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An ascending spinal pathway transmitting a central rhythmic pattern to the magnocellular red nucleus in the cat

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Abstract

The activity of cells in the magnocellular red nucleus (RNm) was recorded extra and intracellularly in the curarized thalamic cat performing fictive locomotion. The locomoter episodes were detected from the rhythmic activity recorded in the motor nerves of the contralateral hindlimb. It was confirmed that, during fictive locomotion, a large proportion of the rubrospinal cells (56% in our sample) exhibit a rhythmic pattern of activity which is synchronized with the efferent spinal motor nerve activity. On the basis of the intracellular recordings it was established that phases of intense synaptic activity with mixed excitatory postsynaptic potentials (EPSPs) and inhibitory postsynaptic potentials (IPSPs) are involved in this rhythmicity. After eliminating the cerebellar input to the RNm, it was observed that the cells still received intense excitatory and inhibitory inputs, resulting in a continuous modulation of their membrane potential, due to the occurrence of EPSPs and IPSPs. During fictive locomotor like activity and after elimination of the cerebellar afferents to the RNm, it was observed that the spontaneous PSPs in RNm cells (in the case of 45% of the cells) were organized in repetitive subthreshold bursts occurring in phase relationships with the activity recorded in the motor nerves. Some extracellularly recorded cells (12%) showed a rhythmic firing pattern. It is generally recognized that, in the thalamic cat preparation, the locomotor pattern observed in efferent nerves originates from the central pattern generator (CPG) of the spinal cord. It therefore seems likely that the rhythmicity observed here in the RNm may originate from the spinal CPG and be transmitted through the spino rubral pathway ascending in the ventral part of the cord. It is concluded that the spino rubral pathway may transmit both somatosensory information and corollary discharges relating to the activity of the spinal CPG for locomotion.

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References

  • Armstrong DM, Edgley SA (1984) Discharges of nucleus inter positus neurones during locomotion in the cat. J Physiol (Lond) 351:411–432

    Google Scholar 

  • Arshavsky YI, Orlovsky GN, Pavlova GA, Perret C (1978) Messages conveyed by descending tracts during scratching in the cat. II. Activity of rubrospinal neurons. Brain Res 159:111–123

    Google Scholar 

  • Arshavsky YI, Orlovsky GN, Perret C (1988) Activity of rubrospinal neurons during locomotion and scratching in the cat. Behav Brain Res 28:193–200

    Google Scholar 

  • Baldissera F, Hultborn H, Illert M (1981) Integration in spinal neuronal systems. In: Brooks VB (eds) Motor control. (Handbook of physiology, sect 1, The nervous system, vol II) American Physiological Society, Bethesda, MD, pp 509–595

    Google Scholar 

  • Brock LG, Coombs JS, Eccles JC (1953) Intracellular recording from antidromically activated motoneurones. J Physiol (Lond) 122:429–461

    Google Scholar 

  • Cabelguen JM, Millanvoye M, Perret C (1973) Caractéristiques centrales et efférentes de l'activité rythmique de type locomoteur chez le chat décortiqué aigu après ablation du cervelet (abstract). J Physiol (Paris) 67:253A

    Google Scholar 

  • Daadi M, Condé F, Gavioli M, Padel Y (1991) Existence of collateral branching to the red nucleus from the spinothalamic system in the cat. Demonstration using a double labelling neuroanatomical method. Eur J Neurosci [Suppl] 4:34

    Google Scholar 

  • Davis R (1969) Brachiorubral and rubrobrachial activity in the cat. Brain Res 15:157–173

    Google Scholar 

  • Dubuc R, Cabelguen JM, Rossignol S (1988) Rhythmic fluctuations of dorsal root potentials and antidromic discharges of primary afferents during fictive locomotion in the cat. J Neurophysiol 60:2014–2036

    Google Scholar 

  • Eccles RM, Lundberg A (1958) Integrative pattern of Ia synaptic actions on motoneurones of hip and knee muscles. J Physiol (Lond) 144:271–298

    Google Scholar 

  • Eccles RM, Lundberg A (1959) Synaptic actions in motoneurones by afferents which may evoke the flexion reflex. Arch Ital Biol 97:199–221

    Google Scholar 

  • Edgerton VR, Grillner S, Sjöström A, Zangger P (1976) Central generation of locomotion in vertebrates. In: Herman R, Grillner S, Stein P, Stuart D (eds) Neural control of locomotion, vol 18. Plenum, New York, pp 439–464

    Google Scholar 

  • Engberg I, Lundberg A (1969) An electromyographic analysis of muscular activity in the hindlimb of the cat during unrestrained locomotion. Acta Physiol Scand 75:614–630

    Google Scholar 

  • Grillner S (1969) The influence of DOPA on the static and the dynamic fusimotor activity to the triceps surae of the spinal cat. Acta Physiol Scand 27:490–509

