Recovery of locomotion after chronic spinalization in the adult cat

84

Brain Resear:h, 412 (1987) 84-95 Elsevier

BRE 12584

Recovery of locomotion after chronic spinalization in the adult cat* H. Barbeau** and S. Rossignol Centre de Recherche en Sciences Neurologiques, DOpartementde Physiologie, FacultOde MOdecine, UniversitO de MontrOal, Montreal, Que. (Canada) (Accepted 14 October 1986) Key words: Spinal cat; Locomotion; Training; Kinematics; Electromyogram (EMG)

Cats were spinalized (Tl3) as adults and were trained to walk with the hindlimbs on a treadmill. After 3 weeks to 3 months and up to 1 year depending on the animal, all were capable of walking on the plantar surface of the feet and support the weight of the hindquarters. Interactive training appeared to accelerate the recovery of locomotion and maintain smooth locomotor movements. Despite the obvious loss of voluntary control and equilibrium which the experimenter partially compensated for by maintainingthe thorax and/or the tail, the cats could walk with a regular rhythm and a well-coordinated hindlimb alternation at speeds of 0.1-1.2 m/s. Cycle duration as well as stance and swing duration resembled those of normal cats at comparable speeds. The range of angular motion was also similar to that observed in intact cats as was the coupling between different joints. The EMG activity of the hindlimb and lumbar axial muscles also retained the characteristics observed in the intact animal. Some deficits such as a dragging of the foot in early swing and diminution of the angular excursion in the knee were seen at later stages. Thus, the adult spinal cat preparation is considered as a useful model to study the influence of different types of training and of different drugs or other treatments in the process of locomotor recovery after injury to the spinal cord.

INTRODUCTION Following a complete transection (T10-T12) of the spinal cord at 1 - 2 weeks of age, kittens can walk on a treadmill without requiring any particular training 6,14:9. The locomotor kinematics is well adapted to the speed of the treadmill and the electromyograms ( E M G s ) of muscles acting at different joints are similar to those of the intact cat, both with respect to timing and shape. The animals also develop enough force to support the weight of the hindquarters 6. The coordination between the hindlimbs is strictly out-of-phase as during walk or trot in intact animals or can be in-phase as seen in gallop. Furthermore, these animals are capable of adapting the locomotor patterns to different d e m a n d s such as walking with the two hindlimbs at different speeds thus mim-

icking conditions found when turning7. Finally, these animals showed well-adapted and well-organized reflex responses to cutaneous inputs or perturbations of the step cycle s . In contrast, Eidelberg et al. z reported that after spinal transection at T 6 - T s, adult cats did not walk as well as kittens. Indeed, even 8 weeks after spinalization, the adult cats were incapable of supporting their hindquarters and showed transient support only with pinching of the skin at the base of the tail. There was a lack of coordination between the hindlimbs and a marked variability in the duration of the hindlimb step cycles: the mean value of the cycles for a given speed was the same but the standard deviation was 5 - 1 0 times greater than in the prespinalization period. The knee and ankle m o v e m e n t s could be uncoupled and the feet often dragged forward on the

* Preliminary results have been reported elsewhere 15'16. ** Present address: School of Physical and Occupational Therapy, Faculty of Medicine, McGill University, Montr6al, Qu6. Canada. Correspondence: S. Rossignol, Centre de Recherche en Sciences Neurologiques, Facultd de M6decine, Universit6 de Montrdal, C.P. 6128, Succursale A, Montreal, Qud. H3C 3J7 Canada. 0006-8993/87/$03.50~ 1987 Elsevier Science Publishers B.V. (Biomedical Division)

