Fine motor control deficits in monkeys following dorsal column lesions


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Fine motor control deficits in monkeys following dorsal column lesions
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vi, 131 leaves : ill. ; 29 cm.
Glendinning, Diana Louise Schulmann, 1961-
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Research   ( mesh )
Spinal Cord Injuries -- complications   ( mesh )
Movement Disorders   ( mesh )
Motor Skills -- physiology   ( mesh )
Macaca   ( mesh )
Proprioception -- physiology   ( mesh )
Department of Neuroscience thesis Ph.D   ( mesh )
Dissertations, Academic -- College of Medicine -- Department of Neuroscience -- UF   ( mesh )
bibliography   ( marcgt )
non-fiction   ( marcgt )


Thesis (Ph.D.)--University of Florida, 1991.
Includes bibliographical references (leaves 115-130).
Statement of Responsibility:
by Diana Schulmann Glendinning.
General Note:
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University of Florida
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I would like to thank my advisor, Charles Vierck, for his many
contributions to this thesis, his expertise and unrelenting optimism, and for
building my jazz collection to three times its original size. I also thank the
members of my committee, Brian Cooper, Christiana Leonard, Floyd
Thompson, and Donald Stehouwer for their guidance and critical evaluation
of my ideas. I give a special thanks to Brian Cooper for his good counsel and
for suffering through my early attempts at electrical programming, and to
Christiana Leonard for teaching me histological techniques and providing
good advice over the years.
I am also very grateful to Anwarul Azam for his invaluable technical aid,
especially in moments of crisis; Jean Kaufman for teaching me how to build with
plexiglass and to work with and care for monkeys; Robert Friedman, James
Makous, and Carol Martin-Elkins for their camaraderie, editorial help, and
generous assistance in experiments; Dr. Valenstein and Barbara Haus for
sharing laboratory space, equipment, and monkeys with me; Babbette Botchin
and Dan Thiel for veterinary care beyond the call of duty; Tim Cera, Ralph
Breslow and Laura Kasper for help with data analysis; Martha Clendennin for her
guidance and support; NIMH for financial support; and my parents, Simone and
Marcel Schulmann, for their endless support and for doing their best to
understand the vague and slow progression of a doctoral program. Last of all, I
thank John Glendinning for his advice on this manuscript and for his unrequited
patience, good humor, and loving support throughout my doctoral program.


PaAC NO LEDGEMENT .............................................................................................ii
ACKNOW LEDGEMENTS ............................................................................................. ii

ABSTRACT.............................................................................................................. .v


1 GENERAL INTRODUCTION ...........................................................................1...

Fine Motor Deficits in Primates Caused by Fasciculus Cuneatus
Lesions................................................................................................................. 1
Anatomy and Physiology of the Fasciculus Cuneatus..............................5...
Overview of Dissertation............................................................................... 11

FASCICULUS CUNEATUS LESIONS ..................................................... 12

Methods .............................................................................................................. 13
Results......................................................................................................... 18
Discussion...................................................................................................... 24


Methods........................................................................................................... 48
Results ................................................................................................................ 56
Discussion..................................................................................................... 61


Methods.............................................................................................................. 99
Results............................................................................................................ 101
Discussion.................................................................................................... 102

5 GENERAL DISCUSSION .......................................................................... 108

The Unique Role of Sensory Feedback in Fine Finger Movements.....108
Regulation of Sensory Feedback.............................................................1... 10
Mechanisms for Sensory Gating..............................................................1... 12

REFERENCES ....................................................................................................... 115

BIO G RAPHICAL SKETC H ................................................................................... 131

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



Diana Schulmann Glendinning

December 1991

Chairperson: Charles J. Vierck, Jr.
Major Department: Neuroscience

I examined motor deficits caused by interruption of the fasciculus
cuneatus (FC), the forelimb component of the dorsal columns (DCs) in
Macaca arctoides. In experiment 1, the grasping patterns used by three
monkeys reaching for and grabbing small food items were analyzed using
videography. Grasping style, joint angles, and grip apertures were
measured. Normal monkeys used mainly precision grasps to acquire items
and formed a consistent and small grip aperture during the approach.
Grasps involved a combination of joint movements--i.e., flexion and extension
at contiguous joints. The FC transected monkeys 1) stopped using precision
grasps, 2) formed excessively large or small grip apertures, and 3) never

combined joint movements. Thus, FC lesions disrupted precision grasping
by impairing the ability to posture the fingers and perform complex multi-joint
In experiment 2, I determined whether the FCs 1) are critical for
adjusting finger position and 2) contribute to the M2 long-latency reflex.
Three monkeys were trained to hold the index finger stationary for three
seconds. Constant or variable resistive loads were applied to the finger
through a torque motor. Monkeys resisted the loads to maintain finger
position. To elicit stretch reflexes, torques pulses were applied during the
holding task. Activity in the first digit intrinsic muscles was recorded
electromyographically. Complete FC lesions in two monkeys impaired
positioning ability, as resistive loads displaced the finger. Typical M2
responses also disappeared. In contrast, a partial FC lesion affected the
ability to posture minimally, and the M2 reflex was intact.
In experiment 3, I used a standard clinical test to examine
proprioception in two monkeys. The test did not identify deficits following FC
lesions. However, following a total lesion of the FC, proprioception was
impaired for low velocity displacements. The results indicate that the FC
provides proprioceptive cues from the finger, but the clinical test is too crude
to detect this contribution.
In summary, results from a series of three experiments suggest that
motor deficits in FC-lesioned primates are related to an inability to assume
and adjust finger positions. Losses of automatic servo-responses and/or
diminished proprioception might contribute to these changes.


Fine Motor Deficits in Primates Caused by Fasciculus Cuneatus Lesions

The clinical literature from as early as 1832 contains descriptions of
motor deficits resulting from interruption of the dorsal columns (DC) of the
spinal cord. These reports attribute clumsiness and ataxia of the limbs to a
loss of limb position and/or movement sense (see Wall, 1970; Nathan et al.,
1986). Because lesions are rarely verified histologically in such clinical
reports, animal models have been necessary to confirm that movement is, in
fact, impaired by isolated DC transactions. Carnivores, rodents, and
primates have all been examined for the effects of DC lesions on motor
behavior. Neverthless, the only appropriate models for the study of fine
finger movements are primates capable of prehension.
The first confirmation that DC interruption impaired motor function in
primates was provided by Ferraro and Barrera in 1934. They severed the
cervical DCs, which included the fasciculus cuneatus (FC), the forelimb
component of the DCs. Through standard neurological examinations and
behavioral observations of monkeys, they concluded that the hallmark deficit
following DC interruption was a loss of fine grasping movements, such as
those used to manipulate food or other objects. Although less refined
grasping was largely unaffected, they reported that even these grasps were

abnormal, and marked by inaccurate placement of the fingers between cage
wires during climbing. Because lesioned monkeys often assumed unusual
positions for long periods of time, Ferraro and Barrera concluded that a loss
of proprioception was the primary defect responsible for abnormal forelimb
movements. Gilman and Denny-Brown (1966) described similar motor
deficits in monkeys after FC lesions and posited that these deficits were
limited to movements directed into extrapersonal space, since self-grooming
movements looked normal. In addition, the authors described a loss of
relatively independent (or fractionated) finger movements. They attributed
motor deficits to disturbed parietal lobe function. In a more recent study
examining natural grooming movements by videography, Leonard et al.
(1991) also identified fine movement abnormalities (decreased frequency of
particular types of grooming movements and/or altered kinematics). In that
study, a comparison between movements directed to extrapersonal and
intrapersonal space showed that both were equally affected. Execution was
abnormal irrespective of the spatial location of the hand.
The above-mentioned studies, which employed behavioral
observation of natural movements and standard clinical testing, all drew the
same conclusion: that FC lesions produced distal motor deficits. In contrast,
studies which have utilized operant conditioning of primates to examine
distinct movements have reported contradictory findings. Discrepancies in
this literature, however, can be attributed to differences in 1) the degree of
precision required by the task and 2) the segments of the arm--distal or
proximal--involved in the testing procedure.
In studies which have measured grasping success, with no added
demands for accuracy, FC lesions reportedly produce no motor deficits. For

example, Brinkman and Porter (1978) observed that monkeys could retrieve
raisins out of small wells after FC lesions and concluded that there were no
deficits in distal forelimb movements. Asanuma and Arissian (1984) drew the
same conclusion using a task that involved time constraints, thereby
increasing demands for accuracy. Monkeys had to retrieve raisins out of
wells that were spinning on a disk, and were scored according to the highest
speed at which they could empty the wells. Although the scores did not
recover to pre-operative levels, and a persistent "clumsiness" of the hand
was noted, these authors concluded that the lesions had no lasting effect.
They based this interpretation on the fact that the monkeys were able to
complete grasps. Using an analogous task, Vierck (1975, 1978) reported
similar results but attributed greater significance to the appearance of
"clumsiness" and concluded that the FCs were necessary for the normal
execution of fine movements.
Another discrepancy in the literature appears to be due to the
differential effect of FC lesions on distal and proximal movements. FC
lesions do not appear to influence movement in proximal limbs. For
instance, no deficits were identified in monkeys trained to track visual targets
using flexion-extension movements of the elbow (Eidelberg et al. 1976).
Likewise, FC lesions had no effect or a transient effect on performance of
either a bar pull task or a reaching task, both of which involved mainly the
shoulder and elbow joints (Brinkman and Porter,1978; Vierck, 1982a).
Rapidly alternating flexion and extension of the wrist and postural
adjustments of the trunk also remain normal after FC interruption (Beck,
1973; Vierck, 1978).

In contrast to the experiments with proximal movements, tasks
involving the distal forelimb have revealed persistent deficits. FC-lesioned
monkeys do not recover when required to accurately position the hand and
fingers to fit into small compartments (Vierck, 1978). Cooper et al. (1988,
1991) have also shown a persistent inability of FC-lesioned monkeys to 1)
fractionate finger movements -- i.e., move the index finger independently
from the other fingers; 2) combine flexion and extension movements within
one finger; and 3) actively track a tactile stimulus with the fingers.
Taken together, the experiments described above suggest a role for
the DCs in controlling certain movements in the distal hand and fingers.
Below is a list of the abnormalities in fine finger movements as identified
through controlled experiments using primates.
1) Disturbed precision grasping
2) Loss of finger fractionation
3) Inability to combine flexion and extension movements within one
4) Inability to orient spatially the fingers and hand
5) Inability to track moving tactile stimuli
Why should FC lesions selectively disturb distal, precision-type movements
without affecting simple flexion-extension movements at proximal joints?
One similarity among the affected activities is that they involve independent
movements at separate joints and/or fingers. To accomplish this, low grades
of muscle activity must be balanced among several muscles acting
synergistically at each finger. Accurate regulation of muscle activity is
especially important within the finger-hand complex, where most muscles
act over more than one joint. Muscle activity needs to be finely adjusted so

that forces exerted 1) onto a joint do not produce excessive or insufficient
movement, 2) onto a limb segment do not produce movement at more joints
or fingers than intended, and 3) onto an object do not result in its being
dropped or slipping through the fingers. The main focus of the experiments
described below was to examine the effects of FC lesions on the ability to
regulate small amounts of muscle activity. In contrast to other studies, the
test procedures enabled the direct effects of muscular activity on isolated
joint movements to be quantified.

Anatomy and Physiology of the Fasciculus Cuneatus

The FC is a diverse pathway with numerous rostral projections. There
are many routes by which these afferents might influence fine movements.
These are described below.

