes in reactivity similar to those observed
following carrageenan injection (See Figure 3-8).
Following saline injection, mean activation threshold was reduced from 14.1 +
15.0 N in pre-saline condition to 11.5 7.5 N These changes were relatively small
compared to changes observed following carrageenan (11.2 + 9.9 to 5.1 + 3.7 N).
Statistical comparisons indicated that the mean changes in activation threshold was
significantly less in saline than carrageenan treated cases (T = -2.2; DF = 15; p = 0.04)).

Figure 3-7. Demonstration of sensitization (enhanced reactivity). Six of 11 units
were characterized in normal tissue and then tested again after acutely
inflamed (AI) with carrageenan. Power functions generated from
retesting in acutely inflamed tissue were positioned below and/or to the
left of power functions fitted on normal tissue. N, normal, Min,
inflamed; HR, inflamed.

A
D
REACTIVITY IN VERTICAL PLANE: NORMAL TO INFLAMED REACTIVITY IN HORIZONTAL PLANE: NORMAL TO INFLAMED
DYNAMIC FORCE: UNIT #1 DYNAMIC FORCE: UNIT #2
Ln Foro* fr'towior*)
Ln Fore* t^*wton*)
N 1 KR 3 l-R
1 FR 2 FR
B
E
REACTIVITY IN VERTICAL PLANE: NORMAL TO INFLAMED REACTIVITY IN HORIZONTAL PLANE: NORMAL TO INFLAMED
DYNAMIC FORCE: UNIT #3 DYNAMIC FORCE: UNIT #5
Ln Fore* Ln Fore* 1 HR
2-5 HR
c
F
REACTIVITY IN VERTICAL PLANE: NORMAL TO INFLAMED REACTIVITY IN HORIZONTAL PLANE: NORMAL TO INFLAMED
DYNAMIC FORCE: UNIT #4 DYNAMIC FORCE: UNIT #6
Ln Fore* f'tewtora)
Ln Fore* f'fewtont)
T- N
- 90
2 FR
V- N
- 1 FR

Figure 3-8. Reactivity of nociceptors exposed to saline. Five units transduced
dynamic force in both the pre- and post-saline conditions. A) and B)
demonstrate quantative changes in dynamic force reactivity. C), D) and
E) show no enhanced reactivity.

43
A B
REACTIVITY IN HORIZONTAL PLANE: SALINE CONTROL REACTIVITY IN HORIZONTAL PLANE: SALINE CONTROL
DYNAMIC FORCE: LEFT LATERAL UNIT #3 DYNAMIC FORCE: LEFT LATERAL UNIT #6
Ln Foro* t'tewton*J
Ln Fore* r*wlon*J
S1H
C D
REACTIVITY IN HORIZONTAL PLANE: SALINE CONROL REACTIVITY IN HORIZONTAL PLANE: SALINE CONTROL
DYNAMIC FORCE: LEFT LATERAL UNIT #2 DYNAMIC FORCE: LEFT LATERAL UNIT #7
E
REACTIVITY IN HORIZONTAL PLANE: SALINE CONTROL
DYNAMIC FORCE: RIGHT LATERAL UNIT #1
0 1 2 3 4 5
Ln Foro O't*wton*>
n
- S1h#3
- S2K3

44
Therefore while shifts in activation threshold could occur following repeated testing, the
changes that followed carrageenan injection were significantly greater.
In experiment I, it was determined that most TMJ nociceptors transduced dynamic
force and velocity, but few transduced either static force, movement or position.
Following acute exposure to carrageenan, qualitative changes in coding capacities were
noted; that is, afferents coded for stimulus features not previously transduced.
Qualitative improvements were observed for most units for either dynamically or
statically applied stimuli. Eight of 11 nociceptors acquired either dynamic or static coding
ability (Table 3-4). Four of 4 units that preferred VP jaw movement and transduced
dynamic force in normal tissue acquired the ability to transduce force velocity (n = 2), static
force (n = 1) or jaw position (n = 1) in inflamed tissue. Two of 5 AI units that preferred
HP movement and transduced dynamic force in normal tissue also acquired the ability to
transduce static force. Acquired coding also appeared in nociceptors that were without
transducing capacity in normal tissue. Two of 7 AI units that preferred HP movement
acquired the capacity to transduce both dynamic and static force. Other changes appeared
as de novo reactivity. Three of 7 units that had only HP jaw movement initially acquired
similar reactivity for VP movement (dynamic force). Six units demonstrated spontaneous
activity after stimulus testing.
The finding that a large proportion (8/11) of nociceptors acquired coding ability
after exposure of carrageenan suggested a qualitative form of sensitization. The nature of
these qualitative changes can be best appreciated by comparing scatter plots representing
comparisons between pre-inflamed and post-inflamed reactivity. Two types of trends (shift
and rotation) were observed. Shift indicates a movement of a scatter of points into graphic
zones of greater sensitivity. Rotation indicates the development of a significant slope
associated with the scatter field of points. Of the 9 of 11 nociceptors that acquired coding
ability, all 9 showed shifts and/or rotation. Figure 3-9 illustrates significant functions of
units that demonstrated shifts and units that demonstrated rotation of scatter point fields.

45
Table 3-4.
EFFECT OF CARRAGEENAN ON TRANSDUCING CAPACITY
Qualitative improvements in reactivity for nociceptors that were
characterized in normal tissue and then tested again subsequent to
carrageenan injection. Eight of 11 nociceptors acquired either dynamic or
static coding ability. Coding ability was also acquired for nociceptors (n =
2) that had no transducing capacity in normal tissue. Three units that
responded to horizontal plane movement acquired vertical plane reactivity in
acutely inflamed tissue. Six units demonstrated spontaneous activity after
stimulus testing in acutely inflamed tissue.
UNIT
PLANE
PRE-INFLAMED
POST-INFLAMED
CODING
SHIFT
OTHER
MOVEMENT
POST-TEST
SPONTAN.
ACTIVITY
1
VP
DYNAMIC FORCE
MOVEMENT
STATIC FORCE
POSITION
DYNAMIC FORCE
FORCE VELOCITY
MOVEMENT
STATIC FORCE
POSITION
YES

YES
2
VP
DYNAMIC FORCE
DYNAMIC FORCE
STATIC FORCE
YES

YES
3
VP
DYNAMIC FORCE
STATIC FORCE
DYNAMIC FORCE
FORCE VELOCITY
STATIC FORCE
YES

NObE
4
VP
DYNAMIC FORCE
FORCE VELOCITY
MOVEMENT
DYNAMIC FORCE
MOVEMENT
POSITION
YES

LONE
Note: VP, vertical plane

46
Table 3-4 (cont'd).
UNIT
PLANE
PRE-INFLAMED
POST-INFLAMED
CODING
SHIFT
OTHER
MOVEMENT
POST-TEST
SPONTAN.
ACTIVITY
5
HP
DYNAMIC FORCE
YES
FORCE VELOCITY
YES
YES
STATIC FORCE
YES
6
HP
DYNAMIC FORCE
DYNAMIC FORCE
FORCE VELOCITY
FORCE VELOCITY
STATIC FORCE
YES

YES
7
HP
DYNAMIC FORCE
DYNAMIC FORCE
OPEN: CODE
NO\E
FORCE VELOCITY
FORCE VELOCITY
OPEN: CODE
STATIC FORCE
YES
OPEN: NON-CODE
8
HP
DYNAMIC FORCE
DYNAMIC FORCE
YES
FORCE VELOCITY
FORCE VELOCITY


STATIC FORCE
STATIC FORCE
9
HP
DYNAMIC FORCE
DYNAMIC FORCE

OPEN: CODE
YES
1 0
HP
DYNAMIC FORCE
DYNAMIC FORCE
STATIC FORCE
STATIC FORCE


NOME
1 1
HP
DYNAMIC FORCE
YES
OPEN: NON-CODE

FORCE VELOCITY
YES
OPEN: NON-CODE
STATIC FORCE
YES
OPEN: NON-CODE
NONE
Note: HP, horizontal plane

Figure 3-9. Comparison between pre-inflamed and post-inflamed reactivity in scatter plot forms. Two types of trends are
displayed (rotation and shift). A,B,C and D) Units manifesting both rotation and shift to the left of scatter field.
E,F,G.and H) Units manifesting rotation. Functions fit to scatter plots indicate significant transduction capacity was
acquired. N, normal or pre-inflamed case; HR, hours afer carrageenan injection; M, minutes after carrageenan
injection.

A
REACTIVITY IN VERTICAL PLANE: NORMAL TO INFLAMED
FORCE VELOCITY: UNIT #1
0 1 2 3 4 5 6
Ln Velocity (Newtons/sec)
o n 2m* 2 m-+- 3m* 3 m
B
REACTIVITY IN VERTICAL PLANE: NORMAL TO INFLAMED
FORCE VELOCITY: UNIT #3
Ln Velocity (Newtons/sec)
O N 1 HR 1 HR
C
REACTIVITY IN HORIZONTAL PLANE: NORMAL TO INFLAMED
STATIC FORCE: UNIT #2
0 1 2 3 4 5 6
Ln Force (Newtons)
O N 2 m 2 m
D
REACTIVITY IN HORIZONTAL PLANE; NORMAL TO INFLAMED
STATIC FORCE: UNIT #7
Ln Force (Newtons)
O n
1 l-R
1 HR

E
REACTIVITY IN VERTICAL PLANE: NORMAL TO INFLAMED
STATIC FORCE: UNIT #2
Ln Velocity (Newtons/sec)
O N 1 hfl 1 HR
F
REACTIVITY IN HORIZONTAL PLANE: SALINE CONTROL
FORCE VELOCITY:LEFT LATERAL UNIT #2
0 1 2 3 4 5 6
Ln Velocity (Newtons/sec)
O N 1 HR 1 HR
Figure 3-9. (cont'd)
G
REACTIVITY IN HORIZONTAL PLANE: NORMAL TO INFLAMED
STATIC FORCE: UNIT #1
Ln Force (Newtons)
O N 1 HR 1 HR
-P.
VO
6
5
4
3
2
1
0
0 1 2 3 4 5 6
Ln Force (Newtons)
O N 30 M 30 M-t-- 1 HR + 1 HR
H
REACTIVITY IN HORIZONTAL PLANE: NORMAL TO INFLAMED
STATIC FORCE: UNIT #3

50
Of the 9 units exhibiting rotation, 4 also shifted. It was possible that shift was a more
mature form of sensitization that followed rotation. In units which were examined over
several hours, 2 of 2 units that exhibited rotations subsequently manifested shifts of their
scatter plot field (See Figure 3-9).
Control tests indicted that qualitative changes could also be observed after saline
injection. In 1 of 8 cases, a qualitative improvement was observed in dynamic coding
capacity (Table 3-5). Thus, improved dynamic reactivity is possible as the result of saline
injection. However, the tendency towards acquired coding appeared to be greater for
carrageenan-induced inflammation (8 of 11 cases).
In summary, experiments were performed to characterize the response properties of
presumed nociceptors in normal and inflamed capsular tissue of the TMJ. Most TMJ
afferents preferred either movement in the horizontal or vertical plane. Their reactivity
functions were best described by power functions fit between dynamic force, force velocity
and response interval. In normal tissue, TMJ afferents had properties of nociceptors, in
that the activation threshold was at the extreme range of jaw movement, either in the
exponential portion or in the transition zone between the linear and exponential force-
movement curves that described jaw movement. It was predicted that TMJ nociceptors
would sensitize following exposure to carrageenan. To test this, populations of afferents
were sampled in previouslyly inflamed tissue and their responses compared to those of
afferent populations in normal tissue. Improved reactivity was observed, especially
reactivity to dynamic stimuli (dynamic force and force velocity). To avoid sampling errors
that could have biased these observations, units were characterized in acutely inflamed
tissue after being characterized in normal tissue. These afferents manifested similar
quantitative improvements in dynamic reactivity. Additionally, qualitative improvements of
coding capacity were observed. Acquisition of coding capacity following acute
inflammation suggested afferent sensitization.

51
TABLE 3-5
EFFECT OF SALINE ON TRANSDUCING CAPACITY
UNIT
PLANE
PRE-CODING
POST-CODING
CODINC
SHIFT
OTHER
MOVEMENT
POST-TEST
SPONTAN.
ACTIVITY
1
HP
DYNAMIC FORCE
FORCE VELOCITY
STATIC FORCE
DYNAMIC FORCE
FORCE VELOCITY
STATIC FORCE


NONE
2
HP
DYNAMIC FORCE
STATIC FORCE
DYNAMIC FORCE
FORCE VELOCITY
STATIC FORCE
YES

NONE
3
HP
DYNAMIC FORCE
STATIC FORCE
DYNAMIC FORCE
STATIC FORCE


NONE
4
HP
DYNAMIC FORCE
FORCE VELOCITY
MOVEMENT
STATIC FORCE
POSITION



NONE
5
HP
NON-CODING
NON-CODING


NONE
6
HP
DYNAMIC FORCE
DYNAMIC FORCE


NONE
7
HP
DYNAMIC FORCE
STATIC FORCE
DYNAMIC FORCE
STATIC FORCE


NOME
8
HP
STATIC FORCE
STATIC FORCE


NONE
Note: Changes in reactivity for 8 units after exposure to saline. One of 8 units acquired coding ability
for force velocity. HP, horizontal plane.

CHAPTER 4
DISCUSSION
Afferents were isolated from the trigeminal ganglion and efforts were made to
determine whether they had nociceptive properties. Tests included quantification of
response range, identification of relevant stimulus variables and the tendency to sensitize.
Afferents that are nociceptors should transduce noxious stimuli (Sherrington, 1947), while
other joint afferents (proprioceptors) would be expected to be most reactive in the normal
range of motion, be bidirectionality sensitive, and exhibit spontaneous activity (Burke et
al., 1988; Macefield et al., 1990, Dom et al., 1991).
The relationship between applied force and mandibular movement was examined to
determine the "noxious range" and compare it with the threshold of afferents. The noxious
range is likely to correspond to that portion of the force/jaw movement relationship where
forces increased exponentially with jaw movement. TMJ afferents were activated at or near
the beginning of the exponential phase and their firing became asymptotic in the exponential
phase. Thus, a preference for high forces (mean activation threshold = 20.6 11.0N) at
extremes of the mandibular range of motion (mean activation threshold = 13.7 5.4; mean
frequency asymptote = 49.6 + 20.7 N) suggested that these TMJ afferents were
nociceptors.
In contrast, a small group of units (n = 3) had responses to both jaw opening and
closing. Their properties are distinct from populations of afferents which may be important
in signalling tissue damage. Their activation thresholds (1.1 0.9 N) and range of
reactivity (1.1 0.9 to 10.4 4.1 N) are considerably different from that of nociceptors
described above, and respond chiefly to innocuous joint movement within the physiological
52

53
range of motion. Afferents with similar properties have been observed in the cat knee joint
(Dom, et al., 1991). In this study, large diameter afferents (Group II) responded
exclusively in the normal range of motion, were directionally sensitive, and demonstrated
no resting activity. Whereas activity in nociceptors is likely to contribute to joint pain,
these low threshold afferents may contribute to proprioception or sensations of pressure
(Burke et al., 1988; Macefield et al., 1990; see Appendix B).
In other laboratories, recordings have been made from group III and IV joint
afferents innervating the cat knee (Burgess and Clark, 1969; Clark, 1975; Schaible and
Schmidt, 1983b). Schaible and Schmidt (1983b) divided their joint afferents into 4
subgroups which were differentiated, in part, by their qualitative response to movement.
They defined nociceptors as those afferents that responded through, beyond or exclusively
beyond the normal range of joint motion. These afferents had a steep rise in discharge
frequency during forceful rotational movements, similar to those described previously
(Burgess and Clark, 1969; Coggeshall et al., 1983). These observations compare
favorably with ours, in that intense mechanical stimulation is needed to achieve a maximum
response. It is difficult to make detailed comparisons between the response properties of
afferents described by Schaible and Schmidt and others with those in our experiments, as
no attempt was made by them to quantify the properties of afferents other than local
pressure thresholds. Our experiments represent the first quantification of nociceptor
reactivity across a range of suprathreshold stimuli with verification of the relationship
between movement, response minima and maxima.
Early experiments created some confusion as to the basic properties of joint
afferents. Studies that have examined the activity of mechanoreceptors supplying cat joint
tissues (Burgess and Clark, 1969; Clark and Burgess, 1975; Rossi and Grigg, 1982)
primarily emphasized proprioception, and addressed the questions as to whether position
sense is coded by joint or muscle afferent fibers. They determined that joint afferents are
only responsive at the extremes of the movement range, seemingly ruling out any useful

54
role in proprioception and clouding the functional distinction between free nerve endings
(nociceptors) and well recognized encapsulated Golgi and Ruffini type end organs which
are found throughout the capsule (Thilander, 1961; Ishibashi, 1966). Yet, others have
reported that many afferents respond within the normal range movement (Klineberg et al.,
1971; Lund and Matthews, 1981; Schaible and Schmidt, 1983b; Dorn et al., 1991).
Microneurographic studies appear to have resolved this confusion in favor of the findings
of Schmidt and company. These studies have examined the behavior of neuronal
populations that signal joint position and mechanosensibility in humans. Burke et al.,
(1988) recorded responses of joint, muscle and cutaneous mechanoreceptors associated
with finger joints to position and movement. Whereas most responded at the limits of joint
rotation, a few afferents responded within the normal range. It is unclear whether the
former group could code for pain, as pain was never induced by the movements, but the
latter group appears to be appropriate for proprioceptive function. The relatively small
population (3 of 16 cases) that provided a proprioceptive code was not dissimilar to our
own (3 of 36 cases). Microstimulation of similar groups of joint afferents innervating
finger joints indicated that innocuous sensations of movement or deep pressure were
evoked (Macefield, et al., 1990). Thus, a proprioceptive role for joint afferents seems to
be confirmed, although they may represent a small portion of the afferent population.
Sensitization of TMJ Nociceptors
Nociceptors in all preparations will sensitize following exposure to extreme heat
(Burgess and Perl, 1967; Beck et al., 1974; Fitzgerald and Lynn, 1977; Campbell et al.,
1979), mechanical forces (Reeh et al., 1987) or proinflammatory substances (Schaible and
Schmidt, 1988a; Berberich et al., 1988; Cooper et al., 1991), and these are reflected as
changes in central reactivity (Neugebauer and Schaible, 1990; see Appendix D). Sensitized
nociceptors in skin, muscles and joints have enhanced reactivity to thermal, mechanical

55
and/or chemical stimuli. In our experiments, where afferents were sampled from
previously inflamed capsular tissue or where characterized afferents were retested in acutely
inflamed tissue, a variety of forms of sensitization was found. These changes included a
significant decrease in mean activation threshold, shifts in stimulus response functions and
qualitative forms of sensitization. Additional changes were observed for afferents in the PI
condition (frequency asymptote and intercept) that were not replicated in the AI condition.
Recent experiments on cat knee joint nociceptors (Schaible and Schmidt, 1988b)
have also produced evidence of changes in reactivity following carrageenan injection. Over
half of the units that were classified as nociceptors in normal tissue responded to innocuous
joint movements in the normal range of motion after inflammation. In effect, such
enhanced reactivity, from extremes of movement to the normal range of motion indicates a
decreased activation threshold. In our experiments, decreases in activation threshold were
observed following carrageenean-induced inflammation. These decreased activation
thresholds fell within the linear phase of force-movement relationship.
In our study, qualitative forms of sensitization were also observed. These appeared
both in carrageenan treated nociceptors (8 of 11 cases), and infrequently in saline treated
controls (1/8). The nature of these qualitative changes can be best appreciated by
comparing scatter plots representing comparisons between preinflamed and postinflamed
reactivity. It is important to examine scatter plots because the acquisition of transducing
ability could have represented a distorted outcome. For example, outliers could have
rendered functions insignificant where they were otherwise significant. However,
examination of plots following carrageenan showed new relationships between force and
response interval and shifts to greater reactivity.
Two types of trends were observed: rotation and shift. Rotational trends were
indicated by a change in slopes which suggested increased proportional reactivity. A shift
to the left represented a decrease in activation threshold that was seen consistently in AI and
PI conditions for units with extant coding capacity. The shifts that were observed, were

56
less likely to be related to the development of qualitative changes than rotation. Rotation
represents a new functional reactivity in the form of a proportional response to imposed
forces. The basis of the qualitative changes could be either receptor based metabolic
alteration secondary to the generation of proinflammatory substances, or could result from
improved mechanical coupling between the receptor and the applied force.
Edema is a major component of inflammation that may impact on mechanical
coupling. Afferent terminals of small fibers that are located in the area of inflammation are
subject to an altered physical environment as a consequence of fluid extravasation. What
effect local changes from edema may have in the responsiveness of joint receptors is
unclear. In other preparations, edema may act to enhance or deter afferent responsiveness,
the direction of the effect being dependent on tissue properties that are peculiar to each site
(Cooper et al, 1990).
Acquisition of transducing capacity could be similar to observations of recruited
activity described by other laboratories. This "recruitment" of afferents was observed in
the cat knee joint preparation (Schaible and Schmidt, 1985, 1988b) and also in cutaneous
preparations (Handwerker et al., 1991). A distinction between our observations and those
of Schaible and Schmidt is that our sensitized afferents all have some pre-existing
reactivity. We did not observe recruitment as silent units which "wake up." Given this,
recruited activity and acquired coding may be distinct forms of sensitization. Our failure to
observe recruitment may be due to methodological constraints of our preparation. In our
experiments, extracellular recordings of neural activity in the trigeminal ganglion limits the
number of neurons that could be recorded at any site. Very few cell bodies are in the
functional range of the microelectrode. On the other hand, in teased fiber preparations such
as those used by Schaible, Schmidt and Handwerker, electrodes have essentially zero
impedance, therefore many more afferents can be recorded from simultaneously. This
makes it more likely for recruitment to be observed.

