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Functional modulation of the human flexion and crossed extension reflexes by body position
ELSEVIER
Neuroscience Letters 209 (1996) 215-217
N[UROSCIEliC[ LETTERS
Functional modulation of the human flexion and crossed extension reflexes by body position Nicole Paquet*, Felix Tam, Christina W.Y. Hui-Chan ~ School of Physical and Occupational Therapy and Physiology Department, Faculty of Medicine, McGill University, Montreal, Quebec, Canada Received 21 February 1995; revised version received 16 April 1996; accepted 16 April 1996
Abstract
The effects of body po,;ition on the electrically evoked flexion (FR) and crossed extension reflexes (CER) were investigated in humans. The FR area in the ipsilateral tibialis anterior muscle was significantly smaller during sitting than supported stance by 36% (P < 0.01). In contrast, the excitability of extensor muscles on both sides was enhanced in standing. For instance, twice as many subjects manifested a response in the ipsilateral vastus lateralis (VL) and the contralateral VL and/or soleus muscles (i.e. the CER) in standing than sitting. The FR and CER modulation observed seems to be dictated by the difference in functional demand between sitting and supported stance.
Keywords: Flexion reflex; Crossed extension reflex; Body position; Human
In healthy humans, changes in body position are known to modify the excitability of lower limb muscle responses to various types of stimulation. For example, in comparison with sittin~g, the standing position was found to enhance the restabilizing response in the tibialis anterior (TA) muscle to sudden toe-up rotation of the support platform [ 1]. In contra:~t, the area of response in the ipsilateral TA muscle (iTA) to painful electrical stimulation of the foot, i.e. the flexion reflex (FR), was reduced in standing [5]. Although opposite to each other, the effects of standing on these reflexes were appropriate to the task; i.e., the maintenance of a stable standing position. When the FR stimulation is of sufficient intensity, it can be accompanied by a response in the contralateral extensor muscles named the crossed extension reflex (CER) [6]. A questio~ arises as to whether the influence of body position on the FR and CER excitability is similar or not. For instance, is the modulation of the FR and CER determined by the functional requirement of a specific
* Corresponding author. Aerospace Medical Research Unit, McGill University, 3655 Drummond. Room 1220, Montreal, PQ H3G IY6, Canada. Tel.: + I 514 3986025; fax: + 1 514 3988241 ; c-mail: gsnp~physocc Jan.mcgill.ca. I Current address: Department of Rehabilitation Sciences, Hong Kong Polytechnic University, Hong Kong.
body position? The objective of this study was to compare the effect of sitting and supported stance on the FR and CER. A total of 17 healthy subjects with a mean age (+_SD) of 26 ± 3 years was examined. In the sitting condition, subjects (n = 12) semi-reclined with the knees fixed in a flexed position of about 140 ° and the ankles at about 90 ° . In the standing condition, they (n = 13) stood on a platform with head, shoulders and trunk fixed to a back support by means of straps and canvas, with their neck maintained in the neutral position by a neck collar. In order to prevent the known habituation of the FR with repetitive stimulation [2], a tonic contraction of 10-20% of the maximum voluntary contraction was maintained in the iTA muscle in both conditions. The level of this background contraction was computer-controlled. A train of electrical pulses (1 ms at 200 Hz) of 30 ms duration was given to the right tibial nerve via a surface electrode maintained under pressure behind the medial malleolus, at an intensity of 3-5 times the sensory threshold (group mean 3.9 +_ 1.8 times). The surface EMG activity was recorded in the TA, soleus (SO), and vastus lateralis (VL) muscles on both sides during 500 ms, i.e. 100 ms prior to and 400 ms after the electrical stimulation. The EMG signals were preamplified (gain= 10), amplified (gain = 100), band-pass filtered (20-1400 Hz)
0304-3940/96/$12.00 © I996 Elsevier Science Ireland Ltd. All rights reserved PII: S 0 3 0 4 - 3 9 4 0 ( 9 6 ) 1 2 6 4 9 - 3
216
N. Paquet et al. /Neuroscience Letters 209 (1996) 215-217
63
iTA
It,t8
WL
cSO
to v I
0
100
200
300
400
'
0
100
200
300
400
Time (ms)
Time (ms)
Fig. 1. Mean EMG traces from 6-10 trials in one subject, recorded in the iTA, iVL and cSO muscles during sitting (first column) and standing (second column). Time 0 represents the onset of electrical stimulation. The horizontal line on each trace was drawn to mask the stimulus artifact. The response latency is indicated as the number above the arrows.
