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Reflex effects of muscle afferents on antagonist studied on single firing motor units in man
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Eh<'troencephalography and Clinical Neurophysiology, 1980, 5 0 : 2 1 4 -22~ © Elsevier/North-Holland Scientific Publishers, Ltd.
R E F L E X EFFECTS OF MUSCLE A F F E R E N T S ON ANTAGONIST STUDIED ON SINGLE FIRING MOTOR UNITS IN MAN L.P. KUDINA Institute for Problems o f i n formation Transmission, U.S.S.R. Academy o f Sciences, Moscow (U.S.S.R.) (Accepted for publication: May 7, 1980)
The reciprocal inhibition of antagonist motoneurones caused b y Ia afferents has been an object of intense study since Sherrington's works. Experiments on animals have made it possible to reveal the convergence of excitatory and inhibitory drives on Ia inhibitory interneurones as well as to consider some functional aspects of such convergence (see Hultborn 1976). However, the part played b y the reciprocal inhibition in m o t o r control is not clear and even revealing the inhibition in intact human beings is very difficult. Studies carried o u t b y various researchers have yielded contradictory results. Opinions differ on the effect of electric stimulation of a mixed nerve (Ia afferents) on a human antagonist. According to Tanaka et al. (Mizuno et al. 1971; Tanaka 1974, 1976), reciprocal inhibition, estimated by its effect on the amplitude of the antagonist monosynaptic response, is absent in healthy man at rest b u t is observed under voluntary contraction of the muscle whose afferents are stimulated. On the other hand, the same technique employed by other researchers (Paillard 1955; Kots and Zhukov 1971) revealed a distinct reciprocal inhibition at rest. Agarwal and Gottlieb (1972), Ashby and LaBeUe (1977) and Ashby and Zilm (1978) described the reciprocal inhibitory effect of electric stimulation of Ia afferents on the voluntary activity of the antagonist. Hagbarth (1962) reported, however, that the reciprocal inhibition o f the antagonist voluntary activity is distinctly
revealed only after tetanization of Ia afferents. When a different method of activating Ia afferents was used, i.e., that of eliciting the tendon reflex, the excitatory effect on the antagonist was observed in summated EMGs instead of the expected reciprocal inhibition (Rao 1965; Agarwal et al. 1970; Gurfinkel and Paltsev 1973). Thus, the efficiency of reciprocal inhibition in intact human beings is questionable. The aim of the present work is to study the effect of electric stimulation of a nerve and of tendon percussion on single m o t o r units (MUs) of a human antagonist and to analyse the characteristics of the reciprocal inhibition effect on firing motoneurones. Some of the results were reported earlier (Kudina 1976, 1978).
Methods The study was carried o u t on 6 healthy volunteers. The subject sat comfortably in an armchair and the knee angle was 90 ° . The nerves innervating m. rectus fem., m. soleus and m. tibialis ant, (we shall refer to these as agonists) were electrically stimulated and the effect of the stimulation on their antagonists -- m. biceps fern., m. tibialis ant., m. soleus and m. gastrocnemius m e d . - was studied. The stimuli were applied to n. femoralis at the inguinal ligament, to n. tibialis at
REFLEX EFFECTS ON MOTOR UNITS OF ANTAGONIST the popliteal fossa and to n. peroneus at the level of the caput fibulae, respectively. Surface bipolar electrodes were used and single stimuli with a duration of 1 msec were applied (up to 90--150 stimuli in each experiment). As is known, when the strength of mixed nerve stimulation increases the monosynaptic reflex gradually diminishes and at high stimulus strengths completely disappears. Also, in some muscles (including m. tibialis ant.) the H reflex is either very weak or absent at high as well as at low stimulus strengths. In all such cases we presumed that the effect of afferent volleys on Ia inhibitory interneurones was not suppressed. Hence, we used stimuli evoking the H reflex in the agonist (not less than 20% of Hmax) or, in the absence of the H reflex, the M response (not less than 10% of Mmax) or both. The knee tendon reflex was evoked by a hammer and its effect on the antagonist was also studied. The EMG of the agonist was picked up b y surface electrodes. Stimulation of afferents was carried o u t during weak voluntary contraction of the investigated antagonist. Most of the experiments were made with the f o o t freely moving; in some experiments it had to be fixed to avoid displacement of the electrodes. The potentials of single MUs of the antagonist were picked up by bipolar needle electrodes. MUs were identified visually. Post-stimulus histograms for 162 MUs in 24 experiments were plotted. The bin width was 5 msec; bin deviations were considered reliable ( P < 0.05) if the number of potentials within a bin went b e y o n d the limits of n + 2 x/fi, where fi is the average number of potentials in a bin of the pre~stimulus segment of the histogram. In 19 experiments the effect of nerve stimulation on the duration of interspike intervals of 43 MUs was also analysed. The mean interval of background activity was calculated as the average of 5--6 intervals preceding each stimul u s and the duration of the interval within which the afferent volley occurred was expressed as percentage of the mean interval in the pre-stimulus period.
