Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Fibre type composition of single motor units during synapse elimination in neonatal rat soleus muscle

Abstract

Skeletal motor neurones innervate the specialized ‘types’ of fibres comprising most mammalian muscles in a characteristic fashion: each motor neurone forms a ‘motor unit’ by innervating a set of fibres all of the same type1–4. Because the type expression of adult muscle fibres is plastic and apparently controlled by their innervation, each motor neurone is thought to impose a common type differentiation on all the fibres in its motor unit4–6. However, the situation in developing muscles cannot be this simple. Muscle fibres in neonates receive synaptic input from several motor neurones and achieve the adult, single innervation only after a period of ‘synapse elimination’7,8. Despite this polyneuronal innervation, differentiated fibre types are present in neonatal muscles9–14. This means either that the motor neurones polyne-uronally innervate fibres in a random fashion and type expression is not determined by innervation or that the polyneuronal innervation is ordered in such a way that each fibre could receive unambiguous instructions for type differentiation. We have investigated these possibilities here by determining the fibre type composition of motor units in neonatal rat soleus muscle. We find that even during the time of poly neuronal innervation each motor neurone confines its innervation to largely one of two fibre types present in the muscle. Therefore, some mechanism during early development segregates the synapses of two groups of soleus motor neurones onto two separate populations of soleus muscle fibres.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Landmesser, L. T. A. Rev. Neurosci. 3, 279–302 (1980).

    Article  CAS  Google Scholar 

  2. Buchthal, F. & Schmalbruch, H. Physiol. Rev. 60, 90–142 (1980).

    Article  CAS  Google Scholar 

  3. Burke, R. E. & Edgerton, V. R. in Exercise and Sport Sciences Reviews (eds Wilmore, J. H. & Keogh, J. F.) 31–81 (Academic, New York, 1975).

    Google Scholar 

  4. Vrbova, G., Gordon, T. & Jones, R. Nerve-Muscle Interaction (Chapman & Hill, London, 1978).

    Book  Google Scholar 

  5. Pette, D. (ed.) Plasticity of Muscle (Walter de Gruyter, Berlin, 1980).

  6. Jolesz, F. & Sreter, F. A. A. Rev. Physiol. 43, 531 –552 (1981).

    Article  CAS  Google Scholar 

  7. Redfern, P. A. J. Physiol, Lond. 209, 701–709 (1970).

    Article  CAS  Google Scholar 

  8. Brown, M. C., Jansen, J. K. S. & Van Essen, D. J. Physiol., Lond. 261, 387–422 (1976).

    Article  CAS  Google Scholar 

  9. Riley, D. A. Expl Neurol. 56, 400–409 (1977).

    Article  CAS  Google Scholar 

  10. Brooke, M. H., Williamson, E. & Kaiser, K. K. Archs Neurol. 25, 360–366 (1971).

    Article  CAS  Google Scholar 

  11. Rubinstein, N. A. & Kelly, A. M. Devl Biol. 62, 473–485 (1978).

    Article  CAS  Google Scholar 

  12. Rubinstein, N. A. & Kelly, A. M. J. Cell Biol. 90, 128–144 (1981).

    Article  CAS  Google Scholar 

  13. Butler-Browne, G. S. & Whalen, R. G. Devl Biol. 102, 324–334 (1984).

    Article  CAS  Google Scholar 

  14. Rowlerson, A. J. Physiol., Lond. 301, 19P (1980).

  15. Whalen, R. G. et al. Nature 292, 805–809 (1981).

    Article  ADS  CAS  Google Scholar 

  16. Gauthier, G. F., Lowey, S., Benfield, P. A. & Hobbs, A. W. J. Cell Biol. 92,471–484 (1982).

    Article  CAS  Google Scholar 

  17. Fitzsimons, R. B. & Hoh, J. F. Y. J. Neurol. Sci. 52, 367–384 (1981).

    Article  CAS  Google Scholar 

  18. Edström, L. & Kugelberg, E. J. Neurol. Neurosurg. Psychiat. 31, 424–433 (1968).

    Article  Google Scholar 

  19. Kugelberg, E. J. neurol. Sci. 27, 269–289 (1976).

    Article  CAS  Google Scholar 

  20. Burke, R. E., Levine, D. N., Tsairis, P. & Zajac, F. E. J. Physiol., Lond. 234,723–748 (1973).

    Article  CAS  Google Scholar 

  21. Pearse, A. G. E. Histochemistry, Theoretical and Applied (Little, Brown, Boston, 1968).

    Google Scholar 

  22. Thompson, W. J. J. Physiol., Lond. 335, 343–352 (1983).

    Article  CAS  Google Scholar 

  23. Thompson, W. & Jansen, J. K. S. Neuroscience 2, 523–535 (1977).

    Article  CAS  Google Scholar 

  24. Betz, W. J., Caldwell, J. H. & Ribchester, R. R. J. Physiol., Lond. 297, 463–478 (1979).

    Article  CAS  Google Scholar 

  25. McLennan, I. S. Devl Biol. 97, 229–238 (1983).

    Article  CAS  Google Scholar 

  26. Elizalde, A., Huerta, M. & Stefani, E. J. Physiol., Lond. 340, 513–524 (1983).

    Article  CAS  Google Scholar 

  27. Gambke, B., Lyons, G. E., Haselgrove, J., Kelly, A. M. & Rubinstein, N. A. FEBS Lett. 156, 335–339 (1983).

    Article  CAS  Google Scholar 

  28. Butler, J., Cosmos, E. & Brierley, J. J. expl. Zool. 224, 65–80 (1982).

    Article  CAS  Google Scholar 

  29. Vogel, M. W. & Landmesser, L. T. Soc. Neurosci. Abstr. 9, 62 (1983).

    Google Scholar 

  30. Kugelberg, E., Edström, L. & Abbruzzese, M. J. Neurol. Neurosurg. Psychiat. 33, 319–329 (1970).

    Article  CAS  Google Scholar 

  31. Gauthier, G. F. & Hobbs, A. W. Expl Neurol. 76, 331–346 (1982).

    Article  CAS  Google Scholar 

  32. Gordon, H. thesis, Calif. Inst. Tech. (1983).

  33. Thompson, W. J., Sutton, L. & Riley, D. A. Soc. Neurosci. Abstr. 9, 321(1983).

    Google Scholar 

  34. Guth, L. & Samaha, F. J. Expl Neurol. 28, 365–367 (1970).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Thompson, W., Sutton, L. & Riley, D. Fibre type composition of single motor units during synapse elimination in neonatal rat soleus muscle. Nature 309, 709–711 (1984). https://doi.org/10.1038/309709a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/309709a0

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing