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Ontogenetic effects of midthoracic spinal cord compression on hindlimb sensorimotor function and spinal cord tissue loss

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Ontogenetic effects of midthoracic spinal cord compression on hindlimb sensorimotor function and spinal cord tissue loss
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McEwen, Melanie Lynn, 1969-
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Age groups ( jstor )
Inclined planes ( jstor )
Infants ( jstor )
Lesions ( jstor )
Locomotion ( jstor )
Physical trauma ( jstor )
Postoperative period ( jstor )
Rats ( jstor )
Spinal cord ( jstor )
Walking ( jstor )
Dissertations, Academic -- Psychology -- UF ( lcsh )
Psychology thesis, Ph.D ( lcsh )
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Thesis (Ph.D.)--University of Florida, 2000.
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Includes bibliographical references (leaves 98-111).
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Printout.
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Vita.
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by Melanie Lynn McEwen.

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ONTOGENETIC EFFECTS OF MIDTHORACIC SPINAL CORD COMPRESSION
ON HINDLIMB SENSORIMOTOR FUNCTION AND SPINAL CORD TISSUE LOSS
















By

MELANIE LYNN MCEWEN


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

UNIVERSITY OF FLORIDA



























Copyright 2000

By

Melanie Lynn McEwen













ACKNOWLEDGMENTS

I would like to thank my family for their constant love and support through this

journey, with special thanks to my parents for teaching me what it means to work hard

and to pursue your dreams. I would also like to thank my committee members, Dr.

Donald J. Stehouwer, Dr. Carol Van Hartesveldt, Dr. W. Keith Berg, Dr. Frans van

Haaren, and Dr. Dena R Howland, for their time and efforts in helping me achieve my

goals, as well as providing me with a standard of professionalism to which I will aspire. I

would like to extend special thanks to my advisor, Dr. Donald J. Stehouwer, for allowing

me the freedom to pursue my own research interests and for teaching me what it means to

be a good mentor. Many thanks are extended to two undergraduate students, Sarah Baker

and Laura Aldarondo, who helped me care for the animals when my experiments began.

My gratitude also goes out to the Center for Neurobiological Sciences and the

Department of Psychology for the financial support throughout the years and to my dance

teachers, Peggie Nolan Lamb, Stephanie Revelli, and Bill Adams, for the much needed

stress relief and for pushing me to excel physically, as well as mentally. I would like to

offer thanks to all of my friends, old and new, for their constant emotional support, care,

and understanding. Finally, I want to offer special thanks to a subset of that group, my

fellow graduate students. Although 'thank you' does not quite express my feelings of

gratitude, I want to thank all of them for all of the laughs, without which I could never

have made it this far.














TABLE OF CONTENTS




ACKNOW LEDGM ENTS ..................................................................... iii

ABSTRACT ..................................... ............ vi

CHAPTERS

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

Behavioral Sequelae Following Injury to the Mature Spinal Cord .............. 1
Behavioral Sequelae Following Injury to the Developing Spinal Cord ......... 5
Neuroanatomical Sequelae Postinjury .............................................. 7
Locomotor Development ......................................... ............. 8
Significance of Current Research ................................................... 11

2 MATERIALS AND METHODS ..................................... ........... 13

Subjects ............ .. ....................... ..... ................ .... 13
Surgery ......... .. ................... ...... .................. .... ......... 13
Behavioral Testing ........................................... ..... 14
Histology .................. .... .. ... ...... ............. ............... 19
Data Analyses ..... ...... ................. ...... ........... ....................... 20
Statistics ........................... ............. ........ .... ...... ..................... 23

3 RESULTS .................. ......... ................. ....... ............. 25

Righting ............... .. ..... ...... ... ........... .. 25
Overground W walking ............... ................. ....... .................. 28
Beam W walking ...................................... ................... ......... 31
Obstacle Avoidance ................... ........... .... ....... .............. 46
Parallel Bar W walking ............................ ........... .................. 50
Inclined Plane .......................................... ............. ................ ..... 52
Hot Plate ......................................................... 56
Lesion Size ................. ..... ............. ....................... 59








4 DISCUSSION .................................... ...... .. ... .............. 67

Age-Dependent Effects of Midthoracic Spinal Cord Compression .............. 68
Neuroanatomical Contributions to Recovery of Function ........................... 75
Sensorimotor Recovery Postinjury is Task-Dependent ............................. 83
M ethodological Considerations ...................................................... 87
Concluding Remarks and Implications ................ .......................... 89

APPENDICES

A BASSO, BEATTIE, AND BRESNAHAN (BBB) LOCOMOTOR RECOVERY
SCALE ........................................ 92

B NUMBER OF RATS IN EACH STATISTICAL ANALYSIS ...................... 94

C BODY WEIGHT IN GRAMS (+ SEM) ON EACH POSTOPERATIVE DAY ... 97

REFERENCES ....................................... ............... ...................... 98

BIOGRAPHICAL SKETCH .............................................. .................112













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

ONTOGENETIC EFFECTS OF MIDTHORACIC SPINAL CORD COMPRESSION
ON HINDLIMB SENSORIMOTOR FUNCTION AND SPINAL CORD TISSUE LOSS

By

Melanie Lynn McEwen

May 2000


Chairman: Donald J. Stehouwer
Major Department: Psychology

Traumatic spinal cord injury (SCI) in humans is most prevalent in young adult

males. Although human infants are not exempt from SCI, ontogenetic changes in the

behavioral and neuroanatomical sequelae following incomplete SCI have not been

evaluated. Injury to the developing cord may have unique consequences for behavioral

recovery, making necessary the elucidation of the effects of SCI in infancy. In the

present experiments, midthoracic spinal cords of 5-, 15-, or 60-day-old rats were

compressed with forceps by 0%/ (sham), 85%, or 95% of the uncompressed width. On

postoperative days 1, 7, 14, 21, and 28, hindlimb sensorimotor function was quantified

during beam- and parallel bar walking, on an inclined plane, and on a hot plate. Results

from those tasks were compared to ratings of overground walking, which are typically

used with adult animals following traumatic SCI. The amount of tissue at the lesion

epicenter was then quantified. Despite significant spinal cord damage, few tasks

distinguished between rats that received sham surgery or the lesser compression as

vi








neonates. Hindlimb sensorimotor function was severely disrupted on most tasks

following the lesser compression on postnatal day (PND) 60 or the greater compression

on PND 5, 15, or 60. In contrast, ratings of overground walking suggested that hindlimb

sensorimotor function was near-normal in rats that received the greater compression as

neonates or the lesser compression as young-adults. The amount of tissue at the lesion

epicenter decreased during ontogeny in rats that received the lesser compression, but did

not differ with age in rats that received the greater compression of the cord. Results of

the present experiments suggest that ratings of overground locomotion may not

accurately depict sensorimotor dysfunction postinjury and that additional deficits may be

revealed on tasks that challenge hindlimb function. Furthermore, hindlimb sensorimotor

function postinjury is not solely dependent on the amount of tissue at the lesion epicenter,

which presumably reflects the amount of communication between spinal and supraspinal

circuits. Ontogenetic changes in sensorimotor performance postinjury most likely

depend on the tissue reaction to injury and to the combination of neuroanatomical,

neurophysiological, and behavioral compensatory mechanisms invoked during recovery.













CHAPTER 1
INTRODUCTION


Behavioral Sequelae following Injury to the Mature Spinal Cord


Traumatic injury to the human spinal cord is most prevalent in young adult males.

Behavioral consequences of spinal cord injury (SCI) are dependent on the severity of the

impact, as well as the level of the spinal cord that is damaged. Consequences of thoracic

and lumbar injuries can range from paresis to paralysis of the legs, whereas cervical

injuries can result in quadriplegia. Other consequences immediately following injury

may include bladder and sexual dysfunctions. In the weeks that follow the injury, the

patient may recover some motor function, but recovery is dependent on severity of injury.

However, muscular spasticity and chronic pain may develop and hinder functional

locomotion. Magnetic resonance imaging with clinical evaluation has enabled clinicians

to better predict neurologic recovery following injury. However, resolution of the injury

site is limited (Croul & Flanders, 1997). Because SCI is so prevalent, animal models of

spinal cord contusion/compression have been developed to aid understanding of the

behavioral changes and the underlying pathophysiological mechanisms that follow SCI.

Models of spinal cord contusion/compression, rather than transaction, are used because

the human spinal cord is rarely transected following injury and the neuroanatomical

changes that occur in the spinal cord following incomplete SCI in animals closely

resemble the changes that occur in the human spinal cord. Generally, there is preferential








degeneration of spinal cord gray matter, with the amount of gray and white matter

remaining at the lesion epicenter dependent on the severity of the injury.

Early attempts to study SCI in animals were crude relative to current standards (see

Dohrmann, 1972). Allen (1911) was the first to attempt to produce a clinically relevant

and reproducible model of human SCI by dropping a weight from various heights onto

the exposed spinal cord of adult female dogs. With this model, the spinal cord lesion is

due to the force of the rapid impact, the concomitant dorsoventral compression of the

spinal cord, and the propagation of shock waves through the tissues and fluids.

Significant correlations have been found among (1) height from which the weight is

dropped and lesion length or white matter spared at the lesion epicenter; (2) behavioral

score on an open field test and lesion length, gray matter at the lesion epicenter, or

remaining white matter; and (3) the degree of incline that balance and position were

maintained on an inclined plane and remaining gray- or white matter at the lesion

epicenter (Noble & Wrathall, 1985; also see Basso, Beattie, & Bresnahan, 1996).

Depending on the severity of injury, adult animals recover some hindlimb function

during the 3- to 4-week postoperative period (Gale, Kerasidis, & Wrathall, 1985). Since

its invention, the weight-drop model has been modified to improve reproducibility of the

injury. Many current systems use electronic closed-loop feedback devices to monitor

parameters of the injury (e.g. Bresnahan, Beattie, Todd, & Noyes, 1987). Thus, animals

may be discarded initially if parameters of the injury do not meet criterion.

Despite these improvements, behavioral outcome following injury varies with

parameters of the weight-drop method, which makes it difficult to compare treatment

effectiveness across laboratories. The behavioral and neuropathological characteristics of








a given injury vary with the size of the weight used and the height from which it was

dropped (Daniell, Francis, Lee, & Ducker, 1975; Dohrmann & Panjabi, 1976). Not all

weight-drop devices utilize an impounder; use of an impounder requires that the height of

the weight/rod be increased to produce injuries of equal severity to those in which the

weight/rod impacts the spinal cord directly. Severity of injury can also vary with the size

of the impounder contact area (Gerber & Corrie, 1979) or with the mass of the impounder

(Koozekanani, Vise, Hashemi, & McGhee, 1976). Inherent properties of the spinal cord

(see Bresnahan et al., 1987; Koozekanani et al., 1976) or differences in surgical technique

(e.g. size of the laminectomy; Koozekanani et al., 1976) may also alter neurologic

outcome. Furthermore, smaller spinal cords will suffer a greater degree of compression

than a larger cord following a given drop-mass energy (Koozekanani et al., 1976), which

makes age-related comparisons difficult.

Because of shortcomings with the weight-drop method and because a single model

of SCI in animals may not represent all forms of SCI in humans, other models of SCI

have been developed. Use of various models of SCI may also enable one to determine

the parameters of SCI that predict behavioral outcome following injury. Rivlin and Tator

(1978) studied the effects of a contusion injury by applying aneurysm clips of known

forces to the spinal cord of adult female dogs for various lengths of time. Although the

amount and speed of compression can not be controlled with this technique, it has the

advantage that there is no confounding by movement of the spinal cord or vertebral

column during impact. Those authors found that the duration of compression was

important in determining recovery of function after acute compression; an 8-week

postoperative recovery period was required for maximum levels of recovery in some








groups of animals. Subsequent research determined that functional recovery varies with

both force and duration of compression (Dolan, Tator, & Endrenyi, 1980). Similarly,

duration of compression and pressure on the spinal cord are important factors that

determine hindlimb function following circumferential compression of the spinal cord by

an inflatable extradural cuff(Tator, 1973), which may reproduce the symptoms and

neuropathology of dislocation or fracture-dislocation of the spinal column in humans.

With that model, recovery is maximal within 12 postoperative weeks. Models of slow

spinal cord compression, which may reproduce the neuropathological changes in the

spinal cord following tumor growth, include compression by intradural balloons (e.g.

Tarlov, Klinger, & Vitale, 1953), forceps (Gruner, Yee, & Blight, 1996) or slow addition

of weights to an impounder resting on the spinal cord (Eidelberg, Staten, Watkins,

McGraw, & McFadden, 1976). Amount (Gruner et al., 1996), speed (Tarlov et al., 1953),

and duration (Tarlov et al., 1953) of compression, affect neurologic outcome. As with

contusion injuries, surviving white matter postcompression is correlated with behavioral

outcome (Gruner et al., 1996) and a 3- to 4-week postoperative period is generally

sufficient for maximum recovery.

Functional changes are evident with each type of SCI described, but the degree of

sensorimotor impairment depends on how the spinal cord is injured. Complicating

matters further, researchers of different laboratories rarely quantify these functional

differences and use their own rating scale to assess hindlimb sensorimotor function

postinjury. These motor performance scales include the 5- and 6-pt. modified Tarlov

scales (e.g., Tator, 1973; Wrathall, Pettegrew, & Harvey, 1985), the 15-pt. Ohio State

motor scale (e.g., Saruhashi & Young, 1994), the 21-pt. Basso, Beattie, and Bresnahan








(BBB) locomotor recovery scale (e.g., Basso et al., 1996), and the 100-pt. Combined

Behavioral Score (CBS; e.g., Kerasidis, Wrathall, & Gale, 1987). On most scales, higher

scores represent greater hindlimb function postinjury, but lower scores on the CBS scale

represent greater hindlimb function. Although rating systems are adequate for rapid

assessment of gross locomotor skill, rating systems are subjective and overground

walking does not provide a stringent test of hindlimb function. Thus, there is a need for a

standardized battery of tests that challenge hindlimb performance, for which

sensorimotor function can be quantified following incomplete SCI.


Behavioral Sequelae following Injury to the Developing Spinal Cord


Although human infants are not exempt from SCI, the neuropathological and

behavioral effects of spinal cord contusion/compression have not been studied in young

animals. Each year, approximately 230-500 children younger than 15 years of age

sustain SCIs. The most common cause of pediatric SCI is motor vehicle accidents, but an

increasing number is due to domestic violence. Sporting accidents are common causes of

SCI in older children and adolescents. Uncommon etiologies of pediatric SCI include

injuries from automotive lap-belts, the birthing process, child abuse, and C,-C,

subluxation associated with tonsillitis or pharyngitis (Vogel, Mulcahy, & Betz, 1997; also

see Hadley, Zabramski, Browner, Rekate, & Sonntag, 1988; Ruggieri, Smarason, & Pike,

1999; Vogel & Lubicky, 1995). Pediatric SCI is distinguished from SCI in adults in that

the neuropathological and behavioral manifestations following injury in infants interact

with normal processes of growth and development. Thus, the recovery process and

treatments designed for adults may not generalize to infants.








Most of what is known about the effects of SCI in young animals is from studies in

which the spinal cord was transected. Although most descending long fiber tracts

innervate the spinal cord by birth (Leong, Shieh, & Wong, 1984), rats gradually recover

hindlimb support and walking when the midthoracic spinal cord is completely transected

prior to postnatal day (PND) 12. However, when the transaction is made after PND 15,

there is increased spinal shock and little recovery of hindlimb function, if any (Stelzner,

Ershler, & Weber, 1975; Weber & Stelzner, 1977). That change in the degree of

recovery from spinal cord transaction corresponds to a period of rapid synaptogenesis in

the lumbar spinal cord (Gilbert & Stelzner, 1979), which suggests that lumbar motor

circuits become dependent on supraspinal inputs for normal function. There is no

evidence for neural growth across the transaction site (e.g., Cummings, Bernstein, &

Stelzner, 1981; Howland, Bregman, Tessler, & Goldberger, 1995). Therefore, recovery

of function after spinal cord transaction in young rats is probably due to synaptic

reorganization of immature circuits (Weber & Stelzner, 1977). Similar age-dependent

changes in response to contusive/compressive SCI may exist. Preliminary results from

our laboratory (McEwen & Stehouwer, 1998a) suggest that hindlimb dysfunction results

in greater hindlimb dysfunction following midthoracic spinal cord compression on PND

30, than on PND 5 or 15. However, the hindlimb sensorimotor function of rats of all

three age groups improved during the 10-day postoperative period. Although the spinal

cord of 5-day-old rats was compressed by 90%0/ of the uncompressed width, the

overground locomotion of those rats was subjectively similar to that of sham controls.

