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Ia presynaptic inhibition in human wrist extensor muscles: Effects of motor task and cutaneous afferent activity
J. Physiol. (Paris) 93 (1999) 395−401 © 1999 E´ditions scientifiques et médicales Elsevier SAS. All rights reserved
Ia presynaptic inhibition in human wrist extensor muscles: Effects of motor task and cutaneous afferent activity Jean Marc Aimonetti*, Annie Schmied, Jean-Pierre Vedel, Simone Pagni Laboratoire de Physiologie et Physiopathologie Neuromusculaire Humaine, CNRS-NBM, 31, chemin Joseph-Aiguier, 13402 Marseille cedex 20, France
(Received 11 September 1998; accepted 3 February 1999)
Abstract — The task-dependence of the presynaptic inhibition of the muscle spindle primary afferents in human forearm muscles was studied, focusing in particular on the modulation associated with the co-contraction of antagonist muscles and the activation of cutaneous afferents. The changes known to affect the motoneuron proprioceptive assistance during antagonist muscle co-activation in human leg and arm muscles were compared. The evidence available so far that these changes might reflect changes in the presynaptic inhibition of the muscle spindle afferent is briefly reviewed. The possible reasons for changes in presynaptic inhibition during the antagonist muscle co-contraction are discussed. Some new experiments on the wrist extensor muscles are briefly described. The results showed that the changes in the Ia presynaptic inhibition occurring during the co-contraction of the wrist flexor and extensor muscles while the hand cutaneous receptors were being activated (the subject’s hand was clenched around a manipulandum) could be mimicked by contracting the wrist extensor muscles alone while applying extraneous stimulation to the hand cutaneous receptors. It is concluded that besides the possible contribution of inputs generated by the co-contraction of antagonist muscles and by supraspinal pathways, cutaneous inputs may play a major role in modulating the proprioceptive assistance during manipulatory movements. © 1999 E´ditions scientifiques et médicales Elsevier SAS motor control / motor unit / presynaptic inhibition / wrist muscles
1. The importance of antagonist muscle co-contraction in motor control Tilney and Pike (1925) have reported that ‘muscular co-ordination depends primarily on the synchronous co-contraction relation in the antagonist muscle groups’ (quoted by [39]). The most obvious functional consequence of the co-contraction of antagonist muscles is that it might enhance the joint stiffness, as first established by Paillard [30] in the case of human leg muscles. Co-contraction results in a greater joint stiffness than that which results from adding together the activation of the two separate antagonist muscle groups (cf. [2]). In the case of arm muscles, the co-activation of the extensor and flexor muscles of the fingers and the wrist constitutes the basis of the human handling and gripping repertoire. Several studies based on electromyographic recordings from the human forearm and hand muscles have provided evidence that a complex pattern of synergistic antagonist muscle coactivation occurs during power gripping and handling [8, 23], which has been also observed in monkeys [15]. In human arm muscles, the co-activation of antagonist muscles might be a powerful mechanism contributing to the learning of a new motor skill. To produce these complex patterns of co-activation, the sensory inputs (the cutaneous afferents in particular) and the supraspinal inputs which control the motor * Correspondence and reprints
nuclei of synergist and antagonist muscles have to be finely adapted to this particular situation, where the activity of antagonist muscles has opposite effects. The task-dependent changes in the monosynaptic Ia muscle spindle afferent inputs to the motoneurons might be of great functional significance in the human arm muscles which contribute to everyday manipulatory movements. Little is known, however, about the respective contributions of the various pathways which mediate the interactions between antagonist motoneuron pools [3, 19, 36]. In the present study, it was proposed to investigate how the monosynaptic Ia muscle spindle afferent inputs to the motoneurons are altered during the co-activation of antagonist muscles (figure 1). 2. The changes in the monosynaptic control exerted by the muscle spindle Ia afferents on motoneuron activity during the co-contraction of antagonist muscles In a study on task-dependent changes in the effectiveness of the monosynaptic Ia muscle spindle afferent inputs to the motoneurons of human leg muscles, Paillard [30] established that the reflex response of the soleus muscle to electrical stimulation of the muscle spindle primary afferents (H-reflex) was dramatically enhanced when all the muscles of the leg were co-activated. Nielsen and Kagamihara [29] have observed on the contrary that the soleus H-reflex was
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Figure 1. Motor and sensory spinal pathways relevant to the present study. According to Day et al. [10], the Ia afferents originating from the median nerve might be connected to the interneurons of the Ia presynaptic inhibitory pathways of the wrist extensor motor nuclei. A conditioning stimulus applied to the median nerve might therefore induce Ia presynaptic inhibition, and thus to a decrease in the subsequently tested extensor H-reflex.
lower during the co-contraction of antagonist muscles than during the contraction of an agonist alone. In the latter study however, the subjects were asked to selectively and moderately activate specific leg muscles; whereas in Paillard’s study, the subjects had to strongly co-activate all their leg muscles. This methodological difference might explain the contradictory findings. The soleus H-reflex was also weaker when the subjects were asked to walk on a narrow beam than when they walked on a larger beam [22]. The authors in question reported that the subjects tended to co-activate their leg muscles to a greater extent when walking on a narrow beam, which might explain the weaker H-reflex, in keeping with the data by Nielsen and Kagamihara [29].
