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A neuronal mechanism for sensory gating during locomotion in a vertebrate

Abstract

The response of the foot to touch during walking depends on whether it is in the air or on the ground. In most animals, reflex responses to external stimuli are similarly adapted to their timing in the locomotor cycle, but there is only fragmentary information about the neural mechanisms involved. In arthropods, reflex modulation can occur in the sensory receptors themselves1 and in neurons that discharge during locomotion2,3. By recording with dye-filled microelectrodes from neurons in the spinal cord of frog embryos, we describe reflex modulation at the level of sensory interneurons. Sensory inputs from skin receptors excite a specific class of spinal sensory interneuron whose activity leads to reflex bending of the body away from the stimulus. During swimming, these inputs are gated by rhythmic postsynaptic inhibition, so that sensory drive reaches motor neurons only at phases in the locomotor cycle when the resulting contraction would likewise turn the embryo away from the stimulated side. Such gating of sensory pathways could be a general feature of all locomotor systems where responses to sensory stimuli need to be adapted to the phase of locomotion.

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References

  1. Sillar, K. T. & Skorupski, P. J. Neurophysiol. 55, 678–688 (1986).

    Article  CAS  Google Scholar 

  2. Reichert, H. & Rowell, C. H. F. J. Neurophysiol. 53, 1201–1218 (1985).

    Article  CAS  Google Scholar 

  3. Reichert, H., Rowell, C. H. F. & Gris, C. Nature 315, 142–144 (1985).

    Article  ADS  Google Scholar 

  4. Clarke, J. D. W. & Roberts, A. J. Physiol., London. 354, 345–362 (1984).

    Article  CAS  Google Scholar 

  5. Roberts, A., Dale, N., Evoy, W. H. & Soffe, S. R. J. Neurophysiol. 54, 1–10 (1984).

    Article  Google Scholar 

  6. Roberts, A. & Clarke, J. D. W. Phil. Trans. R. Soc. Lond. B. 296, 195–212 (1982).

    Article  CAS  Google Scholar 

  7. Clarke, J. D. W., Hayes, B. P., Hunt, S. P. & Roberts, A. J. Physiol., London. 348, 511–525 (1984).

    Article  CAS  Google Scholar 

  8. Sillar, K. T. & Roberts, A. J. Neurosci. (in the press).

  9. Dale, N. J. Physiol., London. 363, 61–70 (1985).

    Article  CAS  Google Scholar 

  10. Dale, N., Ottersen, O. P., Roberts, A. & Storm-Mathisen, J. Nature 324, 255–257 (1987).

    Article  ADS  Google Scholar 

  11. Kahn, J. A. & Roberts, A. Phil. Trans. R. Soc. Lond. B 296, 229–243 (1982).

    Article  CAS  Google Scholar 

  12. Sillar, K. T. J. Physiol., London. 382, 181P (1986).

    Google Scholar 

  13. Roberts, A., Soffe, S. R. & Dale, N. in Neurobiology of Vertebrate Locomotion (eds Grillner, S. et al.) 279–306 (Macmillan, London, 1986).

    Book  Google Scholar 

  14. Bässler, U. Biol. Cybern. 24, 47–49 (1976).

    Article  Google Scholar 

  15. Skorupski, P. & Sillar, K. T. J. Neurophysiol. 55, 689–695 (1986).

    Article  CAS  Google Scholar 

  16. Andersson, O., Forssberg, H., Grillner, S. & Lindquist, M. Brain Res. 149, 503–507 (1978).

    Article  CAS  Google Scholar 

  17. Forssberg, H. J. Neurophysiol 42, 936–963 (1979).

    Article  CAS  Google Scholar 

  18. Wallén, P. Expl Brain Res. 39, 193–202 (1980).

    Article  Google Scholar 

  19. Grillner, S. in Handbook of Physiology Vol. 3. (ed. Brook, V.) 1179–1236 (American Physiological Society, Bethesda, 1981).

    Google Scholar 

  20. McClellan, A. D. & Grillner, S. Brain Res. 269, 237–250 (1983).

    Article  CAS  Google Scholar 

  21. Crenna, P. & Friggo, C. Expl Neurol. 85, 336–345 (1984).

    Article  CAS  Google Scholar 

  22. Belanger, M. & Patla, A. E. Neurosci. Lett. 19, 175–184 (1984).

    Google Scholar 

  23. Lennard, P. R. & Hermanson, J. W. Trends Neurosci. 8, 483–487 (1985).

    Article  Google Scholar 

  24. Lennard, P. R. J. Neurosci. 5, 1434–1445 (1985).

    Article  CAS  Google Scholar 

  25. Bayev, K. V. & Kostyuk, P. G. Neuroscience 7, 1401–1409 (1982).

    Article  CAS  Google Scholar 

  26. Nieuwkoop, P. D. & Faber, J. Normal Tables of Xenopus laevis (Daudin) (North-Holland, Amsterdam, 1956).

  27. Stewart, W. W. Cell 14, 741–751 (1978).

    Article  CAS  Google Scholar 

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Sillar, K., Roberts, A. A neuronal mechanism for sensory gating during locomotion in a vertebrate. Nature 331, 262–265 (1988). https://doi.org/10.1038/331262a0

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