Because subjective ratings of overground walking may not be a sensitive test of hindlimb

function, kinematic analyses were subsequently used to quantify the limb movements of








neonatal rats during L-DOPA-induced air-stepping following midthoracic spinal cord

compression. On postoperative day 1 or 11, few parameters of limb movement were

significantly altered from sham controls, even though the spinal cord was compressed by

90% of the uncompressed width on PND 4 (McEwen & Stehouwer, 1998b). In contrast,

severe hindlimb dysfunction results when the adult spinal cord is compressed by

approximately 60%/ of the uncompressed width (see Gruner et al., 1996). Together, these

results suggest an age-related decline in sensorimotor function following spinal cord

compression. However, age-related changes in properties of the spinal cord tissue (e.g.,

elasticity; see Horie, Ikuta, & Takenaka, 1990) or its response to injury may influence

behavioral outcome.


Neuroanatomical Sequelae Postinjury


Mechanical damage to the central nervous system (CNS), not only directly causes

tissue necrosis, but also triggers a cascade of neurochemical changes that ultimately

results in additional, delayed tissue damage. These neurochemical changes include

release of polyunsaturated fatty acids, decreased free intracellular Mg", release of

platelet-activating factor, release of free radicals, elevations in dynorphin, serotonin, and

excitatory amino acids, NMDA receptor activation with increased intracellular Ca2 and

Na', release of inflammatory agents, decreased blood flow, and decreased glucose

utilization (see Faden, 1996; Janssen & Hansebout, 1989). A primary purpose of

studying SCI in animals is to understand these pathophysiological changes occurring in

the spinal cord and to identify successful therapeutic treatments following injury.








Although the biochemical changes in the infant spinal cord following incomplete

SCI have not been elucidated, the biochemical changes and neural tissue reactions

following hypoxic-ischemic injury to the neonatal brain (Berger & Gamier, 1999;

Giacoia, 1993) resemble the changes that occur in the mature spinal cord following

traumatic SCI. However, behavioral consequences of such injury-induced changes are

not necessarily equivalent in infant and adult animals. Insulin-induced hypoglycemia is

neuroprotective to hypoxic-ischemic damage to the adult brain (Nedergaard & Diemer,

1987), whereas hypoglycemic conditions exacerbate the lesion in the infant brain (Yager,

Heitjan, Towfighi, & Vannucci, 1992). Cell death is greater following transaction of the

developing spinal cord than following transaction of the mature spinal cord (e.g.,

Prendergast & Stelzner, 1976). However, the spinal cord of young rats has greater

functional autonomy following complete transaction than does the mature spinal cord

(Stelzner et al., 1975; Weber & Stelzner, 1977). Recovery processes following injury to

the neonatal central nervous system occur in conjunction with normal processes of

growth and development, which may afford the neonate greater recovery of locomotor

skill following SCI. Therefore, treatments designed for adults may not have the same

effects in infants. Elucidation of the neonatal reaction to traumatic SCI is needed.


Locomotor Development


Development of coordinated locomotor behavior is dependent on the maturation

and integration of numerous neural and nonneural subsystems, each of which has its own

developmental time-course. Human infants gradually develop independent walking over

the first 15 postnatal months (Forssberg, 1985; McGraw, 1940; Shirley, 1973). Human









infants generally progress through stages of head-raising, raising their upper body with

their forearms, and crawling before independent walking (Shirley, 1973), but perform

stepping movements from birth if held erect (Forssberg, 1985; McGraw, 1940).

However, the capacity for infant stepping disappears after the first two months, which has

been described as the "inactive period" (Forssberg, 1985; McGraw, 1940). After the

inactive period, infants initiate locomotor movements by crawling and then as supported

locomotion when held under the arms (Forssberg, 1985). Several months later children

begin to walk without support (Forssberg, 1985; McGraw, 1940; Shirley, 1973).

Gradually, the walking pattern is transformed, late in the second postnatal year, to the

adult plantigrade pattern, which is characterized by a heel-strike in front of the body

(Statham & Murray, 1971; Sutherland, Olshen, Cooper, & Woo, 1980).

Rats are also born relatively immature, but rapidly develop the raised, quadrupedal

posture for walking during the first 15 days. By PND 4 or 5, forelimb movements

become frequent. At this stage, the forelimbs act as paddles, but provide minimal

forward propulsion because the hindlimbs do not support the body. Since the hindlimbs

are anchored, the forelimbs pivot the animal around the pelvis. "Pivoting" is the

predominant form of locomotion by the end of the first postnatal week. By PND 8, head

raising is observed and the hindlimbs begin to provide some propulsive force, although

the hindlimbs are often unable to keep up with the forelimbs and are dragged behind.

Trunk elevation emerges around PND 10 or 11 and is predominant by day 12 or 13. True

quadrupedal walking emerges when rats open their eyes on PND 14 or 15. Locomotor

speed subsequently increases and fast running appears by PND 16. However, immaturity

of the locomotor skills of the rats are evident beyond PND 21 when rats are required to







10
ambulate over a slippery terrain (Altman & Sudarshan, 1975). In fact, the mature pattern

of paw contact with the surface continues to develop beyond PND 30 (Clarke &

Williams, 1994).

Although rats do not show the raised, quadrupedal posture and walking prior to

about PND 15, that does not mean that the neural circuits that mediate coordinated

locomotion are not in place and functional. In fact, coordinated locomotor behavior is

observed during the first postnatal week under conditions in which the postural demands

are reduced, such as during swimming (e.g., Bekoff& Trainer, 1979), during air-stepping

(e.g., Van Hartesveldt, Sickles, Porter, & Stehouwer, 1991), following administration of

catecholaminergic agents in vivo (e.g., Kellogg & Lundborg, 1972), or following

administration of drugs to a brainstem-spinal cord preparation in vitro (e.g., Atsuta,

Abraham, Iwahara, Garcia-Rill, & Skinner, 1991). Similarly, human infants show

rhythmical, coordinated movements shortly after birth when held erect (McGraw, 1940)

or placed in a prone position in water (McGraw, 1939). Human infants also continue to

step during the "inactive period" (Forssberg, 1985; McGraw, 1940) when the weight of

the limbs is reduced by submerging them in water (Thelen, Fisher, & Ridley-Johnson,

1984).

Because the neural and nonneural mechanisms required for adultlike locomotion in

rats mature postnatally, investigation into the development of locomotion in rats may

provide insight into how the motor system is constructed. In fact, some behavioral traits

of the damaged, mature system are analogous to the behavioral traits of the immature

system. Infant reflexes return in aged individuals (Paulson & Gottlieb, 1968) and

patients with Parkinson's Disease no longer walk with a heel strike, but walk on their toes








like young children (cf Forssberg, Johnels, & Steg, 1984; Statham & Murray, 1971).

The nervous system utilizes similar mechanisms to reinnervate denervated tissue

postinjury as are used by the developing system for initial outgrowth and innervation of

target tissues. Because recovery from injury to the developing nervous system occurs on

a background of normal processes important for growth and development, the developing

nervous system may compensate for lost inputs postinjury, resulting in reconstruction of

the developing nervous system. Determination of the behavioral effects of damage to the

immature nervous system is important because prolonged activation of those

compensatory mechanisms may have numerous behavioral effects, ranging from

complete sensorimotor recovery to additional sensorimotor impairments.


Significance of Current Research


SCI in humans occurs in a wide variety of ways, so the tissue (see Bunge, Puckett,

& Hiester, 1997; Kraus, 1996) and behavioral responses to injury may vary with injury

type. Thus, all forms of SCI in humans may not be simulated by a single model of SCI

and justifies the development of different animal models. However, with such different

techniques to produce SCI, accurate determination of the extent of the lesion and residual

hindlimb function is necessary. Knowledge of age-related differences in the effects of

SCI will aid determination of the generalizability of postinjury treatments. The purpose

of the present experiments was to develop a set of behavioral tasks that challenge

hindlimb sensorimotor function postinjury and to examine the effects of age on recovery

of function. Although the size of the spinal cord increases with age, proposed procedures

enabled compression of the spinal cord by the same relative amount during ontogeny.







12
Descending, ascending, and segmental systems that survive SCI and guide recovery of

hindlimb sensorimotor function may vary with the age of the animal, as well as severity

of injury. Therefore, age-related differences in the amount of tissue at the lesion

epicenter following midthoracic spinal cord compression will suggest age-related

changes in the relative importance of descending inputs or compensation by spinal

systems in recovery of hindlimb sensorimotor function. Because human infants and rats

progress through similar stages of locomotor development, a greater understanding of the

effects of injury to the spinal cord of human infants may be achieved by studying the

effects of injury to the spinal cord of developing rats.














CHAPTER 2
MATERIALS AND METHODS


Subjects


Subjects were 5-, 15-, and 60-day-old Sprague-Dawley rats born in the vivarium at

the University of Florida Department of Psychology. Adult breeder Sprague-Dawley rats

(Zivic-Miller) were housed and bred in a temperature-controlled colony room on a 12:12

hr light/dark cycle with food and water available adlibitum. Breeding cages were

checked twice daily for litters and the day of birth was considered PND 0. Litters were

culled to 10 pups (5 males and 5 females, when possible) within 24 hr of birth and

remained with their dams until surgery and behavioral testing. On PND 25, rats were

weaned and housed in gang-cages by sex. On PND 45, rats were housed in pairs and

were then handled daily prior to surgery.


Surgery


A split-litter design was used so surgery was performed under aseptic conditions

on two litters on the same day; half of the male and female rats from each litter received

one of the three surgical treatments below. On PND 5, 15, or 60, rats were anesthetized

(hypothermia on PND 5; Metofane on PND 15 or 60) and dorsal incisions were made in

the skin and underlying muscles. A midthoracic laminectomy was performed and the

width of the spinal cord was measured using the coordinate system of a







14
micromanipulator. Tips of a pair of forceps (Dumont #5) were bent so the arms closed in

parallel to each other and were inserted into the vertebral column, between the vertebral

walls and the lateral margins of the spinal cord. Sham surgery consisted of no further

manipulation. To produce the SCI, forceps were slowly closed until contact was made

with an automotive ignition gauge inserted between the arms of the forceps (see Gruner

et al., 1996). Spinal cords were compressed for 15 s by 0% (sham), 85%, or 95% of the

initial, uncompressed width (also see McEwen & Stehouwer, 1998a). At most ages,

muscle and skin were closed in layers using silk sutures and the wound was covered with

New Skin liquid bandage (Medtech Laboratories, Jackson) to prevent wicking; the skin of

60-day-old rats was closed with wound clips. Rats were placed on a heating pad for 2-3

hr to recover and were placed in the colony room until behavioral testing and sacrifice.

Bladders of 60-day-old rats were manually expressed three times daily until self-

expressing and the hindquarters were washed as needed. Bladders of the 5- and 15-day-

old rats were not expressed manually because the dam performed this function and

micturition was not severely compromised following injury. Weight gain of all rats was

monitored daily. Seven to 8 subjects comprised each of the 9 experimental groups.


Behavioral Testing


Froot Loops cereal was the food reward during behavioral testing and was placed

into the home cage, beginning the week prior to the testing phase to reduce the effects of

neophobia. On postoperative days (PODs) 1, 7, 14, 21, and 28, rats were tested for

hindlimb sensorimotor function on a battery of tasks. On PODs 1 and 7 for rats of the

youngest age group, the battery of tasks included ratings of olfactory-induced walking








(from Jamon & Clarac, 1998), followed by righting, and then determination of latencies

to withdraw one hindpaw from the surface of a hotplate. For all other experimental

groups and PODs, the sensorimotor battery included ratings of voluntary overground

walking, followed by walking across beams of various widths, walking across parallel

bars of various distances apart, maintenance of position and balance on an inclined plane,

and finally latencies to lick one hindpaw on a hot plate. Except during testing on the

parallel bars where rats received multiple successive trials with the bars various distances

apart, rats of all experimental groups were tested on one particular task before proceeding

to the next behavioral task. Because rats were allowed to rest in the home cage between

tasks, sensorimotor performance was probably not significantly affected by fatigue of the

rat. A lateral view of each rat was videotaped during testing to aid determination of

forelimb and hindlimb performance. A mirror was placed at a 45-degree angle beneath

each elevated apparatus to enable simultaneous recording of the lateral and ventral views

of each rat. A 5-cm-thick foam pad was placed below these apparatuses to prevent injury

if an animal fell.


Righting

Rats younger than 15 days of age were placed supine on a flat surface and allowed

to right. Approximately 5 righting episodes were initiated on PODs I and 7 for each rat

of the youngest age group. Righting matures rapidly during the first week of postnatal

life in rats (Tilney, 1934). Because righting by infant rats is dependent on hindbrain and

spinal cord structures (Bignall, 1974), observations of righting by infant rats of the

present experiments enabled an assessment of the functional efficacy of descending

systems following spinal cord compression early in postnatal life.









Overground Walking

Rats, 15 days of age or older, were placed on a flat surface and allowed to walk

freely. Prior to PND 15, a plastic tube filled with soiled shavings was placed over the

nose of the rat for olfactory-induced locomotion (Jamon & Clarac, 1998). The 21-point

BBB locomotor recovery scale was used to assess hindlimb locomotor function (see

Appendix A). Because rating scales are subjective, hindlimb motor function was rated on

two separate occasions by the same individual for subsequent determination of intrarater

reliability. Spontaneous locomotion occurs following a precollicular-premammillary

transaction through the brain, suggesting that descending systems of the midbrain activate

spinal motor circuits. Coordinated walking of all four limbs then requires the integrated

activity of spinal and supraspinal systems (see Grillner, 1975; Whelan, 1996). Therefore,

ratings of overground locomotion during the recovery period were included to suggest the

degree of spared function and plasticity of(1) supraspinal systems, which are required for

activation of spinal motor circuits during spontaneous locomotion, (2) propriospinal

systems, which are important for coordinated movements between limb girdles, and (3)

intraspinal systems, which are important for hindlimb joint movement and weight support

following spinal cord compression.


Beam Walking

Rats, 15 days of age or older, were placed on one end of 112 cm long, inclined

beams (7 degrees) of various widths (3.0, 2.2, or 0.5 cm) and allowed to walk the length

of the beam to reach the goal box with the food reward. The beams were covered in

smooth contact paper to prevent soiling of the wood by the rats. The corticospinal tract is

important for limb positioning during walking (Hicks & D'Amato, 1975). Therefore, rats








were required to walk across beams of various widths to provide a measure of the

functional efficacy of the corticospinal system.


Object Avoidance

This test utilized the same procedures as described for beam walking, except that 4

obstacles of various heights (0.5, 1.2, 1.7, and 2.7 cm above the surface of the runway)

were equally spaced along each of the three types of beams. Obstacles were centered

along the width of each beam and were 1.1, 0.7, or 0.2 cm in diameter for the 3.0, 2.2, or

0.5 cm wide beams, respectively. The coordinated walking of decerebrate animals

(precollicular-premammillary transaction) is described as purposeless because the

animals walk aimlessly around the room and do not respond properly to obstacles in the

environment (see Grillner, 1975; Hinsey, Ranson, & McNattin, 1930). Therefore, the

obstacle avoidance task, which requires the rats to step over obstacles during beam

walking, was included as a further test of the functional efficacy of forebrain/cortical

descending corticospinall) systems. Because stimulation to the dorsum of the foot of

spinal animals initiates limb flexion (see Grillner, 1975), performance on this task will

also provide evidence for the functional efficacy of spinal systems if stepping over the

obstacles requires activation of spinal reflexes.


Parallel Bar Walking

Rats, 15 days of age or older, were placed on one end of parallel, inclined (7

degrees) wooden rods (112 cm long, 9 mm diameter) that were initially 2.7 cm apart.

Rats were allowed to traverse the parallel bars to reach the goal box with the food reward.

The distance between the bars was increased in 0.5 cm increments until the rat failed to








traverse the two bars using completely weight-supported steps or the rats walked along a

single bar to reach the goal box. The parallel bars were covered with smooth contact

paper to prevent soiling of the wood by the rats. Because walking across parallel bars

requires greater accuracy of limb placement and coordination between limb girdles than

does walking overground or across flat beams, this task was included as a more stringent

test of the functional efficacy of the corticospinal system, as well as efficacy of

propriospinal systems of the spinal cord.


Inclined Plane

Rats, 15 days of age or older, were tested for the maximum degree of incline on

which they maintained position and balance without falling for at least 5 s. Modified

from Rivlin and Tator (1977), the inclined plane was a flat board, covered in smooth

contact paper, that was initially set 15-degrees above horizontal. Rats were placed onto

the inclined plane at a 45-degree angle from horizontal (head up) and tested for

maintenance of position and balance for at least 5 s. The incline of the plane was

increased in 10-degree increments until the rat failed to maintain position and balance for

the duration of the time limit. To determine the threshold value within that 10-degree

window, the range was repeatedly narrowed by half the distance until threshold was

determined. Although hindlimb weight-support is accomplished by spinal motor circuits

in animals with complete spinal cord transactions, the hindquarters generally fall to one

side or the other (see Grillner, 1975), suggesting that the pathways important for balance

were disrupted. Therefore, the inclined plane task was included in the sensorimotor

battery of the present experiments to suggest alterations following spinal cord

compression in the functional efficacy of ascending and descending systems, such as the








spinocerebellar and vestibulospinal tracts, that would be important maintenance of

balance on the inclined plane.


Hot Plate

Rats, 15 days of age or older, were placed on a hot plate preheated to 51 C and

monitored for the time elapsed before the rat licked one of its hindpaws. Rats younger

than 15 days of age were held around the trunk with the plantar surface of the foot

touching the hot plate and observed for the latency to withdrawal one hindpaw from the

hot plate surface (on PODs 1 and 7 following surgery on PND 5). A time limit of 30 s

was used to ensure that there was no tissue damage to the feet of an unresponsive rat.

Based on previous research with adult (see Irwin, Houde, Bennett, Hendershot, &

Seevers, 1951) and infant (see Stelzner et al., 1975) animals, withdrawal responses to

sensory stimulation are primarily controlled by spinal sensorimotor circuits. In contrast,

forebrain circuits are required for the hindpaw lick response on the hotplate (Woolf,

1984). Therefore, the hotplate task was included to provide an assessment of the

functional efficacy of spinal sensorimotor circuits during the first postoperative week in

rats of the youngest age group and of ascending and descending sensorimotor circuits in

rats of all other ages and on all other PODs.


Histology


On POD 29, rats were deeply anesthetized with sodium pentobarbital and perfused

with heparinized-saline and 1.0%/ paraformaldehyde-1.25% glutaraldehyde in 0.1M

phosphate buffered saline (PBS; pH 7.2-7.4). Spinal cords were removed and stored at 40

C in 30% sucrose-formalin for at least 3 days and a 2 cm section of spinal cord








20
containing the injury site was embedded in 30% albumin-3% gelatin. Once hardened in

formaldehyde, the blocks were trimmed and embedded in 3% agar to improve adherence

of the block to the microtome stage. Spinal cords were then cut into 40 upm transverse

(coronal) sections on a freezing-stage sliding microtome, mounted on chrom-alum

gelatin-coated slides, and air-dried. Sections were stained using a modification of the

Kluver-Barrera method: (1) dehydrate in 95% ethanol (30 min); (2) immerse in 0.1%

Luxol Fast Blue MBSN, preheated to 600 C (16-24 hr); (3) rinse in 95% ethanol; (4) rinse

in distilled water; (5) differentiate in 0.1% lithium carbonate (2-5 min); (6) differentiate

in 70%/ ethanol (5-30 min); (7) wash in distilled water; (8) immerse in 0.1% cresyl violet

(5 min); (9) rinse in distilled water; (10) immerse in 70% ethanol, then 95% ethanol (2

min each); (11) differentiate in 95% ethanol + glacial acetic acid; (12) dehydrate in 95%

ethanol (2 min), then 1000/o ethanol (2 x 1 min); (13) clear in xylene, coverslip with

Permount.


Data Analyses


Righting

Videotapes were played in slow-motion (1/26" normal speed) for qualitative

assessment of surgery-related behavioral changes in righting. Videotapes were then

played frame-by-frame (30 frames/s) and the positions of the head, trunk, and limbs were

drawn for one rat that represented the righting of all rats within that experimental group.

Successive images were usually separated by less than 0.23 s (7 frames). In a few cases,

righting was interrupted by a brief period of quiescence so as much as 1.03 s (31 frames)








21
elapsed between drawings. For this and all subsequent analyses, videotapes were scored

under experimentally blind conditions with respect to the surgical condition of the rat.


Overground Walking

From videotapes, hindlimb locomotor function was assessed with the BBB

locomotor recovery scale as described above.


Beam Walking

Episodes from rats that crossed the 3.0- and 2.2 cm wide beams to reach the goal

box were analyzed from videotapes for the number of hindlimb slips. Because the

number of steps required to cross the beams decreased with age, the number of hindlimb

slips was converted to a percentage of the number of hindlimb steps used to cross the

beam. Any step during which the abdomen of the rat touched the beam (non-weight-

supported) or any step during which the abdomen remained elevated above the beam

(weight-supported), but the foot fell below the beam, was counted as a slip. For rats in

which the majority of steps during beam walking were weight-supported, videotapes

were also played frame-by-frame (60 frames/s) for determination of footfall patterns and

the time interval between stance and lift off of successive limbs. Two limbs were

considered to be in stance together if 67 msec or more (4 frames or more) elapsed

between surface contact by one foot and lift off of the successive limb. The instances in

which 2, 3, or 4 feet were simultaneously in stance were counted and converted to

percentages of the total number of footfall patterns used to traverse the beam. Except for

rats that received sham surgery on PND 60, most rats did not traverse the 0.5 cm wide

beam using weight-supported steps, so the results of that task are not considered further.








Obstacle Avoidance

On each POD, only those rats that successfully traversed the 3.0 and 2.2 cm wide

beams were tested for obstacle avoidance. Videotapes were used to determine the tallest

obstacle that rats stepped over, without falling or dragging the abdomen. Most rats did

not walk across the 0.5 cm wide beam with obstacles using weight-supported steps, so the

results of that task are not considered further.


Parallel Bars

All rats, 15 days of age or older, were tested for walking across the parallel bars.

From videotapes, behavioral analyses were as described above.


Inclined Plane and Hot Plate

Measures were as described above.


Histologic Evaluation

The section through the lesion that depicted the greatest amount of tissue loss was

designated as the lesion epicenter and was magnified and projected onto a digitizing

tablet. Outlines of all patches containing clear CNS tissue were traced using a digitizing

pen and a computer was used to calculate the area of the spinal cord tissue at the lesion

epicenter. Tissue that was characterized by reactive astrocytes, fibrous scarring, or

Wallerian degeneration (see Reier, Eng, & Jakeman, 1989) were excluded. Because the

cross-sectional area of the spinal cord increases during ontogeny, the absolute amount of

spinal cord tissue at the lesion epicenter of rats of the present experiments that received a

spinal cord compression was determined and converted to a percentage of control tissue

size. Because the myelin was not evenly stained with luxol fast blue in all tissue sections








23
following the differentiation process, no distinctions were made between gray and white

matter during quantification of the cross-sectional area of tissue at the lesion epicenter.

Due to problems with tissue adherence to the slides, several tissue sections were lost for

each subject and prevented quantification of lesion length or lesion volume.


Statistics


A descriptive analysis of surgery-related alterations to righting was intended and,

therefore, no statistical analyses were performed on data from that behavioral task. One-

factor Kruskal-Wallis nonparametric statistics were used to test for significant effects of

age, surgery, or POD on data that were characterized by mutually exclusive categories

with an inherent order among them. Those data included ratings of overground walking,

stepping over obstacles the four obstacles of different heights, and walking across parallel

bars that were separated in 0.5 cm increments. Post-hoc comparisons were performed

using Mann-Whitney U tests (a = 0.05). Intrarater reliability on ratings of overground

locomotion was determined with Kendall's coefficient of concordance for nonparametric

statistics (W = 0.9932, p <0.001). In cases where the two locomotor ratings were not in

agreement, the mean of those values was assigned to that subject for subsequent

statistical analyses. All other data were measured at the cardinal level and were tested for

significant main effects of age, surgery, and POD, as well as their interactions, using

analyses of variance (ANOVAs) as specified. For ease of data interpretation, 3-factor

ANOVAs were not conducted. Data from the hotplate and inclined plane tasks were

analyzed with 2-factor ANOVAs with 1 repeated measure (surgery x POD) for each age

group and with 2-factor ANOVAs with 1 repeated measure (age x POD) for each surgery








group. The percentage ofhindlimb slips and the percentage of footfall patterns

characterized by 2, 3, or 4 feet in stance during beam walking were analyzed using 2-

factor ANOVAs with I repeated measure (surgery x POD) for each age group, as well as

2-factor ANOVAs with 1 repeated measure (age x POD) for each surgery group.

Following surgery on PND 60, only rats that received sham surgery walked across the

beams using weight-supported steps so data on percentages of footfall patterns was

analyzed with 1-factor repeated measures ANOVAs (POD). Some rats failed to traverse

the beams on a particular day (generally on POD 1), which resulted in missing values for

the repeated measure. In those cases, the missing values were estimated and the degrees

of freedom were reduced accordingly (GB-STAT). Absolute amounts of tissue at the

lesion epicenter and percentages of control tissue size were analyzed with 2-factor

ANOVAs (age x surgery). Post-hoc multiple comparisons were performed using

Duncan's new multiple range test (a = 0.05). For each age and injury group, ratings of

overground walking on POD 28 were plotted as a function of injury level and absolute

tissue size at the lesion epicenter was plotted as a function of injury level. Data were

tested for the strength of the correlation using Spearman's Rank Correlation Coefficient

(a = 0.05). Because the number of subjects that successfully completed some of the tasks

varied by POD, the number of subjects comprising each statistical analysis is included as

Appendix B.













CHAPTER 3
RESULTS


Righting


When placed in a supine position on POD 1, rats that received sham surgery or the

lesser compression rocked their outstretched fore- and hindlimbs in opposite directions,

until rostrocaudal axial rotation of the body and righting was achieved (Fig. IA). When

rats that received the greater compression were placed in a supine position on POD 1, the

hindlimbs remained flexed and the hindquarters immediately fell to one side, which was

followed by righting of the head and shoulders. Sometimes righting was aided in those

rats by ventroflexion of the upper body, which lifted the head and shoulders off ofthe

ground. Some rats that received the greater compression never pulled the hindlimbs up

under the body to complete the righting sequence. Instead, the hindlimbs continued to lie

to one side of the body (Fig. 1B). On POD 7, limb extension and axial rocking of the

fore- and hindquarters of rats that received sham surgery or the lesser compression was

exaggerated relative to the limb and body movements on POD 1. Eventually, righting

began at the head and shoulders and proceeded caudally until axial rotation of the entire

body was achieved (Fig. 2A). On POD 7, the amount of rocking of the fore- and

hindquarters during attempts to right was diminished and the hindlimbs were slightly

flexed in rats that received the greater compression, relative to sham controls. Righting

was then achieved by axial rotation of the head and shoulders, followed by the hindlimbs.








cr~fi


<^^C.


c\zrI~


Figure 1. Righting sequence on postoperative day I day following compression of the spinal cord of 5-day-old rats.
Depicted from left to right are: A) a series of postures during righting of a representative rat that received sham surgery on
postnatal day 5 and B) a series of righting postures of a rat that received 95% compression of the spinal cord on postnatal day
5. Righting of age-matched rats that received 85% compression were indistinguishable from sham controls and, therefore,
not included.


e;t


,: ?

CI~S


c,


zb


,9


N


C"sz










~zI~jI


^--^7-

r-' C'


1.


Figure 2. Righting on postoperative day 7 following compression of the spinal cord of 5-day-old rats.
Depicted from left to right are: A) a series of postures during righting of a representative rat that received sham surgery on
postnatal day 5 and B) a series of righting postures of a rat that received 95% compression of the spinal cord on postnatal
day 5. Righting of age-matched rats that received 85% compression were indistinguishable from sham controls
and, therefore, not included.


A
^3.


4)


S:W


%2:)


~~i~4~CTb~


U







28
Often the hindlimbs were pulled under the body, as found for sham controls. However,

the hindlimb joints were unusually extended during weight support, which lifted the

hindquarters above the table surface (Fig. 2B).


Overground Walking


There was an age-related decline in the quality of overground walking in rats that

received compression of the spinal cord (Fig. 3). In rats of the youngest age group,

surgery-related differences in overground walking were apparent on PODs 1, 14, 21, and

28 [Hs(2) > 8.72, ps < 0.05]. By the end of the postoperative period, rats of the youngest

age group that received the greater compression retained deficiencies in toe clearance,

paw position at lift off, tail position, and trunk stability during walking (ps < 0.05).

Overground walking of age-matched rats that received the lesser compression or sham

surgery did not differ significantly (ps > 0.05). Compression of the 15-day-old spinal

cord also had surgery-dependent effects on overground walking throughout the

postoperative period [Hs(2) > 15.0, ps < 0.005]. Specifically, overground walking was

indistinguishable throughout the postoperative period between rats that received the

lesser compression or sham surgery on PND 15 (ps > 0.05). Rats that received the

greater compression on PND 15 dragged the hindlimbs on POD 1 and only slightly

moved one or two of the hindlimb joints, if any, during locomotion. By POD 7, those

rats recovered hindlimb weight-supported stepping, but remained deficient throughout the

postoperative period in either toe clearance or paw position, tail position, and trunk

stability, relative to rats of the other two groups (ps < 0.05). Surgery on PND 60 also

significantly altered overground walking throughout the postoperative period [Hs(2) >















Surgery PND 5


--- Sham
--A- 85% Compression
-0- 95% Compression
Surgery PND 15


Surgery PND 60


Postoperative Day


Figure 3. Median ratings of overground walking throughout the 4-week postoperative period for rats that received sham
surgery, 85% compression, or 95% compression on postnatal day 5, 15, or 60. On the Basso, Beattie, and Bresnahan (BBB)
21-point scale, higher numbers reflect greater motor function, with a score of 21 representing overground walking of
uninjured, adult rats. Ratings less than 21 in rats that received sham surgery on postnatal day 5 or 15 reflect immaturity of
the motor system, rather than surgery-related deficits in motor function.









15.0, ps < 0.005]. Rats that received midthoracic spinal cord compression on PND 60

dragged the hindlimbs on POD 1 (ps < 0.05), which did not differ significantly between

rats of the two compression groups (ps > 0.05). Young-adult rats that received the lesser

compression recovered hindlimb weight-supported stepping and coordination across limb

girdles within the first postoperative week, but deficiencies in toe clearance, paw

placement, tail position, and trunk stability remained throughout the remainder of the

postoperative period. Young-adult rats that received the greater compression recovered

extensive movement of the hindlimb joints by POD 14, but never recovered weight-

supported stepping or coordination across limb girdles (ps < 0.05). Except for rats that

received sham surgery on PND 60 and were rated as 'normal' throughout the

postoperative period [H(4) = 0.00, p > 0.05], overground walking of rats of all other age

and surgery groups improved during the postoperative period [Hs(4) > 18.73, ps < 0.005].

Between PODs 1 and 14, locomotor function of sham controls differed between

rats of the three age groups [Hs(3) > 11.76. ps < 0.005]. Following sham surgery, rats of

the youngest age group had lower locomotor scores on PODs 1, 7, and 14 and rats of the

intermediate age group had lower scores on POD 1, relative to rats of the oldest age

group (ps <0.05). Those findings reflect the locomotor immaturity of neonatal rats on

those PODs. On PODs 21 and 28, overground walking was mature and was

indistinguishable among rats of the three age groups that received sham surgery [Hs(2) =

0.00, ps > 0.05]. Overground walking of rats that received either amount of spinal cord

compression also resulted in significant effects of age throughout the postoperative

period [Hs(2) > 12.13, ps < 0.005]. Once overground walking was mature on PODs 21

and 28, rats of the youngest two age groups that received the lesser compression were








indistinguishable from each other (ps > 0.05), whereas rats that received a similar

compression on PND 60 maintained deficiencies in paw position at lift off tail elevation,

and trunk stability (ps < 0.05). In contrast, there was an age-dependent decrease on

PODs 21 and 28 in hindlimb motor function during overground walking of rats that

received the greater compression (ps < 0.05).


Beam Walking


3.0 cm Beam

Percentage of hindlimb slips

Rats that received sham surgery on PND 5 traversed the 3.0 cm beam by POD 14,

when a raised, quadrupedal posture was achieved. Rats that received sham surgery on

PND 15 or 60 traversed the beam throughout the postoperative period. Not all rats of

each age and compression group crossed the beam on all PODs (see Appendix B).