and sampled at a frequency of 4 kHz. The activation latency and the offset of muscle responses were defined as the moment the rectified signal exceeded and fell below the mean _ 2 SDs of the mean baseline. Since the iTA FR was present in every subjects and in a majority of trials (see below), the response latency and area were calculated from individual responses for the iTA muscle. These variables were calculated from the averaged response for the other muscles, due to the small number of subjects manifesting these responses (see Fig. 2). The area was calculated between the onset and offset, from which the area of a corresponding segment of the baseline was subtracted. The means were calculated only for the trials showing a reflex. Unpaired Student's t and MannWhitney tests were used to identify significant effects of body position on the dependent variables. Fig. 1 illustrates examples of averaged responses to FR stimulation obtained in the iTA, ipsilateral VL (iVL) and contralateral SO (cSO) muscles of one subject during sitting and supported stance. In the sitting position, this subject manifested only a FR in the iTA muscle. In supported stance, the iTA FR area was smaller than that in sitting by 4%. The FR was accompanied by a response in the iVL muscle and a CER in the cSO muscle. Note that the background activity was similar in the two body positions. The group analysis revealed that in comparison with the sitting position, the mean iTA FR area in supported stance was significantly reduced by 36% (Student's t-test, P < 0.01; 1.21 _0.62/aV/s in sitting versus 0.77 _ 0.47/tV/s in standing). The mean frequency of iTA FR occurrence tended to be lower in supported
stance (73% of trials) than in sitting (86% of trials). The mean iTA FR latency was similar in supported stance (70 + 11 ms) and in sitting (70 + 10 ms). Fig. 2 shows that a similar proportion of subjects manifested a FR in the iTA muscle in the two body posi-
100 90,
80' ~
7o
~
6o
,.
50
~
4o
~
3o
m
~
2o 1o
TA
SO Ipsllateral
VL
TA
SO
VL
contralateral
Fig 2 Proportion of subjects manifesting EMG responses to the electrical stimulation in the ipsilateral and contralateral TA, SO and VL muscles during sitting and standing. The two arrows indicates the largest differences between sitting and standing.
N. Paquet et al. / Neuroscience Letters 209 (1996) 215-217
tions. In contrast, a response in the iVL muscle was evoked in twice as many subjects during supported stance (10/13 subjects) as in :sitting (5/12; P = 0 . 1 1 , Fisher's exact test). Similarly, a CER in the cSO and/or cVL muscle was found in twice as many subjects in supported stance (6/13) than in sitting (3/11). We found that the mean iTA FR area of healthy subjects was significantly sraaller in supported stance than in sitting by 36% (P < 0.01). This indicates that the FR excitability was reduced iF standing. The extent of this decrease, however, was about half the reduction that was found in freely standirtg subjects [1]. This difference could be attributable to the different body support provided in the two experiments. Body support was found to reduce the excitability of lower limb postural responses in standing subjects [4]. Our body support might have attenuated the influence of standing on the FR excitability. As a consequence, the effect of standing on the FR area would be smaller between supported stance and sitting, than between free-standing and sitting. Our main finding is 1-hat the decreased FR excitability in supported stance was accompanied by an enhancement of the extensor muscle ,excitability on both sides. On the ipsilateral side, a response in the iVL muscle was observed in a majority of subjects during supported stance (77%), but only in a mir~ority during sitting (42%). On the contralateral side, a CER in the cSO and/or cVL muscle was also found in twice as many subjects in supported stance than in sitting. Thus, body position modulated the excitability of the FR and extensor responses (which includes the CER) in a reciprocal manner. Since this reciprocal modulation is likely appropriate to ensure a stable standing position, it suggests that the functional demand could dictate the modulation of muscle responses to FR stimulation. In spinal cats walking on a treadmill, the same electrical stimulation of the dorsum of the foot evoked an ipsilateral flexion and contralateral extension of the limb during swing, and an ipsilateral extension during stance
217