57
Factors Contributing to Sensitization
Mechanical sensitization of joint afferents, following inflammation, is likely to be
due to the production and release of endogenous substances. Injection of carrageenan
produces a rapid inflammation that has been characterized in a number of behavioral and
physiological preparations (Vinegar et al., 1987). Various factors may contribute to
sensitization of joint afferents during carrageenan-induced inflammation, including both
edema and the formation and release of algesics.
Changes in the response properties of joint afferents during inflammation have been
attributed to the actions of bradykinin, prostaglandins, and serotonin. These mediators
may alter mechanical responsivity of afferents, modify chemical responsivity, activate
afferents or a combination of the three. Changes in reactivity of small fibers in inflamed
tissue to bradykinin have been observed (Kanaka et al., 1985; He et al., 1990; Grubb et
al., 1991). Bradykinin activates most group III and IV units that responded to passive joint
movement. Bradykinin also activates afferents otherwise classified as "silent" (Heppleman
et al., 1987).
Joint afferents can also be activated by prostaglandin (E or I). Prostaglandins Ei or
E2 activated small afferents which responded to passive joint movement (Heppleman et al.,
1985; Schaible and Schmidt, 1988a), and modified mechanical responses of these
afferents. Following exposure to PGE2, most group III and some group IV units showed
enhanced joint movement reactivity and responded within the normal range of motion.
These PGE2-evoked increases in unit responsiveness paralleled those observed during
acute arthritis (Schaible and Schmidt, 1985, 1988a). Similar properties have been
prescribed for PGI2, and it has been suggested that PGI2 may be the dominant PG in joint
afferent sensitization ( Birrell et al., 1991; McQueen et al., 1991).
Interactions between pro-inflammatory mediators are also likely to be important, but
they have not been determined in much detail. Prostaglandin Ej (Schaible, 1983) and

58
prostaglandin E2 (Grubb et al., 1991) have been shown to sensitize joint nociceptors to
bradykinin. This may impact both on movement sensitive and tonic forms of joint pain.
Serotonin is also important in nociceptor sensitization. The effect of 5-HT on
response characteristics of small afferent fibers have been studied in normal and inflamed
cat knee joints (Heppelman et al., 1987) and rat ankle joints (Birrell et al., 1990; Grubb et
al., 1988). Most group III and IV fibers that showed reactivity to cat knee movement were
also activated by 5-HT. Units recorded from normal rat ankle joints were excited by 5-HT
and showed enhanced activity in arthritic joints.
The consequences of carrageenan injections are very complex, and have not been
determined for joints specifically (Vinegar et al., 1987). One sequence of events that
occurs in skin, during the initial stage of inflammation (0-60 min) suggests a divergence
from mechanisms proposed for sensitization of joint afferents. Immediately after injection
of carrageenan, small amounts are absorbed by mast cells. The cytotoxic action of
carrageenan initiates the arachidonate metabolic cascade and mast cell degranulation.
Endoperoxides and serotonin are released. The endoperoxides are not believed to be
prostaglandins but are believed to be reactive intermediates, and bradykinin is not believed
to play a role. This stands in contrast to studies directly implicating bradykinin, PGE's and
PGI2 in afferent sensitization and at the very least implicates that additional factors may
play a role in carrageenan inflammation. The role of 5-HT in carrageenan induced arthritis
is also unclear. While 5-HT is released by carrageenan in rats, it is unlikely to be directly
released in other species due to the absence of 5-HT in mast cells. Serotonin may be more
important when vascular damage occurs (Zeller et al, 1983; Garcia-Leme, 1989). This
may, in fact, be more relevant to TMJ dysfunction.
Clearly, reactivity to a host of algesics is shared by most small diameter afferents
innervating joint tissue. Bradykinin, prostaglandins and perhaps 5-HT may play a role in
afferent sensitization in inflamed joints. However, in each instance, it is not clear what is
meant by normal range of motion and it is not clear to what extent shifts produced by

59
bradykinin, PGE2 or serotonin are the basis for changes produced with carrageenan or
other proinflammatory substances. The lack of detail in this respect is partly due to the
absence of quantification of stimulus and response variables. Quantification of neural
activity in respect to threshold, range and salient stimulus features (static or dynamic
reactivity) should permit a fuller evaluation of role played by these substances and others in
modification of joint nociceptor reactivity.

APPENDIX A
DEVELOPMENT AND MAINTENANCE OF TMJ PAIN
Many theories have been advanced to account for the production of TMJ pains.
(For reviews, see Deboever, 1973; Dubner et al., 1978, Yemm, 1979). TMJ dysfunction
may account not only for pain in the joint itself, but also for pain arising from associated
facial structures.
Intra-articular Origins of TMJ Pain
1) Pressure Theory
Pressure theories have been the most prevalent explanations for the production of
TMJ pain. These theories suggest that disruption of the normal articular mechanics may
impose abnormal pressures on structures of the TMJ. Costen (1934) postulated that facial
pain associated with the TMJ was a consequence of pressure on the auriculotemporal nerve
brought about by impaction of the condyle against the tympanic plate. Anatomically, this
theory is untenable since the auriculotemporal nerve ramifies before reaching the TMJ. The
articular branches of the auriculotemporal nerve arise at the medialposterior aspect of the
neck of the condyle and ascend into the soft tissue of the joint inferior to the tympanic plate.
The auriculotemporal nerve is vulnerable to pressure at its proximal course. The
auriculotemporal nerve arises from the posterior trunk of the mandibular nerve along the
medial surface of the lower belly of the lateral pterygoid muscle. Entrapment of the
auriculotemporal nerve in the lateral pterygoid muscle has been demonstrated in 5% of
60

61
cadaver specimens (Loughner et al., 1990). Pressure in the form of compression by a
hyperactive lateral pterygoid muscle may produce pain and/or paresthesia. Furthermore,
patients with an internal derangement of the TMJ often have accompanying spasticity of the
lateral pterygoid muscle.
Pressure on the posterior attachment tissues by the condyle could also cause TMJ
pain (Sicher, 1955). Posterior displacement of the condyle or spastic contracture of the
superior belly of the lateral pterygoid muscle may result in anterior displacement of the
disc. As a consequence, the posterior attachment tissues are positioned where forces
generated during mastication may produce local pressure on these highly vascularized and
innervated tissues.
Local joint pressure may activate mechanoreceptive nociceptors in connective tissue
such as the posterior attachment tissues. Inflammation could result from trauma due to a
sudden, intense impact or from repeated pressure. Endogenous algesics released in the
zone of inflammation may sensitize joint nociceptors by decreasing threshold and
increasing response to mechanical stimuli (Heppelman et al., 1985).
A common procedure thought to discern anterior displacement of the disc is the
impact-loading test. Manual loading applied in an anterior-superior direction at the
posterior portion of the body of the mandible impacts the condyle into the articular fossa.
If pain is evoked, it is thought that the disc is displaced and the condyle is impacting onto
the posterior attachment tissues. However, disc displacement may exist without impact
loading pain. This is assessed by imaging techniques, such as arthrography or magnetic
resonsance imaging. Therefore, direct pressure on the disc or posterior attachment tissues
is not sufficient to explain TMJ pain in all cases.
A corollary notion related to Sichers theory was advanced by Frost (1968) to
explain some patterns of joint pain. Frost hypothesized that bone pain may be evoked by
the pressure of two articulating, irregular, joint surfaces in the absence of an intact
interposing disc. Presumably, the irregular bony surfaces represent osteoarthritic changes.

62
Other investigators (Kreutziger and Mahan, 1975) have included arthroses of bony
structures as causative factors in TMJ pain. Besides the degenerative processes that may
occur in the bony anatomy of the TMJ, degenerative changes of the villi of the synovium
have been claimed to be causally related to TMJ pain (Olson, 1969). Supposedly,
disruption of the secretory function of the villi can disturb proper nutrition and lubrication
of the TMJ resulting in TMJ dysfunction.
2) Tension Theory
Tension theories of TMJ pain can be divided into static and dynamic. Static state
involves a resting position of the mandible. Dynamic state involves active or passive jaw
movement. Anteriormedial displacement of the disc may generate static tension on the
posterior and lateral aspects of the capsule (Dubner et al., 1978) where the greatest member
of mechanoreceptors are located (Zimny, 1988). It is possible that resting tension will
produce prolonged discharge in TMJ nociceptors. If the anteriormedial displacement of the
disc is advanced, there is a release of the disc attachment at the lateral pole of the condyle
which untethers the disc from the lateral aspect of the TMJ. In this case, the posterior
attachment tissues are vulnerable to tension from a disc displacement during static
conditions.
Patients suffering from pain in the TMJ often demonstrate symptoms of capsulitis;
this included pain on local palpation or pain during small movements within the normal
range of motion. Inflammatory processes in the TMJ may initiate or potentiate TMJ pain
(Dubner et al., 1978). Dynamic theories propose that pain is produced during jaw
movement by excitation of functionally distinct types of mechanoreceptors in the capsule
and posterior attachment tissues. Activation may be enhanced by capsulitis. Zimmy
(1988) advanced a conceptual model of TMJ pain during jaw movement. As the condyle
rotates and translates freely through intermediate degrees of angle, the capsule and posterior
attachment tissues are deformed. Such deformation is normally insufficient to excite
mechanoreceptors. As the condyle approaches its border movement, the capsule and

63
posterior attachment tissues become taut. Mechanoreceptors in the capsule and posterior
attachment tissues are activated by the resultant tension. Thus, these mechanoreceptors
appear to act as detectors that sense the safe limits of joint movement. Supposedly, jaw
movement beyond safe limits can represent real or potential tissue damaging stimuli. If
these mechanoreceptors are nociceptors, they may be sensitized following capsulitis so that
small movements in the functional range of motion produce pain. Clark and Burgess
(1975) suggested that large, myelinated afferents signal the pressure felt as the extremes of
joint movement are reached. These investigators demonstrated that slowly adapting
receptors in the capsule were excited only at extremes of flexion and extension of the knee
joint of the cat (Burgess and Clark, 1969). On the other hand, Schaible and Schmidt
(1983b) attribute a similar detection role for small fibers which are active only at the
borders of the joint movement.
Following capsulitis, the tension required to produce activation of nociceptors
might be greatly reduced. Animals studies in the cat knee joint (Schaible and Schmidt,
1988b) and rat ankle joint (Guilbaud, 1988) have demonstrated increased responsiveness
of group III and IV afferents to innocuous mechanical stimulation after induction of acute
inflammation The relationship between nociceptor discharge and capsular tension is yet to
be demonstrated.
The reactivity of mechanoreceptors in the capsule of the cat knee have been used to
assess tension produced by joint movement (Grigg and Hoffman, 1989; Hoffman and
Grigg, 1989). The frequency of neurons with receptive fields in the posterior capsule
showed a linear relationship with tension applied (knee extension) at the area of the
receptive field. The posterior joint capsule was minimally loaded even during
hyperextension movements.

64
Extra-articular Theories of TMJ pain
Distinct theories of the origin of extra-articular pain have arisen, and include the
myofascial pain theory and referred pain theory.
1) Myofascial Pain Theory
The myofascial pain theory postulates chronic hyperactivity in head and neck
musculature as a causative agent in extra-articular pain. The myofascial pain theory
suggests that the chronicity of muscle pain is due to the "trigger point" (Travell, 1976).
The trigger point is defined as a localized area of chronic inflammation of fibrous
connective tissue in muscle. Histological examination of biopsy material from trigger
points in patients suffering from interstitial myofibrositis reveal degranulated mast cells and
platelet clots (Awad, 1973). The author proposes a hypothesis suggesting that trauma-
induced extravasation of platelets leads to release of 5-HT which subsequently results in
edema and vasoconstriction. The release of such endogenous algesics in muscle may play
a role in the pain and tenderness associated with trigger points. For example, activation of
group IV afferent neurons in cat muscle have been demonstrated by close arterial injection
of bradykinin, 5-HT or histamine (Mense and Schmidt, 1974). Serotonin may also
sensitize mucosal nociceptors to mechanical stimuli (Friedman et al., 1988; Cooper et al.,
1991).
Muscle pain and the reduction of pain free jaw movement are frequent complaints of
patients with facial pain. The limitation of jaw movement may involve the modulation of
the reflex control of masticatory muscles (Klineberg, 1971; Dubner et al., 1978).
Greenfield and Wyke (1966) studied the role of TMJ afferents in reflexes that modify the
activity of muscles of mastication. The experimental procedure involved detaching all the
supra- and infra-mandibular muscles at their insertions from one half of the cat mandible.
Movement of the ipsilateral half of the mandible resulted in activation or inhibition of

65
dissected muscles. Similar responses were produced in the detatched muscles by direct
tension on the capsule after condylectomy.
Jaw movement has been shown to modulate the firing pattern of alpha motoneurons
in the trigeminal motor nucleus in cats (Kawamura et al., 1967). These investigators
demonstrated changes in the discharge rate of motor neurons of the masseter muscle in
response to passive rotation of the ipsilateral condyle. Rotating the condyle to an open
position evoked an increase in firing pattern of masseter motoneurons. A closed position
evoked a decrease in firing pattern.
Abe and Kawamura (1973) recorded efferent discharges from branches of the
mandibular nerve which innervate the masseter and digastric muscles. Ipsilateral condylar
rotation to an open position inhibited alpha-motor units in the masseteric nerve. Local
mechanical stimulation of the posterior part of the TMJ capsule inhibited the discharge
pattern of masseteric neurons and facilitated motor fibers innervating the digastric muscle.
It is not surprising that afferent activity from mechanoreceptors in the TMJ modulate
efferent activity in masticatory muscles in order to coordinate jaw movement. The presence
of chronic activation of TMJ afferents may induce chronic reflex activation of facial
musculature. Chronic activation may produce muscle pain that limits movement.
Clinically, bruxism has been associated with muscle hyperactivity and TMJ
dysfunction. Bruxism is defined as a nonfunctional voluntary or involuntary mandibular
activity featuring habitual grinding or clenching of the teeth (Kawamura, 1980). Chronic,
repetitive mandibular movement seen in bruxism is thought to deliver excessive reaction
forces to the TMJ which could produce local inflammatory changes. Putative causes of
bruxism include occlusal stress, CNS and hereditary factors.
2) Referred pain theory
Pain may be referred to the TMJ from other head and neck regions (Bell, 1969).
Travell (1976) suggested that continuous hyperactivity of muscles from the head and neck
may refer pain to the TMJ. The explanations for the origin of referred pain have largely

66
ruled out nerve branching in the periphery as a source of referred pain. The convergence
theory of referred pain invokes a central locus of action in the superficial layers of the
medullary dorsal hom. Noxious input from different sources converge on transmission
cells responding to noxious input (for review, see Fields, 1987). Pain may be mistakenly
mislocated to an area distant from the site of origin due to expectation or previous
experience with pain in the referred site.
In most cases, TMJ pain is not restricted to the joint but is also associated with
extra-articular regions. The most common areas are ipsilateral eyeball, superciliary ridge,
deep masseter muscle, and angle of mandible (Mahan and Ailing, 1991). The
craniovertebral junction and upper neck are other referral sites of TMJ pain (Schellhas et
al 1989).

APPENDIX B
PSYCHOPHYSICS OF TMJ DISORDERS
Pain and mandibular dysfunction are two-common manifestations of TMJ
disorders. Pain can occur when the mandible is at rest or during function. Disordered
movement of the mandible is a sign of mandibular dysfunction (i.e. the inability to
masticate properly). Patients suffering from TMJ disorders often complain of pain while
chewing. Whether mandibular dysfuntion is directly or indirectly due to TMJ disorder or
due uniquely to pain that results from jaw movement is unclear.
Chewing efficiency, jaw movement, biting force and perception of jaw position are
quantifiable features of mastication. A review of the literature reveals studies which have
been directed at investigating the relationship betwen TMJ disorders and mastication.
There has been little psychophysical experimentation involved in quantifying pain
associated with mandibular dysfunction. Even though most of these studies pertain to
treatment efficacy, understanding the relationship between TMJ disorders and mastication
may be valuable in understanding the relationship between pain and TMJ disorders.
Chewing Efficiency
Typically, the clinical appraisal of individuals chewing efficiency is limited to a
subjective report provided by the patient. Early investigators (Christiansen, 1922;
Dahlberg, 1942) developed the technique of using a series of sieves with different mesh
sizes and test materials for chewing in order to estimate chewing efficiency. A simple
67

68
method that can be used clinically to assess chewing efficiency was developed by Loos
(1963) and modified by Carlsson and Helkimo (1972). Test material is chewed for 10, 20
or 40 seconds.
Masticated test materials are then measured in millimeters. Chewing efficiency is rated
according to the size of the material and number of seconds of chewing.
A more elaborate, standardized measure of chewing efficiency, called the
Coefficient of Masticatory Performance, was developed by Manly and Braley (1950). The
Coefficient of Masticatory Performance was defined as the percentage of chewed peanuts
that pass through a 10-mesh screen sieve after being subjected to 20 masticatory strokes.
Rominger and Rugh (1986), utilizing this test, compared the chewing performance of a
group of patients with TMJ dysfunction to a group of normal controls. The patient group
had significantly lower coefficient scores than the normal control group. Lemke et al.
(1987) investigated the level of masticatory efficiency of post-TMJ surgical patients several
years after treatment. These investigators found that the post-surgery group had
significantly lower chewing efficiency scores than a group of non-treated non-
dysfunctional patients.
Taken together, these studies indicate a negative relationship between chewing
efficiency and TMJ disorders. Whether the inability to chew efficiently is due to the TMJ
pain or associated muscular pain is uncertain.
Jaw Movement
The sensory apparatus of the TMJ is thought to play a role in the synchronizing
mechanisms involved with the control of jaw movement (Sicher, 1955). The influences of
TMJ afferents on functional jaw movements has been studied in both normal subjects and
patients suffering from TMJ disorders. In normal subjects, Posselt and Thilander (1965)
anesthetized the lateral part of the TMJ capsule. They observed an increase in lateral

69
movement and maximum opening. The authors suggested that the lateral ligament may be
associated with a protective mechanism during extreme opening. Klineberg (1980) also
anesthetized the TMJs of normal subjects and observed an increase in size of the envelope
of function (range of motion), and suggested that mechanoreceptors of the TMJ play a
modulatory role in motor control of the mandible.
One measure of jaw movement is maximum range of motion (ROM). The
measurement is made for opening, lateral and protrusive excursions. An assessment of
ROM for normal subjects has been reported by Posselt (1968). For normal subjects (adult
males) maximum opening averages 50-60 mm; hinge opening, 20-25 mm; lateral excursion
from midline, 10 mm; and protrusive excursion, 10 mm. Anaesthesization of the lateral
capusle of the TMJ increased hinge opening and protrusion by 10-15% (Posselt and
Thilander, 1965). For patients suffering from TMJ disorders, ROM is generally limited
compared to normal subjects. Helkimo (1974) devised a pain-dysfunction index which
rates severity of mandibular function in regard to pain report for jaw movement and TMJ
palpation. This index was modified by Zarb and Carlsson (1988). Normal ROM was >39
mm for opening and >6 mm for lateral excursions. For patients, ROM was 30-39 mm for
opening and 4-6 mm for lateral excursions. Patients with this amount of impairment
reported pain during at least one jaw movement and pain on palpation of the TMJ's. For
other patients, ROM was <30 mm for opening and <4 mm for lateral excursions. Patients
with this amount of impairment reported during 2 or more jaw movements and pain on
palpation of the TMJ's.
Many clinicians observe a decrease in ROM for patients suffering from TMJ
disorders. These patients are often hesitant to open their mouth maximally because of real
or expected pain. As a result, a measure of ROM may result in a value less than the patient
is actually capable of producing. Therefore, other components of mastication may be more
likely to be reliable measures of jaw function. Moreover, the movements of the mandible

70
that are made during mastication are well within the border movements of the mandible as
defined by the ROM (Okeson, 1989).
Jaw Position
One feature of mandibular function is the ability to control the position of the
mandible within the limits of one's maximum ROM. An important question in the literature
dealing with proprioception is whether position sense is signalled by joint or muscle
afferents. Part of the literature implicates joint afferents (For reviews see Rose and
Mountcastle, 1959; Skoglund, 1973; Dubner et al., 1978); another part of the literature
implicates muscle afferents (for review, see Burgess et al., 1982). It is reasonable to
explain joint position sense in terms of both joint and muscle afferent input.
Jaw position sense has been studied in both normal subjects and patients suffering
from TMJ disorders. Thilander (1961) assessed perception of mandibular position before
and after unilateral or bilateral anesthetization of the TMJ in normal subjects. The results
showed that subjects had more difficulty returning to an initial jaw position, following
anesthetization. Larsson and Thilander (1964) explored the relationship between position
sense and local mechanical pressure applied to the TMJ in normal subjects. The authors
found that position sense was not influenced by local pressure. When the local pressure
was reported to be painful, again position sense was not affected. However, when the
joint was locally anesthetized, jaw position sense deteriorated. If then, local pressure was
applied to the joint during the course of anesthesia, position sense returned to normal
levels. Presumably, local pressure recruited muscle afferents. Input from muscle
mechanoreceptors may have provided the sensory feedback necessary to restore position
sense. The authors reported that ansethetization of the TMJ was performed by infiltration
into the skin and tissues lateral to the capsule. This technique may have not anesthetized
the TMJ completely.

