Brain Research, 548 (1991) 172-178 © 1991 Elsevier Science Publishers B.V. 0006-8993/91/$03.50 A DONIS 000689939116573S
Modulation of human short latency reflexes between standing and walking John Dennis Brooke, David Frederic Collins, Susanne Boucher and William Evans Mcltroy Biophysics Interdepartmental Group and School of Human Biology, The University of Guelph, Guelph, Ont. (Canada) (Accepted 4 December 1990) Key words: Movement modulation; Presynaptic inhibition; Reflex; Gait
Inhibition of the magnitude of soleus muscle homonymous (H) reflexes occurs in humans when walking, compared to standing. The cttrrent study asked, (1) was the task modulation of Ia reflexes limited to soleus muscle, (2) was there support for attributing a presynaptic source to the inhibition in humans and (3) did an oligosynaptic short latency reflex show similar task modulation? In 3 subjects, H reflexes were evoked in vastus medialis and soleus, at 4 levels of contraction in the target muscle, with constant stimulus intensity when walking and standing. The reflex magnitudes in both muscles were significantly inhibited during the contractions for walking, compared to standing. Such inhibition also occurred in H reflexes of tibialis anterior muscle. An excitatory oligosynaptic reflex was then evoked in vastus medialis, through low intensity stimulation of the commin peroneal nerve during walking and standing. The mean amplitudes of this reflex were not significantly different (P < 0.05) between the two conditions, at any contraction level. The depression of quadriceps H reflexes, compared to the oligosynaptic reflexes through the same quadriceps motoneuronal pool in the same task, strongly suggested that the inhibition of H reflexes arose at other sites besides the motoneuronal cell body and proximal dendrites. We conclude that Ia H reflexes of various leg muscles of humans are inhibited when walking but that this does not generalize to the oligosynaptic short latency reflex between the anterior shank and thigh. INTRODUCTION The m a g n i t u d e of Ia H o m o n y m o u s (H) reflexes in h u m a n soleus muscle ( S O L ) is inhibited when walking, c o m p a r e d to standing, even when the contraction level of the muscle is the same for the two conditions 7 ' 2 1 . Inhibition also occurs in running, c o m p a r e d to walking s. It is i m p o r t a n t to know w h e t h e r this Ia reflex modulation is p r e s e n t in o t h e r muscles. If the inhibition is specific to the soleus H reflex, this influences the i n t e r p r e t a t i o n of the likely effect of this inhibition during locomotion. O n the same grounds, it is also important to know w h e t h e r the m o d u l a t i o n from standing to walking occurs in low threshold reflexes which do not arise from l a fibers. To address the first matter, H reflexes were e v o k e d in the knee extensor muscle vastus medialis, the ankle dorsiflexor muscle tibialis anterior and a plantar flexor of the ankle, soleus. F o r the second matter, the vastus medialis muscle was also excited oligosynaptically over a short latency p a t h w a y from the c o m m o n peroneal nerve 2°. Ia fibers do not conduct the latter reflex. The evidence suggests a Ib path 3a8'24. These e x p e r i m e n t s gave us the o p p o r t u n i t y to address a 3rd issue. The depression of soleus H reflexes when walking, c o m p a r e d to standing, has been attributed to
presynaptic inhibition s. F o r studies on humans, it is argued that, because the ongoing electromyographic ( E M G ) activity is unchanged b e t w e e n the two tasks, the excitability of the postsynaptic m e m b r a n e is unchanged 7' 13. C o m p u t e r modeling supports this 9. A l s o , postsynaptic inhibition induced in the d e c e r e b r a t e cat did not produce the depression of soleus m o n o s y n a p t i c reflexes when the m o t o n e u r o n a l pool was active 1°. This result suggested, by exclusion, that presynaptic inhibition was n e e d e d to achieve the m o d u l a t i o n of the a m p l i t u d e of the monosynaptic reflex. In the present study, two reflexes were transmitted through the same, vastus medialis, mo~toneuronal pool. Because the reflexes were m o d u l a t e d quite differently, this furnished further indirect evidence that the depression of H reflexes in humans is occurring at sites o t h e r than the postsynaptic s o m a and proximal dendrites of the m o t o n e u r o n . This work has been r e p o r t e d in part in abstract 11a2.
MATERIALS AND METHODS Seven informed volunteers between 23 and 26 years of age took part in the experiments. None reported any history of neuromuscular or metabolic disease. The experimental procedures were approved by the university committee for the ethics of experiments
Correspondence: J.D. Brooke, The Human Neurophysiology Laboratory, School of Human Biology, University of Guelph, Guelph, Ont., Canada, N1G 2Wl.
