thought to reflect complex interactions evoked by changes in afferent activity Southampton General Hospital, Southampton, S09 4XY
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1 J. Phy8iol. (1983), 337, pp With 6 text-ftgures Printed in Great Britain SPINAL INHIBITION IN MAN: DEPRESSION OF THE SOLEUS H REFLEX BY STIMULATION OF THE NERVE TO THE ANTAGONIST MUSCLE BY AMIRA EL-TOHAMY AND E. M. SEDGWICK From the Department of Clinical Neurophysiology, Wessex Neurological Centre, Southampton General Hospital, Southampton, S9 4XY (Received 23 July 1982) SUMMARY 1. A period of inhibition of the soleus H reflex, called D1 inhibition, follows stimulation of the nerve to the antagonist muscles, the peroneal nerve, in normal man. 2. The results confirm earlier descriptions of D1 and show an intracord latency of approximately 4-5 msec and a reduction of the H reflex by about 6 %. D1 reaches its maximum 15-2 msec after stimulation and its duration is more than 3 msec. 3. Effective stimuli were volleys of two to five pulses given as 1 msec duration bursts at a strength of 1-2 motor thresholds. Cutaneous afferents were ineffective and. the possibility that D1 is mediated by low threshold muscle afferents is discussed. 4. D1 produces the same proportions of inhibition of the H reflex when the H reflex is facilitated by plantarflexion or depressed by dorsiflexion. INTRODUCTION The soleus H reflex is easily recorded in man and has been employed as an index of monosynaptic excitability and of the different inhibitory mechanisms operating at cord segmental level. Tanaka (1974) showed that a conditioning volley to the peroneal nerve would produce three distinct and separate periods of inhibition of the soleus H reflex. The first, at condition-test intervals of -5 msec, was shown to be mediated by I a inhibitory interneurones. The second period from 5-8 msec was called D1 by Tanaka and likened to presynaptic inhibition seen in animals but it was not studied in detail. The third period of inhibition, D2, from 9-13 msec was thought to reflect complex interactions evoked by changes in afferent activity following a twitch of the ankle dorsiflexors. In this paper some of the properties of D1 are investigated and compared with inhibitory processes recorded in laboratory animals and in man. The possibility that D1 may be mediated by group II afferents is discussed. METHODS Experiments were carried out on fifteen normal unpaid volunteers aged between 24 and 45 years. The procedures described were approved by the hospital ethical committee. The subjects were positioned supine and comfortably on a couch with head and shoulders raised
2 498 A. EL-TOHAMY AND E. M. SEDGWICK and hip and knee flexed by supporting pillows. Our methods closely followed the recommendations for recording H reflexes set out in Desmedt (1973). The soleus H reflex was obtained by stimulating the tibial nerve at the popliteal fossa using a unifocal cathode electrode 1 mm in diameter positioned over the nerve. Pulses of 1 msec duration were passed between this and a large e.c.g. plate electrode placed just above the patella. The peroneal nerve was stimulated through a bipolar electrode pair 32 mm apart positioned over the nerve at the head of the fibula with the proximal electrode acting as the cathode. Volleys of three pulses, -5 msec in duration, were given by a Digitimer high voltage stimulator (type 372) controlled by a Digitimer pulse programmer. Position indicator Peroneal nerve Tibial nerve j > ~~~~~~~~~~Weights Soleus - recording Fig. 1. The disposition of the stimulating and recording electrodes on the leg is shown. A bipolar electrode was used to stimulate the peroneal nerve and a unifocal electrode arrangement for the tibial nerve. In those experiments involving dorsiflexion, the foot was made to support its own and added weights; position was maintained with the help of a goniometer whose scale was visible to the subject. Recording from the soleus muscle was by Copland-Davies clip-on electrodes placed 3 mm apart over the soleus muscle with the proximal electrode approximately 4 mm above the insertion of the heads of gastrocnemius into the Achilles tendon (Hugon, 1973; Desmedt, 1973). The subject was earthed by a band electrode placed around the leg between the stimulating and recording electrodes. The signal was amplified