71
Interdental thickness discrimination is one method that has been used to analyze the
position sense of the mandible. Interdental thickness discrimination is the ability to detect
differences in the thickness of test materials placed between opposing teeth. Caffese et al.,
(1973) studied the possible influence of TMJ receptors in tactile occlusal perception by
assessing minimal thickness detection between opposing teeth before and after
anesthetization of the TMJ. These authors found significant differences in threshold
detection in the anesthetized joint compared to the normal joint. On the other hand, Siirila
and Laine (1972) obtained different results from their study of interdental thickness
discrimination. Anesthetization of TMJ did not significantly diminish subjects ability to
detect differences in thickness between teeth at various degrees of mouth opening.
Morimoto and Kawamura (1978) obtained similar results and suggested that the muscle
spindles in the muscles of mastication are mainly responsible for size discrimination.
If mechanoreceptors of the TMJ play a role in jaw position sense, their influence
maybe modulated by TMJ disorders. Ransjo and Thilander (1963) studied position sense
of the mandible in patients with TMJ disorders which were thought to be of myogenic
origin or due to functional malocclusion. The authors assumed that functional
malocclusion caused impairment of TMJ receptors. Position sense was found to be poorer
for the malocclusion group compared to the normal group. Position sense of the myogenic
group was normal. Amelioration of TMJ symptoms after treatment was accompanied by
improvement in the perception of jaw position. This study is in accord with the previous
work of Thilander (1961) suggesting that TMJ mechanoreceptors play a major role in the
ability to perceive position sense of the mandible.
A more recent study by van Willigen et al., (1986) investigated perception of jaw
position in subjects with symptoms of TMJ disorders. They found that all subjects with
craniomandibular dysfunction demonstrated greater mismatches of jaw position compared
with normal subjects. On the other hand, other studies present contrasting evidence
(Christensen and Troest, 1975; Morimoto and Kawamura, 1978; Broekhuijsen and van

72
Willigen, 1983; van der Berghe et al., 1987). Morimoto and Kawamura (1978) tested
interdental thickness discrimination in 8 patients with unilateral or bilateral mandibular
condyles that were either surgically mobilized or removed. The authors failed to observe
any lessened capacity to discriminate thickness. These authors concluded that TMJ
receptors were not essential to size discrimination ability.
Broekhuijsen and van Willigen (1983) studied position sense of the mandible in
normal subjects before and after injection of the TMJ capsule bilaterally with local
anesthetic. Perception of mandibular position was unaffected by anesthetization of the
TMJs. Van den Berghe et al., (1987) assessed position sense of the mandible in patients
suffering from TMJ disorders before and after treatment. Patients' abilities to determine
jaw position were unchanged after successful treatment.
The relative unimportance of joint afferents in assessing position and movement is
noted for a variety of joints. In the human knee joint, injection of local anesthetic into the
joint does not deteriorate the subjects ability to detect passive angular displacements of five
degrees (Clark et al, 1979). Moreover, total joint replacement of the hip produces little
impairment of sensations associated with joint movement (Grigg et al, 1973).
In summary, the ability to control the position of the jaw is an important aspect of
mandibular function. Position sense has been studied in both normal subjects and patients
suffering from TMJ disorders. The preponderance of the evidence suggests that sensory
input from the TMJ contributes little information in controlling the position of the mandible.
Bite Force
Different parameters of bite force, such as maximum bite force, submaximal bite
force and bite force discrimination have been investigated in an effort to assess mandibular
function.

73
Maximum Bite Force
The maxmum bite force is the measure of the greatest force which an individual can
produce by biting on an instrument containing a force transducer. The maximal level of
bite force that an individual is capable of producing is rarely required or utilized during
chewing. Therefore, the relevance of maximum bite force as a measure of mandibular
function is uncertain. Also, a measure of maximum bite force may result in a value less
than an individual is capable or willing to produce. Clark et al., (1984) reported that the
maximum bite force of normal subjects is limited by pain tolerance. Patients suffering from
TMJ disorder may be incapable of producing maximum bite force due to the direct effect of
mandibular dysfunction or unwillingness to bite normally due to the indirect effect of pain.
Such may be the case in several studies that assessed maximum bite force in patients
suffering from TMJ disorders (Helkimo et ah, 1975; Sheikolelam et ah, 1982). Helkimo
et ah (1975) reported that maximum bite force was lower in a patient group with TMJ
disorders than for a control group. Patients' level of maximum bite force increased
following treatment. Sheikolelam et al., (1982) observed that maximum bite force was
significantly less for their patients with TMJ disorders than for normal controls.
Submaximal Bite Force
One important component of the normal chewing cycle is the individuals ability to
produce and control relatively low levels of biting force. Submaximal bite force is the
measure of different levels of biting force below maximum bite force. It seems reasonable
to suggest that impaired mandibular function may result in impairment of the ability to
control submaximal bite force. Several studies have investigated submaximal bite force in
patients with mandibular dysfunction (Helkimo et ah, 1975; Agerberg, 1988). Bite force
was registered with different types of bite beams incorporating a force transducer. A
common feature of patient populations was pain in the TMJ. These studies reported that

74
patients had lower values for submaximal bite force (3-25 kg) compared to control subjects
(5-50 kg).
Bite Force Discrimination
In order for an individual to control the different levels of bite force, he/she must be
able to discriminate differences in the intensity of their own biting force. The role of TMJ
mechanoreceptors in bite force discrimination has been investigated in normal subjects
(Williams et al., 1984; Williams et al., 1989). Bite force was assessed before, during and
after anesthetization of the TMJ by auriculotemporal nerve block (Williams et al., 1984) or
infiltration into the superior joint cavity (Williams et al., 1989). These studies suggest that
the TMJ mechanoreceptors do not appear to be responsible for discrimination of bite force.
In summary, maximum bite force, submaximal bite force and bite force
discrimination are three commonly used measures of mandibular function. Studies
assessing maximum and submaximal bite force indicate that patients suffering from TMJ
disorders have decreased bite force strength. The ability to discriminate bite force levels
has not been studied in patients having TMJ disorders. Neither maximum bite force,
submaximal bite force nor bite force discrimination measures have provided clear
information on the relationship between TMJ sensory input and mandibular function.

APPENDIX C
NEUROANATOMY OF THE TMJ
Until Thilanders (1961) comprehensive, anatomical and histological study of the
innervation of the human TMJ, research on innervation of the TMJ involved macroscopic
studies. Riidinger (1857) observed that the auriculotemporal nerve coursed to the posterior
aspect of the joint where three or four articular branches entered the capsule. The anterior
aspect of the capsule received one or two twigs derived from the masseteric and deep
temporal nerves. Textbooks describing the TMJ generally accepted Riidingers findings.
Moreover, other anatomists (Guerrier and Bolonyi, 1948; Baumann, 1951; Hromada,
1960) are in agreement with the neural topography described by Riidinger but for the
possible exception of the contribution of the facial nerve.
Some sensory fibers travel in the facial nerve, which is otherwise devoted to motor
function. These afferent fibers constitute about 15% of the total nerve fiber population
(Foley, 1960). Guerrier and Bolonyi (1948) reported that branches of the facial nerve
always terminated in the lateral surface of the TMJ. Hromada (1960) stated that a twig
from the facial nerve passed into the lateral aspect of the capsule in about half of his
dissected specimens. On the other hand, Thilander (1961) reported that, immediately
lateral to the capsule, a twig from the facial nerves courses in an anterior direction but does
not ramify into the joint. Kerr (1962) also reported that afferents of the facial nerve
terminate only in the dermatomes of Cl and C2 in the cat. Our observations (unpublished)
suggest that the facial nerve does not innervate the TMJ of the human. However, the facial
75

76
nerve was seen to communicate with the auriculotemporal nerve distal to the TMJ.
In contrast to the innervation of the human TMJ, the facial nerve of the goat
communicates with the auriculotemporal nerve proximal to the articular branches. The
functional implications of this topography are unclear. Some afferents from the TMJ may
travel centrally in the facial nerve or afferents in the facial nerve travel in the
auriculotemporal nerve.
Thilander (1961) reported that the auriculotemporal nerve is the major sensory
nerve of the TMJ. The branches from the auriculotemporal nerve innervate the posterior,
medial, and lateral aspect of the anterior capsule. These branches enter the inferior aspect
of the capsule along the neck of the condyle. This observation is not in accord with
Rudinger (1857) who reported that the articular branches of the auriculotemporal nerve
passed between the condyle and the pars tympanica. However, a recent study (Loughner et
al., 1990) confirms Thilander's report. In this laboratory, macroscopic dissections of the
TMJ of the goat (unpublished) show a similar course of the auriculotemporal nerve and
distribution of articular branches.
According to Hilton's Law (1879), nerves that innervate the muscles that move a
particular joint also contribute to innervation of the joint. Surprisingly, that contribution is
only about 30% of the total TMJ innervation (Thilander, 1961). Twigs from the masseteric
nerve innervate parts of the anterior capsule and anterior aspect of the medial capsule. The
posterior deep temporal nerve innervate the lateral anterior aspect of the capsule. The
auriculotemporal nerve supplies the remaining 70% of the TMJ.
Thilander (1961) estimated that the human TMJ is innervated by an average of 1500
peripheral afferent fibers. The auriculotemporal nerve contributes two thirds of the total
amount. The greatest number of the articular fibers have a diameter between 1 and 2 |xm
and probably terminate as free endings in the capsule, posterior attachment tissues and
adventitia of blood vessels associated with the joint. Other afferent fibers, though fewer in
number, and ranging from 6 to 11 (im, terminate in complex neural endings.

77
The posterior attachment tissues contain a rich plexus of nerve fibers from the
auriculotemporal nerve. Hall et al., (1985) identified and quantified the types of nerve
fibers in the posterior attachment tissues. The authors found that the majority of axons
were unmyelinated. The lateral portion of the posterior attachment tissues contain
significantly higher percentage of unmyelinated fibers. Other investigators (Weinmann and
Sicher, 1951; Sicher, 1955) have reported abundant innervation in association with blood
vessels in the loose connective tissue between the posteror border of the articular disc and
the capsule.
A few nerve fibers have been observed in the synovial membrane of the human
TMJ (Thilander, 1961; Ishibashi, 1966). Ishibashi, (1974) found free nerve endings and
glomerular endings beneath the superficial cell layer of the synovial membrane located on
the posterior aspect of the TMJ. Bemick (1962) described encapsulated end bulbs in the
synovial folds in the TMJ of the rat. These observations appear to contradict those who
believe that the synovial tissue serves no sensory function (Olson, 1969). Although the
nerve endings in the synovial membrane have been reported to be closely associated with
blood vessels (Hagen-Torn, 1882; Davis, 1945), unmyelinated nerve fibers have been
described in the synovium separated from blood vessels (Kellgren and Samuel, 1950;
Rossie, 1950). Kawamura et al. (1967) found Golgi-type endings in the synovial tissue
layer of the TMJ of the cat but not in the synovial membrane itself. Whether the synovial
membrane is innervated or not, the justapositon of afferent fibers allows sensibility in the
territory of the synovium.
As reported by Thilander (1961), the articular disc contained no nerve endings.
However, other investigators (Ishibashi, 1966; Schmid, 1969; Zimny and St. Onge, 1987)
described articular nerves innervating the periphery of the disc in the human TMJ. Similar
results were reported in the monkey (Keller and Moffet, 1968), in the rat (Bernick, 1962)
and in the mouse (Frommer and Monroe, 1966). These studies are consistent with
histological studies of fetal material. Kitamura (1974) reported that, in the 5th month in

78
tero, nerve fibers were observed in the disc; further development was accompanied by a
reduction in disc innervation. Corroboration of the influence of growth on disc innervation
came from Hromada (1960), who observed free nerve endings in the disc of various
animals; at older ages such endings were limited to the periphery of the disc. By
comparison, the nerve supply to the meniscus of the human knee remains unclear (For
review see Zimny, 1988). The most recent study (Albright and Zimny, 1987) reports that
free and complex nerve endings were observed in outer and middle one-third of the
meniscus; whereas, no innervation was found in the inner one-third.
Innervation of the TMJ of the monkey and cat resemble that of the human joint
(Franks, 1965; Keller and Moffett, 1968). Branches from the deep temporal and
masseteric nerves supply the anterior capsule, and the articular branches of the
auriculotemporal nerve supply the TMJ posteriorly. Preliminary macrodissection of the
nerves innervating the TMJ of one goat was performed in this laboratory. The
auriculotemporal nerve gave off three articular branches along the posterior aspect of the
neck of the condyle. The articular branches ascended into the fatty and fibrous articular
tissue. The termination of the temporal branch of the auriculotemporal nerve appeared in
the facial skin inferior to the zygomatic arch. The masseteric nerve was observed to arise
from the anterior trunk of the mandibular nerve, course lateral along the anterior border of
the capsule of the TMJ and terminate in the superficial and deep masseter muscle. Twigs
from the masseteric nerve appeared to enter the anteriorlateral aspect of the capsule.
Tissues surrounding articulations possess fewer types of receptors than muscle or
cutaneous tissue. Thilander (1961) described four types of neural endings in the human
TMJ: Ruffini-like receptors, modified Pacinian endings, Golgi tendon organs and free
nerve endings. Ishibashi (1966) also reported the presence of free nerve endings and
complex terminal expansions in the human TMJ. Keller and Moffett (1968) reported free
and complex nerve endings in the TMJ of monkeys. Many investigators have identified

79
free and complex nerve endings in the TMJ of the cat (Kawamura and Majima, 1964;
Greenfield and Wyke, 1966; Kawamura et al., 1967; Wyke, 1967; Klineberg, 1971).
The three types of complicated nerve endings were sparsely distributed compared to
the free nerve endings. The most common complex ending is the Ruffini ending. Ruffini-
like endings were encountered in the lateral and posteriorlateral aspect of the capsule in
humans (Thilander, 1961). Griffin and Harris (1975) described a thinly unencapsulated
corpuscle located close to the periosteum of the neck of the condyle and in the lateral and
medial aspects of the capsule fat pads. These receptors may have been similar to the
Ruffini endings described by Klineberg (1971) in the TMJ of the cat. The Ruffini-type,
low theshold mechanoreceptors were once thought to signal joint position (Boyd and
Roberts, 1953; Boyd, 1954; Cohen, 1955; Skoglund, 1956, 1973). However, other
investigators (Burgess and Clark, 1969; McCall et al., 1974; Clark and Burgess, 1975;
Clark, 1975; Grigg, 1975; Grigg and Greenspan, 1977) have shown that Ruffini endings
are seldom active at intermediate positions of the cat knee joint. They are responsive to
extremes of joint movement. Consequently, these receptors are unlikely the peripheral
neural substrate that code for position sense. Instead, Ruffini endings appear to signal the
torque produced when the joint is extended and/or rotated at the limit of the range of
motion. (Grigg et al., 1982a).
Pacinian endings were found in the lateral aspect of the capsule (Thilander, 1961).
Paciniform-type end organs in cats have a similar distribution as Ruffini endings but less
dense (Kawamura et al., 1967; Klineberg, 1971). Golgi tendon organs were located in the
temporomandibular ligament and anterior capsule (Thilander, 1961; Griffin et al., 1965).
In the anterior capsule, the Golgi end organ was in series with the extrafusal fibers of the
lateral pterygoid muscle and tendon fasciculi of the capsular tissue or the fibrous tissue of
the pes menisci. In the temporomandibular ligament the Golgi end organ was thought to be
in series with fibers of the deep masseter muscle. Both Paciniform endings and Golgi
tendon organs are thought to respond like comparable endings found in cutaneous and

80
muscle tissue (Willis and Coggeshall, 1978). However, Grigg et al., (1982b) showed that
in the cat knee, Golgi tendon organs responded to local pressure applied perpendicular to
the capsule but not to tension applied parallel to the capsule.
Free nerve endings are the most abundant receptor in the capsule of the human
TMJ. Presumably, free nerve endings derived from myelinated afferents subserve fast pain
sensibility and nociceptive somatic reflexes; free nerve endings derived from unmyelinated
nerve fibers may subserve slow pain sensibility or innervate vascular elements. Free
ending receptor specializations have yet to be defined. In sympathectomized cats, sensory
nonmedullated plexuses have been found in the inner layers of the fibrous capsule, adjacent
synovial tissues and adventitia of blood vessels in the knee joint of cat (Samuel, 1952).
Free endings have been described in the joint capsule, joint ligaments and periarticular fat
pads (Greenfield and Wyke, 1966). Similar results have been reported by Freeman and
Wyke (1967). Free endings characteristic of group III and IV afferents have been
described in the Archilles tendon of the cat as well (Andres et al., 1980). Some of these
free endings may be nociceptors.
Although there are great variations in the morphology of the TMJ between species,
the innervation of the TMJ is quite similar (Kawamura, 1980). The distribution and
appearance of receptors may vary with age and species (Polacek, 1966), but the types of
receptors are consonant across species including human.
In summary, the mammalian TMJ contains four types of receptors (for review see
Skoglund, 1973; Zimny, 1988). The Ruffini and Paciniform mechanoreceptors are
innervated by medium-sized (Ab) myelinated fibers, the Golgi tendon organ by large (Aa)
myelinated fibers and the free endings by fine myelinated and unmyelinated afferents.