The effectiveness of the Ia muscle spindle afferent inputs to the motoneurons has also been investigated in human forearm muscles during the co-activation of antagonist muscles. The authors of the earliest studies on these lines dealt with the stretch reflex [2, 12, 13]. In these studies, the stretch reflex gain and the stiffness of various distal muscles were compared during two motor tasks. The subjects were asked either to maintain the force or the position constant. This position control task generally involves co-activation of the antagonist muscles. In this task, the components of the stretch reflex from 50 to 90 ms which were not monosynaptic were enhanced in the flexor pollicis longus and the extensor digitorum communis muscles [1, 21] and in the first dorsal interosseus and the wrist flexor carpi radialis muscles [12, 13]. In the human wrist extensor carpi radialis muscles, Schmied et al. [35] have investigated the taskdependence of the effectiveness of the monosynaptic Ia muscle spindle afferent inputs to the wrist extensor motoneurons by applying either mechanical stimulation to the tendons of the wrist extensor muscles (tendinous reflex) or electrical stimulation to the radial nerve (H-reflex). In both cases, the motoneuronal pool reflex responses were found to be larger when the subjects co-activated their antagonist muscles by clenching their hand around a manipulandum (figure 2D) than when they contracted their wrist extensor muscles alone (figure 2B). The task-dependence of the Ia reflex loop efficiency appears to have differential effects depending on the muscle involved. During ankle muscle co-contraction, the down-regulation of the proprioceptive assistance might contribute to postural control by preventing the oscillations in the agonist-antagonist system which might occur if the Ia monosynaptic reflex pathway gain was set too high [22, 29]. In the forearm muscles, the co-activation of antagonist muscles has been reported to enhance the proprioceptive assistance [2, 21, 35]. Since the leg and arm muscles are engaged in various day-to-day motor activities, this functional difference might be in keeping with the findings that opposite modulations of the Ia reflex loop efficiency occurs during the co-activation of human leg and arm muscles.
3. Evidence for the involvement of presynaptic inhibition The results of the previous studies indicate that various changes in the effectiveness of the monosynaptic Ia muscle spindle afferent inputs to the motoneurons of the human leg and arm muscles occur during the co-activation of antagonist muscles, depending on the muscles. This therefore raises the question as to
Ia presynaptic inhibition in human wrist extensor muscles
Figure 2. Experimental set-up. A. The H-reflex and the single motor unit reflex responses elicited in the wrist extensor carpi radialis muscles by applying electrical stimulation to the radial nerve (test stimulation) were conditioned by electrically stimulating the primary afferents of the median nerve with a 20-ms delay (conditioning stimulation). The subjects were asked either to simply contract their wrist extensor muscles (B) or to do so while mechanical stimulation was being applied to the skin of their finger tips (C), or to co-activate the wrist extensor and flexor muscles by clenching their hand around a manipulandum (D).
what mechanisms might be responsible for these differential task-effects. The first hypothesis is that the efficiency of the gamma drive might be enhanced during the coactivation of antagonist muscles as compared with an isolated agonist muscle contraction. This possibility does not account satisfactorily, however, for the results obtained in the H-reflex studies [22, 29, 30, 35], since task-dependent changes in the reflex responses were observed upon applying electrical stimulation, which is known to by-pass the muscle spindle sensitivity. During the co-contraction of antagonist human muscles, various task-dependent changes in the efficiency of the Ia reflex loop have been observed without any significant changes in the M-wave amplitude [29], the mean integrated EMG activity [35], and at the single motor unit level without any changes in the mean duration of the inter-spike interval [35]. In the simulation study by Capaday and Stein [7], although the M-wave and the mean integrated EMG activity remained constant throughout various reflex recordings, the sole mechanism liable to explain the changes in the H-reflex gain was a change in the
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efficiency of the Ia presynaptic inhibition. Despite the differences observed in the changes in the efficiency of the Ia reflex loop between the human leg and arm muscles, Ia presynaptic inhibition therefore in both cases been thought to possibly constitute the mechanism underlying these task-dependent changes. Since its discovery by Frank and Fuortes [14], the presynaptic inhibition acting at the sensory afferent terminals has been more and more widely assumed to contribute importantly to motor control by modulating the amplitude of the motoneuron monosynaptic EPSPs originating from Ia afferents (cf. [32, 33]). Ia presynaptic inhibition is accompanied by primary afferent depolarization, which results from the activation of axo-axonic GABA-ergic synapses [32]. Ia presynaptic inhibition has been investigated in human upper and lower limb muscles. The earliest method developed consisted of applying vibration briefly to the homonymous tendons in order to decrease the test H-reflex [11]. Unfortunately, the activity of the homonymous Ia muscle spindle afferents induced by the vibration can cause post-activation depression at the Ia synapse, thus reducing the responsiveness of the H-reflex without any presynaptic inhibitory effects [9]. Morin et al. [27] have introduced a new method for assessing the presynaptic inhibition of soleus Ia fibres in humans from the heteronymous facilitation of the soleus H-reflex produced by a preceding Ia volley induced by vibrating the tendons of the tibialis anterior muscle. Some recent techniques for exploring single motor unit activity have been developed [16, 39]. The motor unit response to the stimulation of homonymous Ia muscle spindle afferents yields a peak at a latency compatible with monosynaptic activation in the post-stimulus time histograms. Upon making comparisons with animal data, Hultborn et al. [16] observed that the first 0.5 ms of the reflex peak can be taken to be purely monosynaptic, since it cannot be contaminated by any oligosynaptic components. An increase or a decrease in the number of counts during this first 0.5 ms can therefore be safely taken to reflect changes in the Ia presynaptic inhibition. Using this method, changes in the presynaptic inhibition of Ia fibres to soleus motoneurons were first observed during voluntary plantar flexion [26]. More recently, the task-dependent changes in the efficiency of the Ia reflex loop induced by the co-contraction of antagonist muscles were investigated at the single motor unit level in the leg muscles [29] and in the arm muscles [35]. The down-regulation of the effectiveness of the Ia reflex loop in the leg muscles [29] and its up-regulation in the arm muscles [35] during their co-contraction have been both interpreted in terms of changes in Ia presynaptic inhibition.