173 on humans, To record E M G activity, surface Ag-AgCl electrodes were placed with centers 3 cm apart longitudinally over the belly of the muscles. They were approximately 3 cm medial to the mid-line of the thigh for vastus medialis (VM), proximal on tibialis anterior (TA), starting approximately 9 cm distal to the border of the patella, and distal on SOL with the most distal electrode being 4 cm proximal to the junction with the Achilles tendon. These sites were intended to minimize cross-talk. Ag-AgCI stimulating electrodes were placed on the skin longitudinal to the nerve, with the anode distal. Delivery of the 1 ms square wave stimulus (Grass $88 stimulator and Grass SIU5 stimulus isolation unit), was controlled by computer. The impedance at recording and stimulation sites was below 10 kf2 (Grass E2M5 Impedance Meter at 30 Hz). The signal was amplified 201)0 times (Grass P511 amplifiers) with the band pass filter at 3-300 Hz, digitized at an A/D interface (Labmaster, Tecmar) at a sampling rate of 500 Hz, and stored on a microcomputer (modified IBM-PC). Data were collected online for 100 ms periods. There were 3 experiments, each involving 3 subjects (two subjects participated in two experiments); (1) stimulation of the femoral nerve, at the femoral triangle, to evoke M and H waves in VM. (The M waves arose from direct stimulation of a motoneuronai axons to VM.) The stimulus intensity to evoke small M waves also led to H reflexes that were near to their maximum amplitudes. (2) stimulation of the tibial nerve at the popliteal fossa, to evoke H waves and M waves in SOL, and (3) low threshold stimulation of the common peroneal nerve (CPN) just distal to caput fibula, to evoke reflex excitation, designated 'PQ' (peroneal nerve to quadriceps), in vastus medialis. This stimulation of CPN also evoked H reflexes and M waves in TA. The mean stimulus intensity for CPN was 1.3 MT, evoking PQ excitation which was just below maximum magnitude for that reflex. Approximately 15 s elapsed between stimulations. In each experiment, subjects walked on a treadmill (Collins High Speed Model) at a cadence of 120 steps per minute, with a stride length which was comfortable for them. Three or 4 levels of ongoing contraction in the target muscle were studied, both walking and when subjects stood unsupported. Habituation trials were provided until the subject felt at ease walking on the treadmill. During the walk, the computer-controlled stimulation was triggered via a pressure transducer (Hewlett Packard 270 and Hewlett Packard Carrier Preamp #88056). The amplifier output passed through a custom built Schmidt trigger and monostable multivibrator to emit a 20/~s square wave pulse. This provided a digital input to the computer. The small sensor, which did not impede the gait, was located on the heel of the shoe of the experimental leg. As illustrated in Fig. 1, the stimulus (shown by the vertical arrow) occurred 30 ms after heel strike, when VM, SOL and TA were active. EMG levels were monitored on an oscilloscope, so that the subject could match the magnitude of contraction when standing with that when walking. Contraction levels were increased during walking by raising the grade of the treadmill in stages from horizontal to 15% grade, and also by adding backpack loads to the subject. During standing, subjects increased the contraction levels by shifting their weight progressively more onto the experimental leg. Additionally, for higher contraction levels during standing, subjects were requested to either rise up on the toes (to increase SOL activity), or to flex the experimental leg to not more than 135 ° at the knee (to increase VM activity). Rest periods were incorporated, to avoid subject fatigue. The magnitude of the M wave in the homonymous muscle was used as a measure of stimulation constancy. (The M wave reflected the stimulation current directly applied to the motoneuronal axons. It did not reflect the excitability of the motor pool.) The mean of 3 maximum M waves (M max) was measured from peak to peak, for each subject during both standing and walking. The stimulation was then adjusted to evoke a fixed percentage of the appropriate M max. When online inspection revealed that the magnitude of an M wave exceeded + 5% M max of its intended value, that sample was not collected. The sampling of M waves was made without reference to the size of the accompanying reflex, A 30 ms delay on the stimulator allowed post hoc calculation of the
ongoing EMG activity prior to stimulation. This level was standardized against the average of 3 maximal voluntary isometric contractions (MVC) for each subject. Ongoing EMG activity was assessed from the 30 ms of the averaged, full wave rectified trace before the stimulus, for each contraction level. Mean peak to peak magnitudes of H reflexes were calculated from 40 samples per subject. The average 95% confidence interval for these
a) SOL i ~
so ~t v
l so ms
._j 7s ~ v so ms Fig. 1. Raw surface E M G activity in one subject over 3 cycles of walking at a cadence of 120 steps per minute, beginning at heel strike, a: soleus muscle (SOL), b: vastus medialis muscle (V.M.), and c: tibialis anterior muscle (T.A.). The moment of stimulation is shown by the vertical arrows.