Following surgery on PND 5, the percentage of slips during beam walking resulted in a

significant effect of surgery x POD [F(4, 42) = 21.23, p < 0.001; Fig. 4]. The percentage

of hindlimb slips during beam walking was indistinguishable on PODs 14 to 28 between

rats that received the lesser compression or sham surgery (ps > 0.05). In contrast, the

percentages of hindlimb slips were significantly elevated in rats that received the greater

compression (ps < 0.05), except on POD 21 when the percentage of hindlimb slips was

not different from rats that received the lesser compression (p > 0.05). Although the

percentage of hindlimb slips of rats of the youngest age group was relatively constant

throughout the postoperative period following the lesser compression or sham surgery (ps

> 0.05), the percentage of hindlimb slips of the 3 rats that crossed the beam following















Surgery PND 5


-i- Sham
--A-- 85% Compression
--- 95% Compression

Surgery PND 15


Surgery PND 60


Postoperative Day


Figure 4. Numbers of hindlimb steps that were characterized by slips are represented as percentages of the total number of
hindlimb steps required to cross the 3.0 cm wide beam. Percentages of hindlimb slips (+ SEM) are shown for each
postoperative day of interest for rats that received sham surgery, the 85% compression, or the 95% compression on postnatal
day 5, 15, or 60. Only 3 rats that received the 95% compression on PND 5 and 3 rats that received the 85% compression on
PND 60 traversed the beam.








greater compression of the cord significantly increased between PODs 21 and 28 (p <

0.05). Rats that received the lesser compression on PND 15 had a higher percentage of

hindlimb slips than age-matched rats that received sham surgery [F(1, 14) = 8.15, p <

0.05]. The percentage of hindlimb slips in those groups of rats decreased during the

postoperative period [F(4, 56) = 47.83, p < 0.001], mainly between PODs 1 and 7 (p <

0.05), with little change thereafter (ps > 0.05). Following surgery on PND 60, the

percentage ofhindlimb slips resulted in a significant surgery x POD interaction [F(1, 14)

= 27.48, p = 0.001]. When rats that received the lesser compression on PND 60 began

traversing the beam on POD 21, the percentage of hindlimb slips was elevated over sham

controls (ps < 0.05), but the percentage of hindlimb slips decreased between PODs 21

and 28 (p < 0.05). The percentage of hindlimb slips did not change significantly during

the postoperative period in rats that received sham surgery on PND 60 [F(4, 28) = 2.39, p

> 0.05].

Following sham surgery, the percentage of hindlimb slips of rats of the three age

groups resulted in a significant age x POD interaction for PODs 14 to 28 [F(4, 42) = 3.93,

p < 0.01]. Specifically, rats that received sham surgery on PND 5 had a higher

percentage of hindlimb slips on POD 14 than rats that received sham surgery on PND 15

(p < 0.05) and rats that received sham surgery on PND 15 had more hindlimb slips on

POD 28 than rats that received sham surgery on PND 60 (p < 0.05). The percentage of

hindlimb slips of rats that received surgery on PND 15 or 60 also resulted in a significant

age x POD interaction between PODs 1 and 28 [F(4, 56) = 3.59, p < 0.05]. Specifically,

the percentage of hindlimb slips was elevated on POD 1 in rats that received sham

surgery on PND 15, relative to rats that received sham surgery on PND 60 (p < 0.05).









The percentage of hindlimb slips during beam walking of rats that received the lesser

compression resulted in a significant effect of age x POD when data were compared

across rats of all three age groups [F(2, 21) = 8.30, p < 0.01]. Among rats that received

the lesser compression, there was an age-dependent increase in the percentage of

hindlimb slips on PODs 21 and 28 (ps < 0.05). Most rats that received the greater

compression of the cord did not walk across the beam, which precluded an examination

of age-dependent effects of the greater compression on beam walking.

Footfall patterns

Footfall patterns could not be determined for rats that dragged their abdomens

across the beam, rather than walking with weight-supported steps (see Appendix B).

While traversing the 3.0 cm wide beam, rats primarily used a lateral sequence walking

gait in which 3 limbs remained in contact with the beam and stepping of the left

hindlimb, was followed by the left forelimb, then the right hindlimb and finally by the

right forelimb. Among all rats that received the greater compression of the spinal cord,

only 2 rats that received the compression on PND 5 traversed the beam using weight-

supported steps on PODs 14 and 21 and only 1 rat of that age group traversed the beam

on POD 28. Therefore, footfall patterns were statistically analyzed for rats that received

either the lesser compression or sham surgery, but data for rats that received the greater

compression on PND 5 were included in the figures for comparison. Between PODs 14

and 28, the percentage of footfall patterns in which rats of the youngest age group

maintained 2 (Fig. 5), 3 (Fig. 6), or 4 (Fig. 7) limbs on the beam was not dependent on

surgery [Fs(1, 14) < 0.06, ps > 0.05] or on POD [Fs(2, 28) < 1.97, ps > 0.05]. In contrast,

the percentage of footfall patterns in which rats that received surgery on PND 15














Surgery PND 5


-I- Sham
--A-- 85% Compression
-0-- 95% Compression
Surgery PND 15


Surgery PND 60


i 7 14 21 28


7 14 21 28 1 7 14 21 28


Postoperative Day


Figure 5. Rats crossed the 3.0 cm beam with either 2, 3, or 4 limbs in stance simultaneously. This figure depicts the
percentage of support patterns ( SEM) used throughout the postoperative period in which the body weight was supported by
2 feet on the beam for rats that received surgery on postnatal day 5, 15, or 60. Most rats that received the 95% compression
at any age or the 85% compression on postnatal day 60 did not cross the beam using weight-supported steps and were not
included in this analysis.


10




!0


A-.K--^-------5
Jl I ,' "--- v_______ ^ ~~*- -^'_________
















Surgery PND 5


--- Sham
--A-- 85% Compression
-O- 95% Compression

Surgery PND 15


Surgery PND 60


0 -......... 1 ---- -------- .--- 4 ---------- 4--
a "^i---C-A-A
o ........-o

0

0-


1 7 14 21 28 1 7 14 21 28 1 7 14 21 28
Postoperative Day
Figure 6. Rats traversed the 3.0 cm beam with either 2, 3, or 4 limbs in stance simultaneously. This figure depicts the
percentage of support patterns (+ SEM) used throughout the postoperative period in which the body weight was supported by
3 feet on the beam for rats that received surgery on postnatal day 5, 15, or 60. Most rats that received the 95% compression
at any age or the 85% compression on postnatal day 60 did not cross the beam using weight-supported steps and were not
included in this analysis.















Surgery PND 5


-5- Sham
--A-- 85% Compression
0-- 95% Compression

Surgery PND 15


Surgery PND 60


Postoperative Day


Figure 7. Rats traversed the 3.0 cm beam with either 2, 3, or 4 limbs in stance simultaneously. This figure depicts the
percentage of support patterns ( SEM) used throughout the postoperative period in which the body weight was supported by
4 feet on the beam for rats that received surgery on postnatal day 5, 15, or 60. Most rats that received the 95% compression
at any age or the 85% compression on postnatal day 60 did not cross the beam using weight-supported steps and were not
included in this analysis.








maintained 2, 3, or 4 feet on the 3.0 cm wide beam resulted in significant effects of

surgery x POD [Fs(4, 56) > 2.97, ps < 0.05]. Rats that received sham surgery had a

higher percentage of footfall patterns with 3 limbs in stance between PODs 14 and 28 (ps

< 0.05), but a lower percentage of footfall patterns with 4 limbs in stance on PODs 14

and 21 (ps < 0.05), relative to rats that received the lesser compression. In addition, the

percentage of footfall patterns with 2 limbs in stance was lower on POD 7 in rats that

received sham surgery on PND 15 than in age-matched rats that received the greater

compression (p < 0.05). Although footfall patterns were analyzed statistically only for

rats that received sham surgery on PND 60, data from the 1 rat that received the lesser

compression on PND 60 and traversed the beam using weight-supported steps on POD 28

was included in the figure for comparison. Although the percentage of footfall patterns

characterized by 3 or 4 feet in stance did not change significantly during the

postoperative period [Fs(4, 28) < 2.31, ps > 0.05], there was a significant change in the

percentage of footfall patterns characterized by 2 feet in stance in rats that received sham

surgery on PND 60 [F(4, 28) = 3.44, p < 0.05]. Specifically, the percentage of footfall

patterns with 2 feet in stance was higher on PODs 21 and 28 than on other days of the

postoperative period (ps < 0.05).


2.2 em Beam

Percentage of hindlimb slips

Rats that received sham surgery on PND 5 traversed the 2.2 cm wide beam,

beginning on POD 14 when a raised, quadrupedal posture was achieved. Most rats that

received sham surgery on PND 15 or 60 traversed the beam throughout the postoperative

period. Not all rats of each age and injury group traversed the beam on all PODs (see








Appendix B). Following surgery on PND 5, the percentage ofhindlimb slips during

beam walking resulted in significant effects of surgery [F(2, 21) = 5.24, p < 0.05] and

POD [F(2, 42) = 23.27, p < 0.001; Fig. 8]. Specifically, the percentage of hindlimb slips

was higher in rats that received the greater compression than in rats that received the mild

compression (p < 0.05) and the percentage of hindlimb slips decreased between PODs 14

and 21 (p < 0.05), with no significant change thereafter (p > 0.05). The percentage of

hindlimb slips of rats that received the lesser compression on PND 15 was elevated,

relative to age-matched sham controls [F(l, 14) = 7.91, p < 0.05]. Furthermore, the

percentage of hindlimb slips of those rats during beam walking resulted in a significant

effect of POD [F(4, 56) = 14.99, p <0.001]. Specifically, the percentage of hindlimb

slips decreased between PODs 1 and 7 (p < 0.05), with little change thereafter (ps >

0.05). When rats that received the lesser compression on PND 60 began traversing the

beam on POD 21, the percentage ofhindlimb slips resulted in a significant effect of

surgery x POD [F(l, 14) = 13.12, p < 0.01]. Specifically, the percentage of hindlimb

slips of rats that received the lesser compression on PND 60 was elevated over sham

controls on PODs 21 and 28 (ps < 0.05), but decreased significantly in those rats between

the two PODs (p < 0.05). The percentage of hindlimb slips of rats that received surgery

on PND 60 also resulted in a significant effect of POD [F(4, 28) = 2.72, p < 0.05].

Specifically, the percentage of hindlimb slips was higher on POD 1 than on PODs 14, 21,

or 28 (ps < 0.05).

Between PODs 14 and 28, the percentage of hindlimb slips by rats that received

sham surgery resulted in a significant age x POD interaction [F(4, 42) = 3.45, p < 0.05].

On POD 14, the percentage ofhindlimb slips decreased with increased age of the rat















Surgery PND 5


-N- Sham
--A-- 85% Compression
-0- 95% Compression

Surgery PND 15


Surgery PND 60


Postoperative Day


Figure 8. Numbers of hindlimb steps characterized by slips are represented as percentages of the total number of hindlimb
steps required to cross the 2.2 cm wide beam. Percentages of hindlimb slips ( SEM) are shown for each postoperative day
of interest for rats that received sham surgery, the 85% compression, or the 95% compression on postnatal day 5, 15, or 60.
Only 3 rats that received the 95% compression on PND 5 and 3 rats that received the 85% compression on PND 60 traversed
the beam.








(ps < 0.05). On POD 21, rats that received sham surgery on PND 15 had higher

percentages of hindlimb slips than the young-adult rats (ps < 0.05), but rats of the two

youngest age groups did not differ from each other (p > 0.05). The percentages of

hindlimb slips of rats of the three age groups that received sham surgery did not

significantly differ on POD 28 (ps > 0.05). When the entire postoperative period was

examined in rats that received surgery on PND 15 or 60, the percentage ofhindlimb slips

was higher in rats that received surgery on PND 15 than on PND 60 [F(1, 14) = 10.76, p

< 0.01]. Furthermore, the percentage of hindlimb slips throughout the postoperative

period for rats of those two age groups resulted in a significant effect of POD [F(4, 56) =

6.77, p < 0.001]. The percentage of hindlimb slips decreased between PODs 1 and 7 (p <

0.05), with little change thereafter (ps > 0.05). When rats received the lesser compression

on PND 5 or 15, there was no significant effect of surgery [F(1, 14) = 0.32, p > 0.05] or

POD [F(2, 28) = 2.94, p > 0.05] on the percentage ofhindlimb slips between PODs 14

and 28. When the effects of the lesser compression were examined on PODs 21 and 28

among rats of the three age groups, the percentage of hindlimb slips resulted in a

significant effect of age x POD [F(2, 21) = 24.72, p < 0.001]. Specifically, the

percentage ofhindlimb slips was elevated on PODs 21 and 28 in rats that received the

lesser compression on PND 60, than in rats of the youngest two age groups (ps < 0.05).

Rats that received the lesser compression on PND 15 had a higher percentage of hindlimb

slips on POD 21 than rats that received a similar compression on PND 5 (p < 0.05).

Footfall patterns

Footfall patterns could not be determined for rats that dragged their abdomens

across the beam, rather than walked with weight-supported steps (see Appendix B).









While crossing the 2.2 cm beam, rats primarily used a lateral sequence walking gait in

which 3 limbs remained in contact with the 2.2 cm wide beam and stepping of the left

hindlimb was followed by the left forelimb, then the right hindlimb and finally by the

right forelimb. Following surgery on PND 5, only 2 rats that received the greater

compression traversed the beam using weight-supported steps on POD 21 and 1 rat

traversed the beam on POD 28. Therefore, footfall patterns were statistically analyzed

for rats that received either the lesser compression or sham surgery, but data for rats that

received the greater compression were included in the figures for comparison. Following

surgery on PND 5, the percentage of footfall patterns in which 2 (Fig. 9), 3 (Fig. 10), or 4

(Fig. 11) limbs were in stance during beam walking did not result in significant effects of

surgery [Fs(1, 14) < 3.01, ps > 0.05]. The percentage of footfall patterns characterized by

3 limbs in stance changed during the postoperative period [F(2, 28) = 5.56, p < 0.01].

Specifically, the percentage of footfall patterns with 3 feet in stance was higher on POD

21 than on any other POD in rats of the youngest age group (ps < 0.05). Following

surgery on PND 15, the percentages of footfall patterns in which 2 or 4 limbs were

simultaneously in stance during walking across the 2.2 cm wide beam were higher in rats

that received the lesser compression than in age-matched rats that received sham surgery

[Fs(1, 14) < 9.65, ps < 0.01], whereas the percentage of footfall patterns with 3 feet in

stance was lower in rats that received the lesser compression than in rats that received

sham surgery [F(1, 14) = 52.37, p < 0.001]. The percentage of footfall patterns

characterized by 3 feet in stance changed significantly between PODs 7 and 28 [F(3, 42)

= 3.36, p < 0.05] and was characterized by a higher percentage on POD 7 than on POD

28 (p < 0.05). Although footfall patterns were only analyzed for rats that received sham














Surgery PND 5


--- Sham
--A-- 85% Compression
-0- 95% Compression

Surgery PND 15


Surgery PND 60


0

0-

0


0


0
1 7 14 21 28 1 7 14 21 28 1 7 14 21 28
Postoperative Day


Figure 9. Rats crossed the 2.2 cm beam with either 2, 3, or 4 limbs in stance simultaneously. This figure depicts the
percentage of support patterns ( SEM) used throughout the postoperative period in which the body weight was supported by
2 feet on the beam for rats that received surgery on postnatal day 5, 15, or 60. Most rats that received the 95% compression
at any age or the 85% compression on postnatal day 60 did not cross the beam using weight-supported steps and were not
included in this analysis.
















Surgery PND 5


-I- Sham
--A-- 85% Compression
-0- 95% Compression

Surgery PND 15


Surgery PND 60


10 ... .. ..... .U i-I--m !----- I

10- 0 ---- -a----

.0.

:0

0,
1 7 14 21 28 1 7 14 21 28 1 7 14 21 28
Postoperative Day
Figure 10. Rats crossed the 2.2 cm beam with either 2,3, or 4 limbs in stance simultaneously. This figure depicts the
percentage of support patterns (+ SEM) used throughout the postoperative period in which the body weight was supported by
3 feet on the beam for rats that received surgery on postnatal day 5, 15, or 60. Most rats that received the 95% compression
at any age or the 85% compression on postnatal day 60 did not cross the beam using weight-supported steps and were not
included in this analysis.















Surgery PND 5


-0- Sham
--A-- 85% Compression
-0-- 95% Compression
Surgery PND 15


Surgery PND 60


80-

60-

40- A

20 --.......