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4. Possible reasons for changes in Ia presynaptic inhibition during co-activation of antagonist muscles Among the various possible explanations for the co-contraction-dependent changes in Ia presynaptic inhibition, the first is that the muscle spindle afferents originating from the antagonist muscles might play a major role, as originally observed in leg muscles [40]. In the human wrist myotatic unit, Day et al. [10] have reported that the Ia muscle spindle afferents from the wrist flexor muscles projected to the interneurons of the extensor Ia presynaptic inhibitory pathways (figure 1). A conditioning stimulation applied to the median nerve decreased the H-reflex recorded in the wrist extensor muscles 20 ms later: this decrease probably reflected the Ia presynaptic inhibition induced by the flexor afferent stimulation [4]. On the other hand, the efficiency of the Ia presynaptic inhibition pathway is known to be modulated by cutaneous afferents. In cats, cutaneous afferents are known to inhibit the spinal interneurons which mediate the Ia presynaptic inhibition [24], especially the firstorder interneurons [5], and thus to decrease the primary afferent depolarization generated by the activity of group I sensory afferents [33]. Inhibitory effects of cutaneous afferents on the Ia presynaptic inhibition have been also observed in human leg [17, 18] and forearm muscles [4, 28]. Lastly, it is well known that the interneurons mediating Ia presynaptic inhibition are controlled by several supraspinal inhibitory and excitatory pathways, as established in animal studies (reviewed in [3]) and suggested from human recordings during voluntary contraction [26, 29]. A supraspinal down-regulation of Ia presynaptic inhibition has been found to exist by Iles [17], who reported that the transcranial magnetic stimulation reduced the amount of Ia presynaptic inhibition more strongly during voluntary plantar flexion than at rest. In forearm muscles, the Ia presynaptic inhibition, as assessed from the effects of radial nerve electrical stimulation on the H-reflex in the wrist flexor muscles, decreased dramatically after transcranial electrical or magnetic stimulation [25]. The results of all these studies converge to suggest that the Ia presynaptic inhibition may be modulated tonically during voluntary contraction via the activity of supraspinal pathways. 5. Evidence for the involvement of hand cutaneous receptor inputs In some recent experiments [1], the question was addressed as to whether changes in Ia presynaptic inhibition might be at the origin of the task-dependent changes in the monosynaptic Ia muscle spindle affer-
ent inputs to the motoneurons of the wrist extensor muscles. Special attention was paid here to the possible contribution of hand cutaneous afferent inputs to these changes in Ia presynaptic inhibition. Seven subjects were asked either to selectively activate their wrist extensor muscles by pushing with the back of their hand against a force transducer device, keeping their finger relaxed, or to co-activate their wrist extensor and flexor muscles by clenching their hand around a manipulandum (figure 2B, D). The H-reflex and the single motor unit reflex responsiveness elicited in the wrist extensor carpi radialis muscles by electrically stimulating the radial nerve were conditioned by electrically stimulating the median nerve with a conditioning-test interval of 20 ms in order to evoke Ia presynaptic inhibition. The 20 ms delay has been reported to correspond to the peak in the Ia presynaptic inhibition obtained when using the procedures described by Berardelli et al. [4]. In the control sessions run without any conditioning stimulation, the H-reflex (figure 3A) and the motor unit reflex responses (figure 3B) recorded during wrist extension were significantly weaker than during hand clenching, which was in keeping with the previous findings by Schmied et al. [35]. In both motor tasks, the burst of the flexor Ia muscle spindle afferents induced a decrease in the extensor H-reflex and motor unit reflex responsiveness after a 20-ms conditioningtest interval: this decrease was significantly greater during wrist extension than during hand clenching. These changes in the proprioceptive assistance were observed at the motoneuron pool level without any significant changes in the M-wave amplitude, or the mean integrated EMG activity, and at the single motor unit level without any significant changes in the motoneuron excitatory drive in terms of the interspike interval duration. The purely monosynaptic components of the motor unit reflex responses recorded during wrist extension were weaker than during hand clenching (figure 3C), which suggests that the Ia presynaptic inhibition was stronger during wrist extension. The question now arises as to what mechanisms might underlie the task-dependent changes in the Ia presynaptic inhibition. During hand clenching, many cutaneous receptors in the palm and fingers are liable to be activated [20]. These inputs might reduce the Ia presynaptic inhibition [34] and thus enhance the H-reflex and the motor unit response probability as compared with wrist extension. In order to test this hypothesis, the subjects were asked to perform wrist extension while the skin of the palm and the finger tips of their hand was being mechanically stimulated using a soft rotative brush (figure 2C). During wrist extension with cutaneous stimulation, both the H-reflex and the single motor unit reflex responses were similar to
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Figure 3. Changes in the presynaptic inhibition of the wrist extensor motoneuron responses induced by stimulating antagonist Ia afferents. The presynaptic inhibition induced by stimulating flexor Ia muscle spindle afferents was assessed from the decrease in the H-reflex amplitude (A) and in the motor unit response probability (whole peak B, first 0.5 ms bins C). The Ia presynaptic inhibition was stronger during wrist extension (squares), but reached similar levels during both wrist extension with cutaneous stimulation (triangles) and hand clenching (circles). This suggests that the cutaneous afferents activated by the brush mimicked the effects of the cutaneous afferents activated during hand clenching, i.e., that they decreased the Ia presynaptic inhibition and thus enhanced the proprioceptive assistance to the wrist extensor motoneurons.