    Google Scholar 

  • Grillner S (1981) Control of locomotion in biped, tetrapods and fish. In: Brooks VB (eds) Motor control. (Handbook of physiology, Sect 1, The nervous system, vol II) American Physiological Society, Bethesda, MD, pp 1179–1236

    Google Scholar 

  • Grillner S (1986) The effect of lDOPA on the spinal cord. Relation to locomotion and the half center hypothesis. In: Grillner S, Stein PSG, Stuart DG, Forssberg H, Herman RM (eds) Neurobiology of vertebrate locomotion. (International symposium series, vol 45) Wenner-Gren, Stockton, NY, pp 269–277

    Google Scholar 

  • Grillner S, Zangger P (1974) Locomotor movements generated by the deafferented spinal cord. Acta Physiol Scand 91:38A-39A

    Google Scholar 

  • Holmqvist B, Lundberg A, Oscarsson O (1960) Supraspinal inhibitory control of transmission to three ascending spinal pathways influenced by the flexion reflex afferents. Arch Ital Biol 98:60–80

    Google Scholar 

  • Jankowska E, Jukes MGM, Lund S, Lundberg A (1967a) The effect of DOPA on the spinal cord. 5. Reciprocal organization of pahtways transmitting excitatory action to alpha motoneurones of flexors and extensors. Acta Physiol Scand 70:369–388

    Google Scholar 

  • Jankowska E, Jukes MGM, Lund S, Lundberg A (1967b) The effect of DOPA on the spinal cord. 6. Half centre organization of interneurones transmitting effects from the flexor reflex afferents. Acta Physiol Scand 70:389–402

    Google Scholar 

  • fnLundberg A (1959) Integrative significance of patterns of connections made by muscle afferents in the spinal cord. In: Congress International de Ciencias Fisiologicas XXI, Buenos Aires, pp 100–105

  • Lundberg A (1969) Reflex control of stepping. In: The Nansen Memorial Lecture V, Universitetsforlaget Oslo, pp 5–42

  • Lundberg A (1982) Inhibitory control from the brain stem of transmission from primary afferents to motoneurones, primary afferent terminals and ascending pathways. In: Sjölund B, Börklund A (eds) Brain stem control of spinal mechanism. Elsevier Biomedical, Amsterdam, pp 179–224

    Google Scholar 

  • Lundberg A, Oscarsson O (1962) Two ascending spinal pathways in the ventral part of the cord. Acta Physiol Scand 54:270–286

    Google Scholar 

  • Murakami F, Katsumaru H, Wu JY, Matsuda T, Tsukahara N (1983) Immunocytochemical demonstration of GABAergic synapses on identified rubrospinal neurons. Brain Res 267:357–360

    Google Scholar 

  • Orlovsky GN (1972a) Activity of rubrospinal neurons during locomotion. Brain Res 46:99–112

    Google Scholar 

  • Orlovsky GN (1972b) Work of the neurons of the cerebellar nuclei during locomotion. Biophysics 17:1177–1185

    Google Scholar 

  • Orlovsky GN, Feldman AG (1972) Role of afferent activity in the generation of stepping movements. Neurophysiology 4:304–310

    Google Scholar 

  • Orsal D, Perret C, Cabelguen JM (1988) Comparison between ventral spinocerebellar and rubrospinal activities during locomotion in the cat. Behav Brain Res 28:159–162

    Google Scholar 

  • Oscarsson O (1973) Functional organization of spinocerebellar paths. In: Iggo A (eds) Somatosensory system. (Handbook of sensory physiology, vol II) Springer, Berlin Heidelberg New York, pp 339–380

    Google Scholar 

  • Padel Y, Armand J, Smith AM (1972) Topography of rubrospinal units in the cat. Exp Brain Res 14:363–371

    Google Scholar 

  • Padel Y, Bourbonnais D (1985) A ventral spinal pathway transmitting sensory input to rubrospinal cells in the cat. Neurosci Lett [Suppl 22] S8

  • Padel Y, Jeneskog T (1981) Inhibition of rubrospinal cells by somaesthetic afferent activity. Neurosci Lett 21:177–182

    Google Scholar 

  • Padel Y, Relova JL (1988) A common somaesthetic pathway to red nucleus and motor cortex. Behav Brain Res 28:153–157

    Google Scholar 

  • Padel Y, Relova JL (1991) Somatosensory responses in the cat motor cortex. I. Identification and course of an afferent pathway. J Neurophysiol 66:2041–2058

    Google Scholar 

  • Padel Y, Sybirska E (1984) Where is the synaptic relay in the sensory pathway to red nucleus? Neurosci Lett [Suppl 18] S391

