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Modulation of short latency cutaneous excitation in flexor and extensor motoneurons during fictive locomotion in the cat

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Summary

We examined modulation of transmission in short-latency, distal hindlimb cutaneous reflex pathways during fictive locomotion in 19 decerebrate cats. Fictive stepping was produced either by electrical stimulation of the mesencephalic locomotor region (MLR) or by administration of Nialamide and 1-DOPA to acutely spinalized animals. Postsynaptic potentials (PSPs) produced by electrical stimulation of low threshold afferents (< 2.5 times threshold) in the superficial peroneal (SP), sural, saphenous or medial plantar nerves were recorded intracellularly from various extensor (n = 28) and flexor (n = 24) motoneurons and averaged throughout the step cycle, together with voltage responses to intrasomatic constant current pulses (in order to monitor relative cell input resistance). Each motoneuron studied displayed rhythmic background oscillations in membrane potential and correlated variations in input resistance. The average input resistance of extensor motoneurons was lowest during mid-flexion, when the cells were relatively hyperpolarized and silent. Conversely, average input resistance of flexor motoneurons was highest during mid-flexion, when they were depolarized and active. The amplitude of the minimum-latency excitatory components of PSPs produced by cutaneous nerve stimulation were measured from computer averaged records representing six subdivisions of the fictive step cycle. Oligosynaptic EPSP components were consistently modulated only in the superficial peroneal responses in flexor motoneurons, which exhibited enhanced amplitude during the flexion phase. With the other skin nerves tested (sural, saphenous, and plantar), no consistent patterns of modulation were observed during fictive locomotion. We conclude that transmission through some, but not all, oligosynaptic excitatory cutaneous pathways is enhanced by premotoneuronal mechanisms during the flexion phase of fictive stepping in several cat hindlimb motor nuclei. The present results suggest that the patterns of interaction between the locomotor central pattern generator and excitatory cutaneous reflex pathways depend on the source of afferent input and on the identity of the target motoneuron population.

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References

  • Abraham LD, Marks WB, Loeb GE (1985) The distal hindlimb musculature of the cat: cutaneous reflexes during locomotion. J Neurophysiol 58: 594–603

    Google Scholar 

  • Anderson O, Forssberg H, Grillner S, Lindquist M (1978) Phasic gain control of the transmission in cutaneous reflex pathways to motoneurons during ‘fictive’ locomotion. Brain Res 149: 503–507

    Google Scholar 

  • Bayev KV, Kostyuk PG (1982) Polarization of primary afferent terminals of lumbosacral cord elicited by the activity of spinal locomotor generator. Neuroscience 7: 1401–1409

    Google Scholar 

  • Burke RE, Fedina L, Lundberg A (1971) Spatial synaptic distribution of recurrent and group Ia inhibitory systems in cat spinal motoneurons. J. Physiol (Lond) 214: 304–326

    Google Scholar 

  • Burke RE, Fleshman JW (1986) Strategies to identify interneurons involved in locomotor pattern generation in the mammalian spinal cord. In: Grillner S, Stein PSG, Stuart DG, Herman R (eds) Neurobiology of vertebrate locomotion: Wenner-Gren Center International Symposium, Vol. 45. Macmillan, London, pp 245–268

    Google Scholar 

  • Burke RE, Jankowska E, ten Bruggencate G (1970) A comparison of peripheral and rubrospinal synaptic input to slow and fast twitch motor units of triceps surae. J. Physiol (Lond) 207: 709–732

    Google Scholar 

  • Chandler SH, Baker LL, Goldberg LJ (1984) Characterization of synaptic potentials in hindlimb motoneurons during 1-DOPA-induced fictive locomotion in acute and chronic spinal cats. Brain Res 303: 91–100

    Google Scholar 

  • Coombs JS, Eccles JC, Fatt P (1955) The inhibitory suppression of reflex discharges from motoneurons, J. Physiol (Lond) 130: 396–413

    Google Scholar 

  • Dubuc R, Cabelguen J-M, Rossignol S (1985) Rhythmic antidromic discharges of single primary afferents recorded in cut dorsal root filaments during locomotion in the cat. Brain Res 359: 375–378