Afferents in the FC

The FC comprises a heterogeneous population of primary (Shriver et
al., 1968) and nonprimary afferents (Rustioni et al., 1979), originating from
both cutaneous and deep receptors of the ipsilateral forelimb (Whitsel et aL,
1969). Because few studies have examined the properties of the FCs in
primates, much of the information is available only in carnivores.*
The cutaneous population of FC fibers consists of both slowly and
quickly adapting mechanoreceptors, with an apparent preponderance of the

* To designate the animal that was studied, the references in this section will be labelled with
the following abbreviations: "c" cat; "m" monkey; "h" human; "r" raccoon; "rt" rat.

latter (r: Pubols and Pubols, 1973). Muscle afferents include both group I
and II (c: Rosen and Sjolund, 1973). The skin (c: Uddenberg, 1968a,b;
Fyffeet al., 1986) and joints (c: Millar, 1979; Tracey, 1980) are also
represented in therFCs, but these projections have not been fully
characterized. In addition, unmyelinated fibers have recently been
discovered to ascend the DCs (h: Briner et al., 1988; rt: Patterson et al.,
Descending propriospinal fibers course through the FC (m: Burton and
Loewy, 1976), although their function is unclear. The fibers originate in
upper spinal cord levels, the raphe nuclei and the mesencephalic reticular
formation (c: Tohyama et al., 1979 a, b).

Protection of FC Fibers to the Main and External Cuneate Nuclei
FC fibers terminate in the main cuneate nucleus (MCN) and external
cuneate nucleus (ECN) of the medulla. The MCN consists of two nuclear
divisions: the pars rotunda and pars triangularis (m: Ferraro and Berrerra,
1935; Rustioni etal., 1979).
FC afferents segregate by modality among the ECN and the two
portions of the MCN, although this division is not absolute (c: Dykes et al.,
1982; Surmeier and Towe, 1987). Primary afferents from cutaneous
receptors terminate preferentially in the somatotopically arranged pars
rotunda, also known as the cell cluster region of the MCN (c: Dykes et al.,
1982). Here, the distal extremities have an expanded represention relative
to the proximal extremities (m: Florence et al., 1989; Shriver et al., 1968), and
neurons have small receptive fields that are mainly cutaneous (c: Dykes et
al., 1982). Pars rotunda cells are securely linked with a small number of

primary afferents, and are thus capable of accurately transmitting both
temporal and spatial information (c: Ferrington et al., 1987). Pars rotunda
cells also receive descending input from area 3b, to which they ultimately
project (m: Cheema etal., 1985).
Surrounding the pars rotunda is the pars triangularis, which receives
projections from primary muscle and joint afferents and second-order
afferents (m: Hummelsheim etal., 1985; Rustioni etal., 1979). The muscle
afferents projecting to this region appear to be mainly group I (m:
Hummelsheim and Wiesendanger, 1985; c: Rosen, 1969a). Similar to the
linkage of primary cutaneous afferents in pars rotunda, most MCN cells
receiving deep inputs are driven by only a small number of primary afferents
from single muscles that are somatotopically arranged (c: Dykes et al., 1982;
Rosen, 1969b; Rosen and Sjolund, 1973; Surmeier and Towe, 1987). Thus,
temporal and spatial information from deep receptors appears to be
transmitted reliably. Second-order projections to pars triangularis originate
from cells in lamina IV-VI (m: Rustioni, 1977). Pars triangularis cells
receiving the second-order projections are probably distinct from those
receiving projections from deep, primary afferents (c: Rosen, 1969b). Cells
responding to the second-order afferents respond to a wide range of
cutaneous mechanical stimuli, but receptive fields are small (similar in size to
those of primary afferents; c: Uddenburg, 1968b). Pars triangularis cells also
receive descending inputs from the sensorimotor cortex (primarily areas 1
and 2, but also 3a, 3b, and 5), reticular formation, and red nucleus (m:
Bentivolgio and Rustioni, 1986; c: Edwards, 1972; Scheibel and Scheibel,

Primary afferents from muscle and joint receptors also project directly
to the somatotopically organized ECN (m: Hummelsheim et al., 1985; c:
Nyberg and Blomqvist, 1984). This nucleus appears to be activated mainly
by group I muscle afferents, but also responds to group II and tendon organ
afferents (c: Rosen and Sjolund, 1973; m: Hummelsheim and Wiesendanger,

Efferent Projections of the Cuneate Nuclei
The modality specificity of neurons in the MCN and ECN is maintained
in rostral projections. Two relatively direct pathways send cutaneous and
proprioceptive FC information to the cortex, and both could influence the
output of the motor cortex.
Cells in pars rotunda of the MCN send cutaneous information to a core
region of nucleus ventroposterolateralis caudalis (VPLc) of the thalamus (m:
Berkley et al, 1986), which in turn projects to somatosensory cortical areas
3b and 1 (m: Jones, 1984). Proprioceptive neurons of the pars triangularis
and ECN project to a more anterior region of VPLc (Jones, 1983a) and to a
border region between nucleus ventroposterolateralis oralis (VPLo) and
VPLc (m: Boivie and Boman, 1981; Berkley,1983; Maendly et al., 1981).
VPLo is the main thalamic relay for cerebellar afferents and projects to area 4
(Jones 1983b). The anterior VPLc and the border area project to areas 3a
and 2 of the somatosensory cortex (m: Jones, 1983a; Maendly etal., 1981).
Information from 3a can reach the motor cortex directly (c: Zarzecki et al.,
1978), or through efferent connections with area 2. Area 2 projects to area 1,
which sends cortico-cortical fibers into area 4 (m: Jones, 1983b). The border
area is also believed by some to project directly to the motor cortex (c:

Asanuma et al, 1979; Strick, 1976), although this is somewhat controversial
(m: Jones, 1983b; Tracey et al., 1980a). There are differing opinions as to
where 3a ends and 4 begins, as well as whether the VPLo-VPLc border is
distinct from VPLo (cf. m: Jones 1983b; Maendly et al., 1981).
Irrespective of how many synapses are interposed, proprioceptive and
cutaneous information from the FC have relatively direct access to the motor
cortex. The FC probably carries the majority of the peripheral signals
transmitted to the motor strip, as FC transactions completely abolish
responses of area 4 cells to deep and superficial forelimb stimulation (m:
Asanuma et al., 1980; Brinkman et al., 1978). Most likely, the FC influences
movement by regulating the pyramidal tract, since the latter appears to be
specialized for distal movements (m: Clough et al., 1971; Koeze et al. 1968),
and FC lesions and pyramidal lesions produce virtually identical deficits (m:
Cooper et al., 1991; Lawrence and Kuypers, 1968; Tower, 1940, Vierck,
1975, 1978).
In addition to the cortical targets, the dorsal column nuclei project to
other motor areas. A major cerebellar projection, the cuneocerebellar tract,
is formed by fibers from ECN and pars triangularis. These convey both
muscular and cutaneous information to ipsilateral lobule V of the pars
intermedia, as well as to lobules IV, VI, IX and the paramedian lobule (c:
Cooke et al., 1971; Rinvik and Walberg, 1975). The dorsal column nuclei
also project, mostly contralaterally, to the inferior olivary nuclei to activate
climbing fibers projecting to the medial and anterior lobes of the cerebellum
(m: Brodal and Kawamura, 1980; c: Molinari, 1984, 1985). Given that the
cerebellum also projects to the motor cortex via VPLo, the FC might also
influence the motor cortex through these projections, albeit less directly.

However, it is doubtful that this route mediates the short-latency responses of
motor cortex cells to afferent input, given that cerebellar cells respond at
longer latencies than motor cortex cells to peripheral stimuli (c: Eccles et al.,
1974), and cerebellar ablation does not affect the area 4 evoked potential (c:
Malis et al., 1953).
Other targets of the pars triangularis include the nonspecific thalamic
nuclei, rostral mesencephalon, tectum, pretectum, spinal cord and
cerebellum (m: Berkley et al., 1980; for review, see Berkley etal., 1986).
These projections might influence hand and finger movements without
directly influencing the motor cortex.

Several afferent types course through the FCs. Deep and cutaneous
afferents generally follow different paths, although some degree of
convergence exists at each rostral relay. The most segregated afferents
appear to be the primary cutaneous afferents projecting from the distal limb
to the pars rotunda region of the main cuneate nucleus. Here, synapses are
secure, and somatotopic information is thought to be reliably transmitted to
the VPL and the somatosensory cortex.
Primary afferents from the joints and muscles are more likely to project
to pars triangularis and the somatotopically organized ECN nuclei. Again,
tight synaptic coupling between these cells results in efficient and accurate
conveyance of information in the temporal and spatial domains. Both deep
and superficial afferent types follow a relatively direct route to the
sensorimotor cortex and cerebellum. The multi-modal, cutaneous afferents

which originate in the dorsal horn also project to several subcortical motor
regions, where they might influence movements.

Overview of Dissertation

In the following chapters, I have sought to determine 1) which aspects
of movements are impaired by FC lesions, and 2) whether vernier control of
small movements and postures is normal after the lesions. In chapter 2, I use
frame-by-frame video analysis to discern specific movement alterations
during precision grasping. In chapter 3, I describe experiments designed to
test the hypothesis that FC lesions disturb the ability to adopt and adjust
finger positions. Transcortical reflexes are also elicited in these experiments,
as these are believed to be important for postural maintenance. In chapter 4,
I examine the possible role of proprioceptive disturbances in fine
movements. Chapter 4 is written with a clinical orientation, as I utilize a
common neurological test which is purported to detect proprioceptive deficits
following DC lesions. In chapter 5 the results of these experiments are
discussed in terms of possible sensorimotor mechanisms.


Precision grasping is a sensorimotor activity, involving adaptations of
finger movements to physical properties of an object. When approaching an
object to be grasped, a primate postures the fingers to match the shape and
size of the object (Jeannerod and Biguer, 1982). Once contact is made,
tactile cues are needed to position the object between the fingers and to
discern the forces required to lift the item (Westling and Johansson, 1984).
Proprioceptive and tactile feedback are, therefore, expected to be essential
for the successful performance of precision grasp. Among the pathways in
the spinal cord that could provide this feedback, the fasciculus cuneatus (FC)
may be the most important. The FC provides the most direct sensory input to
neurons of the pyramidal tract (Asanuma et al., 1980; Brinkman and Porter,
1978), a pathway known to be required for precision grasping (Tower, 1940;
Lawrence and Kuypers, 1968; Chapman and Weisendanger, 1982). The
FCs may, therefore, constitute the major afferent component of a unique
sensorimotor system for prehension, with the pyramidal tract as the efferent
Although several investigators have examined the role of the FCs in
grasping by evaluating hand functions after FC lesions, a consensus has not
been reached. Some investigators have reported that grasping and finger
movements are abnormal following FC interruption (Ferraro and Barrera,

1934; Beck, 1976; Gilman and Denny-Brown, 1966; Eidelberg etal., 1976;
Vierck, 1975, 1978, 1982a; Cooper et al., 1988; Cooper et al., 1991), while
others have reported full recovery of motor function and have argued against
a critical role for the FC in motor feedback (Brinkman and Porter, 1978;
Asanuma and Arissian, 1984). The lack of agreement appears to be related
to the manner in which the previous investigations evaluated the completion
of goal directed behaviors. Without imposing demands on precision and
speed, or specifically evaluating the execution of the grasp, motor deficits
might not be detected. In quantitative assessments of grasping performance,
which involved extraction of objects from small wells, or posturing of the hand
and fingers to fit into a small compartment, Vierck (1975, 1978, 1982a)
showed that while fine motor abilities gradually improve after FC lesions, they
never fully recover--that is, pre-operative performance levels are not
achieved for tasks normally accomplished with precision grasp. These
investigations revealed permanent deficits in orientation of the hand during
approach and grasp of an object, but the movements were not captured in a
manner that permitted a full description of alterations in form. In this study, I
attempt to identify the specific changes that impair precision grasp of small

The grasping patterns of three adult male stumptailed macaques
(Macaca arctoides) were studied. The monkeys, referred to as M,S, and W,
lived with 1-2 conspecifics in outdoor enclosures at the University of Florida
Primate Facility. M and S were captured in the wild and brought directly to

the University of Florida; W was born in the laboratory colony. None of the
monkeys had been used previously in other experiments. However, all three
monkeys were part of a larger experiment in which the effects of FC
transaction on fractionated finger movements were studied (Cooper et al.,
1991). On the days of the grasping sessions, the monkeys did not perform
the fractionation task. They received food rewards during testing (Purina
monkey chow, raisins, peanuts, and fruit) and then received the chow ad
libitum for 1-2 hours after the daily testing. Water was always available.