[3]. In healthy humans, this 'phase-dependent reflex reversal' was even observed within muscles of the lower limb [7]. These results suggested that the reflex modulation during gait was governed by the alternating supporting task of the lower limb during the gait cycle. In the present experiment, no such reversal in the reflex behavior was observed during the change between sitting and standing. However, we found a meaningful adjustment in FR and extensor response excitability. From a functional point of view, the reduced FR excitability combined with the increased extensor response excitability is likely appropriate to maintain a stable standing position. The authors acknowledge the financial support by the Parkinson's Foundation of Canada and a studentship from the Medical Research Council of Canada to N.P. [1] Allum, J.H.J. and Pfaltz, C.R., Visual and vestibular contribution to pitch sway stabilization in the ankle muscles of normal and patients with bilateral peripheral vestibular deficits, Exp. Brain Res., 58 (1985) 82-94. [2] Chan, C.W.Y. and Tsang, H.H.Y., A quantitative study of flexion reflex in man: relevance to pain research. In H.L. Fields, R. Dubner and F. Cerveno (Eds.), Advances in Pain Research and Therapy, Vol. 9, Raven Press, New York, 1985, pp. 361-369. [3] Forssberg, H., Grillner, S. and Rossignol, S., Phasic gain control of reflexes from the dorsum of the paw during spinal locomotion, Brain Res., 132 (1977) 121-139. [4] Nardone, A., Giordano, A., Corra, T. and Schieppati, M., Responses of leg muscles in humans displaced while standing: effects of types of perturbation and postural set, Brain, 80 (1990) 65-84. [5] Rossi, A. and Decchi, B., Flexibility of lower limb reflex responses to painful cutaneous stimulation in standing humans: evidence of load-dependent modulation, J. Physiol. (London), 481.2 (1994) 521-532. [6] Sherrington, C.S., Flexion reflex of the limb, crossed-extension reflex and reflex stepping and standing, J. Physiol. (London), 40 (1910) 28-121. [7] Yang, J.F. and Stein, R.B., Phase-dependent reflex reversal in human leg muscles during walking, J. Neurophysiol., 63 (1990) 1109-1117.
Neuroscience Letters 209 (1996) 215-217
N[UROSCIEliC[ LETTERS
Functional modulation of the human flexion and crossed extension reflexes by body position Nicole Paquet*, Felix Tam, Christina W.Y. Hui-Chan ~ School of Physical and Occupational Therapy and Physiology Department, Faculty of Medicine, McGill University, Montreal, Quebec, Canada Received 21 February 1995; revised version received 16 April 1996; accepted 16 April 1996
Abstract
The effects of body po,;ition on the electrically evoked flexion (FR) and crossed extension reflexes (CER) were investigated in humans. The FR area in the ipsilateral tibialis anterior muscle was significantly smaller during sitting than supported stance by 36% (P < 0.01). In contrast, the excitability of extensor muscles on both sides was enhanced in standing. For instance, twice as many subjects manifested a response in the ipsilateral vastus lateralis (VL) and the contralateral VL and/or soleus muscles (i.e. the CER) in standing than sitting. The FR and CER modulation observed seems to be dictated by the difference in functional demand between sitting and supported stance.
Keywords: Flexion reflex; Crossed extension reflex; Body position; Human
In healthy humans, changes in body position are known to modify the excitability of lower limb muscle responses to various types of stimulation. For example, in comparison with sittin~g, the standing position was found to enhance the restabilizing response in the tibialis anterior (TA) muscle to sudden toe-up rotation of the support platform [ 1]. In contra:~t, the area of response in the ipsilateral TA muscle (iTA) to painful electrical stimulation of the foot, i.e. the flexion reflex (FR), was reduced in standing [5]. Although opposite to each other, the effects of standing on these reflexes were appropriate to the task; i.e., the maintenance of a stable standing position. When the FR stimulation is of sufficient intensity, it can be accompanied by a response in the contralateral extensor muscles named the crossed extension reflex (CER) [6]. A questio~ arises as to whether the influence of body position on the FR and CER excitability is similar or not. For instance, is the modulation of the FR and CER determined by the functional requirement of a specific
* Corresponding author. Aerospace Medical Research Unit, McGill University, 3655 Drummond. Room 1220, Montreal, PQ H3G IY6, Canada. Tel.: + I 514 3986025; fax: + 1 514 3988241 ; c-mail: gsnp~physocc Jan.mcgill.ca. I Current address: Department of Rehabilitation Sciences, Hong Kong Polytechnic University, Hong Kong.
