Brain Research, 582 (1992) 85-93 © 1992 Elsevier Science Publishers B.V. All rights reserved. 0006-8993/92/$05.00
85
BRES 17781
Movement features and H-reflex modulation. II. Passive rotation, movement velocity and single leg movement W.E. Mcllroy, D.F. Collins and J.D. Brooke School of Human Biology and Biophysics Interdepartmental Group, University of Guelph, Guelph, Ont. (Canada) (Accepted 21 January 1992)
Key words: Spinal; Ia; Joint; Leg; Pattern; Contraction
Modulation of soleus H-reflex magnitudes during pedalling, and their approximation when seated with appropriate joint positions and contractile activity was demonstrated in the previous paper. The present study investigated the modulation of H-reflexes during (A) pedalling movement in the absence of contractile activity, (B) different movement velocities and (C) movement of a single limb. Using a customized tandem cycle ergometer, seated subjects with trunk supported relaxed their leg muscles and allowed their legs to be rotated. Their feet were supported on the pedals with the ankle braced. Reflexes were collected at four phases in the movement cycle (with some at 13 phases) and with speeds of 5-60 revolutions per min (cycle times from 12 to 1 s). The results showed that (i) reflex magnitude substantially decreased with limb rotation (P < 0.05). The degree of inhibition was dependent on the phase position. (ii) Increasing speed of passive rotation increased the inhibition at all positions, but was most pronounced near the fullest flexion of hip and knee. When subjects actively pedalled, the relationship between speed and inhibition remained. (iii) When the contralateral leg was moved and the target leg was stationary, crossed projection of reflex inhibition was clear. (iv) The reflex gain measured during active pedalling of one leg was similar to that observed during two legged pedalling. Again, a crossed effect from the contralateral leg could be observed. We conclude that the net influence of discharge from movement-elicited afference is inhibitory on this reflex path and that the reflex modulation during pedalling arises from overlaid sources. From the two papers in this present set of studies, we suggest that tonic inhibition over the whole movement cycle is relieved by overlaid reflex excitation during active pedalling, particularly during the phase when the leg extends. Each component, inhibition and excitation, is multisourced with overlap of effects from peripheral discharge. INTRODUCTION O u r understanding of the specific sources of reflex m o d u l a t i o n , characterized in rhythmic m o v e m e n t s such as walking and pedalling 4'5'6'1°, remains limited. This particular study investigates three factors in an a t t e m p t to detail the source of the m o d u l a t i o n o b s e r v e d during the rhythmic pedalling r e p o r t e d in the preceding p a p e r 5. The three factors investigated included contributions to reflex m o d u l a t i o n arising from (1) muscle contraction, (2) m o v e m e n t velocity and (3) the contralateral limb. Accounting for the source(s) of the m o d u l a t i o n of the H reflex t h r o u g h o u t the cycle of rhythmic m o v e m e n t has focused on the association b e t w e e n peripherally docum e n t e d events and the magnitude of the e v o k e d reflex 46,10. F o r e x a m p l e , the previous p a p e r in this series 5 rep o r t e d that some of the differences b e t w e e n soleus Hreflexes expressed during pedalling, c o m p a r e d to sitting, could be accounted for by differences in the activation level of muscles a r o u n d the ankle joint and the angle of the joints of the leg. In m a n y cases this focus is directed
to the activation of specific muscles and the association to H-reflex modulation. This could easily be extended, from tibialis anterior and soleus, to the numerous muscles activated during such rhythmic lower limb movements. Interestingly enough, the nature of the potential association b e t w e e n muscle contraction and the gain of the H reflex during m o v e m e n t remains speculative. The association with contraction could be the product of changes resulting from the contraction (i.e., array of sensory discharge) or the result of parallel or concomitant control influences arriving with the m o t o r volley. Clearly an i m p o r t a n t question is w h e t h e r the m o d u l a t i o n of soleus H-reflexes is d e p e n d e n t on contraction of those muscles involved in generating the m o v e m e n t . This can be identified by studying m o v e m e n t in the absence of contraction. To test this we c o m p a r e d soleus H-reflex magnitudes when pedalling to those during passive rotation of the limbs through the same range of joint movement. In the latter condition the leg muscles of the subjects were relaxed, and no contraction was o b s e r v e d
Correspondence: J.D. Brooke, The Human Neurophysiology Laboratory, School of Human Biology, University of Guelph, Guelph, Ont., Canada, NIG 2Wl.
86 using e l e c t r o m y o g r a m s ( E M G s ) . T h e m o v e m e n t of stationary p e d a l l i n g is well suited for this type of c o m p a r ison. T h e o b s e r v a t i o n of d e m o n s t r a b l e inhibition t h r o u g h out the p e d a l cycle in the passive c o n d i t i o n led us to c o m p a r e d i f f e r e n t speeds of m o v e m e n t d u r i n g passive r o t a t i o n , to establish w h e t h e r t h e r e was an association b e t w e e n the o b s e r v e d inhibition and the rate of m o v e m e n t . T h e r e are several r e a s o n s for suspecting such an association b e t w e e n
movement
velocity and
H-reflex
m a g n i t u d e . O n e r e a s o n is that the inhibition m a y be the p r o d u c t of sensory discharge associated with the m o v e -
University committee for the ethics of experiments on humans. Details of EMG recording, nerve stimulation and data-processing techniques can be found in the preceding article 5. E x p e r i m e n t 1 - Pedalling versus passive rotation
In Experiment 1, reflexes were evoked at 13 equispaced pedal positions under two conditions. One condition involved normal, 'active', pedalling. The other condition involved 'passive rotation'. During the latter condition the experimental ergometer was connected, in tandem, with a second ergometer. In this way the subjects' limbs were moved, 'passively', throughout the pedal cycle, by a second cyclist. Subjects were requested to remain as relaxed as possible. Subjects wore a clinical brace which immobilised the right ankle at an angle of 90°. Ongoing EMG activity in tibialis anterior and soleus was monitored to ensure there was no activity in these muscles. Four subjects participated in this study.
m e n t ; if so an increase in net inhibition w o u l d be exp e c t e d as the rate of m o v e m e n t increases. This c o u l d be o b s e r v e d o v e r a wide r a n g e of m o v e m e n t velocities. Alt e r n a t e l y , such m o d u l a t i o n m a y be associated with the phase lag o f E M G c o r r e c t i o n s , i n t r o d u c e d by the reflex l o o p delay, which could disrupt o n g o i n g p r o p u l s i v e activity, at high cycle rates TM. T h e results s h o w e d a clear association b e t w e e n the rate of m o v e m e n t and the reflex inhibition. This lead us to c o n d u c t a third e x p e r i m e n t in which we e v a l u a t e d the m o d u l a t i o n of H - r e f l e x e s during d i f f e r e n t speeds of active pedalling. T h e p u r p o s e of this e x p e r i m e n t was to establish w h e t h e r the relationship b e t w e e n limb m o v e m e n t velocity and H - r e f l e x m o d u l a t i o n was m a i n t a i n e d during active m o v e m e n t , despite t h e differences in muscular c o n t r a c t i o n
levels associated
E x p e r i m e n t s 2 a n d 3 - M o v e m e n t velocity
For the subsequent experiments the apparatus was further modified to permit subjects to sit, well supported, in a chair behind the ergometer. This modification was made to reduce any potential effect of postural instability upon the reflex magnitude. Subjects found it very easy to remain relaxed throughout the passive rotation motion when in this position. Reflexes were evoked at four pedal positions; 15, 39, 69 and 92% of the cycle, with zero as topdead-center for the experimental leg. These positions correspond to 55°, 140°, 250° and 330° into the pedal cycle. Four subjects participated in the second experiment. H reflexes were evoked when the subjects (1) sat, (2) actively pedalled at 60 rpm, and (3) had their legs passively rotated at three pedal rates (10, 30, 60 rpm). Data were also collected during passive rotation at 5 rpm in three of the four subjects. During the sitting and passive rotation trials, subjects were instructed to remain relaxed. In experiment three, H reflexes were sampled when subjects were 1) sat and 2) actively pedalling at three speeds (10, 30, 60 rpm). Four more subjects participated in this third experiment.