174 means was + 15%. With 80 samples collected for the mean magnitude of the oligosynapticreflex to VM, the average 95% confidence band for the means was ___22%.
EMGs of VM, TA and SOL during gait Fig. 1 shows the raw EMG activity of one subject during walking, for the duration of one complete cycle of leg movement, at a cadence of 120 steps per minute on the treadmill. Heel strike occurred at the start of the collection, which was for 1 s. Traces from 3 cycles are superimposed. As Fig. la shows, the activity in SOL began close to heel strike and remained throughout the stance phase of the walk. As with the quadriceps muscle, it eccentrically contracted to resist the yielding flexion of the joint, followed by concentric contraction for the joint extension. Fig. lb shows that VM was active prior to heel strike. It remained active through the moment of stimulation, shown by the vertical arrows 30 ms into the
traces. Fig. lc shows that there were two separate bursts of activity in TA. The first occurred to dorsiflex the foot so that it cleared the ground during the swing phase. The second burst was initiated approximately 70 ms before heel strike and ended shortly thereafter. This second burst may ensure that the foot is smoothly plantarflexed after heel strike. By inspecting at the moment shown by the stimulation arrows, it can be seen that all 3 muscles were active at this point in time. The pattern of EMG discharge during the gait was consistent among the subjects, resembling that described by Winter 3~.
Modulation of VM H reflex Mean H reflexes in VM are shown in Fig. 2a for standing and for 30 ms after heel strike when walking, in one subject at the 3rd level of contraction in VM. The distribution of the 40 trials making up the mean is shown by the lines for + 1 S.D. The mean reflex latency was 19.9 ms. It can be seen that the magnitude of this reflex was reduced while walking, compared to standing.
a) Vastus Medialis Homonymou8
From FN n = 40
- 1 SD lmV 5 ms
Soleus Homonymoul Reflex From
n = 40
+ 1 SD S
x - 1 SD
400 g V
Vuttm M ~ l l a l l s Hetemeymous Reflex From CPN n = 80
. 1 SD
Fig. 2. Mean reflex EMG activity from single subjects, both standing and walking. The distribution of individual trials is shown by + 1 S.D. 'S' shows the stimulus artifact, and 'M' the wave evoked by directly stimulating the a motoneuronal axon concomitantly with the large diameter afferents, a: the H reflex in vastus medialis muscle, after stimulation of the femoral nerve (FN) at the femoral triangle. Means are from 40 samples, b: the H reflex in soleus muscle, after stimulation of the tibial nerve (TN) at the popliteal fossa. Means are from 40 samples, c: the heteronymous reflex (PQ) in vastus medialis muscle, after stimulation of the common peroneal nerve (CPN) at caput fibula.
175 Modulation of VM H-reflex
Fig. 3. Mean values from 3 subjects (with bars for + S.E.M. from the pooled S.E. for each subject) for the peak to peak magnitudes of reflexes evoked when standing and walking, with a range of levels of contraction in the target muscles (as % maximum voluntary isometric contraction), a: the H reflex in vastus medialis, from stimulation of the femoral nerve, b: the H reflex in soleus muscle, following stimulation of the tibial n e l w e and c ; the short latency heteronymous reflex in vastus medialis muscle, from stimulation of the common peroneal nerve.
7 6 s
4 3 _ _ 2
eo % max volunlary contraction in VM ~,ten~.g -~ w°,k~ng
pooling S.E.M. s from individual subjects. This S.E.M. reflects the precision of measuring around a mean value for a subject.) W h e n walking, the VM H reflex did not increase with increasing level of contraction in VM. The slopes of the regression lines between standing and walking were significantly different (P < 0.05). The stimulation intensity was kept constant by online monitoring of the M wave elicited in VM ('M' on Fig. 2a). The mean M wave evoked in VM, over the 3 subjects, was 13.6% M max during standing and 13.5% M max during walking. The mean latencies of the VM H reflex, over the 3 subjects, were 18.5 ms, for both standing and walking.
Modulation of Soleus H-reflex
a -------------~-~ ~ E
Fig. 3a shows this reduction in the mean magnitudes from 3 subjects, over 4 levels of contraction in VM. (Also shown are standard errors (S.E.M.s), obtained from
-- - - ~
Modulation of SOL H reflex 0
% maxvoluntary contractionin SOL stanaing ~ *,,k~n9 Means for thgeeSUbj4Ctaand S.E.
Modulation of VM Heteronymous reflex
the regression lines between standing and walking were significantly different (P < 0.05). The intercepts were not significantly different (P > 0.05). During walking, the magnitude of the S O L H reflexes did not increase as the level of contraction increased (P > 0.05). The mean amplitude of the M wave was 11.2% M max standing and 8.5% M max walking. The mean latency for the H reflex across the 3 subjects was 28.6 ms for standing and 30.6 ms for walking.
~, 0.2 0
60 80 max voluntary contraction in VM standing
Fig. 2b shows mean amplitudes ( + 1 S.D. for the distribution of individual trials) for S O L H reflexes in one subject walking and standing, at the 3rd level of contraction in the S O L muscle. The latency of the H reflex for this subject was 31.3 ms. It can be seen that the reflex magnitude was reduced when walking. The mean values from 3 subjects, illustrated in Fig. 3b for 4 levels of contraction, show that the SOL H magnitude was attenuated when walking. The slopes of
Modulation of TA H reflex Movement-induced attentuation of H reflexes in TA was also investigated in one subject. Three measurements of reflex magnitude when standing at contraction levels of 24-48% maximum voluntary contraction in T A provided an average magnitude of 0.48 m V (range 0.39-0.61
176 mV respectively), with latency for the average of 34.1 ms. The mean reflex magnitude when walking with contraction of 44.5% maximum voluntary contraction in TA was 0.1 mV. At 58% maximum voluntary contraction in TA when walking, the reflex magnitude was again 0.1 mV, with reflex latency of 35.6 ms for walking. The magnitudes of M waves evoked in TA were 10.9% M max standing and 10.6% M max walking,
Modulation of VM heteronymous reflex The mean PQ reflex response in VM is shown in Fig. 2c, for a subject at the 3rd contraction level during standing and walking. Also shown, as + 1 S.D., is the spread of the 80 trials making up the mean. Eighty samples were taken so as to reduce the range of random variation in the mean E M G line. The remaining variation is shown in Fig. 2c as the small changes in magnitude over the 30 ms before the stimulus, 'S'. The peak-to-peak magnitude of the PQ reflex was significantly greater than that random variation (P < 0.05). The mean reflex response was initiated 27.7 ms after stimulation. It can be seen that the PQ reflexes of this subject were little different in magnitude over the two conditions, For 3 subjects, the mean magnitudes of the PQ response in VM, when walking and when standing at different levels of contraction in VM, are shown in Fig. 3c. The PQ reflex magnitudes at 30 ms after heel strike when walking were not depressed like H reflexes, when compared at the same level of contraction on the regression line for means during standing. The slopes of the two regression lines for VM were not significantly different between standing and walking (P < 0.05). There were some intersubject differences, with one subject showing significantly elevated PQ reflexes when walking compared to standing, and another showing a 25% fall in PQ amplitude when walking at the first contraction level. The mean amplitudes of M waves evoked in TA by the stimulation, were 22% of M max when standing and 20% when walking. The mean latencies over the 3 subjects, from averaged trials, were 28.5 ms standing and 27.9 ms walking. The amplitude of the reflex significantly increased with increasing contraction in VM, in both conditions, DISCUSSION We conclude that Ia H reflex depression when humans walk, in comparison to when they stand, is not limited to soleus, the muscle reported to date 7'8'13'21. The present results show depression occurs also in vastus medialis and tibialis anterior muscles. We also conclude that short latency reflexes which are not monosynaptically evoked by Ia fibers may not show
the depression of reflex magnitude. Such depression did not occur in the oligosynaptic reflex (probably Ib) to excite vastus medialis from the common peroneal nerve 3' 2o This maintenance of magnitude of the non-Ia reflex, when the legs are active, is similar to the maintenance of the magnitude of that reflex when pedalling compared to sitting 2. (With pedalling, soleus H reflexes are depressed, compared to sitting (unpublished observations).) One reason for the difference between the H and PQ reflexes may be that the latter can be controlled through its interneurons. Additionally, the reflexes may differ in the site of the inhibition imposed on them. The differences in modulation of la and non-la reflexes are not felt to stem from inadequate experimental control. The 95% confidence bands for the mean magnitudes of both kinds of reflexes were narrow for each subject. Also, reflexes were only collected when concomitant M wave magnitudes were within 5% M max of their intended value. We do not feel that afferent refractoriness, from high levels of traffic, was the cause of the reduced reflex magnitude. Such refractoriness of Ia, Ib or cutaneous fibers, for movements such as those studied presently, has not been observed in the cat 25 or inferred in humans 7. Changes in the tibio-tarsal or femoro-tibial angles between