85 belt during swing until lift-off late in swing. According to this study, such locomotor performance did not improve with daily testing. The results of this study were largely supported by a more recent report by Robinson and Goldberger TM. In another study, Smith et al. 19 compared the locomotor capabilities of kittens spinalized at 2 and 12 weeks both with and without exercising. The locomotor performance of both exercised and non-exercised groups of 2-week-old kittens rated better on the average than that of the 12-week-old kittens. In this later group, the 4 non-exercised cats only had periodic weight support and dragged their hindpaws on the belt. In the exercised group, 2 out of 5 demonstrated weight bearing during stance, a plantar digitigrade paw contact, a proper range of angular motion and were capable of walking at speeds up to 1.0 m/s. This suggested an improvement of the locomotor performance with training (see also ref. 9). However, this study indicates that the animals cordotomized at 12 weeks of age showed poor weight support up to about 2 months and that cats which supported their weight did so only in the third month. No detailed evaluation of this recovery period is given for these animals. Finally, defects in locomotor performance were described such as an absence of yield during stance and an uncoupling of the ankle and knee joints. The present study was designed to document in some details the recovery of locomotion after spinalization in adult cats from the first day post-spinalization up to the moment of weight support and plantar digitigrade walking and also to analyze E M G and kinematic characteristics of the step cycle when the animals reached a stable state. This study was needed, on the one hand, to evaluate the benefits of regular interactive locomotor training and, on the other hand, to provide a base line for other studies using chemical agents or other interventions that may influence the recovery process and the locomotor performance after spinalization in adults. MATERIALS AND METHODS

General procedures A complete spinal transection at Tl2-Ti3 was perforrred in 6 adult male cats weighing 3.6-4.5 kg in sterile conditions under sodium pentobarbital (35

mg/kg) anesthesia. The spinal cord was exposed by a laminectomy of one vertebra and part of a spinal segment was removed without sparing the ventral artery. The completeness of the section was verified with an operating microscope. A piece of absorbable gelatin sponge (Gelfoam) was placed between the rostral and caudal portions of the divided spinal cord. The transection was also verified postmortem by histological examination of longitudinal sections of the cord stained with the Klfiver-Barrera method. Only one or two cats were kept at the same time and they were housed in individual cages and inspected daily. The bladder was emptied with a catheter for the first week and then manually once or twice a day thereafter. The survival time of the 6 cats which participated in this study varied from 2 to 52 weeks following the transection. Detailed results from 3 cats (B, 52 weeks; E, 32 weeks; and F, 25 weeks) were specifically used for the present study while only partial results were utilized from the 3 other cats (A, 2 weeks; C, 8 weeks; and D, 6 weeks).

Training procedure Following spinalization, all cats were trained on the treadmill 2 to 3 times per week for at least half an hour. These training sessions were over and above the experiments during which the animal walked sometimes for more than an hour. During these training or experimental sessions, one animal (cat B) was fitted with an adjustable soft leather jacket which covered the thorax as well as the base of the neck and forelimbs. The jacket was well tolerated and was used as an aid to partially offset the equilibrium deficit by maintaining lateral stability while the animal walked with the hindlimbs and the two forelimbs rested on a stationary platform above the belt. In cats E and F, this jacket was not used. Due to an increased adductor tonus, a separator was placed between the limbs to prevent the hindlimbs from impeding each other. In the first few weeks after spinalization, manual stimulation of the perineal region and the base of the tail was used to induce locomotion or increase the amplitude of the steps while weight support was provided by the experimenter who held the tail. In each session, the animal was led to progressively support more weight at different treadmill speeds. This was achieved by a continual interaction between the animal and the experimenter who deter-

86 mined how much weight the animal could support in any particular experimental session. This method was considered better than mechanical holding devices such as belts put around the abdomen 4 or the groin since these are not easily adapted to the particular evolving capabilities of the animal, session after session, and can also interact with walking by providing abnormal cutaneous inputs from the inguinal region.