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Results
(a) The inhibitory effect The mean frequency of the background firing of single MUs in the voluntarily contracted antagonist varied from 6 to 12 imp/ sec. During stimulation of n. femoralis and n. tibialis evoking the H reflex, the H reflex together with the M response, or only the latter in the agonist, the antagonist MU interspike interval within which the afferent volley arrived often became longer (Fig. l a : MU marked b y a cross, Fig. l b ) . This proved the existence of the reciprocal inhibitory effect on the antagonist MUs. The stimulation of n. peroneus, evoking the M response in m. tibialis ant. (the H reflex was absent or very weak in this muscle), also caused lengthening of MU interspike intervals in the antagonist (Fig. lc). In some cases, however, the dura-
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Fig. 2. Post-stimulus histograms of the potentials of the antagonist's firing MUs during nerve stimulation. a: 26 MUs of m. biceps fem. during stimulation of n. femoralis (7 experiments), b: 58 MUs of m. tibialis ant. during stimulation of n. tibialis (6 experiments). c: 48 MUs of m. triceps surae during stimulation of n. peroneus (6 experiments), x-axis = time (0 = moment of stimulation); y-axis = number of MU impulses (shaded parts of columns = impulses of newly recruited MUs). Horizontal bar under the histogram denotes the period of reliable decrease of MU discharge probability (P < 0.05), i.e., period of reciprocal inhibition. t i o n o f t h e i n t e r s p i k e interval w i t h i n w h i c h a volley arrived did n o t b e c o m e longer (Fig. l a : MU m a r k e d b y circles). F o r a m o r e reliable demonstration of reciprocal inhibition posts t i m u l u s h i s t o g r a m s w e r e used. In all t h e e x p e r i m e n t s t h e h i s t o g r a m s s h o w e d a reliable d e c r e a s e in t h e p r o b a b i l i t y o f MU discharge a f t e r a s t i m u l u s , i.e., t h e histograms revealed the inhibitory effect (Fig. 2). T h e l a t e n c y o f i n h i b i t i o n was e i t h e r e q u a l t o t h a t o f t h e H r e f l e x o f t h e agonist or e x c e e d e d it b y several m i l l i s e c o n d s ( n o t m o r e t h a n a bin, i.e. 5 m s e c ) . T h e i n h i b i t i o n was
clearly e x p r e s s e d in all the 3 cases, i.e. w h e ~ either H or M r e s p o n s e o f t h e agonist or b o t h w e r e r e c o r d e d . This shows t h a t w h e n t h e H r e s p o n s e is d i m i n i s h e d d u e to an increased s t i m u l u s s t r e n g t h , as well as w h e n it is a b s e n t {in m. tibialis ant.), t h e a f f e r e n t volley c o m i n g to la i n h i b i t o r y i n t e r n e u r o n e s is n o t suppressed. At a s u f f i c i e n t s t i m u l u s s t r e n g t h t h e inhibit o r y e f f e c t was f o l l o w e d b y e x c i t a t i o n , w h i c h m a n i f e s t e d itself in an increased discharge p r o b a b i l i t y o f firing MUs a n d in t h e recruitm e n t o f n e w o n e s (Fig. 2). T h e e x c i t a t o r y e f f e c t was m o r e p r o n o u n c e d w i t h a freely moving foot. T h e d u r a t i o n o f i n h i b i t i o n in p o s t - s t i m u l u s h i s t o g r a m s f o r MUs o f m . biceps f e m . a n d m. t r i c e p s surae was 1 0 - - 2 0 m s e c , a value close to t h a t o f t h e agonist m o n o s y n a p t i c r e s p o n s e (H reflex) in EMG. T h e i n h i b i t i o n lasted m u c h longer ( 2 5 - - 5 0 m s e c ) in p o s t - s t i m u l u s histog r a m s f o r MUs o f m . tibialis ant. On stimulat i o n o f n. tibialis t h e E M G o f m . tibialis ant. o f t e n s h o w e d , a p a r t f r o m t h e e f f e c t o f reciprocal i n h i b i t i o n , t h e r e c r u i t m e n t o f n e w MUs with the latency of the M response and, sometimes, w i t h t h a t o f t h e H reflex. This shows t h a t d u r i n g s t i m u l a t i o n o f n. tibialis at the p o p l i t e a l fossa e f f e r e n t a n d a f f e r e n t fibres o f n. p e r o n e u s w e r e also s t i m u l a t e d . I t is possible t h a t in this case t h e i n h i b i t o r y e f f e c t o f n. peroneus stimulation (recurrent inhibition?) was a d d e d to t h e r e c i p r o c a l i n h i b i t i o n . T h e r e c i p r o c a l i n h i b i t i o n in p o s t - s t i m u l u s h i s t o g r a m s was m u c h s h o r t e r t h a n t h e interspike interval o f MUs. I t was i n t e r e s t i n g to s t u d y t h e e f f e c t s o f such i n h i b i t i o n o n t h e dur a t i o n o f t h e i n t e r s p i k e interval in w h i c h it o c c u r r e d . T h e changes in t h e interval d u r a t i o n o f MUs o f m . biceps f e m . a n d m . t r i c e p s surae did n o t f o l l o w a d e f i n i t e p a t t e r n : a l o n g w i t h l e n g t h e n e d intervals t h e r e w e r e q u i t e a n u m b e r o f intervals w i t h i n t h e limits o f fluctuat i o n o f t h e m e a n interval a n d t h e r e w e r e s o m e s h o r t e r intervals as well (Fig. 3b}. In t h o s e experiments where facilitation after inhibition was well p r o n o u n c e d t h e m a j o r i t y o f intervals were short.
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it proved ineffective: the interval either remained unchanged or became shorter (Fig. 3c, the left part of the diagram). The latter took place if facilitation following inhibition occurred within the same interspike interval. The majority of intervals of m. tibialis ant. MUs (the inhibition duration in the poststimulus histogram 25--50 msec and the facilitation following it rather weak) were lengthened and the efficiency of inhibition increased when the volley occurred closer to the end of the interval (Fig. la: MU marked by a cross).
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Fig. 3. Different methods of revealing reciprocal inhibition (MUs of m. gastrocnemius med., stimulation of n. peroneus), a: post-stimulus histogram (3 MUs); arrow shows latency of H reflex, other designations same as on Fig. 2. b: statistical analysis of interspike intervals of one of 3 MUs presented in histogram (155 tests): duration of interval within which volley arrived as percentage of mean interval of background firing• c: same MU as in b: dependence between volley efficiency and m o m e n t of volley arrival within an interspike interval, y-axis = same values as in b; x-axis = time between preceding MU impulse and m o m e n t of volley arrival as percentage of background mean interval.
(b) The excitatory effect In contrast to the H reflex volley the tendon reflex volley had an excitatory effect on the antagonist MUs. In 5 experiments on 3 subjects the activity of 30 MUs of m. biceps fem. during the knee reflex was analysed. A typical result is seen in Fig. 4. The response to a volley included the discharge of firing MUs (often with a shortened interspike interval) and of newly recruited ones. The response was synchronous with the agonist tendon reflex. Thus, during the evoked tendon reflex,
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The statistical analysis showed that the efficiency of an inhibitory volley depended on the moment within an interspike interval at which this volley occurred. This moment was determined as described below. The latency of the inhibitory effect was found in the post-stimulus histogram and the duration of the interval between the Iast regular impulse and the arrival of the inhibitory volley was calculated for each test as a percentage of the mean interval of the background firing. When inhibition lasted 10--20 msec the lengthening of an interspike interval was observed if the inhibitory volley occurred closer to the end of the interval (Fig. 3c, the right part of the scatter diagram). If the inhibitory volley occurred in the first part of the interval
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Fig. 5. Revealing weak excitatory drive, caused by nerve stimulation, on firing MUs of the antagonist (m. biceps fern. and m. triceps surae) by analysis of interspike intervals, a: duration of MU interspike intervals, ending synchronously with H reflex of the agonist as percentage of background mean interval (data of 10 experiments); though no increase of discharge probability is revealed in post-stimulus histograms, the shortening of intervals is reliable, b: example of interval shortening (circle denotes premature discharge); calibration = 200 pV, other designations as in Fig. 1.