    Google Scholar 

  • Duysens J, Loeb GE (1980) Modulation of ipsi- and contralateral reflex responses in unrestrained walking cats. J Neurophysiol 44: 1024–1037

    Google Scholar 

  • Duysens J, Pearson KG (1976) The role of cutaneous afferents from the distal hindlimb in the regulation of the step cycle of thalamic cats. Exp Brain Res 24: 245–255

    Google Scholar 

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

    Google Scholar 

  • Feldman AG, Orlovsky GN (1975) Activity of interneurons mediating reciprocal Ia inhibition during locomotion. Brain Res 84: 181–194

    Google Scholar 

  • Fleshman JW, Lev-Tov A, Burke RE (1984) Peripheral and central control of flexor digitorum longus and flexor hallucis longus motoneurons: the synaptic basis of functional diversity. Exp Brain Res 54: 133–149

    Google Scholar 

  • Fleshman JW, Rudomin P, Burke RE (1988) Supraspinal control of a short-latency cutaneous pathway to hindlimb motoneurons. Exp Brain Res 69: 449–459

    Google Scholar 

  • Forssberg H (1979) Stumbling corrective reaction: a phase-dependent compensatory reaction during locomotion. J. Neurophysiol 42: 936–953

    Google Scholar 

  • Forssberg H, Grillner S, Rossignol S (1975) Phase dependent reflex reversal during walking in chronic spinal cats. Brain Res 85: 103–107

    Google Scholar 

  • Forssberg H, Grillner S, Rossignol S (1977) Phasic gain control of relexes from the dorsum of the paw during spinal locomotion. Brain Res 132: 121–139

    Google Scholar 

  • Gossard JP, Cabelguen JM, Saltiel P, Drew T, Rossignol S (1987) Rhythmic modulation of cutaneous afferent membrane potential during fictive locomotion in the cat. Soc. Neurosci Abstr 13: 321.9

    Google Scholar 

  • Grillner S, Shik ML (1973) On the descending control of the lumbosacral spinal cord from the “mesencephalic locomotor region”. Acta Physiol Scand 87: 320–333

    Google Scholar 

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

    Google Scholar 

  • Grillner S, Zangger P (1979) On the central generation of locomotion in the low spinal cat. Exp Brain Res 34: 241–261

    Google Scholar 

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

    Google Scholar 

  • Jordan LM (1983) Factors determining motoneuron rhythmicity during fictive locomotion. Soc Exp Biol Symp 37: 423–444

    Google Scholar 

  • Kniffki KD, Schomburg ED, Steffens H (1981) Effects from fine muscle and cutaneous afferents on spinal locomotion in cats. J. Physiol (Lond) 319: 543–554

    Google Scholar 

  • Loeb GE, Marks WB, Hoffer JA (1987) Cat hindlimb motoneurons during locomotion. IV. Participation in cutaneous reflexes. J Neurophysiol 57: 563–573

    Google Scholar 

  • O'Donovan MJ, Pinter MJ, Dum RP, Burke RE (1982) Actions of FDL and FHL muscles in intact cats: functional dissociation between anatomical synergists. J. Neurophysiol 47: 1126–1143

    Google Scholar 

  • Omeniuk DJ, Schmidt BJ, Burke RE (1986) Central latencies of PSPs evoked by low threshold cutaneous afferents in cat α-motoneurons. Soc Neurosci Abstr 12: 70.6

    Google Scholar 

  • Orsal D, Perret C, Cabelguen J-M (1986) Evidence of rhythmic inhibitory synaptic influences in hindlimb motoneurons during fictive locomotion in the thalamic cat. Exp Brain Res 64: 217–224

    Google Scholar 

  • Perret C (1983) Centrally generated pattern of motoneuron activity during locomotion in the cat. Soc Exp Biol Symp 37: 405–422

    Google Scholar 

  • Perret C, Cabelguen J-M (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 

  • Pratt CA, Jordan L (1987) Ia inhibitory interneurons and Renshaw cells as contributors to the spinal mechanisms of fictive locomotion. J. Neurophysiol 57: 56–71

    Google Scholar 

  • Rall W (1967) Distinguishing theoretical synaptic potentials computed for different somadendritic distributions of synaptic input. J. Neurophysiol 30: 1138–1168