Grasping Experiment
Each monkey was seated in a chair that was fitted with a flat wooden
board extending 20 inches from the monkey's navel. The torso was
restrained by the board, and one hand was restrained with a piece of soft
leather. The other hand had six pieces of high gain reflective tape (3 mm2; 3-
M) attached to the following anatomical landmarks: 1) forefinger tip, 2) thumb
tip, 3) second distal interphalangeal (DIP) joint, 4) second proximal
interphalangeal joint, 5) second metacarpophalangeal joint, and 6) radial
styloid process. Small bits of highly preferred food (peanuts, raisins, and
banana pellets) were placed one at a time onto the board for the monkey to
grasp. The food items were chosen because they were a small size which
elicited precision grasp. Each grasp was filmed with a video camera that had
a rotary shutter (RSC-1010, Sony). The camera was positioned at right
angles to the moving hand. All the animals were familiar with the food bits
and grasping apparatus prior to the videotaping session.
Approximately 20 to 30 grasps were completed in each session. The
left hand of monkeys M and W was tested 3 times pre-operatively. Monkey S,

who was often uncooperative, could only be videotaped successfully for one
day pre-operatively on the left side. Post-operatively, each hand of each
monkey was videotaped twice. In each case, testing occurred between 1.5
and 10 months after surgery, well after the acute post-operative recovery
period, which lasts approximately 3 weeks (Vierck, 1982b). No significant
differences in the form of grasping were found between testing sessions
within either the pre-operative or post-operative conditions (see below).

Videotape Analysis
The videotapes of the grasps were replayed (using a Panasonic
recorder, VHS AG-6300 MD), and a list of grasps was made for each video
session by two independent investigators. The list included the counter
number of each grasp, the grasped object, the grasp style, the result of the
grasp (miss or success) and whether or not the picture was clear. The inter-
rater reliability for grasp style was 91 %. From this list, 15 grasps were
randomly chosen for analysis of the grip formation and grasp kinematics.
Grasps that involved transverse motion were excluded from the analyses to
avoid problems with parallax.
Grasp style. The four most common grasp styles were "TIP-TIP",
"FINGER CURL", "PALM", and "THUMB to DORSUM" (Figure 2-1). Post-
operatively, other styles of grasp were occasionally observed to involve
bizarre finger-object relationships, including sticking the food to the skin or in
the palm crease.
Grip formation. An example of a typical, normal precision grasp is
shown in Figure 2-2. Grip formation began as the hand approached a food
object, with the first two finger tips separating slightly, in apparent anticipation

of precision grasp (Figure 2-2A-2C). The fingers were postured so that
minimal movement was needed at the termination of the reach to grasp the
Grip formation was evaluated by measuring the distance between the
tips of the thumb and forefinger (grip aperture) at each frame beginning 150
ms prior to contact with the table surface. Variations in the aperture were
also calculated, to determine the capacity to consistently reproduce the
object-specific movement. To normalize the aperture measurements, each
one was multiplied by the ratio of actual finger length to the measured finger
length. This corrected for any slight changes in the distance between the
hand and the camera at each videotaping session.
Grasps were not subdivided according to food type or grasping style
for the analyses of either grip formation or grasp kinematics (below).
Preliminary measurements showed that neither measurement depended on
these variables.

Grasp kinematics. The angles of the metacarpophalangeal, proximal
interphalangeal, and distal interphalangeal (DIP) joints were measured
during three stages of the videotaped grasp: 1) table contact, 2) object
contact, and 3) the moment the hand was lifted off the table (with or without
the item). Joint angles were measured directly off of the video screen, using
a hand-held goniometer. To determine the amount of movement that
occurred with the fingers on the table, the difference between the joint angles
at table contact and object contact was measured. The duration of table
contact was calculated as the time between table contact and lift. Monkey S

was excluded from this analysis because of a prior injury to the left proximal
interphalangeal joint.

Surgery and Histology
After training, each monkey received a FC transaction. Surgeries
were performed under aseptic conditions, with the animals under general
anesthetic (Halothane). The surgical procedure involved performing a
laminectomy at one or two cervical vertebrae, reflecting the dura, visualizing
the spinal cord through a dissecting microscope, and approximating the FC
location by visualizing the medial dorsal sulcus and dorsal root entry zones.
Small portions of white matter were severed with precision forceps.
Separate unilateral lesions were made on monkeys M and W, with
approximately one year separating the right and left lesions. Monkey S
received a bilateral lesion at one surgery. Each animal was given
prophylactic antibiotics oxytetracyclinee) following surgery.
Testing began one month later, after the stitches had been removed
and the animals had been returned to the communal outdoor enclosures. At
this time they had recovered from the acute motor effects of the surgery
(Vierck, 1982b). Following the behavioral testing, the monkeys were
overdosed with Pentobarbitol and perfused with 10% formalin. Sections
were cut at 501pm, using a freezing microtome, and stained with 0.5% cresyl
violet. The lesions were visualized and drawn from an image projected by a
Leitz macroprojector.

Data Analysis
All comparisons were between the pre- and post-operative conditions.
Pre-operative data for the right hand were unavailable for monkeys W and M,
because the right sided lesions predated this study, and for monkey S,
because of a lack of reliable data. Therefore, all post-operative comparisons
were made relative to pre-operative performance of the left hand. It is
doubtful that lateral asymmetries confounded the results for the right hand,
since pre-operative differences have not been observed for any other
measurements of fine motor control in these same animals (see Leonard, et
al., 1991, and Cooper, et al., 1991).
The data were subjected to tests for normality (Statworks; Rafferty et
al., 1985), and parametric or nonparametric tests were used accordingly. To
justify pooling data across days, tests were made for between day differences
for each parameter, using ANOVA or Kruskal-Wallis tests. Pre- and post-
operative means for grip-aperture were compared using a two-way ANOVA
with time as a repeated measure. Differences in the variability of the grip
apertures were determined by an F-test for differences between coefficients
of variation for each time (Zar, 1984). Mann-Whitney U-tests were used to
compare median durations of table contact and joint movements during table
contact. DIP joint angle means were compared using unpaired t-tests.


The only complete lesion of the FC was on the left side of Monkey W
(W-left). The other lesions spared a small portion of either the dorsolateral

portion of the FC (S-Right, W-Right, M-Right) or the deep, ventrolateral part of
the FC (M-Left) (Figure 2-3). The sparing of dorsolateral fibers would have
preserved only some of the input from segments at or near the level of the
lesion. The FC lesion affecting the right hand of monkey S extended into the
anterior funiculus and contralateral anterolateral funiculus and therefore
could have affected other ascending sensory pathways (e.g. spinothalamic).
The lesion affecting the left hand of monkey S incorporated the dorsolateral
funiculus and the anterior funiculi. This lesion probably disrupted both motor
pathways (e.g., corticospinal and rubrospinal), and other somatosensory
pathways (e.g., dorsolateral pathways to the lateral cervical and cuneate
nuclei). Because of the extent of this lesion, which produced a hemi-paresis,
data from S-left were not included in the movement analyses.

Grasp Styles
Pre-operatively, the grasps were almost always successful (85-96%;
Table 2-1). Tip-tip precision grasps were the most common, occurring 80-
90% of the time (Table 2-2). Figure 2-2 shows an example of a typical
precision grasp in a normal monkey. Occasionally, the monkeys used the
finger-curl or palmar styles. In the finger-curl, the object was folded into the
creases of the index finger. In a palmar grasp, the object was brought into
the palm by one or more of the fingers.
Severance of the FC resulted in grasping deficits in all cases, except
for M-left, in which the lesion was incomplete ventrally. The deficits were
characterized either by failed grasp attempts (Table 2-1), or by successful
grasps that were achieved by non-precision movements. Misses were
generally characterized by complete grasping actions; either the hand

missed the object entirely, or the grasping movement flicked the object away.
Successful grasps were variable in form and infrequently (0-27%) involved
the finger tips (Table 2-2). Post-operatively, the grasps were usually (61-
80%) made with the finger-curl or palmar styles. Although these same styles
were also observed pre-operatively (albeit rarely), the post-operative forms
differed markedly. Independent movement of the index finger was never
observed; all of the fingers moved together when forming the hand for each
grasp. Also, the thumb movement was abnormal. Instead of being directed
toward the tip of the second finger, the thumb flexed with the other fingers,
ending up either in the palm, against the side of the first finger, or over the
dorsum of the fingers.
Some differences in post-operative grasp performance were noted
among the monkeys. These differences corresponded to lesion extent.
Monkey S was not able to pick up the small items with the left hand following
the lesion that damaged the left lateral funiculus and both ventral funiculi.
With the right hand, which was probably affected by damage to both the FC
and other tracts, Monkey S (S-right) missed the objects more often than the
other animals. S-right used the same grasp styles as the other FC-lesioned
monkeys, but whereas the other monkeys occasionally formed tip-tip
precision grasps, S-right never did. Thus, the more extensive interruption of
pathways for S-right increased the severity of the grasping deficit. Grasping
was unchanged in M-left, with sparing of the deep ventrolateral portion of the
FC. There were no substantial differences in the success rate for post-
operative grasping among the other cases of partial or total lesions of the FC.
However, the grasping style of W-left, with a total FC lesion, was more
affected than the two cases with partial lesions (i.e., dorsolateral sparing of

the FC: M-right, W-right). W-left used the finger tips less than either W-right or
M-right (14% vs. 27% and 24%, respectively), and W-left tended to use the
whole palm more frequently.
Post-operatively, all the monkeys (except M-left, with deep sparing of
FC) supinated the hand, and sometimes the forearm, following both
successful and unsuccessful grasp attempts. It appeared that they did not
know if they had captured the object and were turning the hand to look for the

Grip Formation
Pre-operatively, the animals reliably maintained a small grip aperture
as the hand approached objects (Figure 2-4, top panels). The consistency of
this approach to grasp is illustrated quantitatively by the low coefficient of
variation (CV) of grip apertures across grasp trials for each monkey (Figure 2-
4, bottom panels). Grip formation was clearly altered for animals post-
operatively. In two cases, grip apertures were significantly larger throughout
the entire period of grip formation (S-right: F(7,7)=83.60 ; P <0.0001; W-Right:
F(11,9)=16.83: P < 0.0006), without any change in the coefficient of variation
(all F-values nonsignificant at P : 0.05). The hyperextension of the fingers
that characterized the increased grip aperture is illustrated in Figure 2-5.
In the two other cases, W-left and M-right, grip apertures were not
increased but were more variable; i.e., the coefficients of variation were
significantly increased (all F-values significant at P 5 0.05). These two
animals sometimes hyperextended the fingers, but at other times did not
open the fingers at all. Thus, the grip apertures were inconsistent and
unrelated to the object. Again, the incomplete lesion on the left side of

monkey M produced no significant changes in either grip aperture
(F(8,11 )=1.27) or coefficient of variation (Figure 2-4). The grip formation
deficit on the right side of Monkey S, with the more extensive lesion, was
qualitatively similar to that of the other animals, but the effect was more
pronounced; i.e., the grip apertures were larger than for the other lesions.
In all post-operative cases, significantly more time was spent with the
fingers moving against the table (P < 0.05; Table 2-3). Also, more joint
movement occurred with the fingers contacting the surface (P 5 0.01; Figure
2-6). The fingers of S-right were in contact with the table surface longer than
any of the other post-operative cases. For the incomplete lesion of M-left,
neither the duration of table contact nor the amount of movement against the
table was increased.