in contrast to electrical activation of Ia afterents, no reciprocal inhibition of the antagonist MUs was revealed. Returning to the experiments with nerve stimulation and comparing the latency of the agonist H reflex and that of reciprocal inhibition in the post-stimulus histograms we noticed that sometimes the inhibitory effect was delayed b y a bin. The question arises whether the lengthened latency was due to interference with the excitatory drive. An attempt has been made to reveal this latter. As mentioned above, the facilitation of m. tibial ant. MUs, synchronous with the H response of m. soleus, can probably be ascribed to a side effect of n. tibialis stimulation at the popliteal fossa on n. peroneus afferents. For m. biceps fem. and triceps surae this is hardly possible since the nerves innervating them are located quite far from the stimulated areas. Therefore only experiments on these t w o muscles were considered. The
durations of interspike intervals which ended within the bin of the histogram preceding inhibition {i.e., coinciding with the beginning of the agonist H response) and in the following bin (in cases of incomplete inhibition) were analysed. One hundred and sixty interspike intervals from 10 experiments were analysed and a statistically significant (P < 0.001) shortening of intervals with respect to the mean background interval was revealed (Fig. 5). This shows the presence of facilitation in motoneurones, b u t the facilitating volley was, apparently, weak. In combination with the reciprocal inhibition, the inhibitory drive was prevalent. Therefore the probability of MU discharge did not increase in the corresponding bin. The excitatory effect was manifested only in the somewhat lengthened latency of inhibition in the post-stimulus histogram and in shortening of some interspike intervals, which could be revealed only statistically.
REFLEX EFFECTS ON MOTOR UNITS OF ANTAGONIST Discussion
The literature shows that one meets with serious difficulties in trying to reveal, in intact man, such a widely known phenomenon as reciprocal inhibition. The method of post-stimulus histograms plotted for single MUs has made it possible to reveal it in all the 3 investigated muscles and to determine its latency and duration. The sensitivity of the method in the study of excitatory and inhibitory effects on a firing motoneurone has been shown by some other authors {Ashby and LaBelle 1977; Person 1977; Ashby and Zilm 1978; Person and Kozhina 1978). Employing this method Ashby and his co-authors revealed reciprocal inhibition of m. soleus and of m. tibialis ant. MUs. In our study the method of post-stimulus histograms combined with the analysis of MU interspike intervals has allowed us not only to reveal the reciprocal inhibition but also to understand the peculiarities of its action on a firing motoneurone. In particular, the dependence o f the inhibitory efficiency on the moment of its occurrence within an interspike interval has been shown. A similar dependence under nociceptive cutaneous stimulation was earlier reported by Kranz et al. (1973). However, this dependence is especiaUy significant in the case of reciprocal inhibition since it is considerably shorter than an interspike interval. The latter became longer only when an inhibitory volley arrived closer to the forthcoming MU discharge than to a previous one. In other cases the inhibitory volley was ineffective (the interval remained unchanged). Thus,. the changes in the duration of an interspike interval cannot be a sufficient criterion of inhibition of such short duration. Among the investigated muscles, in m. tibialis ant. the H reflex is practically absent at rest. Nevertheless stimulation of its mixed nerve of sufficient strength evoked a distinct reciprocal inhibition. It is not quite clear why the H reflex is absent or small in some muscle.
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Some authors believe that there exists tonic presynaptic inhibition {complete or partial) of this reflex in intact human beings (Delwaide 1973; Person and Kozhina 1978; Person and Kudina 1978). If this is true then our data on antagonist reciprocal inhibition in the absence of the agonist H reflex may be attributed to the absence of depression of the Ia afferent endings activating the Ia interneurones. The tendon reflex is generally believed to be evoked by Ia afferents, like the H reflex. However, there are data showing that these two reflexes are somewhat different (Teasdall et al. 1952; Kots 1976). As far as their influence on the antagonist is concerned, the tendon reflex, unlike the H reflex, has a distinct excitatory effect (Rao 1965; Agarwal et al. 1970; Gurfinkel and Paltsev 1973). A hypothesis was advanced that activation of the antagonist by the evoked tendon reflex is caused via the collaterals of the agonist Ia afferents (Gurfinkel and Paltsev 1973; Kudina 1976}. It is based on data showing the existence of excitatory monosynaptic inputs from Ia afferents to the antagonist motoneurones (Eccles et al. 1957; Willis et al. 1966). Some data obtained in this study confirm this view: under electrical stimulation of the nerve a weak excitatory influence, in some cases, preceded the reciprocal inhibition. Under the evoked tendon reflex the excitatory drive on the antagonist was, possibly, augmented by other groups of afferents (Ib and II). The demonstration of reciprocal inhibition during artificial synchronous stimulation of afferent fibres does not solve the problem of its functional role in motor control. As shown by Tanaka (1974) with relatively weak stimuli (apparently more adequate than strong ones), reciprocal inhibition was absent at rest and was revealed only during voluntary contraction of the agonist. Electromyographic study of natural movements in man gives many examples of simultaneous activity of antagonistic muscles, in particular during the formation of motor skills, during walking, etc. (see Person 1965).
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Summary The effects of electrical stimulation of mixed nerves and of the evoked tendon reflex on single firing MUs of antagonists were investigated. The following muscles were studied: m. biceps fem., m. tibialis ant. a n d m. triceps surae. Under a weak voluntary contraction MU potentials were picked up. Post-stimulus histograms of MU potentials were plotted and the duration of interspike intervals in the post-stimulus period was compared with that in the prestimulus period. Under electrical stimulation of the nerve (Ia afferents) a distinct reciprocal inhibition was observed on MUs of all the 3 investigated muscles. In some cases a weak excitatory drive could be revealed along with the reciprocal inhibition. The tendon (knee) reflex was accompanied by a distinct excitatory effect on MUs of the antagonist. The dependence between the efficiency of the inhibitory volley and the m o m e n t within an interspike interval at which the volley arrived was found. The lengthening of an interval was observed only when an inhibitory drive occurred close to its end. The peculiarities of reciprocal inhibition in the firing motoneurone, as well as the possible mechanism of the excitatory effect on the antagonist accompanying the tendon reflex, are discussed.