those observed during hand clenching, at both the control and conditioned sessions (figure 3A). At the single motor unit level, the results showed a similar pattern in terms of the whole motor unit reflex response (figure 3B) and in terms of its earliest components (figure 3C). During these wrist extension experiments, the cutaneous afferents activated by the brush can be said to have mimicked the effects of the cutaneous afferents activated during hand clenching. These cutaneous inputs may have decreased the Ia presynaptic inhibition, and thus enhanced the motor unit reflex response and the H-reflex. This would be in good agreement with previous findings on the wrist flexor muscles, according to electrical stimulation applied to the superficial branches of the radial nerve reduced the amount of presynaptic inhibition by 20%, whereas anaesthesia of the skin of the hand increased the amount of presynaptic inhibition by 10% [4, 28]. In the present study, mechanical stimulation was applied
to the skin of the palm and finger tips of the hand using a method developed on the basis of microneurographic recordings of the sensory afferents in the human lateral peroneal nerve [31] as an alternative to applying electrical stimulation to the superficial branch of the median nerve [28], which is known to produce very narrow and synchronous volleys which are not natural in terms of physiological significance [6]. Nevertheless, the results of all these studies suggest on the whole that a tonic cutaneous influence on the level of excitability might exist in the wrist presynaptic inhibitory pathways. Although the possibility that other processes may be involved certainly cannot be ruled out, these data definitely show that hand cutaneous afferents play a major role in the task-dependent changes in the proprioceptive assistance to the wrist myotatic unit. It is worth noting that these experiments were performed during voluntary contractions. Besides their direct effects on Ia presynaptic inhibition (see above),
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supraspinal pathways have been reported to actually alter the effects of cutaneous afferents on Ia presynaptic inhibition [34]. Interestingly, Sheehy et al. [37] have reported that the writing of a patient with writer’s cramp improved after his hand was injected with local anaesthetic. The latter authors suggested that the anaesthesia may have increased the Ia presynaptic inhibition to more normal level by blocking the cutaneous afferent inputs, and thus have compensated for any deficits in the supraspinal control. In humans as in cats, it therefore seems likely that the interplay between cutaneous and supraspinal afferents might be a major factor contributing to the control of the interneurons mediating presynaptic inhibition and ensuring that the gain of the monosynaptic proprioceptive assistance is adjusted to fit the specific requirements of the ongoing motor task.
Acknowledgments We are grateful to Dr. J. Blanc for correcting the English manuscript and to P.A. Styss for his logistic assistance. This research was supported by Grants from the Association Française contre les Myopathies (A.F.M.), the Fondation pour la Recherche Médicale (F.R.M.), and the Direction des Recherches, Etudes et Techniques (D.R.E.T.-D.G.A.).
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[10] Day B.L., Marsden C.D., Obeso J.A., Rothwell J.C., Reciprocal inhibition between the muscles of the human forearm, J. Physiol. (Lond.) 349 (1984) 519–534. [11] Degail P., Lance J.W., Nielson P.D., Differential effects on tonic and phasic reflex mechanisms produced by vibration of muscles in man, J. Neurol. Neurosurg. Psych. 29 (1966) 1–11. [12] Doemges F., Rack P.M.H., Task-dependent changes in the response of human wrist joints to mechanical disturbances, J. Physiol. (Lond.) 447 (1992) 575–585. [13] Doemges F., Rack P.M.H., Changes in the stretch reflex of the human first dorsal interosseus muscle during different tasks, J. Physiol. (Lond.) 447 (1992) 563–573. [14] Frank K., Fuortes M.G.F., Presynaptic and postsynaptic inhibition of monosynaptic reflexes, Proc. Fed. Am. Soc. Exp. Biol. 16 (1957) 39–40. [15] Hepp-Reymond M.C., Wiesendanger M., Unilateral pyramidotomy in monkeys: Effects of force and speed of a conditioned precision grip, Brain Res. 36 (1972) 117–131. [16] Hultborn H., Meunier S., Morin C., Pierrot-Deseilligny E., Assessing changes in presynaptic inhibition of Ia fibres: a study in man and the cat, J. Physiol. (Lond.) 389 (1987) 729–756. [17] Iles J.F., Evidence for cutaneous and corticospinal modulation of presynaptic inhibition of Ia afferents from the human lower limb, J. Physiol. (Lond.) 491 (1996) 197–207. [18] Iles J.F., Roberts R.C., Inhibition of monosynaptic reflexes in the human lower limb, J. Physiol. (Lond.) 385 (1987) 69–87. [19] Jankowska E., Interneuronal relay in spinal pathways from proprioceptors, Progr. Neurobiol. 38 (1992) 335–378. [20] Johansson R.S., Vållbo A.B., Detection of tactile stimuli thresholds of afferent units related to psychophysical threshold in the human hand, J. Physiol. (Lond.) 297 (1979) 405–422. [21] Kanosue K., Akasawa K., Fujii K., Modulation of reflex activity of motor units in response to stretch of a human finger muscle, Jpn. J. Physiol. 33 (1983) 995–1009. [22] Llewellyn M., Yang J.F., Prochazka A., Human H-reflexes are smaller in difficult beam walking than in normal treadmill walking, Exp. Brain Res. 83 (1990) 22–28. [23] Long C.H., Conrad P.W., Hall E.A., Furler S.L., Intrinsic extrinsic muscle control of the hand in power grip and precision handling, J. Bone Joint Surg. 52 (1970) 853–867. [24] Lund S., Lundberg A., Vytlicky L., Inhibitory action from the flexor reflex afferents on transmission to Ia afferents, Acta Physiol. Scand. 64 (1965) 345–355. [25] Mercuri B., Wassermann E.M., Ikoma K., Samii A., Hallet M., Effects of transcranial electrical and magnetic stimulation on reciprocal inhibition in the human arm, EEG Clin. Neurophysiol. 105 (1997) 87–93. [26] Meunier S., Pierrot-Deseilligny E., Gating of the afferent volley of the monosynaptic stretch reflex during movement in man, J. Physiol. (Lond.) 419 (1989) 753–763. [27] Morin C., Pierrot-Deseilligny E., Hultborn H., Evidence for presynaptic inhibition of muscle spindle Ia afferents in man, Neurosci. Lett. 44 (1984) 137–142. [28] Nakashima K., Rothwell J.C., Day B.L., Thompson P.D., Marsden C.D., Cutaneous effects on presynaptic inhibition of flexor Ia afferents in the human forearm, J. Physiol. (Lond.) 426 (1990) 369–380. [29] Nielsen J., Kagamihara Y., The regulation of disynaptic reciprocal Ia inhibition during co-contraction of antagonistic muscles in man, J. Physiol. (Lond.) 456 (1992) 373–391. [30] Paillard J., Réflexes et régulations d’origine proprioceptive chez l’homme, Arnette, Paris 1955.
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[31] Ribot-Ciscar E., Vedel J.P., Roll J.P., Vibration sensitivity of slowly and rapidly adapting cutaneous mechanoreceptors in the human foot and leg, Neurosci. Lett. 104 (1989) 130–135. [32] Rudomin P., Presynaptic inhibition of muscle spindle and tendon organ afferents in the mammalian spinal cord, TINS 13 (1990) 499–505. [33] Rudomin P., Presynaptic control of synaptic effectiveness of muscle spindle and tendon organ afferents in the mammalian spinal cord, in: Binder M.D., Mendell L.M. (Eds.), The segmental motor system, Oxford University Press, New York, 1990, pp. 349–380. [34] Rudomin P., Jiménez I., Quevedo J., Selectivity of the presynaptic control of synaptic effectiveness of group I afferents in the mammalian spinal cord, in: Rudomin P., Romo R., Mendell L.M. (Eds.), Presynaptic inhibition and neural control, Oxford University Press, Oxford, 1998, pp. 351–366.
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[35] Schmied A., Vedel J.P., Calvin-Figuière S., Rossi-Durand C., Pagni S., Task-dependence of muscle afferent monosynaptic inputs to human extensor carpi radialis motoneurones, EEG Clin. Neurophysiol. 105 (1997) 220–234. [36] Schomburg E.D., Spinal sensorimotor systems and their supraspinal control, Neuro. Res. 7 (1990) 265–340. [37] Sheely M.P., Rothwell J.C., Marsden C.D., Writer’s cramp, Adv. Neurol. 50 (1988) 457–472. [38] Shindo M., Yanagawa S., Morita H., Hashimoto T., Conditioning effect in single human motoneurones: a new method using the unitary H reflex, J. Physiol. (Lond.) 481 (1994) 469–477. [39] Smith A.M., The coactivation of antagonist muscles, Can. J. Physiol. Pharmacol. 59 (1981) 733–747. [40] Tanaka R., Reciprocal inhibition during voluntary movements in man, Exp. Brain Res. 21 (1974) 529–540.
Ia presynaptic inhibition in human wrist extensor muscles: Effects of motor task and cutaneous afferent activity Jean Marc Aimonetti*, Annie Schmied, Jean-Pierre Vedel, Simone Pagni Laboratoire de Physiologie et Physiopathologie Neuromusculaire Humaine, CNRS-NBM, 31, chemin Joseph-Aiguier, 13402 Marseille cedex 20, France
(Received 11 September 1998; accepted 3 February 1999)
Abstract — The task-dependence of the presynaptic inhibition of the muscle spindle primary afferents in human forearm muscles was studied, focusing in particular on the modulation associated with the co-contraction of antagonist muscles and the activation of cutaneous afferents. The changes known to affect the motoneuron proprioceptive assistance during antagonist muscle co-activation in human leg and arm muscles were compared. The evidence available so far that these changes might reflect changes in the presynaptic inhibition of the muscle spindle afferent is briefly reviewed. The possible reasons for changes in presynaptic inhibition during the antagonist muscle co-contraction are discussed. Some new experiments on the wrist extensor muscles are briefly described. The results showed that the changes in the Ia presynaptic inhibition occurring during the co-contraction of the wrist flexor and extensor muscles while the hand cutaneous receptors were being activated (the subject’s hand was clenched around a manipulandum) could be mimicked by contracting the wrist extensor muscles alone while applying extraneous stimulation to the hand cutaneous receptors. It is concluded that besides the possible contribution of inputs generated by the co-contraction of antagonist muscles and by supraspinal pathways, cutaneous inputs may play a major role in modulating the proprioceptive assistance during manipulatory movements. © 1999 E´ditions scientifiques et médicales Elsevier SAS motor control / motor unit / presynaptic inhibition / wrist muscles
1. The importance of antagonist muscle co-contraction in motor control Tilney and Pike (1925) have reported that ‘muscular co-ordination depends primarily on the synchronous co-contraction relation in the antagonist muscle groups’ (quoted by [39]). The most obvious functional consequence of the co-contraction of antagonist muscles is that it might enhance the joint stiffness, as first established by Paillard [30] in the case of human leg muscles. Co-contraction results in a greater joint stiffness than that which results from adding together the activation of the two separate antagonist muscle groups (cf. [2]). In the case of arm muscles, the co-activation of the extensor and flexor muscles of the fingers and the wrist constitutes the basis of the human handling and gripping repertoire. Several studies based on electromyographic recordings from the human forearm and hand muscles have provided evidence that a complex pattern of synergistic antagonist muscle coactivation occurs during power gripping and handling [8, 23], which has been also observed in monkeys [15]. In human arm muscles, the co-activation of antagonist muscles might be a powerful mechanism contributing to the learning of a new motor skill. To produce these complex patterns of co-activation, the sensory inputs (the cutaneous afferents in particular) and the supraspinal inputs which control the motor * Correspondence and reprints