using a band width of 1-1 Hz (3db) and monitored on a storage oscilloscope. The peak to peak amplitude of the H reflex was detected and displayed in numerical form by a purpose built microprocessor (Bragg, 1978). In certain experiments involving muscle activity, isometric voluntary contractions were produced against loads attached to the foot as shown in the diagram (Fig. 1). A goniometer aided the subject in maintaining a constant angle of the ankle. Precautions were taken to ensure the comfort and relaxation of the subject at all times and the duration of recording sessions was limited to achieve this. Changes in stimulation due to movement of the electrodes relative to the nerves were checked carefully and repeatedly by determining thresholds, checking the size of the control H reflex and by monitoring the size and shape of the accompanying direct motor responses. Any run during which these conditions changed was discarded. Stimulation voltages were set by and are expressed in multiples of the motor threshold. The motor threshold was determined by visual inspection and palpation of the muscle and was taken as the point at which a muscle contraction could just be detected. Sensory thresholds were determined in some experiments. Stimulation of the tibial nerve was adjusted so that the H reflex was about 7-8 % of maximum. At this strength there was usually a small direct motor response which was useful for checking the constancy of the stimulus. The H reflex is variable even under the most rigorously controlled conditions; all readings presented here are the mean of at least ten trials and
3 A SPINAL INHIBITION IN MAN 499 s.e. of the means are given in the Figures. The first three to five responses in all runs were discarded to exclude H reflex changes due to the novelty of the stimulus. The H-reflex recovery curve after a single shock has been extensively studied and in some cases it takes 1 see to recover completely. We have used an interstimulus time of3 see at which time the H reflex is 9 % recovered. This seemed a reasonable compromise to keep the duration of the experiments down to an acceptable level. 4-,o 2 A 12 Normal subject 1 I I (Control H-reflex) - (U E x 4- Ir 5k O E Condition-test interval (msec) 12 B L. 4- U - Q E x ) 2 p (Control H-reflex) Condition-test interval (msec) Fig. 2. Inhibition of the H reflex is shown following stimulation of the peroneal nerve with a volley of three pulses at 1-5 motor threshold. A, results on one normal subject who showed I a reciprocal inhibition at rest between and 5 msec. D, is the inhibitory period beginning at 5 msec and reaching maximum at 15-2 msec. B, shows the mean D, obtained in fifteen normal subjects by stimulating the peroneal nerve at 1-5 motor threshold with a volley of three pulses given during a 1 msec gate ending at time = on the abscissa. Means + S.E. of means are plotted. The control plots represent the H-reflex amplitude with no conditioning peroneal stimulation recorded before and after each experimental run. RESULTS Inhibition of the H reflex by a preceding stimulus to the peroneal nerve is shown in Fig. 2. A volley of three pulses at 2/sec was delivered during a 1 msec gate. The condition-test interval given on the abscissa is the time between the end of the conditioning volley and the test stimulus to the tibial nerve. Two periods of inhibition
4 5 A. EL-TOHAMY AND E. M. SEDG WICK are shown. The first lasts 5 msec and is seen in subjects at rest only rarely. Tanaka (1974), showed that this was produced by the Ia inhibitory interneurone and it is not considered further in this paper. The second period of inhibition, called D1 by Tanaka, lasts from 5 to more than 3 msec but is maximal at 15-2 msec. This period is followed immediately by a third inhibition (not shown) which has not been studied by Tanaka (1974), or ourselves. We shall refer to the second period of inhibition as D1; Tanaka suggested that it is a presynaptic inhibition, a point we shall return to in the discussion. D, was present in every normal subject studied although the degree of inhibition was variable. This is not surprising as we made no attempt to achieve maximum inhibition by adjusting the stimulus parameters. Fig. 2 shows D1 for fifteen subjects and the degree of inhibition varied from 15 % to 9 %. The inhibition was maximal at 15 msec