EMG recording and analysis In each session, electromyograms (EMGs) were recorded with pairs of copper wires, insulated except for the tips, which were inserted percutaneously with 21-gauge needles into the belly of different muscles. The E M G signals were differentially amplified (Grass model 7P511 preamplifiers) using a 300 H z - 1 0 kHz bandwidth and recorded on a 14-channel Honeywell FM tape recorder with a frequency response of 2500 Hz. A frame-oriented digital time code was recorded simultaneously on the magnetic tape and the video tape to allow synchronization of the EMGs and the video images by a computer. The recorded E M G data were played back on an electrostatic polygraph (Gould, Model ES 1000). Selected portions of the recordings were digitized at 1 kHz on a PDP 11/34 computer and displayed on a Tektronix 4010 terminal. The method for automatically detecting the onset and offset of E M G bursts and establish timing relationships has been reported elsewhere 21. The EMGs were first integrated by the computer and then represented as series of dots (raster displays) whose density is proportional to the amplitude of the signal (cf. Fig. 1B). In some displays, each channel was also averaged to display the overall time relationships between events as well as their amplitude (cf. Fig. 6C). For the rasters and the averages, the cycles are normalized from 0 to 1. The same display is again repeated from 1 to 2 so as to clearly illustrate those events which occur near the onset of the cycle. In Figs. 1B and 6B, C, the real time scale under the abscissa is derived from the mean cycle time and provides only an approximation of real time values.

Movement recording and analysis Five light reflective targets were fixed to the skin over the ischium, the femoral head, the knee joint, the lateral malleolus and the tarsometatarsal joint. A

shutter video camera with an exposure time o f 2 ms was used for video recordings so that displacements in the sagittal plane could be reconstructed and displayed in the form of stick diagrams (Fig. 5C) or angular displacements of each joint (Fig. 5A, B). Each of the two fields composing a video frame could be used for analysis, thus giving a temporal resolution of 16.7 ms. The X and Y coordinates of the light-reflecting spots were measured directly from the screen of a video monitor with a specially designed cursor arrangement. The onset of stance and swing was measured from successive foot contacts and lifts with an accuracy of + 1 field. The stance length represents the distance travelled by the foot during the period of its contact with the belt. The stance duration is defined as the period of contact of the paw with the belt. To insure that the cats actually followed the treadmill speed when it was held by the tail during the recovery period, the average speed at which the foot travelled while in contact with the belt was measured from the video recordings and compared to the imposed treadmill speed. Sequences in which the limb waited at the end or at the beginning of stance at either very low or very high speeds were then discarded. RESULTS The results are subdivided in two broad sections. The first one deals with the recovery of locomotion and describes the changes in E M G and gait parameters as a function of time after spinalization as well as the adaptation to speed. The second section describes the E M G and gait parameters at the plateau period when the animal has attained a level of stable locomotor performance.

Locomotion during the recovery period An overview. Within 24-48 h of the spinalization, strong pinching of the perineal or abdominal regions could induce a bilateral extension of the hindlimbs upon which brief periods of coordinated stepping (in the air or on the treadmill) were superimposed. In the following 3 weeks, such episodes of air stepping became easier to elicit, with very light pinching, or even tactile stimuli of the same regions. During that period, the animals were also trained to walk on the treadmill. The animals made small stepping movements on the belt, although they generally

87 ers had to be repositioned. In their cages, the animals dragged their hindquarters around, with the knee and ankle in extension and the hip in flexion. Sometimes, the animals could be seen to stand on all fours in their cages. Because of the heavy training and experimental schedule, no more than two spinal cats were kept at the same time. In some periods it was impossible to maintain a schedule of daily training. The minimal training during such periods was not always sufficient to maintain the animal's performance• In those instances, the performance regressed to an earlier stage characterized by shorter steps, unsteady foot placement and inability to support the weight. Gen-

placed their feet on the tip of the toes or the dorsum and could not sustain their weight. Towards the third week, the sole of the foot was occasionally placed properly for a few step cycles usually with some stimulation of the perineum but at times without it. Over the next week in two cats and 2 months in one, there was a marked improvement in the locomotor performance; the steps became larger and there was a bilateral placement of the plantar surface of the foot on the belt. This coincided with the ability of the animals to support the weight of the hindquarters. Such full weight support during walking generally lasted from a minimum of 2-3 min to more than 10 min after which time the animal lost balance and the hindquart0.2 m . s -~ 14 DAYS AFTER S P I N A L I S A T I O N