APPENDIX D
CENTRAL REPRESENTATION OF TMJ AFFERENTS
The central distribution of TMJ afferents has been studied in the trigeminal nuclear
complex. The main sensory nuclei and the dorsal part of the rostral spinal nucleus were
found to contain neurons responsive to isolated condylar movement or pressure applied to
the joint capsule of the cat (Kawamura aand Majima, 1964; Kawamura et al., 1967). The
authors reported simple, qualitative findings describing three types of responses to
ipsilateral condylar rotation (rapidly adapting, slowly adapting and on-off types) and two
types of responses to mechanical stimulation (rapidly adapting and slowly adapting types).
In addition, response patterns of neurons in the trigeminal motor nucleus were recorded
during condylar movements or mechanical stimulation of the joint capsule. As with
responses from the sensory nuclei, no quantification of activity was attempted. Procaine
infiltration into the joint capsule abolished neural responses. Another qualitative study
reported unit activity found in the trigeminal main sensory nucleus and nucleus oralis of the
cat that responded to jaw rotation or pressure applied to the ipsilateral TMJ (Sessle and
Greenwood, 1976). One of these units was antidromically activated from the thalamus.
Other direct projections from the superficial layers of the medullary dorsal horn to the
thalamus have been demonstrated anatomically (Craig and Burton, 1981) and
electrophysiologically (Dostrovsky and Broton, 1985).
The caudal aspects of the trigeminal nucleus complex were found to contain
neurons that are driven by electrical, mechanical, and algesic chemical stimuli applied to the
TMJ (Broton and Sessle, 1988). Neurons in the subnucleus caudalis were first classified
81

82
on the basis of their responsiveness to mechanical stimulation to the skin: low-threshold
mechanoreceptors (LTM), wide dynamic range (WDR) or nociceptive specified (NS).
WDR and NS neurons responded maximally to algesic chemical and intense mechanical
stimulation applied to the joint. TMJ stimulation consisted of local probing or extreme jaw
opening. The majority of single units with TMJ input received convergent input from
cutaneous afferents. Kojima (1990) also found convergence patterns of afferent input from
the TMJ and muscle in the subnucleus caudalis. Most of the units tested were responsive
to mechanical and thermal stimulation of both the TMJ and the masseter muscle.
Extensive convergence of cutaneous and muscle inputs on second-order neurons
that respond to articular movement have been described in the cat knee (Schaible et al.,
1986). In some neurons, maximal responses to joint movement occurred with forced
extension, inward rotation or outward rotation. Other neurons were excited only by
noxious movement. Joint movement was considered noxious if the movement was made
forceably. No quantification of forces was attempted. This report compares favorably
with the effects of TMJ stimulation in neurons in the medullary dorsal horn (Broton and
Sessle, 1988), in that most second order neurons that respond to noxious joint simulation
also receive convergent input from skin and/or muscle. Such central convergence may be
important in explaining the tenderness of skin and/or muscles near the joint that are often
observed clinically when the joint is painful.
Changes in responsiveness in spinal neurons have been investigated during the
development of acute arthritis in the cat knee jont (Neugebauer and Schaible, 1990). All
neurons tested with joint input showed enhanced responsiveness to joint flexion after
induction of inflammation.
Other electrophysiological experiments performed in polyarthritic rats demonstrated
nociceptive inputs from chronically inflamed joints to the ventrobasal thalmus (Guilbaud et
al., 1980; Gautron and Guilbaud, 1982), intralaminar and medial thalamus (Kayser and
Guilbaud, 1984; Dostrovsky and Guilbaud, 1990), and somatosensory cortex (Lamour et

83
al., 1983). One consistent feature of the neuronal reactivity seen in all of these studies is
the increase responsiveness of central neurons to non-noxious stimulation of the inflamed
joints. The central mechanisms which might contribute to changes in responsiveness of
central neurons in arthritic rats is still in question. The alterations in discharge behavior
seen in CNS neurons is likely due, in part, to the changes in responsiveness of joint
receptors due to inflammatory processes.

APPENDIX E
TRIGEMINAL GANGLION
The trigeminal ganglion is situated near the apex of the petrous bone in the middle
cranial fossa. It lies in Meckel's cave near the cavernous sinus and internal carotid artery.
The sensory root (portio major) enters the pons in association with the motor root (portio
minor), which courses dorsomedially, and terminates in the trigeminal nuclear complex.
Sensory input from the face enters the trigeminal ganglion via the opthalamic,
maxillary and mandibular division of the trigeminal nerve. The cell bodies of these afferent
fibers are segregated into discrete clusters (Jerge, 1964; Kerr, 1962).
Retrograph transport of HRP injected into the cat TMJ showed that sensory
neurons originate in the trigeminal ganglion (Romfh et al., 1979; Capra, 1987). Whether
all of the cell bodies of afferent neurons innervating the TMJ are located in the trigeminal
ganglion remains unanswered. There is evidence suggesting that the peripheral spinal
neurons innervate the TMJ. Widenfalk and Wiberg (1990) injected HRP into the TMJ of
rats. Labeled cells were observed ipsilaterally in the second to fifth dorsal root ganglion.
In addition, there is evidence suggesting that the mesencephalic nucleus contains cell bodies
of neurons that terminate in the TMJ. In a preliminary communication, Limwongee (1986)
reported injection of HRP into the TMJ of rat, cat and monkey. He found labeled neurons
in the mesencephalic nucleus at the level of the caudal pons. On the other hand, Corbin
(1940) ablated the mesencephalic nucleus and examined histologically the auriculotemporal
nerve. He found no degenerated fibers. In addition, Chen and Turner (1987) injected
84

85
HRP into the TMJ and insertion of the lateral pterygoid muscle of rats. They found no
central projection to the mesencephalic nucleus.
Somatotopv
There is general agreement that the trigeminal ganglion in cats is somatopically
represented from a medial to lateral direction (Beaudreau and Jerge, 1968; Zucker and
Welker, 1969; Kerr and Lysak, 1964; Darian-Smith et al., 1965; Marfurt, 1981). The
ophthalmic division lies anteriomedially, the mandibular division lies posteriolaterally and
the maxillary division is situated in an intermediate position. Overlap between divisions
has been reported (Marfurt, 1981; Henry et al., 1986). Romfh et al., (1979) and Capra
(1987) reported that injection of HRP into the capsular tissues of the TMJ in the cat resulted
in a restricted distribution of label in the posteriolateral position of the trigeminal ganglion.
Very few labeled cells were found in the most dorsal or in the most ventral areas of the
mandibular division of the trigeminal ganglion. The majority of labeled cells is found
throughout the intermediate zone in the posteriolateral part of the ganglion.
Electrophysiological studies in cats (Capra and Gaitpon, 1981) and in rabbits (Lund and
Matthews, 1981; Appenteng et al., 1982) confirmed that TMJ afferents were located in the
posteriolateral region of the trigeminal ganglion.
In addition to the mediolateral somatotopy studies suggest a dorsoventral
somatotopic organization (Kerr and Lysak, 1964; Marfurt, 1981; Capra, 1987).
Representation of oral and perioral structures appear ventral in the ganglion. Areas remote
from the mouth lie in the dorsum of the ganglion.

APPENDIX F
GROSS ANATOMY
The TMJ in mammals is a ginglymus-arthroidal joint, i.e., a hinge joint capable of
gliding movement (Figure F-l). The craniomandibular articulation involves the condyle of
the mandible juxtaposed with the articular surface of the squamous portion of the temporal
bone. Interposed between the condyle and the articular fossa is an articular disk dividing
the articular space into upper and lower compartments.
The periarticular soft tissue consists of fibrous capsule, posterior attachment
tissues, synovial membrane and accessory ligaments. Except for the synovial membrane,
these tissues serve to limit the range of motion of the joint and to maintain a packed position
(Sicher, 1960; Rocabado, 1983). A packed position is the condyle-disc-fossa relationship
which juxtaposes these TMJ elements at rest and during mandibular movements. The joint
capsule is loose and composed of dense connective tissue with a collagenous matrix richly
supplied with blood vessels and nerves. The dense connective tissue of the capsule is
located primarily on the lateral and medial aspect of the joint and intimately associated with
the temporomandibular and sphenomandibular ligaments, respectively. The anterior
capsule arises from the suture line between the greater wing of the sphenoid bone and the
temporal bone. It inserts on the anteriorlateral aspect of the condylar neck. The loose
connective tissue of the capsule encompasses the joint posteriorly. It arises from the tragal
cartilage laterally and tympanic plate medially. The posterior capsule, as a meshwork of
unorganized collagen fiber, inserts and blends in with the posterior periosteum of the
condylar neck and upper capsule of the parotid gland.
86

87
1. Articular Surface of Glenoid Fossa
2. Superior Cavitt
3. Disc (Stippled Area)
4. Capsule
5. Articular Surface of Condyle
6. Synovial Membrane
7. Squamo-Tympanic Suture
8. Spine of the Sphenoid
9. Vascular Knee of Meniscus
10. Pes Meniscus
11. Superior Belly of Lat. Pterygoid
12. Inferior Belly of Lat. Pterygoid
13. Superior Stratum of Bilaminar Zone of Meniscus
14. Inferior Stratum of Bilaminar Zone of Meniscus
Figure F-l
Schematic diagram of the human temporomandibular joint. Sagittal and
frontal views.
15. Auriculotemporal Nerve
16. BloodVessels
17. Posterior Deep Temporal Nerve
18. Squamo-Sphenoidal Suture
19. Parotid Gland
20. Sphenomandibular Ligament

88
The dense connective tissue of the capsule reinforces the lateral position of the TMJ
and is incorporated into the temporomandibular ligament. Horizontal fibers of the
temporomandibular ligament restrict posterior displacement of the condyle and oblique
fibers tend to limit lateral and inferior displacement (Sicher, 1960; Griffin and Malor,
1974). The posterior attachment tissues consists of collagenous and elastic connective
tissues which extend from the posterior border of the disc to the tympanic plate.
Macroscopic dissections of the goat TMJ were performed in this laboratory. The
articular surface of the condyle is oval in shape, its longer dimension is concave
mediolateral and the shorter dimension is convex anterioposterior. The articular disc is
ovoid, biconcave, and divides the joint into two synovial cavities. The fibrous capsule is
moderately loose which allows for extensive lateral translation of the condyle. The capsule
surrounds the joint, with the exception of the anteriomedial portions, where the lateral
pterygoid muscle attaches to the neck of the condyle. With four exceptions the gross
anatomy of the goat TMJ is similar to the human. First, the lateral aspect of the posterior
attachment tissue extends posteriorly beyond the postglenoid process and attaches to the
inferior surface of the zygomatic process of the temporal bone. This anatomical variation is
associated with the lateralization of the bony articulation of the TMJ beyond the cranial
base. Second, the articular surface of the glenoid fossa is slightly convex in all directions,
rather than concave. To accommodate this convexity the condyle is appropriately concave
along the mediallateral axis. Third, there is no articular eminence. Finally, the lateral
pterygoid muscle attaches to the anteriormedial aspect of the neck of the condyle in a
manner similar to the human, but it does not appear to attach to the disc.
Comparative Anatomy
According to the classification of Turnbull (1970), goats are section II herbivors
while humans are section III omnivores. The TMJ of the goat has been used as an animal

89
model for oral surgery procedures because the anatomy and biomechanics are similar to the
human TMJ (Bifano et alM 1990).
First, for the vertebrate chewing apparatus, the range of motion is generally
confined to those movements necessary for dealing with a particular diet. Due to a coarse
diet of vegetation, ruminants possess a greater range of mandibular movement than do
carnivores. The excursive movements include hinging, lateral translation, slight protrusion
and mediolateral shift. Hinge opening and lateral translational movements are required for
forceful grinding. The lateral pterygoid muscle is the prime mover of the mandible during
lateral translational movements. The lateral excursion, initiated by contraction of either one
of the lateral pterygoid muscles, is a prerequisite to an effective grinding stroke. Both the
goat and human possess a well-developed, lateral pterygoid muscle.
Second, the elevated position of the condyle of the mandible relative to the occlusal
plane benefits the operation of the masseter and medial pterygoid muscles. They function
synergistically to provide powerful bite force needed for grinding activity.
Third, the condyle is convex anteriorposteriorly, which allows some translation
along a convex articular surface of the fossa. Such anteriorposterior translation represents
a common denominator between the TMJ of non-camivorous mammals and the human
joints. In contrast, carnivores have a deep concave articular fossa that allows only hinge
movement and prevents dislocation during seizure of prey.

APPENDIX G
SUMMARY TABLES OF TMJ REACTIVITY
90

TABLE G-l
REACTIVITY IN VERTICAL PLANE
NORMAL TISSUE
FILE
FUNCTION
TEST
FREQ.
THRES
ACT.
THRES
FREQ.
ASYM.
MRI
2
R
RF
(gr)
CV
(m/sec)
1
021691E
E3
Lnl = -1.2LnF
+
7.6
DF
14N
30N
4.3
0.56
3.6
0.7
1
021691E
E3
Lnl = -1.4LnF
+
8.4
M
14*
26'
4.9
0.59
3.6
0.7
2
040690S
S3
Lnl = -3.4LnF
+
11.2
DF
15N
19N
6.5
0.25
28.0
0.4
2
040690S
S3
Lnl = -0.37LnF +
2.9
FV
6 N/s
91 N/s
1.3
0.26
28.0
0.4
2
040690S!
S3
Lnl = -1.8LnF
+
5.5
M
T
10'
3.5
0.20
28.0
0.4
2
040690T
T3
Lnl = -5.0LnF
+
1.0
SF
7.ON
9N
15N
6.0
0.73
28.0
0.4
2
040690T!
T3
Lnl = -5.8 LnF +
17.0
P
10
10
16'
6.6
0.73
28.0
0.4
3
041390K
K7
Lnl = -l.lLnF
+
5.5
DF
13N
31N
2.3
0.10
5.4
3
041390N
N7
Lnl = -0.6LnF
+
4.8
FV
2N/s
90N/s
2.1
0.10
5.4
4
042090H
H6
Lnl = -3.0LnF
+
16.0
DF
.
41N
62N
6.9
0.64
76.0
4
042090H!
H6
Lnl = -5.0LnF
+
16.0
M
8
10
13.0
0.64
76.0
5
102690D
D1
Lnl = -0.8LnF
+
7.0
DF
32N
122N
3.4
0.29
5.4
5
102690D
D1
Lnl = -0.6LnF
+
6.4
FV
42N/s
218N/s
3.3
0.30
5.4
6
110990E
E2
Lnl = -2.7LnF
+
11.0
DF
20N
24N
7.3
0.53
3.6
6
110990E
E2
Lnl = l.lLnF
+
7.7
FV
45 N/s
129N/S
2.8
0.76
3.6
6
110990D
D2
Lnl = -0.9LnF
+
7.0
SF
8.ON
30N
65N
3.8
0.66
3.6
.
6
110990E!
E2
Lnl = -6.6LnF
+
19.0
M
10'
12'
14.0
0.73
3.6
.
7
111490E
E2
Lnl = -1.3LnF
+
8.1
DF
30N
88N
2.8
0.54
29.0
7
111490E
E2
Lnl = -0.3LnF
+
4.6
FV
29 N/s
296N/S
2.9
0.25
29.0
7
111490F
F2
Lnl = -0.44LnF
+
5.7
SF
27N
58N
96N
4.1
0.86
20.0
8
111490L
L3
Lnl = -l.lLnF
+
7.5
DF
.
25N
77N
3.2
0.73
5.4
8
111490L
L3
Lnl = -0.22LnF
+
4.0
FV
11 N/s
142N/S
2.9
0.20
5.4
8
111490J!
J3
Lnl = -6.2LnF
+ 21.0
M
15'
22'
9.0
0.31
5.4
.
9
121490A
A1
Lnl = -1.3LnF
+
9.6
DF
38N
113N
4.0
0.68
12.5
10
030791A
A1
Lnl = -0.9LnF
+
7.2
FV
lON/s
48N/s
6.3
0.50
5.4
11
032091G
G3
Lnl = -0.7LnF
+
6.5
DF
12N
36N
4.3
0.40
5.4
7.5
11
032091G
G3
r
3
M
II
1
p
-J
r
3
T1
+
4.8
FV

6N/s
170N/S
3.9
0.19
5.4
7.5

TABLE G-2
REACTIVITY IN HORIZONTAL PLANE
NORMAL TISSUE
LEFT LATERAL
FILE
FUNCTION
TEST
FREQ.
THRES
ACT.
THRES
FREQ.
ASYM.
MRI
2
R
RF
(gr)
CV
(m/sec)
1
021690A
A1
Lnl =
-1.4LnF +
5.1
SF
3.ON
3.ON
30N
0.5
~0W
8.5
4
2
110990A
A1
Lnl =
-0.4LnF +
5.0
DF
30N
100N
3.3
0.10
15.0
4
3
121990A
A1
Lnl =
-l.OLnF +
5.0
DF
4
6.0N
15N
2.8
0.27
8.5
4
3
121990A
A1
Lnl =
-0.3LnF +
3.4
FV
4
l.ON/s
35N/s
2.3
0.32
8.5
4
011691A
A1
Lnl =
-0.7LnF +
4.8
DF
.
8.ON
33N
2.6
0.40
5.5
2.5
4
011691A
A1
Lnl =
-0.2LnF +
3.8
FV
4
25N/s
267N/s
2.7
0.17
5.5
2.5
4
011691B
B1
Lnl =
-1.8LnF +
8.7
SF
6.0N
16N
42N
2.8
0.97
5.5
2.5
5
011691C
C2
Lnl =
-0.7LnF +
4.8
DF
4
6.0N
34N
2.4
0.77
76.0
4
5
011691C
C2
Lnl =
-0.34LnF +
4.4
FV
4
62N/S
305N/s
2.5
0.34
76.0
4
5
011691D
D2
Lnl =
-1.2LnF +
6.3
SF
4.5N
ION
19N
3.7
0.95
76.0
6
012391A
A2
Lnl =
-0.5LnF +
4.7
DF
4
9.5N
56N
2.8
0.31
29.0
6
012391A
A2
Lnl =
-0.1 LnF +
3.4
FV
4
7.0N/S
119N/s
2.9
0.10
29.0
7
022091A
A1
Lnl =
-1.3LnF +
7.0
DF
4
7.ON
31N
2.9
0.75
15.0
7
022091A
A1
Lnl =
-0.3LnF +
4.7
FV
4
2.0N/S
134 N/s
3.2
0.50
15.0
7
02209IB
B1
Lnl =
-1.4LnF +
8.4
SF
6.ON
12N
38N
3.8
0.64
15.0
8
031391A
A1
Lnl =
-3.0LnF +
14.0
DF
4
18N
34N
3.4
0.73
3.6
9
031391D
D3
Lnl =
-0.42LnF +
5.7
DF
4
5.ON
43N
4.2
0.23
5.5
9
031391D
D3
Lnl =
-0.16LnF +
4.9
FV
4
6.0N/S
171 N/s
4.1
0.16
5.5
10
03209ID
D2
Lnl =
-0.38LnF +
4.6
DF
5.ON
20N
3.6
0.17
3.6
10
03209IE
E2
Lnl =
-0.36LnF +
5.0
SF
2.ON
4.0N
35N
3.8
0.28
3.6
11
032891J
J4
Lnl =
-0.8LnF +
6.9
DF
4
ION
25N
4.7
0.32
5.5
11
032891J
J4
Lnl *
-0.2LnF +
5.0
FV
#
6.0N/S
133N/S
4.0
0.29
5.5
12
042491A
A1
Lnl =
-0.7LnF +
5.3
DF
4
6.0N
19N
3.5
0.60
29.0
13
072691A
A1
Lnl =
-0.78LnF +
5.5
DF
4
13N
40N
2.9
0.19
5.5
14
092791H
H
Lnl =
-0.49LnF +
3.9
DF

3.0N
31N
2.3
0.27
3.6

TABLE G-3
REACTIVITY IN HORIZONTAL PLANE
NORMAL TISSUE
RIGHT LATERAL
FILE
FUNCTION
TEST
FREQ.
THRES
ACT.
THRES
FREQ.
ASYM
MRI
2
R
RF
(gr)
CV
(msec)
1
031391B
B2
Lnl = -0.59LnF + 5.3
DF
8.ON
19N
3.9
0.33
5.5
2
041091A
A2
Lnl = -2.1LnF + 8.3
DF

9.ON
12N
6.0
0.91
5.5
3
042491G2
G3
Lnl = -2.2LnF +10.4
SF
12N
14N
26N
5.0
0.38
5.5
4
0424911
14
Lnl = -2.0LnF + 7.8
DF
.
4.0N
17N
2.7
0.70
5.5
4
0424911
14
Lnl = -0.3LnF + 3.4
FV
2.0N
50N/s
2.2
0.26
5.5
4
042491J
14
Lnl = -4.0LnF +13.0
SF
5.ON
9.ON
14N
6.6
0.97
5.5