and the mean value was 57 %(S.D. = +23 %); that is the H reflex was reduced to 43 % of its control value. The time course and degree of D1 inhibition was constant in any one subject on different occasions. Three subjects were recorded on three separate days and D1 was shown to be very reproduceable. Stimulus intensity and D1 In three subjects the minimal stimulus intensity for D1 was determined. The results are shown in Fig. 3. Stimulus volleys to the peroneal nerve at or below motor threshold produced no inhibition, but strengths of 1-2 motor thresholds and above always produced D1. Therefore, D1 cannot be attributed to volleys in the Ia afferent fibres alone. Maximum D1 was produced by volleys of 1-6 motor thresholds, a further increase produced no additional inhibition. Number of pulses in conditioning volley Fig. 4 shows the raw data from one subject and a histogram plotted from three subjects when one to five pulses at 1-5 motor thresholds were given as the conditioning volley. The pulses were given at different rates but they all fell within a 1 msec gate. Attempts to produce D1 with only one conditioning pulse at 1-5 motor thresholds failed except in one subject where an inhibition of 25 % was recorded. Volleys of four and five pulses were most effective. The experiments reported next have utilized volleys of three pulses at 1P5 motor thresholds. This does not produce maximal inhibition. Similarly we used a sub-maximal H reflex. We did not wish to use stimuli which might saturate those physiological mechanisms which are responsible for the response. Further experiments were designed to show enhancement or reduction of D1 and it was felt that subtle changes might not be observed if maximal or supramaximal stimuli were used. Cutaneous afferent fibres and D1 Stimulation of the peroneal nerve at 1-5 motor thresholds produces a local pricking sensation. To exclude this as the stimulus producing D1, the stimulating electrodes were moved to lie alongside so as not to stimulate the peroneal nerve. D1 could not be produced by this stimulus even though a similar pricking sensation was felt. Neither an increase in stimulus strength nor an increase in the number of pulses in the volley changed the H reflex.
5 A SPINAL INHIBITION IN MAN 51 U 12 1 A Reflex control -a E x 3 Ir 5 I ol L Condition-test interval (msec) ) E x B 21- Control I ' Stimulus strength (motor threshold) Fig. 3. A, D1 following a volley of three pulses in 1 msec is shown at different stimulus strengths: -9, (@ ); 1-2, ( O) and 1-5 ( ) motor threshold. There was no D, with stimulus strengths less than 1 motor threshold. Mean and s.e. of the mean of three subjects. B, effect of changing the intensity of the conditioning stimulus for D1. The points are the mean and S.E. of the mean of one subject using a condition-test interval of 15 msec. The peroneal nerve contains cutaneous afferent fibres some of which join the sural nerve and supply the lateral aspect of the foot. The sural nerve was stimulated at the ankle below the lateral malleolus by means of the bipolar electrode. Stimuli up to six sensory thresholds with five pulses in the volley had no effect on the H reflex. During this experiment the condition-test intervals were adjusted to allow for the extra conduction time from the ankle; this is approximately 1 msec. Muscle activity The H reflex is enhanced and depressed by voluntary activity in the protagonist and antagonist muscles respectively (Hoffmann, 1918; Paillard, 1955; Gottlieb & Agarwal, 1971) and the degree of change in the H reflex is partly dependent upon the phasic characteristics of the voluntary movement (Gottlieb & Agarwal, 1973 a, b).
6 52 A. EL-TOHAMY AND E. M. SEDGWICK A 12 1 C 2 C o E M~ 4Q 2T E 1nPulse F 3% Control B~~~~~~~~o fple Conditioning volley Control Inhibition _s_*~~~~~~~oof\ pul lsees5 2 Pulses 25% R_ - ~ ~ Control 3 Pulses 45% ~~~~~~~ ~~~~~Control _<_ 4 Pulses 48% Control 5 Pulses 63% Fig. 4. A, the histogram shows the degree of D1 with increasing number of pulses in a 1 msec stimulating volley of the peroneal nerve at 1-5 motor thresholds. Data from three subjects have been plotted as means + S.E. of the mean. B, H reflex conditioned by peroneal nerve stimulation at 2 msec; 1-5 motor thresholds. Raw data are shown from one subject; each response consists of three superimposed traces.