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88 erally, the locomotor performance could be completely re-established within a few days with intensive training. The following two sections will illustrate firstly, how the E M G and kinematic gait parameters recorded at the same speed (0.2 m/s) change as a function of time after spinalization and secondly, how these parameters adapt to speed. EMG and kinematic gait parameters. The general characteristics of E M G and gait parameters are illustrated in Fig. 1 taken from walking sequences at 0.2 m/s on 3 different days after spinalization. Fig. 1A shows the raw E M G activity of the knee extensor (vastus lateralis, VL) and the knee flexor and hip extensor (semitendinosus, St) on both sides of the body as well as the corresponding rasters (Fig. 1B). Analyses of video sequences in Fig. 1C show the duration of stance and swing on both sides for several consecutive steps on the same days. At day 14, the cat (animal B) could step on the treadmill provided that the perineum was pinched. The feet were placed on the tip of the toes or sometimes on the dorsum and the animal could not support its weight. The two hindlimbs generally had a good coordination (see Fig. 1C). This was evaluated by measuring the phase of onset of St in one limb in relation to the onset of St in the other limb. These phase values ranged from 0.37 to 0.64 (mean of 0.49) with coefficients of variation (c.v.) ranging from 10.6 to 35.9% (mean of 21.1%). There were some asymmetries between the two sides manifested as differences in amplitude and/or duration, for instance, of VLs. There were also some irregularities as seen in the variation of amplitude and duration of successive VL bursts on any one side. At day 84, the same cat walked on the sole of the feet and supported its weight completely. With the treadmill set again at 0.2 m/s the step cycles were much longer. Asymmetries and irregularities were present but somewhat less pronounced than at 14 days. The phase value for the coordination between the hindlimbs averaged 0.53 while the c.v. dropped from an average of 21.0% in the previous period to 10.0%, indicating a much stabler coordination between the hindlimbs. Note, in the raw E M G s and the corresponding raster, that the interval between the onset of St and that of VL which corresponds grossly to the swing period (see bottom panel) is longer than

at 14 days. The main St burst remains largely the same, but there is now a second much smaller and inconsistent burst in St occurring at about the onset of VL. This second St burst is not seen before the animal can support its weight. At 308 days, the pattern is quite stable and the coordination is at 0,53 with a c.v. of 9.6%. Note that the extensor EMG bursts on both sides were often asymmetric due to the fact that the cat usually leaned more on one side, in this case the ipsilateral side. The changes in the duration of the step cycles and that of the VL and St bursts as a function of time after spinalization of animal B are shown for one speed (0.2 m/s) in Fig. 2A. Up to about 9(1 days, there is a progressive increase in the step cycle duration as well as in the overall duration of the extensor VL. Measurements taken in the period corresponding to day 14 to day 82 indicated a progressive lengthening of the cycle from 682 + 60.7 to 959 _+ 132 ms at 82 days. The c.v. ranged from 6.1 to 13.7% (mean of 9.5%). Thereafter, depending on days, the c.v. of cycle duration varied from 4.2 to 10.1% with a mean of7.4f4. The increase in the cycle duration is due to an increase in the duration of extensor muscle activity (see curve of VL in Fig. 2A) as well as to a lengthening of the period between the onset of the main St burst and the onset of the VL burst (as mentioned before). The duration of the first St burst remains approximately constant throughout (see Fig. 2A) although it tends to get shorter at about 6 months (see also Fig. 1A), which might correspond also to an observed decrease in the overall excursion of the knee joint at that time (not illustrated). Fig. 2B compares, in 3 cats (B, E and F), the changes in step cycle duration measured at one speed (0.2 m/s) at different times after spinalization. The arrows indicate the day on which each cat was capable of plantar digitigrade walking: tn those 3 animals, the cycle duration continued to increase until the end of the third month after spinalization even if the digitigrade walking started at the end of the first month (cats E and F). Fig. 2C shows the stance length (see Methods) of the 3 adult spinal cats (B, E and F) at different days following spinalization. The stance length of cat B increased from 8.0 + 2.0 cm at day 14 to 13.8 _+ 0.8 cm at day 308 for the same speed of 0.2 m/s. The stance length of cats E and F also increased with time and

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intensive training, the cat was able to support its own weight and the stance length increased dramatically for the same speed (see isolated symbol at the upper left). Speed adaptation, Fig. 3A illustrates the relationship between both the duration of the step cycle and the duration of the extensor and flexor activity, with the speed of the treadmill at two different days (14 and 84 days) after spinalization. On the 14th day (dashed lines), as the treadmill speed was increased, the duration of the step cycle shortened. The reduction of the cycle was principally due to a decrease of the VL duration while the St duration remained approximately constant. At day 84, there was an upward shift of the step cycle and the VL duration at all speeds investigated corresponding to the previously mentioned lengthening of the step cycles (see Fig. 2A). The St duration at all speeds was relatively constant and was similar to that found at 14 days. Fig. 3B plots, for cat B, these changes in the step cycle duration as a function of speed (0.2-1.2 m/s) and several days, ranging from 12 to 308 days after spinalization. Throughout the recovery period (curves 12-69 included), the step cycle duration and the speed relationship showed a progressive upward shift until it reached a plateau at around 3 months post-transection (82 days). It can also be noted that the cat could follow treadmill speeds of 1.2 m/s during the plateau period, whereas it only occasionally reached 1.0 m/s during the recovery (see Methods). For each speed and for each day, the c.v. of the step cycles were calculated. It was observed that the overall stability of the walking pattern was better at speeds of 0.4-0.8 m/s. At low speeds (0.1-0.2 m/s), the phase coupling between the hindlimbs, although near 0.5 could vary greatly with the c.v. in the order of 30% and above. At higher speeds (0.4-0,8 m/s), the c.v. would drop sharply to 5 - 1 0 % indicating a good coordination between the limbs.

Locomotion at the plateau period Gait parameters at different speeds. Fig. 4A illusstabilized with a similar pattern. For cat E, measurements of the stance length were taken a few days apart. On day 27, the cat was held by the tail and the stance length value is indicated by the symbol connected to the main curve for cat E. On day 29, after

trates the stance and the swing duration as a function of the treadmill speed for cat E at the plateau period while the cat walked with weight support. Fig. 4B represents, for the same animal, the changes in stance length with increasing treadmill speed. It is

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91 in the order of 35 ° , the knee 55 ° and the ankle 60 ° (see also Fig. 4C). From the duty cycle in Fig. 5A it can be seen that all joints start flexing slightly before foot lift-off. The hip leads the other joints and flexes throughout swing; the knee somewhat leads the ankle and attains its peak flexion before the ankle. After foot contact, there is generally only a small yield particularly in the ankle (see oblique arrow in Fig. 5A). Measurements of the knee angle are inaccurate due to the skin slippage over the joint and therefore the yield is difficult to define in that joint. This yield is notably small in this range of slow speeds. Fig. 5A and B also represent the muscular activity of the ipsilateral and contralateral knee flexors (St) and knee extensors (VL) in cat E in relation to joint angles of the ipsilateral side. The ipsilateral St burst starts at the onset of knee flexion and sometimes after it and is present in the first half of the flexion period. The onset of the knee extensor activity (VL) occurred during the last part of E1 (see indications in the duty graph) and continued at a maximum level until the end of E3, when it stopped abruptly. In some experiments (cat B) the VL activity had two consecutive peaks. In Fig. 5B, the activity of some other muscles acting around the hip and ankle is represented for the

notable that the stance length increases regularly from 0.1 to 0.8 m/s with the slope being particularly marked for speeds ranging from 0.1 to 0.4 m/s. Other sequences studied in a similar manner tended to show that the stance length reached a plateau at around 0.8 m/s suggesting that further increases in speed, if possible, would be achieved by a change in step frequency. Finally, Fig. 4C displays the total angular excursion of the 3 joints at different walking speeds. There is a tendency for an increase in the overall amplitude of the walking movement as speed increased although no systematic analysis of this relationship was made. At speeds above 1.0-1.2 m/s, all tested animals were unable to follow the treadmill belt and steps became disorganized. We have observed only rarely a few quasi in-phase movements of both hindlimbs but not enough to establish that these animals could indeed gallop. EMG of limb muscles and kinematics at one speed. Fig. 5C shows, in stick diagram form, a representative step cycle taken at 0.4 m/s. There was definitely a tendency to drag the foot in the first part of swing but thereafter, the foot was clearly elevated above ground. This could vary however on different days. The corresponding joint angles are illustrated in Fig. 5A. It can be observed that the total hip excursion is

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92 same cat but from different cycles. The hip flexor (iliopsoas, IP) showed activity during the whole of the swing phase. The ankle flexor (tibialis anterior, TA) was activated in the first part of F and stopped during the last part of E 1. Finally, the ankle extensor gastrocnemius lateralis (GL) was activated in E 1 and continued throughout most of the stance phase. Note the sharp onset of iGL compared to iVL.

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to the single VL burst (Fig. 6A). These two bursts of_ ten had different durations and amplitudes. The rasters (Fig. 6B) and the averaged E M G (Fig. 6C) display 14 consecutive step cycles. Note that the Mfl muscles discharge prior to the onset of each VL. When the VL durations were asymmetrical, the duration of the MfL bursts associated with one VL was longer on the side of the shortest VL. For speeds between 0.1 and 0.8 m/s, there was a significant correlation between the step cycle duration, and the end and beginning of the Mfl burst as well as between the end of coVL activity and the end or beginning of the Mfl burst. These patterns remained constant in 4 different experiments.

20

Fig. 6. A, raw EMGs; B, raster; and C, average of the limb and back muscles activity taken at 159 days post-spinalization in eat B at 0.4 m/s.

Recovery of locomotion functions in the adult spinal cat: importance of locomotor training The present results indicate that despite gross motor deficits such as loss of voluntary movements and loss of equilibrium, adult cats can recuperate locomotor functions of the hindlimbs after spinalization. This confirms the basic observations of others 4JsJ9 although some discrepancies still remain. In some other studies 4J4'18, weight support was absent up to 8 weeks after spinalization. In the present results, the first cat which was kept for a long period (cat B) indeed developed plantar and digitigrade placement and weight support only around the third month. However, two other cats intensely trained to support their weight did so during the fourth week after spinalization. This appears to be about the earliest weight support that can be achieved. When weight support was achieved, the cats could step with great regularity up to 1.0-1.2 m/s in a well-coordinated fashion and with a proper range of motion. These results thus stress the importance of proper locomotor training in the recovery process following spinalization in older animals, as suggested b y Smith et al. 19 and Giuliani et al. 9. Indeed, Shurrager and Dykman ~ postulated that performance of spinalized kittens was also due to the intensive rehabilitation therapy they underwent. More recent work provides some quantitative documentation of the effects of training on weight bearing ]lJ2 as well as possible mechanisms that might explain the differences of the walking behavior when animals are exercised r7

93 During the optimal plateau period, the spinal animals maintained their locomotor performance with a minimum of training. When this minimum was not kept, however, it was observed, in one cat, that the performance reverted to an earlier stage although it could be completely re-established within 2 days of intensive training. Considering the contribution of the training programs to the recovery process, further studies with a larger, stratified sample would be required to differentiate the relative importance of the training factor in relationship to other factors involved in the recovery period. Such study has recently been partly achieved by Lovely et al. 12.

EMG activity during locomotion of the adult chronic spinal cat Analyses of the EMG activity indicate many similarities with the patterns observed in spinal kittens 6 as well as intact cats 2'5'13. For instance, the extensor muscles initiate their activity before foot contact 5 i.e. during the E 1 phase and differences in profiles such as the abrupt onset of gastrocnemius muscle and slow onset of vastus lateralis are also observed. Lumbar axial muscles such as the multifidus also have all the main characteristics of double burst activity described in intact 2 and thalamic cats 21. The flexor muscles also have these similarities. For instance, the semitendinosus usually starts at the end of stance and often has a smaller burst at the time of onset of activity in extensor muscles. Some EMG abnormalities were sometimes found. For instance, the semitendinosus could start later than in normal cats and this could account for the foot drag observed. There was also a tendency for segmentation of the EMG at a clonus-like frequency. There are also indications that the pattern of discharge of some muscles may evolve with time; for instance, the semitendinosus activity tends to get shorter several months after spinalization which also corresponds to a decrease in the overall knee flexion at this time. Whether these changes coincide with histochemical changes, for instance, remains to be studied. A degradation of locomotor performance with time was also reported by Lovely et a1.12.

Kinematics of locomotion in adult chronic spinal cat Kinematic analyses also indicate that there are

similarities between the walking movements of the adult chronic spinal cats and chronic spinal kittens 6'19. Comparisons with the intact cat are sometimes more difficult because of the limited range of speeds that the spinal animal can follow. Walking movements below speeds of 1.0 m/s are often represented by a few values only in studies of intact cat locomotion (see ref. 10 for instance). However, if one compares the cycle duration, for instance at 0.4 m/s, the intact cat has a step cycle of about 700 ms whereas the cycle duration of the spinal cat is around 800 ms in the present study. Given coefficients of variation in the order of 10-20% these values are quite similar. This comparison is also valid for the spinal kitten in which the step cycle is also in the order of 650-700 ms at that speed 6. Similar values were obtained in adult chronic spinal cats 4. There is also a general agreement between the range of values for stance and swing at the different speeds in the different preparations. It is of interest that all cats attained the~ir longest step cycle after about 3 months (Fig. 2B) and remained there. This corresponded in one cat to the onset of weight support but, in two other cats, digitigrade walking and weight support were already present after 1 month. This is certainly the result of numerous factors which cannot be separated at this time. The amplitude of the angular excursion at different joints is very similar indeed to that of the spinal kitten for comparable speeds. The total hip excursion is close to 35 °, while that of the knee and ankle is around 50° (ref. 6). The hip excursion may be larger in intact cats by about 10° (ref. 10) although the excursion of the other joints is very similar to that obtained in walk or trot. Similar amplitude ranges of movements were obtained by others 4A9. It has been emphasized by Eidelberg et al. 4 and reiterated by Smith et a1.19 that there is an uncoupling in the angular movement of the knee and the ankle in the adult spinal cat. This is not apparent either in the spinal kitten 6 or in the present work. Fig. 5D indeed illustrates quite clearly that the angular movements resemble those found in normal cats. However, such an uncoupling could occur in those instances where the ankle overextended at the end of extension or when the foot grossly dragged over the belt. This was, however, not the rule.

94 A n o t h e r point often raised is the absence of yield. It is quite clear in Fig. 5 A that there is a yield particularly visible at the ankle. It a p p e a r s to be small even though a direct comparison with normal cats at the same speed is not available. Observations of intact cats indicate that the yield is quite small when walking at similar low speeds. It also seems that this decrease in yield gets m o r e evident at a much later stage when the animal clearly walks on stiffer legs (around 6 months post-spinalization).

c o m o t o r functions in adults and that indeed it may even be generally n e e d e d in the adult (see also refs. 11 and 12). Knowing that this result can be achieved, it will thus be possible to study in m o r e detail the effect of different training p r o c e d u r e s or different classes of chemicals on this recovery process as has already been done 1,15.

Concluding remarks

This work was s u p p o r t e d by a group grant of the Medical Research Council of Canada. H . B . received a F R S Q postdoctoral fellowship as well as a H e r b e r t Jasper postdoctoral fellowship from the Centre de Recherche en Sciences Neurologiques of the Faculty of Medicine. W e wish to thank Ms. Janyne Provencher for the careful handling of the animals during experiments as well as her participation in the analyses. We also wish to thank S. Bergeron, R. Bouchoux, G. Blanchette, Jocelyn L a p o i n t e and S. Burke for their essential technical help.

The above results suggest that, even as adults, cats can recuperate l o c o m o t o r functions of the hindlimbs with weight support of the hindquarters and plantar digitigrade placement of the feet after spinal transection. It is generally considered that the age of spinalization is i m p o r t a n t and that adults do not r e c u p e r a t e l o c o m o t o r functions as well as young animals 3-4,1~-2". W i t h o u t denying the validity of this observation, it is, however, suggested here that p r o p e r interactive training may greatly improve the recovery of such 1o-

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ACKNOWLEDGEMENTS

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