with the different
m o v e m e n t speeds. T h e p r e s e n t studies limited the m o v e m e n t f u r t h e r by e v a l u a t i n g the c o n t r i b u t i o n to H reflex m o d u l a t i o n m a d e by m o v e m e n t of a single limb. P e d a l l i n g is characteristically g e n e r a t e d as a p a t t e r n of activity f r o m left and right legs. In the l o c o m o t o r g e n e r a t o r of the spinal cat, unilateral stimulation of the dorsal roots o f t e n increases the d u r a t i o n o r intensity of the c o n t r a l a t e r a l , as well as ipsilateral, bursts of fictive l o c o m o t i o n at the v e n t r a l roots 15. M o r e r e c e n t w o r k o n the v e r t e b r a t e p a t t e r n gene r a t o r for s w i m m i n g l o c o m o t i o n has r e v e a l e d p o w e r f u l inhibitory p r o j e c t i o n s t h r o u g h the c o n t r a l a t e r a l inhibitory i n t e r n e u r o n 16. O n e q u e s t i o n naturally arises: is s o m e of the influence o n the soleus H reflex during p e d a l l i n g associated with e v e n t s r e l a t e d to m o v e m e n t of the contralateral limb? In the p r e s e n t study we d e l i m i t e d the p e d a l l i n g m o v e m e n t to a single limb in an a t t e m p t to f u r t h e r isolate the source of the m o d u l a t i o n s e e n during passive and active r o t a t i o n . MATERIALS AND METHODS Twenty-one subjects participated in this study. All subjects were informed volunteers and none reported any history of neuromuscular or metabolic disease. Mean age across all experiments was 24.2 years. The experimental procedures were approved by the
Experiments 4 and 5 - Single limb m o v e m e n t
Four subjects participated in the fourth experiment which investigated reflexes evoked during passive rotation of the limbs under four conditions. The stimulus was delivered at the pedal positions used in Expts. 2 and 3. The four conditions were: 1) sitting; 2) passive rotation of both legs, 3) passive rotation of the target (right) limb with the contralateral limb stationary, and 4) the target limb stationary and the contralateral limb passively rotated. Movement velocity was maintained at 60 rpm. During sitting trials, the target limb was placed in the appropriate crank position for comparison. During one-legged rotation of the contralateral limb, the target limb was fixed in one position for all four phase points. In this position the angles of the hip, knee and ankle were approximately 100°, 110°, and 90°, respectively. An additional trial of control, sitting, reflexes was collected with the target limb in this position, while both limbs were stationary, in three subjects. In all trials subjects remained relaxed. In the fifth experiment data were collected from five subjects at four pedal positions (25, 50, 75 and 100% of the crank cycle) under four conditions. (These crank positions correspond to 90°, 180°, 270°, 360° past top-dead-center.) The same protocol was followed as in Experiment 4 with the exception that limbs were actively pedalled by the subject instead of passively moved. The conditions included: (1) sitting, (2) pedalling, (3) target (right) limb pedalling and the contralateral limb stationary, and (4) the target limb stationary and the contralateral limb pedalling. In the latter trials the stationary limb was placed so that it was 180° out of phase from the active limb at the time of stimulation. When the target limb was stationary subjects matched ankle joint position (and, consequently, knee and hip angle) and ongoing soleus contraction levels to those found at the same positions when pedalling. Pedalling frequency was maintained at 60 rpm and the light power output ranged from 30 to 60 W.
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Fig. 1. The top panel displays the H-reflex magnitudes, expressed as a percent of M response maximum (Mmax), sampled during pedalling and passive rotation trials. The lines represent the averaged H-reflex magnitude measured for 13 crank positions from a single subject (dashed - pedalling, solid - passive rotation). The filled circles represent the average response magnitude across seven subjects for each of four crank positions (15, 39, 69, 92% of the cycle). Standard errors of the mean are displayed. Data points from passive rotation trials are displayed with the lower deviation bar and pedalling averages with the upper deviation bar. The bottom three panels display the average M response (A), and pre-stimulus contraction levels of (B) soleus (SOL) and (C) tibialis anterior (TA) for both pedalling and passive rotation for all 13 crank positions. These are data from the same subject as in part A.
Statistical analysis Average H and M responses, measured peak to peak, were calculated from each block of 20 trials for each subject. These were expressed as a percentage of the maximum M responses which could be recorded (Mmax). In addition, integrated pre-stimulus activity in soleus and tibialis anterior EMGs was averaged over the same trial blocks. Averages from the various crank positions from each subject were used in the analysis, to compare mean responses measured during each of the trial conditions. A 2-way analysis of variance (ANOVA), blocked on subjects, assessed the differences due to crank position, movement condition and the interaction between these factors. Post-hoc multiple comparisons (Scheffe's test) were used to determine the details of the significant differences between mean levels of these factors. Statistical significance was denoted when P _< 0.05.
RESULTS Experiment 1 - Passive rotation versus pedalling o f the lower limbs Data from four subjects from each of Experiments 1 and 2 were used to make the comparison between passive rotation and pedalling at 60 rpm. Four crank posi-
tions, c o m m o n to all subjects (15, 39, 69 and 92% of the cycle), were used in the analysis. O n e subject in Experiment 1 found it difficult to relax soleus muscle during passive rotation and as a result was excluded from the analysis. It is worth noting that the use of the chair in E x p e r i m e n t 2, in place of the cycle ergometer, allowed subjects to relax more easily during passive rotation, since the trunk and head were supported along with lateral m o v e m e n t of the upper leg. The modulation of H-reflexes during active pedalling was similar to that reported previously. It was characterized by larger H-reflexes during the power phase of m o v e m e n t and substantially inhibited responses in the recovery phase. The m e a n magnitude of the peak H-reflex at a crank position of 15% (55 °) was 61.2% Mmax (SE 11.4) averaged over all seven subjects. Fig. 1A displays the average H-reflex magnitude for 13 equispaced crank positions sampled during active pedalling from a single subject. The m e a n H-reflex magnitudes, averaged across all 7 subjects, are displayed for the four crank positions,
88 using filled circles. The upper standard error band is shown. Overall, the H-reflex during active pedalling, averaged across subjects and the four crank positions, was 30.0% Mma x (S.E. 6.8). The H-reflexes sampled during passive rotation are also displayed in Fig. 1A. The solid line displays the average for 13 equispaced crank positions for a single subject. There was clear depression of the H-reflexes across all crank positions. The average H-reflex magnitudes across the 7 subjects, sampled at the four crank positions, are also displayed. Overall, the H-reflex during passive rotation, averaged across subjects and the four crank positions, was 15.2% Mma x (S.E. 4.7). The large magnitude of the responses of one of the seven subjects severely skewed this data set. Accordingly, the data were log transformed for analysis. The subsequent A N O V A revealed that the magnitudes of the H-reflexes sampled during passive rotation were significantly lower than those sampled during active pedalling (Ft, 6 = 8.09, P = 0.03). Specifically, the H-reflexes were significantly smaller during passive rotation at two of the four crank positions which were compared (15 and 39% of the cycle). There was profound inhibition at 69% (250 °) of the cycle in both movement conditions. Mean H-reflexes were 7.6 and 14.9% Mmax for active and passive movement, respectively, at this crank position. These differences in H-reflex magnitude were contrasted by stable M responses across crank positions and between active pedalling and passive rotation. This is displayed for a single subject in Fig. lB. No significant differences were observed in the M response due to crank (F3,1s = 1.47, P = 0.26), or movement condition (F1, 6 = 0.32, P = 0.59). This provided security about the stability of the stimulus intensity delivered to the tibial nerve. There were significant differences in the level of contraction of muscles between the passive rotation and active pedalling. In pedalling, the phasic bursts of activity were, as anticipated, distinguishable between crank positions. In contrast, there was no measurable activation of tibialis anterior or soleus associated with the passive movement alone, as reflected by the EMGs. Fig. 1C and D displays the average pre-stimulus contraction level for soleus and tibialis anterior, respectively, for a single subject. Experiment 2 - H magnitude and movement rate during passive rotation
Changes in movement speed, during passive movement of the limbs, altered the magnitude of the evoked H-reflexes. Four subjects, from Experiment 2, all demonstrated a decreasing H-reflex with higher movement speeds. Overall, there were significant differences be-
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Crank position (% of cycle) Fig. 2. Mean H-reflex magnitudes across the four subjects and three speeds for (A) passive rotation of the legs and (B) active pedalling of the limbs. Also shown are the mean response magnitude when subjects were sitting with the limbs at the same crank positions. All magnitudes are expressed as a percent of M response maximum
(Mmax).
tween the different movement speeds ( F 2 , 6 -~" 126.8, P = 0.0001). Multiple comparisons of means revealed that the largest H-reflex magnitude was associated with the slowest movement speeds and lower H-reflexes with faster speeds. The overall means, across subjects and crank positions, were 51.6% (S.E. 5.9), 22.8% (S.E. 4.8), and 10.0% Mma x ( S . E . 3.0) for 10, 30, and 60 rpm, respectively (Fig. 2A). The change in the magnitude of the H-reflex was approximately linear, with a negative slope, with the change in crank velocity. There were significant differences in the H-reflexes between crank positions (F3, 9 = 6.22, P = 0.01). The effect of the different velocities of rotation varied at the different positions, with reflexes most inhibited at the 92% (330 °) of cycle position. Three subjects were also
89
measured at 5 rpm. The only point to show significant inhibition at this speed, to 42.1% Mmax, (S.E. 5.3), was that for 92% of the cycle. H-reflexes collected when subjects were sat with the limb at similar positions to those during passive pedalling are also displayed in Fig. 2A. The magnitude of the Hreflexes during passive rotation were smaller than those collected during sitting. (The only exceptions were when the H-reflexes sampled at 5 rpm were slightly larger than when sitting, for the crank positions of 15 and 39% of the cycle.) The M responses were not significantly different across crank positions (F3, 9 = 1.34, P = 0.32) or movement speeds (F2, 6 = 0.41, P = 0.68). The average M response, averaged across all trials and subjects, was 16.3% Mma x (S.E. 0.5). The levels of contraction in soleus and tibialis anterior during passive rotation, prior to the stimulus, were also not significantly different across trials and crank positions.