0
1 7 14 21 28 1 7 14 21 28 1 7 14 21 28
Postoperative Day
Figure 11. Rats traversed the 2.2 cm beam with either 2, 3, or 4 limbs in stance simultaneously. This figure depicts the
percentage of support patterns ( SEM) used throughout the postoperative period in which the body weight was supported by
4 feet on the beam for rats that received surgery on postnatal day 5, 15, or 60. Most rats that received the 95% compression
at any age or the 85% compression on postnatal day 60 did not cross the beam using weight-supported steps and were not
included in this analysis.









surgery on PND 60, data from the 1 rat that traversed the beam using weight-supported

steps following the lesser compression were included in the figure for comparison. As

found for rats of the other age groups, rats that received sham surgery on PND 60

primarily used a footfall pattern in which 3 limbs were simultaneously in stance during

beam walking. However, the percentage of footfall patterns characterized by 2 or 4 limbs

in stance changed significantly during the postoperative period [Fs(4, 28) > 3.23, ps <

0.05]. The percentage of footfall patterns with 2 limbs in stance was higher on PODs 14

and 28 than on POD 1 (ps < 0.05). The percentage of footfall patterns with 4 limbs in

stance was higher on PODs 1 and 7 than on PODs 14 and 28 (ps < 0.05).


Obstacle Avoidance


3.0 cm Beam

Only rats that successfully crossed the 3.0 and 2.2 cm wide beams were tested for

obstacle avoidance (see Appendix B). Throughout the postoperative period, the height of

the obstacles that rats successfully stepped over while traversing the 3.0 cm beam was not

significantly altered by spinal cord compression on PND 5 [Hs(2) < 5.11, ps > 0.05],

PND 15 [Hs(l) < 2.26, ps > 0.05], or PND 60 [Hs(l) = 2.67, ps > 0.05; Fig. 12]. Only

rats that received sham surgery on PND 5 stepped over significantly taller obstacles on

the 3.0 cm beam during the postoperative period [H(2) = 10.64, p < 0.005]. On POD 7

when rats that received sham surgery on PND 15 or 60 both traversed beams, there was

an age-related increase in the height of obstacles that rats successfully stepped over [H(l)

= 6.62, p < 0.01]. Among rats of all three age groups that received sham surgery, there

were significant age-related increases in the height of the obstacles that rats successfully
















Surgery PND 5


--- Sham
--A-- 85% Compression
-0-- 95% Compression
Surgery PND 15


Surgery PND 60


U






a
-o
0
0

'-
-o
C


1 7 14 21 28 i 7 14 21 28 7 14 21 28

Postoperative Day



Figure 12. Only rats that successfully traversed the 3.0 cm wide beam with weight-supported steps were tested for obstacle
avoidance. This figure depicts the tallest obstacle (0.5, 1.2, 1.7, or 2.7 cm) on the 3.0 cm beam that rats of each experimental
group successfully traversed following sham surgery, 85%, or 95% compression of the spinal cord on PND 5, 15, or 60.
Only 3 rats of the youngest age group that received 95% compression of the spinal cord and only 3 rats of the oldest age
group that received 85% compression of the cord performed this task.


2.0-
A.U-~ ~ ~ ~ ~~ ~~~,,,------ -----------------i----------------I -------------------- ___--__---------.

M--* *-*--*-----*---



1.0-



0.0 .








stepped over on PODs 14 [H(2) = 13.02, p < 0.005] and 28 [H(2) = 7.44, p < 0.05].

Among rats that received the lesser compression, there was no effect of age on the height

of the obstacles successfully crossed on POD 14 [H(1) = 0.86, p > 0.05] or on PODs 21

and 28 [Hs(2) < 0.83, ps > 0.05].


2.2 cm Beam

Only rats that successfully traversed the 3.0 cm wide beam with obstacles were

tested for obstacle avoidance on the 2.2 cm wide beam (see Appendix B). Throughout

the postoperative period, the maximum height of the obstacles that rats successfully

stepped over while traversing the 2.2 cm wide beam was not significantly altered by the

compression injury on PND 5 [Hs(2) < 4.69, ps > 0.05] or PND 15 [Hs(l) < 1.08, ps >

0.05; Fig. 13]. In contrast, rats that received the lesser compression on PND 60 did not

step over the tallest two obstacles [Hs(l) = 6.00, ps < 0.05]. Only rats that received sham

surgery [H(2) = 9.63, p < 0.01] or the lesser compression [H(2) = 12.72, p < 0.005] on

PND 5 stepped over significantly taller obstacles during the postoperative period. On

POD 7 when rats that received sham surgery on PND 15 or 60 both traversed the beam,

there was an age-related increase in the height of the obstacles that rats successfully

stepped over [H(1) = 9.93, p < 0.005]. When rats of all three age groups that received

sham surgery traversed the beam, there were age-related increases throughout the rest of

the postoperative period in the height of the obstacles that rats successfully stepped over

[Hs(2) < 8.54, ps < 0.01]. Rats that received the lesser compression on PND 15

successfully stepped over taller obstacles on POD 14 than rats that received a similar

compression on PND 5 [H(l) = 9.05, p < 0.005]. When rats of all three age groups that

received the lesser compression traversed the beam, there were no significant effects of















Surgery PND 5


-- Sham
--A-- 85% Compression
-0- 95% Compression
Surgery PND 15


Surgery PND 60


i-,






C"
0r



O

I-


i 7 14 21 28 1 7 14 21 28 i 7 14 21 28
Postoperative Day


Figure 13. Only rats that successfully traversed the 2.2 cm wide beam with weight-supported steps were tested for obstacle
avoidance. This figure depicts the tallest obstacle (0.5, 1.2, 1.7, or 2.7 cm) on the 2.2 cm beam that rats of each experimental
group successfully traversed following sham surgery, 85%, or 95% compression of the spinal cord on PND 5, 15, or 60.
Only 3 rats of the youngest age group that received 95% compression of the spinal cord and only 3 rats of the oldest age
group that received 85% compression of the cord performed this task.


3.0


2.0.

1-. --------------- --------A

1.0- .. .0 "

001.






50
age on the height of the obstacles that rats stepped over while traversing the 2.2. cm beam

[Hs(2) < 2.63, ps > 0.05].


Parallel Bar Walking


All rats were tested for parallel bar walking, but not all rats successfully traversed

the bars. Although rats that received sham surgery or the lesser compression on PND 5

traversed parallel bars between PODs 14 and 28 that were increasingly far apart [Hs(2) >

8.26, ps < 0.05], there was no significant effect of surgery when each POD was examined

separately [Hs(2) < 4.03, ps > 0.05; Fig. 14]. Surgery on PND 15 did significantly affect

performance on the parallel bars between PODs 7 and 28 [Hs(2) < 13.54, ps < 0.005].

Specifically, rats that received the greater compression on PND 15 did not traverse the

parallel bars throughout the postoperative period (ps < 0.05), whereas rats of the other

two groups traversed parallel bars that were of similar distances apart (ps > 0.05). Rats of

the latter two groups traversed parallel bars throughout the postoperative period that were

increasingly far apart [Hs(4) > 15.02, ps < 0.005]. Most rats that received a spinal cord

compression on PND 60 did not traverse the parallel bars throughout the postoperative

period, resulting in significant effects of surgery [Hs(2) > 11.48, ps < 0.005]. Rats that

received sham surgery on PND 60 crossed parallel bars during the postoperative period

that were increasingly far apart [H(4) = 23.51, p < 0.005].

On POD 7 when rats that had received sham surgery on PND 15 or 60 traversed

the parallel bars, there was an age-related increase in the distance between the parallel

bars that rats traversed [H(1) = 7.17, p < 0.01]. The age-related increase in the distance

between the parallel bars successfully traversed by rats that received sham surgery















Surgery PND 5


--- Sham
--A-- 85% Compression
-0--- 95% Compression

Surgery PND 15


Surgery PND 60


10.

_ 8.

2 6.

S4.

2.

0.

I


Figure 14. This figure depicts the maximum distance between the parallel bars that was crossed on each postoperative day by
rats that received sham surgery, 85%, or 95% compression of the spinal cord on PND 5, 15, or 60.


7 14 21 28 1 7 14 21 28 1 7 14 21 28
Postoperative Day


0..---------- ------------&'I




0-


v









continued was also evident between PODs 14 and 28 when rats of all three age groups

traversed the bars [Hs(2) > 13.04, ps < 0.005]. Among rats that received the lesser

compression, there was an effect of age on the distance between the parallel bars

traversed between PODs 14 and 28 [Hs(2) > 7.17, ps < 0.05]. Specifically, rats that

received the lesser compression on PND 15 crossed parallel bars that were further apart

on POD 14 than did rats of the other two age groups (ps < 0.05). Rats that received the

lesser compression on PND 5 or 15 traversed parallel bars on PODs 21 and 28 that were

further apart than rats that received similar compressions on PND 60 (ps < 0.05), with no

significant difference between rats of the former two groups (ps > 0.05).


Inclined Plane


Between PODs 14 and 28 for rats that received surgery on PND 5 [F(2, 21) = 7.55,

p < 0.01] and throughout the postoperative period for rats that received surgery on PND

15 [F(2, 20) = 56.98, p < 0.01], performance on the inclined plane was surgery-dependent

(Fig. 15). Rats of both age groups that received sham surgery or the lesser compression

maintained balance on a steeper incline than age-matched rats that received the greater

compression (ps < 0.05), with little difference between the former two groups (p > 0.05).

Performance on the inclined plane also improved during the postoperative period in rats

that received surgery on PND 5 [F(2, 42) = 28.51, p < 0.01] or 15 [F(4, 80)= 25.54, p <

0.01]. Following surgery on PND 5 or 15, balance on successively higher inclines was

achieved between the first two test sessions (regardless of POD; ps < 0.05), with little

change thereafter (ps > 0.05). Performance on the inclined plane following surgery on

PND 60 resulted in significant effects of surgery [F(2, 20) = 21.40, p < 0.01], POD














Surgery PND 5


--- Sham
--A-- 85% Compression
-0 95% Compression

Surgery PND 15


Surgery PND 60


Postoperative Day


Figure 15. Following sham surgery, 85% compression, or 95% compression on postnatal days 5, 15, or 60, rats were tested
throughout the 4-week postoperative period for the maximum degree of incline (C SEM) that the rats maintained posture and
balance for at least 5 s on the inclined plane.







54
[F(4, 80) = 10.85, p < 0.01], and surgery x POD [F(8, 80) = 3.56, p < 0.05]. Specifically,

the maximum incline on which rats of that age group maintained their balance was higher

throughout the postoperative period in rats that received sham surgery than in rats that

received the greater compression (ps < 0.05). In contrast, rats that received the lesser

compression, performed similarly to rats that received the greater compression on POD 1

(p > 0.05), but were similar to rats that received sham surgery throughout the remainder

of the testing period (ps > 0.05).

The maximum degree of incline on which rats maintained balance and position

throughout the postoperative period was dependent on the age of the rat at the time of

surgery. Age-related changes in performance on the inclined plane following sham

surgery on PND 15 or 60 resulted in a significant effect of age x POD [F(4, 56) = 5.85, p

< 0.01]. On POD 1, rats that received sham surgery on PND 15 maintained balance on a

shallower incline than rats that received the surgery on PND 60 (p < 0.05), whereas the

opposite was true on PODs 7 and 21 (ps < 0.05). An effect of age was also noted

between PODs 14 and 28 when rats of all three ages were tested on the inclined plane

[F(4, 42) = 8.39, p < 0.01]. Specifically, rats that received sham surgery on PND 5

maintained balance on a shallower incline on POD 14 than rats of the other two age

groups (ps < 0.05). Rats of the youngest two age groups maintained position on a higher

incline on POD 21 than rats of the oldest age group (ps < 0.05), with little difference

between the former two groups (ps > 0.05). Rats that received the lesser compression on

PND 15 or 60 maintained balance and position on a lower incline on POD 1 than on any

other day [F(4, 52) = 24.07, p < 0.01], but rats that received the lesser compression on

PND 15 generally maintained position and balance on a higher incline than rats that








received a similar compression on PND 60 [F(1, 13) = 6.46, p < 0.05]. When rats of all

three ages were tested on the inclined plane, performance resulted in a significant age x

POD interaction [F(4, 40) = 4.18, p < 0.01]. Except on POD 14 when rats that received

the lesser compression on PND 15 maintained balance on a higher incline than rats that

received a similar compression on PND 5 (ps < 0.05), rats of those two age groups

maintained position on a higher incline than rats of the oldest age group (ps < 0.05), with

little difference between the former two groups (ps > 0.05). Following the greater

compression on PND 15 or 60, performance on the inclined plane resulted in a significant

effect of age x POD [F(4, 52 = 3.15, p < 0.05]. Specifically, rats that received the greater

compression on PND 15 maintained position and balance on a higher incline on POD 7

(p < 0.05), than rats that received a similar compression on PND 60, with little difference

throughout the rest of the postoperative period (ps > 0.05). Among rats of all three age

groups, performance on the inclined plane following the greater compression resulted in a

significant effect of age x POD [F(4, 40) = 3.13, p < 0.05]. Rats that received the greater

compression on PND 5 maintained balance on a steeper incline on POD 21 than rats of

the other two age groups (ps < 0.05) and on POD 28 than rats of the oldest age group (p <

0.05). Because absolute weight [F(2, 61) = 0.34, p > 0.05] and relative weight gain [F(2,

61) = 1.74, p > 0.05] of the rats were not significantly affected by surgery, decreased

performance on the elevated beams and the inclined plane by rats that received

midthoracic spinal cord compression was not due to surgery-related differences in the

weights of the rats (see Appendix C).









Hot Plate


In rats of all three groups that received surgery on PND 5, latencies to withdraw or

to lick one hindpaw resulted in significant effects of POD [F(4, 84) = 144.40, p < 0.01]

and surgery x POD [F(8, 84) = 4.72, p < 0.01; Fig. 16]. Except for rats that received the

greater compression, latencies to withdraw one hindpaw increased between PODs I and 7

for rats that received the lesser compression or sham surgery on PND 5 (ps < 0.05), with

no significant difference between those two groups (ps > 0.05). Latencies to lick one

hindpaw decreased significantly between PODs 14 and 28 for rats of those two surgery

groups (ps < 0.05), with no difference between surgery groups (ps > 0.05). In contrast,

latencies to withdraw one hindpaw were shorter on POD 7 (ps < 0.05) and latencies to

lick one hindpaw were longer on POD 28 (ps < .05) for rats that received the severe

compression, relative to rats of the other two surgery groups. Latencies to lick one

hindpaw following surgery on PND 15 resulted in significant effects of surgery [F(2, 20)

= 54.28, p < 0.01], POD [F(4, 80)= 38.25, p < 0.01], and surgery x POD [F(8, 80) =

10.52, p <0.01]. Hindpaw licking on the hot plate did not emerge during the 30 s time

limit in rats of that age group until POD 7, at which time lick latencies were longer in rats

that received the spinal cord compression than in rats that received sham surgery (ps <

0.05). Latencies to lick one hindpaw then decreased during the postoperative period for

rats that received the lesser compression or sham surgery (ps < 0.05), with no difference

them (ps > 0.05). In contrast, rats that received the greater compression on PND 15 never

licked the hindpaws within the 30 s time limit (ps < 0.05). Latencies to lick one hindpaw

following surgery on PND 60 also resulted in significant effects of surgery [F(2, 20) =

78.89, p < 0.01], POD [F(4, 80) = 6.29, p < 0.01], and surgery x POD [F(8, 80) = 2.56,















Surgery PND 5


--- Sham
--A-- 85% Compression
0-- 95% Compression

Surgery PND 15


Surgery PND 60


Postoperative Day


Figure 16. Following sham surgery, 85%, or 95% compression of the spinal cord on postnatal day 5, 15, or 60, rats were
primarily tested throughout the 4-week postoperative period for the latency ( SEM) to lick one of the hindpaws on a hot
plate. Data on postoperative days I and 7 of rats of the youngest age group represent the latencies ( SEM) to withdraw one
hindpaw from the surface of the hot plate.







58
p < 0.05]. Latencies to lick one hindpaw were much longer throughout the postoperative

period in rats of that age group that received a spinal cord compression than in rats that

received sham surgery (ps < 0.05), with little difference between the two compression

groups (ps > 0.05). Lick latencies decreased between PODs 1 and 7 in young-adult rats

that received sham surgery (p < 0.05) with little change thereafter (ps > 0.05).

Performance on the hot plate also resulted in a significant age x POD interaction

for rats that received sham surgery [F(8, 84) = 33.02, p < 0.001], the lesser compression

[F(8, 80) = 25.95, p < 0.001], or the greater compression [F(8, 80) = 145.48, p < 0.001].

