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Reflex responses of human thigh muscles to non-noxious sural stimulation during stepping
378
Brain Research, 288 (1983) 378-38t) Elsevier
Reflex responses of human thigh muscles to non-noxious sural stimulation during stepping KENRO KANDA* and HITOSHI SATO** Department of Physiology, School of Medicine, Chiba University, Chiba 280 (Japan) (Accepted August 23rd, 1983) Key words: sural stimulation - - reflex response - - EMG - - thigh muscles - - human stepping
An investigation of reflex responses of leg muscles to sural stimulation during stepping was performed on human subjects, Non-noxious electrical stimulation applied during the swing phase or the latter half of the stance phase produced a mixed increase and decrease of EMG activity in the hamstring muscles. No response or very weak response was observed when the same stimulus was applied during either quiet standing or various levels of constant voluntary effort at varying hip and knee joint angles. It has been reported that a weak electrical stimulation applied to the sural nerve or to the skin of the foot elicits a reflex response in various leg muscles, or modifies the transmission in some spinal reflex pathways of the healthy adult human 2.11,14.15. This reflex transmission depends on posture and/or muscle activity2,12,15. The significance of this cutaneous reflex has been discussed in relation to human bipedal gait and postural control of the positioning of the foot 11.14,15. Effect of tactile and/or non-noxious electrical stimulation applied to the cat paw during ambulation has also been studied extensively 3-10.13.a6. It has been suggested that the reflex responses of the cat to cutaneous stimulation are modulated during ambulation by the spinal locomotor oscillator 1,5.9. The present study was undertaken to explore a similar phasic modulation of reflex response to non-noxious sural stimulation during human stepping. Three subjects between the ages of 26 and 38 years with no history of neuromuscular disease were examined (15 experiments). Subjects were asked to step in one spot in time to clicks that were emitted at 1.1 s intervals. The E M G of the hamstring and the quadriceps femoris muscles was recorded with bipolar surface electrodes that were placed over the semitendi-
nosus and the vastus lateralis muscles. A non-noxious electrical stimulation (a train of 5 pulses of 0.2 or 1 ms duration with a 3 ms interval) was applied to the sural nerve at a point just below the lateral maleollus. The probability of stimulation during each step cycle was independent of prior stimulation. Approximately 50% of the steps were stimulated. E M G of each step cycle was recorded on FM tape (DC5 kHz) which later was sorted into groups with and without sural stimulation. Each group of records was rectified and averaged 50-100 times separately, The averaged E M G of the non-stimulated, control step cycle was subtracted from that of the stimulated step cycle in order to evaluate the effect of sural stimulation. When non-noxious electrical stimulation (usually 1.5 times perceptual threshold) was applied to the sural nerve during the early stance phase, no reflex response could be induced in the ipsilateral hamstring muscles (Fig. 1E, F). On the other hand, the same stimulus applied during the latter half of the stance and the swing phases produced a mixture of decreased and increased E M G activity (Fig. tB, C, E, F). During the stance phase, the E M G activity was initially inhibited and then subsequently facilitated.
* Present address: Department of Physiology, Tokyo Metropolitan Institute of Gerontology, 35-2 Sakaecho, Itabashi-ku, Tokyo 173, Japan. ** Present address: Department of Physiology, Nippon Medical School, 1-1-5 Sendagi, Bunkyo-ku, Tokyo 113, Japan. Correspondence: K. Kanda, Department of Physiology, Tokyo Metropolitan Institute of Gerontology, 35-2 Sakaecho, ltabashi-ku, Tokyo 173, Japan. 0006-8993/83/$03.00 ~ 1983 Elsevier Science Publishers B.V.
379
but a d e c r e a s e c o u l d usually b e d e t e c t e d a b o u t 60-
the phase of the step cycle at which the stimulus was applied. In one experiment (subject K), a single
70 ms after t h e o n s e t o f s t i m u l a t i o n (69.6 ms for sub-
s h o c k was c a p a b l e o f p r o d u c i n g a r e f l e x r e s p o n s e . In
j e c t I, 70.4 ms for s u b j e c t K and 59.6 ms f o r s u b j e c t
this p a r t i c u l a r case, the latency o f the d e c r e a s e in
S). T h e s e v a l u e s r e m a i n e d c o n s t a n t i r r e s p e c t i v e o f
E M G activity was 69 ms. This v a l u e is v e r y close to
The onset of the response was difficult to determine,
that o b t a i n e d in t h e r e p e t i t i v e s t i m u l a t i o n experim e n t s . T h e r e f o r e , all t h e s e v a l u e s s e e m to be close to the actual t i m e it t a k e s for an i m p u l s e to travel t h r o u g h t h e r e f l e x arc. C o n d u c t i o n v e l o c i t i e s o f the sural and t h e tibial ( m o t o r ) n e r v e s in s u b j e c t K w e r e . . . .
48.8 m/s and 57.5 m/s, r e s p e c t i v e l y . F r o m t h e s e val-
D ld°o
E
ues t h e central latency of the i n h i b i t o r y reflex response was c a l c u l a t e d as b e i n g a b o u t 41.6 ms. In addition to t h e s e r e s p o n s e s , a short l a t e n c y i n c r e a s e ( a b o u t 50 ms after the o n s e t of s t i m u l a t i o n ) in E M G activity was o b s e r v e d in s o m e e x p e r i m e n t s w h e n the stimulation
was
applied
during
the
swing p h a s e
(Fig. 1E). T h e o n g o i n g activity in the q u a d r i c e p s f e m o r i s was i n f l u e n c e d by t h e s a m e stimulus a p p l i e d d u r i n g the
100 i
Fig. 1. Effect of stimulation of the sural nerve on the activity of the hamstring muscles during stepping. A: rectified and averaged EMG activity of the quadriceps femoris muscles during the control step cycle in which the sural nerve was not stimulated (average of 50 trials). B: same as in A, except that data were simultaneously recorded from the hamstring muscles. C: same as in B, except that the sural nerve was stimulated 450 ms after the foot made contact with the ground. The stimulus artifact is indicated by an arrow. Note that a marked decrease in EMG activity was induced about 70 ms after the stimulation. Compare record C with B. D: hip (&) and knee (O) joint angles during a control step cycle. Mean periods of the stance phase of the right, stimulated leg (upper bar), and left, nonstimulated leg (lower bars) are also indicated. E: records showing the effect of sural stimulation applied 6 different times during the step cycle. In order to evaluate the effect, the average of 50 control step cycles (such as B) was subtracted from the average of 50 step cycles in which the sural nerve was stimulated (such as C). The downward deflection from the baseline indicates decrease in activity, and upward deflection indicates increased activity as compared with the activity in the control step cycle. Arrows and numbers in each record indicate the stimulus artifacts and times when the stimulation was applied. Measurements were begun at the point when the foot made contact with the ground. Results shown in E were summarized in F. The inhibitory effect (O) and the excitatory one which follows the inhibition (©) were plotted against the time of stimulation. The zero level indicates normal activity in the muscle, and --100% represents complete inhibition of activity. Excitation is expressed as a percentage of the maximal activity during the control step. All records and figures shown start at the point when the foot first made contact with the ground. The time-scale in F is applicable to all records.
stance p h a s e ; h o w e v e r , n o r e s p o n s e was o b s e r v e d d u r i n g the swing phase. T h e r e s p o n s e in this m u s c l e was w e a k , but its p a t t e r n was similar to the initial de-
C
, 0.2s
/
Fig. 2. Effects of sural stimulation on the EMG activity of hamstring muscles during stepping and steady voluntary contraction. A: rectified and averaged EMG activity of hamstring muscles during stepping in which the sural nerve was stimulated at 450 ms after foot contact (average of 50 trials). B: same as in A, except that this was obtained during control step cycles without sural stimulation. C: difference between A and B, showing the net effect of the stimulation. D: effect of sural stimulation on the EMG activity of hamstring muscles during steady voluntary contraction in the same subject. This was obtained immediately after A and B were measured. Stimulus conditions were exactly the same as in A. Knee and hip joint angles were 175° and 170°, respectively. E: same as in D, except that knee and hip joint angles were 130° and 150° , respectively. Note that effect of sural stimulation was very different during stepping and steady voluntary contraction. Spikes under asterisks are stimulus artifacts, Lack of EMG activity is indicated by the baselines in A, B, D and E, whereas the baseline in C indicates the activity level during the control step cycle.
380 crease and subsequent increase in E M G activity, seen in the hamstring muscles. The same stimulus did not induce any response in either the hamstring or quadriceps femoris muscles during quiet standing. T h e effect was also investigated during various levels of constant voluntary effort at varying hip and knee joint angles. E i t h e r no response or a very weak response in E M G activity was seen in the hamstring muscles (Fig. 2D, E) and a weak decrease was observed in the quadriceps. These results suggest that the reflex arc producing the response during stepping is closely related to the neuronal circuit responsible for l o c o m o t i o n , and that the reflex transmission is actively gated as has been suggested1,5, 9. The reflex responses to cutaneous stimulation seem to be m o d u l a t e d by the spinal locom o t o r oscillator during h u m a n a m b u l a t i o n , although the possibility that inputs from the skin, joints and muscles during stepping m a y be different from those during steady voluntary effort at certain joint angles also must be t a k e n into account. Changes in motion of the stimulated leg were not d e t e c t e d in the present experiments. This may be attributed at least in part
to our e x p e r i m e n t a l m e t h o d in which the subject was asked to step at a constant rate and knew that he did not need to c o m p e n s a t e for this stepping movement. The present e x p e r i m e n t showed that sural stimulation during stepping p r o d u c e d a complex response of inhibition and excitation while in previous cat experiments the same sural stimulation p r o d u c e d a pure excitatory response in the flexor muscles (see refs. 4, 7). In the present series of experiments, the response pattern did not seem to be altered by changing the stimulus intensity (up to 5 times perceptual threshold). The decrease in E M G activity of the hamstring muscles does not seem to be part of the startle response because the stimulation intensity was weak and the response p a t t e r n was completely reversed in other leg muscles.
1 Andersson, O., Grillner, S., Lindquist, M. and Zomlefer, M., Peripheral control of the spinal pattern generators for locomotion in cat, Brain Research, 150 (1978) 625-630. 2 Bergego, C., Pierrot-Deseilligny, E. and Mazieres, L., Facilitation of transmission in Ib pathways by cutaneous afferents from the contralateral foot sole in man, Neurosci. Lett., 27 (1981) 297-301. 3 Duysens, J., Reflex control of locomotion as revealed by stimulation of cutaneous afferents in spontaneously walking premammillary cats, J. Neurophysiol., 40 (1977) 737-751. 4 Duysens, J. and Loeb, G. E., Modulation of ipsi- and contralateral reflex responses in unrestrained walking cats, J. Neurophysiol., 44 (1980) 1024-1037. 5 Duysens, J., Loeb, G. E. and Weston, B. J., Crossed flexor reflex responses and their reversal in freely walking cats, Brain Research, 197 (1980) 538-542. 6 Duysens, J. and Pearson, K. G., The role of cutaneous afferents from the distal hindlimb in the regulation of the step cycle of thalamic cats, Exp. Brain Res., 24 (1976) 245-255. 7 Forssberg, H., Stumbling corrective reaction: a phase-dependent compensatory reaction during locomotion, J. NeurophysioL, 42 (1979) 936-953. 8 Forssberg, H., Grillner, S. and Rossignol, S., Phase dependent reflex reversal during walking in chronic spinal cats, Brain Research, 85 (1975) 103-107.
9 Forssberg, H., Grillner, S. and Rossignol, S., Phasic gain control of reflexes from the dorsum of the paw during spinal locomotion, Brain Research, 132 (1977) 121-139. 10 GriUner, S. and Rossignot, S., Contralaterat reflex reversal controlled by limb position in the acute spinal cat injected with clonidine i.v.. Brain Research, 144 (1978) 411-414. 11 Hugon, M.. Exteroceptive reflexes to stimulation of the sural nerve in normal man. In Desmedt, J. E. (Ed.), New Developments in Electromyography and Clinical Neurophysiology, Vol. 3, Karger, Basel, 1973, pp. 713-729. 12 Lisin, V. V., Frankstein, S. I. and Rechtmann, M. B.. The influence of locomotion on flexor reflex of the hind limb in cat and man, Exp. Neurol., 38 (1973) 180--183. 13 Matsukawa, K., Kamei, H.. Minoda, K. and Udo, M.. Interlimb coordination in cat. I. Behavioral and eleetromyographic study on symmetric limbs of decerebrate and awake walking cats, Exp. Brain Res., 46 (1982) 425-437. 14 Pierrot-Deseilligny, E., Bergego, C., Katz, R. and Morin, C., Cutaneous depression of Ib reflex pathways to motoneurones in man, Exp. Brain Res., 42 (1981) 351-361. 15 Pierrot-Deseflligny, E., Bergego, C. and Katz, R., Reversal in cutaneous control of Ib pathways during human voluntary contraction, Brain Research, 233 (1982) 400-403. 16 Wand, P., Prochazka, A. and Sontag, K.-H., Neuromuscular responses to gait perturbations in freely moving cats, Exp. Brain Res., 38 (1980) 109-114.
The authors would like to thank Professor S. H o m ma for encouraging this work, Professor H. Kasai and Mr. T. Sakai for allowing us to use a locomotion analysis system consisting of a TV c a m e r a and a mic r o c o m p u t e r which they had d e v e l o p e d , and Mrs. S. A s a k i for typing the manuscript.
Brain Research, 288 (1983) 378-38t) Elsevier
Reflex responses of human thigh muscles to non-noxious sural stimulation during stepping KENRO KANDA* and HITOSHI SATO** Department of Physiology, School of Medicine, Chiba University, Chiba 280 (Japan) (Accepted August 23rd, 1983) Key words: sural stimulation - - reflex response - - EMG - - thigh muscles - - human stepping
An investigation of reflex responses of leg muscles to sural stimulation during stepping was performed on human subjects, Non-noxious electrical stimulation applied during the swing phase or the latter half of the stance phase produced a mixed increase and decrease of EMG activity in the hamstring muscles. No response or very weak response was observed when the same stimulus was applied during either quiet standing or various levels of constant voluntary effort at varying hip and knee joint angles. It has been reported that a weak electrical stimulation applied to the sural nerve or to the skin of the foot elicits a reflex response in various leg muscles, or modifies the transmission in some spinal reflex pathways of the healthy adult human 2.11,14.15. This reflex transmission depends on posture and/or muscle activity2,12,15. The significance of this cutaneous reflex has been discussed in relation to human bipedal gait and postural control of the positioning of the foot 11.14,15. Effect of tactile and/or non-noxious electrical stimulation applied to the cat paw during ambulation has also been studied extensively 3-10.13.a6. It has been suggested that the reflex responses of the cat to cutaneous stimulation are modulated during ambulation by the spinal locomotor oscillator 1,5.9. The present study was undertaken to explore a similar phasic modulation of reflex response to non-noxious sural stimulation during human stepping. Three subjects between the ages of 26 and 38 years with no history of neuromuscular disease were examined (15 experiments). Subjects were asked to step in one spot in time to clicks that were emitted at 1.1 s intervals. The E M G of the hamstring and the quadriceps femoris muscles was recorded with bipolar surface electrodes that were placed over the semitendi-
nosus and the vastus lateralis muscles. A non-noxious electrical stimulation (a train of 5 pulses of 0.2 or 1 ms duration with a 3 ms interval) was applied to the sural nerve at a point just below the lateral maleollus. The probability of stimulation during each step cycle was independent of prior stimulation. Approximately 50% of the steps were stimulated. E M G of each step cycle was recorded on FM tape (DC5 kHz) which later was sorted into groups with and without sural stimulation. Each group of records was rectified and averaged 50-100 times separately, The averaged E M G of the non-stimulated, control step cycle was subtracted from that of the stimulated step cycle in order to evaluate the effect of sural stimulation. When non-noxious electrical stimulation (usually 1.5 times perceptual threshold) was applied to the sural nerve during the early stance phase, no reflex response could be induced in the ipsilateral hamstring muscles (Fig. 1E, F). On the other hand, the same stimulus applied during the latter half of the stance and the swing phases produced a mixture of decreased and increased E M G activity (Fig. tB, C, E, F). During the stance phase, the E M G activity was initially inhibited and then subsequently facilitated.
* Present address: Department of Physiology, Tokyo Metropolitan Institute of Gerontology, 35-2 Sakaecho, Itabashi-ku, Tokyo 173, Japan. ** Present address: Department of Physiology, Nippon Medical School, 1-1-5 Sendagi, Bunkyo-ku, Tokyo 113, Japan. Correspondence: K. Kanda, Department of Physiology, Tokyo Metropolitan Institute of Gerontology, 35-2 Sakaecho, ltabashi-ku, Tokyo 173, Japan. 0006-8993/83/$03.00 ~ 1983 Elsevier Science Publishers B.V.
379
but a d e c r e a s e c o u l d usually b e d e t e c t e d a b o u t 60-
the phase of the step cycle at which the stimulus was applied. In one experiment (subject K), a single
70 ms after t h e o n s e t o f s t i m u l a t i o n (69.6 ms for sub-
s h o c k was c a p a b l e o f p r o d u c i n g a r e f l e x r e s p o n s e . In
j e c t I, 70.4 ms for s u b j e c t K and 59.6 ms f o r s u b j e c t
this p a r t i c u l a r case, the latency o f the d e c r e a s e in
S). T h e s e v a l u e s r e m a i n e d c o n s t a n t i r r e s p e c t i v e o f
E M G activity was 69 ms. This v a l u e is v e r y close to
The onset of the response was difficult to determine,
that o b t a i n e d in t h e r e p e t i t i v e s t i m u l a t i o n experim e n t s . T h e r e f o r e , all t h e s e v a l u e s s e e m to be close to the actual t i m e it t a k e s for an i m p u l s e to travel t h r o u g h t h e r e f l e x arc. C o n d u c t i o n v e l o c i t i e s o f the sural and t h e tibial ( m o t o r ) n e r v e s in s u b j e c t K w e r e . . . .
48.8 m/s and 57.5 m/s, r e s p e c t i v e l y . F r o m t h e s e val-
D ld°o
E
ues t h e central latency of the i n h i b i t o r y reflex response was c a l c u l a t e d as b e i n g a b o u t 41.6 ms. In addition to t h e s e r e s p o n s e s , a short l a t e n c y i n c r e a s e ( a b o u t 50 ms after the o n s e t of s t i m u l a t i o n ) in E M G activity was o b s e r v e d in s o m e e x p e r i m e n t s w h e n the stimulation
was
applied
during
the
swing p h a s e
(Fig. 1E). T h e o n g o i n g activity in the q u a d r i c e p s f e m o r i s was i n f l u e n c e d by t h e s a m e stimulus a p p l i e d d u r i n g the
100 i
Fig. 1. Effect of stimulation of the sural nerve on the activity of the hamstring muscles during stepping. A: rectified and averaged EMG activity of the quadriceps femoris muscles during the control step cycle in which the sural nerve was not stimulated (average of 50 trials). B: same as in A, except that data were simultaneously recorded from the hamstring muscles. C: same as in B, except that the sural nerve was stimulated 450 ms after the foot made contact with the ground. The stimulus artifact is indicated by an arrow. Note that a marked decrease in EMG activity was induced about 70 ms after the stimulation. Compare record C with B. D: hip (&) and knee (O) joint angles during a control step cycle. Mean periods of the stance phase of the right, stimulated leg (upper bar), and left, nonstimulated leg (lower bars) are also indicated. E: records showing the effect of sural stimulation applied 6 different times during the step cycle. In order to evaluate the effect, the average of 50 control step cycles (such as B) was subtracted from the average of 50 step cycles in which the sural nerve was stimulated (such as C). The downward deflection from the baseline indicates decrease in activity, and upward deflection indicates increased activity as compared with the activity in the control step cycle. Arrows and numbers in each record indicate the stimulus artifacts and times when the stimulation was applied. Measurements were begun at the point when the foot made contact with the ground. Results shown in E were summarized in F. The inhibitory effect (O) and the excitatory one which follows the inhibition (©) were plotted against the time of stimulation. The zero level indicates normal activity in the muscle, and --100% represents complete inhibition of activity. Excitation is expressed as a percentage of the maximal activity during the control step. All records and figures shown start at the point when the foot first made contact with the ground. The time-scale in F is applicable to all records.
stance p h a s e ; h o w e v e r , n o r e s p o n s e was o b s e r v e d d u r i n g the swing phase. T h e r e s p o n s e in this m u s c l e was w e a k , but its p a t t e r n was similar to the initial de-
C
, 0.2s
/
Fig. 2. Effects of sural stimulation on the EMG activity of hamstring muscles during stepping and steady voluntary contraction. A: rectified and averaged EMG activity of hamstring muscles during stepping in which the sural nerve was stimulated at 450 ms after foot contact (average of 50 trials). B: same as in A, except that this was obtained during control step cycles without sural stimulation. C: difference between A and B, showing the net effect of the stimulation. D: effect of sural stimulation on the EMG activity of hamstring muscles during steady voluntary contraction in the same subject. This was obtained immediately after A and B were measured. Stimulus conditions were exactly the same as in A. Knee and hip joint angles were 175° and 170°, respectively. E: same as in D, except that knee and hip joint angles were 130° and 150° , respectively. Note that effect of sural stimulation was very different during stepping and steady voluntary contraction. Spikes under asterisks are stimulus artifacts, Lack of EMG activity is indicated by the baselines in A, B, D and E, whereas the baseline in C indicates the activity level during the control step cycle.
380 crease and subsequent increase in E M G activity, seen in the hamstring muscles. The same stimulus did not induce any response in either the hamstring or quadriceps femoris muscles during quiet standing. T h e effect was also investigated during various levels of constant voluntary effort at varying hip and knee joint angles. E i t h e r no response or a very weak response in E M G activity was seen in the hamstring muscles (Fig. 2D, E) and a weak decrease was observed in the quadriceps. These results suggest that the reflex arc producing the response during stepping is closely related to the neuronal circuit responsible for l o c o m o t i o n , and that the reflex transmission is actively gated as has been suggested1,5, 9. The reflex responses to cutaneous stimulation seem to be m o d u l a t e d by the spinal locom o t o r oscillator during h u m a n a m b u l a t i o n , although the possibility that inputs from the skin, joints and muscles during stepping m a y be different from those during steady voluntary effort at certain joint angles also must be t a k e n into account. Changes in motion of the stimulated leg were not d e t e c t e d in the present experiments. This may be attributed at least in part
to our e x p e r i m e n t a l m e t h o d in which the subject was asked to step at a constant rate and knew that he did not need to c o m p e n s a t e for this stepping movement. The present e x p e r i m e n t showed that sural stimulation during stepping p r o d u c e d a complex response of inhibition and excitation while in previous cat experiments the same sural stimulation p r o d u c e d a pure excitatory response in the flexor muscles (see refs. 4, 7). In the present series of experiments, the response pattern did not seem to be altered by changing the stimulus intensity (up to 5 times perceptual threshold). The decrease in E M G activity of the hamstring muscles does not seem to be part of the startle response because the stimulation intensity was weak and the response p a t t e r n was completely reversed in other leg muscles.
1 Andersson, O., Grillner, S., Lindquist, M. and Zomlefer, M., Peripheral control of the spinal pattern generators for locomotion in cat, Brain Research, 150 (1978) 625-630. 2 Bergego, C., Pierrot-Deseilligny, E. and Mazieres, L., Facilitation of transmission in Ib pathways by cutaneous afferents from the contralateral foot sole in man, Neurosci. Lett., 27 (1981) 297-301. 3 Duysens, J., Reflex control of locomotion as revealed by stimulation of cutaneous afferents in spontaneously walking premammillary cats, J. Neurophysiol., 40 (1977) 737-751. 4 Duysens, J. and Loeb, G. E., Modulation of ipsi- and contralateral reflex responses in unrestrained walking cats, J. Neurophysiol., 44 (1980) 1024-1037. 5 Duysens, J., Loeb, G. E. and Weston, B. J., Crossed flexor reflex responses and their reversal in freely walking cats, Brain Research, 197 (1980) 538-542. 6 Duysens, J. and Pearson, K. G., The role of cutaneous afferents from the distal hindlimb in the regulation of the step cycle of thalamic cats, Exp. Brain Res., 24 (1976) 245-255. 7 Forssberg, H., Stumbling corrective reaction: a phase-dependent compensatory reaction during locomotion, J. NeurophysioL, 42 (1979) 936-953. 8 Forssberg, H., Grillner, S. and Rossignol, S., Phase dependent reflex reversal during walking in chronic spinal cats, Brain Research, 85 (1975) 103-107.
9 Forssberg, H., Grillner, S. and Rossignol, S., Phasic gain control of reflexes from the dorsum of the paw during spinal locomotion, Brain Research, 132 (1977) 121-139. 10 GriUner, S. and Rossignot, S., Contralaterat reflex reversal controlled by limb position in the acute spinal cat injected with clonidine i.v.. Brain Research, 144 (1978) 411-414. 11 Hugon, M.. Exteroceptive reflexes to stimulation of the sural nerve in normal man. In Desmedt, J. E. (Ed.), New Developments in Electromyography and Clinical Neurophysiology, Vol. 3, Karger, Basel, 1973, pp. 713-729. 12 Lisin, V. V., Frankstein, S. I. and Rechtmann, M. B.. The influence of locomotion on flexor reflex of the hind limb in cat and man, Exp. Neurol., 38 (1973) 180--183. 13 Matsukawa, K., Kamei, H.. Minoda, K. and Udo, M.. Interlimb coordination in cat. I. Behavioral and eleetromyographic study on symmetric limbs of decerebrate and awake walking cats, Exp. Brain Res., 46 (1982) 425-437. 14 Pierrot-Deseilligny, E., Bergego, C., Katz, R. and Morin, C., Cutaneous depression of Ib reflex pathways to motoneurones in man, Exp. Brain Res., 42 (1981) 351-361. 15 Pierrot-Deseflligny, E., Bergego, C. and Katz, R., Reversal in cutaneous control of Ib pathways during human voluntary contraction, Brain Research, 233 (1982) 400-403. 16 Wand, P., Prochazka, A. and Sontag, K.-H., Neuromuscular responses to gait perturbations in freely moving cats, Exp. Brain Res., 38 (1980) 109-114.
The authors would like to thank Professor S. H o m ma for encouraging this work, Professor H. Kasai and Mr. T. Sakai for allowing us to use a locomotion analysis system consisting of a TV c a m e r a and a mic r o c o m p u t e r which they had d e v e l o p e d , and Mrs. S. A s a k i for typing the manuscript.