Differential effects of stimulation of the cat's red nucleus on lumbar alpha motoneurones and their Renshaw cells

Springer Science and Business Media LLC - Tập 62 - Trang 161-174 - 1986
H. -D. Henatsch1, J. Meyer-Lohmann1, U. Windhorst1, J. Schmidt1
1Zentrum Physiologie und Pathophysiologie der Universität Göttingen, Abteilung Neuro- und Sinnesphysiologie, Göttingen, Germany

Tóm tắt

1. The red nucleus region was stereotaxically stimulated with short trains of high-frequency alternating current pulses in anaesthetized cats. The effects were studied, in contralateral lumbar segments, on the responses of microrecorded individual Renshaw cells (RCs) to antidromic or orthodromic test shocks of ventral root or muscle nerve fibres. Monosynaptic reflexes (MRs) of their motoneurone pools were recorded from one of the cut lumbar ventral roots. Averages of 10–20 replicate test responses of the RC (converted into instantaneous frequency curves, IFCs) and of the MR shapes were computed and graphically displayed. 2. Orthodromic (afferent) test shocks induced simultaneously MRs as well as responses of a RC belonging to the same motor pool. From their paired records at systematically varied shock strengths, whole “linkage characteristics” of the relation between the two events could be obtained, representing the functional linkage from the motoraxon collaterals to the RC under study. The overall result of rubral conditioning was a change in the course of the characteristic, which indicated a reduction of this linkage (= relative inhibition of the RC against its recurrent input). 3. Sequential trials with test shocks of constant, submaximal strength were performed with 45 individual RCs. The clearest results were obtained with RC responses to antidromic ventral root shocks: 65% of the RCs were partially inhibited by rubral conditioning. Interposed minor facilitory subcomponents could be seen in the course of inhibited IFCs. Mixed sequences of manifest inhibitory/facilitory effects were observed in 11%; reversed sequences (facilitory/inhibitory) did not occur. A pure but weak facilitation was found in only one case, paralleled by an increase of the MR. RCs belonging to either extensor or flexor motor pools were affected about equally. A little over 20% of the tested RCs remained uninfluenced by rubral stimulation. 4. The MRs, induced by constant, submaximal, orthodromic test shocks, were usually enhanced with only few exceptions, by rubral stimulation. The effects on the orthodromic RC responses were mainly inhibitory, but could be more or less masked by the concurrent increase of the MR, providing a stronger recurrent input to the RC. Such inhibition could be uncovered, however, by observing the above described linkage change. 5. Variation of several parameters of rubral conditioning (train duration, timing of train with respect to test shock, strength of train) modified the inhibitory effects on antidromic RC responses to a certain extent without changing their principal character. Higher conditioning strengths frequently induced mass discharges of previously silent motoneurones, but at the same time an increased inhibition of the concurrent RC responses. 6. Spontaneous RC activity (in the absence of test stimuli) occurred infrequently and was weak and interrupted by silent periods. When this persisted long enough for testing repeated rubral stimulation, a strong initial inhibition lasting up to several hundred ms was found, sometimes followed by some oscillations of the average discharge rate. 7. The predominant combination of concurrent effects of the conditioning, namely, inhibition of RCs and facilitation of motoneurones, indicated independent (and mostly divergent) control of the two target neurones by the red nucleus. It is concluded that in this way the RCs can be flexibly and transiently decoupled to some degree from their recurrent motoneuronal input.