Grasp Kinematics
Normally, precision grasp incorporates a complex multi-joint pattern in
which proximal flexion and distal extension are combined within the joints of
the index finger (Figure 2-2). The DIP joint fully extends (to nearly 1800) at
the final grasp position. Following the FC transactions, the DIP joint angle
was modified. It was not extended when the final grasp position was reached
(Figure 2-5 and Table 2-4). In M-right and W-left, the DIP joint was
significantly more flexed than normal. This flexion resulted in smaller sample
sizes, because the DIP joint flexed behind the thumb, obscuring it from the
camera's view. For W-right, the DIP joint was hyperextended as a result of
pressing the fingers against the table. To be sure of this, food bits were
offered directly from an investigators hand to prevent table contact. In this
situation, the distal joint hyperflexed, as it had with the other two cases.

Therefore, in all post-operative cases, the monkeys terminated grasps with
flexion at all joints of the index finger. This pattern of overall flexion was
consistently different from the pre-operative pattern of combined flexion and
Even though the proximal segment of the hand could not be visualized
sufficiently to produce reliable measurements of the joint angles at the wrist,
our subjective impression was that the wrists were less extended following
the lesions. This was true for all cases. An extreme example of this post-
operative positioning is shown in Figure 2-5 (compare to Figure 2-2).

FC interruption impaired the ability of monkeys to form precision
grasps, resulting in less effective food acquisition. When an object was
grasped, it was usually carried in the palm or under the fingers. Tip to tip
prehension was observed only occasionally in some animals after the
lesions. Grasps by the lesioned animals were characterized by 1) abnormal
grip formation, 2) more movement of the fingers against the table surface, 3)
excessive DIP flexion, and 4) a loss of independent finger movements.
These precision grasping deficits were unchanged over the period of testing-
-10 months.
No major differences were identified between the post-operative
grasping patterns of W-left (with a total lesion of the FC) and either W-right or
M-right, in which the lesions were partial, with dorsolateral sparing.
However, in the one instance of a lesion that spared fibers in the deep ventral
area of the FC, no post-operative defects were found. The post-operative
grasping patterns of S-right were the same as those of the other animals, but

the deficits were slightly more pronounced. This animal had a total lesion of
the right FC, and there was damage to other pathways in the ventral columns
and the contralateral, lateral funiculus.


Although motor deficits for the distal forelimb have previously been
reported to follow FC lesions (Vierck et al., 1987, and references therein), the
nature of the movement disorder was not determined in those studies. It is
clear from the present results that interruption of the FC produces discrete
changes in the style and form of one type of fine movements of the ipsilateral
hand. Despite these alterations of precision grasp, less refined grasping is
still possible and is used to accomplish most tasks, albeit with reduced
accuracy and effectiveness.
Abnormalities in post-operative movements began during grip
formation, as the hand approached an object. FC-lesioned animals did not
produce the small, graded movements that are normally used to form the
grip, and that determine the success of precision grasp (Jeannerod and
Biguer, 1982). The movements that were made during grip formation were
generally characterized by hyperextension of all the fingers and an enlarged
grip aperture. The movements used to close the fingers onto the items were
also exaggerated; they were characterized by overall flexion of the finger,
instead of differentiated flexion and extension among the separate joints of
one finger. Another post-operative deviation in grasp was the extended
contact of the fingers with the table surface--a pattern previously observed on
a task involving the hindlimb with dorsal column lesioned animals (Vierck,

1978). The increased contact might be a strategy used by the monkeys to
control the movements required to grasp and hold an object.
In addition to the abnormalities in grasp preparation, the final form of
the grasps used by the lesioned monkeys changed, and it rarely involved
apposition of the thumb and finger tips. Instead, finger-curl and palmar
grasps were common; these were grasps in which food bits were scooped
into the creases of the fingers or palms, with little or no involvement of the

Mechanisms Underlying Deficits
Previous investigators have drawn different conclusions as to the
mechanism underlying motor impairments that follow FC lesions. Some
authors have suggested that a loss of deep muscle and joint feedback
explains the deficits (Ferrarro and Berrera, 1934; Sjoqvist and Weinstein,
1942; Rosen and Asanuma, 1972; Marsden et al., 1977b). Others have
favored the explanation that it is tactile input from the finger tips that is
needed (Gilman and Denny-Brown, 1966; Wall, 1970). Tactile afferents were
believed to contribute to movements of the hands by triggering instinctive
grasp reflexes (Gilman and Denny-Brown, 1966; Rosen and Asanuma,
1972), or by initiating and sustaining exploratory finger movements (Wall,
1970). These latter interpretations are not highly relevant to the grip
formation phase of precision grasp, however, since it is a planned movement
that begins before the skin is stimulated through touch (Jeannerod and
Biguer, 1982). The present results implicate afferents in the FCs for control of
the fingers before a tactile cue "triggers" movement. In this respect, tactile
afferents may contribute to grip formation because, together with muscle and

joint afferent groups, they contribute to proprioception of the hand and fingers
(Gandevia and McCloskey, 1976a; Moberg, 1983).
During grip formation, deep and/or superficial afferents in the FCs may
be important for two aspects of finger movements, planning and execution.
To plan an appropriate set of muscular commands for grip, the motor cortex is
believed to utilize visual information about the shape, texture, and size of an
object, as well as proprioceptive information about the position of the fingers
and the hand (Arbib, 1981; Jeannerod and Biguer, 1982). The grip aperture
is planned according to the visually assessed size of the object (Jeannerod,
1986). The motor commands required to create this aperture depend on the
position of the hand and fingers and the tensions within the hand muscles.
The critical visual information for the guidance of grasping appears to
access the motor cortex directly from the visual cortex (Brinkman and
Kuypers, 1972; Haaxma and Kuypers, 1975). The relevant proprioceptive
information appears to be conveyed by the FC, either directly from a FC-
thalamocortical projection (Asanuma et al., 1980; Lemon and Burg, 1979), or
indirectly via the somatosensory cortex (Jones et al., 1978). Monkeys with
FC interruption or disconnection of the visual and motor areas of the cortex
display similar motor deficits: grip formation is disrupted and grasping does
not begin until the fingers contact the support surface (Brinkman and
Kuypers, 1972). Proprioception is believed to be disrupted by FC lesions
(Ferraro and Berraro, 1934; Gilman and Denny-Brown, 1966; Marsden etal.,
1977; Nathan, et al., 1986), although it has yet to be systematically examined.
Without a proprioceptive image of the hand to combine with visuomotor cues,
the motor cortex may be unable to plan the appropriate commands for grip

FC afferents may also be required for execution of the precise
movements needed to form a grasp. Once initiated, the movements are fast
(-180 ms), are not visually guided (Jeannerod and Biguer, 1982), and
involve movement at several unsupported joints. These constraints probably
intensify the dependence of these movements on transmission through the
FCs, given that precision movements that are executed more slowly, with
visual guidance and physical support, are substantially less impaired
following FC transaction (Leonard et a., 1991). Muscle afferents, in
particular, are believed to contribute to the execution of small movements
through cerebellar circuits (Hore and Vilis, 1984) or transcortical loops
(Evarts, 1985a). Within the motor cortex, a distinct set of corticomotoneurons
appears to be specialized for controlling precision grasp (Muir and Lemon,
1983), and these may be preferentially regulated by sensory feedback from
the FCs (Asanuma et a., 1980; Fromm and Evarts, 1978; Evarts, 1985a).
Following FC interruption, the grasping movements observed were
characteristic of power-grasping (Napier, 1956), which is believed to be
controlled by a separate set of corticomotoneurons (Muir and Lemon, 1983).
Perhaps the power grasping system is not as dependent on sensory
feedback as fine grasp (Lemon, 1981).
It is not clear from the present results whether the deficits in motor
planning or execution result from interruption of distinct FC-lemniscal or FC-
cerebellar projections. Specific lesions and experiments will be needed to
determine answers to these questions. For example, comparing the present
results with those of Jeannerod (1986) suggests some differences in the
consequences of lesions in the medial lemniscus vs. the FC. Jeannerod
described a patient in whom an occipital bone fracture resulted in apparently

selective damage to the medial lemniscus. This patient, like the monkeys
described in the present paper, either hyperextended the fingers or failed to
form a consistent grip aperture during grasp preparation, when vision of the
hand was occluded. Vision enabled normal grip formation, although the
duration of the pre-grasping period was increased, probably due to the
longer time needed to process visual feedback (Keele and Posner, 1968).
Unlike this patient, the FC-lesioned animals never performed normal grasp,
despite the fact that the hand was in full view. It may be that the animals were
never "motivated" to convert to visuomotor loops to compensate for the
somatosensory loss, since they were eventually rewarded (i.e., they collected
and ate the item) even if they used an abnormal grasp.
Alternatively, the FC lesioned animals may have been more impaired
than the patient described by Jeannerod because the lesions in the monkeys
involved an additional set of afferent projections to those interrupted by the
medial lemniscus lesion. Besides deafferenting cells with thalamic
projections in the medial lemniscus, FC lesions also interrupt afferents to
neurons that project to the cerebellum and other subcortical nuclei (see
above). Others have reported that motor deficits are more severe following
dorsal column lesions, as compared to either lesions of the main cuneate
nucleus (excluding the external cuneate nucleus) or the medial lemniscus
(Melzack and Bridges, 1971; Heckman and Bourassa, 1981), suggesting that
non-lemniscal projections of the dorsal columns are essential for motor
The results of the left-sided lesion of monkey M, with a small amount of
sparing in the deepest portion of the FC, may identify a portion of the FC that
is important for movement control. This monkey displayed no deficit in either

grasping or grooming (Leonard et al., 1991) beyond a slight clumsiness on
the first post-operative day. If the primate FC is organized as the cat FC, the
spared fibers in M-left would have included the post-synaptic dorsal column
pathway (Uddenburg, 1968a), and primary muscle afferent fibers (Rosen,
1969; Dykes et al., 1982), both of which have non-lemniscal terminations
(Rosen, 1969; Rustioni etal., 1979; Hummelsheim and Wiesendanger, 1985;
Fyffe et al., 1986). Further investigations are needed to determine whether
anatomically distinct portions of the FC are important for selective aspects of
fine motor control.
In conclusion, the results of this study show that interruption of the FC
alters precision grasping in monkeys. The observation that some grasping
remains after the lesion probably accounts for some earlier reports that
grasping is normal after FC interruption. The form of the residual grasping
movements, however, is clearly altered. These results indicate that the fine
coordination of finger movements is accomplished by a sensorimotor
integration, requiring afferent information ascending the FC.