nuclei of synergist and antagonist muscles have to be finely adapted to this particular situation, where the activity of antagonist muscles has opposite effects. The task-dependent changes in the monosynaptic Ia muscle spindle afferent inputs to the motoneurons might be of great functional significance in the human arm muscles which contribute to everyday manipulatory movements. Little is known, however, about the respective contributions of the various pathways which mediate the interactions between antagonist motoneuron pools [3, 19, 36]. In the present study, it was proposed to investigate how the monosynaptic Ia muscle spindle afferent inputs to the motoneurons are altered during the co-activation of antagonist muscles (figure 1). 2. The changes in the monosynaptic control exerted by the muscle spindle Ia afferents on motoneuron activity during the co-contraction of antagonist muscles In a study on task-dependent changes in the effectiveness of the monosynaptic Ia muscle spindle afferent inputs to the motoneurons of human leg muscles, Paillard [30] established that the reflex response of the soleus muscle to electrical stimulation of the muscle spindle primary afferents (H-reflex) was dramatically enhanced when all the muscles of the leg were co-activated. Nielsen and Kagamihara [29] have observed on the contrary that the soleus H-reflex was
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Figure 1. Motor and sensory spinal pathways relevant to the present study. According to Day et al. [10], the Ia afferents originating from the median nerve might be connected to the interneurons of the Ia presynaptic inhibitory pathways of the wrist extensor motor nuclei. A conditioning stimulus applied to the median nerve might therefore induce Ia presynaptic inhibition, and thus to a decrease in the subsequently tested extensor H-reflex.
lower during the co-contraction of antagonist muscles than during the contraction of an agonist alone. In the latter study however, the subjects were asked to selectively and moderately activate specific leg muscles; whereas in Paillard’s study, the subjects had to strongly co-activate all their leg muscles. This methodological difference might explain the contradictory findings. The soleus H-reflex was also weaker when the subjects were asked to walk on a narrow beam than when they walked on a larger beam [22]. The authors in question reported that the subjects tended to co-activate their leg muscles to a greater extent when walking on a narrow beam, which might explain the weaker H-reflex, in keeping with the data by Nielsen and Kagamihara [29].
The effectiveness of the Ia muscle spindle afferent inputs to the motoneurons has also been investigated in human forearm muscles during the co-activation of antagonist muscles. The authors of the earliest studies on these lines dealt with the stretch reflex [2, 12, 13]. In these studies, the stretch reflex gain and the stiffness of various distal muscles were compared during two motor tasks. The subjects were asked either to maintain the force or the position constant. This position control task generally involves co-activation of the antagonist muscles. In this task, the components of the stretch reflex from 50 to 90 ms which were not monosynaptic were enhanced in the flexor pollicis longus and the extensor digitorum communis muscles [1, 21] and in the first dorsal interosseus and the wrist flexor carpi radialis muscles [12, 13]. In the human wrist extensor carpi radialis muscles, Schmied et al. [35] have investigated the taskdependence of the effectiveness of the monosynaptic Ia muscle spindle afferent inputs to the wrist extensor motoneurons by applying either mechanical stimulation to the tendons of the wrist extensor muscles (tendinous reflex) or electrical stimulation to the radial nerve (H-reflex). In both cases, the motoneuronal pool reflex responses were found to be larger when the subjects co-activated their antagonist muscles by clenching their hand around a manipulandum (figure 2D) than when they contracted their wrist extensor muscles alone (figure 2B). The task-dependence of the Ia reflex loop efficiency appears to have differential effects depending on the muscle involved. During ankle muscle co-contraction, the down-regulation of the proprioceptive assistance might contribute to postural control by preventing the oscillations in the agonist-antagonist system which might occur if the Ia monosynaptic reflex pathway gain was set too high [22, 29]. In the forearm muscles, the co-activation of antagonist muscles has been reported to enhance the proprioceptive assistance [2, 21, 35]. Since the leg and arm muscles are engaged in various day-to-day motor activities, this functional difference might be in keeping with the findings that opposite modulations of the Ia reflex loop efficiency occurs during the co-activation of human leg and arm muscles.
3. Evidence for the involvement of presynaptic inhibition The results of the previous studies indicate that various changes in the effectiveness of the monosynaptic Ia muscle spindle afferent inputs to the motoneurons of the human leg and arm muscles occur during the co-activation of antagonist muscles, depending on the muscles. This therefore raises the question as to
Ia presynaptic inhibition in human wrist extensor muscles
Figure 2. Experimental set-up. A. The H-reflex and the single motor unit reflex responses elicited in the wrist extensor carpi radialis muscles by applying electrical stimulation to the radial nerve (test stimulation) were conditioned by electrically stimulating the primary afferents of the median nerve with a 20-ms delay (conditioning stimulation). The subjects were asked either to simply contract their wrist extensor muscles (B) or to do so while mechanical stimulation was being applied to the skin of their finger tips (C), or to co-activate the wrist extensor and flexor muscles by clenching their hand around a manipulandum (D).