On PODs 1 and 7, lick latencies were shorter rats that received sham surgery on PND 60

than on PND 15 (ps < 0.05). When lick latencies were assessed in rats of all three age

groups, lick latencies were increasingly short on each POD with increased age of the rat

(ps < 0.05), with little difference on PODs 21 and 28 between rats that received sham

surgery on PND 15 or 60 (ps > 0.05). On PODs 1 and 7, there were no significant

differences in the latencies to lick one hindpaw by rats that received the lesser

compression on PND 15 or 60 (ps > 0.05). However, lick latencies of rats that received

the lesser compression on PND 15 decreased throughout the rest of the postoperative

period and were generally shorter than lick latencies of rats of the other two age groups

that received the lesser compression (ps < 0.05). Except on POD 28 when rats that

received the lesser compression on PND 5 licked the hindpaws sooner than rats that

received the injury on PND 60 (p < 0.05), lick latencies of rats of those two age groups

were not different from each other (ps > 0.05). Except on POD 28 in rats of the youngest

age group (ps < 0.05), rats that received the greater compression of the spinal cord did not

lick the hindpaws within the 30 s time limit (ps > 0.05).








Lesion Size


The rostral-most lesion was located between vertebral T4-Ts and the caudal-most

lesion was located between vertebral Ts-T9. Except for rats that received the greater

compression on PND 5 [R = -0.72, p < 0.05], hindlimb sensorimotor function on POD 28

was not dependent on lesion location [-0.13 < Rs < 0.38, ps > 0.05; Fig. 17]. Although

lesion length was not quantified, no lesion extended further than two segments rostral to,

or caudal from, the lesion epicenter. The lesion epicenter was characterized by

preferential loss of spinal cord gray matter, with the amounts of gray and white matter

present depending on severity of compression (Figs. 18, 19, & 20). Generally, there was

almost complete loss of central gray matter, accompanied by a small central cavitation, in

rats that received the lesser compression on PND 5 or 15. When age-matched rats

received the greater compression injury, there was complete elimination of central gray

matter and significant degeneration of white matter. In those rats, the white matter

generally consisted either of a thin strip or a thin ring of tissue that ranged in thickness

between 12.5 pmu and 350 pm or between 8.25 pm and 175 mn for rats that received the

greater compression on PND 5 or 15, respectively. Following compression of the 60-

day-old spinal cord, the lesion epicenter of rats of both injury groups was largely filled

with fibrous scar tissue and contained little CNS tissue that was not undergoing Wallerian

degeneration.

Although there was significant spinal cord damage in rats of both compression

groups, the cross-sectional area of the tissue at the lesion epicenter resulted in a

significant age x surgery interaction [F(4, 61) = 41.48, p < 0.001; Fig. 21]. Following the

lesser spinal cord compression, the amount of tissue at the lesion epicenter was













Surgery PND 5


T5 T6 T7 T8


* Sham
A 85% Compression
0 95% Compression
Surgery PND 15


T5 T6 T7 T8


Surgery PND 60


T4 T5 T6 T7 T8 T9


Midthoracic Spinal Cord Segment Injured

Figure 17. Ratings of overground locomotion on postoperative day 28 are depicted as a function of the midthoracic spinal
cord segment that contained the lesion epicenter for each rat that received sham surgery, the 85% compression, or the 95%
compression on postnatal day 5, 15, or 60. A score of 21 represents the overground walking of an uninjured, adult rat.


0 A a A a I A A a A a g
0 0 0 0 AA
5 0 O A 0


.0 0
5 0 0 0

50 0


















































Figure 18. Representative photomicrographs of the lesion epicenter, 29 days following
surgery to the midthoracic spinal cord of 5-day-old rats. Calibration bar = 500 Gpn.
A) sham; B) 85% compression; C) 95% compression.


















































4


Figure 19. Representative photomicrographs of the lesion epicenter, 29 days following
surgery to the midthoracic spinal cord of 15-day-old rats. Calibration bar = 500 pm.
A) sham; B) 85% compression; C) 95% compression.







63































"4






7.













Figure 20. Representative photomicrographs of the lesion epicenter 29 days following
surgery to the midthoracic spinal cord of 60-day-old rats. Calibration bar = 500 Jim.
A) sham; B) 85% compression; C) 95% compression.













Surgery PND 5


3.


2.


0.


Surgery PND 15


Surgery PND 60


Sham 85% 95% Sham 85% 95% Sham 85% 95%


Figure 21. This figure depicts the amount of spinal cord tissue at the lesion epicenter ( SEM) following sham surgery, 85%
compression, or 95% compression on postnatal day 5, 15, or 60. The cross-sectional area of the spinal cord increased with age.
Therefore, the amount of tissue at the lesion epicenter of rats that received 85% or 95% compression of the spinal cord was
also calculated as a percentage of the size of the spinal cord of age-matched controls (insets).









significantly decreased in rats of the oldest age group than in rats of the other two age

groups (ps < 0.05). However, there was no significant difference in the amount of tissue

at the lesion epicenter of rats of the three age groups that received the greater

compression (ps > 0.05). Within each injury group, there was little difference in the

amount of tissue at the lesion epicenter of rats that received the compression as neonates

(ps > 0.05). Spinal cord size of rats that received sham surgery increased during

ontogeny (ps < 0.05). When the absolute amount of tissue at the lesion epicenter was

expressed as a percentage of control tissue size, the percentage of tissue at the lesion

epicenter was also larger in rats that received the lesser compression than in rats that

received the greater compression [F(1, 40) = 31.64, p < 0.001]. However, the age x

surgery interaction was also significant [F(2, 40) = 7.25, p < 0.01]. Subsequent analyses

revealed that the percentage of tissue at the lesion epicenter decreased with increased

severity of compression in rats that received surgery on PND 5 or 15 (ps < 0.05), but did

not significantly differ between the two groups that received a spinal cord compression

on PND 60 (p > 0.05). The percentage of tissue at the lesion epicenter decreased with

increased age in rats that received the lesser compression (ps < 0.05). However, there

was no significant difference in the percentage of tissue at the lesion epicenter of rats of

the three age groups that received the greater compression (ps > 0.05). Except for rats

that received the greater compression on PND 15 [R = 0.77, p < 0.05], the amount of

spinal cord tissue at the lesion epicenter was not dependent on the spinal cord level [-0.53

< Rs < 0.33, ps > 0.05; Fig. 22].














Surgery PND 5


* Sham
A 85% Compression
0 95% Compression

Surgery PND 15


Surgery PND 60


4.0
| U
3.5-
3.0-
2.5-
2.0.
1.5- A
1.0O
0.5AA A A A
0.0o O n O 0 9 9 A


I-
U
0
5.
o

U,
s

*s


T5 T6 T7 T8


T4 T5 T6 T7 T8 T9


Midthoracic Spinal Cord Segment Injured


Figure 22. This figure shows the amount of spinal cord tissue at the lesion epicenter, for individual rats that received sham
surgery, the 85% compression, or the 95% compression, as a function of the midthoracic spinal cord segment that was injured
on postnatal day 5, 15, or 60.


T4 T5 T6 T7 T8 T4















CHAPTER 4
DISCUSSION


Because the spinal cord of adult humans is rarely transected during injury, animal

models of incomplete SCI have been developed to elucidate the behavioral and

neuroanatomical sequelae postinjury. Although human infants are not exempt from

traumatic SCI, the effects of incomplete injury to the developing spinal cord have not

been thoroughly investigated. Instead, most knowledge regarding the effects of SCI

during development has been obtained from infant animals with partial or complete

spinal cord transactions. The consequences of injury to the neonatal central nervous

system are not necessarily the same as the consequences of injury to the mature nervous

system (see Kolb, Holmes, & Whishaw, 1987; Kolb & Whishaw, 1985; Yager, Shuaib, &

Thornhill, 1996; Stelzner et al., 1975; Weber & Stelzner, 1977). Recovery processes

invoked following traumatic injury to the immature nervous system act on a background

of processes important for normal growth and development. For those reasons, efficacy

of treatments designed for adults following traumatic SCI may not be the same in infants

and obligates elucidation of the behavioral, neuroanatomical, and neurophysiological

effects of pediatric SCI. The first aim of the present experiments was to quantify age-

related changes in the behavioral and neuroanatomical consequences of midthoracic

spinal cord compression. Rating scales are commonly used with adult animals with SCIs

to describe locomotor function during overground walking. However, ratings of

overground walking provide only a subjective assessment of gross locomotor skill.

67







Therefore, the second aim of the present experiments was to compare ratings of

overground walking with performance on a quantitative battery of tasks that challenge

hindlimb sensorimotor function postinjury. Results of the present experiments suggest

(1) an age-dependent decrease in hindlimb sensorimotor function following midthoracic

spinal cord compression, (2) that ratings of overground locomotion do not accurately

depict deficits in hindlimb function postinjury, and (3) that numerous tests should be

employed to fully characterize injury-related sensorimotor deficits.


Age-Dependent Effects of Midthoracic Spinal Cord Compression


In adult animals, one factor that contributes to neurologic outcome following SCI

is the amount of compression that the spinal cord undergoes during the traumatic event

(Gruner et al., 1996). Elucidation of age-related changes in the behavioral and

neuroanatomical effects of midthoracic spinal cord compression is complicated by an

age-dependent increase in the size of the spinal cord. Therefore, spinal cords of rats of

the present experiments were compressed by a percentage of the uncompressed width of

the spinal cord to produce compressions of the same relative amount in rats of the three

age groups. Regardless of age, increasing the amount of compression decreased hindlimb

function on the sensorimotor battery of tasks. Although spinal cords of rats of the present

experiments were compressed by the same relative amount (within an injury group)

during ontogeny, hindlimb sensorimotor function postinjury decreased with increased age

of the rat. Previous reports with adult animals suggest that there is preferential

degeneration of spinal cord gray matter following traumatic SCI and that the amount of

white matter spared depends on the severity of the injury (e.g., Blight, 1983; Noble &








Wrathall, 1985). Furthermore, the quality of hindlimb sensorimotor function is

proportional to the amount of tissue spared at the lesion epicenter (e.g., Basso et al.,

1996; Noble & Wrathall, 1985). In the present experiments, the amount of tissue at the

lesion epicenter decreased with increased compression of the spinal cord in rats of the

youngest two age groups. However, there was no significant difference in the amount of

tissue at the lesion epicenter between the two groups of rats that received spinal cord

compression on PND 60. Furthermore, an age-related decrease in the amount of tissue at

the lesion epicenter was found only among the three groups of rats that received the

lesser compression. Thus, results of the present experiments do not completely support a

direct relationship between the amount of tissue at the lesion epicenter and the quality of

hindlimb sensorimotor function.

Performance on the sensorimotor battery of tasks of rats of the present experiments

that received the lesser compression on PND 5 was indistinguishable from sham controls

throughout the postoperative period. Performance of rats that received the lesser

compression on PND 15 was only marginally different from sham controls during beam

walking. Rats of that age group that received the injury had a higher percentage of

hindlimb slips during beam walking than did age-matched controls. Those rats were also

more likely to traverse the beams with all four feet in stance than age-matched controls,

which would afford rats that received the compression greater stability during beam

walking. Speed of walking across the beams was not measured in the present

experiments because forward progression by rats of all ages was interrupted by pauses.

Footfall patterns vary with speed of locomotion (Hildebrand, 1989), so greater use of a 4-

limb footfall pattern by rats that received the lesser compression on PND 15 may reflect a








70
slower walking speed on the beam, relative to sham controls. Because rats often paused

with all four feet on the beam following a slip or fall, elevations in the percentage of

footfalls with 4 limbs in stance may be confounded by the injury-related increase in the

percentage ofhindlimb slips.

Despite few changes to sensorimotor functioning in rats that received the lesser

compression on PND 5 or 15, midthoracic gray matter had completely degenerated in

most rats and, in some cases, resulted in the formation of a small central cavity. The

cross-sectional area of tissue at the lesion epicenter decreased between rats of these two

age groups. Degeneration of midthoracic gray matter would mainly cause loss of sensory

input from a few dermatomes and loss of interneurons and motoneurons important for

control of axial muscles or for autonomic functions. Therefore, few alterations to

hindlimb sensorimotor function would be expected with minimal impingement of the

lesion on white matter tracts. In support of this notion, kainic acid, which selectively

kills neurons without damaging fibers of passage (e.g., Coyle & Schwarcz, 1976),

produces minor locomotor deficits in ratings of overground walking when injected into

the midthoracic spinal cord of rats (Magnuson, Trinder, Zhang, Burke, Morassutti, &

Shields, 1999). Thus, the failure of all behavioral tasks of the present experiments to

clearly distinguish between rats that received the lesser compression or sham surgery on

PND 5 suggests that descending, ascending, propriospinal, and intraspinal systems of rats

that received the lesser compression were functioning in a near-normal capacity.

Because the corticospinal tract is important for accuracy of limb placement during

walking (Hicks & D'Amato, 1975), elevations in the percentage ofhindlimb slips during

beam walking by rats that received the lesser compression on PND 15 suggests that the








spinal cord lesion in those rats impinged upon axons of that descending, supraspinal

system.

In contrast to the effects of injury to the neonatal spinal cord, behavioral

performance of rats that received the lesser compression on PND 60 was severely

disrupted on all tasks, except overground walking and the inclined plane. Rats of that

experimental group suffered an initial loss of hindlimb joint movement and weight

support following spinal cord compression. Hindlimb weight support, stepping, and

coordination between brachial and pelvic girdles dramatically improved in those rats

during the first postoperative week. By the end of the postoperative period, there were

only deficiencies in foot position at lift off, tail position, and trunk stability. Except for

an initial deficit on POD 1, performance of those rats on the inclined plane was also

similar to sham controls throughout the remainder of the postoperative period.

As expected from the behavioral findings, the percentage of tissue at the lesion

epicenter was smaller in rats that received the lesser compression on PND 60 than in rats

that received a similar compression on PND 5 or 15. In fact, there was almost complete

loss of all CNS tissue at the lesion epicenter of rats of the oldest age group. The spinal

cord cavity mainly contained astrocytic scarring and the small patches of CNS tissue that

remained were undergoing Wallerian degeneration. However, it is likely that there were

functional axons coursing through this necrotic tissue that contributed to hindlimb motor

function following compression of the 60-day-old spinal cord. Although cats can be

trained to support the weight of the hindquarters following spinal cord transaction (see

Hodgson, Roy, de Leon, Dobkin, & Edgerton, 1994; Lovely, Gregor, Roy, & Edgerton,

1986), rats that receive no special training following spinal cord transaction do not use






72
the hindlimbs for weight support (Weber & Stelzner, 1977). Pathways of the ventral and

ventrolateral spinal cord seem to be important for locomotor control (see Eidelberg,

1981; Eidelberg, Story, Walden, & Meyer, 1981; Steeves & Jordan, 1980). Lesions of

the motor cortex of rats causes the limbs to slip off of beams, whereas walking over a flat

surface is not disrupted (Hicks & D'Amato, 1975). More recent evidence shows that

animals walk with the hindlimbs following complete transaction of the ventral and

ventrolateral tracts, but hindlimb posture and weight support is severely reduced (for

review see Rossignol, Chau, Brustein, Belanger, Barbeau, & Drew, 1996). The initial

loss of hindlimb weight support and stepping in rats of the oldest age group was probably

due to spinal shock. The mature spinal cord is dependent on inputs from descending

systems for normal functioning (see Weber & Stelzner, 1977). Spinal shock is a

decreased responsivity of motor circuits following denervation and may be due, at least in

part, to overactivity ofintraspinal inhibitory system (see Robinson & Goldberger, 1986b;

Simpson, Robertson, & Goodman, 1993). Recovery of overground walking in rats that

received the lesser compression on PND 60 suggests that some fibers of tracts of the

ventral and ventrolateral spinal cord survived the injury and contributed to overground

walking. However, it is important to note the importance of sensory influences on motor

function (see Delcomyn, 1980). Stretching of the skin during overground walking may

have indirectly activated locomotor circuits caudal to the lesion, which could enhance

locomotor function. Although such mechanisms would aid locomotor function in rats of

all age and injury groups, the effect may be more dramatic in rats in which the amount of

tissue at the lesion epicenter was severely reduced, which presumably reflects severe

impairment in communication between supraspinal and spinal sensorimotor systems.