TABLE G-4
REACTIVITY IN THE VERTICAL PLANE
IN PREVIOUSLY INFLAMED TISSUE
FILE
FUNCTION
TEST
FREQ.
THRES
ACT.
THRES
FREQ.
ASYM
2
R
MRI
(m/sec)
RF
(gr)
cv
(m/sec)
1
021089B2
B2
Lnl = -0.29LnF+ 3.3
FV
9.0N/S
60N/S
0.11
2.2
15.0
2
021089T
T7
Lnl = -0.49LnF+ 3.0
DF
1.0N
4.ON
0.10
2.5
15.0
2
021089T
T7
Lnl = -0.5LnF + 3.3
FV
0.8N/S
26N/s
0.26
2.7
15.0
3
021089EE
Ell
Lnl = -1.6LnF + 2.5
DF
0.35N
1.0N
0.19
3.2
15.0
3
021089EE
Ell
Lnl = -2.4LnF + 3.2
FV
0.4N/S
3.3N/S
0.85
0.6
15.0
4
021089JJ
J13
Lnl = -1.8LnF + 5.4
DF
4.0N
8.ON
0.11
2.9
15.0
4
021089JJ
J13
Lnl = -0.5LnF + 3.2
FV
0.8N/S
58N/s
0.41
1.2
15.0
5
041091E
E3
Lnl = -l.lLnF + 9.1
DF
28N
67 N
0.50
5.1
5.0
5
041091E
E3
Lnl = -0.26LnF+ 5.2
FV
lON/s
40N/s
0.20
4.3
5.0
5
041091E!
E3
Lnl = -6.6LnM + 24.0
M
17
20
0.46
17.0
5.0
5
041091F
F3
Lnl = -0.68LnF+ 6.3
SF
3.ON
4.0N
19N
0.44
4.5
5.0
5
041091F!
F3
Lnl = -2.0 LnP + 10.0
P
v
10
17
0.42
6.1
5.0
REACTIVITY IN HORIZONTAL PLANE
IN PREVIOUSLY INFLAMED TISSUE
LEFT LATERAL
FILE
FUNCTION
TEST
FREQ.
THRES
ACT.
THRES
FREQ.
ASYM.
2
R
MRI
(m/sec)
RF
(gr)
CV
(m/sec)
1
033090T
T15
Lnl = -0.2 LnF + 3.0
FV
7.5N/S
54N/s
2.2
0.12
125.0
0.67
1
033090U
U15
Lnl =-1.9LnF + 9.6
SF
9. IN
9.IN
32N
3.7
0.28
125.0
0.67
1
033090TS
T15
Lnl = -0.84LnF+ 6.6
DF
19N
55N
3.6
0.20
125.0
0.67
2
0509910
02
Lnl = -0.59LnF+ 5.9
DF

18N
65N
3.6
0.36
5.5


95
TABLE G-5
TMJ NOCICEPTOR REACTIVITY IN NORMAL TISSUE
VERTICAL PLANE
Test Conditions
with RF (n=18)
without RF (n-9)
code (n=ll)
no code (n=7)
code (n=8)
no code (n=l)
Dynamic Force
10
8
6
3
Force Velocity
8
10
4
5
Movement
5
10
2
3
Static Force
3
12
1
4
Position
1
14
0
4
Conduction
Velocity
0.4 to 7.5
m/sec
(n=4)
0.75 to 1.5
m/sec
(n=2)


Post-test
Spontaneous
Activity
2
0
0
0

96
TABLE G-6
TMJ NOCICEPTOR REACTIVITY IN NORMAL TISSUE
HORIZONTAL PLANE
Test Conditions
with RF (n=18)
without RF (n-9)
code(n=14)
no code(n=3)
code (n=l)
no code (n=4)
Dynamic Force
13
4
0
3
Force Velocity
7
9
0
3
Static Force
5
11
0
0
Conduction
Velocity
2.5 to 3.3
m/sec
(n=2)
0.5
m/sec
(n=l)


Post-test
Spontaneous
Activity
1
0
0
0

97
TABLE G-7
TMJ NOCICEPTOR REACTIVITY
IN PREVIOUSLY INFLAMED TISSUE
Test Conditions
with RF (n=7)
without RF (n-8)
code (n=7)
no code(n=0)
code (n=6)
no code(n=2)
Dynamic Force
6
0
4
2
Force Velocity
6
0
5
2
Movement
1
0
0
0
Static Force
2
0
0
0
Position
1
0
0
0
Conduction
Velocity
0.7m/sec
(n=l)
0
0
0
Post-test
Spontaneous
Activity
0
0
0
0

98
TABLE G-8
TMJ NOCICEPTOR REACTIVITY
IN ACUTELY INFLAMED TISSUE
Test Conditions
with RF (n=ll)
code (n=9)
acquired coding (n=8)
Dynamic Force
9
2
Force Velocity
4
4
Movement
2
0
Static Force
4
5
Position
1
1
Conduction
Velocity
0.8 to 6.0
m/sec
(n=6)

Post-test
Spontaneous
Activity

6

99
TABLE G-9
TMJ NOCICEPTOR REACTIVITY
IN SALINE INJECTED TISSUE
Test Conditions
with RF (n=8)
code(n=7)
acquired coding (n=l)
Dynamic Force
6
0
Force Velocity
2
1
Movement
0
0
Static Force
6
0
Position
0
0
Conduction
Velocity
0.5-8.5
m/sec
(n=2)

Post-test
Spontaneous
Activity

0

100
TABLE G-10
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE VERTICAL PLANE
UNIT#1
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
12N
1.7N
-10.3N
Freq. Asymptote
50N
69N
19N
Mean Rate
3.4
2.7
-0.7
Slope
-0.44
-0.19
-0.25
Freq. Thres.



2
R
0.18
0.44
0.26
Static Force
Act. Thres.
7N
1.6
-5.4N
Freq. Asymptote
17N
30N
13N
Mean Rate
4.5
5.1
0.6
Slope
-0.4
-0.68
-0.28
Freq. Thres.
10N
1.6N
-8.4N
2
R
0.23
0.60
0.42
Position
Act. Thres.
10.5
3.4
-7.1
Freq. Asymptote
16
22
ON
b
o
Mean Rate
5.2
3.3
-1.5
Slope
-1.1
-1.2
-0.1
Freq. Thres.
10.0
2.7
-7.3
2
R
0.35
0.79
0.44
Movement
Act. Thres.
9.8
6.2
-3.6
Freq. Asymptote
14
25
11
Mean Rate
7.3
3.13
-4.13
Slope
-4.0
-0.5
3.5
Freq Thres.



i
R
0.6
0.47
-0.13
Force Velocity
Act. Thres.
2.0 N/s
Freq. Asymptote
317 N/s
Mean Rate
2.8
Slope
-0.11
Freq Thres.
2
-
R
0.35

101
TABLE G-11
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE VERTICAL PLANE
UNIT #2
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
6.0N
27 N
21N
Freq. Asymptote
33N
66N
33N
Mean Rate
4.8
3.0
-1.8
Slope
-0.44
-0.46
0.01
Freq. Thres.



2
R
0.42
0.11
-0.31
Movement
Act. Thres.
8.0
23*
15*
Freq. Asymptote
24
28
4.0*
Mean Rate
4.1
7.3
3.2
Slope
-0.8
-2.5
1.7
Freq. Thres.



Z
R
0.48
0.19
-0.29
Static Force
Act. Thres.
25N
Freq. Asymptote

59N

Mean Rate
.
3.6
Slope
.
-1.5

Freq Thres.

12.0

2
R
.
0.62
.

102
TABLE G-12
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE VERTICAL PLANE
UNIT #3
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
26N
40.7N
14.7N
Freq. Asymptote
50N
76N
26N
Mean Rate
4.4
2.8
-1.6
Slope
-2.7
-1.17
-1.5
Freq. Thres.



2
R
0.50
0.10
-0.40
Movement
Act. Thres.
21"
24"
3.0
Freq. Asymptote
26
25.5
-0.5
Mean Rate
14
22
8.0
Slope
-7.0
-7.9
0.9
Freq. Thres.
24"
26
20
2
R
0.40
0.90
0.50
Force Velocity
Act. Thres.
Freq. Asymptote
20.0N/S
285N/S
Mean Rate
Slope
Freq Thres.
2
R
1.9
-0.4
0.13

103
TABLE G-13
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE VERTICAL PLANE
UNIT #4
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
17N
49N
32N
Freq. Asymptote
7.5N
23N
15.5N
Mean Rate
3.8
3.7
-1.1
Slope
-0.6
-1.0
0.4
Freq. Thres.



2
R
0.33
0.52
0.19
Movement
Act. Thres.
18
ir
-7.0*
Freq. Asymptote
29*
20
-9.0*
Mean Rate
5.3
4.2
-1.1
Slope
-2.1
-1.7
-0.4
Freq. Thres.


.
L
R
0.32
0.66
0.34
Position
Act. Thres.
20
Freq. Asymptote
29
Mean Rate
7.7
Slope
-3.3
Freq. Thres.
2
-14.7'
R

0.65
Force Velocity
Act. Thres.
2.2N/S
Freq. Asymptote
23.5N/S
.
Mean Rate
3.2
.
Slope
-0.12

Freq Thres.
2


R
0.11


104
TABLE G-14
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #1
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
Freq. Asymptote
Mean Rate
Slope
Freq. Thres.
2
R
1.4N
34N
4.1
-0.6
0.45
Force Velocity
Act. Thres.
Freq. Asymptote
Mean Rate
Slope
Freq. Thres.
3.0N/S
132N/s
3.9
-0.08
z
R
0.12
Static Force
Act. Thres.
10.7N
Freq. Asymptote
29N
Mean Rate
Slope
Freq Thres.
2
R
4.6
-0.97
2.8N
0.37

105
TABLE G-15
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #2
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
2.7N
1.3N
-1.4N
Freq. Asymptote
30N
32N
2.0N
Mean Rate
2.0
3.4
0.5
Slope
-1.1
-0.5
-0.6
Freq. Thres.



2
R
0.63
0.49
-0.14
Force Velocity
Act. Thres.
lN/s
1.6N/S
0.6N/S
Freq. Asymptote
286N/S
185N/S
-lOlN/s
Mean Rate
2.5
3.5
1.0
Slope
-0.26
-0.17
-0.09
Freq. Thres.



L
R
0.30
0.29
-0.01
Static Force
Act. Thres.
Freq. Asymptote
Mean Rate
Slope
Freq Thres.
2
R
3.2N
30N
4.2
-0.6
2.1N
0.63

106
TABLE G-16
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #3
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
3.0N
6.3N
3.3N
Freq. Asymptote
33N
13N
-20N
Mean Rate
2.9
4.0
1.1
Slope
-0.58
-1.0
1.32
Freq. Thres.



2
R
0.53
0.64
0.11
Force Velocity
Act. Thres.
lN/s
13N/s
12N/s
Freq. Asymptote
171N/s
179N/S
8N/s
Mean Rate
3.1
2.9
-0.2
Slope
-0.18
-1.2
1.38
Freq. Thres.



/
R
0.38
0.69
0.31
Static Force
Act. Thres.
Freq. Asymptote
Mean Rate
Slope
Freq Thres.
2
R
3.9N
7.9N
4.7
-2.0
2.9N
0.60

107
TABLE G-17
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #4
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
9.5N
6.4N
-3.1N
Freq. Asymptote
52N
50N
-2.0N
Mean Rate
3.2
3.4
0.2
Slope
-0.27
-0.7
0.43
Freq. Thres.



2
R
0.11
0.60
0.49
Force Velocity
Act. Thres.
27N/s
5.0N/S
-22N/s
Freq. Asymptote
333N/S
155N/S
-178N/S
Mean Rate
2.9
3.1
-0.2
Slope
-0.34
-0.25
-0.09
Freq. Thres.



2
R
0.39
0.26
-0.13
Static Force
Act. Thres.
19N
18N
-1.0N
Freq. Asymptote
41N
52N
1 IN
Mean Rate
4.2
3.7
-0.5
Slope
-1.04
-1.5
0.46
Freq Thres.
10.7N
9.0N
-1.7N
2
R
0.50
0.70
0.20

108
TABLE G-18
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #5
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
13.6N
1.4N
-12.2N
Freq. Asymptote
17.9N
8.8N
-9. IN
Mean Rate
4.7
2.5
-2.2
Slope
-4.3
-1.5
-2.8
Freq. Thres.



2
R
0.84
0.28
-0.56

109
TABLE G-19
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #6
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
27 N
ION
-17N
Freq. Asymptote
58N
34N
-24N
Mean Rate
3.5
2.9
-0.6
Slope
-0.88
-0.34
0.54
Freq. Thres.



2
R
0.30
0.28
-0.02
Static Force
Act. Thres.
35N
6.0N
-29N
Freq. Asymptote
41N
48N
7.ON
Mean Rate
7.9
4.6
-3.3
Slope
-1.5
-0.3
-1.2
Freq. Thres.
4.0N
5.ON
1.0N
2
R
0.90
0.38
-0.52

110
TABLE G-20
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #7
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
7.9N
Freq. Asymptote
30N
Mean Rate
4.8
Slope
-1.04
Freq. Thres.


2
R
.
0.58
Movement
Act. Thres.
l.ON/s
Freq. Asymptote
40N/s
Mean Rate
4.6
Slope
-0.32
Freq. Thres.
2

R
0.40
Force Velocity
Act. Thres.
3.IN
Freq. Asymptote
4.3N
Mean Rate
8.3
Slope
-2.7
Freq Thres.
2
3.IN
R
.
0.47

Ill
TABLE G-21
FFFFrT OF S At INF
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #1
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
4.3N
6.4N
2.1N
Freq. Asymptote
26N
35N
9.0N
Mean Rate
2.5
3.2
0.7
Slope
-2.1
-0.74
-1.36
Freq. Thres.



2
R
0.77
0.27
-0.50
Force Velocity
Act. Thres.
7.ON
5.0N/S
-2.0N
Freq. Asymptote
122N
154N/s
13N/s
Mean Rate
2.0
2.6
0.6
Slope
-0.57
-0.21
-0.36
Freq. Thres.



2
R
0.42
0.31
-0.11
Static Force
Act. Thres.
7.IN
2.8N
-4.3N
Freq. Asymptote
27 N
29N
2.0N
Mean Rate
2.9
2.9
0.0
Slope
-1.5
-.72
-0.78
Freq Thres.
7.ON
1.4N
-5.6N
2
R
0.60
0.68
0.08

112
TABLE G-22
FFFFrT OF SAI INF
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #2
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
6.9N
7.ON
0.1N
Freq. Asymptote
48N
46
-2.0N
Mean Rate
3.6
3.5
-0.1
Slope
-0.35
-0.62
0.27
Freq. Thres.



2
R
0.20
0.59
0.39
Static Force
Act. Thres.
20N
11N
-9.0N
Freq. Asymptote
49N
60N
1 IN
Mean Rate
4.0
3.1
-0.9
Slope
-1.4
-0.99
-0.42
Freq. Thres.

9.0N
-5.0N
2
R
0.66
0.52
-0.14
Force Velocity
Act. Thres.
13N/s
Freq. Asymptote
179N/9
Mean Rate
3.3
Slope
-0.4
Freq Thres.
2

R
0.63

113
TABLE G-23
FFFFCT OF SAT INF
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #3
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
13N
15N
2.0N
Freq. Asymptote
49N
28N
-21N
Mean Rate
3.5
3.5
0.0
Slope
-0.74
-0.83
0.09
Freq. Thres.



2
R
0.45
0.28
-0.11
Static Force
Act. Thres.
1 IN
7.ON
-4.0N
Freq. Asymptote
38N
41N
3.0N
Mean Rate
3.75
3.71
-0.04
Slope
-0.53
-0.48
-0.05
Freq. Thres.
8.ON
6.ON
-2.0N
2
R
0.36
0.28
-0.08

114
TABLE G-24
EFFECT OF SALINE
REACTIVITY IN THE VERTICAL PLANE
UNIT #4
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
Freq. Asymptote
Mean Rate
Slope
Freq. Thres.
2
R
5.7N
54N
3.2
-0.55
0.53
Force Velocity
Act. Thres.
11N
Freq. Asymptote
257N
Mean Rate
3.1
Slope
-0.3
Freq. Thres.
2

R
0.51
Movement
Act. Thres.
9.9
Freq. Asymptote
25
Mean Rate
3.9
Slope
-1.5
Freq. Thres.
2

R
0.58
Static Force
Act. Thres.
6.4N
Freq. Asymptote
50N
Mean Rate
3.4
Slope
-0.8
Freq Thres.
3.ON
2
R
0.65
Position
Act. Thres.
Freq. Asymptote
Mean Rate
Slope
Freq Thres.
2
R
15
25
5.6
-0.32
9.0
0.62

115
TABLE G-25
ppppOT OF SAI INF
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #6
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
46N
25N
-21N
Freq. Asymptote
71N
59N
-12N
Mean Rate
5.5
4.2
-1.3
Slope
-1.7
-1.2
-0.05
Freq. Thres.



2
R
0.37
0.43
-0.06

116
TABLE G-26
PPPPPX ("\p CAT TVfp
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #7
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
7.4N
1 IN
3.6N
Freq. Asymptote
59N
68N
9.0N
Mean Rate
3.6
3.8
0.2
Slope
-0.54
-0.27
-0.27
Freq. Thres.



2
R
0.32
0.20
-0.12
Static Force
Act. Thres.
11N
8.6N
-2.4N
Freq. Asymptote
60N
60N
0.0N
Mean Rate
3.3
3.9
0.6
Slope
-1.30
-0.53
-0.77
Freq. Thres.
5.ON
6.0N
1.0N
2
R
0.77
0.60
-0.17

117
TABLE G-27
FFFFrT OF SAT INF
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #8
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
7.0N
5.ON
-2.0N
Freq. Asymptote
48N
56N
8.ON
Mean Rate
3.3
3.2
-0.1
Slope
-0.78
-0.86
0.08
Freq. Thres.



2
R
0.37
0.73
0.36

LIST OF REFERENCES
Abe K and Kawamura Y (1973). A study on inhibition of masseteric a-motor fibre
discharges by mechanical stimulation of the temporomandibular joint in the cat.
Arch Oral Biol 18: 301-304.
Agerberg G (1988). Bite force after temporomandibular joint surgery. Int J Oral
Maxillofac Surg 17: 177-180.
Albright D and Zimny ML (1987). Mechanoreceptors in the human medial meniscus. Anat
Rec (Abstract) 218: 6A-7A.
Andres KH, von Diiring M, Janig W and Schmidt RF (1980). Sensory innervation of the
Achilles tendon by group III and IV afferent fibers. Anat Embryol 172:145-156.
Appenteng K, Lund JP and Sequin JJ (1982). Behavior of cutaneous mechanoreceptors
recorded in mandibular division of gasserian ganglion of the rabbit during
movements of lower jaw. J Neurophysiol 47: 151-166.
Awad EA (1973). Interstitial myofibrositis: Hypothesis of the mechanism. Arch Phys
Med Rehabil 54: 449-453.
Baumann JA (1951). Contribution letude de l'innervation de 1articulation
temporomaxillaire. Compt rend Assoc Anat 38: 120.
Beaudeau DE and Jerge CR (1968). Somatotopic representation into the gasserian
ganglion of tactile peripheral fields in the cat. Arch Oral Biol 131: 247-256.
Beck PW, Handwerker HO and Zimmerman M (1974). Nervous outflow from the cat's
foot during noxious radiant heat stimulation. Brain Res 67: 373-386.
Bell WE (1969). Nonsurgical management of pain-dysfunction syndrome. J Am Dent
Assoc 79: 161-170.
Berberich P, Hoheisel V and Mense S (1988). Effects of a carragenan-induced myositis on
the discharge properties of group III and IV muscle receptors in the cat. J
Neurophysiol 59: 1395-14$).
Bemick S (1962). The vascular and nerve supply to the temporomandibular joint of the
rat. Oral Surg Oral Med Oral Path 15: 488-498.
Bifano CA, Grellner T, Houston G, Farr SC, Ehler WJ, Cissik JH and Chastain M
(1990). Cryogenically preserved adult and juvenile goat mandibular condylar
transplantation. Oral Surg Oral Med Oral Pathol 69: 291-298.
Birrell GJ, McQueen DS, Iggo A, and Grubb BD (1990). The effects of 5-HT on articular
sensory receptors in normal and arthritic rats. Br J Pharmacol 101: 715-721.
118

119
Birrell GJ, McQueen DS, Iggo A and Grubb BD (1991). PGl2-induced activation and
sensitization of articular mechanoreceptors. Neuroscience Letters, 124: 5-8.
Boyd IA (1954). The histological structure of the receptors in the knee joint of the cat
correlated with their physiological response. J Physiol (Lond) 124: 476-488.
Boyd IA and Roberts TDM (1953). Proprioceptive discharges from stretch-receptors in the
knee joint of the cat. J Physiol (Lond) 122: 38-58.
Broekhuijsen ML and van Willigen JD. (1983). Factors influencing jaw position sense in
man. Arch Oral Biol 28: 387-391.
Broton JG and Sessle BJ (1988). Reflex excitation of masticatory muscles induced by
algesic chemicals applied to the temporomandibular joint of the cat. Arch Oral Biol
33: 741-747.
Broton JG, Hu JW and Sessle BJ (1988). Effects of temporomandibular joint stimulation
on nociceptive and nonnociceptive neurons of the cats trigeminal subnucleus
caudalis (Medullary dorsal hom). J Neurophysiol 59: 1575-1589.
Burgess PR and Clark FJ (1969). Characteristics of knee joint receptors in the cat. J
Physiol (Lond) 203: 317-335.
Burgess PR and Perl EF (1967). Myelinated afferent fibers responding specifically to
noxious stimulation of the skin. J Physiol (Lond) 190: 541-562.
Burgess PR, Wei JY, Clark FJ and Simon J (1982). Signaling of kinesthetic information
by peripheral sensory receptors. Ann Rev Neurosci 5: 171-187.
Burke D, Gandevia SC and Macefield G (1988). Responses to passive movement of
receptors in joint, skin and muscle of the human head. J Physiol 402: 347-361.
Caffese RG, Carraro JJ and Albano EA (1973). Influence of temporomandibular joint
receptors on tactile occlusal perception. J Periodont Res 8:400-403.
Campbell JN, Meyer RA and LaMotte RH (1979). Sensitization of myelinated nociceptive
afferents that innervate monkey hand. J Neurophysiol 42: 1669-1679.
Capra HF (1987). Localization and central projections of primary afferent neurons that
innervate the temporomandibular joint in cats. Somatosensory Research 4: 201-
213.
Capra NF and Gatipon GB (1981). Unit activity of trigeminal ganglion neurons recorded
during jaw opening and closing. Society of Neuroscience Abstracts 6: 674.
Carlsson GE and Helkimo M (1972). Funktionell undersokning av tuggapparaten. In:
Holst Nordish klinisk odontologi 8-1-1-21, Forlaget for Faglitteratur, Copenhagen.
Chen TT and Turner DF (1987). Sensory innervation of the temporomandibular joint. J
Dent Res Abstracts 66: 1044.
Christensen LV and Troest T (1975). Clinical kinesthetic experiments on the lateral
pterygoid muscle and temporomandibular joint in man. Scand J Dent Res 83: 238-
244.