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Experiment 3 - H-magnitude and m o v e m e n t rate during active pedalling The H-reflex changed in magnitude in the third experiment, when the rate of movement of active pedalling altered. The overall means of the H-reflexes were 24.2% (S.E. 3.9) 16.8% (S.E. 4.2) and 10.8% Mmax (S.E. 2.9) for 10, 30 and 60 rpm pedalling rates, respectively (Fig. 2B). These differences, indicating a negative linear relationship between speed and H-reflex magnitude, were significant (F2, 6 = 11.3, P = 0.009). The interaction between crank position and m o v e m e n t speed was also significant (F6,17 -- 9.3, P = 0.0001) revealing the position specific influence of changes in velocity. As before, there was no significant difference between the mean M responses over trials (F2, 6 = 1.94, P = 0.22) or crank positions (F3, 9 = 2.27, P = 0.15). There were, due to the active pedalling, significant differences between the magnitudes of both soleus and tibialis anterior contraction levels over different movement speeds. Generally, the higher the m o v e m e n t speed the higher the level of soleus contraction. This was most evident at crank positions 15 and 39% of the cycle. In contrast, the magnitude of tibialis anterior responses was often larger in the slow movements as opposed to the faster rotations. Experiment 4 - H-magnitude during passive movement o f a single limb Passive rotation of both limbs was also conducted in Experiment 4. The H-reflex observed during passive rotation of both limbs was similar to that demonstrated in Experiment 1. The H-reflexes were significantly lower than those evoked when subjects were sitting at all four
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Fig. 3. A: mean H-reflex magnitudes as a percent of Mmax across all four subjects recorded at four positions around the pedal cycle. Data were recorded during sitting, passive rotation of both legs, passive rotation of the target leg and passive rotation of the contralateral leg. B: H-reflex magnitudes for three subjects recorded from the stationary limb fixed at one position when the contralateral limb was being passively rotated (hatched bars) vs. control reflexes from the same limb when both limbs were relaxed and stationary (filled bars). The standard deviations are also displayed.
crank positions, as Fig. 3A shows. The mean H-reflexes were 10.0 (S.E. 2.9), 4.6 (S.E. 1.2), 5.6 (S.E. 2.3) and 2.8 ( 0 . 9 ) % Mma x for 15, 39, 69 and 92% of the movement cycle, respectively. In contrast, H-reflexes sampled when the subjects sat, with the limb positioned at these crank positions were 54.5 (S.E. 3.0), 59.2 (S.E. 5.2), 72.3 (S.E. 3.2) and 57.8 (S.E. 6.2) % of M . . . . respectively. During the passive movement of both legs, the M waves were not significantly different across the crank positions. The H-reflexes sampled when only the target limb was being passively rotated were also strongly inhibited. These H-reflexes were not significantly different from Hreflexes sampled when both legs were rotated. The mean
90 sponses were constant for the target limb. In all three subjects, for whom means and standard deviations are displayed, the differences between these two conditions were significant. This clearly highlights the inhibitory contribution made by the moving contralateral limb, not confounded by differences in events occurring at the target leg. In all trials the M responses were stable across phase positions. The global average of M response magnitude was 15.4 % Mma x ( S . E . 1.6) averaged across all subjects, trials and phase positions. During these passive movement trials little or no activity was recorded from soleus or tibialis anterior.
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Fig. 4. Mean data across all five subjects for (A) H-reflex magnitudes as a percent of Mmaxand pre-stimulus contraction levels as a percent of MVC for (B) tibialis anterior and (C) soleus EMG activity recorded at four positions around the pedal cycle. Data were recorded during sitting, normal pedalling (both legs) and onelegged pedalling when the target limb was stationary (contralateral leg) and moving (target leg).
responses were 7.9 (S:E. 2.3), 6.5 (S.E. 1.8), 5.0 (S.E. 2.2) and 2.7 (S.E. 0.6) % Mma x averaged across subjects, for crank positions of 15, 39, 69 and 92% of the cycle (Fig. 3A). H-reflexes evoked in the target limb (right leg) when it was stationary, and when, at the same time, the contralateral limb was passively rotated, were significantly lower than those evoked when subjects were sitting with both legs stationary (Fig. 3A). However, they were significantly higher than those evoked when both legs or the target leg were passively rotated. The mean values, averaged across subjects, were 33.9 (S.E. 8.1), 33.4 (S.E. 7.6), 30.2 (S.E. 5.4) and 33.8 (S.E. 7.1) % Mmax for each of the four crank positions. As mentioned, these H-reflexes fell in-between those evoked during sitting and those from passive rotation trials involving both legs. In the above comparisons, the limb was adjusted to the appropriate crank position for the sitting trials. Fig. 3B shows H-reflex amplitudes when the target leg was kept in a fixed position, for the comparison of sitting versus the contralateral leg being passively rotated. The differences between these trials could only be accounted for by differences in the events associated with the contralateral limb since limb position, contraction and M re-
H-reflexes evoked during active rotation with both limbs were similar to those documented in the previous studies 5. The H-responses were large in the power producing phase and inhibited in the recovery phase. The mean H-reflexes, averaged across subjects, were 69.4 (S.E. 15.4), 15.2 (S.E. 5.3), 2.6 (S.E. 0.3) and 44.0 (S.E. 11.2)% Mma x for 25, 50, 75 and 100% of the cycle respectively (Fig. 4A). The H-reflexes sampled during sitting significantly differed across crank positions. This modulation was anticipated since the contraction of soleus was matched to the contraction at each phase point during active pedalling. The average H-reflex magnitudes are displayed in Fig. 3A. The mean H-reflexes sampled during sitting were 85.0 (S.E. 7.2), 78.5 (S.E. 4.8), 52.5 (S.E. 11.7) and 45.9 (S.E. 14.4) % mmax for the four crank positions, respectively. There were no significant differences in the magnitudes of the H-reflex between one legged pedalling with the target limb and two legged pedalling. The magnitude of the H-reflexes, during pedalling of the target limb, were 77.8 (S.E. 10.6), 10.0 (S.E. 4.9), 2.2 (S.E. 0.5) and 28.9 (S.E. 4.5) % M .... for 25, 50, 75 and 100% of the cycle, respectively. This contrasted the differences observed between two legged pedalling and one legged pedalling with the contralateral limb. Fig. 3A displays the mean H-reflexes measured at each of the four crank positions (note that 0 and 100% are the same data point). When the contralateral limb actively pedalled, while the target limb was stationary, there was significant modulation of the H-reflex, across phase positions. The mean H-reflex magnitude was 83.6 (S.E. 6.7), 46.2 (S.E. 11.4), 25.0 (S.E. 8.6), and 19.7 (S.E. 5.2) % Mma x for the target limb placed at 25, 50, 75 and 100% of the crank cycle, respectively. The H-reflexes sampled at 50% (180 °) and 75% (270 °) of the cycle were both significantly lower than sitting and significantly higher than pedalling with both legs or the target leg. In contrast data sampled at
91 25% (90 °) and 100% (360 °) of the cycle were similar between these movement conditions. The H-reflexes from contralateral limb movement fell between sitting and double leg movement and this was similar to that observed when the limbs were moved passively. The results of the two experiments were also similar in that the responses seen during movement of the single target limb matched those seen with movement of both limbs. In all trials the M responses were stable across phase positions. The global average of M response magnitude was 16.4 % Mmax (S.E. 1.7) averaged across all subjects, trials and phase positions. When the target limb was actively pedalling (1 or 2 legged) the E M G activity of tibialis and soleus anterior, summarized in Fig. 4B and 4C, was characteristic of normal pedalling. During pedalling with only the contralateral limb the magnitude of soleus contraction in the target limb was matched to active pedalling with both legs, while the activity for tibialis anterior was not matched. DISCUSSION The present results confirm those in the previous paper in this journal, identifying extensive modulation of soleus H-reflexes during a cycle of pedalling, compared to control reflexes when sitting 3'5. The first paper reported that some of this movement modulation may be accounted for by activation of the muscles around the ankle. The present paper addressed three factors: the role of (1) movement contraction, (2) movement velocity and (3) the contralateral limb on the modulation of H-response during rhythmic movement of the legs. To the first question, 'is the reflex modulated in the absence of the muscular activity to drive the limbs', the unequivocal answer is 'yes'. The movement of passive rotation at 60 rpm elicits substantial modulation, with a predominance of reflex inhibition when compared to seated responses. In addition, there was occasionally a modest increase in reflex gain in the extension phase of passive rotation, similar in time to that observed for active rotation. To the second question, 'is reflex modulation related to the velocity of limb movement?', the answer again is 'yes'. The approximately linear relationship between the extent of the inhibition and the speed of movement is support for the idea that movement-induced sensory discharge underlies the inhibition. Such a relationship suggests a relatively simple transformation of sensory inputs into changes in reflex gain. Further, the effect appearing at very low speeds implies that the inhibition may require only modest levels of such discharge for it to appear. We have no direct information as to the sensory
modalities involved. There is obvious opportunity for contributions from haptic, joint and muscle mechanoreceptors. The net influence of discharge from these sensory receptors during physical movement of the limbs is expressed as inhibition on the Ia spinal route to this autogenic muscle. The presence of reflex inhibition in the recovery phase at very low speeds (cycle time 12 s) allows us to reject the view that the reflex is suppressed because the reflex loop delay would lead to a disruptive phase lag in E M G corrections at high speeds TM. The answer to the third question, 'can modulation arise from movement of the contralateral limb?', is also 'yes'. Two interesting new findings arise: (1) reflex modulation in the moving leg is the same whether subjects move only the target leg or move both legs, and (2) the movement of the contralateral limb leads to clear changes in response magnitudes in the stationary target limb (these responses lie in-between those evoked during sitting and those occurring with movement of both legs). Clearly, the bilateral nature of the movement was not necessary for the modulation of the reflex to be fully expressed. This is consistent with the similarity between reflex modulations observed in the moving limb during one and two legged walking 1°. One could conclude, as Crenna and Frigo 1° did, that there was no contralateral effect on the reflex modulation. However, contralateral effects, primarily inhibition, are present. (The reflex excitation in the stationary leg at 25% (90 °) past top-deadcenter (Fig. 4B), during active pedalling by the other leg, reflects also the contraction of soleus muscle in the stationary leg at that particular position. Thus, the reflex excitation should not be attributed simply to a contralateral influence.) The reflex inhibition from the contralateral limb was less powerful than that from the ipsilateral one alone. It is possible that effects of limb movement from passively moving limbs are additive and that those from the target limb have a greater weighting than those from the contralateral. This would account for the observation that H-reflexes from contralateral limb movement were intermediary between those when sitting and those when the target leg was rotated. The lack of difference in inhibition observed between movement of the target leg or both legs may be the result of an inability to observe further inhibitory effects rather than an absence of any contralateral effect. Use of E M G to estimate the integrity of this spinal reflex limits one's ability to estimate the 'true' inhibitory influence. It would be possible to increase the inhibitory drive, pre- or postsynaptically, beyond that necessary to suppress H-reflexes. A substantial part of this study characterized the Hreflex modulation during passive rotation of the limbs. Technical deficiencies are not the cause of the observed