what mechanisms might be responsible for these differential task-effects. The first hypothesis is that the efficiency of the gamma drive might be enhanced during the coactivation of antagonist muscles as compared with an isolated agonist muscle contraction. This possibility does not account satisfactorily, however, for the results obtained in the H-reflex studies [22, 29, 30, 35], since task-dependent changes in the reflex responses were observed upon applying electrical stimulation, which is known to by-pass the muscle spindle sensitivity. During the co-contraction of antagonist human muscles, various task-dependent changes in the efficiency of the Ia reflex loop have been observed without any significant changes in the M-wave amplitude [29], the mean integrated EMG activity [35], and at the single motor unit level without any changes in the mean duration of the inter-spike interval [35]. In the simulation study by Capaday and Stein [7], although the M-wave and the mean integrated EMG activity remained constant throughout various reflex recordings, the sole mechanism liable to explain the changes in the H-reflex gain was a change in the
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efficiency of the Ia presynaptic inhibition. Despite the differences observed in the changes in the efficiency of the Ia reflex loop between the human leg and arm muscles, Ia presynaptic inhibition therefore in both cases been thought to possibly constitute the mechanism underlying these task-dependent changes. Since its discovery by Frank and Fuortes [14], the presynaptic inhibition acting at the sensory afferent terminals has been more and more widely assumed to contribute importantly to motor control by modulating the amplitude of the motoneuron monosynaptic EPSPs originating from Ia afferents (cf. [32, 33]). Ia presynaptic inhibition is accompanied by primary afferent depolarization, which results from the activation of axo-axonic GABA-ergic synapses [32]. Ia presynaptic inhibition has been investigated in human upper and lower limb muscles. The earliest method developed consisted of applying vibration briefly to the homonymous tendons in order to decrease the test H-reflex [11]. Unfortunately, the activity of the homonymous Ia muscle spindle afferents induced by the vibration can cause post-activation depression at the Ia synapse, thus reducing the responsiveness of the H-reflex without any presynaptic inhibitory effects [9]. Morin et al. [27] have introduced a new method for assessing the presynaptic inhibition of soleus Ia fibres in humans from the heteronymous facilitation of the soleus H-reflex produced by a preceding Ia volley induced by vibrating the tendons of the tibialis anterior muscle. Some recent techniques for exploring single motor unit activity have been developed [16, 39]. The motor unit response to the stimulation of homonymous Ia muscle spindle afferents yields a peak at a latency compatible with monosynaptic activation in the post-stimulus time histograms. Upon making comparisons with animal data, Hultborn et al. [16] observed that the first 0.5 ms of the reflex peak can be taken to be purely monosynaptic, since it cannot be contaminated by any oligosynaptic components. An increase or a decrease in the number of counts during this first 0.5 ms can therefore be safely taken to reflect changes in the Ia presynaptic inhibition. Using this method, changes in the presynaptic inhibition of Ia fibres to soleus motoneurons were first observed during voluntary plantar flexion [26]. More recently, the task-dependent changes in the efficiency of the Ia reflex loop induced by the co-contraction of antagonist muscles were investigated at the single motor unit level in the leg muscles [29] and in the arm muscles [35]. The down-regulation of the effectiveness of the Ia reflex loop in the leg muscles [29] and its up-regulation in the arm muscles [35] during their co-contraction have been both interpreted in terms of changes in Ia presynaptic inhibition.
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4. Possible reasons for changes in Ia presynaptic inhibition during co-activation of antagonist muscles Among the various possible explanations for the co-contraction-dependent changes in Ia presynaptic inhibition, the first is that the muscle spindle afferents originating from the antagonist muscles might play a major role, as originally observed in leg muscles [40]. In the human wrist myotatic unit, Day et al. [10] have reported that the Ia muscle spindle afferents from the wrist flexor muscles projected to the interneurons of the extensor Ia presynaptic inhibitory pathways (figure 1). A conditioning stimulation applied to the median nerve decreased the H-reflex recorded in the wrist extensor muscles 20 ms later: this decrease probably reflected the Ia presynaptic inhibition induced by the flexor afferent stimulation [4]. On the other hand, the efficiency of the Ia presynaptic inhibition pathway is known to be modulated by cutaneous afferents. In cats, cutaneous afferents are known to inhibit the spinal interneurons which mediate the Ia presynaptic inhibition [24], especially the firstorder interneurons [5], and thus to decrease the primary afferent depolarization generated by the activity of group I sensory afferents [33]. Inhibitory effects of cutaneous afferents on the Ia presynaptic inhibition have been also observed in human leg [17, 18] and forearm muscles [4, 28]. Lastly, it is well known that the interneurons mediating Ia presynaptic inhibition are controlled by several supraspinal inhibitory and excitatory pathways, as established in animal studies (reviewed in [3]) and suggested from human recordings during voluntary contraction [26, 29]. A supraspinal down-regulation of Ia presynaptic inhibition has been found to exist by Iles [17], who reported that the transcranial magnetic stimulation reduced the amount of Ia presynaptic inhibition more strongly during voluntary plantar flexion than at rest. In forearm muscles, the Ia presynaptic inhibition, as assessed from the effects of radial nerve electrical stimulation on the H-reflex in the wrist flexor muscles, decreased dramatically after transcranial electrical or magnetic stimulation [25]. The results of all these studies converge to suggest that the Ia presynaptic inhibition may be modulated tonically during voluntary contraction via the activity of supraspinal pathways. 5. Evidence for the involvement of hand cutaneous receptor inputs In some recent experiments [1], the question was addressed as to whether changes in Ia presynaptic inhibition might be at the origin of the task-dependent changes in the monosynaptic Ia muscle spindle affer-