Increased sparing of neurons of the rubrospinal (Fehlings & Tator, 1995; Midha,

Fehlings, Tator, Saint-Cyr, & Guha, 1987), vestibulospinal, reticulospinal, and

raph6spinal (Midha et al., 1987) systems have been correlated with higher scores on the

inclined plane. Because performance on the inclined plane was largely intact in rats of

this experimental group, hindlimb sensorimotor performance following the lesser

compression on PND 60 was likely influenced by contributions from those supraspinal,

descending systems. In contrast to the near-normal performances during overground

walking and on the inclined plane, only 3 rats that received the lesser compression on

PND 60 walked on the elevated beams or parallel bars by PODs 21 and 28. Severe

impairments in beam- and parallel bar walking suggest that the spinal cord lesion

disrupted fibers of the corticospinal tract because performance on those tasks require

greater accuracy of limb placement than does overground walking. In addition, most rats

that received the lesser compression on PND 60 did not lick the hindpaws within the 30 s

time limit on the hotplate. Nociceptive pathways for cutaneous pain largely ascend in the

ventrolateral spinal cord (Willis & Westlund, 1997) and forebrain circuits are required for

the hindpaw lick response on the hotplate (Woolf 1984). Therefore, results of the

present experiments suggest functional disruption of ascending nociceptive pathways or

descending motor pathways important for that behavioral response.

In rats of all three age groups that received the greater compression of the spinal

cord, performance on all behavioral tasks was disrupted. Ratings of overground walking

most clearly illustrate an age-related decrease in sensorimotor function in these rats.

Overground walking of rats of the youngest age group was rated near-normal by the end

of the postoperative period. However, those rats retained deficiencies in foot position at









lift off, tail position, and trunk stability. Rats that received a similar compression on

PND 15 were also deficient for toe clearance during the swing phase of the step cycle.

Following compression of the 60-day-old spinal cord, the hindquarters of most rats no

longer supported weight and the hindlimb movements were not apparently coordinated

with forelimb movements. Among all rats that received the greater compression, only 3

rats that received the injury on PND 5 traversed the elevated beams and parallel bars.

Furthermore, only rats that received the compression on PND 5 licked the hindpaws on

the hotplate within the 30 s time limit (on POD 28 only).

Only a thin strip or thin ring of white matter remained at the lesion epicenter of

rats that received the greater compression on PND 5 or 15, whereas the lesion epicenter

of rats of the oldest age group contained astrocytic scarring and was devoid ofCNS

tissue. However, some functional axons may have been dispersed throughout the

necrotic tissue and contributed to hindlimb sensorimotor functioning. The age-dependent

decrease in the quality of overground walking of rats of that received the greater

compression suggests an age-dependent impingement of the lesion on descending fibers

of the ventral and ventrolateral tracts, as well as on ascending and propriospinal systems.

However, the cross-sectional area of tissue at the lesion epicenter of rats of this injury

group did not differ significantly with age. Thus, reorganization ofintraspinal systems

may have played a greater role in the recovery of locomotor function of rats of the

youngest age groups than in rats of the oldest age group.









Neuroanatomical Contributions to Recovery of Function


Regardless of the age of the rat at the time of surgery, there was evidence for

improvement in hindlimb sensorimotor function during the 4-week postoperative period,

as has been reported following injury to the adult spinal cord (e.g, Gale et al., 1985;

Gruner et al., 1996). Rats of the present experiments that received a spinal cord

compression on PND 5 or 15 had greater locomotor function immediately postinjury

(sparing), as well as greater recovery of hindlimb sensorimotor function during the

postoperative period than rats that received similar compressions on PND 60. This age-

dependent decrease in sparing and recovery of function postinjury exemplifies the infant

lesion effect (e.g., Bregman & Goldberger, 1982; 1983a; Robinson & Goldberger,

1986a). Behavioral recovery following injury to the developing spinal cord occurs on a

background of processes active for normal growth and maturation. Thus, performance of

rats of the two youngest age groups on the battery of tasks of the present experiments was

largely influenced by sensorimotor maturation.

Rats are altricial mammals that rapidly develop the raised, quadrupedal posture for

walking within the first two weeks of postnatal life (Altman & Sudarshan, 1975).

However, locomotor skills continue to develop throughout the first postnatal month (see

Altman & Sudarshan, 1975; Clarke & Williams, 1994). In the present experiments, a

rating of'21' on the BBB locomotor recovery scale represents the hindlimb locomotor

function of intact, adult rats. Although the BBB locomotor recovery scale was not ideal

for describing locomotor function of neonatal rats, the scale enabled a rough description

of age-related changes in locomotor function. Relative to control rats of the oldest age

group, low scores on PODs 1, 7, and 14 of rats that received the lesser compression or








sham surgery on PND 5 and the low score on POD 1 of rats that received the lesser

compression or sham surgery on PND 15 reflect locomotor immaturity, rather than

surgery-related deficits. Generally, those rats continued to show outward rotation of the

hindfeet at lift off after all other characteristics of the gait (including toe clearance, tail

elevation, and trunk stability) were mature. The smooth surface of the inclined beams

and parallel bars may have also revealed the immature locomotor skills of the young rats

(also see Altman & Sudarshan, 1975). The percentage ofhindlimb slips during beam

walking was initially high and scores on the inclined plane were initially low in rats that

received sham surgery as neonates. Rats that received surgery as neonates also stepped

over increasingly tall objects on the beams and traversed parallel bars that were

increasingly far apart during the postoperative period. Those latter two findings probably

reflect ontogenetic increases in the size of the rat.

Sensorimotor immaturity of rats of the youngest two age groups was also revealed

on the hot plate task. Tailflick (withdrawal) latencies in response to noxious heating of

the tail of an adult rat reflect activation of spinal circuits (see Irwin et al., 1951). Relative

to adult rats, cutaneous reflexes of young rats are exaggerated in amplitude and duration

(e.g., Stelzner, 1971), suggesting that inhibition of spinal circuits by supraspinal systems

is immature in young animals. Inhibitory systems, such as those that descend as the

dorsolateral funiculus (Fields & Basbaum, 1978), mature anatomically (Leong et al.,

1984) and functionally (e.g., Fitzgerald & Koltzenberg, 1986; Van Praag & Frenk, 1991)

during the first three postnatal weeks. In the present experiments, latencies to withdraw

one hindpaw from the surface of the hot plate increased between PODs 1 and 7 in rats

that received sham surgery on PND 5, reflecting the age-related increase in descending







77
inhibition of spinal reflexes. Forebrain circuits are required to lick the hindpaws on the

hot plate (Woolf, 1984). Therefore, failure of rats of the youngest two age groups

(regardless of surgery group) to lick one hindpaw on the hot plate on the first day of

testing (regardless of POD) reflects immaturity of sensory or motor systems important for

that behavioral response to noxious heat (also see McEwen & Tucker, 2000). Adult rats

that are familiar with the hot plate testing environment have shorter lick latencies than

naive rats, which are due to a reduction in novelty-induced analgesia (Bardo & Hughes,

1979; Gamble & Milne, 1989; Plone, Emerich, & Lindner, 1996). In the present

experiments, latencies to lick one hindpaw on the hot plate decreased between PODs 1

and 7 in rats that received sham surgery on PND 60. That finding probably reflects a

reduction in novelty-induced analgesia with experience, rather than maturation of sensory

or motor systems.

In addition to contribution by normal processes of growth and development,

compensatory changes invoked following an injury may lead to greater recovery of

function of rats that received an injury during infancy than in adulthood. Descending

systems that survive an injury (spared systems) have been shown to contribute to

locomotor recovery in adult animals through activation of commissural collaterals (e.g.,

Harris, Little, & Goldstein, 1994) and through sprouting (e.g., Aoki, Fujito, Satomi,

Kurosawa, & Kasaba, 1986). However, injury to the developing nervous system results

in sprouting that is more rapid (e.g., Gall & Lynch, 1978; 1981) and more profuse (e.g.,

Gomez-Pinilla, Villablanca, Sonnier, & Levine, 1986; Hulsebosch & Coggeshall, 1983;

Prendergast & Misantone, 1980) than in the mature system. Furthermore, upregulation of

postsynaptic receptors following injury to the adult nervous system denervationn








supersensitivity) may also aid locomotor function postinjury by enhancing

responsiveness of lumbar motor circuits to diminished descending inputs. However,

receptor levels are already elevated in the immature nervous system, relative to adults

(e.g., Gonzalez, Fuchs, & Droge, 1993; Kalb, Lidow, Halsted, & Hockfield, 1992), which

may provided enhanced responsiveness of lumbar motor circuits of the immature cord

and support greater locomotor function immediately postinjury. Those compensatory

changes postinjury may partly explain the rapid improvements in functional recovery of

rats of the present experiments following compression of the infant spinal cord than

following compression of the 60-day-old spinal cord. For example, rats that received the

greater compression of the spinal cord on PND 15 showed the largest improvement in

overground walking and the largest reduction in the percentage of hindlimb slips during

beam walking between PODs 1 and 7. In contrast, the largest improvement in

overground walking in rats that received the greater compression on PND 60 occurred

within the first two postoperative weeks and the percentage ofhindlimb slips during

beam walking only decreased slightly during the last two days of the postoperative

period.

Although fibers of most descending systems have reached the lumbosacral spinal

cord by birth (Leong et al., 1984), some of those projection systems are not mature and

continue to expand their innervation of spinal circuits during postnatal life. Therefore,

late-developing systems that were not injured by compression of the developing spinal

cord may continue to grow and innervate targets caudal to the lesion. Descending

projections by catecholaminergic (Aramant, Giron, & Ziegler, 1986; Rajaofetra, Poulat,

Marlier, Geffard, & Privat, 1992; Tanaka, Takahashi, Miyamoto, Old, Cho, & Okuno,






79
1996) and serotonergic (Bregman, 1987; Rajaofetra, Sandillon, Geffard, & Privat, 1989;

Tanaka, Mori, & Kimura, 1992) systems of the brainstem continue to mature in

distribution and density during the first 2 to 3 postnatal weeks. In addition, the

corticospinal tract, originating from the most posterior cortex, does not reach the

midthoracic spinal cord until around PND 7 (Joosten, Gribnau, & Dederen, 1987).

Although those projections are normally retracted during development (Joosten et al.,

1987), they may continue to grow caudally in the injured spinal cord to form functional

synaptic connections with denervated targets. Evidence suggests that fibers of

developing tracts that survive an injury do grow around a lesion (e.g., Bernstein &

Stelzner, 1983; Bregman & Goldberger, 1983b). In addition, exuberant connections that

are already in place at the time of injury may be maintained (see Stanfield, 1989) and

contribute to locomotor sparing and recovery of function following injury to the infant

spinal cord. The extent to which late-developing fiber systems contributed to locomotor

recovery in rats of the present experiments is not clear. Because the spinal cords were

harvested 29 days following the midthoracic spinal cord compression, the amount of

tissue at the lesion epicenter of rats of the oldest age group reflects the amount of tissue

that was spared postinjury. In contrast, the amount of tissue at the lesion epicenter of rats

of the two youngest age groups probably reflects growth of late-developing fiber systems,

as well as sparing of more mature systems, such as the rubrospinal system (see Shieh,

Leong, & Wong, 1983) that survived the injury.

Irrespective of contributions by descending systems to locomotor recovery,

changes in intraspinal functioning are also likely to contribute to functional recovery

following SCI. Evidence suggests that functional autonomy or adaptability of spinal






80
motor circuits decreases with age. Following complete spinal cord transaction, rats less

than 12 days of age recover good hindlimb posture and overground walking, despite

isolation of lumbar motor circuits from descending and propriospinal systems. In

contrast, complete transaction of the spinal cord on PND 15 or later results in increased

spinal shock and little recovery of hindlimb function, if any (Stelzner et al., 1975; Weber

& Stelzner, 1977). The age-dependent decrease in locomotor recovery from spinal cord

transaction corresponds to a period of rapid synaptogenesis in the developing lumbar

spinal cord (Gilbert & Stelzner, 1979), which suggests that lumbar motor circuits become

more dependent on supraspinal inputs for normal functioning after PND 15 (Weber &

Stelzner, 1977). The age-related decrease in functional autonomy of the spinal cord

corresponds to an age-related increase in intraspinal inhibitory systems, which seem to be

dependent on descending input for complete development (see Robinson & Goldberger,

1986b). In contrast, immature lumbar motor circuits may reorganize following spinal

cord transaction and functionally compensate for the missing inputs (Weber & Stelzner,

1977). Reorganization may be accomplished by sprouting of dorsal roots or intact

intraspinal fiber systems of the caudal spinal cord (see Stelzner & Cullen, 1991).

The importance of spinal motor circuits in the recovery of hindlimb function

following injury to the midthoracic spinal cord is further illustrated by the finding that

locomotor function of infant rats with SCIs deteriorates on tasks that test the functional

efficacy of descending motor circuits (McEwen & Stehouwer, 1998b). L-DOPA-induced

air-stepping has been utilized to study locomotor development in newborn rats because

postural demands are eliminated and locomotor development can be studied in vivo.

Briefly, neonatal rats were suspended in harnesses to eliminate postural demands and








administered L-DOPA (sc) to activate locomotor circuits. Under those conditions, L-

DOPA reliably induces coordinated air-stepping of all four limbs of 5- to 20-day-old

intact rats (McCrea, Stehouwer, & Van Hartesveldt, 1994; Stehouwer, McCrea, & Van

Hartesveldt, 1994; Van Hartesveldt et al., 1991). Following midthoracic spinal cord

transaction, hindlimb air-stepping is virtually eliminated (Iwahara, Van Hartesveldt,

Garcia-Rill, & Skinner, 1991; McEwen, Van Hartesveldt, & Stehouwer, 1997), unless

excitatory input to lumbar motor circuits is augmented (Arnaiz, Stehouwer, & Van

Hartesveldt, 1997; McEwen et al., 1997). Therefore, L-DOPA-induced air-stepping may

provide a test of the functional efficacy of descending catecholaminergic, and possibly

serotonergic (Commissiong & Sedgwick, 1979; but see Goldstein & Frenkel, 1971;

Hollister, Breese, & Mueller, 1979), systems following SCI. Although rats recover good

overground walking following transaction of the immature spinal cord (Stelzner et al.,

1975; Weber & Stelzner, 1977), kinematic analyses of limb movements during L-DOPA-

induced air-stepping reveal persistent deficits and progressive loss of locomotor function

of infant rats in which the spinal cord was compressed by 95% of the uncompressed

width (McEwen & Stehouwer, 1998b). Greater reorganization of lumbar spinal circuits

and activation of peripherally driven reflex mechanisms may explain greater recovery of

hindlimb function in rats of the present experiments that received such an injury as

neonates than as young-adults. This is not to say that there is no reorganization by spinal

circuits of the mature system. Rats of the oldest age group in the present experiments

that received the greater compression recovered some hindlimb function during the

postoperative period, despite presumed elimination of descending and ascending fibers at

the lesion epicenter.









However, hindlimb sensorimotor function postinjury depends, not only on the

extent and distribution of spared systems, but also on the functional integrity of those

systems. Axons that survive an injury lose their myelin sheath (Blight, 1983), which

decreases conduction velocity or causes nerve conduction block (Young, 1989). Thus,

demyelinated systems that survive the injury would contribute little to behavioral sparing

or recovery postinjury. Because demyelination and spontaneous remyelination are slow

processes that occur for a year following weight-drop injury to the adult rat spinal cord

(Salgado-Ceballos, Guizar-Sahagun, Feria-Velasco, Grijalva, Espitia, Ibarra, & Madrazo,

1998), functional recovery during the 4-week postoperative period of the present

experiments was probably not due to remyelination of surviving fiber systems. Although

lesion lengths were not quantified in the present experiments, lesions did not extend more

than two segments rostral to, or caudal from, the lesion epicenter. Hindlimb rhythm-

generating circuits are located within the caudal thoracic and lumbar segments of the

spinal cord (Cowley & Schmidt, 1997; Kjaerulff& Kiehn, 1996; Kremer & Lev-Tov,

1997; but see Cazalets, Borde, & Clarac, 1995), but the entire extent of the lesions did not

extend beyond the midthoracic cord and probably did not impinge directly on hindlimb

motor circuits. However, there is evidence to suggest transsynaptic degeneration of

motoneurons caudal to a spinal cord lesion in adults (Eidelberg, Nguyen, Polich, &

Walden, 1989; but see Bjugn, Nyengaard, & Rosland, 1997), which could indirectly alter

rhythm-generating circuits and impair hindlimb sensorimotor function.