7 A SPINAL INHIBITION IN MAN The degree of depression of the H reflex by voluntary contraction of the antagonist muscles is said to be dependent upon the degree of contraction (Gottlieb, Agarwal & Stark, 197; Gottlieb & Agarwal, 1971). This relationship was re-examined and found not to hold in these experiments. The results showed a constant degree of H-reflex inhibition regardless of the tension produced by muscle contraction. A band was attached round the foot and a string ran from it, over a potentiometric goniometer to a box containing weights up to 5 kg. The angle of the ankle joint was held at 12 degrees and the pretibial muscles had to be contracted to maintain this angle even against gravity. The joint angle was displayed on a meter and the subject instructed to keep a constant position despite the variations caused by H-reflex twitches. Control 1- g E kg Force of antagonist contraction Fig. 5. The effect of antagonist muscle contraction graded by weights on the soleus H-reflex amplitude. Columns indicate the mean + S.E. of the mean of five subjects. The weight supported by the antagonist is shown at the base of each column. 1 % represents the size of the H reflex when all muscles were at rest. During contraction, even against gravity, the H reflex in the soleus was depressed to less than 4 % of its control value and the depression remained at that value, even when kg weights were added to the ankle. Fig. 5 shows the results of experiments on five normal subjects. Less detailed experiments were done with plantarflexion. The subject voluntarily plantarflexed his ankle against the resistance offered by the experimenter's hand. A facilitation of approximately 15 % in the H reflex occurred. Several mechanisms must contribute to the H-reflex depression during contraction of the antagonist (see Discussion). One mechanism might be that responsible for D1. If this were the case then further stimulation of the peroneal nerve might be expected to produce little or no further inhibition for two possible reasons: (a), the volley fails to reach the cord because the nerve fibres responsible are already operating to capacity with naturally generated impulses; the 'busy line' reason. (b), the D1 mechanism may be heavily committed as one of the mechanisms producing the inhibition and an additional volley might fail because the mechanism was already fully operative.
8 s - E A. EL-TOHAMY AND E. M. SEDGWICK Experiments in which the pretibial muscle actively supported the ankle and additional weights and in which D1 was simultaneously measured by a peroneal volley, disclosed that D1 was still present to approximately the same degree and with the same time course. The H reflex, which was already inhibited by 6 % due to dorsiflexion was further depressed to approximately 3 % of its value during dorsiflexion. Furthermore D1 was independent of the force of muscle contraction up A 2 - Plantarflex ion 18. against resistance a) B E 14 - Dorsiflexion x 12 ) - 4, ~ -F n- I a 1a 1a 1I 1a _ IL _ kg -5 kg 1 kg 2 kg 3 kg 5 kg Muscle tension Fig. 6. Effect of dorsiflexion and plantarflexion on D1. In A, the ankle was plantarflexed against a moderate resistance. The first column of the pairs represents the size of the H reflex and the second column the size of the H reflex during D1. The left-hand pair represents the findings at rest and the right-hand pair the response during plantarflexion. In B, the H reflex during dorsiflexion of the ankle alone or ankle plus weights is set at 1 % and the corresponding H-reflex size during D1 shown alongside. Means + S.E. of the mean plotted. to 5 kg. The D1 mechanism was therefore not compromised during voluntary activity in the antagonist muscle. The converse experiment to determine whether D1 was present during plantarflexion showed that it was. DISCUSSION Mizuno, Tanaka & Yanagisawa (1971), first described a period of inhibition of the tibial H reflex following a volley of pulses in the peroneal nerve. They called this D, and noted that it began 5-7 msec after the last of three conditioning pulses to the peroneal nerve of a strength of 1' motor threshold but in one subject with a stimulus of -96 motor threshold. The duration of D1 was up to 6 or 9 msec (Tanaka, 1974).
9 A SPINAL INHIBITION IN MAN Our own findings are in agreement with those of the Japanese workers. The onset of D1 was always 5-7 msec after the last conditioning pulse rising to a maximum at 15-2 msec. Contrary to Mizuno et al. (1971) we were unable to detect D1 with conditioning pulses less than 1. motor threshold and a stimulus of 1P2 motor thresholds was the minimum. Even volleys of up to seven pulses at 1 motor threshold failed to produce a detectable D1. A conditioning volley of two or more pulses was essential and we only once succeeded in producing D1 with single conditioning pulses even at strengths up to 8 motor thresholds. It is not clear whether the Japanese workers ever produced D1 with a single conditioning pulse in normal subjects. Their figures of traces show usually three shock artefacts but Mizuno et al. (1971) show D1 in a patient with athetosis where apparently a single conditioning pulse was used. The requirement of a volley of impulses for D1 indicates that the inhibitory mechanism is activated only after temporal summation of two or more impulses. In these experiments it was not possible to time the arrival of the afferent volley at the cord, but the latencies suggest a delay of several milliseconds in the spinal cord after arrival of the peroneal volley and before D1 is expressed. This time could be as long as 15 msec (time from the start of the peroneal volley to the tibial nerve test stimulus). Some of this time is required for temporal summation of two or more impulses, some is lost because the peroneal nerve was stimulated further down the leg than the tibial and some is taken because the tibial test volley in I a fibres travels faster than the peroneal volley which is probably in group II afferents (see below). Group II fibres are known to conduct very slowly in the cord (Brown, 1981) and group II inhibition is at least disynaptic. Stauffer, Watt, Taylor, Reinking & Stuart (1976) measured an intracord delay of msec to the start of group II evoked i.p.s.p.s which had a rise time of msec. An intracord delay of several milliseconds is consistent with the known latency of group II inhibition and with presynaptic inhibition. The delay is considered too short to allow for a long-loop reflex mechanism but would be consistent with an oligosynaptic segmental pathway. 55 Nerve fibres mediating D1 Ia fibres. The Japanese school clearly demonstrated an I a reciprocal inhibition from the ankle dorsiflexors to the plantarflexors in normal subjects and in patients with upper motoneurone lesions (Mizuno etal ; Tanaka, 1972,1974,1976; Yanagisawa, Tanaka & Itoh, 1976; Yanagisawa & Tanaka, 1978; Yanagisawa, 198; Tanaka, 198). The conditioning stimuli for activating the Ia reciprocal inhibitory pathway was considerably less than I motor threshold and produced maximum effects at 115 motor thresholds. D1 did not appear until stimulus strengths were 1-2 motor thresholds. It can be concluded that Ia volleys are not sufficient to produce D1. Ib axons. A stimulus of 1-2 motor thresholds would be expected to excite a substantial proportion of I b axons from Golgi tendon organs of the pretibial muscles. lb inhibition, however, is to homologous and synergist motoneurones (Haase, Cleveland & Ross, 1975) whereas D1 is an inhibition of antagonist muscles. Recently, however, Jankowska, Johannisson & Lipski (1981 a, b) have shown Ib excitation of non-reciprocal inhibitory interneurones of lamina V-VI whose axons are widely distributed. However, inhibition of triceps surae from pretibial muscles was not
10 56 A. EL-TOHAMY AND E. M. SEDGWICK shown. PresumedIb inhibition of synergist ankle plantarflexors has been shown in man by Pierrot-Desielligny, Katz & Moria (1979). The distribution, stimulus requirements and timing ofib inhibition were quite different from those of D1. Group II axons. The human peroneal nerve contains a substantial number of cutaneous and articular afferent fibres (Sunderland, 1978). Some of these fibres were stimulated as evidenced by the subjects reporting referred sensations. Some of the sensory fibres from the peroneal nerve join the sural nerve which can be stimulated at the lateral malleolus of the ankle. This is a pure sensory nerve with no muscle afferents. The experiments showed no change in the H reflex after stimulation of the sural