120
Christiansen EG (1922). Nogen undersokelser angaaende det naturlige of det kunstige
tandsaets tuggeevhe. Norske Tandlaegeforen Tid 32: 259-288.
Clark FJ (1975). Information signalled by sensory fibers in medial articular nerve. J
Neurophysiol 38: 1461-1472.
Clark FJ and Burgess PR (1975). Slowly adapting receptors in cat knee joint: Can they
signal joint angle? J Neurophysiol 38: 1448-1463.
Clark FJ, Horch KW, Bach SM and Larson GF (1979). Contributions of cutaneous and
joint receptors to static knee-position in man. J Neurophysiol 42: 877-88.
Clark GT, Carter MC and Beemsterboer PL (1984). Bite force to EMG ratio during
various isometric tasks sustained to pain tolerance. Pain (Supplement) 2: 423.
Coggeshall RE, Hong KAP, Langford LA, Schaible H-G and Schmidt RF (1983).
Discharge characteristics of fine medial articular afferents at rest and during passive
movements of inflamed knee joints. Brain Res 272: 185-188.
Cohen LA (1955). Activity of knee joint proprioceptors recorded from the posterior
articular nerve. Yale J Biol Med 28: 225-232.
Cooper B, Ahlquist M, Friedman RM and LaBanc J (1991). Properties of high threshold
mechanoreceptors in goat oral mucosa. II. Dynamic and static reactivity in
carrageenan-inflamed mucosa. J Neurophysiol 66: 1280-1290.
Cooper B, Ahlquist M, Friedman R, Loughner B and Heft M (1990). Mechanical
sensitization of HTMS and its relation to tissue compliance. Society of
Neuroscience Abstracts 16: 720.
Cooper B, Ahlquist M, Friedman R, Loughner B and Heft M (1991). Properties of high
threshold mechanoreceptors in the oral mucosa. I: Responds to dynamic and static
pressure. J Neurophysiol 66: 1272-1279.
Corbin B (1940). Observations in the peripheral distribution of fibers arising in the
mesencephalic nucleus of the fifth cranial nerve. J Comp Neurol 73: 153-177.
Costen JB (1934). Syndrome of ear and sinus symptoms dependent upon disturbed
function of the temporomandibular joint. Ann Otol Rhin Laryng 43: 1-15.
Craig AD and Burton H (1981). Spinal and medullary lamina 1 projection to nucleus
submedius and medial thalamus: a possible pain center. J Neurophysiol 45: 443-
466.
Dahlberg B (1942). The masticatory effect. Acta Med Scand (Supplement) 139: 1-156.
Darian-Smith I, Mutton P and Proctor R (1965). Functional organization of tactile
cutaneous afferents within the semilunar ganglion and trigeminal spiral tract of the
cat. J Neurophysiol 28: 682-694.
Davis DV (1945). Anatomy and physiology of diarthrodial joints. Ann Rheumat Dis 5:

121
Deboever JA (1973). Functional disturbances of the temporomandibular joints. Oral Sri
Rev 1: 100-117.
Dorn T, Schaible H-G and Schmidt RF (1991). Response properties of thick myelinated
group II afferents in the medial articular nerve of normal and inflamed knee joints of
the cat. Som and Mot Res 8: 127-136.
Dostrovsky JO and Broton JG (1985). Antidromic activation of neurons in the medullary
dorsal horn from stimulation in nucleus submedius. Society of Neuroscience
Abstracts 11: 411.
Dostrovsky JO and Guilbaud G (1990). Nociceptive responses in medial thalamus of the
normal and arthritic rat. Pain 40: 93-104.
Dubner R, Sessle BJ and Storey AT (1978). The Neural Basis of Oral and Facial
Function. Plenum, New York, p. 147-174.
Fields HL (1987). Pain. McGraw-Hill, New York, p. 79-99.
Fitzgerald M and Lynn D (1977). The sensitization of high threshold mechanoreceptors
with myelinatde axons by repeated heating. J Physiol (Lond) 265: 549-563.
Foley JO (1960). A quantitative study of the functional components of the facial nerve.
Am J Anat 107: 237-244.
Franks AS (1965). De beheersing van de bewegingen in het koakgewricht. Nederl T
Tandheelk 72: 605.
Freeman MAR and Wyke B (1967). The innervation of the knee joint: An anatomical and
histological study in the cat. J Anat 101: 505-532.
Friedman R, Cooper BY, Ahlquist ML and Loughner BA (1988). Sensitization of high
threshold mechanoreceptors in the oral cavity of the goat. Society of Neuroscience
Abstracts 14: 562.
Frommer J and Monroe CW (1966). The morphology and distribution of nerve fibers and
endings associated with the mandibular joint of the mouse. J Dent Res 45:1762-
1766.
Frost HM (1968). Musculoskeletal pain. In: Facial Pain. CC Ailing (ed), Lea and
Febiger, Philadelphia, p. 153-173.
Garcia-Leme, J (1989). Hormones and Inflammation. CRC Press Inc, Boca Raton,
Florida, p. 61-64.
Gautron M and Guilbaud G (1982). Somatic responses of ventrobasal thalamic neurons in
polyarthritic rats. Brain Res 237: 459-471.
Greenfield BE and Wyke B (1966). Reflex innervation of the temporomandibular joint.
Nature (Lond) 211: 940-941.
Griffin CJ and Harris R (1975). Innervation of the temporomandibular joint. Aust Dent J
20: 78-85.

122
Griffin CJ and Malor R (1974). An analysis of controlled mandibular movement. Monogr
Oral Sci Physiol, Karger, Basel, Vol 4, p. 151-169.
Griffin CJ, Sharpe CJ and Gee E (1965). Inhibition of the linguo-mandibular reflex. I.
Golgi type organs at the pes menisci. Aust Dent J 10: 376-379.
Grigg P (1975). Mechanical factors influencing response of joint afferent neurons from cat
knee. J Neurophysiol 38: 1473-1484.
Grigg P, Finerman GA and Riley LH (1973). Joint-position sense after total hip
replacement. J Bone Joint Surg 55A: 1016-25.
Grigg P and Greenspan BJ (1977). Response of primate joint afferent neurons to
mechanical stimulation of knee joint. J Neurophysiol 40: 1-8.
Grigg P and Hoffman AH (1989). Calibrating joint capsule mechanoreceptors as in vivo
soft tissue load cells. J Biomechanic 22: 781-785.
Grigg P, Hoffman AH and Fogarty KE (1982a). Properties of Golgi-Mazzoni afferents in
cat knee joint capsule, as revealed by mechanical studies of isolated joint capsule. J
Neurophysiol 47: 31-40.
Grigg P, Hoffman AH and Fogarty KE (1982b). Properties of Ruffini afferents revaled by
stress analysis of isolated sections of cat knee capsule. J Neurophysiol 47: 41-57.
Grigg P, Schaible H-G and Schmidt RF (1986). Mechanical sensitivity of Group III and
IV afferents from posterior articular nerve in normal and inflamed cat knee. J
Neurophysiol 55: 635-643.
Grubb BD, Birrell GJ, McQueen DS and Iggo, A (1991). The role of PGE in the
sensitization of mechanoreceptors in normal and inflamed ankle joints of the rat.
Exp Brain Res 84: 383-392.
Grubb BD, McQueen DS, Iggo A, Birrell GJ and Dutia MB (1988). A study of 5-HT-
receptors associated with afferent nerves located in normal and inflamed rat ankle
jonts. Agents and Actions 25: 216-218.
Guerrier Y and Bolonyi F (1948). Linnervation de larticulation temporo-maxillaire. Ann
- doto-laryng 65: 109.
Guilbaud G (1988). Peripheral and central electrophysiological mechanisms of joint and
muscle pain. In: Proceedings of the Vth World Congress on Pain. R Dubner, GF
Gebhart and MR Bond (eds), Elsevier, New York, p. 201-215.
Guilbaud G, Iggo A and Tegner R (1985). Sensory receptors in ankle joint capsules of
normal and arthritic rats. Exp Brain Res 58: 29-40.
Guilbaud G, Peschanski M, Gautron M and Binder D (1980). Neurons responding to
noxious stimulation in VB complex and caudal adjacent regions in the thalamus of
the rat. Pain 8: 303-318.
Hagen-Torn O (1882). Entivicklung und Bau der Synovialmembranen. Arch mikrosk
Anat 21: 591.

123
Hall MB, Parker T, Cherry J and Ballinger WE (1985). Innervation of the bilaminar zone
in human temporomandibular joints. In: Case Reports and Outline, 67th Annual
Meeting and Scientific Sessions. AAOMS, Washington DC, p. 77.
Handwerker HO, Anton and Rech PW (1987). Discharge patterns of afferent cutaneous
nerve fibers from the rat's tail during prolonged noxious mechanical stimulation.
Exp. Brain Res 66: 421-431.
Handwerker HO, Kilo S and Rech PW (1991). Unresponsive afferent nerve fibers in the
sural nerve of the rat. J Physiol 435: 229-242.
He X, Schepelmann K, Schaible H-G and Schmidt RF (1990). Capsaicin inhibits
reponses of fine afferents from the knee joint of the cat to mechanical and chemical
stimuli. Brain Research, 530: 147-150.
Helkimo E, Carlson GE and Carmeli Y (1975). Bite force in patients with functional
disturbances of the masticatory system. J Oral Rehab 2: 397-406.
Helkimo M (1974). Studies of function and dysfunction of the masticatory system. II.
Index for anammestic and clinical dysfunctiona and occlusal state. Sved Dent J 67:
101-121.
Helkimo M (1979). Epidemiological surveys of dysfunction of the masticatory system.
In: Temporomandibular Joint Function and Dysfunction. GA Zarb and C
Carlsson (eds) Mosby, St. Louis, p. 175.
Henry ML, Johnson L, Mahan PE and Westrum L (1986). Somatotopic organization of
dental structures within the feline V ganglion. J Dent Res (Suppl) 64: 210.
Heppelman B, Herbert MK, Schaible H-G and Schmidt RG (1987). Morphological and
physiological characteristics of the innervation of cat's normal and arthritic knee
joint. In: Effects of Injury on Trigeminal and Spinal Somatosensory Systems. LM
Pubols and BJ Sessle (eds). Alan Liss Inc, New York, p. 19-27.
Heppleman B, Schaible H-G and Schmidt RF (1985). Effects of prostaglandins Ei and E2
on the mechanosensitivity of group III afferents from normal and inflamed cat knee
joints. In: Advances in Pain Research and Therapy. HF Fields, R Dubner and F
Cervero (eds), Raven Press, New York, p. 91-101.
Hilton J (1879). In: Jacobson WHA. Rest and pain. Butterworth and Company, New
York, p. 96.
Hoffman AH and Grigg P (1989). Measurement of joint capsule tissue loading in the cat
knee using calibrated mechanoreceptors. J Biomechanics 22: 787-791.
Hromada J (1960). Beitrag zur Kenutnis der Entwicklung und der Variabilitat der
Lamellenkorperchen in der Gelenkkapsel und im periartikulren Gewebe beim
meschlichen Fetus. Acta Anat 40: 27-40.
Ishibashi K (1966). Studies in innervation of human mandibular joint. Jap J Oral Biol 8:
46-57.
Ishibashi K (1974). Innervation of human temporomandibular joint in adult. Bull Tokyo
Med Dent Univ 21 (Suppl): 86-88.

124
Jerge CR (1964). The neurologic mechanism underlying cyclic jaw movements. J Prosth
Dent 14: 667-681.
Kanaka R, Schaible H-G and Schmidt RF (1985). Activation of fine articular afferent units
by bradykinin. Brain Res 327: 81-90.
Kawamura Y (1980). Neurophysiology. In: The Temporomandibular Joint. A Biological
Basis for Clinical Practice. BG Sarnat and DM Laskin (eds), Charles Thomas,
Springfield, Illinois, p. 114-126.
Kawamura Y and Abe K (1974). Role of sensory information from temporomandibular
joint. Bull Tokyo Med Dent Univ 21 (Suppl) 78-82.
Kawamura Y and MajimaT (1964). Temporomandibular joint's sensory mechanisms
controlling activities of jaw muscles. J Dent Res 43: 150.
Kawamura Y, Majima T and Kato I (1967). Physiological role of deep mechanoreceptors
in temporomandibular joint capsule. J Osaka Univ Dent Sch 7: 63-76.
Kayser V and Guilbaud G (1984). Further evidence for changes in the responsiveness of
somatosensory neurons in arthritic rats: a study in the posterior intralaminar region
of the thalmus. Brain Res 323: 144-147.
Keller JH and Moffet BC (1968). Nerve endings in the temporomandibular joint of the
rhesus macaque. Anat Rec 160: 587-594.
Kerr FWL (1962). Correlated light and electron microscopic observations on the normal
trigeminal gangion and sensory root in man. J Neurosurg (Suppl) 26: 132-137.
Kerr FWL and Lysak WR (1964). Somatotopic organization of trigeminal ganglion
neurons. Arch Neurol 11: 593-602.
Kitamura H (1974). Development of the Temporomandibular Joint Innervation. Bull
Tokyo Med Dent Univ 21 (Suppl): 83-85.
Klineberg I (1971). Structure and function of temporomandibular joint innervation. Am
Roy Coll Surg 49: 268-288.
Klineberg I (1980). Influence of temporomandibular articular mechanoreceptors on
functional jaw movements. J Oral Rehab 7: 307-317.
Klineberg I, Greenfield BE and Wyke BD (1970). Afferent discharges from
temporomandibular articular mechanoreceptors. Arch Oral Biol 15: 935-952.
Klineberg I, Greenfield BE and Wyke BD (1971). Afferent from discharges from
temporomandibular articular mechanoreceptors: an experimental analysis of their
behavorial characteristics in the cat. Arch Oral Biol 16: 1463-1479.
Kojima Y (1990). Convergence patterns of afferent information from the
temporomandibular joint and masseter muscle in the trigeminal subnucleus caudalis.
Brain Research Bulletin 24: 609-616.

125
Kreutziger KL and Mahan PE (1975). Temporomandibular degenerative joint disease.
Part I. Anatomy, pathophysiology and clinical description. Oral Surg Oral Med
Oral Pathol 40: 165-182.
Lamour Y, Guilbaud G and Wilier JC (1983). Altered properties and laminar distribution
of neuronal responses to peripheral stimulation in the Sm I cortex of the arthritic rat.
Brain Res 273: 183-187.
Larsson LE and Thilander B (1964). Mandibular positioning. The effect of pressure on the
joint capsule. Acta Neurol Scand 40: 131-143.
Lemke R, Dolwick MF, Hogan B and Rugh JO (1987). Masticatory efficiency of post-
TMJ surgery patients. LADR Abstracts 66:118.
Li JCR (1969). Statistical Inference. Edwards Brothers, Ann Arbor, Michigan.
Limwongee V (1986). Cell body location of trigeminal sensory neuron innervating the
temporomandibular joint in rat, cat and monkey. Society of Neuroscience Abtracts
12: 333.
Loos S (1963). A simple test of masticatory function. Int Dent J 13: 615-616.
Loughner B, Larkin LH and Mahan PE (1990). Nerve entrapment in the lateral pterygoid
muscle. Oral Surg Oral Med Oral Path 69: 299-306.
Lund JP and Matthews B (1981). Responses of temporomandibular joint afferents
recorded in the gasserion ganglion of the rabbit to passive movements of the
mandible. In: Oral-Facial Sensory and Motor Functions. Y Kawamura and R
Dubner (eds), Quintessence, Chicago, p. 153-160.
Macefield G, Gandevia SC and Burke D (1990). Perceptual responses to microstimulation
of single afferents innervating joints, muscles and skin of the human hand. J
Physiol 429: 113-129.
Mahan PE and Ailing CC (1991). Facial Pain. 3rd edition Lea and Febiger, Philadelphia.
Manly RS and Braley LC (1950). Masticatory Performance and Efficiency. J Dent Res
29: 448-462.
Marfurt CF (1981). The somatotopic organization of the cat trigeminal ganglia as
determined by the horseradish peroxidase technique. Anat Rec 201: 105-118.
McCall WD, Farias MC, Williams WJ and Bement SL (1974). Static and dynamic
responses of slowly adapting joint receptors. Brain Res 70: 221-243.
McQueen DS, Iggo A, Birrell GJ and Grubb BD (1991). Effects of paracentamol and
aspirin on neural activity of joint mechanoreceptors in adjuvant arthritis. Br J
Pharmacol 104: 178-182.
Mense S and Schmidt RF (1974). Activation of group IV afferent units from muscle by
algesic agents. Brain Res 72: 305-310.

126
Morimoto T and Kawamura Y. (1978). Interdental thickness discrimination and position
sense of the mandible. In: Oral Physiology and Occlusion. JH Perryman (ed),
Pergaman, New York, p. 149-169.
Neugebauer V and Schaible H-G (1990). Evidence for a central component in the
sensitization of spinal neurons with joint input during development of acute arthritis
in cats knee. J Neurophysiol 64: 299-311.
Okeson JP (1989). Management of temporomandibular disorders and occlusion. 2nd
edition,Mosby, St Louis, p. 87-104.
Olson A (1969). Temporomandibular joint function and functional disturbances. Dent
Clinics North Am 13: 643-648.
Polacek P (1966). Receptors of the joints: Their structure, variability and classification.
Acta Facultat Med Universitat Brunensis 23: 1-107.
Posselt U and Thilander B (1965). Influence of the innervation of the temporo-mandibular
capsule on mandibular border movements. Acta Odont Scand 23: 601-613.
Posselt V (1968). Physiology of occlusion and rehabilitation. 2nd edition, Blackwell,
Oxford.
Ransjo K and Thilander B. (1963). Perception of mandibular position in cases of
temporomandibular joint disorders. Odontolgiska Foreningens Tidskrift 71: 134-
144.
Reeh PW, Bayer L, Kocher L and Handwerker HO (1987). Sensitization of nociceptive
cutaneous nerve fibers from the rat's tail by noxious mechanical stimulation. Exp
Brain Res 65: 505-512.
Rocabado M (1983). Arthrokinematics of the temporomandibular joint. Dent Clin North
Am 27: 573-594.
Rominger JW and Rugh JD (1986). Comparison of masticatory performance of TMJ
dysfunction subjects and controls. J Dent Res 29: 448-462.
Romfh JH, Capra NF and Gatipon GB (1979). The trigeminal nerve and the
temporomandibular joint of the cat: a horseradish peroxidase study. Exp Neurol
65: 99-106.
Rose JE and Mountcastle VB (1959). Touch and kinesthesia. In: Handbook of Physiology.
J Field (ed), Amer Physiol Soc, Wash DC, vol 1, p. 387-429.
Rossi A and Grigg P (1982). Characteristics of hip joint mechanoreceptors in the cat. J
Neurophysiol 27: 573-594.
Rossie F (1950). Sur linnervation fine de la capsule articularie. Acta Anat 10: 161-232.
RiidingerN (1857). Die Gelenknerven des menschlichen. Korpers, Erlangen.
Samuel EP (1952). The autonomic and somatic innervation of the articular capsule. Anat
Rec 113:53-70.

