Skip to main content
Log in

A switch between two modes of synaptic transmission mediated by presynaptic inhibition

  • Letter
  • Published:

From Nature

View current issue Submit your manuscript

Abstract

PRESYNAPTIC inhibition reduces chemical synaptic transmission in the central nervous system between pairs of neurons1–4, but its role(s) in shaping the multisynaptic interactions underlying neural network activity are not well studied. We therefore used the crustacean stomatogastric nervous system to study how presynaptic inhibition of the identified projection neuron, modulatory commissural neuron 1 (MGN1), influences the MCN1 synaptic effects on the gastric mill neural network. Tonic MCN1 discharge excites gastric mill network neurons and activates the gastric mill rhythm5,6. One network neuron, the lateral gastric (LG) neuron, presynaptically inhibits MCN1 and is electrically coupled to its terminals5,6. We show here that this presynaptic inhibition selectively reduces or eliminates transmitter-mediated excitation from MCN1 without reducing its electrically mediated excitatory effects, thereby switching the network neurons excited by MCN1. By switching the type of synaptic output from MCN1 and, hence, the activated network neurons, this presynaptic inhibition is pivotal to motor pattern generation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Clarac, F., El Manira, A. & Cattaert, D. Curr. Opin. Neurobiol. 2, 764–769 (1992).

    Article  CAS  Google Scholar 

  2. Watson, A. H. D. Comp. Biochem. Physiol. A 103, 227–239 (1992).

    Article  CAS  Google Scholar 

  3. Rudomin, P., Quevedo, J. & Eguibar, J. R. Curr. Opin. Neurobiol. 3, 997–1004 (1993).

    Article  CAS  Google Scholar 

  4. Nusbaum, M. P. Curr. Opin. Neurobiol. 4, 909–914 (1994).

    Article  CAS  Google Scholar 

  5. Nusbaum, M. P., Weimann, J. M., Golowasch, J. & Marder, E. J. Neurosci. 12, 2706–2714 (1992).

    Article  CAS  Google Scholar 

  6. Coleman, M. J. & Nusbaum, M. P. J. Neurosci. 14, 6544–6552 (1994).

    Article  CAS  Google Scholar 

  7. Selverston, A. I. & Moulins, M. The Crustacean Stomatogastric System (Springer, Berlin, 1987).

    Book  Google Scholar 

  8. Harris-Warrick, R. M., Marder, E., Selverston, A. I. & Moulins, M. Dynamic Biological Networks: The Stomatogastric Nervous System (MIT Press, Massachusetts, 1992).

    Google Scholar 

  9. Weimann, J. M. & Marder, E. Curr. Biol. 4, 896–902 (1994).

    Article  CAS  Google Scholar 

  10. Weimann, J. M., Meyrand, P. & Marder, E. J. Neurophysiol. 65, 111–122 (1991).

    Article  CAS  Google Scholar 

  11. Harris-Warrick, R. M., Nagy, F. & Nusbaum, M. P. in Dynamic Biological Networks: The Stomatogastric Nervous System (eds Harris-Warrick, R. M., Marder, E., Selverston, A. I. & Moulins, M.) 87–137 (MIT Press, Massachusetts, 1992).

    Google Scholar 

  12. Coleman, M. J., Nusbaum, M. P., Cournil, I. & Claiborne, B. J. J. comp. Neurol. 325, 581–594 (1992).

    Article  CAS  Google Scholar 

  13. Norris, B. J., Coleman, M. J. & Nusbaum, M. P. J. Neurophysiol. 72, 1451–1463 (1994).

    Article  CAS  Google Scholar 

  14. Segev, I. J. Neurophysiol. 63, 987–998 (1990).

    Article  CAS  Google Scholar 

  15. Toth, P. T., Bindokas, V. P., Bleakman, D., Colmers, W. F. & Miller, R. J. Nature 364, 635–639 (1993).

    Article  ADS  CAS  Google Scholar 

  16. Cattaert, D., El Manira, A. & Clarac, F. J. Neurophysiol. 67, 610–624 (1992).

    Article  CAS  Google Scholar 

  17. Small, S. A., Cohen, T. E., Kandel, E. R. & Hawkins, R. D. J. Neurosci. 12, 1616–1627 (1992).

    Article  CAS  Google Scholar 

  18. Haydon, P. G., Man-Son-Hing, H., Doyle, R. T. & Zoran, M. J. Neurosci. 11, 3851–3860 (1991).

    Article  CAS  Google Scholar 

  19. Bennett, M. V. L. & Verselis, V. K. Semin. Cell Biol. 3, 29–47 (1992).

    Article  CAS  Google Scholar 

  20. Coleman, M. J. thesis, Univ. Alabama at Birmingham (1995).

  21. Harris-Warrick, R. M. & Marder, E. A. Rev. Neurosci. 14, 39–58 (1991).

    Article  CAS  Google Scholar 

  22. Marder, E. & Weimann, J. M. in Neurobiology of Motor Programme Selection: New Approaches to Mechanisms of Behavioral Choice (eds Kien, J., McCrohan, C. & Winlow, W.) 3–19 (Manchester Univ. Press, Manchester, 1992).

    Book  Google Scholar 

  23. Rossignol, S. & Dubuc, R. Curr. Opin. Neurobiol. 4, 894–902 (1994).

    Article  CAS  Google Scholar 

  24. Grillner, S. et al. Trends Neurosci. 18, 270–279 (1995).

    Article  CAS  Google Scholar 

  25. Spruston, N., Schiller, Y., Stuart, G. & Sakmann, B. Science 268, 297–300 (1995).

    Article  ADS  CAS  Google Scholar 

  26. Magee, J. C. & Johnston, D. Science 268, 301–304 (1995).

    Article  ADS  CAS  Google Scholar 

  27. Alford, S., Christenson, J. & Grillner, S. Eur. J. Neurosci. 3, 107–117 (1991).

    Article  Google Scholar 

  28. Sillar, K. T. & Simmers, A. J. J. Neurosci. 14, 2636–2647 (1994).

    Article  CAS  Google Scholar 

  29. Katz, P. S. & Frost, W. N. J. Neurosci. 15, 6035–6045 (1995).

    Article  CAS  Google Scholar 

  30. Dixon, D. B., Takahashi, K.-I. & Copenhagen, D. R. Neuron 11, 267–277 (1993).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Coleman, M., Meyrand, P. & Nusbaum, M. A switch between two modes of synaptic transmission mediated by presynaptic inhibition. Nature 378, 502–505 (1995). https://doi.org/10.1038/378502a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/378502a0

  • Springer Nature Limited

This article is cited by

Navigation