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:

Multiple innervation of cerebellar Purkinje cells by climbing fibres in staggerer mutant mouse

Abstract

Development of the peripheral nervous system involves an initial overgrowth of synaptic contacts, followed later by the regression of the redundant connections1–4. Similarly, in the central nervous system, the adult-type one-to-one relationship between climbing fibres (CFs) and cerebellar Purkinje cells (PCs) is preceded at early developmental stages by a multiple innervation of PCs by CFs5. The regression of the supernumerary contacts fails to occur when PCs develop in a cellular environment devoid of granule cells6–9, suggesting that it may depend on the formation of synapses between parallel fibres and PCs. However, one cannot preclude the possibility that granule cells intervene in the regressive process by a nonsynaptic action, for instance by emitting a chemical signal at the level of their soma, which could act on the CF-PC synapses. In this respect, the recessive staggerer (sg) mutation10, is of special interest because one of its major phenotypical expressions in homozygous sg/sg animals is the selective and almost complete absence of synapse formation between parallel fibres and Purkinje cells, in spite of the presence of an initially important number of granule cells and of parallel fibres during the synaptogenesis period, that is, until about the end of the 3rd post-natal week. Later on, the relay cells progressively die, probably because of the absence of synaptic contacts with PCs11–13. This is in marked contrast with the other agranular animals studied so far (X-ray irradiated rats and weaver mutant mice6,7,9) where granule cells lack from the very beginning6,9,12. As the staggerer mutation does not prevent the formation of functional synapses between CFs and PCs14, it was important to establish whether PCs can reach the adult-type monoinnervation in the mutant. We show here that each PC is contacted by several CFs in the adult homozygous staggerer mouse, thus supporting the first hypothesis.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Similar content being viewed by others

References

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

    Article  CAS  Google Scholar 

  2. Bagust, J., Lewis, D. M. & Westerman, R. A. J. Physiol., Lond. 229, 241–255 (1973).

    Article  CAS  Google Scholar 

  3. Bennett, M. R. & Pettigrew, A. G. J. Physiol., Lond. 241, 515–545 (1974).

    Article  CAS  Google Scholar 

  4. Lichtman, J. W. J. Physiol., Lond. 273, 155–177 (1977).

    Article  CAS  Google Scholar 

  5. Crepel, F., Mariani, J. & Delhaye-Bouchaud, N. J. Neurobiol. 7, 579–582 (1976).

    Article  CAS  Google Scholar 

  6. Woodward, D. J., Hoffer, B. J. & Altman, J. J. Neurobiology 5, 283–304 (1974).

    Article  CAS  Google Scholar 

  7. Crepel, F. & Mariani, J. J. Neurobiol. 7, 579–582 (1976).

    Article  CAS  Google Scholar 

  8. Mariani, J., Crepel, F., Mikoshiba, K., Changeux, J. P. & Sotelo, C. Phil. Trans. R. Soc. 281, 1–28 (1977).

    Article  CAS  Google Scholar 

  9. Crepel, F. & Delhaye-Bouchaud, N. J. Physiol., Lond. 290, 97–112 (1979).

    Article  CAS  Google Scholar 

  10. Sidman, R. L., Lane, P. W. & Dickie, M. M. Science 137, 610–612 (1962).

    Article  ADS  CAS  Google Scholar 

  11. Landis, D. J. Cell. Biol. 51, 159 a (1971).

    Google Scholar 

  12. Sidman, R. L. in Cell Interactions (ed. Silvestri, L. G.) 1–13 (North-Holland, Amsterdam, 1972).

    Google Scholar 

  13. Sotelo, C. & Changeux, J. P. Brain Res. 67, 519–526 (1974).

    Article  CAS  Google Scholar 

  14. Crepel, F. & Mariani, J. Brain Res. 98, 135–147 (1975).

    Article  CAS  Google Scholar 

  15. Guastavino, J. M. C.r. hebd. Séanc. Acad. Sci., Paris 286, 137–139 (1978).

    CAS  Google Scholar 

  16. Eccles, J. C., Llinas, R. & Sasaki, K. J. Physiol., Lond. 182, 268–296 (1966).

    Article  CAS  Google Scholar 

  17. Llinas, R. & Volkind, R. A. Expl Brain Res. 18, 69–87 (1973).

    Article  CAS  Google Scholar 

  18. Eccles, J. C. The Physiology of Synapses (Springer, New York, 1964).

    Book  Google Scholar 

  19. Llinas, R. & Nicholson, C. J. Neurophysiol. 39, 311–323 (1976).

    Article  CAS  Google Scholar 

  20. Woodward, D. J., Hoffer, B. J., Siggins, G. R. & Bloom, F. E. Brain Res. 34, 73–97 (1971).

    Article  CAS  Google Scholar 

  21. Crepel, F. Brain Res. 35, 272–276 (1971).

    Article  CAS  Google Scholar 

  22. Hirano, M. D. & Dembitzer, H. J. Neuropath. exp. Neurol. 34, 1–11 (1975).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Crepel, F., Delhaye-Bouchaud, N., Guastavino, J. et al. Multiple innervation of cerebellar Purkinje cells by climbing fibres in staggerer mutant mouse. Nature 283, 483–484 (1980). https://doi.org/10.1038/283483a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/283483a0

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