127
Schaible HG (1983). Sensitization by prostaglandin E¡. Naunyn-Schmiedebergs Arch
Pharmacol (Suppl) 352: R98.
Schaible HG and Schmidt RF (1983a). Activation of groups III and IV sensory units in
medial articular nerve by local mechanical stimulation of knee joint. J Neurophysiol
49: 35-44.
Schaible HG and Schmidt RF (1983b). Responses of fine medial articular nerve afferents
to passive movement of knee joint. J Neurophysiol 49: 1118-1126.
Schaible HG and Schmidt RF (1984). Mechanosensibility of joint receptors with fine
afferent fibers. Exp Brain Res (Suppl 9), p. 284-297.
Schaible HG and Schmidt RF (1985). Effects of an experimental arthritis in the sensory
properties of fine articular afferent units. J Neurophys 54: 1109-1122.
Schaible HG, Schmidt RF and Willis WD (1986). Responses of spinal cord neurons to
stimulation of articular afferent fibers in the cat. J Physiol 372: 575-593.
Schaible HG and Schmidt RF (1988a). Excitation and sensitization of fine articular
afferents from cat's knee joint by prostaglandin E2. J Physiol 403: 91-104.
Schaible HG and Schmidt RF (1988b). Direct observations of the sensitization of articular
afferents during an experimental arthritis. In: Proceedings of the Vth World
Congress of Pain. R Dubner, GF Gebhart, MR Bond (eds), Elsevier, New York,
p. 44-50.
Schellhas KP, Wilkes CH and Baker CC (1989). Facial pain, headache and
temporomandibular joint inflammation. Headache 29: 228-231.
Schmid F (1969). On the nerve distribution of the temporomandibular joint capsule. Oral
Surg Oral Med Oral Path 28: 63-65.
Sessle BJ and Greenwood IF (1976). Inputs to trigeminal brainstem neurons from facial,
oral, tooth, and pharyngolaryngeal tissues. I. Responses to innocuous and
noxious stimuli. Brain Res 117: 211-226.
Sicher H (1955). Structural and functional basis for disorders of the temporomandibular
articulation. J Oral Surg 13: 275-279.
Sicher H (1960). Oral anatomy. 3rd edition, Mosby, St. Louis, p. 166-168.
Siirila HA and Laine P (1972). Sensory thresholds in discriminating differences in
thickness between the teeth by different degrees of mouth opening. Proc Finn Dent
Soc 68: 134-139.
Sheikoleham A, Mller E and Lous I (1982). Postural and maximal activity in elevators of
mandible before and after treatment of functional disorders. Scand J Dent Res 90:
37-46.
Sherrington CS (1947). The Integrative Action of the Nervous System. Yale Univesity
Press, New Haven, Connecticut p. 228.

128
Skoglund S (1956). Anatomical and physiological studies of knee joint innervation in the
cat. Acta Physiol Scand (Supplement 36) 124: 1-101.
Skoglund S. (1973). Joint receptors and kinaesthesis. In: Handbook of Sensory
Physiology. A Iggo (ed), Vol II, Somatosensory System. Springer-Verlag, Berlin,
p. 111-136.
Solberg, WK (1987). Epidemiological findings of importance to management of
temporomandibular disorders. In: Perspectives in Temporomandibular Disorders.
GT Clark and WK Solbert (eds). Quintessence Publishing Co, Chicago, p. 27-44.
ThilanderB (1961). Innervation of temporomandibular joint capsule in man. Trans R
School Dent Umea 2: 1-67.
Travell J (1976). Myofascial trigger points: clinical view. In: Advances in Pain Research
and Therapy. JJ Bonica and D Albe-Fessard (eds), Raven, New York, p. 919-
926.
Turnbull WD (1970). Mammalian masticatory apparatus. Fieldiana. Geology. Vol 18,
No 2 (Field Museum of Natural History, Chicago).
van den Berghe L, de Boever JA, Brockhuijsen ML and van Willigen JD (1987). On the
perception of the preferred jaw position in patients with symptoms of
temporomandibular disorders. J Craniomand Pract 5: 344-350.
van Willigen JD, Broekhuijsen ML, de Bont LGM and van der Kuijl B (1986). On the
perception of jaw position and bite force by subjects with craniomandibular
disorders. J Craniomand Pract 4: 128-133.
Vinegar R, Truax JF, Selph JH, Johnston PR, Venable AL and McKenzie KK (1987).
Pathway to carrageenan-induced inflammation in the hind limb of the rat.
Federation Proc 46: 118-126.
Weinmann JP and Sicher H (1951). Histophysiology of the temporomandibular jont. In:
The Temporomandibular Joint. BG Samat (ed), Thomas, Springfield, p. 71-75.
Widenfalk B and Wiberg M (1990). Origin of sympathetic and sensory innervation of the
temporo-mandibular joint. A retrograde axonal tracing study in the rat.
Neuroscience Letters 109: 30-35.
Williams WN, Henry MA and Mahan PE (1989). The effect of experimental anesthetization
of temporomandibular joint superior cavity on bite force discrimination. J
Craniomand Pract 7: 194-199.
Williams WN, LaPointe LL, Mahan PE and Cornell CE (1984). The influence of TMJ and
central incisors impairment on bite force discrimination. J Craniomand Pract 2: 119-
124.
Willis WD and Coggeshall RE (1978). Sensory Mechanisms of the Spinal Cord. Chapter
2. Plenum Press, New York, p. 9-51.
Yemm R (1979). Neurophysiologic studies of temporomandibular joint dysfunction. In:
Temporomandibular Joint Function and Dysfunction. GA Zarb and CE Carlsson
(eds), Mosby, St Louis, p. 215-237.

129
Zarb GA and Carlsson GE (1988). Examination and differential diagnosis of occlusal
problems. In: A Textbook of Occlusion. HD Mohl, GA Zarb, GE Carlsson and
JO Rugh (eds), Quintessence, Chicago, p. 185-207.
Zeller J, Wussbarth E, Baruth B, Mielke H and Deicher H (1983). Serotonin content of
platelets in inflammatory rheumatic diseases. Correlation with clinical activity.
Arthritis Rheum 26: 532-540.
Zimny ML (1988). Mechanoreceptors in articular tissue. Am J Anat 182: 16-32.
Zimny ML and St. Onge M (1987). Mechanoreceptors in the temporomandibular articular
disk. J Dent Res 66: 237.
Zucker E and Welker WI (1969). Coding of somata sensory input by vibrissae neurons in
the rats trigeminal ganglion. Brain Res 12: 138-156.

BIOGRAPHICAL SKETCH
I was bom on December 13, 1943, in Greensburg, Pennsylvania. I attended
Pennsylvania State University between 1961 and 1965 where I received a Bachelor of
Science degree in biochemistry. I attended New York University between 1965 and 1969
where I received a Doctor of Dental Surgery degree in dentistry. In 1985 and 1986, I
attended the University of Florida as a postgraduate fellow in the Facial Pain Center of the
dental school. I received a Masters of Anatomy degree in the Department of Anatomy and
Cell Biology, University of Florida between 1986 and 1987. I pursued a Doctor of
Philosophy degree in the Department of Oral Biology, University of Florida, between 1987
and 1992, and will graduate in May, 1992.
130

I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
Parker MahanfChairman
Distinguished Service Professor
of Oral Biology
I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
Brian Cooper, Cochairman
Assistant Professor of Neuroscience
I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a;
dissertation for the degree of Doctor of Philosophy.
'Charles Viei
Professor

I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
This dissertation was submitted to the Graduate Faculty of the College of Medicine
and to the Graduate School and was accepted as partial fulfillment of the requirements for
the degree of Doctor of Philosophy.
May 1992
Dean, College of Medicine
Dean, Graduate School

UNIVERSITY OF FLORIDA
3 1262 08554 7213



98
TABLE G-8
TMJ NOCICEPTOR REACTIVITY
IN ACUTELY INFLAMED TISSUE
Test Conditions
with RF (n=ll)
code (n=9)
acquired coding (n=8)
Dynamic Force
9
2
Force Velocity
4
4
Movement
2
0
Static Force
4
5
Position
1
1
Conduction
Velocity
0.8 to 6.0
m/sec
(n=6)

Post-test
Spontaneous
Activity

6


24
TMJ FORCE/MOVEMENT RELATIONSHIPS: VERTICAL PLANE
Figure 3.3. (contd)


108
TABLE G-18
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #5
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
13.6N
1.4N
-12.2N
Freq. Asymptote
17.9N
8.8N
-9. IN
Mean Rate
4.7
2.5
-2.2
Slope
-4.3
-1.5
-2.8
Freq. Thres.



2
R
0.84
0.28
-0.56


Figure 3-3. Relationships between applied force and vertical plane movements of the
mandible. Ten biphasic curves indicated that low forces were sufficient to
open the jaw through most of its range of motion. High forces produce
minimal degrees of opening where the joint encounters considerable
resistance from soft tissue. In each case, the TMJ nociceptor begins to
respond at the point indicated by the arrow.


50
Of the 9 units exhibiting rotation, 4 also shifted. It was possible that shift was a more
mature form of sensitization that followed rotation. In units which were examined over
several hours, 2 of 2 units that exhibited rotations subsequently manifested shifts of their
scatter plot field (See Figure 3-9).
Control tests indicted that qualitative changes could also be observed after saline
injection. In 1 of 8 cases, a qualitative improvement was observed in dynamic coding
capacity (Table 3-5). Thus, improved dynamic reactivity is possible as the result of saline
injection. However, the tendency towards acquired coding appeared to be greater for
carrageenan-induced inflammation (8 of 11 cases).
In summary, experiments were performed to characterize the response properties of
presumed nociceptors in normal and inflamed capsular tissue of the TMJ. Most TMJ
afferents preferred either movement in the horizontal or vertical plane. Their reactivity
functions were best described by power functions fit between dynamic force, force velocity
and response interval. In normal tissue, TMJ afferents had properties of nociceptors, in
that the activation threshold was at the extreme range of jaw movement, either in the
exponential portion or in the transition zone between the linear and exponential force-
movement curves that described jaw movement. It was predicted that TMJ nociceptors
would sensitize following exposure to carrageenan. To test this, populations of afferents
were sampled in previouslyly inflamed tissue and their responses compared to those of
afferent populations in normal tissue. Improved reactivity was observed, especially
reactivity to dynamic stimuli (dynamic force and force velocity). To avoid sampling errors
that could have biased these observations, units were characterized in acutely inflamed
tissue after being characterized in normal tissue. These afferents manifested similar
quantitative improvements in dynamic reactivity. Additionally, qualitative improvements of
coding capacity were observed. Acquisition of coding capacity following acute
inflammation suggested afferent sensitization.


G SUMMARY TABLES OF TMJ REACTIVITY 90
LIST OF REFERENCES 118
BIOGRAPHICAL SKETCH 130
v


120
Christiansen EG (1922). Nogen undersokelser angaaende det naturlige of det kunstige
tandsaets tuggeevhe. Norske Tandlaegeforen Tid 32: 259-288.
Clark FJ (1975). Information signalled by sensory fibers in medial articular nerve. J
Neurophysiol 38: 1461-1472.
Clark FJ and Burgess PR (1975). Slowly adapting receptors in cat knee joint: Can they
signal joint angle? J Neurophysiol 38: 1448-1463.
Clark FJ, Horch KW, Bach SM and Larson GF (1979). Contributions of cutaneous and
joint receptors to static knee-position in man. J Neurophysiol 42: 877-88.
Clark GT, Carter MC and Beemsterboer PL (1984). Bite force to EMG ratio during
various isometric tasks sustained to pain tolerance. Pain (Supplement) 2: 423.
Coggeshall RE, Hong KAP, Langford LA, Schaible H-G and Schmidt RF (1983).
Discharge characteristics of fine medial articular afferents at rest and during passive
movements of inflamed knee joints. Brain Res 272: 185-188.
Cohen LA (1955). Activity of knee joint proprioceptors recorded from the posterior
articular nerve. Yale J Biol Med 28: 225-232.
Cooper B, Ahlquist M, Friedman RM and LaBanc J (1991). Properties of high threshold
mechanoreceptors in goat oral mucosa. II. Dynamic and static reactivity in
carrageenan-inflamed mucosa. J Neurophysiol 66: 1280-1290.
Cooper B, Ahlquist M, Friedman R, Loughner B and Heft M (1990). Mechanical
sensitization of HTMS and its relation to tissue compliance. Society of
Neuroscience Abstracts 16: 720.
Cooper B, Ahlquist M, Friedman R, Loughner B and Heft M (1991). Properties of high
threshold mechanoreceptors in the oral mucosa. I: Responds to dynamic and static
pressure. J Neurophysiol 66: 1272-1279.
Corbin B (1940). Observations in the peripheral distribution of fibers arising in the
mesencephalic nucleus of the fifth cranial nerve. J Comp Neurol 73: 153-177.
Costen JB (1934). Syndrome of ear and sinus symptoms dependent upon disturbed
function of the temporomandibular joint. Ann Otol Rhin Laryng 43: 1-15.
Craig AD and Burton H (1981). Spinal and medullary lamina 1 projection to nucleus
submedius and medial thalamus: a possible pain center. J Neurophysiol 45: 443-
466.
Dahlberg B (1942). The masticatory effect. Acta Med Scand (Supplement) 139: 1-156.
Darian-Smith I, Mutton P and Proctor R (1965). Functional organization of tactile
cutaneous afferents within the semilunar ganglion and trigeminal spiral tract of the
cat. J Neurophysiol 28: 682-694.
Davis DV (1945). Anatomy and physiology of diarthrodial joints. Ann Rheumat Dis 5:


APPENDIX E
TRIGEMINAL GANGLION
The trigeminal ganglion is situated near the apex of the petrous bone in the middle
cranial fossa. It lies in Meckel's cave near the cavernous sinus and internal carotid artery.
The sensory root (portio major) enters the pons in association with the motor root (portio
minor), which courses dorsomedially, and terminates in the trigeminal nuclear complex.
Sensory input from the face enters the trigeminal ganglion via the opthalamic,
maxillary and mandibular division of the trigeminal nerve. The cell bodies of these afferent
fibers are segregated into discrete clusters (Jerge, 1964; Kerr, 1962).
Retrograph transport of HRP injected into the cat TMJ showed that sensory
neurons originate in the trigeminal ganglion (Romfh et al., 1979; Capra, 1987). Whether
all of the cell bodies of afferent neurons innervating the TMJ are located in the trigeminal
ganglion remains unanswered. There is evidence suggesting that the peripheral spinal
neurons innervate the TMJ. Widenfalk and Wiberg (1990) injected HRP into the TMJ of
rats. Labeled cells were observed ipsilaterally in the second to fifth dorsal root ganglion.
In addition, there is evidence suggesting that the mesencephalic nucleus contains cell bodies
of neurons that terminate in the TMJ. In a preliminary communication, Limwongee (1986)
reported injection of HRP into the TMJ of rat, cat and monkey. He found labeled neurons
in the mesencephalic nucleus at the level of the caudal pons. On the other hand, Corbin
(1940) ablated the mesencephalic nucleus and examined histologically the auriculotemporal
nerve. He found no degenerated fibers. In addition, Chen and Turner (1987) injected
84


21
Therefore, relationships between applied force and jaw movement were examined to
determine the noxious range and compare it with afferent discharge properties.
Due to physical constraints of the preparation, force-movement relationships could
only be examined for VP units. Characterization of force-movement relationships in the
vertical plane revealed a biphasic relationship between applied force and mandibular
movement (Figure 3-3). Linear force-movement relationships gave way to exponential
force-movement relationships when the mandible reached an extreme of opening. It is
likely that this exponential phase corresponds to the noxious range. Force-movement
curves of VP units (n = 10) were best described by power functions (Table 3-1). Power
functions were the best fit in 10 of 10 cases (R2 = 0.92 0.06). The functional range of
VP units may be graphically assessed by observing activation thresholds plotted on force-
movement curves. As can be seen in Figure 3-3, nearly all afferents began to respond in
the transition zone between the linear and exponential phases of the curves. This can be
examined statistically by examining the functions fit below the point of activation. For the
10 cases in which power functions were fit, activation threshold occurred during portions
of the curves which were exponentially accelerating (6/10 cases, R2 = 0.86 + 0.17). In 4
cases, activation thresholds occurred in portions of the curve in which force was increasing
linearly (R2 = 0.88 0.19). The activation thesholds of these 4 units occurred at forces
approaching the power phase of the curve. The observed preference for high forces (mean
activation threshold for force = 20.6 11.0 N; mean frequency asymptote = 49.6 + 20.7
N) at extremes of the range of motion (mean activation threshold at 13.7 5.4; mean
frequency asymptote = 20.4 5.9) suggested that these TMJ afferents were nociceptors.
Characterization of TMJ Nociceptors in Normal Tissue
Units were classified according to their preferred movement plane. Preferred
movement was defined as that plane of motion in which mandibular excursion evokes the


A
POST
B
MED


BIOGRAPHICAL SKETCH
I was bom on December 13, 1943, in Greensburg, Pennsylvania. I attended
Pennsylvania State University between 1961 and 1965 where I received a Bachelor of
Science degree in biochemistry. I attended New York University between 1965 and 1969
where I received a Doctor of Dental Surgery degree in dentistry. In 1985 and 1986, I
attended the University of Florida as a postgraduate fellow in the Facial Pain Center of the
dental school. I received a Masters of Anatomy degree in the Department of Anatomy and
Cell Biology, University of Florida between 1986 and 1987. I pursued a Doctor of
Philosophy degree in the Department of Oral Biology, University of Florida, between 1987
and 1992, and will graduate in May, 1992.
130


TABLE 3-3. Mean values of properties of TMJ nociceptors.
A. NORMAL TISSUE
Test
n
Slope
Intercept
Act.
Thres.
Freq.
Asym.
Freg.
Thres.
2
R
MRI
DF
23
-1.2 + 0.9
7.3 3.1
15.9 11.3
47.0 31.5
0.42 0.22
3.71.4
FV
15
-0.4 + 0.3
4.8 1.4
17.3 18.9
156.5 83.0
0.30 0.18
3.11.1
M
5
-4.2 + 2.4
14.0 6.7
10.8 3.6
16.0 7.5
0.49 0.23
9.94.8
SF
8
-1.6 + 1.5
5.9 2.4
17.7 18.3
42.5 26.5
7.9 + 7.9
0.75 0.23
3.6 1.5
P
1
-5.8
17
10
16
10
0.73
6.6
B. PREVIOUSLY INFLAMED TISSUE
Test
n
Slope
Intercept
Act.
Thres.
Freq.
Asym.
Freg.
Thres.
2
R
MRI
DF
6
-1.1 +0.5
5.42.4
7.6 10.2
33.3 32-1
0.24 0.16
3.50.9
FV
6
-0.7 +0.8
3.50.8
4.8 4.5
40.2 22-2

0.33 0.78
2.2 1.3
M
1
-6.6
24
17
20

0.46
17
SF
2
-1.3 +0.9
7.92.3
6.5 3.6
25.5 9-2
6.1 + 4.3
0.36 0.11
4.1 0.6
P
1
-2.0
10.0
10
17
7
0.42
6.1
C. A or
fELY INFLAMED 1
"ISSUE
Test
Cond
n
Slope
Intercept
Act.
Thres.
Freq.
Asym.
Freg.
Thres.
2
R
MRI
DF
Pre
9
-1.3 +1.4
7.4
4.1
12.9 + 9.0
41.4 +
13.3
0.43 0.23
4.3 +
2.1
DF
Post
9
-0.9 +0.6
5.5
1.4
11.4 +13.5
41.3
24.9
0.38 0.20
3.2 +
0.5
FV
Pre
2
-0.2 +0.06
4.4
0.5'
14.0 + 18.4
252.0 114.6
#
0.39 0.07
3.0 +
0.1
FV
Post
2
-0.7 +0.7
5.6
3.3
9.0 + 5.7
167.0 +
16.9
0.48 0.30
3.0 +
0.1
M
Pre
3
-3.3 +3.3
13.8
9.9
15.7 + 6.8
26.3 +
2.5
#
0.40 0.08
7.8 +
5.4
M
Post
3
-4.0 +3.4
15.8
10.7
19.3 + 7.2
24.5 +
4.1
0.58 0.36
11.1 +
9.5
SF
Pre
3
-1.0 +0.6
7.4
2.0
20.3 + 14.0
33.0 +
13.9
8.2+ 3.7
0.54 0.34
5.5 +
2.1
SF
Post
3
-0.8 +0.6
6.4
2.2
8.5 + 8.4
43.3 +
11.7
5.2+ 3.7
0.58 0.15
4.5 +
0.7
P
Pre
1
-1.1
7.1
10.5
16
10
0.35
5.2
P
Post
1
-1.2
6.8
3.4
22
2.7
0.79
3.3


APPENDIX B
PSYCHOPHYSICS OF TMJ DISORDERS
Pain and mandibular dysfunction are two-common manifestations of TMJ
disorders. Pain can occur when the mandible is at rest or during function. Disordered
movement of the mandible is a sign of mandibular dysfunction (i.e. the inability to
masticate properly). Patients suffering from TMJ disorders often complain of pain while
chewing. Whether mandibular dysfuntion is directly or indirectly due to TMJ disorder or
due uniquely to pain that results from jaw movement is unclear.
Chewing efficiency, jaw movement, biting force and perception of jaw position are
quantifiable features of mastication. A review of the literature reveals studies which have
been directed at investigating the relationship betwen TMJ disorders and mastication.
There has been little psychophysical experimentation involved in quantifying pain
associated with mandibular dysfunction. Even though most of these studies pertain to
treatment efficacy, understanding the relationship between TMJ disorders and mastication
may be valuable in understanding the relationship between pain and TMJ disorders.
Chewing Efficiency
Typically, the clinical appraisal of individuals chewing efficiency is limited to a
subjective report provided by the patient. Early investigators (Christiansen, 1922;
Dahlberg, 1942) developed the technique of using a series of sieves with different mesh
sizes and test materials for chewing in order to estimate chewing efficiency. A simple
67


100
TABLE G-10
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE VERTICAL PLANE
UNIT#1
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
12N
1.7N
-10.3N
Freq. Asymptote
50N
69N
19N
Mean Rate
3.4
2.7
-0.7
Slope
-0.44
-0.19
-0.25
Freq. Thres.