Rdsumd Effets rdflexes des affdrents musculaires sur l'antagoniste, dtudids sur des unitds motrices isoldes chez l'homme Les effets de la stimulation dlectrique des nerfs mixtes, et du rdflexe tendineux, sur la ddcharge d'une unitd motrice isolde (UM) d'antagoniste ont ~td ~tudids. Les muscles suivants ont ~td testds: m. biceps fem., m. tibial ant. et m. triceps sural. Les potentiels d'UM dtaient enregistr~s sous contraction volontaire mdnag~e. Les histogrammes poststimulus des ddcharges d'UM ont ~td tracds et
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la durde des intervalles interspikes dans cette pdriode post-stimulus a dtt~ comparde avec celle de la pdriode prdcddant le stimulus. Lots de la stimulation dlectrique du nerf (affdrents Ia), une nette inhibition rdciproque a ~td observde, pour les UM des 3 muscles testds. Dans quelques cas, une action excitatrice ldgdre a pu ~tre notde, en m~me temps que l'inhibition rdciproque. Le rdflexe tendineux patellaire dtait accompagnd par un net effet excitateur des UM de l'antagoniste. L'efficacitd de la volde inhibitrice s'est montrd ddpendre de l'instant off survenait la volde ~ l'intdrieur de l'intervalle. Un allongement de l'intervalle n'dtait observd que lorsqu'un influx inhibiteur arrivait t o u t pros de sa fin. Les particularitds de l'inhibition rdciproque de la ddcharge de motoneurones, ainsi que les m~canismes de l'effet excitateur des antagonistes qui accompagne le rdflexe tendineux sont discutds. The author is grateful to Dr. R.S. Person for valuable discussion.
References Agarwal, G.C. and Gottlieb, G.L. The muscle silent period and reciprocal inhibition in man. J. NeuroL Neurosurg. Psychiat., 1972, 35: 72--76. Agarwal, G.C., Berman, B.M., LShnberg, P. and Stark, L. Studies in postural control systems. II. Tendon jerk input. IEEE Trans. Syst. Sci. Cybernet., 1970, SSC-6 : 122--126. Ashby, P. and LaBelle, K. Effects of extensor and flexor group I afferent volleys on the excitability of individual soleus motoneurones in man. J. Neurol. Neurosurg. Psychiat., 1977, 40; 910--919. Ashby, P. and Zilm, D. Synaptic connections to individual tibiatis anterior motoneurones in man. J. Neurol. Neurosurg. Psychiat., 1978, 41: 684---689. Delwaide, P.J. Human monosynaptic reflexes and presynaptic inhibition. An interpretation of spastic hyperreflexis. In: J.E. Desmedt (Ed.), New Developments in Electromyography and Clinical Neurophysiology, Vol. 3. Karger, Basel, 1973: 508-522. Eccles, J.C., Eccles, R.M. and Lundberg, A. The convergence of monosynaptic excitatory afferents on to m a n y different species of alpha-motoneurones. J. Physiol. (Lond.), 1957, 137: 22--50.
REFLEX EFFECTS ON MOTOR UNITS OF ANTAGONIST Gurfinkel, V.S. and Paltsev, E.J. Antagonistic muscle response to the tap on the tendon. Neurofisiologiya (Kiev), 1973, 5: 70--76. Hagbarth, K.-E. Post-tetanic potentiation of myotatic reflexes in man. J. Neurol. Neurosurg. Psychiat., 1962, 25: 1--10. Hultborn, H. Transmission in the pathway of reciprocal Ia inhibition to motoneurones and its control during the tonic stretch reflex. In: S. Homma (Ed.), Understanding the Stretch Reflex. Progress in Brain Research, Vol. 44. Elsevier, Amsterdam, 1976 : 235--254. Kots, Ja.M. On the nature of tendon reflex. Fiziol. (~elov., 1976, 2: 599--610. Kots, Ja.M. and Zimkov, V.I. On supraspinal control over segmentary centres of muscles-antagonists in man. III. 'Tuning' of a spinal apparatus of reciprocal inhibition during the organization of voluntary movement. Biofizika, 1971, 16: 1085--1092. Kranz, H., Adorjani, C. and Baumgartner, G. The effect of nociceptive cutaneous stimuli of human motoneurones. Brain, 1973, 96: 571--590. Kudina, L.P. Effect of tendon reflex on motoneurons of human antagonistic muscle. Neurofiziologiya (Kiev), 1976, 8: 624--631. Kudina, L.P. Study of the reciprocal inhibition on discharging human m o t o r units. Neurofiziologiya (Kiev) 1978, 10: 626--635. Mizuno, Y., Tanaka, R. and Yanagisawa, N. Reciprocal group I inhibition on triceps surae motoneurons in man. J. Neurophysiol., 1971, 34: 1010--1017. Paillard, J. R~flexes et R~gulations d'Origine Proprioceptive chez l'Homme, l~tude Neurophysiologique et Psychophysiologique. Librairie Arnette, Paris, 1955.
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Person, R.S. Antagonistic Muscles in Human Movements. Nauka, Moscow, 1965. Person, R.S. Study of H-reflex of human hand muscles by means of post-stimulus histogram method. Neurofiziologiya (Kiev), 1977, 9: 647--650. Person, R.S. and Kozhina, G.V. Study of orthodromic and antidromic effects of nerve stimulation on single motoneurones of human hand muscles. EMG clin. Neurophysiol., 1978, 18: 437--456. Person, R.S. and Kudina, L.P. On 'tuning' mechanism of segmentary apparatus before voluntary movement. Neurofiziologiya (Kiev), 1978, 10: 322--324. Rao, V.R. Reciprocal inhibition: inapplicability to tendon jerks. J. Postgrad. Med., 1965, 11: 123-125. Tanaka, R. Reciprocal Ia inhibition during voluntary movements in man. Exp. Brain Res., 1974, 21: 529--540. Tanaka, R. Reciprocal Ia inhibition and voluntary movements in man. In: S. Homma (Ed.), Understanding the Stretch Reflex. Progress in Brain Research, Vol. 44. Elsevier, Amsterdam, 1976: 291--302. Teasdall, R.D., Languth, H.W. and Magladery, J.W. Electrophysiological studies of reflex activity in patients with lesions of the nervous system. IV. A note on the tendon jerk. Bull. Johns Hopk. Hosp., 1952, 91: 267--275. Willis, W.D., Tate, G.W., Ashworth, R.D. and Willis, J.C. Monosynaptic excitation of m6toneurons of individual forelimb muscles. J. Neurophysiol., 1966, 29: 410--424.