92 modulation of H reflexes during these trials. There was control of limb position when sitting, and of stimulus constancy, throughout the experiment. There was control of sitting support, to remove any descending influences due to postural instability 1. The latter was a possibility for trials which were run with subjects seated on the ergometer. However, the revised apparatus, from which the majority of the data were collected, provided ample stability to allow the subject to relax completely. As a further confirmation of experimental control, we note that the reflex modulations were consistently observed in all subjects. An important observation is that the reflex inhibition, with passive rotation of the limb, is not uniform across the cycle. In the extension phase for the leg, there is a partial release of inhibition. Also, when it is modestly expressed at lower speeds, it is strongest at one phase in the cycle, the final part of recovery of the leg. These are not effects associated with contractile activity in the leg muscles. If, as we suspect, the inhibition of passive rotation arises from movement-related sensory discharge, then this may connect to differential discharge rates of involved receptors over the movement cycle. The inhibition appears most during the flexion phase for hip and knee, peaking close to the fullest flexion that occurs. (The ankle was braced against movement.) We do not know whether such modulation arises from changing discharge of receptors and/or selective gating through membrane changes in spinal neurons. For instance, for the latter, a potent role exists for hip joint receptors to reset the central pattern generated in the locomotor activity of the spinal cat 2. It is possible that the use of the ankle brace led to differential discharge of cutaneous receptors which may have influenced H-reflex modulation. We think that any contribution specific to the use of the brace is likely limited. This is based on similarities between active pedalling with and without the brace. It is also based on similarities in the recovery phase of active pedalling without the brace and passive rotation with the brace. Movement depression of H-reflexes has been attributed to inhibition which occurs before the motoneuronal soma and proximal dendrites 4'6 and which is probably presynaptic on the Ia afferent 9. It may be that such inhibition accounts for the depression of H-reflexes that we see over the movement as a whole. We did not set out to separate pre- and postsynaptic inhibitory effects. It is possible that modulation of H-reflex magnitude, during passive rotation or in the recovery phase of active movement, may be partly accounted for by subthreshold changes at the motoneuron. The only evidence we have for favouring the presynaptic source, is that such profound inhibition proved impossible to achieve
using post-synaptic inhibition of motoneurons during tictive locomotion in the decerebrate cat 9 or through manipulating a computer model of the human motoneuron 7. It is reassuring that the both the velocity dependent modulation and the contralateral effects seen during passive rotation were evident during active pedalling. This gives us some security that the influences seen in the passive rotation are contributing to the H-reflex modulation during active pedalling. The period of inhibition in the recovery phase of both movements may share similar origins. The modest increase in gain during the power phase of passive movement arises from a source independent of the muscular activity to move the limbs. The increased gain during active pedalling may arise in part from a common source leading to this contraction independent modulation. Additional increases in gain during active pedalling may arise from contraction-related facilitation of the m o t o n e u r o n a l pool 19'22. It does appear that the soleus contraction is necessary to promote the full increase in the magnitude of H-reflexes observed during the power (extension) phase of normal pedalling. Depression of reflex magnitude to near zero in the recovery phase of passive rotation demonstrates that neither the inhibitory effect of reciprocal inhibition from the tibialis anterior contraction T M nor of ankle dorsiflexion H'21, are required to obtain this effect. (Recall that the ankle was braced in the present experiments.) This is not to say that these movement features cannot contribute to modulation. Rather, that they are not essential for the observed reflex inhibition. We propose that there are complementary sources of movement-induced modulation of soleus H-reflexes during pedalling. These sources might sum to a greater effect on the muscle than that seen in the target E M G during normal pedalling. As an example, inhibition of the reflex is profound when only one leg is passively moved, even with ankle movement prevented. Yet, significant inhibition also arises from movement of the contralateral leg. Further, contraction of the ipsilateral tibialis anterior muscle, which contraction occurs in normal pedalling during the phase when the H-reflex is inhibited, substantially inhibits the reflex4. Clearly occlusion of neuronal pools could be occurring during normal pedalling. The lack of further inhibition, e.g., compared to passive single-leg activity, likely reflects an inability to measure further increases in suppression of the reflex at the level of the EMG. We suspect that occlusion occurs for some tasks. For other tasks the complementary sources of inhibition may be additive in their effect. In yet others the inhibition may arise from only a subset of sources. We propose that the physical movement of the limb
93 lays down the most basic, tonic, inhibition on the gain of the target reflex pathway. The inhibition can arise from slow m o v e m e n t of the single limb with b r a c e d ankle, in the absence of contraction of any muscles of the leg. This tonic inhibition seems related to the n u m b e r of involved sensory endings, for there is inhibition from the single leg alone and further inhibition from the contralateral one. It also seems related to the rate of discharge of those endings; the inhibition increases as the velocity of m o v e m e n t increases from a very low level. We consider that the inputs leading to this inhibition vary over the m o v e m e n t cycle, thus accounting for the differential attenuation of the H-reflex magnitude during changes in velocity of rotation. We expect that the o b s e r v e d increase in reflex gain during the p o w e r phase of active pedalling is the net o u t c o m e of the interaction of the inhibitory and facilitatory influences at the spinal neuronal pools. This interaction at times m a y obscure the measurable relationship b e t w e e n soleus contraction and the magnitude of the H-reflex. This could account for the suggestion that H-reflexes in walking are not directly associated with the level of contraction 8. M o v e m e n t of the ankle joint and the effects from contraction of o t h e r muscles of the leg, including h e t e r o n y m o u s projections 2°, must be a d d e d to these sources of excitatory modulation. T h e r e likely are o t h e r significant p e r i p h e r a l sources of
m o d u l a t i o n , not yet explicated 12. The whole represents an overlapping array of m o d u l a t o r y inputs from features of the m o v e m e n t . In some instances it can be shown that these arise from peripheral r e c e p t o r discharge and in others this is suspected. T h e r e has been interest in identifying central features of tasks, which features are also likely associated with the m o d u l a t i o n of H-reflexes. It is possible that such central features, perhaps in parallel with descending motor volleys, are i m p o r t a n t in defining the increase in excitability during the power-producing phase of the movement 8. Llewellyn et al. 17 have suggested that task difficulty is important. D y h r e - P o u l s e n et al. 13 have also suggested that the type of task, hopping versus landing from a jump, m a y be important. The present work exposes the consequences of events from the m o v e m e n t itself. In the light of this work, we conclude that one should only invoke a central descending source for reflex m o d u l a t i o n during m o v e m e n t after strict enquiry has been m a d e about the effects that are arising from the peripheral receptor sources associated with the movement itself.
REFERENCES
J. Physiol., 416 (1989) 255-272. 12 Dietz, V., Trippel, M., Discher, M., Horstmann, G.A., Compensation of h.uman stance perturbations: selection of the appropriate electromyographic pattern. Neurosci. Lett., 126 (1991) 71-74. 13 Dyhre-Poulson, P., Simomsen, E.B., Voigt, M., Dynamic control of muscle stiffness and H reflex modulation during hopping and jumping in man, J. Physiol., 437 (1991) 287-304. 14 Grillner, S., Muscle stiffness and motor control-forces in the ankle during locomotion and standing. In A.A. Gydikov, N.T. Tankov, D.S., Kosarov (Eds.), Motor Control, Plenum, New York, 1973, pp. 195-215. 15 Grillner, S,, Zangger, P., On the central generation of locomotion in the low spinal cat, Exp. Brain Res., 34 (1979) 241-261. 16 Grillner, S., Buchanan, J.T., Lansner, A,, Simulation of the segmental burst generating network for locomotion in lamprey, Neurosci. Lett., 89 (1988) 31-35. 17 Llewellyn, M., Yang, J.E, Prochazka, A., Human H-reflexes are smaller in difficult beam walking than in normal treadmill walkin, Exp. Brain Res., 83 (1990) 22-28. 18 Meunier, S., Morin, C., Changes in presynaptic inhibition of Ia fibres during voluntary dorsiflexion of the foot, Exp. Brain Res., 76 (1989) 510-518. 19 Paillard, J., R~flexes et rdgulations d' origine proprioceptive chez l'homme, Arnette, Paris. 20 Pierrot-Deseilligny, E., Morin, C., Bergego, C., Tankov, N., Pattern of group I fibre projections from ankle flexor and extensor muscles in man, Exp. Brain Res., 42 (1981) 337-350. 21 Romano, C., Schieppati, M., Reflex excitability of human soleus motoneurons during voluntary shortening or lengthening contractions, J. Physiol., 390 (1987) 271-284. 22 Verrier, M.C., Alterations in H reflex magnitude by variations in baseline EMG excitability, Electroencephalogr. Clin. Neurophysiol., 60 (1985) 492-499.
