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Experimental Brain Research

, Volume 68, Issue 3, pp 643–656 | Cite as

Proprioceptive input resets central locomotor rhythm in the spinal cat

  • B. A. Conway
  • H. Hultborn
  • O. Kiehn
Article

Summary

The reflex regulation of stepping is an important factor in adapting the step cycle to changes in the environment. The present experiments have examined the influence of muscle proprioceptors on centrally generated rhythmic locomotor activity in decerebrate unanesthetized cats with a spinal transection at Th12. Fictive locomotion, recorded as alternating activity in hindlimb flexor and extensor nerves, was induced by administration of nialamide (a monoamine oxidase inhibitor) and L-DOPA. Brief electrical stimulation of group I afferents from knee and ankle extensors were effective in resetting fictive locomotion in a coordinated fashion. An extensor group I volley delivered during a flexor burst would abruptly terminate the flexor activity and initiate an extensor burst. The same stimulus given during an extensor burst prolonged the extensor activity while delaying the appearance of the following flexor burst. Intracellular recordings from motoneurones revealed that these actions were mediated at premotoneuronal levels resulting from a distribution of inhibition to centres generating flexor bursts and excitation of centres generating extensor bursts. These results indicate that extensor group I afferents have access to central rhythm generators and suggest that this may be of importance in the reflex regulation of stepping. Experiments utilizing natural stimulation of muscle receptors demonstrate that the group I input to the rhythm generators arises mainly from Golgi tendon organ Ib afferents. Thus an increased load of limb extensors during the stance phase would enhance and prolong extensor activity while simultaneously delaying the transition to the swing phase of the step cycle.

Key words

Spinal cord Motoneurones Fictive locomotion Group I afferents Resetting Entrainment 