    Google Scholar 

  • Rall W, Burke RE, Smith TG, Nelson PG, Frank K (1967) Dendritic location of synapses and possible mechanisms for the monosynapatic EPSP in motoneurons. J Neurophysiol 30: 1169–1193

    Google Scholar 

  • Schmidt BJ, Meyers DER, Tokuriki M, Fleshman JW, Burke RE (1986) Modulation of short latency EPSPs from cutaneous afferents to FDL motoneurons during fictive locomotion in the cat. Soc Neurosci Abstr 12: 242.9

    Google Scholar 

  • Schmidt BJ, Meyers DER, Fleshman JW, Tokuriki M, Burke RE (1988) Phasic modulation of short latency cutaneous excitation in flexor digitorum longus motoneurons during fictive locomotion. Exp Brain Res 71: 568–578

    Google Scholar 

  • Schmidt BJ, Meyers DER, Tokuriki M, Fleshman JW, Burke RE (1987) Modulation of short latency cutaneous excitation in flexor and extensor motoneurons during fictive locomotion in the cat. Soc. Neurosci Abstr 13: 232.9

    Google Scholar 

  • Schomburg ED, Behrends HB (1978) Phasic control of the transmission in the excitatory and inhibitory reflex pathways from cutaneous afferents to alpha-motoneurons during fictive locomotion in cats. Neurosci Lett 8: 277–282

    Google Scholar 

  • Schomburg ED, Behrends HB, Steffens H (1978) Alteration of transmission in segmental pathways from flexor reflex afferents (FRA) to alpha-motoneurons during spinal locomotor activity. Neurosci Lett Suppl 1: S 103

    Google Scholar 

  • Schomburg ED, Behrends HB, Steffens H (1981) Changes in segmental and propriospinal reflex pathways during spinal locomotion. In: Taylor A, Prochazka A (eds) Muscle receptors and movement. Macmillan, London, pp 413–425

    Google Scholar 

  • Shefchyk SJ, Jordan LM (1985a) Motoneuron input-resistance changes during fictive locomotion produced by stimulation of the mesencephalic locomotor region. J Neurophysiol 54:1101–1108

    Google Scholar 

  • Shefchyk, SJ and Jordan, LM (1985b) Excitatory and inhibitory postsynaptic potentials in alpha-motoneurons produced during fictive locomotion by stimulation of the mesencephalic locomotor region. J. Neurophysiol 53: 1345–1355

    Google Scholar 

  • Shik ML, Severin FV, Orlovsky GN (1966) Control of walking and running by means of electrical stimulation of the midbrain. Biophysics 11: 756–765

    Google Scholar 

  • Smith TG, Wuerker RB, Frank K (1967) Membrane impedance changes during synaptic transmission in cat spinal motoneurons. J. Neurophysiol 30: 1072–1096

    Google Scholar 

  • Zar JH (1984) Biostatistical analysis. Prentice-Hall, Englewood Cliffs NJ

    Google Scholar 

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Author notes

  1. B. J. Schmidt

    Present address: Dept. of Neurology, Univ. of Manitoba School of Medicine, Winnipeg, Manitoba, Canada

  2. D. E. R. Meyers

    Present address: Bekesy Laboratory of Neurobiology, University of Hawaii at Manoa, Honolulu, Hawaii

  3. M. Tokuriki

    Present address: Dept. of Veterinary Physiology, Faculty of Agriculture, Yamaguchi University, Yamaguchi, Japan

Authors and Affiliations

  1. Laboratory of Neural Control, National Institute of Neurological and Communicative Disorders and Stroke, National Institutes of Health, 20892, Bethesda, MD, USA

    B. J. Schmidt, D. E. R. Meyers, M. Tokuriki & R. E. Burke

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  1. B. J. Schmidt
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  2. D. E. R. Meyers
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  3. M. Tokuriki
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  4. R. E. Burke
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Schmidt, B.J., Meyers, D.E.R., Tokuriki, M. et al. Modulation of short latency cutaneous excitation in flexor and extensor motoneurons during fictive locomotion in the cat. Exp Brain Res 77, 57–68 (1989). https://doi.org/10.1007/BF00250567

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  • DOI: https://doi.org/10.1007/BF00250567

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