nerve. Recently, Delwaide, Crenna & Fleron (1981) showed a minor degree of inhibition after sural nerve stimulation which they attributed to group II afferents. This phenomenon awaits further evaluation, but from the available data on timing and stimulus strengths it seems probable that D1 cannot be evoked by low threshold cutaneous afferents. Group II muscle afferents. The central role of groupii muscle afferents is poorly understood. Lloyd (1943) and Eccles & Lundberg (1959) showed that stimulation of muscle nerves at groupii strength produced facilitation of flexors and inhibition of extensor motoneurones. Use of spike-triggered averaging by Stauffer et al. (1976) showed monosynaptic excitation of homonymous and synergist motoneurones but in only one of twenty-two antagonist motoneurones. However di- or tri-synaptic i.p.s.p.s were seen in five of twenty-two antagonist motoneurones. A stimulus of 1-2 motor thresholds would be expected to excite a significant proportion of groupii fibres but a stimulus of less than 1- motor threshold probably excites none. Fu & Schomberg (1974) showed that the thresholds for group II axons to lie mainly between 1 and 2 motor thresholds in the cat. Maximal D1 was seen at stimulus strengths of 1-6 motor thresholds. Neither thresholds nor conduction velocity of human group II fibres is known but it seems unlikely that stimulus strengths of 1-6 motor thresholds would recruit all group II fibres. Human neurophysiology. Although D1 was discovered some time ago, it has not been subject to detailed investigation. The I a interneurone inhibition, Renshaw inhibition and I b inhibition have already been investigated in man by techniques using the H reflex. Table 1 summarizes the properties of these inhibitory processes. An unexpected property of D1 was that it appeared to be proportionally controlled. The same proportion of inhibition was produced regardless of whether the H reflex had been facilitated or depressed by voluntary activity in protagonist or antagonist muscles respectively. Depression of the H reflex during contraction of the antagonist muscle is a well known phenomenon (Paillard, 1955) but there have been few quantitative studies to relate the degree of depression to the activity in the antagonist muscles. Our results contrast with those of Gottlieb, Agarawal & Stark (197), who showed fluctuations in H reflex amplitude according to foot torque and phasic changes in torque. If the mechanism of the depression of the H reflex during antagonist activity uses the same interneurones as D1 a concurrent evocation of D1 might find its pathways already engaged and little or no inhibition would be produced. In fact a clearly defined D1 is seen during dorsiflexion with forces up to 5 kg. It must therefore engage other pathways.
11 A SPINAL INHIBITION IN MAN TABLE 1. Spinal inhibitory mechanisms in man Inhibitory mechanism D, Renshaw Ia reciprocal lb Latency and duration (msec) (8) (28) (5)_ (8-9) Muscle nerve stimulated Antagonist Agonist Antagonist Synergist Stimulus strength 1-2 > 1 < 1 < 1 (motor threshold) Volley pulses Voluntary contraction No change Facilitated of agonist Voluntary contraction No change Facilitated of antagonist References* (1) (2), (3), (4) (1) (3) * (1) Tanaka (1974); (2) Pierrot-Deseilligny, Bussel, Held & Katz (1975); (3) Pierrot-Deseilligny et al. (1979); (4) Veale & Rees (1973). D1 then is an inhibitory mechanism with different properties from those inhibitions previously described in human cord. Comparison with data available from animal experiments suggest that D1 may be derived from activity in the low-threshold muscle afferents and that group II afferents may play an important part. Its physiological role in the control of movement is unknown yet its absence in some subjects with spasticity indicates that it is regulated from higher centres and it may well be relevant to the pathophysiology of spasticity (El-Tohamy & Sedgwick, 1981). A.E-T. was supported by a grant from the Egyptian Government. We are grateful to Eileen Rodhouse for typing the manuscript. 57 REFERENCES BRAGG, N. L. (1977). An E.M.G. recording instrument. M.Sc. thesis, University of Southampton. BROWN, A. G. (1981). Organization in the Spinal Cord. Berlin, New York: Springer-Verlag. DELWAIDE, P. J., CRENNA, P. & FLERON, M. H. (1981). Cutaneous nerve stimulation and motoneuronal excitability. I. Soleus and tibialis anterior excitability after ipsilateral and contralateral sural nerve stimulation. J. Neurol. Neuro8urg. P8ychiat. 