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:

Heightened synaptic plasticity of hippocampal CA1 neurons during a Cholinergically induced rhythmic state

Nature volume 364, pages 723–725 (1993)Cite this article

Abstract

BRAIN cholinergic neurons are critical for memory function1,2 and their loss may contribute to memory impairment in Alzheimer's disease3. One role of cholinergic neurons is to elicit an oscillatory activity called theta rhythm4 in the hippocampus, a brain region involved in memory processing5. Theta rhythm occurs during periods of learning6,7, but its effect on the synaptic plasticity that underlies learning remains unclear. We have studied synaptic plasticity in hippocampal slices during theta-frequency oscillations induced by a cholinergic agonist8–10. Here we report that during these oscillations, synapses are in a state of heightened plasticity and can be modified by what would otherwise be ineffective stimulation. This heightened plasticity is sensitive to the timing of incoming stimuli with respect to the oscillatory activity. The results suggest that cholinergic systems may affect memory formation through the induction of an oscillatory state in which the requirements for synaptic plasticity are dramatically altered.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Similar content being viewed by others

References

  1. Fibiger, H. C. Trends Neurosci. 14, 220–223 (1991).

    Article  CAS  Google Scholar 

  2. Aigner, T. G. & Mishkin, M. Behavl neural Biol. 45, 81–87 (1986).

    Article  CAS  Google Scholar 

  3. Coyle, A. E., Price, D. L. & DeLong, M. R. Science 219, 1184–1190 (1983).

    Article  ADS  CAS  Google Scholar 

  4. Bland, B. H. Prog. Neurobiol. 26, 1–54 (1986).

    Article  CAS  Google Scholar 

  5. Squire, L. R. Memory and Brain (Oxford Univ. Press, 1987).

    Google Scholar 

  6. Winson, J. Science 201, 160–163 (1978).

    Article  ADS  CAS  Google Scholar 

  7. Otto, T., Eichenbaum, H., Wiener, S. I. & Wible, S. G. Hippocampus 1, 181–192 (1991).

    Article  CAS  Google Scholar 

  8. Konopacki, J., Maclver, M. B., Bland, B. H. & Roth, S. H. Brain Res. 405, 196–198 (1987).

    Article  CAS  Google Scholar 

  9. Konopacki, J., Bland, B. H. & Roth, S. H. Brain Res. 455, 110–114 (1988).

    Article  CAS  Google Scholar 

  10. MacVicar, B. A. & Tse, F. W. Y. J. Physiol., Lond. 417, 197–212 (1989).

    Article  CAS  Google Scholar 

  11. Dutar, P. & Nicoll, R. A. J. Neurosci. 8, 4214–4224 (1988).

    Article  CAS  Google Scholar 

  12. Nicoll, R. A., Malenka, R. C. & Kauer, J. A. Physiol. Rev. 70, 513–565 (1990).

    Article  CAS  Google Scholar 

  13. Colom, L. V., Nassif-Caudarella, S., Dickson, C. T., Smythe, J. W. & Bland, B. H. Hippocampus 1, 381–390 (1991).

    Article  CAS  Google Scholar 

  14. Eichenbaum, H., Kuperstein, M., Fagan, A. & Nagode, J. J. Neurosci. 7, 716–732 (1987).

    Article  CAS  Google Scholar 

  15. Traub, R. D., Miles, R. & Buzsa´ki G. J. Physiol., Lond. 451, 653–672 (1992).

    Article  CAS  Google Scholar 

  16. Llina´s, R. R. Science 242, 1654–1664 (1988).

    Article  ADS  Google Scholar 

  17. Gray, C. M., Konig, P., Engel, A. K. & Singer, W. Nature 338, 334–337 (1989).

    Article  ADS  CAS  Google Scholar 

  18. Pavlides, C., Greenstein, Y. J., Grudman, M. & Winson, J. Brain Res. 439, 383–387 (1988).

    Article  CAS  Google Scholar 

  19. Larson, J., Wong, D. & Lynch, G. Brain Res. 368, 347–350 (1986).

    Article  CAS  Google Scholar 

  20. Stanton, P. K. & Sejnowski, T. J. Nature 339, 215–218 (1989).

    Article  ADS  CAS  Google Scholar 

  21. Rose, G. M. & Dunwiddie, T. V. Neurosci. Lett. 69, 244–248 (1986).

    Article  CAS  Google Scholar 

  22. Christie, B. R. & Abraham, W. C. Neuron 9, 79–84 (1992).

    Article  CAS  Google Scholar 

  23. Halliwell, J. V. Prog. Brain Res. 84, 255–272 (1990).

    Article  CAS  Google Scholar 

  24. Markram, H. & Segal, M. J. Physiol., Lond. 427, 381–393 (1990).

    Article  CAS  Google Scholar 

  25. Markram, H. & Segal, M. J. Physiol., Lond. 447, 513–533 (1992).

    Article  CAS  Google Scholar 

  26. Burgard, E. C. & Sarvey, J. M. Neurosci. Lett. 116, 34–39 (1990).

    Article  CAS  Google Scholar 

  27. Schulz, P. E. & Johnston, D. Soc. Neurosci. Abstr. 16, 655 (1990).

    Google Scholar 

  28. Brocher, S., Artola, A. & Singer, W. Brain Res. 573, 27–36 (1992).

    Article  CAS  Google Scholar 

  29. Alger, B. E. et al. in Brain Slices (ed. Dingledine, R.) 381–437 (Plenum, New York, 1984).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology and Center for Complex Systems, Brandeis University, Waltham, Massachusetts, 02254–9110, USA

    Patriclo T. Huerta & John E. Lisman

Authors
  1. Patriclo T. Huerta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John E. Lisman
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huerta, P., Lisman, J. Heightened synaptic plasticity of hippocampal CA1 neurons during a Cholinergically induced rhythmic state. Nature 364, 723–725 (1993). https://doi.org/10.1038/364723a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/364723a0

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

Advanced 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