Eh<'troencephalography and Clinical Neurophysiology, 1980, 5 0 : 2 1 4 -22~ © Elsevier/North-Holland Scientific Publishers, Ltd.
R E F L E X EFFECTS OF MUSCLE A F F E R E N T S ON ANTAGONIST STUDIED ON SINGLE FIRING MOTOR UNITS IN MAN L.P. KUDINA Institute for Problems o f i n formation Transmission, U.S.S.R. Academy o f Sciences, Moscow (U.S.S.R.) (Accepted for publication: May 7, 1980)
The reciprocal inhibition of antagonist motoneurones caused b y Ia afferents has been an object of intense study since Sherrington's works. Experiments on animals have made it possible to reveal the convergence of excitatory and inhibitory drives on Ia inhibitory interneurones as well as to consider some functional aspects of such convergence (see Hultborn 1976). However, the part played b y the reciprocal inhibition in m o t o r control is not clear and even revealing the inhibition in intact human beings is very difficult. Studies carried o u t b y various researchers have yielded contradictory results. Opinions differ on the effect of electric stimulation of a mixed nerve (Ia afferents) on a human antagonist. According to Tanaka et al. (Mizuno et al. 1971; Tanaka 1974, 1976), reciprocal inhibition, estimated by its effect on the amplitude of the antagonist monosynaptic response, is absent in healthy man at rest b u t is observed under voluntary contraction of the muscle whose afferents are stimulated. On the other hand, the same technique employed by other researchers (Paillard 1955; Kots and Zhukov 1971) revealed a distinct reciprocal inhibition at rest. Agarwal and Gottlieb (1972), Ashby and LaBeUe (1977) and Ashby and Zilm (1978) described the reciprocal inhibitory effect of electric stimulation of Ia afferents on the voluntary activity of the antagonist. Hagbarth (1962) reported, however, that the reciprocal inhibition o f the antagonist voluntary activity is distinctly
revealed only after tetanization of Ia afferents. When a different method of activating Ia afferents was used, i.e., that of eliciting the tendon reflex, the excitatory effect on the antagonist was observed in summated EMGs instead of the expected reciprocal inhibition (Rao 1965; Agarwal et al. 1970; Gurfinkel and Paltsev 1973). Thus, the efficiency of reciprocal inhibition in intact human beings is questionable. The aim of the present work is to study the effect of electric stimulation of a nerve and of tendon percussion on single m o t o r units (MUs) of a human antagonist and to analyse the characteristics of the reciprocal inhibition effect on firing motoneurones. Some of the results were reported earlier (Kudina 1976, 1978).
Methods The study was carried o u t on 6 healthy volunteers. The subject sat comfortably in an armchair and the knee angle was 90 ° . The nerves innervating m. rectus fem., m. soleus and m. tibialis ant, (we shall refer to these as agonists) were electrically stimulated and the effect of the stimulation on their antagonists -- m. biceps fern., m. tibialis ant., m. soleus and m. gastrocnemius m e d . - was studied. The stimuli were applied to n. femoralis at the inguinal ligament, to n. tibialis at
REFLEX EFFECTS ON MOTOR UNITS OF ANTAGONIST the popliteal fossa and to n. peroneus at the level of the caput fibulae, respectively. Surface bipolar electrodes were used and single stimuli with a duration of 1 msec were applied (up to 90--150 stimuli in each experiment). As is known, when the strength of mixed nerve stimulation increases the monosynaptic reflex gradually diminishes and at high stimulus strengths completely disappears. Also, in some muscles (including m. tibialis ant.) the H reflex is either very weak or absent at high as well as at low stimulus strengths. In all such cases we presumed that the effect of afferent volleys on Ia inhibitory interneurones was not suppressed. Hence, we used stimuli evoking the H reflex in the agonist (not less than 20% of Hmax) or, in the absence of the H reflex, the M response (not less than 10% of Mmax) or both. The knee tendon reflex was evoked by a hammer and its effect on the antagonist was also studied. The EMG of the agonist was picked up b y surface electrodes. Stimulation of afferents was carried o u t during weak voluntary contraction of the investigated antagonist. Most of the experiments were made with the f o o t freely moving; in some experiments it had to be fixed to avoid displacement of the electrodes. The potentials of single MUs of the antagonist were picked up by bipolar needle electrodes. MUs were identified visually. Post-stimulus histograms for 162 MUs in 24 experiments were plotted. The bin width was 5 msec; bin deviations were considered reliable ( P < 0.05) if the number of potentials within a bin went b e y o n d the limits of n + 2 x/fi, where fi is the average number of potentials in a bin of the pre~stimulus segment of the histogram. In 19 experiments the effect of nerve stimulation on the duration of interspike intervals of 43 MUs was also analysed. The mean interval of background activity was calculated as the average of 5--6 intervals preceding each stimul u s and the duration of the interval within which the afferent volley occurred was expressed as percentage of the mean interval in the pre-stimulus period.
