Long-term potentiation is associated with increases in quantal content and quantal amplitude (original) (raw)

Nature volume 357, pages 240–244 (1992)Cite this article

Abstract

LONG-TERM potentiation (LTP) of synaptic transmission in CA1 neurons of the hippocampus, elicited by the conjunction of presynaptic firing and postsynaptic depolarization, is an important model of plasticity, which may underlie memory storage1–3. Although induction of LTP takes place in the postsynaptic cell4–7, it is not clear whether it is expressed through an enhancement of transmitter release8–12 or through an increased postsynaptic response to the same amount of transmitter13–6. Analysis of the trial-to-trial amplitude fluctuations of synaptic signals, that is quantal analysis, gives an important insight into the probabilistic mechanisms of transmission, although attempts to apply it to the mode of expression of LTP have so far yielded inconsistent results9–12,15, at least in part because they have relied on models of transmitter release that have not been confirmed experimentally17–19. Here we report clear evidence for quanta! fluctuation in a subset of cells. Induction of LTP in these cells causes abrupt increases in either quantal content or quantal amplitude, or both. This shows that two different mechanisms can underlie the maintenance of LTP.

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References

  1. Bliss, T. V. P. & Lømo, T. J. Physiol. 232, 331–356 (1973).
    Article CAS Google Scholar
  2. Bliss, T. V. P. & Lynch, M. A. in Long-term Potentiation; From Biophysics to Behavior (eds Landfield, P. W. & Deadwyler, S. A.) 3–72 (Liss, New York, 1988).
    Google Scholar
  3. Nicoll, R. A., Kauer, J. A. & Malenka, R. C. Neuron 1, 97–103 (1988).
    Article CAS Google Scholar
  4. Wigström, H., Gustafsson, B., Huang, Y.-Y. & Abraham, W. C. Acta physiol. scand. 126, 317–319 (1986).
    Article Google Scholar
  5. Malinow, R. & Miller, J. P. Nature 320, 529–530 (1986).
    Article ADS CAS Google Scholar
  6. Kelso, S. R., Ganong, A. H. & Brown, T. H. Proc. natn. Acad. Sci. U.S.A. 83, 5326–5330 (1986).
    Article ADS CAS Google Scholar
  7. Sastry, B. R., Goh, J. W. & Auyeung, A. Science 232, 988–990 (1986).
    Article ADS CAS Google Scholar
  8. Dolphin, A. C., Errington, M. L. & Bliss, T. V. P. Nature 297, 496–498 (1982).
    Article ADS CAS Google Scholar
  9. Voronin, L. L., Kuhnt, U. & Hess, G. Neurophysiology 22, 341–347 (1990).
    Article Google Scholar
  10. Malinow, R. & Tsien, R. W. Nature 346, 177–180 (1990).
    Article ADS CAS Google Scholar
  11. Bekkers, J. M. & Stevens, C. F. Nature 346, 724–729 (1990).
    Article ADS CAS Google Scholar
  12. Malinow, R. Science 252, 722–724 (1991).
    Article ADS CAS Google Scholar
  13. Kauer, J. A., Malenka, R. C. & Nicoll, R. A. Neuron 1, 911–917 (1988).
    Article CAS Google Scholar
  14. Muller, D., Joly, M. & Lynch, G. Science 242, 1694–1697 (1988).
    Article ADS CAS Google Scholar
  15. Foster, T. C. & McNaughton, B. L. Hippocampus 1, 79–91 (1991).
    Article CAS Google Scholar
  16. Manabe, T., Renner, P. & Nicoll, R. A. Nature 355, 50–55 (1992).
    Article ADS CAS Google Scholar
  17. Edwards, F. Nature 350, 271–272 (1991).
    Article ADS CAS Google Scholar
  18. Korn, H. & Faber, D. S. Trends Neurosci. 14, 439–445 (1991).
    Article CAS Google Scholar
  19. Clements, J. D. Nature 353, 396 (1991).
    Article ADS CAS Google Scholar
  20. Bekkers, J. M., Richerson, G. B. & Stevens, C. F. Proc. natn. Acad. Sci. U.S.A. 87, 5359–5362 (1990).
    Article ADS CAS Google Scholar
  21. Larkman, A., Stratford, K. & Jack, J. Nature 350, 344–347 (1991).
    Article ADS CAS Google Scholar
  22. Redman, S. Physiol. Rev. 70, 165–198 (1990).
    Article CAS Google Scholar
  23. Zucker, R. S. J. Physiol. 229, 787–810 (1973).
    Article CAS Google Scholar
  24. Kullmann, D. M. J. Neurosci. Meth. 30, 231–245 (1989).
    Article CAS Google Scholar
  25. Dempster, A. P., Laird, N. M. & Rubin, D. B. J. R. statist. Soc. B 39, 1–21 (1977).
    Google Scholar
  26. Gull, S. F. & Daniell, G. J. Nature 272, 686–690 (1978).
    Article ADS Google Scholar
  27. Nicoll, R. A. & Alger, B. E. J. Neurosci. Meth. 4, 153–156 (1981).
    Article CAS Google Scholar
  28. Coleman, P. A. & Miller, R. F. J. Neurophysiol. 61, 218–230 (1989).
    Article CAS Google Scholar
  29. Blanton, M. G., Lo Turco, J. J. & Kriegstein, A. R. J. Neurosci. Meth. 30, 203–210 (1989).
    Article CAS Google Scholar
  30. Horn, R. & Marty, A. J. gen. Physiol. 92, 145–159 (1988).
    Article CAS Google Scholar

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  1. Roger A. Nicoll: To whom correspondence should be addressed

Authors and Affiliations

  1. Departments of Pharmacology and Physiology, School of Medicine, University of California, San Francisco, San Francisco, California, 94143-0450, USA
    Dimitri M. Kullmann & Roger A. Nicoll

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  1. Dimitri M. Kullmann
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  2. Roger A. Nicoll
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Kullmann, D., Nicoll, R. Long-term potentiation is associated with increases in quantal content and quantal amplitude.Nature 357, 240–244 (1992). https://doi.org/10.1038/357240a0

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