1 Allum J.H.J., Organization of stabilizing reflex responses in fibialis anterior muscles following ankle flexion perturbations of standing man, Brain Res., 264 (1983) 297-301. 2 Andersson O., Grillner, S., Peripheral control of the cats step cycle. II. Entrainment of the central pattern generators for locomotion by sinusoidal hip movements during 'fictive locomotion', Acta Physiol. Scand., 118 (1983) 229-239. 3 Boorman, G.I., Becker, W.J., Lee, R.G., Modulation of the H-reflex during stationary cycling in normal humans and patients with spinal spasticity, Neurosci. Abstr., 15 (1989) 691. 4 Brooke, J.D., Collins, D.E, Boucher, S., McIlroy, W.E., Modulation of human short latency reflexes between standing and walking, Brain Res., 548 (1991) 172-178. 5 Brooke, J.D. McIlroy, W.E., Collins, D.E Movement features and H reflex modulation. I. Pedalling versus matched controls, Brain Res., 582 (1992) 78-84. 6 Capaday, C., Stein, R.B., Amplitude modulation of the soleus H reflex in the human during walking and standing. J. Neurosci., 6 (5) (1986) 1308-1313. 7 Capaday, C., Stein, R.B., A method for the simulation of the reflex output of a motoneurone pool. J. Neurosci. Methods, 21 (1987) 91-104. 8 Capaday, C., Stein, R.B., Difference in the amplitude of the human soleus H reflex during walking and running. J. Physiol., 392 (1987) 513-522. 9 Capaday, C., Stein, R.B., The effects of post-synaptic inhibition on the monosynaptic reflex of the cat at different levels of motoneuron pool activity. Exp. Brain Res., 77 (1989) 577-584. 10 Crenna, P., Frigo, C., Excitability of the soleus H reflex arc during walking and stepping in man, Exp. Brain Res., 66 (1987) 49-60. 11 Crone, C., Nielson, J., Spinal mechanisms in man contributing to reciprocal inhibition during voluntary dorsiflexion of the foot,
Acknowledgements. We appreciate the technical support of J. Hoare. This work was supported by a Grant from the Natural Sciences and Engineering Research Council of Canada No. A0025.
85
BRES 17781
Movement features and H-reflex modulation. II. Passive rotation, movement velocity and single leg movement W.E. Mcllroy, D.F. Collins and J.D. Brooke School of Human Biology and Biophysics Interdepartmental Group, University of Guelph, Guelph, Ont. (Canada) (Accepted 21 January 1992)
Key words: Spinal; Ia; Joint; Leg; Pattern; Contraction
Modulation of soleus H-reflex magnitudes during pedalling, and their approximation when seated with appropriate joint positions and contractile activity was demonstrated in the previous paper. The present study investigated the modulation of H-reflexes during (A) pedalling movement in the absence of contractile activity, (B) different movement velocities and (C) movement of a single limb. Using a customized tandem cycle ergometer, seated subjects with trunk supported relaxed their leg muscles and allowed their legs to be rotated. Their feet were supported on the pedals with the ankle braced. Reflexes were collected at four phases in the movement cycle (with some at 13 phases) and with speeds of 5-60 revolutions per min (cycle times from 12 to 1 s). The results showed that (i) reflex magnitude substantially decreased with limb rotation (P < 0.05). The degree of inhibition was dependent on the phase position. (ii) Increasing speed of passive rotation increased the inhibition at all positions, but was most pronounced near the fullest flexion of hip and knee. When subjects actively pedalled, the relationship between speed and inhibition remained. (iii) When the contralateral leg was moved and the target leg was stationary, crossed projection of reflex inhibition was clear. (iv) The reflex gain measured during active pedalling of one leg was similar to that observed during two legged pedalling. Again, a crossed effect from the contralateral leg could be observed. We conclude that the net influence of discharge from movement-elicited afference is inhibitory on this reflex path and that the reflex modulation during pedalling arises from overlaid sources. From the two papers in this present set of studies, we suggest that tonic inhibition over the whole movement cycle is relieved by overlaid reflex excitation during active pedalling, particularly during the phase when the leg extends. Each component, inhibition and excitation, is multisourced with overlap of effects from peripheral discharge. INTRODUCTION O u r understanding of the specific sources of reflex m o d u l a t i o n , characterized in rhythmic m o v e m e n t s such as walking and pedalling 4'5'6'1°, remains limited. This particular study investigates three factors in an a t t e m p t to detail the source of the m o d u l a t i o n o b s e r v e d during the rhythmic pedalling r e p o r t e d in the preceding p a p e r 5. The three factors investigated included contributions to reflex m o d u l a t i o n arising from (1) muscle contraction, (2) m o v e m e n t velocity and (3) the contralateral limb. Accounting for the source(s) of the m o d u l a t i o n of the H reflex t h r o u g h o u t the cycle of rhythmic m o v e m e n t has focused on the association b e t w e e n peripherally docum e n t e d events and the magnitude of the e v o k e d reflex 46,10. F o r e x a m p l e , the previous p a p e r in this series 5 rep o r t e d that some of the differences b e t w e e n soleus Hreflexes expressed during pedalling, c o m p a r e d to sitting, could be accounted for by differences in the activation level of muscles a r o u n d the ankle joint and the angle of the joints of the leg. In m a n y cases this focus is directed
to the activation of specific muscles and the association to H-reflex modulation. This could easily be extended, from tibialis anterior and soleus, to the numerous muscles activated during such rhythmic lower limb movements. Interestingly enough, the nature of the potential association b e t w e e n muscle contraction and the gain of the H reflex during m o v e m e n t remains speculative. The association with contraction could be the product of changes resulting from the contraction (i.e., array of sensory discharge) or the result of parallel or concomitant control influences arriving with the m o t o r volley. Clearly an i m p o r t a n t question is w h e t h e r the m o d u l a t i o n of soleus H-reflexes is d e p e n d e n t on contraction of those muscles involved in generating the m o v e m e n t . This can be identified by studying m o v e m e n t in the absence of contraction. To test this we c o m p a r e d soleus H-reflex magnitudes when pedalling to those during passive rotation of the limbs through the same range of joint movement. In the latter condition the leg muscles of the subjects were relaxed, and no contraction was o b s e r v e d
Correspondence: J.D. Brooke, The Human Neurophysiology Laboratory, School of Human Biology, University of Guelph, Guelph, Ont., Canada, NIG 2Wl.
86 using e l e c t r o m y o g r a m s ( E M G s ) . T h e m o v e m e n t of stationary p e d a l l i n g is well suited for this type of c o m p a r ison. T h e o b s e r v a t i o n of d e m o n s t r a b l e inhibition t h r o u g h out the p e d a l cycle in the passive c o n d i t i o n led us to c o m p a r e d i f f e r e n t speeds of m o v e m e n t d u r i n g passive r o t a t i o n , to establish w h e t h e r t h e r e was an association b e t w e e n the o b s e r v e d inhibition and the rate of m o v e m e n t . T h e r e are several r e a s o n s for suspecting such an association b e t w e e n
movement
velocity and
H-reflex
m a g n i t u d e . O n e r e a s o n is that the inhibition m a y be the p r o d u c t of sensory discharge associated with the m o v e -
University committee for the ethics of experiments on humans. Details of EMG recording, nerve stimulation and data-processing techniques can be found in the preceding article 5. E x p e r i m e n t 1 - Pedalling versus passive rotation
In Experiment 1, reflexes were evoked at 13 equispaced pedal positions under two conditions. One condition involved normal, 'active', pedalling. The other condition involved 'passive rotation'. During the latter condition the experimental ergometer was connected, in tandem, with a second ergometer. In this way the subjects' limbs were moved, 'passively', throughout the pedal cycle, by a second cyclist. Subjects were requested to remain as relaxed as possible. Subjects wore a clinical brace which immobilised the right ankle at an angle of 90°. Ongoing EMG activity in tibialis anterior and soleus was monitored to ensure there was no activity in these muscles. Four subjects participated in this study.
m e n t ; if so an increase in net inhibition w o u l d be exp e c t e d as the rate of m o v e m e n t increases. This c o u l d be o b s e r v e d o v e r a wide r a n g e of m o v e m e n t velocities. Alt e r n a t e l y , such m o d u l a t i o n m a y be associated with the phase lag o f E M G c o r r e c t i o n s , i n t r o d u c e d by the reflex l o o p delay, which could disrupt o n g o i n g p r o p u l s i v e activity, at high cycle rates TM. T h e results s h o w e d a clear association b e t w e e n the rate of m o v e m e n t and the reflex inhibition. This lead us to c o n d u c t a third e x p e r i m e n t in which we e v a l u a t e d the m o d u l a t i o n of H - r e f l e x e s during d i f f e r e n t speeds of active pedalling. T h e p u r p o s e of this e x p e r i m e n t was to establish w h e t h e r the relationship b e t w e e n limb m o v e m e n t velocity and H - r e f l e x m o d u l a t i o n was m a i n t a i n e d during active m o v e m e n t , despite t h e differences in muscular c o n t r a c t i o n
levels associated
E x p e r i m e n t s 2 a n d 3 - M o v e m e n t velocity
For the subsequent experiments the apparatus was further modified to permit subjects to sit, well supported, in a chair behind the ergometer. This modification was made to reduce any potential effect of postural instability upon the reflex magnitude. Subjects found it very easy to remain relaxed throughout the passive rotation motion when in this position. Reflexes were evoked at four pedal positions; 15, 39, 69 and 92% of the cycle, with zero as topdead-center for the experimental leg. These positions correspond to 55°, 140°, 250° and 330° into the pedal cycle. Four subjects participated in the second experiment. H reflexes were evoked when the subjects (1) sat, (2) actively pedalled at 60 rpm, and (3) had their legs passively rotated at three pedal rates (10, 30, 60 rpm). Data were also collected during passive rotation at 5 rpm in three of the four subjects. During the sitting and passive rotation trials, subjects were instructed to remain relaxed. In experiment three, H reflexes were sampled when subjects were 1) sat and 2) actively pedalling at three speeds (10, 30, 60 rpm). Four more subjects participated in this third experiment.