Tài liệu tham khảo

Appelberg B, Hulliger M, Johansson H, Sojka P (1982) An intracellular study of rubrospinal and rubro-bulbospinal control of lumbar gamma-motoneurones, Acta Physiol Scand 116: 377–386 Benecke R, Böttcher U, Henatsch HD, Meyer-Lohmann J, Schmidt J (1975) Recurrent inhibition of individual Ia inhibitory interneurones and disinhibition of their target alphamotoneurones during muscle stretches. Exp Brain Res 23: 13–28 Benecke R, Meyer-Lohmann J, Guntau J (1976) Inverse changes in the excitability of Renshaw cells and alpha-motoneurones induced by interpositus stimulation. Pflügers Arch 365: 218 Brodal A (1981) Neurological anatomy in relation to clinical medicine, 3rd edn. Oxford University Press, New York London Toronto Fromm C, Evarts EV, Kröller J, Shinoda Y (1981) Activity of motor cortex and red nucleus neurons during voluntary movements. In: Pompeiano O, Ajmone Marsan C (eds) Symposium “Brain mechanisms and perceptual awareness”. Raven Press, New York, pp 269–294 Fromm C, Haase J, Wolf E (1977) Depression of the recurrent inhibition of extensor motoneurones by the action of group II afferents. Brain Res 120: 459–468 Granit R (1958) Neuromuscular interaction in postural tone of the cat's isometric soleus muscle. J Physiol (Lond) 143: 387–402 Granit R (1970) The basis of motor control. Academic Press, New York London Granit R, Haase J, Rutledge LT (1960) Recurrent inhibition in relation to frequency of firing and limitation of discharge rate of extensor motoneurones. J Physiol (Lond) 154: 308–328 Haase J, Cleveland S, Ross HG (1975) Problems of postsynaptic autogenous and recurrent inhibition in the mammalian spinal cord. Rev Physiol Biochem Pharmacol (Ergebn Physiol) 73: 73–129 Haase J, Van der Meulen JP (1961) The effects of supraspinal stimulation on Renshaw cells belonging to extensor motoneurones. J Neurophysiol 24: 510–520 Haase J, Vogel B (1971) Direkte und indirekte Wirkungen supraspinaler Reizungen auf Renshaw-Zellen. Pflügers Arch 325: 334–346 Henatsch HD (1979) Supraspinal influences on the alpha motoneurone-Renshaw cell linkage. Neurosci Lett Suppl 3: 315 Henatsch HD (1983) Facts and hypotheses on the supraspinal control of the spinal Renshaw cell-motoneurone system. In: Speckmann EJ, Elger CE (eds) Epilepsy and motor system. Urban-Schwarzenberg, München Wien Baltimore, pp 78–99 Henatsch HD, Kaese HJ, Langrehr D, Meyer-Lohmann J (1961) Einflüsse des motorischen Cortex der Katze auf die Renshaw-Rückkopplungshemmung der Motoneurone. Pflügers Arch 274: 51 Henatsch HD, Meyer-Lohmann J (1971) The possible contribution of an abnormal Renshaw inhibition to extrapyramidal rigidity. Proc Internat Union Physiol Sci 9: 243 Henatsch HD, Student C, Student U, Takano K (1976) Controlled variations of input-output parameters affecting the active tension-extension diagram during muscle stretch. In: Homma S (ed) Understanding the stretch reflex. Progr Brain Res 44: 403–412 Henatsch HD, Windhorst U (1981) Die Relevanz spinaler Interneuronen-Systeme und ihrer supraspinalen Kontrollen für die Pathogenese von Spastik. In: Bauer HJ, Koella WP, Struppler A (eds) Therapie der Spastik — eine Bilanz. Symposium, Verl f angew Wissenschaften, München, pp 39–54 Hongo T, Jankowska E, Lundberg A (1969a) The rubrospinal tract. I. Effects on alpha-motoneurones innervating hindlimb muscles in cats. Exp Brain Res 7: 344–364 Hongo T, Jankowska E, Lundberg A (1969b) The rubrospinal tract. II. Facilitation of interneuronal transmission in reflex paths to motoneurones. Exp Brain Res 7: 365–391 Hongo T, Jankowska E, Lundberg A (1972) The rubrospinal tract. IV. Effects on interneurones. Exp Brain Res 15: 54–78 Hultborn H, Lindström S, Wigström H (1979) On the function of recurrent inhibition in the spinal cord. Exp Brain Res 37: 399–403 Hultborn H, Pierrot-Deseilligny E (1979) Changes in recurrent inhibition during voluntary soleus contraction in man studied by an H-reflex technique. J Physiol (Lond) 297: 229–251 Hultborn H, Pierrot-Deseilligny E, Wigström H (1979) Recurrent inhibition and afterhyperpolarization following motoneuronal discharge in the cat. J Physiol (Lond) 297: 253–266 Illert M, Lundberg A, Tanaka R (1976) Integration in descending motor pathways controlling the forelimb in the cat. 2. Convergence on neurones mediating disynaptic cortico-motoneuronal excitation. Exp Brain Res 26: 521–540 Jankowska E (1978) Some problems of projections and actions of cortico- and rubrospinal fibres. J Physiol (Paris) 74: 209–214 Jankowska E, Lindström S (1971) Morphological identification of Renshaw cells. Acta Physiol Scand 81: 428–430 Katz R, Pierrot-Deseilligny E (1982) Recurrent inhibition of alpha-motoneurons in patients with upper