Table 2-1. Percentage of times the monkeys missed a food object during a
grasp attempt with the left (L) or the right (R) hand. The total number of grasp
attempts for each condition is indicated in parentheses.

% of missed grasps

Monkey Side Pre-op Post-op

W L 4 20
(71) (80)

R --- 29

M L* 15 8
(54) (89)

R --- 51
S L 6 100
(16) (50)
R --- 61

* This monkey had an incomplete interruption of FC
afferents from the left side.

Table 2-2. Comparison of the percent
monkeys before and after FC lesions.

occurence of different grasp styles in
Only successful grasp attempts are

% of successful grasps

Finger Thumb-
Condition Monkey Hand (n) Tip-tip curl Palm dorsum Other

Pre-op W L (68) 94 2 1 0 3
M L (46) 81 13 6 0 0
S L (15) 94 0 6 0 0

Post-op W L (64) 14 19 61 5 1
R (66) 27 29 32 3 9

M L* (82) 80 1 18 0 1

R (51) 24 49 27 0 0

S L (0**)

R (36) 0 0 87 13 0

* Indicates a lesion that incompletely interrupted afferents from the left hand.
** Monkey S was unable to grasp any of the food items we offered him after an
extensive lesion on the left side.

Table 2-3. The duration of finger contact with the table surface before and
after FC lesions. The total number of grasps for each condition is in
parentheses. Medians were compared using Mann-Whitney U-tests (with
normal approximation). NS, P > 0.05; P 5 0.05; ** P 0.01.

Median length (ms)

Monkey Hand Pre-op Post-op z-value

W L 60 120 -2.84 *
(15) (12)

R --- 105 -3.17**

M L+ 30 60 -1.30 NS
(12) (13)

R --- 90 -3.16**
S L 30 --
R ---- 330 -3.84 **

+ Indicates an incomplete interruption of FC afferents from the left hand.

Table 2-4. Mean DIP joint angles SE at the end of a grasp in monkeys W
and M before and after FC lesions. Pre-operative DIP joint angles from the
left hand of each monkey were compared to the post-operative angles from
the left and right hand with unpaired t-tests. The number of grasps for each
treatment condition is indicated in parentheses. NS P > 0.05; P < 0.01; **
P < 0.0001.

DIP joint angle (0)

Monkey Hand Pre-op Post-op t-value

W L 181.5 3.6 145.0 20.4 2.91 *
(20) (6)

R --- 226.2 3.0 -9.52 **
M L+ 167.8 5.5 152.7 4.6 1.88 NS
(16) (12)

R --- 120.2 3.1 5.55**

+ Indicates an incomplete interruption of FC afferents from the hand.

Figure 2-1. Four grasp styles most commonly used by monkeys during pre-
and post-operative testing. TIP-TIP prehension is the same precision grasp
used by humans and described by Napier (1956). FINGER-CURL grasping
involves curling the object into the crease of the second and/or the third
fingers. In the PALM style, the object was brought into the palm by the
fingers. THUMB-TO-DORSUM was a less common style in which the
object was placed between the thumb and a closed fist.


Tip-Tip Finger-Curl

Palm Thumb to Dorsum

Figure 2-2. FC lesions on each side of three monkeys. The figures are
drawn directly from projected spinal cord sections. The cervical level of
each lesion is written in each box.





C3 1 C4


Figure 2-3. Videotaped frames of a normal grasp approach and positioning
of the fingers for a precision type (TIP-TIP) grasp by Monkey W (left side).
Frames A-D are separated by 60 ms.





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yi g i L ^-


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S gs

Sts I0

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(wLUw) eJnliedy d!Ju

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Figure 2-5. Videotaped frames of abnormal grip formation in Monkey S
(post-operative right hand) performing a PALM grasp. 60 ms separated
frames A-D.



Figure 2-6. Median number of degrees moved at each joint during the
period of table contact for two monkeys. Differences were measured by a
Mann-Whitney U-test. + P< 0.01; P < 0.005; ** P < 0.0005.




SI.tLe Post

MCP PJoint



Interruption of the FC, a sensory pathway that carries information from
the skin, muscles, and joints of the forelimb, produces a variety of deficits in
natural and learned finger movements in primates (Chapter 2, Cooper et al.,
1991, Leonard et al., 1991, Vierck, 1975, 1978). Many of these deficits are
characterized by inaccurate positioning of the hands and fingers. Examples
include 1) loss of precise thumb and finger apposition during both grasp
preparation (Chapter 2) and "plucking" (one type of precision grasping
common during grooming; Leonard et al., 1991), 2) inability to posture the
hand to fit into small compartments (Vierck, 1978), 3) inaccurate placement of
the fingers in wire meshing during climbing (Gilman and Denny-Brown, 1966
and personal observation), and 4) inability to fractionate the fingers, i.e., hold
some fingers still, while moving others (Cooper et al., 1991). In this chapter, I
examine the hypothesis that these fine motor disturbances reflect a primary
inability to adopt and maintain positions (or postures) with the fingers
accurately. I test the prediction that FC lesions will disturb and/or eliminate:
1) the ability to adjust the position of the finger during changing conditions,
and 2) transcortical reflexes, which are believed to participate in these
There is some evidence that FC interruption disrupts the ability to
finely adjust the magnitude of activity in the finger muscles. First, monkeys

use greater than normal forces to push buttons with the fingers when
performing ballistic movements (Cooper et al., 1991). Second, force
regulation with the hand is less accurate after FC lesions in monkeys (Dyhre-
Poulsen, 1965). Thus, poor finger positioning could be related to an inability
to gradate finger movements.
Fine regulation of finger movements is expected to depend on
sensory feedback to the motor cortex (Evarts, 1985b; Sanes et al., 1985),
although this hypothesis has never been tested directly. Evidence suggests
that proprioceptive feedback to the cortex is gated, so that it increases in
proportion to the demands for precision control. Corticomotoneurons
(CMNs), motor cortex cells which form the direct pathway to finger
motoneurons (Clough 1971; Koeze et al., 1968), are more responsive to
kinesthetic input during precision movements than during large, fast
movements (Cheney and Fetz, 1980; Fromm and Evarts, 1978). This
feedback is most likely carried in the FC, as it forms a direct pathway to the
motor cortex (Asanuma et al., 1980; Brinkman et al., 1978). An open and
pertinent question, then, is whether FC lesions impair the ability to finely
adjust finger position. Such a disturbance would explain many of the
selective deficits in finger movements following FC interruption.
Long-latency reflexes are late muscular responses to limb
perturbations that are larger than the early, segmental reflex (Hammond,
1955). They are believed to reflect the feedback regulation of the motor
cortex by proprioceptive afferents (Evarts, 1973; Mathews, 1991; Phillips,
1969). Consistent with the hypothesis that this input to the cortex is critical for
fine movements, the reflexes are more effective in restoring position for small,
rather than large, disturbances of the finger (Marsden et al., 1981). The first

of these responses, termed M2 by Tatton et al. (1975), appears to be "servo-
like", with properties similar to the segmental reflex (Evarts and Tanji, 1976;
Strick, 1978). The M2 response is thought to be elicited by signals that pass
first through the FC, and relay in the postcentral gyrus to reach the motor
cortex. This purported route is based on evidence that presumed lesions of
the dorsal columns, and lesions of the post-central gyrus, abolish the M2
response (Marsden, 1977b; Tatton et al., 1975). Despite this speculation, the
hypothesis that the reflex requires an intact FC has never been tested in
cases of verified lesions.
In this study, macaques were trained to maintain postures with the
index finger. The ability to adjust the finger to changing external loads was
tested, and the M2 response was elicited and measured
electromyographically. Both the behavioral performance and the presence of
the M2 were examined after FC lesions.


Three female adult stumptail macaques (Macaca arctoides; B, T, and
S) were subjects in this study. The monkeys had not been involved
previously in any behavioral testing or neurobiological experimentation.
They were housed in large outdoor enclosures, each with one other
Each monkey worked best under one of two feeding regimens:
monkeys T and S worked for their daily monkey chow, and monkey B for
small pieces of fruit. Following testing, each received the remainder of the

daily monkey chow, and was then food deprived for 22 hours before training
on the subsequent day. Excess water was always available.

Finger positioning task
Each monkey was trained daily to sit calmly in a chair with the left arm,
wrist, and fingers immobilized with custom-fitted splints (Figure 3-1 A). The
apparatus permitted only flexion and extension movements of the index
finger at the metacarpophalangeal (MCP) joint.
Each monkey was trained on two positioning tasks. Both tasks
required the monkey to hold the index finger in 100 ( 50) of MCP flexion
against external torques for 3 seconds to receive a food reward (Figure 3-
2A). In the hold task, the experimenter manually moved the finger into the
target zone, using a small handle attached to the transducer axle (Figure 3-
1A), and then initiated a trial. In the move and hold task, the monkey had to
move its finger into the target zone; in so doing, it initiated the trial. Again, the
finger position had to be maintained for 3 seconds to receive a reward. The
trial initiation procedures were designed to lessen the probability that trials
would be run while the monkey was still eating, or otherwise not attending to
the tasks. For the hold task, the experimenter waited to initiate a trial until the
monkey exerted some pressure against the splint. For the move and hold
task, the experimenter waited until the monkey appeared to be attentive and
then turned a switch, which set the program into a "ready" mode and also
served as an auditory cue for the monkey to move. The monkey could then
initiate a trial whenever it chose by moving its finger.
For both tasks, trial onset was signalled by a "hold" tone that lasted for
as long as the finger was in the correct position. If the finger remained still for

the duration of the trial, a second tone was sounded, the "correct" tone, and
the monkey was rewarded. Movement outside of the target zone at any time
turned off the "hold" tone, elicited a third tone (the "error" tone), and caused
the trial to be aborted.
All of the monkeys learned to perform both tasks in flexion. Monkey B
also learned to extend the finger for the two tasks. The other two monkeys
would not hold against loads that opposed extension despite 4 months of
attempted training, possibly because extension is a less natural movement.
The resistive loads (0.33, 0.66, and 1.0 Nm) that opposed finger
positioning were generated by a brushless DC torque motor (Aeroflex
TQ34W-1 HA) that was controlled by a computer program (Exgen; Cooper et
a/., 1986). A torque was either maintained throughout the trial (constant
torque condition; Figure 3-28) or it increased during the hold portion of either
task (variable torque condition). In the latter condition, the torque increased
0.66 Nm (from 0.33 to 1.0 Nm) over 840 ms. Because the extensor muscles
were weaker than the flexors, only the two lower levels of constant torque
were used for monkey B when performing the tasks in extension.
As the finger and hand were positioned underneath the torque motor
and angular transducer, they were not visible to the monkeys. Visual
feedback could be provided with a panel of small, horizontally aligned LEDs
(Figure 3-1 B) attached to the testing chair. The panel was positioned at the
monkey's eye level, approximately 10" from its face. The LEDs were
controlled by the output of the angular transducer, and indicated finger
position to the monkey; they were lit in sequence by each progressive 20 of

All monkeys were trained to perform the two tasks with visual feedback
from the display panel. The panel was turned off after they had learned the
task, so that all pre-operative scores were collected without visual feedback.
The feedback was reintroduced post-operatively to aid recovery. When a
monkey reached >50% success on a given task (and condition), the panel
was again turned off.