215
Results
(a) The inhibitory effect The mean frequency of the background firing of single MUs in the voluntarily contracted antagonist varied from 6 to 12 imp/ sec. During stimulation of n. femoralis and n. tibialis evoking the H reflex, the H reflex together with the M response, or only the latter in the agonist, the antagonist MU interspike interval within which the afferent volley arrived often became longer (Fig. l a : MU marked b y a cross, Fig. l b ) . This proved the existence of the reciprocal inhibitory effect on the antagonist MUs. The stimulation of n. peroneus, evoking the M response in m. tibialis ant. (the H reflex was absent or very weak in this muscle), also caused lengthening of MU interspike intervals in the antagonist (Fig. lc). In some cases, however, the dura-
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Fig. 2. Post-stimulus histograms of the potentials of the antagonist's firing MUs during nerve stimulation. a: 26 MUs of m. biceps fem. during stimulation of n. femoralis (7 experiments), b: 58 MUs of m. tibialis ant. during stimulation of n. tibialis (6 experiments). c: 48 MUs of m. triceps surae during stimulation of n. peroneus (6 experiments), x-axis = time (0 = moment of stimulation); y-axis = number of MU impulses (shaded parts of columns = impulses of newly recruited MUs). Horizontal bar under the histogram denotes the period of reliable decrease of MU discharge probability (P < 0.05), i.e., period of reciprocal inhibition. t i o n o f t h e i n t e r s p i k e interval w i t h i n w h i c h a volley arrived did n o t b e c o m e longer (Fig. l a : MU m a r k e d b y circles). F o r a m o r e reliable demonstration of reciprocal inhibition posts t i m u l u s h i s t o g r a m s w e r e used. In all t h e e x p e r i m e n t s t h e h i s t o g r a m s s h o w e d a reliable d e c r e a s e in t h e p r o b a b i l i t y o f MU discharge a f t e r a s t i m u l u s , i.e., t h e histograms revealed the inhibitory effect (Fig. 2). T h e l a t e n c y o f i n h i b i t i o n was e i t h e r e q u a l t o t h a t o f t h e H r e f l e x o f t h e agonist or e x c e e d e d it b y several m i l l i s e c o n d s ( n o t m o r e t h a n a bin, i.e. 5 m s e c ) . T h e i n h i b i t i o n was
clearly e x p r e s s e d in all the 3 cases, i.e. w h e ~ either H or M r e s p o n s e o f t h e agonist or b o t h w e r e r e c o r d e d . This shows t h a t w h e n t h e H r e s p o n s e is d i m i n i s h e d d u e to an increased s t i m u l u s s t r e n g t h , as well as w h e n it is a b s e n t {in m. tibialis ant.), t h e a f f e r e n t volley c o m i n g to la i n h i b i t o r y i n t e r n e u r o n e s is n o t suppressed. At a s u f f i c i e n t s t i m u l u s s t r e n g t h t h e inhibit o r y e f f e c t was f o l l o w e d b y e x c i t a t i o n , w h i c h m a n i f e s t e d itself in an increased discharge p r o b a b i l i t y o f firing MUs a n d in t h e recruitm e n t o f n e w o n e s (Fig. 2). T h e e x c i t a t o r y e f f e c t was m o r e p r o n o u n c e d w i t h a freely moving foot. T h e d u r a t i o n o f i n h i b i t i o n in p o s t - s t i m u l u s h i s t o g r a m s f o r MUs o f m . biceps f e m . a n d m. t r i c e p s surae was 1 0 - - 2 0 m s e c , a value close to t h a t o f t h e agonist m o n o s y n a p t i c r e s p o n s e (H reflex) in EMG. T h e i n h i b i t i o n lasted m u c h longer ( 2 5 - - 5 0 m s e c ) in p o s t - s t i m u l u s histog r a m s f o r MUs o f m . tibialis ant. On stimulat i o n o f n. tibialis t h e E M G o f m . tibialis ant. o f t e n s h o w e d , a p a r t f r o m t h e e f f e c t o f reciprocal i n h i b i t i o n , t h e r e c r u i t m e n t o f n e w MUs with the latency of the M response and, sometimes, w i t h t h a t o f t h e H reflex. This shows t h a t d u r i n g s t i m u l a t i o n o f n. tibialis at the p o p l i t e a l fossa e f f e r e n t a n d a f f e r e n t fibres o f n. p e r o n e u s w e r e also s t i m u l a t e d . I t is possible t h a t in this case t h e i n h i b i t o r y e f f e c t o f n. peroneus stimulation (recurrent inhibition?) was a d d e d to t h e r e c i p r o c a l i n h i b i t i o n . T h e r e c i p r o c a l i n h i b i t i o n in p o s t - s t i m u l u s h i s t o g r a m s was m u c h s h o r t e r t h a n t h e interspike interval o f MUs. I t was i n t e r e s t i n g to s t u d y t h e e f f e c t s o f such i n h i b i t i o n o n t h e dur a t i o n o f t h e i n t e r s p i k e interval in w h i c h it o c c u r r e d . T h e changes in t h e interval d u r a t i o n o f MUs o f m . biceps f e m . a n d m . t r i c e p s surae did n o t f o l l o w a d e f i n i t e p a t t e r n : a l o n g w i t h l e n g t h e n e d intervals t h e r e w e r e q u i t e a n u m b e r o f intervals w i t h i n t h e limits o f fluctuat i o n o f t h e m e a n interval a n d t h e r e w e r e s o m e s h o r t e r intervals as well (Fig. 3b}. In t h o s e experiments where facilitation after inhibition was well p r o n o u n c e d t h e m a j o r i t y o f intervals were short.
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it proved ineffective: the interval either remained unchanged or became shorter (Fig. 3c, the left part of the diagram). The latter took place if facilitation following inhibition occurred within the same interspike interval. The majority of intervals of m. tibialis ant. MUs (the inhibition duration in the poststimulus histogram 25--50 msec and the facilitation following it rather weak) were lengthened and the efficiency of inhibition increased when the volley occurred closer to the end of the interval (Fig. la: MU marked by a cross).
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Fig. 3. Different methods of revealing reciprocal inhibition (MUs of m. gastrocnemius med., stimulation of n. peroneus), a: post-stimulus histogram (3 MUs); arrow shows latency of H reflex, other designations same as on Fig. 2. b: statistical analysis of interspike intervals of one of 3 MUs presented in histogram (155 tests): duration of interval within which volley arrived as percentage of mean interval of background firing• c: same MU as in b: dependence between volley efficiency and m o m e n t of volley arrival within an interspike interval, y-axis = same values as in b; x-axis = time between preceding MU impulse and m o m e n t of volley arrival as percentage of background mean interval.
(b) The excitatory effect In contrast to the H reflex volley the tendon reflex volley had an excitatory effect on the antagonist MUs. In 5 experiments on 3 subjects the activity of 30 MUs of m. biceps fem. during the knee reflex was analysed. A typical result is seen in Fig. 4. The response to a volley included the discharge of firing MUs (often with a shortened interspike interval) and of newly recruited ones. The response was synchronous with the agonist tendon reflex. Thus, during the evoked tendon reflex,
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The statistical analysis showed that the efficiency of an inhibitory volley depended on the moment within an interspike interval at which this volley occurred. This moment was determined as described below. The latency of the inhibitory effect was found in the post-stimulus histogram and the duration of the interval between the Iast regular impulse and the arrival of the inhibitory volley was calculated for each test as a percentage of the mean interval of the background firing. When inhibition lasted 10--20 msec the lengthening of an interspike interval was observed if the inhibitory volley occurred closer to the end of the interval (Fig. 3c, the right part of the scatter diagram). If the inhibitory volley occurred in the first part of the interval
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Fig. 5. Revealing weak excitatory drive, caused by nerve stimulation, on firing MUs of the antagonist (m. biceps fern. and m. triceps surae) by analysis of interspike intervals, a: duration of MU interspike intervals, ending synchronously with H reflex of the agonist as percentage of background mean interval (data of 10 experiments); though no increase of discharge probability is revealed in post-stimulus histograms, the shortening of intervals is reliable, b: example of interval shortening (circle denotes premature discharge); calibration = 200 pV, other designations as in Fig. 1.