with the different
m o v e m e n t speeds. T h e p r e s e n t studies limited the m o v e m e n t f u r t h e r by e v a l u a t i n g the c o n t r i b u t i o n to H reflex m o d u l a t i o n m a d e by m o v e m e n t of a single limb. P e d a l l i n g is characteristically g e n e r a t e d as a p a t t e r n of activity f r o m left and right legs. In the l o c o m o t o r g e n e r a t o r of the spinal cat, unilateral stimulation of the dorsal roots o f t e n increases the d u r a t i o n o r intensity of the c o n t r a l a t e r a l , as well as ipsilateral, bursts of fictive l o c o m o t i o n at the v e n t r a l roots 15. M o r e r e c e n t w o r k o n the v e r t e b r a t e p a t t e r n gene r a t o r for s w i m m i n g l o c o m o t i o n has r e v e a l e d p o w e r f u l inhibitory p r o j e c t i o n s t h r o u g h the c o n t r a l a t e r a l inhibitory i n t e r n e u r o n 16. O n e q u e s t i o n naturally arises: is s o m e of the influence o n the soleus H reflex during p e d a l l i n g associated with e v e n t s r e l a t e d to m o v e m e n t of the contralateral limb? In the p r e s e n t study we d e l i m i t e d the p e d a l l i n g m o v e m e n t to a single limb in an a t t e m p t to f u r t h e r isolate the source of the m o d u l a t i o n s e e n during passive and active r o t a t i o n . MATERIALS AND METHODS Twenty-one subjects participated in this study. All subjects were informed volunteers and none reported any history of neuromuscular or metabolic disease. Mean age across all experiments was 24.2 years. The experimental procedures were approved by the
Experiments 4 and 5 - Single limb m o v e m e n t
Four subjects participated in the fourth experiment which investigated reflexes evoked during passive rotation of the limbs under four conditions. The stimulus was delivered at the pedal positions used in Expts. 2 and 3. The four conditions were: 1) sitting; 2) passive rotation of both legs, 3) passive rotation of the target (right) limb with the contralateral limb stationary, and 4) the target limb stationary and the contralateral limb passively rotated. Movement velocity was maintained at 60 rpm. During sitting trials, the target limb was placed in the appropriate crank position for comparison. During one-legged rotation of the contralateral limb, the target limb was fixed in one position for all four phase points. In this position the angles of the hip, knee and ankle were approximately 100°, 110°, and 90°, respectively. An additional trial of control, sitting, reflexes was collected with the target limb in this position, while both limbs were stationary, in three subjects. In all trials subjects remained relaxed. In the fifth experiment data were collected from five subjects at four pedal positions (25, 50, 75 and 100% of the crank cycle) under four conditions. (These crank positions correspond to 90°, 180°, 270°, 360° past top-dead-center.) The same protocol was followed as in Experiment 4 with the exception that limbs were actively pedalled by the subject instead of passively moved. The conditions included: (1) sitting, (2) pedalling, (3) target (right) limb pedalling and the contralateral limb stationary, and (4) the target limb stationary and the contralateral limb pedalling. In the latter trials the stationary limb was placed so that it was 180° out of phase from the active limb at the time of stimulation. When the target limb was stationary subjects matched ankle joint position (and, consequently, knee and hip angle) and ongoing soleus contraction levels to those found at the same positions when pedalling. Pedalling frequency was maintained at 60 rpm and the light power output ranged from 30 to 60 W.
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Fig. 1. The top panel displays the H-reflex magnitudes, expressed as a percent of M response maximum (Mmax), sampled during pedalling and passive rotation trials. The lines represent the averaged H-reflex magnitude measured for 13 crank positions from a single subject (dashed - pedalling, solid - passive rotation). The filled circles represent the average response magnitude across seven subjects for each of four crank positions (15, 39, 69, 92% of the cycle). Standard errors of the mean are displayed. Data points from passive rotation trials are displayed with the lower deviation bar and pedalling averages with the upper deviation bar. The bottom three panels display the average M response (A), and pre-stimulus contraction levels of (B) soleus (SOL) and (C) tibialis anterior (TA) for both pedalling and passive rotation for all 13 crank positions. These are data from the same subject as in part A.
Statistical analysis Average H and M responses, measured peak to peak, were calculated from each block of 20 trials for each subject. These were expressed as a percentage of the maximum M responses which could be recorded (Mmax). In addition, integrated pre-stimulus activity in soleus and tibialis anterior EMGs was averaged over the same trial blocks. Averages from the various crank positions from each subject were used in the analysis, to compare mean responses measured during each of the trial conditions. A 2-way analysis of variance (ANOVA), blocked on subjects, assessed the differences due to crank position, movement condition and the interaction between these factors. Post-hoc multiple comparisons (Scheffe's test) were used to determine the details of the significant differences between mean levels of these factors. Statistical significance was denoted when P _< 0.05.
RESULTS Experiment 1 - Passive rotation versus pedalling o f the lower limbs Data from four subjects from each of Experiments 1 and 2 were used to make the comparison between passive rotation and pedalling at 60 rpm. Four crank posi-
tions, c o m m o n to all subjects (15, 39, 69 and 92% of the cycle), were used in the analysis. O n e subject in Experiment 1 found it difficult to relax soleus muscle during passive rotation and as a result was excluded from the analysis. It is worth noting that the use of the chair in E x p e r i m e n t 2, in place of the cycle ergometer, allowed subjects to relax more easily during passive rotation, since the trunk and head were supported along with lateral m o v e m e n t of the upper leg. The modulation of H-reflexes during active pedalling was similar to that reported previously. It was characterized by larger H-reflexes during the power phase of m o v e m e n t and substantially inhibited responses in the recovery phase. The m e a n magnitude of the peak H-reflex at a crank position of 15% (55 °) was 61.2% Mmax (SE 11.4) averaged over all seven subjects. Fig. 1A displays the average H-reflex magnitude for 13 equispaced crank positions sampled during active pedalling from a single subject. The m e a n H-reflex magnitudes, averaged across all 7 subjects, are displayed for the four crank positions,
88 using filled circles. The upper standard error band is shown. Overall, the H-reflex during active pedalling, averaged across subjects and the four crank positions, was 30.0% Mma x (S.E. 6.8). The H-reflexes sampled during passive rotation are also displayed in Fig. 1A. The solid line displays the average for 13 equispaced crank positions for a single subject. There was clear depression of the H-reflexes across all crank positions. The average H-reflex magnitudes across the 7 subjects, sampled at the four crank positions, are also displayed. Overall, the H-reflex during passive rotation, averaged across subjects and the four crank positions, was 15.2% Mma x (S.E. 4.7). The large magnitude of the responses of one of the seven subjects severely skewed this data set. Accordingly, the data were log transformed for analysis. The subsequent A N O V A revealed that the magnitudes of the H-reflexes sampled during passive rotation were significantly lower than those sampled during active pedalling (Ft, 6 = 8.09, P = 0.03). Specifically, the H-reflexes were significantly smaller during passive rotation at two of the four crank positions which were compared (15 and 39% of the cycle). There was profound inhibition at 69% (250 °) of the cycle in both movement conditions. Mean H-reflexes were 7.6 and 14.9% Mmax for active and passive movement, respectively, at this crank position. These differences in H-reflex magnitude were contrasted by stable M responses across crank positions and between active pedalling and passive rotation. This is displayed for a single subject in Fig. lB. No significant differences were observed in the M response due to crank (F3,1s = 1.47, P = 0.26), or movement condition (F1, 6 = 0.32, P = 0.59). This provided security about the stability of the stimulus intensity delivered to the tibial nerve. There were significant differences in the level of contraction of muscles between the passive rotation and active pedalling. In pedalling, the phasic bursts of activity were, as anticipated, distinguishable between crank positions. In contrast, there was no measurable activation of tibialis anterior or soleus associated with the passive movement alone, as reflected by the EMGs. Fig. 1C and D displays the average pre-stimulus contraction level for soleus and tibialis anterior, respectively, for a single subject. Experiment 2 - H magnitude and movement rate during passive rotation
Changes in movement speed, during passive movement of the limbs, altered the magnitude of the evoked H-reflexes. Four subjects, from Experiment 2, all demonstrated a decreasing H-reflex with higher movement speeds. Overall, there were significant differences be-
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Crank position (% of cycle) Fig. 2. Mean H-reflex magnitudes across the four subjects and three speeds for (A) passive rotation of the legs and (B) active pedalling of the limbs. Also shown are the mean response magnitude when subjects were sitting with the limbs at the same crank positions. All magnitudes are expressed as a percent of M response maximum
(Mmax).
tween the different movement speeds ( F 2 , 6 -~" 126.8, P = 0.0001). Multiple comparisons of means revealed that the largest H-reflex magnitude was associated with the slowest movement speeds and lower H-reflexes with faster speeds. The overall means, across subjects and crank positions, were 51.6% (S.E. 5.9), 22.8% (S.E. 4.8), and 10.0% Mma x ( S . E . 3.0) for 10, 30, and 60 rpm, respectively (Fig. 2A). The change in the magnitude of the H-reflex was approximately linear, with a negative slope, with the change in crank velocity. There were significant differences in the H-reflexes between crank positions (F3, 9 = 6.22, P = 0.01). The effect of the different velocities of rotation varied at the different positions, with reflexes most inhibited at the 92% (330 °) of cycle position. Three subjects were also
89
measured at 5 rpm. The only point to show significant inhibition at this speed, to 42.1% Mmax, (S.E. 5.3), was that for 92% of the cycle. H-reflexes collected when subjects were sat with the limb at similar positions to those during passive pedalling are also displayed in Fig. 2A. The magnitude of the Hreflexes during passive rotation were smaller than those collected during sitting. (The only exceptions were when the H-reflexes sampled at 5 rpm were slightly larger than when sitting, for the crank positions of 15 and 39% of the cycle.) The M responses were not significantly different across crank positions (F3, 9 = 1.34, P = 0.32) or movement speeds (F2, 6 = 0.41, P = 0.68). The average M response, averaged across all trials and subjects, was 16.3% Mma x (S.E. 0.5). The levels of contraction in soleus and tibialis anterior during passive rotation, prior to the stimulus, were also not significantly different across trials and crank positions.