body position? The objective of this study was to compare the effect of sitting and supported stance on the FR and CER. A total of 17 healthy subjects with a mean age (+_SD) of 26 ± 3 years was examined. In the sitting condition, subjects (n = 12) semi-reclined with the knees fixed in a flexed position of about 140 ° and the ankles at about 90 ° . In the standing condition, they (n = 13) stood on a platform with head, shoulders and trunk fixed to a back support by means of straps and canvas, with their neck maintained in the neutral position by a neck collar. In order to prevent the known habituation of the FR with repetitive stimulation [2], a tonic contraction of 10-20% of the maximum voluntary contraction was maintained in the iTA muscle in both conditions. The level of this background contraction was computer-controlled. A train of electrical pulses (1 ms at 200 Hz) of 30 ms duration was given to the right tibial nerve via a surface electrode maintained under pressure behind the medial malleolus, at an intensity of 3-5 times the sensory threshold (group mean 3.9 +_ 1.8 times). The surface EMG activity was recorded in the TA, soleus (SO), and vastus lateralis (VL) muscles on both sides during 500 ms, i.e. 100 ms prior to and 400 ms after the electrical stimulation. The EMG signals were preamplified (gain= 10), amplified (gain = 100), band-pass filtered (20-1400 Hz)
0304-3940/96/$12.00 © I996 Elsevier Science Ireland Ltd. All rights reserved PII: S 0 3 0 4 - 3 9 4 0 ( 9 6 ) 1 2 6 4 9 - 3
216
N. Paquet et al. /Neuroscience Letters 209 (1996) 215-217
63
iTA
It,t8
WL
cSO
to v I
0
100
200
300
400
'
0
100
200
300
400
Time (ms)
Time (ms)
Fig. 1. Mean EMG traces from 6-10 trials in one subject, recorded in the iTA, iVL and cSO muscles during sitting (first column) and standing (second column). Time 0 represents the onset of electrical stimulation. The horizontal line on each trace was drawn to mask the stimulus artifact. The response latency is indicated as the number above the arrows.
and sampled at a frequency of 4 kHz. The activation latency and the offset of muscle responses were defined as the moment the rectified signal exceeded and fell below the mean _ 2 SDs of the mean baseline. Since the iTA FR was present in every subjects and in a majority of trials (see below), the response latency and area were calculated from individual responses for the iTA muscle. These variables were calculated from the averaged response for the other muscles, due to the small number of subjects manifesting these responses (see Fig. 2). The area was calculated between the onset and offset, from which the area of a corresponding segment of the baseline was subtracted. The means were calculated only for the trials showing a reflex. Unpaired Student's t and MannWhitney tests were used to identify significant effects of body position on the dependent variables. Fig. 1 illustrates examples of averaged responses to FR stimulation obtained in the iTA, ipsilateral VL (iVL) and contralateral SO (cSO) muscles of one subject during sitting and supported stance. In the sitting position, this subject manifested only a FR in the iTA muscle. In supported stance, the iTA FR area was smaller than that in sitting by 4%. The FR was accompanied by a response in the iVL muscle and a CER in the cSO muscle. Note that the background activity was similar in the two body positions. The group analysis revealed that in comparison with the sitting position, the mean iTA FR area in supported stance was significantly reduced by 36% (Student's t-test, P < 0.01; 1.21 _0.62/aV/s in sitting versus 0.77 _ 0.47/tV/s in standing). The mean frequency of iTA FR occurrence tended to be lower in supported
stance (73% of trials) than in sitting (86% of trials). The mean iTA FR latency was similar in supported stance (70 + 11 ms) and in sitting (70 + 10 ms). Fig. 2 shows that a similar proportion of subjects manifested a FR in the iTA muscle in the two body posi-
100 90,
80' ~
7o
~
6o
,.