in contrast to electrical activation of Ia afterents, no reciprocal inhibition of the antagonist MUs was revealed. Returning to the experiments with nerve stimulation and comparing the latency of the agonist H reflex and that of reciprocal inhibition in the post-stimulus histograms we noticed that sometimes the inhibitory effect was delayed b y a bin. The question arises whether the lengthened latency was due to interference with the excitatory drive. An attempt has been made to reveal this latter. As mentioned above, the facilitation of m. tibial ant. MUs, synchronous with the H response of m. soleus, can probably be ascribed to a side effect of n. tibialis stimulation at the popliteal fossa on n. peroneus afferents. For m. biceps fem. and triceps surae this is hardly possible since the nerves innervating them are located quite far from the stimulated areas. Therefore only experiments on these t w o muscles were considered. The
durations of interspike intervals which ended within the bin of the histogram preceding inhibition {i.e., coinciding with the beginning of the agonist H response) and in the following bin (in cases of incomplete inhibition) were analysed. One hundred and sixty interspike intervals from 10 experiments were analysed and a statistically significant (P < 0.001) shortening of intervals with respect to the mean background interval was revealed (Fig. 5). This shows the presence of facilitation in motoneurones, b u t the facilitating volley was, apparently, weak. In combination with the reciprocal inhibition, the inhibitory drive was prevalent. Therefore the probability of MU discharge did not increase in the corresponding bin. The excitatory effect was manifested only in the somewhat lengthened latency of inhibition in the post-stimulus histogram and in shortening of some interspike intervals, which could be revealed only statistically.
REFLEX EFFECTS ON MOTOR UNITS OF ANTAGONIST Discussion
The literature shows that one meets with serious difficulties in trying to reveal, in intact man, such a widely known phenomenon as reciprocal inhibition. The method of post-stimulus histograms plotted for single MUs has made it possible to reveal it in all the 3 investigated muscles and to determine its latency and duration. The sensitivity of the method in the study of excitatory and inhibitory effects on a firing motoneurone has been shown by some other authors {Ashby and LaBelle 1977; Person 1977; Ashby and Zilm 1978; Person and Kozhina 1978). Employing this method Ashby and his co-authors revealed reciprocal inhibition of m. soleus and of m. tibialis ant. MUs. In our study the method of post-stimulus histograms combined with the analysis of MU interspike intervals has allowed us not only to reveal the reciprocal inhibition but also to understand the peculiarities of its action on a firing motoneurone. In particular, the dependence o f the inhibitory efficiency on the moment of its occurrence within an interspike interval has been shown. A similar dependence under nociceptive cutaneous stimulation was earlier reported by Kranz et al. (1973). However, this dependence is especiaUy significant in the case of reciprocal inhibition since it is considerably shorter than an interspike interval. The latter became longer only when an inhibitory volley arrived closer to the forthcoming MU discharge than to a previous one. In other cases the inhibitory volley was ineffective (the interval remained unchanged). Thus,. the changes in the duration of an interspike interval cannot be a sufficient criterion of inhibition of such short duration. Among the investigated muscles, in m. tibialis ant. the H reflex is practically absent at rest. Nevertheless stimulation of its mixed nerve of sufficient strength evoked a distinct reciprocal inhibition. It is not quite clear why the H reflex is absent or small in some muscle.
219
Some authors believe that there exists tonic presynaptic inhibition {complete or partial) of this reflex in intact human beings (Delwaide 1973; Person and Kozhina 1978; Person and Kudina 1978). If this is true then our data on antagonist reciprocal inhibition in the absence of the agonist H reflex may be attributed to the absence of depression of the Ia afferent endings activating the Ia interneurones. The tendon reflex is generally believed to be evoked by Ia afferents, like the H reflex. However, there are data showing that these two reflexes are somewhat different (Teasdall et al. 1952; Kots 1976). As far as their influence on the antagonist is concerned, the tendon reflex, unlike the H reflex, has a distinct excitatory effect (Rao 1965; Agarwal et al. 1970; Gurfinkel and Paltsev 1973). A hypothesis was advanced that activation of the antagonist by the evoked tendon reflex is caused via the collaterals of the agonist Ia afferents (Gurfinkel and Paltsev 1973; Kudina 1976}. It is based on data showing the existence of excitatory monosynaptic inputs from Ia afferents to the antagonist motoneurones (Eccles et al. 1957; Willis et al. 1966). Some data obtained in this study confirm this view: under electrical stimulation of the nerve a weak excitatory influence, in some cases, preceded the reciprocal inhibition. Under the evoked tendon reflex the excitatory drive on the antagonist was, possibly, augmented by other groups of afferents (Ib and II). The demonstration of reciprocal inhibition during artificial synchronous stimulation of afferent fibres does not solve the problem of its functional role in motor control. As shown by Tanaka (1974) with relatively weak stimuli (apparently more adequate than strong ones), reciprocal inhibition was absent at rest and was revealed only during voluntary contraction of the agonist. Electromyographic study of natural movements in man gives many examples of simultaneous activity of antagonistic muscles, in particular during the formation of motor skills, during walking, etc. (see Person 1965).
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Summary The effects of electrical stimulation of mixed nerves and of the evoked tendon reflex on single firing MUs of antagonists were investigated. The following muscles were studied: m. biceps fem., m. tibialis ant. a n d m. triceps surae. Under a weak voluntary contraction MU potentials were picked up. Post-stimulus histograms of MU potentials were plotted and the duration of interspike intervals in the post-stimulus period was compared with that in the prestimulus period. Under electrical stimulation of the nerve (Ia afferents) a distinct reciprocal inhibition was observed on MUs of all the 3 investigated muscles. In some cases a weak excitatory drive could be revealed along with the reciprocal inhibition. The tendon (knee) reflex was accompanied by a distinct excitatory effect on MUs of the antagonist. The dependence between the efficiency of the inhibitory volley and the m o m e n t within an interspike interval at which the volley arrived was found. The lengthening of an interval was observed only when an inhibitory drive occurred close to its end. The peculiarities of reciprocal inhibition in the firing motoneurone, as well as the possible mechanism of the excitatory effect on the antagonist accompanying the tendon reflex, are discussed.