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Experiment 3 - H-magnitude and m o v e m e n t rate during active pedalling The H-reflex changed in magnitude in the third experiment, when the rate of movement of active pedalling altered. The overall means of the H-reflexes were 24.2% (S.E. 3.9) 16.8% (S.E. 4.2) and 10.8% Mmax (S.E. 2.9) for 10, 30 and 60 rpm pedalling rates, respectively (Fig. 2B). These differences, indicating a negative linear relationship between speed and H-reflex magnitude, were significant (F2, 6 = 11.3, P = 0.009). The interaction between crank position and m o v e m e n t speed was also significant (F6,17 -- 9.3, P = 0.0001) revealing the position specific influence of changes in velocity. As before, there was no significant difference between the mean M responses over trials (F2, 6 = 1.94, P = 0.22) or crank positions (F3, 9 = 2.27, P = 0.15). There were, due to the active pedalling, significant differences between the magnitudes of both soleus and tibialis anterior contraction levels over different movement speeds. Generally, the higher the m o v e m e n t speed the higher the level of soleus contraction. This was most evident at crank positions 15 and 39% of the cycle. In contrast, the magnitude of tibialis anterior responses was often larger in the slow movements as opposed to the faster rotations. Experiment 4 - H-magnitude during passive movement o f a single limb Passive rotation of both limbs was also conducted in Experiment 4. The H-reflex observed during passive rotation of both limbs was similar to that demonstrated in Experiment 1. The H-reflexes were significantly lower than those evoked when subjects were sitting at all four
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Fig. 3. A: mean H-reflex magnitudes as a percent of Mmax across all four subjects recorded at four positions around the pedal cycle. Data were recorded during sitting, passive rotation of both legs, passive rotation of the target leg and passive rotation of the contralateral leg. B: H-reflex magnitudes for three subjects recorded from the stationary limb fixed at one position when the contralateral limb was being passively rotated (hatched bars) vs. control reflexes from the same limb when both limbs were relaxed and stationary (filled bars). The standard deviations are also displayed.
crank positions, as Fig. 3A shows. The mean H-reflexes were 10.0 (S.E. 2.9), 4.6 (S.E. 1.2), 5.6 (S.E. 2.3) and 2.8 ( 0 . 9 ) % Mma x for 15, 39, 69 and 92% of the movement cycle, respectively. In contrast, H-reflexes sampled when the subjects sat, with the limb positioned at these crank positions were 54.5 (S.E. 3.0), 59.2 (S.E. 5.2), 72.3 (S.E. 3.2) and 57.8 (S.E. 6.2) % of M . . . . respectively. During the passive movement of both legs, the M waves were not significantly different across the crank positions. The H-reflexes sampled when only the target limb was being passively rotated were also strongly inhibited. These H-reflexes were not significantly different from Hreflexes sampled when both legs were rotated. The mean
90 sponses were constant for the target limb. In all three subjects, for whom means and standard deviations are displayed, the differences between these two conditions were significant. This clearly highlights the inhibitory contribution made by the moving contralateral limb, not confounded by differences in events occurring at the target leg. In all trials the M responses were stable across phase positions. The global average of M response magnitude was 15.4 % Mma x ( S . E . 1.6) averaged across all subjects, trials and phase positions. During these passive movement trials little or no activity was recorded from soleus or tibialis anterior.
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Fig. 4. Mean data across all five subjects for (A) H-reflex magnitudes as a percent of Mmaxand pre-stimulus contraction levels as a percent of MVC for (B) tibialis anterior and (C) soleus EMG activity recorded at four positions around the pedal cycle. Data were recorded during sitting, normal pedalling (both legs) and onelegged pedalling when the target limb was stationary (contralateral leg) and moving (target leg).
responses were 7.9 (S:E. 2.3), 6.5 (S.E. 1.8), 5.0 (S.E. 2.2) and 2.7 (S.E. 0.6) % Mma x averaged across subjects, for crank positions of 15, 39, 69 and 92% of the cycle (Fig. 3A). H-reflexes evoked in the target limb (right leg) when it was stationary, and when, at the same time, the contralateral limb was passively rotated, were significantly lower than those evoked when subjects were sitting with both legs stationary (Fig. 3A). However, they were significantly higher than those evoked when both legs or the target leg were passively rotated. The mean values, averaged across subjects, were 33.9 (S.E. 8.1), 33.4 (S.E. 7.6), 30.2 (S.E. 5.4) and 33.8 (S.E. 7.1) % Mmax for each of the four crank positions. As mentioned, these H-reflexes fell in-between those evoked during sitting and those from passive rotation trials involving both legs. In the above comparisons, the limb was adjusted to the appropriate crank position for the sitting trials. Fig. 3B shows H-reflex amplitudes when the target leg was kept in a fixed position, for the comparison of sitting versus the contralateral leg being passively rotated. The differences between these trials could only be accounted for by differences in the events associated with the contralateral limb since limb position, contraction and M re-
H-reflexes evoked during active rotation with both limbs were similar to those documented in the previous studies 5. The H-responses were large in the power producing phase and inhibited in the recovery phase. The mean H-reflexes, averaged across subjects, were 69.4 (S.E. 15.4), 15.2 (S.E. 5.3), 2.6 (S.E. 0.3) and 44.0 (S.E. 11.2)% Mma x for 25, 50, 75 and 100% of the cycle respectively (Fig. 4A). The H-reflexes sampled during sitting significantly differed across crank positions. This modulation was anticipated since the contraction of soleus was matched to the contraction at each phase point during active pedalling. The average H-reflex magnitudes are displayed in Fig. 3A. The mean H-reflexes sampled during sitting were 85.0 (S.E. 7.2), 78.5 (S.E. 4.8), 52.5 (S.E. 11.7) and 45.9 (S.E. 14.4) % mmax for the four crank positions, respectively. There were no significant differences in the magnitudes of the H-reflex between one legged pedalling with the target limb and two legged pedalling. The magnitude of the H-reflexes, during pedalling of the target limb, were 77.8 (S.E. 10.6), 10.0 (S.E. 4.9), 2.2 (S.E. 0.5) and 28.9 (S.E. 4.5) % M .... for 25, 50, 75 and 100% of the cycle, respectively. This contrasted the differences observed between two legged pedalling and one legged pedalling with the contralateral limb. Fig. 3A displays the mean H-reflexes measured at each of the four crank positions (note that 0 and 100% are the same data point). When the contralateral limb actively pedalled, while the target limb was stationary, there was significant modulation of the H-reflex, across phase positions. The mean H-reflex magnitude was 83.6 (S.E. 6.7), 46.2 (S.E. 11.4), 25.0 (S.E. 8.6), and 19.7 (S.E. 5.2) % Mma x for the target limb placed at 25, 50, 75 and 100% of the crank cycle, respectively. The H-reflexes sampled at 50% (180 °) and 75% (270 °) of the cycle were both significantly lower than sitting and significantly higher than pedalling with both legs or the target leg. In contrast data sampled at
91 25% (90 °) and 100% (360 °) of the cycle were similar between these movement conditions. The H-reflexes from contralateral limb movement fell between sitting and double leg movement and this was similar to that observed when the limbs were moved passively. The results of the two experiments were also similar in that the responses seen during movement of the single target limb matched those seen with movement of both limbs. In all trials the M responses were stable across phase positions. The global average of M response magnitude was 16.4 % Mmax (S.E. 1.7) averaged across all subjects, trials and phase positions. When the target limb was actively pedalling (1 or 2 legged) the E M G activity of tibialis and soleus anterior, summarized in Fig. 4B and 4C, was characteristic of normal pedalling. During pedalling with only the contralateral limb the magnitude of soleus contraction in the target limb was matched to active pedalling with both legs, while the activity for tibialis anterior was not matched. DISCUSSION The present results confirm those in the previous paper in this journal, identifying extensive modulation of soleus H-reflexes during a cycle of pedalling, compared to control reflexes when sitting 3'5. The first paper reported that some of this movement modulation may be accounted for by activation of the muscles around the ankle. The present paper addressed three factors: the role of (1) movement contraction, (2) movement velocity and (3) the contralateral limb on the modulation of H-response during rhythmic movement of the legs. To the first question, 'is the reflex modulated in the absence of the muscular activity to drive the limbs', the unequivocal answer is 'yes'. The movement of passive rotation at 60 rpm elicits substantial modulation, with a predominance of reflex inhibition when compared to seated responses. In addition, there was occasionally a modest increase in reflex gain in the extension phase of passive rotation, similar in time to that observed for active rotation. To the second question, 'is reflex modulation related to the velocity of limb movement?', the answer again is 'yes'. The approximately linear relationship between the extent of the inhibition and the speed of movement is support for the idea that movement-induced sensory discharge underlies the inhibition. Such a relationship suggests a relatively simple transformation of sensory inputs into changes in reflex gain. Further, the effect appearing at very low speeds implies that the inhibition may require only modest levels of such discharge for it to appear. We have no direct information as to the sensory