44, DE5MEDT, J. E. (1973). A discussion of the methodology of the triceps sure T- and H-reflexes. In New Development8 in Electromyography and Clinical Neurophy8iology, vol. 3, ed. DESMEDT, J. E., pp Basel: Karger. ECCLES, R. M. & LUNDBERG, A. (1959). Synaptic actions in motoneurones by afferents which may evoke the flexion reflex. Arch8 ital. Biol. 97, EL-TOHAMY, A. & SEDGWICK, E. M. (1982). Spinal inhibitory mechanisms in spasticity. Electroenceph. cdin. Neurophy8iol. 53, 1-4P. Fu, T. C. & SCHOMBURG, E. D. (1974). Electrophysiological investigation of the projection of secondary muscle spindle afferents in the cat spinal cord. Acta phy8iol. 8cand. 91, GOTTLIEB, G. L. & AGARWAL, G. C. (1971). Effects of initial conditions on the Hoffman reflex. J. Neurol. Neuroaurg. P8ychiat. 34, GOTTLIEB, G. L. & AGARWAL, G. C. (1973a). Modulation of postural reflexes by voluntary movement. I. Modulation of the active limb. J. Neurol. Neuro8urg. P8ychiat. 36, GOTTLIEB, G. L. & AGARWAL, G. C. (1973b). Modulation of postural reflexes by voluntary movement. II. Modulation at an inactive joint. J. Neurol. Neuro8urg. P8ychiat. 36, GOTTLIEB, G. L., AGARWAL, G. C. & STARK, L. (197). Interactions between the voluntary and postural mechanisms of the human motor system. J. Neurophy8iol. 33, HAASE, J., CLEVELAND, S. & Ross, H.-G. (1975). Problems of postsynaptic autogenous and recurrent inhibition in the mammalian spinal cord. Rev. Physiol. Biochem. Pharmacol. 73,
12 58 A. EL-TOHAMY AND E. M. SEDGWICK HOFFMANN, P. (1918). Uber die Beziehunger der Sehnenreflexe Zur Willkurlichen Bewegung und Zum Tonus. Z. Biol. 68, HUGON, M. (1973). Methodology of the Hoffmann reflex in man. In New Developments in Electromyography and Clinical Neurophysiology, vol. 3, ed. DESMEDT, J. E., pp Basel: Karger. JANKOWSKA, E., JOHANNISSON, T. & LiPSKI, J. (1981 a). Common interneurones in reflex pathways from group I a and Ib afferents of the ankle extensors in the cat. J. Physiol. 31, JANKOWSKA, E., MCCREA, D. & MACKEL, R. (1981 b). Pattern of non-reciprocal inhibition of motoneurones by impulses in group I a muscle spindle afferents in the cat. J. Physiol. 316, LLOYD, D. P. C. (1943). Neuron patterns controlling transmission of ipsilateral hind limb reflexes in cat. J. Neurophysiol. 6, MIZUNO, Y., TANAKA, R. & YANAGISAWA, N. (1971). Reciprocal group I inhibition of triceps surae motorneurones in man. J. Neurophysiol. 34, PAILLARD, J. (1955). Analyse electrophysiologique et comparaison, chez l'homme, du reflexe myotatique. Pfiuigers Arch. 26, PIERROT-DESEILLIGNY, E., BuSSEL, B., HELD, J. P. & KATZ, R. (1975). Excitability of human motoneurones after discharge in a conditioning reflex. Electroenceph. clin. Neurophysiol. 4, PIERROT-DESEILLIGNY, E., KATZ, R. & MORIN, C. (1979). Evidence for lb inhibition in human subjects. Brain Res. 166, 176. STAUFFER, E. K., WATT, D. G. D., TAYLOR, A., REINKING, R. M. & STUART, D. G. (1976). Analysis of muscle receptor connections by spike-triggered averaging. 2. Spindle group II afferents. J. Neurophysiol. 39, SUNDERLAND, S. (1978). Nerves and Nerve Injuries. London: Churchill Livingstone. TANAKA, R. (1972). Activation of reciprocal Ia inhibitory pathway during voluntary motor performance in man. Brain Res. 43, TANAKA, R. (1974). Reciprocal Ia inhibition during voluntary movement in man. Exp. Brain Res. 21, TANAKA, R. (1976). Reciprocal I a inhibition and voluntary movements in man. Understanding the stretch reflex. Prog. Brain Res. 44, TANAKA, R. (198). Inhibitory mechanism in reciprocal innervation in voluntary movements. Prog. clin. Neurophysiol. 8, VEALE, J. L. & REES, S. (1973). Renshaw cell activity in man. J. Neurol. Neurosurg. Psychiat. 36, YANAGISAWA, N. & TANAKA, R. (1978). Reciprocal Ia Inhibition in Spastic Paralysis in Man, EEG suppl. no. 34, ed. COBB, W. A. & VAN DUIJN, H., pp YANAGISAWA, N. (198). Reciprocal reflex connections in motor disorders in man. Prog. clin. Neurophysiol. 8, YANAGISAWA, N., TANAKA, R. & ITO, Z. (1976). Reciprocal Ia inhibition in spastic hemiplegia of man. Brain 99,
(Received 10 April 1956)
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