Testing schedule
Each test day consisted of 15-30 trials per monkey, both pre- and post-
operatively. Pre-operatively, for the more difficult combinations of tasks and
conditions (i.e., the move and hold task performed at the highest constant
torque condition, or either task under the variable torque condition), only one
task and condition were tested daily. With the easier constant torque
conditions, the monkeys generally performed two tasks or two conditions a
day (15 of each). Post-operatively, the monkeys usually performed one task
a day. However, when the monkeys were tested on tasks and conditions in
which they constantly failed (and therefore, did not receive food rewards),
some trials of an easier task were run at the end of the session, to prevent
extinction of the monkey's performance.

Recordings of muscle activity and finger movements
Throughout the pre- and post-operative training, electromyographic
(EMG) signals and finger position were recorded during single trials. Three
days of EMG data, and 3-5 days of finger position data, were collected for
each task and condition both pre-operatively and post-operatively for
monkeys T and B. For monkey S, the first animal to receive a lesion, pre-

operative data were not collected at the lower torque levels. This was
because the extent of the movement deficits was unexpected, and the lower
torque levels had been considered useful for training purposes only.
Therefore, at the 0.33 and 0.66 Nm torque levels, the task was scored but
EMG and finger movement data were not collected. Post-operatively, data
was collected on all conditions for monkey S.
EMG signals were recorded with surface bipolar electrodes (gold disc:
Grass Instruments) pasted onto tattoed marks over the first digit intrinsic
muscles. These muscles, the first dorsal interosseous and lumbricalis, are
the prime movers for MCP flexion when the distal finger joints are straight
(Kendall and McCreary, 1983). For monkey T, the synergistic extrinsic flexor
muscles were also recorded. The tattoo marks maintained consistency in the
recording sites from day to day. For the tattooing procedure, the monkeys
were anesthetized with ketamine hydrochloride, the skin was shaved and
cleansed thoroughly, and two small marks, separated by 1.5 cm, were tattood
onto the skin lateral to the first metacarpal. To locate the best recording site
over the extrinsic flexor muscles for monkey T, the median nerve was
stimulated proximal to the muscles, and the electrodes were used to record
activity at different sites over the muscle bellies. Tattoos were placed over
the best recording sites. This procedure could not be used to locate the best
recording site for the intrinsic muscles because the hands were so small that
the electrodes could fit in only one possible position over the muscles.
Nevertheless, the tattoos were needed to locate this position in the awake,
moving animal.
EMG signals were digitized on line (sampling rate 550 Hz), amplified
(Grass P511 Preamplifier; bandpass 30 Hz-30 kHz), and recorded on a

digital oscilloscope (Computerscope; RC Electronics). Voltage input to the
torque motor and the position signals from the angular transducer were
recorded simultaneously. The trial onset triggered data collection.

Recording of EMG responses to perturbations

Muscular responses to perturbations were measured in monkeys B
and T both pre- and post-operatively. In monkey S, only post-operative
measures were taken. When monkeys B and T had been well trained pre-
operatively, reflexes were recorded for 7-17 days, until at least 60 responses
had been recorded. Generally, several days separated each session.
Reflexes were not recorded until after one month post-operatively for any of
the monkeys.
On the days that reflexes were measured, the monkeys performed the
hold task against the 0.33 Nm constant load. To elicit a reflex, 0.33 Nm was
applied for 2 seconds, and then increased abruptly to 1.65 Nm for 500 ms
(Figure 3-2B). A program was created that generated one torque pulse after
every 2-5 presentations of the constant load. This enabled monkeys to be
rewarded for several trials in between perturbations, which usually pushed
the finger outside of the correct zone.

Surgery and histology
FC lesions were made surgically under sterile conditions. Monkeys
were anesthetized with halothane hydrochloride and a laminectomy was
performed at one or two upper cervical vertebra. With the use of a dissecting
microscope, the dura was reflected, and the left FC was severed using

precision forceps (see preceding Chapter for details). Testing was resumed
10 days following surgery.
After 4-9 months of post-operative data collection, the monkeys were
euthanized with an overdose of barbiturate and perfused through the
descending aorta with 10% formalin, or 4% glutaraldehyde/1.25%
paraformaldehyde. Spinal cord tissue was cut with a freezing microtome,
and alternate sections were stained with cresyl violet and hematoxylin (Weil).
Lesions were visualized and drawn from an image projected by a Leitz

Data Analysis
Scores. The percentage correct on a particular task was defined as the
number correct/total number of trials, for each daily session in which the
animal attempted to position the finger. Since the scores for each condition
were not normally distributed, median percentages of correct responses were
used to make pre- vs. post-operative comparisons. The Mann-Whitney U-test
was used to test for differences (P 5 0.05).

Movement Records. To determine whether performance on the hold
task differed post-operatively, position traces during successful hold trials
were examined at the higher torque levels for each monkey. Two
measurements of the successful responses to applied loads were obtained:
1) compensation, and 2) amplitude. First, the amount of compensation
involved in positioning was determined by classifying trials as either
compensated or uncompensated. If the finger drifted slowly, succumbing to
the load, the trial was classified as uncompensated. Movements were

considered to involve compensation if 1) the finger was held still against the
load for the three seconds, 2) the finger pushed the load in the opposite
direction, or 3) the finger fluctuated, with any combination of pushing and
holding. Chi-square tests were used to compare the pre- and post-operative
performances (P < 0.05). Second, the overall amplitude of the finger
movement during successful hold trials was measured as the difference (in
degrees) of finger movement from the start to the finish of single trials.
Unpaired two-tailed t-tests were used to make pre- and post-operative
comparisons (P < 0.05).
On the move and hold task, two types of post-operative errors were
identified. If the finger reached the target zone but was then displaced out of
the zone, in the direction of the load, the error was defined as a slip. An
overshoot occurred if the amplitude of the initial movement was excessive,
i.e., the finger moved beyond the target. Chi-square tests were used to
evaluate the effects of the lesion on the number of slips and overshoots (P <

EMG and Reflexes. EMG signals were viewed before actual recording
because the signals varied from day to day--probably due to such factors as
slight changes in electrode position, skin resistance, and/or distance
between the two electrodes (Basmajian and DeLuca, 1983). Amplification
was varied (20,000 50,000 x) to bring the overall range of activity during
movement into the 0 to 5 volt range. The EMG data were full-wave rectified
and viewed off-line, together with the position and torque traces.
Reflex data were averaged across trials and days. If single channels
were either noisy or had been physically interrupted, they were not included

in the averages. Because EMG signals were averaged across days, and the
signal varied in size from day to day, they were examined qualitatively. Pre-
operative and post-operative comparisons involved the presence or absence
of a signal, but absolute voltages were not compared.


The finger naturally assumed the target position of 100 of MCP flexion
when it was relaxed; therefore the two postural tasks always involved
opposing a resistive load. Preoperatively, each monkey learned to perform
both tasks under both torque conditions. Percentages correct were
consistently > 70% (top panels of Figures 3-4 and 3-8). One monkey (B) also
successfully learned the two tasks against loads opposing finger extension,
but only for the constant torque conditions (Figure 3-5).

All of the FC lesions were between C4 and C6 (Figure 3-3). Monkeys
S and T had complete lesions of the FC. In Monkey S, the ventral extent of
the lesion also included the central grey matter and a small portion of the
ventral white matter. The lesion of Monkey B was incomplete, with sparing of
the ventral FC. However, histological examination of the brain of this monkey
revealed several cystic-like cavitations, and one of these extended the
central canal into the FC rostral to the lesion. It could not be determined
whether any of the additional FC fibers spared by the lesion were damaged
by the cavity.

Post-operative Task Performance
Retesting of the monkeys began 7-10 days after the surgery. On the
first day of retesting, the hold task was delivered at the lowest constant torque
level (0.33 Nm). Training progressed to also include the move and hold task.
Successively higher levels of constant torque were progressively
reintroduced on both tasks, and by the second month, the variable torque
tasks were also included. Monkey B did not perform against extension loads
until after the 1st post-operative month.
Visual feedback was always provided as tasks and conditions were
first reintroduced. If performance improved to >50% correct, the LED panel
would be turned off for the next presentation of the same set of trials, and
then restored on alternate days. In this way, the effect of the feedback could
be assessed. Comparisons between post-operative scores with and without
visual feedback showed that it had no consistent effect on the scores (Table
3-1). Therefore, data from both conditions were pooled for final scoring.

First month performance
Constant torque condition. During the first post-operative month, each
monkey was tested on both tasks under the constant torque condition. On
the hold task at the lowest torque (0.33 Nm), performance in two of the three
monkeys (S and T) equalled pre-operative levels (80-100%; Figure 3-4). The
third monkey only achieved scores of 11% correct. At the 0.66 Nm level on
the hold task, monkeys S and T also achieved some success (20-40 %),
whereas monkey B did not. None of the monkeys succeeded in positioning
the finger at the highest torque load.

FC lesions decreased performance on the move and hold task much
more than on the hold task. Each of the monkeys failed on the move and
hold task under all torque levels (Figure 3-4).

Post-operative performance for months 2-9
Constant torque condition. The performance of monkeys T and B
improved during months 2-9. For monkey T, the change was minimal, with
improvement up to pre-operative levels at the 0.66 Nm level on the hold task.
Monkey T never achieved pre-operative scores on the move and hold task (at
any of the torque levels) over 2 more months of observation.
There was a dramatic change in the performance of monkey B (with a
partial FC lesion) during months 2-9. Pre-operative scores were achieved for
all torque levels on the hold task. Monkey B also achieved pre-operative
scores on the move and hold task at the lowest torque level. However, at the
0.66 Nm and 1.0 Nm levels scores remained significantly decreased (60%
and 40%) over 7 more months of observation.
FC lesions impaired positioning performance in extension more than
in flexion. Extension scores for monkey B, the only subject that learned to
perform the two tasks in both directions, are shown in Figure 3-5. The post-
operative performance of this monkey did not reach pre-operative success
levels on either task. Performance deteriorated to 0% correct on all of the
tasks and conditions, except for the 0.33 Nm hold task at which the median
score was 40%.
Degree of compensation on hold task. Most of the successful trials
involved compensation pre-operatively (Table 3-2). Post-operatively,
monkey T compensated on significantly fewer trials after a complete FC

lesion, whereas compensation was unchanged following a partial lesion for
monkey B. Since there were no pre-operative data on compensation for
monkey S, its post-operative number of compensated trials was compared to
each of the other two monkeys; it had significantly fewer trials involving
compensation than monkey B (X2=8.4; P=0.004), but a similar number to
monkey T (X2=2.3; P=0.126). Therefore, both monkeys with total lesions
showed a deficiency in compensation, whereas the monkey with a partial
lesion continued to effectively adjust finger position on successful trials.
The degree to which the fingers were displaced by the opposing load
also differed with lesion extent (Table 3-3). Following a total FC lesion, the
finger of monkey T was displaced significantly further than it had been pre-
operatively. Similarly, the finger of monkey S drifted a large amount post-
operatively, and this amplitude was not statistically different from that of
monkey T (t=1; df=50; P > 0.05). Unlike the two monkeys with complete
lesions, monkey B did not slip more post-operatively.
The increased finger displacement in the monkeys with complete FC
lesions was obvious on single position and EMG traces (Figure 3-6). Activity
in the intrinsic muscles decreased progressively as the finger slipped.
One explanation for the increased finger displacement could have
been muscular weakness. This possibility was ruled out, however, since
monkeys were often observed pushing and holding the finger against the 1.0
Nm load in between trials. An example of this behavior is provided in Figure
Types of errors on the move and hold task. On the move and hold task,
errors involved both overshoots and slips. Both occurred at the lower torque
levels, whereas slips constituted the majority at the highest torque level

(Table 3-4). Undershoots could not be measured because of the nature of
the task. The monkeys were not trained to move upon demand, but self-
initiated the trials by moving to the target. Thus, small movements that did not
reach the targets could have been undershoots or non-attempts (i.e., random
Variable torque condition. Because of the failure of monkeys S and T
to successfully oppose the 1.0 Nm load during the hold task, the maximum
level to which the variable torque rose was reduced to 0.66 Nm, the highest
torque level at which these monkeys achieved post-operative success on the
hold task. The torque increased (from 0.33 0.66 Nm) at the same rate as
utilized pre-operatively (Figure 3-2). Despite this adjustment, both monkeys
failed on the two tasks when the torque was varied (Figure 3-8).
For monkey B (partial FC lesion), post-operative performance declined
on the hold task with variable torques, but this decline was not significant
(79% pre-operative vs. 57% post-operative). However, the post-operative
scores on the move and hold task decreased significantly (16% correct). For
all monkeys, errors in the variable torque condition were the result of finger
drift in the direction of the increasing load.

