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:

Temporally distinct pre- and post-synaptic mechanisms maintain long-term potentiation

Abstract

LONG-TERM potentiation (LTP) in the hippocampus is widely studied as the mechanisms involved in its induction and maintenance are believed to underlie fundamental properties of learning and memory in vertebrates1. Most synapses that exhibit LTP use an excitatory amino-acid neurotransmitter that acts on two types of receptor, the N-methyl-D-aspartate (NMDA) and quisqualate receptors2. The quisqualate receptor mediates the fast synaptic response evoked by low-frequency stimulation3,4, whereas the NMDA receptor system is activated transiently by tetanic stimulation, leading to the induction of LTP3,5–7. The events responsible for maintaining LTP once it is established are not known. We now demonstrate that the sensitivity of CA1 neurons in hippocampal slices to ionophoretically-applied quisqualate receptor ligands slowly increases following the induction of LTP. This provides direct evidence for a functional post-synaptic change and suggests that pre-synaptic mechanisms also contribute, but in a temporally distinct manner, to the maintenance of LTP.

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. & Lynch, M. A. Neurol. Neurobiol. 35, 3–72 (1988).

    Google Scholar 

  2. Watkins, J. C. & Evans, R. H. A. Rev. Pharmac. Tox. 21, 165–204 (1981).

    Article  CAS  Google Scholar 

  3. Collingridge, G. L., Kehl, S. J. & McLennan, H. J. Physiol., Lond. 334, 33–46 (1983).

    Article  CAS  Google Scholar 

  4. Blake, J. F., Brown, M. W. & Collingridge, G. L. Neurosci. Lett. 89, 182–186 (1988).

    Article  CAS  Google Scholar 

  5. Harris, E. W., Ganong, A. H. & Cotman, C. W. Brain Res. 323, 132–137 (1984).

    Article  CAS  Google Scholar 

  6. Wigström, H. & Gustafsson, B. Neurosci, Lett. 44, 327–332 (1984).

    Article  Google Scholar 

  7. Herron, C. E., Lester, R. A. J., Coan, E. J. & Collingridge, G. L. Nature 322, 265–268 (1986).

    Article  ADS  CAS  Google Scholar 

  8. Honoré, T. et al. Science 241, 701–703 (1988).

    Article  ADS  Google Scholar 

  9. Andreasen, M., Lambert, J. D. C. & Skovgaard Jensen, M. Neurosci. Lett. 93, 61–66 (1988).

    Article  CAS  Google Scholar 

  10. Neuman, R. S., Ben-Ari, Y., Gho, M. & Cherubini, E. Neurosci. Lett. 92, 64–68 (1988).

    Article  CAS  Google Scholar 

  11. Lambert, J. D. C., Flatman, J. A. & Jahnsen, H. J. Neurosci. Meth. 3, 311–315 (1981).

    Article  CAS  Google Scholar 

  12. Bliss, T. V. P., Douglas, R. M., Errington, M. L. & Lynch, M. A. J. Physiol., Lond. 377, 391–408 (1986).

    Article  CAS  Google Scholar 

  13. Skrede, K. & Malthe-Sorenssen, D. Brain Res. 208, 436–441 (1981).

    Article  CAS  Google Scholar 

  14. Sastry, B. R. Life Sci. 30, 2003–2008 (1982).

    Article  CAS  Google Scholar 

  15. Lynch, G. & Baudry, M. Science 224, 1057–1063 (1984).

    Article  ADS  CAS  Google Scholar 

  16. Kauer, J. A., Malenka, R. C. & Nicoll, R. A. Neuron 1, 911–917 (1988).

    Article  CAS  Google Scholar 

  17. Muller, D., Joly, M. & Lynch, G. Science 242, 1694–1697 (1988).

    Article  ADS  CAS  Google Scholar 

  18. Lynch, G., Gribkoff, V. & Deadwyler, S. A. Nature 263, 151–153 (1976).

    Article  ADS  CAS  Google Scholar 

  19. Mohan, P. M. & Sastry, B. R. Eur. J. Pharmac. 114, 335–341 (1985).

    Article  CAS  Google Scholar 

  20. Taube, J. S. & Schwartzkroin, P. A. J. Neuroscience 8, 1632–1644 (1988).

    Article  CAS  Google Scholar 

  21. Davies, S. N., Fletcher, E. J. & Lodge, D. J. Physiol., Lond. 406, 13P (1988).

    Google Scholar 

  22. Lovinger, D. M., Wong, K. L., Murakami, K. & Routtenberg, A. Brain Res. 436, 177–183 (1987).

    Article  CAS  Google Scholar 

  23. Reymann, K. G., Frey, U., Jork, R. & Matthies, H. Brain Res. 440, 305–314 (1988).

    Article  CAS  Google Scholar 

  24. Malinow, R., Madison, D. V. & Tsien, R. W. Nature 335, 821–824 (1988).

    Article  ADS  Google Scholar 

  25. Hu, G.-Y. et al. Nature 328, 426–429 (1987).

    Article  ADS  CAS  Google Scholar 

  26. Dumuis, A., Sebben, M., Haynes, L., Pin, J.-P. & Bockaert, J. Nature 336, 68–70 (1988).

    Article  ADS  CAS  Google Scholar 

  27. Piomelli, D. et al. Nature 328, 38–43 (1987).

    Article  ADS  CAS  Google Scholar 

  28. Williams, J. H. & Bliss, T. V. P. Neurosci. Lett. 88, 81–85 (1988).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Davies, S., Lester, R., Reymann, K. et al. Temporally distinct pre- and post-synaptic mechanisms maintain long-term potentiation. Nature 338, 500–503 (1989). https://doi.org/10.1038/338500a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/338500a0

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