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:

Associative, bidirectional modifications at the hippocampal mossy fibre–CA3 synapse

Abstract

LONG-TERM potentiation (LTP) and long-term depression (LTD) are activity-dependent changes in synaptic strength that may serve as the cellular mechanisms of information storage in the vertebrate brain1–4. The mossy fibre–CA3 synapse displays NMDA (N-methyl-D-aspartate) receptor-independent forms of LTP5–8 and LTD9–11 that were thought to be non-associative9–11. Here we report that the mossy fibre–CA3 synapse displays each of the known types of LTD in vivo, including associative, heterosynaptic and homosynaptic LTD. These types of LTD are induced when only two of the three conditions necessary for mossy fibre LTP induction are provided. Because some of these conditions can be provided by convergent CA3 afferents, each type of LTD can be induced in an associative manner, which suggests that LTD is involved in associative information storage. Similar to the induction of NMDA receptor-dependent LTD and LTP at other cortical synapses, mossy fibre LTD occurs when synaptic conditions are insufficient to induce LTP, and both LTP and LTD induction are influenced by previous synaptic activity, consistent with the view that common principles govern activity-dependent plasticity at cortical synapses2,12,22.

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. Bliss, T. V. P. & Collingridge, G. L. Nature 361, 31–39 (1993).

    Article  ADS  CAS  Google Scholar 

  2. Artola, A. & Singer, W. Trends Neurosci. 16, 480–487 (1993).

    Article  CAS  Google Scholar 

  3. Linden, D. Neuron 12, 457–472 (1994).

    Article  CAS  Google Scholar 

  4. Martinez, J. L. Jr & Derrick, B. E. A. Rev. Psychol. 47, 173–203 (1995).

    Article  Google Scholar 

  5. Harris, E. W. & Cotman, C. W. Neurosci. Lett. 70, 132–137 (1986).

    Article  CAS  Google Scholar 

  6. Zalutsky, R. A. & Nicoll, R. A. Science 248, 1619–1624 (1990).

    Article  ADS  CAS  Google Scholar 

  7. Derrick, B. E. & Martinez, J. L. Jr J. Neurosci. 14, 4359–4367 (1994).

    Article  CAS  Google Scholar 

  8. Williams, S. & Johnston, D. Neuron 3, 583–588 (1989).

    Article  CAS  Google Scholar 

  9. Weisskopf, M., Zalutsky, R. A. & Nicoll, R. A. Nature 362, 423–427 (1993).

    Article  ADS  CAS  Google Scholar 

  10. Chatterji, S., Stanton, P. & Sejnowski, T. J. Brain Res. 495, 145–150 (1989).

    Article  Google Scholar 

  11. Bradler, J. E. & Barrionuevo, G. Neuroscience 35, 265–271 (1990).

    Article  CAS  Google Scholar 

  12. Bienenstock, E. L., Cooper, L. B. & Munro, P. W. J. Neurosci. 2, 32–48 (1982).

    Article  CAS  Google Scholar 

  13. Derrick, B. E. & Martinez, J. L. Jr Proc. natn. Acad. Sci. U.S.A. 91, 10290–10294 (1994).

    Article  ADS  CAS  Google Scholar 

  14. Wagner, J. J., Caudle, R. M., Neumaier, J. F. & Chavkin, C. Neuroscience 37, 45–53 (1990).

    Article  CAS  Google Scholar 

  15. Caudle, R. M., Wagner, J. J. & Chavkin, C. J. Pharmac. exp. Ther. 258, 18–26 (1991).

    CAS  Google Scholar 

  16. Drake, C. T. et al. J. Neurosci. 14, 3736–3750 (1994).

    Article  CAS  Google Scholar 

  17. Montague, P. R. & Sejnowski, T. J. Learn. Memory 1, 1–33 (1994).

    CAS  Google Scholar 

  18. White, G., Levy, W. B. & Steward, O. J. Neurosci. 64, 1186–1198 (1990).

    CAS  Google Scholar 

  19. Dudek, S. M. & Bear, M. F. Proc. natn. Acad. Sci. U.S.A. 89, 4363–4367 (1992).

    Article  ADS  CAS  Google Scholar 

  20. Derrick, B. E., Rodriguez, S. B., Lieberman, D. N. & Martinez, J. L. Jr J. Pharmac. exp. Ther. 263, 725–733 (1992).

    CAS  Google Scholar 

  21. Mulkey, R. M. & Malenka, R. C. Neuron 9, 967–975 (1992).

    Article  CAS  Google Scholar 

  22. Intrator, N., Bear, M. F., Cooper, L. N. & Paradiso, M. A. In Synaptic Plasticity: Molecular, Cellular, and Functional Aspects (eds Baudry, M., Thompson, R. F. & Davis, J. L.) 147–168 (MIT Press, Cambridge, MA, 1993).

    Google Scholar 

  23. Mayford, M., Wang, J., Kandel, E. R. & O'Dell, T. J. Cell 81, 891–904 (1995).

    Article  CAS  Google Scholar 

  24. Huang, Y.-Y., Colino, A., Selig, D. K. & Malenka, R. C. Science 255, 730–733 (1992).

    Article  ADS  CAS  Google Scholar 

  25. Sejnowski, T. J. J. math. Biol. 4, 303–321 (1977).

    Article  CAS  Google Scholar 

  26. Willshaw, D. & Dayan, P. Neural Comp. 2, 85–93 (1990).

    Article  Google Scholar 

  27. Reiter, H. O. & Stryker, M. P. Proc. natn. Acad. Sci. U.S.A. 85, 3623–27 (1988).

    Article  ADS  CAS  Google Scholar 

  28. Law, C. C. & Cooper, L. N. Proc. natn. Acad. Sci. U.S.A. 91, 7797–7801 (1994).

    Article  ADS  CAS  Google Scholar 

  29. Kirkwood, A., Dudek, S. M., Gold, J. T., Aizenman, C. D. & Bear, M. F. Science 260, 1518–1521 (1993).

    Article  ADS  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Derrick, B., Martinez, J. Associative, bidirectional modifications at the hippocampal mossy fibre–CA3 synapse. Nature 381, 429–434 (1996). https://doi.org/10.1038/381429a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/381429a0

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