The M2 Response
Pre-operatively, monkey T showed a strong M2 response at 35-40 ms
in the intrinsic muscles and at 30-35 ms in the flexor muscles (Figure 3-9).
This is consistent with previously reported onsets (30-40 ms) for the M2 reflex
in the arm and forearm muscles of monkeys (Evarts, 1973; Lee and Tatton,
1975; Miller and Brooks, 1981; Tatton et al., 1975, 1978). Post-operatively,
these responses could not be identified even when a large number of trials

(67-100) were averaged. A gradual increase in activity was apparent at 60-
80 ms. Although pre-operative reflexes were not collected for the other
monkey with a complete lesion (S), the post-operative responses were
similar to those of monkey T (Figure 3-10). No response above the baseline
level was obvious at the normal M2 latency, but EMG activity appeared to
increase at 60-80 ms.
After FC interruption in monkeys S and T, the finger was displaced
abnormally by the perturbation (top traces of Figures 3-9 & 3-10). For
monkey S, this comparison was made by juxtaposing the post-operative
finger position trace to the averaged pre-operative finger position trace of the
other two monkeys.
In contrast to the two monkeys with complete lesions, monkey B
displayed an M2 response in the intrinsic muscles post-operatively. Although
the reflexes were less clear in this animal, increased activity was obvious at
the 30-35 ms latency both pre- and post-operatively (Figure 3-11). The finger
was not displaced more than it had been pre-operatively (top trace of Figure


The principal findings of this study are that complete FC lesions
produce 1) diminished postural control of the index finger, 2) reduced
compensation to changing external loads, and 3) a loss of the typical M2
long-latency response of the index finger. Further, the ability to adjust the
finger to externally applied loads was related to the presence of the M2

response. When the M2 response was present, following a partial lesion,
postural control was normal under most conditions.

Movement Performance and Long-latency Reflexes
Monkeys with total FC lesions generally failed to react to imposed
loads by adjusting finger position throughout the trials. Instead, the EMG
activity in the finger muscles diminished and the finger was displaced
gradually by the opposing torque. Whereas the lower loads did not torque
the finger outside of the correct window, the higher loads (1.0 Nm) and the
variable loads did, resulting in errors.
FC fibers carry information from both deep and superficial afferents,
and both have been shown to influence motor cortex cells (Fetz etal., 1980).
The failure to respond to the gradual displacements covaried with the
disappearance of the M2 long-latency reflex, which is believed to be
mediated by muscle afferents (Mathews, 1989). In the monkeys without the
reflexes, the finger slipped, whereas the monkey with intact reflexes
effectively compensated for most of the torque loads. Thus, the M2 reflex
may contribute to the compensation for small displacements, a conclusion
consistent with a servo-function.
Many investigators have concluded that the M2 is a servo-like
response that passes transcortically (Evarts and Tanji, 1976; Strick, 1978;
Tatton et al., 1978). The M2 response is believed to be initiated by pyramidal
tract neurons that are activated by muscle stretch in much the same way as
motoneurons in the segmental stretch reflex; that is, they respond when the
muscle they control is stretched, irrespective of whether the animal intends to
move in that direction. Marsden et al. (1981) have shown that the reflex is

effective in restoring position, particularly for smaller disturbances of the
Despite the strong relationship between the presence of the M2 and
the ability to adjust finger position, the absence of the M2 response cannot
explain entirely the post-operative movement deficits. Even with a retained
M2 reflex, and presumed sparing of some proprioceptive afferents, the
performance of the monkey with partial tract damage was not normal.
Performance deteriorated on the move and hold task in flexion, and was
significantly decreased on both tasks in extension. Disruption of cutaneous
feedback in all of the monkeys probably also affected finger movements.
Cutaneous input facilitates motoneurons (Johansson and Westling, 1987;
Kanda and Desmedt, 1983). This effect is believed to be mediated partly
through transcortical loops, since long-latency responses to exteroceptive
stimuli have been demonstrated in the fingers (Jenner and Stephens, 1982;
Marsden et al. 1977a), and CMNs respond at short-latency to exteroceptive
inputs (Strick and Preston, 1983; Wise and Tanji, 1981). A consequence of
this influence is that subjects report that more strength is needed to lift a
weight when the skin of the finger is anesthetized (Gandevia and McCloskey,

Role of Proprioception
In addition to the loss of automatic adjustments, compromised
proprioception may have hampered volitional adjustments of finger position.
Proprioceptive tests, described in the next chapter, showed that a monkey
with a completely severed FC could not correctly judge the direction of
passive finger movements when they were slow (< 70/s). Thus, the monkeys

in this experiment might not have sensed the gradual finger slippage.
However, diminished proprioception would not explain the lack of reaction to
faster displacements, as these were easily detected on the proprioceptive
tests. For the monkey who was tested for proprioception, many of the slips
during the hold task were at velocities 7/s (mean 14.80/s).
If a proprioceptive deficit alone had been responsible for the results,
performance should have also been improved in the presence of visual
feedback, as has been the case in experiments with deafferented patients
(Rothwell et al., 1982; Sanes et al., 1985). In those human experiments,
however, an analog signal of limb position was provided to the subjects. It is
possible that the LEDs used in this study, which turned on with every 20 of
movement, were inappropriate for signaling movement to the monkeys.
Alternatively, it is possible that they did not attend to the visual display panel
after learning to perform without it. This could not be assessed with certainty
because the room was dark, but the experimenter saw no evidence that the
monkeys looked at the LED panel post-operatively.
In summary, the deficits in motor control following FC lesions were
probably related to losses of both muscular and cutaneous feedback. The
former seemed to be needed to support automatic adjustments to opposing
loads during postural holding. Cutaneous feedback may have added a
generalized facilitation to muscular activity under normal conditions
(Gandevia and McCloskey, 1977). Either of these afferent groups might have
normally contributed to proprioception of the finger (Clark et al., 1985; Ferrell
and Smith, 1987; Gandevia and McCloskey, 1976a). Thus, diminished
proprioception could have also contributed to the decay in postural control.

The observation that the lesioned animals pushed and held the finger
against even the highest torques in between trials (Figure 3-7) ruled out the
possibility that generalized weakness was responsible for the deficits. The
animals also routinely used the hands to support their body weight as they
climbed about the sides and roofs of the cages, suggesting that their strength
was normal.

Early vs. Late Post-operative Performance
For the first month after the lesion, all the monkeys performed poorly
on all the tasks. Beginning at two months, performance began to improve,
particularly for the monkey with the partial lesion. This recovery was not
progressive, i.e., performance at 2 and 9 months was comparable. The
timing of this change cannot be defined absolutely, since the monkeys were
tested on several tasks and the progress on one task could not be tracked
daily. Nevertheless, the duration of the effect coincides with the early
recovery period following dorsal column lesions described by Vierck (1982b).
It is believed to reflect an anatomical or physiological change, such as
sprouting (Berkley and Vierck, 1987; Vierck, 1982b).

Differential Performance on the Hold and Move and Hold Tasks
All monkeys demonstrated a more severe deficit on the move and hold
task than on the hold task. The two monkeys with complete lesions failed on
the move and hold task at all the torque levels, and the partially lesioned
monkey only succeeded at the lowest torque level. The type of errors on this
task varied, with both overshoots and slips occurring at the two lower loads,
and slipping predominating at the loads (Table 3-4). These results were

similar to those of Sanes et al. (1985), who studied patients with large fiber
sensory neuropathy. In their patients, posture was disrupted more severely
when it was preceded by a small active movement.
Two factors probably contributed to the differential performance on the
two tasks. First, overshooting errors may have been related to an inability to
control the end-points of movement. Deafferented patients will overshoot
movement targets, apparently because an afferent signal normally regulates
the braking of the movement by the antagonist muscle (Forget and Lamarre,
Second, the feedback provided by the experimenter during the hold
task may have been important. During this task, the experimenter judged
when the monkey was "ready" (i.e., exerting force against the torque motor).
Under these conditions, the monkey might have controlled posture by
maintaining a centrally-generated effort that was sensed by the experimenter
(McCloskey et al., 1974; Watson et al., 1984). In the move and hold task, the
experimenter did not give the monkey feedback about the effort, so the CNS
was more dependent on proprioceptive feedback to judge the required
muscular effort.