2
R
0.18
0.44
0.26
Static Force
Act. Thres.
7N
1.6
-5.4N
Freq. Asymptote
17N
30N
13N
Mean Rate
4.5
5.1
0.6
Slope
-0.4
-0.68
-0.28
Freq. Thres.
10N
1.6N
-8.4N
2
R
0.23
0.60
0.42
Position
Act. Thres.
10.5
3.4
-7.1
Freq. Asymptote
16
22
ON
b
o
Mean Rate
5.2
3.3
-1.5
Slope
-1.1
-1.2
-0.1
Freq. Thres.
10.0
2.7
-7.3
2
R
0.35
0.79
0.44
Movement
Act. Thres.
9.8
6.2
-3.6
Freq. Asymptote
14
25
11
Mean Rate
7.3
3.13
-4.13
Slope
-4.0
-0.5
3.5
Freq Thres.



i
R
0.6
0.47
-0.13
Force Velocity
Act. Thres.
2.0 N/s
Freq. Asymptote
317 N/s
Mean Rate
2.8
Slope
-0.11
Freq Thres.
2
-
R
0.35


APPENDIX A
DEVELOPMENT AND MAINTENANCE OF TMJ PAIN
Many theories have been advanced to account for the production of TMJ pains.
(For reviews, see Deboever, 1973; Dubner et al., 1978, Yemm, 1979). TMJ dysfunction
may account not only for pain in the joint itself, but also for pain arising from associated
facial structures.
Intra-articular Origins of TMJ Pain
1) Pressure Theory
Pressure theories have been the most prevalent explanations for the production of
TMJ pain. These theories suggest that disruption of the normal articular mechanics may
impose abnormal pressures on structures of the TMJ. Costen (1934) postulated that facial
pain associated with the TMJ was a consequence of pressure on the auriculotemporal nerve
brought about by impaction of the condyle against the tympanic plate. Anatomically, this
theory is untenable since the auriculotemporal nerve ramifies before reaching the TMJ. The
articular branches of the auriculotemporal nerve arise at the medialposterior aspect of the
neck of the condyle and ascend into the soft tissue of the joint inferior to the tympanic plate.
The auriculotemporal nerve is vulnerable to pressure at its proximal course. The
auriculotemporal nerve arises from the posterior trunk of the mandibular nerve along the
medial surface of the lower belly of the lateral pterygoid muscle. Entrapment of the
auriculotemporal nerve in the lateral pterygoid muscle has been demonstrated in 5% of
60


39
induced inflammation (acutely inflamed or AI). Outcomes of experiments using PI
methods suggested that individually characterized afferents would manifiest improved
dynamic reactivity.
Observations of quantitative shifts in force interval functions were confirmed, and
additional qualitative changes were observed. Eleven units were characterized in normal
tissue and then retested 1-3 h after exposure to carrageenan. Four units responded
preferentially to VP jaw movement and 7 responded best to HP movement. For 9 units that
transduced stimulus intensity in both normal and inflamed tissue, 6 demonstrated enhanced
reactivity for dynamic force (Figure 3-7). Four of these 6 units had post-inflammatory
functions that shifted below the pre-inflammatory function. One of these also showed
leftward shift. Three of 6 units that demonstrated enhanced dynamic force reactivity
showed a leftward function shift relative to pre-inflammatory functions but failed to shift
below the control case. Mean function characteristics for these nociceptors are presented in
Table 3-3.
Experiments were performed to determine whether changes in AI reactivity
occurred as a result of carrageenan or other causes, such as repeated stimulation. In these
control experiments, saline (100 |il) was injected into the area of the RF and into the TMJ
capsule. Reactivity was examined in 8 units after exposure to saline. Five of 8 units
transduced dynamic force in both the pre- and post-saline conditions. While quantitative
changes in reactivity were small following saline injections, there was some indication that
repeated testing could produce qualitative changes in reactivity similar to those observed
following carrageenan injection (See Figure 3-8).
Following saline injection, mean activation threshold was reduced from 14.1 +
15.0 N in pre-saline condition to 11.5 7.5 N These changes were relatively small
compared to changes observed following carrageenan (11.2 + 9.9 to 5.1 + 3.7 N).
Statistical comparisons indicated that the mean changes in activation threshold was
significantly less in saline than carrageenan treated cases (T = -2.2; DF = 15; p = 0.04)).


66
ruled out nerve branching in the periphery as a source of referred pain. The convergence
theory of referred pain invokes a central locus of action in the superficial layers of the
medullary dorsal hom. Noxious input from different sources converge on transmission
cells responding to noxious input (for review, see Fields, 1987). Pain may be mistakenly
mislocated to an area distant from the site of origin due to expectation or previous
experience with pain in the referred site.
In most cases, TMJ pain is not restricted to the joint but is also associated with
extra-articular regions. The most common areas are ipsilateral eyeball, superciliary ridge,
deep masseter muscle, and angle of mandible (Mahan and Ailing, 1991). The
craniovertebral junction and upper neck are other referral sites of TMJ pain (Schellhas et
al 1989).


89
model for oral surgery procedures because the anatomy and biomechanics are similar to the
human TMJ (Bifano et alM 1990).
First, for the vertebrate chewing apparatus, the range of motion is generally
confined to those movements necessary for dealing with a particular diet. Due to a coarse
diet of vegetation, ruminants possess a greater range of mandibular movement than do
carnivores. The excursive movements include hinging, lateral translation, slight protrusion
and mediolateral shift. Hinge opening and lateral translational movements are required for
forceful grinding. The lateral pterygoid muscle is the prime mover of the mandible during
lateral translational movements. The lateral excursion, initiated by contraction of either one
of the lateral pterygoid muscles, is a prerequisite to an effective grinding stroke. Both the
goat and human possess a well-developed, lateral pterygoid muscle.
Second, the elevated position of the condyle of the mandible relative to the occlusal
plane benefits the operation of the masseter and medial pterygoid muscles. They function
synergistically to provide powerful bite force needed for grinding activity.
Third, the condyle is convex anteriorposteriorly, which allows some translation
along a convex articular surface of the fossa. Such anteriorposterior translation represents
a common denominator between the TMJ of non-camivorous mammals and the human
joints. In contrast, carnivores have a deep concave articular fossa that allows only hinge
movement and prevents dislocation during seizure of prey.


PROPERTIES OF TEMPOROMANDIBULAR JOINT NOCICEPTORS
IN NORMAL AND INFLAMED TISSUE
BY
BARRY LOUGHNER
A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL
OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT
OF THE REQUIREMENTS FOR THE DEGREE OF
DOCTOR OF PHILOSOPHY
UNIVERSITY OF FLORIDA


45
Table 3-4.
EFFECT OF CARRAGEENAN ON TRANSDUCING CAPACITY
Qualitative improvements in reactivity for nociceptors that were
characterized in normal tissue and then tested again subsequent to
carrageenan injection. Eight of 11 nociceptors acquired either dynamic or
static coding ability. Coding ability was also acquired for nociceptors (n =
2) that had no transducing capacity in normal tissue. Three units that
responded to horizontal plane movement acquired vertical plane reactivity in
acutely inflamed tissue. Six units demonstrated spontaneous activity after
stimulus testing in acutely inflamed tissue.
UNIT
PLANE
PRE-INFLAMED
POST-INFLAMED
CODING
SHIFT
OTHER
MOVEMENT
POST-TEST
SPONTAN.
ACTIVITY
1
VP
DYNAMIC FORCE
MOVEMENT
STATIC FORCE
POSITION
DYNAMIC FORCE
FORCE VELOCITY
MOVEMENT
STATIC FORCE
POSITION
YES

YES
2
VP
DYNAMIC FORCE
DYNAMIC FORCE
STATIC FORCE
YES

YES
3
VP
DYNAMIC FORCE
STATIC FORCE
DYNAMIC FORCE
FORCE VELOCITY
STATIC FORCE
YES

NObE
4
VP
DYNAMIC FORCE
FORCE VELOCITY
MOVEMENT
DYNAMIC FORCE
MOVEMENT
POSITION
YES

LONE
Note: VP, vertical plane


107
TABLE G-17
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #4
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
9.5N
6.4N
-3.1N
Freq. Asymptote
52N
50N
-2.0N
Mean Rate
3.2
3.4
0.2
Slope
-0.27
-0.7
0.43
Freq. Thres.



2
R
0.11
0.60
0.49
Force Velocity
Act. Thres.
27N/s
5.0N/S
-22N/s
Freq. Asymptote
333N/S
155N/S
-178N/S
Mean Rate
2.9
3.1
-0.2
Slope
-0.34
-0.25
-0.09
Freq. Thres.



2
R
0.39
0.26
-0.13
Static Force
Act. Thres.
19N
18N
-1.0N
Freq. Asymptote
41N
52N
1 IN
Mean Rate
4.2
3.7
-0.5
Slope
-1.04
-1.5
0.46
Freq Thres.
10.7N
9.0N
-1.7N
2
R
0.50
0.70
0.20


2
small fibers that were activated by passive movement of the knee joint, both within and
beyond the normal range of motion. These afferents were categorized into four populations
on the basis of their response range. Afferents of populations I and II responded to
innocuous joint movement in the normal range of motion, but population II responded best
to forceful rotation. Population III units were activated exclusively by forceful movement
and population IV had no response to movement. Based on movement sensitivity,
afferents that responded within the normal range of motion were not considered
nociceptors, while those that respond beyond the normal range were nociceptors.
Subsequent studies by Schaible and Schmidt (1985, 1988b) concentrated on populations
III and IV. However, despite the importance of range for classifying afferents, distinctions
between normal and non-normal ranges have been ancedotal. Quantification of the
relationship between range of motion and afferent activity is still pending.
There are no studies that have examined properties of TMJ nociceptors. Previous
reports have examined the discharge characteristics of afferent traffic in the
auriculotemporal nerve that may contribute to position sense and control of mandibular
movement (Kawamura et al., 1967; Klineberg et al, 1970, 1971; Kawamura and Abe,
1974; Lund and Matthews, 1981). While TMJ nociceptors may have properties similar to
those described for cat knee joint, there are considerable functional and anatomical
differences between these two joints that indicate that properties of TMJ nociceptors should
be determined (see Appendices C and F).
Changes in the properties of TMJ nociceptors (sensitization) may account for some
of the symptoms of TMJ dysfunction. These symptoms include pain during mandibular
movement, pain on local joint palpation, and tonic pain. Changes in nociceptor properties
are likely to be necessary to the development of these forms of pain. As pain on movement
is a primary symptom of TMJ dysfunction, a precise determination of the relationship
between movement and afferent discharges is valuable. Quantification of force and
movement also permits more direct specifications of movements which are outside the


CHAPTER 4
DISCUSSION
Afferents were isolated from the trigeminal ganglion and efforts were made to
determine whether they had nociceptive properties. Tests included quantification of
response range, identification of relevant stimulus variables and the tendency to sensitize.
Afferents that are nociceptors should transduce noxious stimuli (Sherrington, 1947), while
other joint afferents (proprioceptors) would be expected to be most reactive in the normal
range of motion, be bidirectionality sensitive, and exhibit spontaneous activity (Burke et
al., 1988; Macefield et al., 1990, Dom et al., 1991).
The relationship between applied force and mandibular movement was examined to
determine the "noxious range" and compare it with the threshold of afferents. The noxious
range is likely to correspond to that portion of the force/jaw movement relationship where
forces increased exponentially with jaw movement. TMJ afferents were activated at or near
the beginning of the exponential phase and their firing became asymptotic in the exponential
phase. Thus, a preference for high forces (mean activation threshold = 20.6 11.0N) at
extremes of the mandibular range of motion (mean activation threshold = 13.7 5.4; mean
frequency asymptote = 49.6 + 20.7 N) suggested that these TMJ afferents were
nociceptors.
In contrast, a small group of units (n = 3) had responses to both jaw opening and
closing. Their properties are distinct from populations of afferents which may be important
in signalling tissue damage. Their activation thresholds (1.1 0.9 N) and range of
reactivity (1.1 0.9 to 10.4 4.1 N) are considerably different from that of nociceptors
described above, and respond chiefly to innocuous joint movement within the physiological
52


95
TABLE G-5
TMJ NOCICEPTOR REACTIVITY IN NORMAL TISSUE
VERTICAL PLANE
Test Conditions
with RF (n=18)
without RF (n-9)
code (n=ll)
no code (n=7)
code (n=8)
no code (n=l)
Dynamic Force
10
8
6
3
Force Velocity
8
10
4
5
Movement
5
10
2
3
Static Force
3
12
1
4
Position
1
14
0
4
Conduction
Velocity
0.4 to 7.5
m/sec
(n=4)
0.75 to 1.5
m/sec
(n=2)


Post-test
Spontaneous
Activity
2
0
0
0


97
TABLE G-7
TMJ NOCICEPTOR REACTIVITY
IN PREVIOUSLY INFLAMED TISSUE
Test Conditions
with RF (n=7)
without RF (n-8)
code (n=7)
no code(n=0)
code (n=6)
no code(n=2)
Dynamic Force
6
0
4
2
Force Velocity
6
0
5
2
Movement
1
0
0
0
Static Force
2
0
0
0
Position
1
0
0
0
Conduction
Velocity
0.7m/sec
(n=l)
0
0
0
Post-test
Spontaneous
Activity
0
0
0
0


106
TABLE G-16
EFFECT OF CARRAGEENAN IN ACUTELY INFLAMED TISSUE
REACTIVITY IN THE HORIZONTAL PLANE
UNIT #3
Test Condition
Pre
Post
Post-Pre
Dynamic Force
Act. Thres.
3.0N
6.3N
3.3N
Freq. Asymptote
33N
13N
-20N
Mean Rate
2.9
4.0
1.1
Slope
-0.58
-1.0
1.32
Freq. Thres.



2
R
0.53
0.64
0.11
Force Velocity
Act. Thres.
lN/s
13N/s
12N/s
Freq. Asymptote
171N/s
179N/S
8N/s
Mean Rate
3.1
2.9
-0.2
Slope
-0.18
-1.2
1.38
Freq. Thres.



/
R
0.38
0.69
0.31
Static Force
Act. Thres.
Freq. Asymptote
Mean Rate
Slope
Freq Thres.
2
R
3.9N
7.9N
4.7
-2.0
2.9N
0.60


51
TABLE 3-5
EFFECT OF SALINE ON TRANSDUCING CAPACITY
UNIT
PLANE
PRE-CODING
POST-CODING
CODINC
SHIFT
OTHER
MOVEMENT
POST-TEST
SPONTAN.
ACTIVITY
1
HP
DYNAMIC FORCE
FORCE VELOCITY
STATIC FORCE
DYNAMIC FORCE
FORCE VELOCITY
STATIC FORCE


NONE
2
HP
DYNAMIC FORCE
STATIC FORCE
DYNAMIC FORCE
FORCE VELOCITY
STATIC FORCE
YES

NONE
3
HP
DYNAMIC FORCE
STATIC FORCE
DYNAMIC FORCE
STATIC FORCE


NONE
4
HP
DYNAMIC FORCE
FORCE VELOCITY
MOVEMENT
STATIC FORCE
POSITION



NONE
5
HP
NON-CODING
NON-CODING


NONE
6
HP
DYNAMIC FORCE
DYNAMIC FORCE


NONE
7
HP
DYNAMIC FORCE
STATIC FORCE
DYNAMIC FORCE
STATIC FORCE


NOME
8
HP
STATIC FORCE
STATIC FORCE


NONE
Note: Changes in reactivity for 8 units after exposure to saline. One of 8 units acquired coding ability
for force velocity. HP, horizontal plane.


54
role in proprioception and clouding the functional distinction between free nerve endings
(nociceptors) and well recognized encapsulated Golgi and Ruffini type end organs which
are found throughout the capsule (Thilander, 1961; Ishibashi, 1966). Yet, others have
reported that many afferents respond within the normal range movement (Klineberg et al.,
1971; Lund and Matthews, 1981; Schaible and Schmidt, 1983b; Dorn et al., 1991).
Microneurographic studies appear to have resolved this confusion in favor of the findings
of Schmidt and company. These studies have examined the behavior of neuronal
populations that signal joint position and mechanosensibility in humans. Burke et al.,
(1988) recorded responses of joint, muscle and cutaneous mechanoreceptors associated
with finger joints to position and movement. Whereas most responded at the limits of joint
rotation, a few afferents responded within the normal range. It is unclear whether the
former group could code for pain, as pain was never induced by the movements, but the
latter group appears to be appropriate for proprioceptive function. The relatively small
population (3 of 16 cases) that provided a proprioceptive code was not dissimilar to our
own (3 of 36 cases). Microstimulation of similar groups of joint afferents innervating
finger joints indicated that innocuous sensations of movement or deep pressure were
evoked (Macefield, et al., 1990). Thus, a proprioceptive role for joint afferents seems to
be confirmed, although they may represent a small portion of the afferent population.
Sensitization of TMJ Nociceptors
Nociceptors in all preparations will sensitize following exposure to extreme heat
(Burgess and Perl, 1967; Beck et al., 1974; Fitzgerald and Lynn, 1977; Campbell et al.,
1979), mechanical forces (Reeh et al., 1987) or proinflammatory substances (Schaible and
Schmidt, 1988a; Berberich et al., 1988; Cooper et al., 1991), and these are reflected as
changes in central reactivity (Neugebauer and Schaible, 1990; see Appendix D). Sensitized
nociceptors in skin, muscles and joints have enhanced reactivity to thermal, mechanical


A REACTIVITY IN THE VERTICAL PLANE:
DYNAMIC FORCE
0 1 2 3 4 5 6
Ln FORCE (Newtons)
-A- D1 E2 E2 L3 A1
-7- S3 -O- K7 -O- H6 -O- E3 -O- G3
C REACTIVITY IN THE VERTICAL PLANE:
FORCE VELOCITY
-2 -1 0 1 2 3 4 5 6
Ln VELOCITY (Newtons/sec)
-A- D1 E2 L3 A1
-7- S3 -o- N7 -O- G3 -O- G3
B
REACTIVITY IN THE HORIZONTAL PLANE:
DYNAMIC FORCE
0 1 2 3 4 5 6
Ln FORCE (Newtons)
-A- A1 A1 A1 C2 A A1
-A- D -O- J4 -O- A1 D3 A1 + A1
D REACTIVITY IN THE HORIZONTAL PLANE:
FORCE VELOCITY
-2 -1 0 1 2 3 4 5 6
Ln VELOCITY (Newtons/sec)
-A- A1 A1 C2 A2
A1 D3 -V- J4
LO
O