modalities involved. There is obvious opportunity for contributions from haptic, joint and muscle mechanoreceptors. The net influence of discharge from these sensory receptors during physical movement of the limbs is expressed as inhibition on the Ia spinal route to this autogenic muscle. The presence of reflex inhibition in the recovery phase at very low speeds (cycle time 12 s) allows us to reject the view that the reflex is suppressed because the reflex loop delay would lead to a disruptive phase lag in E M G corrections at high speeds TM. The answer to the third question, 'can modulation arise from movement of the contralateral limb?', is also 'yes'. Two interesting new findings arise: (1) reflex modulation in the moving leg is the same whether subjects move only the target leg or move both legs, and (2) the movement of the contralateral limb leads to clear changes in response magnitudes in the stationary target limb (these responses lie in-between those evoked during sitting and those occurring with movement of both legs). Clearly, the bilateral nature of the movement was not necessary for the modulation of the reflex to be fully expressed. This is consistent with the similarity between reflex modulations observed in the moving limb during one and two legged walking 1°. One could conclude, as Crenna and Frigo 1° did, that there was no contralateral effect on the reflex modulation. However, contralateral effects, primarily inhibition, are present. (The reflex excitation in the stationary leg at 25% (90 °) past top-deadcenter (Fig. 4B), during active pedalling by the other leg, reflects also the contraction of soleus muscle in the stationary leg at that particular position. Thus, the reflex excitation should not be attributed simply to a contralateral influence.) The reflex inhibition from the contralateral limb was less powerful than that from the ipsilateral one alone. It is possible that effects of limb movement from passively moving limbs are additive and that those from the target limb have a greater weighting than those from the contralateral. This would account for the observation that H-reflexes from contralateral limb movement were intermediary between those when sitting and those when the target leg was rotated. The lack of difference in inhibition observed between movement of the target leg or both legs may be the result of an inability to observe further inhibitory effects rather than an absence of any contralateral effect. Use of E M G to estimate the integrity of this spinal reflex limits one's ability to estimate the 'true' inhibitory influence. It would be possible to increase the inhibitory drive, pre- or postsynaptically, beyond that necessary to suppress H-reflexes. A substantial part of this study characterized the Hreflex modulation during passive rotation of the limbs. Technical deficiencies are not the cause of the observed
92 modulation of H reflexes during these trials. There was control of limb position when sitting, and of stimulus constancy, throughout the experiment. There was control of sitting support, to remove any descending influences due to postural instability 1. The latter was a possibility for trials which were run with subjects seated on the ergometer. However, the revised apparatus, from which the majority of the data were collected, provided ample stability to allow the subject to relax completely. As a further confirmation of experimental control, we note that the reflex modulations were consistently observed in all subjects. An important observation is that the reflex inhibition, with passive rotation of the limb, is not uniform across the cycle. In the extension phase for the leg, there is a partial release of inhibition. Also, when it is modestly expressed at lower speeds, it is strongest at one phase in the cycle, the final part of recovery of the leg. These are not effects associated with contractile activity in the leg muscles. If, as we suspect, the inhibition of passive rotation arises from movement-related sensory discharge, then this may connect to differential discharge rates of involved receptors over the movement cycle. The inhibition appears most during the flexion phase for hip and knee, peaking close to the fullest flexion that occurs. (The ankle was braced against movement.) We do not know whether such modulation arises from changing discharge of receptors and/or selective gating through membrane changes in spinal neurons. For instance, for the latter, a potent role exists for hip joint receptors to reset the central pattern generated in the locomotor activity of the spinal cat 2. It is possible that the use of the ankle brace led to differential discharge of cutaneous receptors which may have influenced H-reflex modulation. We think that any contribution specific to the use of the brace is likely limited. This is based on similarities between active pedalling with and without the brace. It is also based on similarities in the recovery phase of active pedalling without the brace and passive rotation with the brace. Movement depression of H-reflexes has been attributed to inhibition which occurs before the motoneuronal soma and proximal dendrites 4'6 and which is probably presynaptic on the Ia afferent 9. It may be that such inhibition accounts for the depression of H-reflexes that we see over the movement as a whole. We did not set out to separate pre- and postsynaptic inhibitory effects. It is possible that modulation of H-reflex magnitude, during passive rotation or in the recovery phase of active movement, may be partly accounted for by subthreshold changes at the motoneuron. The only evidence we have for favouring the presynaptic source, is that such profound inhibition proved impossible to achieve
using post-synaptic inhibition of motoneurons during tictive locomotion in the decerebrate cat 9 or through manipulating a computer model of the human motoneuron 7. It is reassuring that the both the velocity dependent modulation and the contralateral effects seen during passive rotation were evident during active pedalling. This gives us some security that the influences seen in the passive rotation are contributing to the H-reflex modulation during active pedalling. The period of inhibition in the recovery phase of both movements may share similar origins. The modest increase in gain during the power phase of passive movement arises from a source independent of the muscular activity to move the limbs. The increased gain during active pedalling may arise in part from a common source leading to this contraction independent modulation. Additional increases in gain during active pedalling may arise from contraction-related facilitation of the m o t o n e u r o n a l pool 19'22. It does appear that the soleus contraction is necessary to promote the full increase in the magnitude of H-reflexes observed during the power (extension) phase of normal pedalling. Depression of reflex magnitude to near zero in the recovery phase of passive rotation demonstrates that neither the inhibitory effect of reciprocal inhibition from the tibialis anterior contraction T M nor of ankle dorsiflexion H'21, are required to obtain this effect. (Recall that the ankle was braced in the present experiments.) This is not to say that these movement features cannot contribute to modulation. Rather, that they are not essential for the observed reflex inhibition. We propose that there are complementary sources of movement-induced modulation of soleus H-reflexes during pedalling. These sources might sum to a greater effect on the muscle than that seen in the target E M G during normal pedalling. As an example, inhibition of the reflex is profound when only one leg is passively moved, even with ankle movement prevented. Yet, significant inhibition also arises from movement of the contralateral leg. Further, contraction of the ipsilateral tibialis anterior muscle, which contraction occurs in normal pedalling during the phase when the H-reflex is inhibited, substantially inhibits the reflex4. Clearly occlusion of neuronal pools could be occurring during normal pedalling. The lack of further inhibition, e.g., compared to passive single-leg activity, likely reflects an inability to measure further increases in suppression of the reflex at the level of the EMG. We suspect that occlusion occurs for some tasks. For other tasks the complementary sources of inhibition may be additive in their effect. In yet others the inhibition may arise from only a subset of sources. We propose that the physical movement of the limb
93 lays down the most basic, tonic, inhibition on the gain of the target reflex pathway. The inhibition can arise from slow m o v e m e n t of the single limb with b r a c e d ankle, in the absence of contraction of any muscles of the leg. This tonic inhibition seems related to the n u m b e r of involved sensory endings, for there is inhibition from the single leg alone and further inhibition from the contralateral one. It also seems related to the rate of discharge of those endings; the inhibition increases as the velocity of m o v e m e n t increases from a very low level. We consider that the inputs leading to this inhibition vary over the m o v e m e n t cycle, thus accounting for the differential attenuation of the H-reflex magnitude during changes in velocity of rotation. We expect that the o b s e r v e d increase in reflex gain during the p o w e r phase of active pedalling is the net o u t c o m e of the interaction of the inhibitory and facilitatory influences at the spinal neuronal pools. This interaction at times m a y obscure the measurable relationship b e t w e e n soleus contraction and the magnitude of the H-reflex. This could account for the suggestion that H-reflexes in walking are not directly associated with the level of contraction 8. M o v e m e n t of the ankle joint and the effects from contraction of o t h e r muscles of the leg, including h e t e r o n y m o u s projections 2°, must be a d d e d to these sources of excitatory modulation. T h e r e likely are o t h e r significant p e r i p h e r a l sources of
m o d u l a t i o n , not yet explicated 12. The whole represents an overlapping array of m o d u l a t o r y inputs from features of the m o v e m e n t . In some instances it can be shown that these arise from peripheral r e c e p t o r discharge and in others this is suspected. T h e r e has been interest in identifying central features of tasks, which features are also likely associated with the m o d u l a t i o n of H-reflexes. It is possible that such central features, perhaps in parallel with descending motor volleys, are i m p o r t a n t in defining the increase in excitability during the power-producing phase of the movement 8. Llewellyn et al. 17 have suggested that task difficulty is important. D y h r e - P o u l s e n et al. 13 have also suggested that the type of task, hopping versus landing from a jump, m a y be important. The present work exposes the consequences of events from the m o v e m e n t itself. In the light of this work, we conclude that one should only invoke a central descending source for reflex m o d u l a t i o n during m o v e m e n t after strict enquiry has been m a d e about the effects that are arising from the peripheral receptor sources associated with the movement itself.
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Acknowledgements. We appreciate the technical support of J. Hoare. This work was supported by a Grant from the Natural Sciences and Engineering Research Council of Canada No. A0025.