Pathways for Long-latency Responses
The fact that the M2 response was lost following complete FC lesions
supports the view that this long-latency reflex traverses the cortex, as
proposed by Phillips (1969). To my knowledge, this is the first evidence that
the reflex disappears after verified FC lesions. Earlier reports have described
the attenuation or disappearance of the M2 in humans with presumed FC
lesions (Jenner and Stephens, 1982; Marsden et al. 1977b). However, those

lesions were never histologically confirmed and were likely to have extended
beyond the dorsal columns, since the symptomatology of the patients differed
from those produced by dorsal column lesions alone (cf. Vierk et al., 1990).
Other evidence supports the view that long-latency reflexes are
transcortical. First, the latency of the response corresponds to the sum of the
time needed for a signal to reach the cortex, and a response to reach the
muscles (Marsden et al, 1973). Second, the CMNs that project to a
perturbed muscle respond at an appropriate latency (20-25 ms) to contribute
to the efferent response (Cheney and Fetz, 1984; Evarts, 1973; Evarts and
Tanji, 1976). Third, the reflex also disappears following lesions of the
postcentral gyrus in monkeys (Tatton et al., 1975).
The argument opposing the transcortical view holds that the
responses are either delayed spinal reflexes resulting from the late arrival of
slower afferents to the spinal cord, or are repeated responses generated by
the intrinsic circuitry of the spinal cord. These alternatives are supported by
two observations. First, the responses have been obtained in spinalized cats
and monkeys (Ghez and Shinoda, 1978; Miller and Brooks, 1981; Tracey et
al., 1980b). However, in those experiments responses were obtained in
anesthetized preparations. Since humans and monkeys do not exhibit the
M2 reflexes unless they are moving volitionally, it is doubtful that the
preparations exhibited normal motoneuron activity. Second, some authors
have recorded repeated discharges in peripheral afferents (Hagbarth et al.,
1981), and concluded that later arriving afferent activity initiates the M2
response. The conditions producing these results, however, differ from those
used in the present study, as well as in most other studies reporting the M2
(Bawa and McKenzie, 1981; Evarts, 1973; Marsden et al., 1977b, 1981;

Tatton et al., 1975). Hagbarth et al. (1981) stretched muscles continuously,
instead of abruptly. The abrupt stretches that were used in this study do not
cause repeated burst activity in muscle afferents (Jahnke and Struppler,
Two other arguments support the view that the M2 traverses the cortex.
First, Mathews (1989) has recently shown that fast afferents elicit the long-
latency reflexes, refuting the hypothesis that later arrival of signals in slower
afferents could explain the long latencies. Second, investigators do not
usually observe M1 (stretch reflex) responses in the finger muscles (present
study; Mathews, 1989; Marsden et al., 1981, 1983). Neither of the alternative
hypotheses could explain the presence of the late response without an early
In the two monkeys that lost the M2 response, increased EMG activity
appeared at 60-80 ms. The most likely explanation is that the delay was
produced by afferents reaching the cortex through slower pathways.
Alternatively, the delayed activity may represent a voluntary response, as
proprioceptive reaction times in monkeys can be as short as 60 ms (Evarts
and Tanji, 1976). It is not clear, however, why an intentional response would
appear post-operatively, when it was absent pre-operatively. The monkeys
probably did not make volitional responses because the fingers were rapidly
displaced outside of the target zone by the perturbation, triggering an error
tone and aborting the trial. An intentional response would have been futile.

Comparison of Present Results to Earlier Reports

Although humans and primates have long been known to display
abnormal hand and finger movements following FC lesions (Ferraro and

Berrera, 1934; and clinical literature reviewed in Nathan et al., 1986), only
recently have studies sought to characterize the impairments. The following
is a list of those aspects of movements in primates that are selectively
affected by the lesions: 1) hand posturing during grooming movements
("sweeping" and "scratching"; Leonard et al., 1991), 2) finger fractionation
(Vierck et al., 1987; Cooper et al., 1991), 3) individuation of movements (i.e.,
flexion and extension) among the three joints of the fingers (previous chapter
and Cooper et al., 1991), 4) precise thumb-to-finger tip posturing during
grooming and grasp preparation (Chapter 2 and Leonard et al., 1991), 5)
hand posturing for insertion into small compartments (Vierck, 1978), and 6)
active tracking of tactile cues to the finger (Cooper et al., 1989). Other
observations include odd posturing of the hand and fingers when they are
not in use (Leonard et al., 1991) and misplacement of the fingers between
the wires of an enclosure during climbing (Ferraro and Berrera, 1934; Gilman
and Denny-Brown, 1966 and personal observation).
Many of the postural deficits could result from the inability to sense and
react to perturbations as shown in the present study. Other movement
deficits are likely to have other explanations. The partially lesioned monkey
in this study was able to posture the fingers, and had retained the M2
response, but was observed having difficulty making fine grasping
movements, and did not appear to fractionate or individuate finger
movements. Therefore, the fibers that were damaged by the lesions
appeared to be critical for aspects of grasping other than posturing; for
example, fractionating finger movements and individuating multi-joint
movements. Vierck (1978) also described abnormal grasping with the
hindlimb following thoracic dorsal column lesions, which leave muscle and

joint afferents intact and affect primarily cutaneous afferents (Whitsel et al.,
Thus, certain fine movements must depend on other attributes of the
FCs besides the proprioceptive long-latency reflexes. For instance, the FCs
may provide cutaneous feedback critical for timing and orienting movements
during precision tasks (Vierck, 1978). Furthermore, maintenance of the map
of the individual fingers in the cortex appears to depend on temporal
disynchronies in afferent input (Clark et aL, 1988), and therefore may be
maintained by the precise spatio-temporal coding properties of FC afferents
(Vierck et al., 1985).

Table 3-1. Effect of removing visual feedback on postoperative performance.
Percent correct for the hold and the move and hold trials are shown during the
two feedback conditions. The difference between the medians is indicated in
the last column. Note that there is no consistent effect of feedback on the

Torque Visual No visual
Monkey Condition (N-m) feedback feedback Difference

B Hold 0.3 74.5 100 +25.5
0.6 86 79 -7
0.3-1.0 36.5 68.5 +10.5

Move & Hold 0.6 66 47 -13
1.0 52 30 -18
0.3-1.0 5.5 24 +18.5
T Hold 0.3 95.5 93 -2.5
0.6 67 75 +8
1.0 0 0 0
0.3-1.0 0 0 0

Move & Hold 0.3 20 22 +2
0.3-1.0 0 0 0
S Hold 0.3 95 80 -15
0.6 60 75 +15
1.0 6 11 +5
0.3 -1.0 0 0 0

Move & Hold 0.3 9 5.5 -3.5
0.6 0 0 0
0.3-1.0 0 0 0

Table 3-2. Percentage of successful trials in which the finger compensated
for opposing loads, by either pushing and/or remaining still. Pre- and post-
operative percentages are compared. The number of observations for each
condition is in parentheses. Note that monkeys with total lesions had a lower
percentage of compensated trials. Pre- and post-operative scores were
compared with chi-square tests. NS, P > 0.5; P 5 0.0001.

% trials compensated
Monkey Lesion (Nm) Pre-op Post-op X2

T total 0.66 92 19 27.3 *
(25) (26)
S total 0.66 --- 38
B partial 0.66 77 75 0.9 NS
(31) (33)
1.00 55 66 0.5 NS
(18) (12)

Table 3-3. Degrees of extension movement pre- and post-operatively during
successful trials on the flexion hold task. Mean SE amplitudes of finger
movement during a trial are indicated; the number of observations for each
condition is in parentheses. Note that the finger is moved further by the
opposing torque in monkeys with total lesions. Pre- and post-operative
means were compared with unpaired t-tests. NS, P > 0.05; P 5 0.001.

Degrees of movement
during successful holds
Monkey Lesion (Nm) Pre-op Post-op t-value

T total 0.66 0.2 0.7 3.7 0.6 3.70 *
(25) (26)
S total 0.66 --- 4.8 0.5
B partial 0.66 1.3 0.6 2.2 0.6 -0.50 NS
(31) (33)
1.00 0.9 0.5 0.3 1.3 1.10 NS
(18) (12)

Table 3-4. Error types made post-operatively during the move and hold
condition. The percentage of errors made by overshooting the target or
slipping below the correct window is shown for each monkey at each torque
level. The actual number of overshoots versus slips within each row was
compared with a chi-square test. NS, P > 0.05; P < 0.05; ** P 0.01.

(Nm) Monkey (n) Overshoots Slips X2

0.33 T (30) 93 7 22.5 **
S (21) 38 62 1.2 NS

0.66 B (37) 60 40 1.3 NS
T (12) 42 58 0.3 NS
S (39) 31 69 5.8 *

1.00 B (54) 26 74 12.5 **
T (12) 0 100 12.0 **
S (21) 0 100 21.0 **

Figure 3-1. A.Testing apparatus. A monkey's left hand was splinted at the
wrist and last 3 fingers. The index finger was splinted separately at the
distal joints, and attached to a torque motor and angular transducer, the
axes of which were aligned with the MCP joint. A small handle on the axle
enabled the experimenter to manually move the finger. A computer
controlled the output of the torque motor and received signals about finger
position from an angular transducer. Finger position signals were also sent
to the visual display panel. B. The visual display panel consisted of a
horizontally arranged row of LEDs. The target finger position was indicated
by large central array of 4 green LEDs (shaded). To the right and left of this
array, rows of 9 red and yellow LEDs turned on with increasing degrees of
movement in either flexion or extension.

Display Panel

. Angular Transducer
A.W ^


Visual Display Panel

O000000000 0000000001
(flexion) t (extension)


Figure 3-2. The positioning tasks and the various torque loads opposing
finger movement. A: The two positioning tasks. Each line represents the
finger position throughout a trial. Trial onset is indicated by an arrow. The
holdtask required the monkey to hold the finger in the target window (100
MCP flexion 50; shaded area) for 3 seconds. The move and hold task
required the monkey to either flex or extend the finger to reach the target
window. A trial was automatically initiated when the finger reached the
target. B: Three types of torque were exerted on the index finger. In the
constant torque condition, one of three torque levels was maintained
throughout a trial. In the variable torque condition, the torque began at a
low level (0.33 Nm) and increased gradually to 1.0 Nm over 840 ms. In the
reflex condition, the torque was held constant at 0.33 for the early part of the
trial and then increased abruptly to 1.65 Nm.


A. Positioning tasks

0 1
40 flex
20 eend
-20 ,

B. Torque loads exerted onto finger







Time (s)
Time (s)

Hold finger

Move &
hold finger




2 3




E w
2 c


O --
0) 0



0 -

(D o a0




CJ 0)



U) 0


-1 0

0 O1














.- E


a o



a 0.



I Sos




I c o-f /

S* E
0E D o


~ ~ a \ *^/\

|1|l l f \ l l [i

o- jO c /yco

0 0 0 0 0
Go jo IT CM 0 co 0 q cV

100JJoo %

l0olioo %

Figure 3-5. Median percentage correct for the two tasks performed in
extension by monkey B. Comparisons between pre- and post-operative (2-9
month) scores were made with the Mann-Whitney U-test. P 0.05.


Monkey B


p pre-operative








Move & Hold

0.3 0.6
Torque (Nm)













E o.

U 00


c oc

E c g

E > 'o

c. c' 5
i 5


& A S


0 -7
0. I



CL c

o 1I


Figure 3-7: Example of monkey S flexing the finger against the 1.0 Nm
torque, post-operatively. The sample was recorded for monkey S in
between test trials for the purpose of demonstrating that the monkeys had
adequate strength to hold the finger against the highest torque load. The
finger position trace is shown in the top trace and the rectified EMG of the
intrinsic muscles in the lower trace.


Rectified EMG
intrinsic muscles

0.0 0.5 1.0 1.5

2.0I I I 3.5
2.0 2.5 3.0 3.5

Time (s)



5 10




.E -


D 0 (0

S. B

.0 0


E 2

0 E
(D 75
> ,-^



Z 0



8 O Dl l

loeuoo %

<. 0 O)
0) 0)
So 0

" > ( c
- C 13

o co"- cL

.2 -- c. 0
>I I(

So >

3 t0 t0

Ca ( 0

015- c o

i- o Q 0 i
_c Z oM .2

O0= 2 11
s)C. 0
0. L o D

0C 0

L 0 Cu 0 a.11



* I

& 6


- I -8 0


...I o

* E9

Cu S


Figure 3-10. Finger position and rectified, averaged EMG during torque
perturbation, for Monkey S (with complete lesion). Only post-operative
traces are shown for this monkey. For comparison, pre-operative position
data from the other two monkeys was averaged (n = 153; solid line), and the
time in which those monkeys showed the M2 response is shaded in on
EMG trace. Post-operative averages for both the position (broken line) and
EMG traces included 57 sweeps. Onset of torque perturbation indicated by

Finger position


Rectified EMG
intrinsic muscles


-40 -20 0 20 40 60 80 100
Time (ms)

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