ent inputs to the motoneurons of the wrist extensor muscles. Special attention was paid here to the possible contribution of hand cutaneous afferent inputs to these changes in Ia presynaptic inhibition. Seven subjects were asked either to selectively activate their wrist extensor muscles by pushing with the back of their hand against a force transducer device, keeping their finger relaxed, or to co-activate their wrist extensor and flexor muscles by clenching their hand around a manipulandum (figure 2B, D). The H-reflex and the single motor unit reflex responsiveness elicited in the wrist extensor carpi radialis muscles by electrically stimulating the radial nerve were conditioned by electrically stimulating the median nerve with a conditioning-test interval of 20 ms in order to evoke Ia presynaptic inhibition. The 20 ms delay has been reported to correspond to the peak in the Ia presynaptic inhibition obtained when using the procedures described by Berardelli et al. [4]. In the control sessions run without any conditioning stimulation, the H-reflex (figure 3A) and the motor unit reflex responses (figure 3B) recorded during wrist extension were significantly weaker than during hand clenching, which was in keeping with the previous findings by Schmied et al. [35]. In both motor tasks, the burst of the flexor Ia muscle spindle afferents induced a decrease in the extensor H-reflex and motor unit reflex responsiveness after a 20-ms conditioningtest interval: this decrease was significantly greater during wrist extension than during hand clenching. These changes in the proprioceptive assistance were observed at the motoneuron pool level without any significant changes in the M-wave amplitude, or the mean integrated EMG activity, and at the single motor unit level without any significant changes in the motoneuron excitatory drive in terms of the interspike interval duration. The purely monosynaptic components of the motor unit reflex responses recorded during wrist extension were weaker than during hand clenching (figure 3C), which suggests that the Ia presynaptic inhibition was stronger during wrist extension. The question now arises as to what mechanisms might underlie the task-dependent changes in the Ia presynaptic inhibition. During hand clenching, many cutaneous receptors in the palm and fingers are liable to be activated [20]. These inputs might reduce the Ia presynaptic inhibition [34] and thus enhance the H-reflex and the motor unit response probability as compared with wrist extension. In order to test this hypothesis, the subjects were asked to perform wrist extension while the skin of the palm and the finger tips of their hand was being mechanically stimulated using a soft rotative brush (figure 2C). During wrist extension with cutaneous stimulation, both the H-reflex and the single motor unit reflex responses were similar to
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Figure 3. Changes in the presynaptic inhibition of the wrist extensor motoneuron responses induced by stimulating antagonist Ia afferents. The presynaptic inhibition induced by stimulating flexor Ia muscle spindle afferents was assessed from the decrease in the H-reflex amplitude (A) and in the motor unit response probability (whole peak B, first 0.5 ms bins C). The Ia presynaptic inhibition was stronger during wrist extension (squares), but reached similar levels during both wrist extension with cutaneous stimulation (triangles) and hand clenching (circles). This suggests that the cutaneous afferents activated by the brush mimicked the effects of the cutaneous afferents activated during hand clenching, i.e., that they decreased the Ia presynaptic inhibition and thus enhanced the proprioceptive assistance to the wrist extensor motoneurons.
those observed during hand clenching, at both the control and conditioned sessions (figure 3A). At the single motor unit level, the results showed a similar pattern in terms of the whole motor unit reflex response (figure 3B) and in terms of its earliest components (figure 3C). During these wrist extension experiments, the cutaneous afferents activated by the brush can be said to have mimicked the effects of the cutaneous afferents activated during hand clenching. These cutaneous inputs may have decreased the Ia presynaptic inhibition, and thus enhanced the motor unit reflex response and the H-reflex. This would be in good agreement with previous findings on the wrist flexor muscles, according to electrical stimulation applied to the superficial branches of the radial nerve reduced the amount of presynaptic inhibition by 20%, whereas anaesthesia of the skin of the hand increased the amount of presynaptic inhibition by 10% [4, 28]. In the present study, mechanical stimulation was applied
to the skin of the palm and finger tips of the hand using a method developed on the basis of microneurographic recordings of the sensory afferents in the human lateral peroneal nerve [31] as an alternative to applying electrical stimulation to the superficial branch of the median nerve [28], which is known to produce very narrow and synchronous volleys which are not natural in terms of physiological significance [6]. Nevertheless, the results of all these studies suggest on the whole that a tonic cutaneous influence on the level of excitability might exist in the wrist presynaptic inhibitory pathways. Although the possibility that other processes may be involved certainly cannot be ruled out, these data definitely show that hand cutaneous afferents play a major role in the task-dependent changes in the proprioceptive assistance to the wrist myotatic unit. It is worth noting that these experiments were performed during voluntary contractions. Besides their direct effects on Ia presynaptic inhibition (see above),
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supraspinal pathways have been reported to actually alter the effects of cutaneous afferents on Ia presynaptic inhibition [34]. Interestingly, Sheehy et al. [37] have reported that the writing of a patient with writer’s cramp improved after his hand was injected with local anaesthetic. The latter authors suggested that the anaesthesia may have increased the Ia presynaptic inhibition to more normal level by blocking the cutaneous afferent inputs, and thus have compensated for any deficits in the supraspinal control. In humans as in cats, it therefore seems likely that the interplay between cutaneous and supraspinal afferents might be a major factor contributing to the control of the interneurons mediating presynaptic inhibition and ensuring that the gain of the monosynaptic proprioceptive assistance is adjusted to fit the specific requirements of the ongoing motor task.
Acknowledgments We are grateful to Dr. J. Blanc for correcting the English manuscript and to P.A. Styss for his logistic assistance. This research was supported by Grants from the Association Française contre les Myopathies (A.F.M.), the Fondation pour la Recherche Médicale (F.R.M.), and the Direction des Recherches, Etudes et Techniques (D.R.E.T.-D.G.A.).
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