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References

  1. Andén N-E, Jukes MGM, Lundberg A, Vyklicky L (1966) The effect of DOPA on the spinal cord 1. Influence on transmission from primary afferents. Acta Physiol Scand 67: 373–386Google Scholar
  2. Andersson O, Forssberg H, Grillner S, Lindquist M (1978a) Phasic gain control of the transmission in cutaneous reflex pathways to motoneurones during ‘fictive locomotion’. Brain Res 149: 503–507Google Scholar
  3. Andersson O, Grillner S (1981) Peripheral control of the cat's step cycle. I. Phase dependent effects of ramp-movements of the hip during “fictive locomotion”. Acta Physiol Scand 113: 89–101Google Scholar
  4. Andersson O, Grillner S (1983) Peripheral control of the cat's step cycle. II. Entrainment of the central pattern generators for locomotion by sinusoidal hip movements during “fictive locomotion”. Acta Physiol Scand 118: 229–239PubMedGoogle Scholar
  5. Andersson O, Grillner S, Lindquist M, Zomlefer M (1978b) Peripheral control of the spinal pattern generators for locomotion in cat. Brain Res 150: 625–630Google Scholar
  6. Bässler U (1986) Afferent control of walking movements in the stick insect Cuniculina impigra. II. Reflex reversal and the release of the swing phase in the restrained foreleg. J Comp Physiol A 158: 351–362Google Scholar
  7. Brown MC, Engberg I, Matthews PBC (1967) The relative sensitivity to vibration of muscle receptors of the cat. J Physiol 192: 773–800Google Scholar
  8. Brown TG (1911) The intrinsic factors in the act of progression in the mammal. Proc R Soc Lond B 84: 308–319Google Scholar
  9. Brown TG (1924) Studies in the physiology of the nerveous system. XXVIII: absence of algebraic equality between the magnitudes of central excitation and effective central inhibition given in the reflex centre of a single limb by the same reflex stimulus. Q J Exp Physiol 14: 1–23Google Scholar
  10. Conway BA, Hultborn H, Kiehn O (1987a) Effects of extensor group I afferent stimulation on rhythmic activity in the spinal cat during locomotion. Neurosci Lett Suppl 29: S64Google Scholar
  11. Conway BA, Hultborn H, Kiehn O (1987b) Resetting rhythmic activity by extensor group I afferent stimulation in the spinal cat during fictive locomotion. Acta Physiol Scand 129 (3): C11Google Scholar
  12. Coombs JS, Eccles JC, Fatt P (1955) The specific ionic conductances and the ionic movements across the motoneuronal membrane that produce the inhibitory post-synaptic potential. J Physiol 130: 326–373Google Scholar
  13. Duysens J, Pearson KG (1980) Inhibition of flexor burst generation by loading ankle extensor muscles in walking cats. Brain Res 187: 321–332Google Scholar
  14. Engberg I, Lundberg A (1969) An electromyographic analysis of muscular activity in the hindlimb of the cat during unrestrained locomotion. Acta Physiol Scand (75): 614–630Google Scholar
  15. Fetz EE, Jankowska E, Johannisson T, Lipski J (1979) Autogenic inhibition of motoneurones by impulses in group Ia muscle spindle afferents. J Physiol 293: 173–195Google Scholar
  16. Forssberg H (1979) Stumbling corrective reaction: A phase-dependent compensatory reaction during locomotion. J Neurophysiol 42: 936–953PubMedGoogle Scholar
  17. Forssberg H, Grillner S, Rossignol S (1977) Phasic gain control of reflexes from the dorsum of the paw during spinal locomotion. Brain Res 132: 121–139Google Scholar
  18. Grillner S (1981) Control of locomotion in bipeds, tetrapods, and fish. In: Brooks VD (ed) Handbook of physiology, Sect 1. The nervous system. II. Motor control. American Physiological Society, Maryland, Waverly Press, pp 1179–1236Google Scholar
  19. Grillner S, Rossignol S (1978) On the initiation of the swing phase of locomotion in the chronic spinal cats. Brain Res 146: 269–277Google Scholar
  20. Grillner S, Zangger P (1974) Locomotor movements generated by the deafferented spinal cord. Acta Physiol Scand 91: 38A-39AGoogle Scholar
  21. Houk J, Henneman E (1967) Responses of Golgi tendon organs to active contractions of the soleus muscle of the cat. J Neurophysiol 30: 466–481Google Scholar
  22. Houk J, Simon W (1967) Responses of Golgi tendon organs to forces applied to muscle tendon. J Neurophysiol 30: 1466–1481Google Scholar
  23. Jankowska E, Jukes MGM, Lund S, Lundberg A (1967a) The effect of DOPA on the spinal cord 5. Reciprocal organization of pathways transmitting excitatory action to alpha motoneurones of flexor and extensors. Acta Physiol Scand 70: 369–388Google Scholar
  24. 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: 389–402Google Scholar
  25. Jankowska E, McCrea DA (1983) Shared reflex pathways from Ib tendon organ afferents and Ia muscle spindle afferents in the cat. J Physiol 338: 99–111Google Scholar
  26. Jansen JKS, Rudjord T (1964) On the silent period and Golgi tendon organs of the soleus muscle of the cat. Acta Physiol Scand 62: 364–379Google Scholar
  27. Lennard PR (1985) Afferent perturbations during “monopodal” swimming movements in the turtle: phase-dependent cutaneous modulation and proprioceptive resetting of the locomotor rhythm. J Neurosci 5: 1434–1445Google Scholar
  28. Lundberg A (1979) Multisensory control of spinal reflex pathways. In: Granit R, Pompeiano O (eds) Reflex control of posture and movement. Prog Brain Res, Vol 50. Eisevier Biomedical Press, Amsterdam, pp 11–28Google Scholar
  29. Pearson KG, Duysens J (1976) Function of segmental reflexes in the control of stepping in cockroaches and cats. In: Herman RM, Grillner S, Stein PSG, Stuart DG (eds) Neural control of locomotion. Plenum Press, New York, pp 519–537Google Scholar
  30. Pollock LJ, Davis L (1923) Studies in decerebration I. A method of decerebration. Arch Neurol Psychiat Chicago 10: 391–398Google Scholar
  31. Schomburg ED, Behrends HB (1978a) Phasic control of the transmission in the excitatory and inhibitory reflex pathways from cutaneous afferents to alpha-motoneurones during fictive locomotion in cats. Neurosci Lett 8: 277–282Google Scholar
  32. Schomburg ED, Behrends HB (1978b) The possibility of phasedependent monosynaptic and polysynaptic Ia excitation to homonymous motoneurones during fictive locomotion. Brain Res 143: 533–537Google Scholar
  33. Sillar KT, Skorupski P, Elson RC, Bush BMH (1986) Two identified afferent neurones entrain a central rhythm generator. Nature 323: 440–443Google Scholar
  34. Viala D, Buser P (1971) Modalités d'otention de rythmes locomoteurs chez le lapin spinal par traitements pharmacologiques (DOPA, 5-HTP, d'amphétamine). Brain Res 35: 151–165Google Scholar

Copyright information

© Springer-Verlag 1987

Authors and Affiliations

  • B. A. Conway
    • 1
  • H. Hultborn
    • 1
  • O. Kiehn
    • 1
  1. 1.Department of NeurophysiologyThe Panum Institute, University of CopenhagenCopenhagenDenmark

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