  • Padel Y, Bourbonnais D, Sybirska E (1986) A new pathway from primary afferents to the red nucleus. Neurosci Lett 64:75–80

    Google Scholar 

  • Padel Y, Sybirska E, Bourbonnais D, Vinay L (1988) Electrophysiological identification of a somaesthetic pathway to the red nucleus. Behav Brain Res 28, 139–151

    Google Scholar 

  • Perret C (1968) Relations entre activités efférentes spontanées de nerfs moteurs de la patte postérieure et activités de neurones du tronc cérébral chez le chat décortiqué. J Physiol (Paris) 60:511–512

    Google Scholar 

  • Perret C (1976) Neural control of locomotion in the decorticate cat. In: Herman RM, Grillner S, Stein PSG, Stuart DG (eds) Neural control of locomotion. Plenum, New York, pp 587–615

    Google Scholar 

  • Perret C, Cabelguen JM (1980) Main characteristics of the hindlimb locomotor cycle in the decorticate cat with special reference to bifunctional muscles. Brain Res 187:333–352

    Google Scholar 

  • Perret C, Millanvoye M, Cabelguen JM (1972) Messages spinaux ascendants pendant une locomotion fictive chez le chat curarisé (abstract). J Physiol (Paris) 65:153A

    Google Scholar 

  • Ralston DD, Milroy AM (1989) Red nucleus of Macaca fascicularis: an electron microscopic study of its synaptic organization. J Comp Neurol 284:602–620

    Google Scholar 

  • Shimamura M, Kogure I, Fuwa T (1984a) Role of joint afferents in relation to the initiation of forelimb stepping in thalamic cats. Brain Res 297:225–234

    Google Scholar 

  • Shimamura M, Kogure I, Fuwa T (1984b) The role of paralemniscal pontine reticular formation in forelimb stepping of thalamic cats. Neurosci Res 1:393–410

    Google Scholar 

  • Steeves JD, Jordan LM (1980) Localization of a descending pathway in the spinal cord which is necessary for control treadmill locomotion. Neurosci Lett 20:283–288

    Google Scholar 

  • Toyama K, Tsukahara N, Udo M (1968) Nature of the cerebellar influences upon the red nucleus neurones. Exp Brain Res 4:292–309

    Google Scholar 

  • Toyama K, Tsukahara N, Kosaka K, Matsunami K (1970) Synaptic excitation of red nucleus neurones by fibers from interpositus nucleus. Exp Brain Res 11:187–198

    Google Scholar 

  • Tsukahara N, Toyama K, Kosaka K, Udo M (1965) “Disfacilitation” of red nucleus neurones. Experientia 21:544–1965

    Google Scholar 

  • Tsukahara N, Toyama K, Kosaka K (1967) Electrical activity of red nucleus neurones investigated with intracellular microelectrodes. Exp Brain Res 4:18–33

    Google Scholar 

  • Viala D, Valin A, Buser P (1974) Relationship between the “late reflex discharge” and locomotor movements in acute spinal cats and rabbits treated with DOPA. Arch Ital Biol 112:299–306

    Google Scholar 

  • Vinay L, Padel Y (1990) Spatiotemporal organization of the somaesthetic projections in the red nucleus transmitted through the spinorubral pathway in the cat. Exp Brain Res 79:412–426

    Google Scholar 

  • Walberg F, Nordby T (1981) A reexamination of the rubroolivary tract in the cat, using horseradish peroxidase as a retrograde and an anterograde neuronal tracer. Neuroscience 6:2379–2391

    Google Scholar 

  • Walberg F, Dietrichs E, Nordby T (1986) The origin and termination of the dentatorubral fibres in the cat as studied with retro grade and anterograde transport of peroxidase labelled lectin. Exp Brain Res 63:294–300

    Google Scholar 

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Author notes

  1. Daniel Bourbonnais

    Present address: Ecole de Réadaptation, Université de Montréal, Succursale A, CP 6128, Montreal, Quebec, Canada

  2. Heinz Steffens

    Present address: Physiologisches Institut der Universität Göttingen, D-37018, Göttingen, Germany

Authors and Affiliations

  1. Faculté de Médecine, Centre de Recherche “Cerveau et Cognition”, CNRS, 133 route de Narbonne, F-31062, Toulouse, France

    Laurent Vinay, Yves Padel, Daniel Bourbonnais & Heinz Steffens

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  1. Laurent Vinay
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  2. Yves Padel
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  3. Daniel Bourbonnais
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  4. Heinz Steffens
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Vinay, L., Padel, Y., Bourbonnais, D. et al. An ascending spinal pathway transmitting a central rhythmic pattern to the magnocellular red nucleus in the cat. Exp Brain Res 97, 61–70 (1993). https://doi.org/10.1007/BF00228817

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  • DOI: https://doi.org/10.1007/BF00228817

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