In contrast to the age-related decrease in recovery of function following spinal

cord transaction (Stelzner et al., 1975; Weber & Stelzner, 1977), hindlimb sensorimotor

function was not dramatically reduced between rats of the present experiments that









received the compression on PND 5 or 15. Because spinal cords of rats of the present

experiments were not completely severed, ascending, descending, and propriospinal

systems that survived the injury remained to contribute to hindlimb sensorimotor

function. In adult animals, survival of only 5-10% of spinal cord axons sustain hindlimb

function following compressive (e.g., Eidelberg, Straehley, Erspamer, & Watkins, 1977)

or contusive (e.g., Blight, 1983) injury to the spinal cord. Descending and propriospinal

systems that survived compression of the midthoracic spinal cord on PND 15 probably

maintained excitability of lumbar motor circuits above some threshold value and

prevented the dramatic reduction in hindlimb sensorimotor function observed following

complete transaction of the spinal cord.


Sensorimotor Recovery Postinjury is Task-Dependent


In general, hindlimb sensorimotor function was better following compression of

the developing spinal cord than following compression of the mature spinal cord.

However, the severity of the injury "changes" with the behavioral or neuroanatomical

measure. Ratings of overground walking are typically used to assess locomotor function

following injury to the spinal cord of adult animals. However, rating scales are

subjective and overground walking does not challenge hindlimb function postinjury. In

the present experiments, rats that received the lesser compression on PND 60 and rats

that received the greater compression on PND 5, 15, or 60 performed considerably better

during overground walking than during walking across the elevated beams or parallel

bars. Those findings suggest that ratings ofoverground walking do not accurately depict

the severity of hindlimb sensorimotor dysfunction postinjury. In addition to contributions









by specific neural systems, differential denervation and reinnervation ofhindlimb

muscles or their motorneurons may also explain the task-dependent performances

postinjury. Severe compression of the spinal cord transiently causes muscle atrophy in

rats (Mayer, Burke, Toop, Walmsley, & Hodgson, 1984), which would result in hindlimb

motor paresis. Therefore, tasks which may require greater hindlimb muscle strength for

successful completion, such as walking across the inclined beams and parallel bars, or

maintaining position and balance on the inclined plane, may reveal hindlimb

sensorimotor impairments that are not evident during less challenging tasks, such as

overground walking. Anterior horn cells that supply proximal muscles are located

ventromedially, whereas those innervating distal muscles are located dorsolaterally

(Romanes, 1951; Sharrard, 1955). The spatial distribution of motoneurons that innervate

proximal and distal muscles would presumably result in differential denervation of those

muscles following spinal cord compression. Humans generally recover use of proximal

muscles before distal muscles following SCI (see Ditunno, Graziani, & Tessler, 1997),

which may be explained by differential sprouting and reinnervation of motoneurons by

descending, propriospinal, or segmental systems that survive the injury. If reinnervation

of proximal muscles (see Nakamura, Fujimura, Yato, & Watanabe, 1996) or of

motoneurons that supplied proximal muscles occurred sooner or to a greater extent than

reinnervation of distal muscles or the motoneurons that supplied distal muscles in rats of

the present experiments, recovery of gross motor skills (e.g., overground walking) may

occur before fine motor control (e.g., beam walking).

Although recovery of locomotor function following SCI depends on

neuroanatomical and neurophysiological changes in the nervous system, postoperative








recovery may also depend on behavioral compensation (see Goldberger, Bregman,

Vierck, & Brown, 1990). Rats are quadrupedal animals and could redistribute their body

weight onto the uninjured forelimbs to compensate for hindlimb motor paresis following

midthoracic SCI. In the present experiments, rats may have redistributed their body

weight to the forelimbs during overground walking, but not during tasks that challenged

hindlimb sensorimotor functioning postinjury. Redistribution of body weight following

midthoracic SCI could be examined by having the animals stand on force plates or walk

across a gait mat. Postural adjustments postinjury may also be identified with kinematic

analyses of joint movement.

Apparent improvements in hindlimb sensorimotor function postinjury may also be

an effect of practice. Following complete isolation from descending circuits, the spinal

cord of adult cats can be trained to bear full weight support and to generate reciprocal

steps on a treadmill (Lovely et al., 1986). Thus, spinal motor circuits do not merely carry

out commands from descending motor circuits, but can learn a motor task. The

information used by the spinal cord is task specific because cats trained to stand do not

walk on a treadmill and cats trained to walk on a treadmill do not stand for long periods

of time (Hodgson et al., 1994). Human infants given daily step training also step more

during testing than infants given daily sit training, but do not sit as long as infants trained

to sit (Zelazo, Zelazo, Cohen, & Zelazo, 1993). Similar training procedures have

improved the locomotor gait of human patients with incomplete SCIs (e.g., Barbeau &

Rossignol, 1994; Dietz, Wirz, Curt, & Colombo, 1998; Fung, Stewart, & Barbeau, 1990).

Because the spinal cord was not completely transected in rats of the present experiments,

supraspinal and spinal systems could participate in motor learning and lead to gradual








improvements in motor function with repeated testing during the 4-week postoperative

period. The rats were free to walk around their home cages between test sessions, so

better performance during overground walking than during beam walking may be

explained by "practice". The effects of practice may also explain the decrease in the

percentage ofhindlimb slips during beam walking between the first two beam sessions

(regardless of POD) in rats of all age and surgery groups that traversed the beams,

because beam walking improved despite continued weight gain of the rats and no further

improvements in overground walking. Furthermore, there was no decrement in the

degree of incline on which the rats maintained balance and position on the inclined plane

during the postoperative period, despite continued weight gain by the rats. The inclined

plane task has been criticized as a test of undamaged (forelimb) systems (Steeves &

Tetzlaff, 1998). In order to maintain position and balance on the inclined plane, the rats

must redistribute their weight and shift their center of gravity as the incline is raised.

Therefore, the test may provide a better assessment of forelimb muscle strength than

hindlimb strength or balance. It seems unlikely that the weekly test sessions in the

present experiments significantly increased muscle strength to account for maintained

performance, despite the dramatic increase in body weight. Instead, it seems more

plausible that rats learned to redistribute their weight during successive tests in which the

plane was gradually raised. However, it is noteworthy that the inclined plane used in the

present experiments was not covered by a rubber mat (see Rivlin & Tator, 1977), but was

modified to have a smooth surface. Therefore, the inclined plane of the present

experiments may have provided a more difficult test for sensorimotor deficits postinjury

than previous reports because there was nothing for rats to grasp and hold onto during








testing. Because the quality of hindlimb function postinjury varied with the task in the

present experiments, numerous tests should be used to fully characterize recovery of

hindlimb sensorimotor function postinjury.


Methodological Considerations


Results of the present experiments show an age-related decline in sensorimotor

function following midthoracic spinal cord compression, which may be due to age-related

changes in neuroanatomical, neurophysiological, or behavioral compensatory

mechanisms during recovery. However, procedures of the present experiments may have

differentially affected locomotor recovery of rats of the three age groups from the outset.

Neurologic outcome following slow compression of the adult spinal cord depends on the

amount (Gruner et al., 1996), speed (Tarlov et al., 1953), and duration (Tarlov et al.,

1953) of the compression. Because the size of the spinal cord increased during ontogeny,

spinal cords of rats of the present experiments were compressed by a percentage of the

uncompressed width of the spinal cord. Increasing the amount of compression increased

severity of dysfunction. Mechanical properties of the spinal cord or its response to injury

may change during ontogeny and contribute to the age-related changes in tissue survival

and neurologic outcome. For example, water content of the infant rat brain is high and

decreases during postnatal life (Himwich, 1962) and membrane elasticity of dorsal root

ganglion neurons decreases during ontogeny in mice (Horie et al., 1990). Although the

amount and duration of compression were controlled across experimental groups of the

present experiments, viscoelastic properties of the spinal cord tissue may alter the amount

ofintraspinal pressure during compression and contribute to the age-related changes in






88
tissue survival postinjury. In addition, 5-day-old rats were anesthetized by hypothermia,

which is neuroprotective to central tissue of the adult and newborn (e.g., Hansebout,

Kuchner, & Romero-Sierra, 1975; Ikonomidou, Mosinger, & Olney, 1989; Kuchner,

Mercer, Pappius, & Hansebout, 1976). Hypothermia may have minimized tissue

degeneration postinjury by stabilizing cell membranes and suppressing destructive

metabolic mechanisms (see Janssen & Hansebout, 1989). Furthermore, the incision site

of rats of all age and injury groups was irrigated with saline, which may have reduced

secondary degeneration by diluting extracellular Ca" and other ions known to exacerbate

secondary injury to nervous tissue (see Faden, 1997; Sabel, Labbe, & Stein, 1985). That

procedure was performed on rats of all age and injury groups, so an age-dependent effect

on behavioral recovery is not likely.

The biochemical cascade that follows traumatic injury to the mature spinal cord

and leads to secondary neural degeneration is well known. Those events include

elevations in excitatory amino acids and other neurotransmitters, inflammatory and

immune responses, production of free radicals, Ca2 and Na' influx, gliosis, and

reductions in blood flow, glucose utilization, and oxygen utilization (see Faden, 1996;

Janssen & Hansebout, 1989). Although the biochemical changes that follow traumatic

injury to the developing spinal cord have not been elucidated, the cascade of biochemical

events that follows ischemic injury to the developing brain is similar to the cascade of

biochemical events that follows injury to the adult spinal cord (see Berger & Gamier,

1999; Giacoia, 1993). However, age-related changes in the magnitude of the release of

various substances or the spinal cord reaction to those biochemical events probably exist.

For example, Yager et al. (1996) reported significantly greater total brain damage in 1-








week, 3-week, and adult rats, than in rats of intermediate ages (6- and 9-week-olds)

following a hypoxic-ischemic brain insult. In addition, injection of the excitatory amino

acid, NMDA, into the striatum produced greater damage in 7-day-old and 3-month-old

rats than in adults (McDonald, Silverstein, & Johnston, 1988; also see Ikonomidou,

Mosinger, & Salles, 1989). In the adult spinal cord, NMDA receptors are restricted to the

substantial gelatinosa, whereas NMDA receptors are distributed throughout the spinal

cord gray matter during early postnatal development. The level of NMDA receptor

binding increased between birth and approximately PND 8 (Gonzalez et al., 1993), but

then decreased in all areas of the spinal cord, except the substantial gelatinosa, until PND

28 (Kalb et al., 1992). Thus, massive efflux of excitatory amino acids from damaged

neurons following traumatic SCI (e.g., Faden, 1996) may have greater adverse effects on

tissue survival in the developing spinal cord because of the elevated levels of receptor

binding sites. Because the reaction of the neonatal nervous system to injury is not the

same as in adults, postinjury treatments designed for adults may not have the same

therapeutic efficacy for infants. Development of effective treatments for injury to the

developing spinal cord is dependent on the elucidation of the biochemical and

neuroanatomical events that follow traumatic SCI.


Concluding Remarks and Implications


Limited evidence suggests good recovery of ambulation following injury to the

spinal cord of human infants. One infant diagnosed with spastic quadriplegia following

injury to the cervical spinal cord at 9 weeks of age eventually gained some ability to

walk, crawl, and manipulate toys. Morphology of the cervical spinal cord also returned






90
to near-normal several months postinjury (Thomas, Robinson, Evans, & Bullock, 1995).

Another infant sustained a complete fracture-dislocation of the lumbar cord, which

resulted in flaccid paralysis of the lower extremities. However, 12 months later, she

regained strength in all lower extremity muscles and walked with orthotic aids (Gabos,

Tuten, Leet, & Stanton, 1998). Because injury to the human infant spinal cord is less

common than in adults, there is danger of misdiagnosis by physicians (see Dickman,

Rekate, Sonntag, & Zabramski, 1989; Hesketh, Eden, Gattamaneni, Campbell, Jenney, &

Lashford, 1998; Rossitch & Oakes, 1992). Therefore, behavioral diagnostics of injury to

the developing spinal cord are needed.

Further investigations into the effects of pediatric SCI are important because

injury to the developing nervous system may result in unique behavioral alterations, not

observed following injury to the mature spinal cord. Following complete crush of the

spinal cord of neonatal opossum, spinal cord morphology was near-normal and the

animals recovered good use of the hindlimbs, as well as coordination between limb

girdles. However, the abnormally high hindlimb stepping that was apparent at weaning

was exaggerated in adulthood and impeded grid walking and climbing (Saunders, Deal,

Knott, Varga, & Nicholls, 1995). Placing responses of kittens were hypermetric and slow

following partial hemisection of the spinal cord and never completely matured (Bregman

& Goldberger, 1982). In the present experiments, comparatively short latencies to

withdraw one hindpaw from the hotplate surface on POD 7 by rats that received the

greater compression on PND 5 reflects the removal of descending inhibitory systems and

supersensitivity of hindlimb sensorimotor circuits to the thermal/noxious stimulus.

Furthermore, rats that received the greater compression on PND 5 stood with ventrum








unusually high off of the table surface following episodes of righting on POD 7.

Although overground walking of those rats was rated as similar to sham controls by the

end of the postoperative period, those rats continued to walk with the ventrum held

higher off of the table surface than sham controls. Such behavioral changes postinjury

must be considered in the design of rehabilitative strategies following injury in infancy.

Pediatric SCI may also change how the nervous system is constructed.

Motoneuron dendrite bundles develop postnatally in kittens and their maturation parallels

the emergence of mature stepping, walking, and weight-bearing (Scheibel & Scheibel,

1970). However, motoneuron dendrite bundles do not mature following spinal cord

transaction (Reback, Scheibel, & Smith, 1982). Transection of the midthoracic spinal

cord of kittens alters the biochemical, histochemical, and contractile properties of the

hindlimb muscles (Johnson, Smith, Eldred, & Edgerton, 1982). Although spinal cord

transaction causes muscle spasticity in both kittens and cats, kittens are more prone to

develop skeletoarticular disorders following SCI than are cats (see Smith, Smith,

Zernicke, & Hoy, 1982). Furthermore, supraspinal systems are required for postnatal

fine-tuning of spinal nociceptive systems, which is altered following damage to the

developing spinal cord (Levinsson, Luo, Holmberg, & Schouenborg, 1999). Because the

consequences of such changes are not completely understood, greater understanding of

the behavioral, neuroanatomical, and neurophysiological effects of injury to the

developing spinal cord is required.













APPENDIX A
BASSO, BEATTIE, AND BRESNAHAN (BBB) LOCOMOTOR RECOVERY SCALE


0 No observable HL movement
1 Slight movement of one or two joints, usually the hip and/or knee
2 Extensive movement of one joint or extensive movement of one joint and slight
movement of one other joint
3 Extensive movement of two joints
4 Slight movement of all three joints of the HL
5 Slight movement of two joints and extensive movement of the third
6 Extensive movement of two joints and slight movement of the third
7 Extensive movement of all three joints of the HL
8 Sweeping with no weight support or plantar placement of the paw with no weight
support
9 Plantar placement of the paw with weight support in stance only (i.e., when
stationary) or occasional, frequent or consistent weight-supported dorsal stepping
and no plantar stepping
10 Occasional weight-supported plantar steps; no FL-HL coordination
11 Frequent to consistent weight-supported plantar steps and no FL-HL coordination
12 Frequent to consistent weight-supported plantar steps and occasional FL-HL
coordination
13 Frequent to consistent weight-supported plantar steps and frequent FL-HL
coordination
14 Consistent weight-supported plantar steps, consistent FL-HL coordination and
predominant paw position during locomotion is rotated (internally or externally)
when it makes initial contact with the surface as well as just before it is lifted off at
the end of stance; or frequent plantar stepping, consistent FL-HL coordination and
occasional dorsal stepping
15 Consistent plantar stepping and consistent FL-HL coordination and no toe clearance
or occasional toe clearance during forward limb advancement; predominant paw
position is parallel to the body at initial contact
16 Consistent plantar stepping and consistent FL-HL coordination during gait and toe
clearance occurs frequently during forward limb advancement; predominant paw
position is parallel at initial contact and rotated at lift off
17 Consistent plantar stepping and consistent FL-HL coordination during gait and toe
clearance occurs frequently during forward limb advancement; predominant paw
position is parallel at initial contact and lift off
18 Consistent plantar stepping and consistent FL-HL coordination during gait and toe
clearance occurs consistently during forward limb advancement; predominant paw
position is parallel at initial contact and rotated at lift off







93

19 Consistent plantar stepping and consistent FL-HL coordination during gait, toe
clearance occurs consistently during forward limb advancement, predominant paw
position is parallel at initial contact andlift off and tail is down part or all of the
time
20 Consistent plantar stepping and consistent coordinated gait, consistent toe
clearance, predominant paw position is parallel at initial contact and lift off and
trunk instability; tail consistently up
21 Consistent plantar stepping and coordinated gait, consistent toe clearance,
predominant paw position is parallel throughout stance, and consistent trunk
stability; tail consistently up




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