walking and standing, are also unlikely to be the source of the differences between the reflexes. During walking, the former joint alters in the wrong direction for reflex depression 29. Changes in the latter joint were found not to alter the magnitude of the PQ reflex 2'4. The oligosynaptic reflex that was not depressed, and one of the H reflexes which was depressed, both activated the motoneuronal pool serving the VM muscle. In that instance in particular, there are grounds for suspecting that the source of the H reflex depression was not the motoneuronai membrane, because the motoneuronal pool continued to fully express the non-Ia reflex. Two matters particularly need to be addressed, with this interpretation of the data. Firstly, the homogeneity of synaptic sites on the motoneuron. In the cat, Ia boutons are located close to the soma and the most proximal branches of the dendrites 5. Thus, if H reflex inhibition had occurred at such postsynaptic sites, it would have also depressed the ongoing E M G and the oligosynaptic reflex. This is because these sites of Ia convergence are close to the trigger zone for the action potential. Inhibition specific to la synapses located on distal dendritic sites is an alternative interpretation of the reflex differences. However, the research literature does not contain information on that issue. The other matter to he considered, is whether the VM motoneurons were separated into subpools, with one of them receiving just the Ia femoral nerve projection,
177 together with postsynaptic inhibition. We consider this unlikely. H o m o n y m o u s Ia fibers are reported to project to close to 100% of motoneurons, not to a subpool, in cat gastrocnemius 22. Also, reports of motoneuronal pool segmentation have been restricted to biarticular muscles 17 and VM is a uniarticular muscle. However, the present results cannot wholly discount that the two types of reflexes could differentially excite the human VM motoneuronal pool. O u r current interpretation is that the difference in reflex expression provides further support, from a new approach, that H reflex depression between such tasks occurs through premotoneuronal mechanisms 8'9'1°'~3'15' 16,21. The premotoneuronal effect is probably presynaptic, although the possibilityofinterneuronallymodulating an oligosynaptic component to the H reflex cannot be wholly discounted, for the present results on humans 6. Modulated presynaptic inhibition could arise from differences in primary afferent traffic to presynaptic inhibitory interneurons 1"26'27, when walking was compared to standing, or from alterations in descending input to such interneurons 1'27. Hultborn et al. 15 favoured the latter at the onset of contraction and inferred a descending origin, on the grounds of insufficient time for contraction-induced afferent discharge to activate spinal inhibitory interneurons, Reflex magnitude increased, with increasing contraction magnitude, for SOL, VM and TA H reflexes when standing and for the short latency oligosynaptic VM responses when standing and when walking. Such corre-
it is clear that such compensation, for electrically evoked Ia reflexes, changes for different tasks. At low levels of muscular contraction in this period, the reflex is inhibited at that point in the walk cycle. The anticipated increase in the reflex, as the walking contractions increase in magnitude, does not occur; presumably the reflex is additionally inhibited. This reveals that the inhibition of the Ia motoneuron reflex is modifiable, even within the phase of the task. One speculates that the brain retains control of the response to environmental perturbations such as muscle stretch and inhibits the reflex during this part of the bipedal activity. The c o m m o n control of Ia fibers seen presently is not generalized between tasks. Katz et al. 16 found, when standing without support was c o m p a r e d to sitting or supported standing, that S O L H reflexes were inhibited, quadriceps H reflexes were increased and TA H reflexes were unchanged in magnitude. Hultborn et al. ~s proposed that presynaptic inhibition was decreased at the onset of a voluntary plantar flexion when seated, for both h o m o n y m o u s and heteronymous Ia projections to SOL. H o m o n y m o u s Ia projections to quadriceps were inhibited at that time. Voluntary knee extension produced the opposite pattern of reflex inhibition. The task appears to be a determinant of the control of the reflex and, presumably, its role in the movement. We next need to know what the central nervous system identifies, in the task, which determines the control of the reflex.
lation of tonic E M G level and Ia reflex magnitude has been reported by several investigators 14"23'3°, Matthews 19 suggesting this provided 'automatic gain compensation',
Acknowledgements. This work was supported by Grant A0025 to J.D.B. from the Natural Sciences and Engineering Research Council of Canada and by scholarships to D.F.C., S.B. and W.E.M. from the University of Guelph. We gratefully acknowledge the advice of Dr. V.B. Brooks and Dr. R.B. Stein in the preparation of the manuscript.
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