Rdsumd Effets rdflexes des affdrents musculaires sur l'antagoniste, dtudids sur des unitds motrices isoldes chez l'homme Les effets de la stimulation dlectrique des nerfs mixtes, et du rdflexe tendineux, sur la ddcharge d'une unitd motrice isolde (UM) d'antagoniste ont ~td ~tudids. Les muscles suivants ont ~td testds: m. biceps fem., m. tibial ant. et m. triceps sural. Les potentiels d'UM dtaient enregistr~s sous contraction volontaire mdnag~e. Les histogrammes poststimulus des ddcharges d'UM ont ~td tracds et
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la durde des intervalles interspikes dans cette pdriode post-stimulus a dtt~ comparde avec celle de la pdriode prdcddant le stimulus. Lots de la stimulation dlectrique du nerf (affdrents Ia), une nette inhibition rdciproque a ~td observde, pour les UM des 3 muscles testds. Dans quelques cas, une action excitatrice ldgdre a pu ~tre notde, en m~me temps que l'inhibition rdciproque. Le rdflexe tendineux patellaire dtait accompagnd par un net effet excitateur des UM de l'antagoniste. L'efficacitd de la volde inhibitrice s'est montrd ddpendre de l'instant off survenait la volde ~ l'intdrieur de l'intervalle. Un allongement de l'intervalle n'dtait observd que lorsqu'un influx inhibiteur arrivait t o u t pros de sa fin. Les particularitds de l'inhibition rdciproque de la ddcharge de motoneurones, ainsi que les m~canismes de l'effet excitateur des antagonistes qui accompagne le rdflexe tendineux sont discutds. The author is grateful to Dr. R.S. Person for valuable discussion.
References Agarwal, G.C. and Gottlieb, G.L. The muscle silent period and reciprocal inhibition in man. J. NeuroL Neurosurg. Psychiat., 1972, 35: 72--76. Agarwal, G.C., Berman, B.M., LShnberg, P. and Stark, L. Studies in postural control systems. II. Tendon jerk input. IEEE Trans. Syst. Sci. Cybernet., 1970, SSC-6 : 122--126. Ashby, P. and LaBelle, K. Effects of extensor and flexor group I afferent volleys on the excitability of individual soleus motoneurones in man. J. Neurol. Neurosurg. Psychiat., 1977, 40; 910--919. Ashby, P. and Zilm, D. Synaptic connections to individual tibiatis anterior motoneurones in man. J. Neurol. Neurosurg. Psychiat., 1978, 41: 684---689. Delwaide, P.J. Human monosynaptic reflexes and presynaptic inhibition. An interpretation of spastic hyperreflexis. In: J.E. Desmedt (Ed.), New Developments in Electromyography and Clinical Neurophysiology, Vol. 3. Karger, Basel, 1973: 508-522. Eccles, J.C., Eccles, R.M. and Lundberg, A. The convergence of monosynaptic excitatory afferents on to m a n y different species of alpha-motoneurones. J. Physiol. (Lond.), 1957, 137: 22--50.
REFLEX EFFECTS ON MOTOR UNITS OF ANTAGONIST Gurfinkel, V.S. and Paltsev, E.J. Antagonistic muscle response to the tap on the tendon. Neurofisiologiya (Kiev), 1973, 5: 70--76. Hagbarth, K.-E. Post-tetanic potentiation of myotatic reflexes in man. J. Neurol. Neurosurg. Psychiat., 1962, 25: 1--10. Hultborn, H. Transmission in the pathway of reciprocal Ia inhibition to motoneurones and its control during the tonic stretch reflex. In: S. Homma (Ed.), Understanding the Stretch Reflex. Progress in Brain Research, Vol. 44. Elsevier, Amsterdam, 1976 : 235--254. Kots, Ja.M. On the nature of tendon reflex. Fiziol. (~elov., 1976, 2: 599--610. Kots, Ja.M. and Zimkov, V.I. On supraspinal control over segmentary centres of muscles-antagonists in man. III. 'Tuning' of a spinal apparatus of reciprocal inhibition during the organization of voluntary movement. Biofizika, 1971, 16: 1085--1092. Kranz, H., Adorjani, C. and Baumgartner, G. The effect of nociceptive cutaneous stimuli of human motoneurones. Brain, 1973, 96: 571--590. Kudina, L.P. Effect of tendon reflex on motoneurons of human antagonistic muscle. Neurofiziologiya (Kiev), 1976, 8: 624--631. Kudina, L.P. Study of the reciprocal inhibition on discharging human m o t o r units. Neurofiziologiya (Kiev) 1978, 10: 626--635. Mizuno, Y., Tanaka, R. and Yanagisawa, N. Reciprocal group I inhibition on triceps surae motoneurons in man. J. Neurophysiol., 1971, 34: 1010--1017. Paillard, J. R~flexes et R~gulations d'Origine Proprioceptive chez l'Homme, l~tude Neurophysiologique et Psychophysiologique. Librairie Arnette, Paris, 1955.
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Person, R.S. Antagonistic Muscles in Human Movements. Nauka, Moscow, 1965. Person, R.S. Study of H-reflex of human hand muscles by means of post-stimulus histogram method. Neurofiziologiya (Kiev), 1977, 9: 647--650. Person, R.S. and Kozhina, G.V. Study of orthodromic and antidromic effects of nerve stimulation on single motoneurones of human hand muscles. EMG clin. Neurophysiol., 1978, 18: 437--456. Person, R.S. and Kudina, L.P. On 'tuning' mechanism of segmentary apparatus before voluntary movement. Neurofiziologiya (Kiev), 1978, 10: 322--324. Rao, V.R. Reciprocal inhibition: inapplicability to tendon jerks. J. Postgrad. Med., 1965, 11: 123-125. Tanaka, R. Reciprocal Ia inhibition during voluntary movements in man. Exp. Brain Res., 1974, 21: 529--540. Tanaka, R. Reciprocal Ia inhibition and voluntary movements in man. In: S. Homma (Ed.), Understanding the Stretch Reflex. Progress in Brain Research, Vol. 44. Elsevier, Amsterdam, 1976: 291--302. Teasdall, R.D., Languth, H.W. and Magladery, J.W. Electrophysiological studies of reflex activity in patients with lesions of the nervous system. IV. A note on the tendon jerk. Bull. Johns Hopk. Hosp., 1952, 91: 267--275. Willis, W.D., Tate, G.W., Ashworth, R.D. and Willis, J.C. Monosynaptic excitation of m6toneurons of individual forelimb muscles. J. Neurophysiol., 1966, 29: 410--424.