motor neuron lesions. Brain 105: 103–124 Koehler W, Windhorst U, Schmidt J, Meyer-Lohmann J, Henatsch HD (1978) Diverging influences on Renshaw cell responses and monosynaptic reflexes from stimulation of capsula interna. Neurosci Lett 8: 35–39 MacLean JB, Leffman H (1967) Supraspinal control of Renshaw cells. Exp Neurol 18: 94–104 Massion J (1967) The mammalian red nucleus. Physiol Rev 47: 383–436 Meyer-Lohmann J, Schaumberg R, Windhorst U (1979) Reversible local cooling as a technique for resolving complex synaptic relay functions of the red nucleus. Neurosci Lett Suppl 3: 115 Nyberg-Hansen R, Brodal A (1964) Sites and mode of termination of rubrospinal fibres in the cat. An experimental study with silver impregnation methods. J Anat (Lond) 98: 235–253 Orlovsky GN (1972) Activity of rubrospinal neurons during locomotion. Brain Res 46: 99–112 Padel Y, Armand J, Smith AM (1972) Topography of rubrospinal units in the cat. Exp Brain Res 14: 363–371 Padel Y, Steinberg R (1978) Red nucleus cell activity in awake cats during a placing reaction. J Physiol (Paris) 74: 265–282 Perciavalle V, Santangelo F, Sapienza S, Savoca F, Urbano A (1978) A ponto-interposito-rubrospinal pathway for single muscle contractions in limbs of the cat. Brain Res 155: 124–129 Piercey MF, Goldfarb J (1974) Discharge patterns of Renshaw cells evoked by volleys in ipsilateral cutaneous and highthreshold muscle afferents and their relationship to reflexes recorded in ventral roots. J Neurophysiol 37: 294–302 Pierrot-Deseilligny E, Bussel B (1975) Evidence for recurrent inhibition by motoneurons in human subjects. Brain Res 88: 105–108 Pierrot-Deseilligny E, Morin C, Katz R, Bussel B (1977) Influence of voluntary movement and posture on recurrent inhibition in human subjects. Brain Res 124: 427–436 Pierrot-Deseilligny E, Morin C (1980) Evidence for supraspinal influences on Renshaw inhibition during motor activity in man. In: Desmedt JE (ed) Spinal and supraspinal mechanisms of voluntary motor control and locomotion. Progr Clin Neurophysiol, Vol 8. Karger, Basel, pp 142–169 Pompeiano O (1984) Recurrent inhibition. In: Davidoff A (ed) Handbook of the spinal cord, Vols 2 and 3, Anatomy and physiology. Marcel Dekker, New York Basel, pp 461–557 Pompeiano O, Wand P, Srivastava UC (1985) Responses of Renshaw cells coupled with hindlimb extensor motoneurons to sinusoidal stimulation of labyrinth receptors in the decerebrate cat. Pflügers Arch (Europ J Physiol) 403: 245–257 Reinoso-Suárez F (1961) Topographischer Hirnatlas der Katze für experimental-physiologische Untersuchungen. E. Merck AG, Darmstadt Ross HG, Cleveland S, Haase J (1972) Quantitative relation of Renshaw cell discharge to monosynaptic reflex height. Pflügers Arch 332: 73–79 Ryall RW (1970) Renshaw cell mediated inhibition of Renshaw cells: pattern of excitation and inhibition from impulses in motor axon collaterals. J Neurophysiol 33: 257–270 Ryall RW (1981) Patterns of recurrent excitation and mutual inhibition of cat Renshaw cells. J Physiol (Lond) 316: 439–452 Ryall RW, Piercey MF (1971) Excitation and inhibition of Renshaw cells by impulses in peripheral afferent nerve fibers. J Neurophysiol 34: 242–251 Ryall RW, Piercey MF, Polosa C (1971) Intersegmental and intrasegmental distribution of mutual inhibition of Renshaw cells. J Neurophysiol 34: 700–707 Ryall RW, Piercey MF, Polosa C, Goldfarb J (1972) Excitation of Renshaw cells in relation to orthodromic and antidromic excitation of motoneurons. J Neurophysiol 35: 137–148 Sachs L (1978) Angewandte Statistik. Statistische Methoden und ihre Anwendungen. Springer, Berlin Heidelberg New York Shapovalov AL (1975) Neuronal organization and synaptic mechanisms of supraspinal motor control in vertebrates. Rev Physiol Biochem Pharmacol (Ergebn Physiol) 72: 1–54 Shinoda Y, Ghez C, Arnold A (1977) Spinal branching of rubrospinal axons in the cat. Exp Brain Res 30: 203–218 Soechting JF, Burton JE, Onoda N (1978) Relationship between sensory input, motor output, and unit activity in interpositus and red nuclei during intentional movement. Brain Res 152: 365–379 Thomas RC, Wilson VJ (1965) Precise localization of Renshaw cells with a new marking technique. Nature (Lond) 206: 211–213 Willis WD (1969) The localization of functional groups of interneurones. In: Brazier A (ed) The interneuron. Univ. of Calif. Press, Berkeley-Los Angeles, pp 267–287 Wilson VJ, Talbot WH, Kato M (1964) Inhibitory convergence upon Renshaw cells. J Neurophysiol 27: 1063–1079 Windhorst U, Ptok M, Meyer-Lohmann J, Schmidt J (1978) Effects of conditioning stimulation of the contralateral n. ruber on antidromic Renshaw cell responses and monosynaptic reflexes. Pflügers Arch 373: (Suppl) R 70