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Two identified afferent neurones entrain a central locomotor rhythm generator

Abstract

Sensory feedback can modulate the intensity and timing of the central rhythms underlying locomotion and adjust them to compensate for natural or experimental perturbations1–4. However, because of the complexity of the neural systems involved, the role of specific sense organs and the function of individual afferent neurones are poorly understood. The thoracic-coxal muscle receptor organ (TCMRO), a proprioceptor of the crayfish walking leg, has only two afferent neurones, the non-spiking S and T fibres. Their receptor potentials encode, respectively, the magnitude and velocity of receptor muscle stretch, which occurs during limb remotion (retraction). Rhythmically stretching the TCMRO entrains a central locomotor rhythm, produced by the thoracic ganglia, in which remotor and promotor motoneurones of the leg discharge in alternation. Intracellular stimulation of the S and T fibres can trigger promotor and remotor bursts, respectively. Here we propose a mechanism for proprioceptive entrainment in terms of the opposite feedback effects of these two afferents. The possible role of these effects in the feedback control of locomotion is also discussed.

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References

  1. Delcomyn, F. Science 210, 492–498 (1980).

    Article  ADS  CAS  Google Scholar 

  2. Roberts, A. & Roberts, B. L. (eds) Symp. Soc. exp. Biol. 37 (1983).

  3. Andersson, O. & Grillner, S. Ada physiol. scand. 118, 229–239 (1983).

    Article  CAS  Google Scholar 

  4. Pearson, K. G., Reye, D. N. & Robertson, R. M. J. Neurophysiol. 49, 1168–1181 (1983).

    Article  CAS  Google Scholar 

  5. Skorupski, P., Sillar, K.T. & Bush, B. M. H. Soc. Neurosci. Abstr. 10,627 (1984).

  6. Skorupski, P. thesis, Univ. Bristol (1985).

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

    Article  CAS  Google Scholar 

  8. Alexandrowicz, J. S. & Whitear, M. J. mar. Biol. Ass., U.K. 36, 603–628 (1957).

    Article  Google Scholar 

  9. Bush, B. M. H. & Roberts, A. J. exp. Biol. 55, 813–832 (1971).

    CAS  PubMed  Google Scholar 

  10. Bush, B. M. H., exp. Biol. Semin. Ser. 6, 147–176 (1981).

    Google Scholar 

  11. Ripley, S. H., Bush, B. M. H. & Roberts, A. Nature 218, 1170–1171 (1968).

    Article  ADS  CAS  Google Scholar 

  12. Bush, B. M. H. & Roberts, A. Nature 218, 1171–1173 (1968).

    Article  ADS  CAS  Google Scholar 

  13. Cannone, A. J. & Bush, B. M. H. J. exp. Biol. 86, 275–303 (1980).

    Google Scholar 

  14. Blight, A. R. & Llinas, R. Phil Trans. R. Soc. B290, 219–276 (1980).

    Article  CAS  Google Scholar 

  15. DiCaprio, R. A. & Clarac, F. J. exp. Biol. 90, 197–203 (1980).

    Google Scholar 

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

    Article  CAS  Google Scholar 

  17. Andersson, O., Grillner, S., Lindquist, M. & Zomlefer, M. Brain Res. 150, 625–630 (1978).

    Article  CAS  Google Scholar 

  18. Bush, B. M. H. & Cannone, A. J. in Feedback and Motor Control in Invertebrates and Vertebrates (eds Barnes, W. J. P. & Gladden, M.) 145–166 (Croom Helm, London, 1985).

    Book  Google Scholar 

  19. Forssberg, H. in Neural Control of Locomotion (eds Herman, R. M., Grillner, S., Stein, P. S. G. & Stuart, D. G.) 647–674 (Plenum, New York, 1976).

    Book  Google Scholar 

  20. Rossignol, S. & Drew, T. in Feedback and Motor Control in Vertebrates and Invertebrates (eds Barnes, W. J. P. & Gladden, M. H.) 355–378 (Croom Helm, London, 1985).

    Book  Google Scholar 

  21. Schomburg, E. D. & Behrends, H. B. Neurosci. Lett. 8, 277–282 (1978).

    Article  CAS  Google Scholar 

  22. Clarac, F. & Chasserat, C. J. exp. Biol. 107, 189–217 (1983).

    Google Scholar 

  23. Bässler, U. Neural Basis of Elementary Behavior in Stick Insects (Springer, Berlin, 1983).

    Book  Google Scholar 

  24. Clarac, F. Trends Neurosci. 7, 293–298 (1984).

    Article  Google Scholar 

  25. Pearson, K. G. & Duysens, J. in Neural Control of Locomotion (eds Herman, R. M., Grillner, S., Stein, P. S. G. & Stuart, D. G.) 519–537 (Plenum, New York, 1976).

    Book  Google Scholar 

  26. Andersson, O., Forssberg, H., Grillner, S. & Wallen, P. Can. J. Physiol. Pharmac. 59, 713–726 (1981).

    Article  CAS  Google Scholar 

  27. Bässler, U. J. comp. Physiol. 158, 351–362 (1986).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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Sillar, K., Skorupski, P., Elson, R. et al. Two identified afferent neurones entrain a central locomotor rhythm generator. Nature 323, 440–443 (1986). https://doi.org/10.1038/323440a0

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