50
~
4o
~
3o
m
~
2o 1o
TA
SO Ipsllateral
VL
TA
SO
VL
contralateral
Fig 2 Proportion of subjects manifesting EMG responses to the electrical stimulation in the ipsilateral and contralateral TA, SO and VL muscles during sitting and standing. The two arrows indicates the largest differences between sitting and standing.
N. Paquet et al. / Neuroscience Letters 209 (1996) 215-217
tions. In contrast, a response in the iVL muscle was evoked in twice as many subjects during supported stance (10/13 subjects) as in :sitting (5/12; P = 0 . 1 1 , Fisher's exact test). Similarly, a CER in the cSO and/or cVL muscle was found in twice as many subjects in supported stance (6/13) than in sitting (3/11). We found that the mean iTA FR area of healthy subjects was significantly sraaller in supported stance than in sitting by 36% (P < 0.01). This indicates that the FR excitability was reduced iF standing. The extent of this decrease, however, was about half the reduction that was found in freely standirtg subjects [1]. This difference could be attributable to the different body support provided in the two experiments. Body support was found to reduce the excitability of lower limb postural responses in standing subjects [4]. Our body support might have attenuated the influence of standing on the FR excitability. As a consequence, the effect of standing on the FR area would be smaller between supported stance and sitting, than between free-standing and sitting. Our main finding is 1-hat the decreased FR excitability in supported stance was accompanied by an enhancement of the extensor muscle ,excitability on both sides. On the ipsilateral side, a response in the iVL muscle was observed in a majority of subjects during supported stance (77%), but only in a mir~ority during sitting (42%). On the contralateral side, a CER in the cSO and/or cVL muscle was also found in twice as many subjects in supported stance than in sitting. Thus, body position modulated the excitability of the FR and extensor responses (which includes the CER) in a reciprocal manner. Since this reciprocal modulation is likely appropriate to ensure a stable standing position, it suggests that the functional demand could dictate the modulation of muscle responses to FR stimulation. In spinal cats walking on a treadmill, the same electrical stimulation of the dorsum of the foot evoked an ipsilateral flexion and contralateral extension of the limb during swing, and an ipsilateral extension during stance
217
[3]. In healthy humans, this 'phase-dependent reflex reversal' was even observed within muscles of the lower limb [7]. These results suggested that the reflex modulation during gait was governed by the alternating supporting task of the lower limb during the gait cycle. In the present experiment, no such reversal in the reflex behavior was observed during the change between sitting and standing. However, we found a meaningful adjustment in FR and extensor response excitability. From a functional point of view, the reduced FR excitability combined with the increased extensor response excitability is likely appropriate to maintain a stable standing position. The authors acknowledge the financial support by the Parkinson's Foundation of Canada and a studentship from the Medical Research Council of Canada to N.P. [1] Allum, J.H.J. and Pfaltz, C.R., Visual and vestibular contribution to pitch sway stabilization in the ankle muscles of normal and patients with bilateral peripheral vestibular deficits, Exp. Brain Res., 58 (1985) 82-94. [2] Chan, C.W.Y. and Tsang, H.H.Y., A quantitative study of flexion reflex in man: relevance to pain research. In H.L. Fields, R. Dubner and F. Cerveno (Eds.), Advances in Pain Research and Therapy, Vol. 9, Raven Press, New York, 1985, pp. 361-369. [3] Forssberg, H., Grillner, S. and Rossignol, S., Phasic gain control of reflexes from the dorsum of the paw during spinal locomotion, Brain Res., 132 (1977) 121-139. [4] Nardone, A., Giordano, A., Corra, T. and Schieppati, M., Responses of leg muscles in humans displaced while standing: effects of types of perturbation and postural set, Brain, 80 (1990) 65-84. [5] Rossi, A. and Decchi, B., Flexibility of lower limb reflex responses to painful cutaneous stimulation in standing humans: evidence of load-dependent modulation, J. Physiol. (London), 481.2 (1994) 521-532. [6] Sherrington, C.S., Flexion reflex of the limb, crossed-extension reflex and reflex stepping and standing, J. Physiol. (London), 40 (1910) 28-121. [7] Yang, J.F. and Stein, R.B., Phase-dependent reflex reversal in human leg muscles during walking, J. Neurophysiol., 63 (1990) 1109-1117.