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Synaptic excitation produces a long-lasting rebound potentiation of inhibitory synaptic signals in cerebellar Purkinje cells

Nature volume 356, pages 601–604 (1992)Cite this article

Abstract

PERSISTENT changes in synaptic efficacy are thought to underlie the formation of learning and memory in the brain1. High-frequency activation of an afferent excitatory fibre system can induce long-term potentiation2,3, and conjunctive activation of two distinct excitatory synaptic inputs to the cerebellar Purkinje cells can lead to long-term depression of the synaptic activity of one of the inputs4. Here we report a new form of neural plasticity in which activation of an excitatory synaptic input can induce a potentiation of inhibitory synaptic signals to the same cell. In cerebellar Purkinje cells stimulation of the excitatory climbing fibre synapses is followed by a long-lasting (up to 75 min) potentiation of γ-aminobutyric acid A (GABAA) receptor-mediated inhibitory postsynaptic currents (i.p.s.cs), a phenomenon that we term rebound potentiation. Using whole-cell patch-clamp recordings in combination with fluorometric video imaging of intracel-lular calcium ion concentration, we find that a climbing fibre-induced transient increase in postsynaptic calcium concentration triggers the induction of rebound potentiation. Because the response of Purkinje cells to bath-applied exogenous GABA is also potentiated after climbing fibre-stimulation with a time course similar to that of the rebound potentiation of i.p.s.cs, we conclude that the potentiation is caused by a calcium-dependent upregula-tion of postsynaptic GABAA receptor function. We propose that rebound potentiation is a mechanism by which in vivo block of climbing fibre activity induces an increase in excitability in Purkinje cells5,6. Moreover, rebound potentiation of i.p.s.cs is a cellular mechanism which, in addition to the long-term depression of parallel fibre synaptic activity4, may have an important role for motor learning in the cerebellum.

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References

  1. Kandel, E. & Schwartz, J. Science 229, 433–443 (1982).

    Article  ADS  Google Scholar 

  2. Collingridge, G. L. & Singer, W. Trends pharmac. Sci. 11, 290–296 (1990).

    Article  CAS  Google Scholar 

  3. Kuba, K. & Kumamoto, E. Prog. Neurobiol. 34, 197–269 (1990).

    Article  CAS  Google Scholar 

  4. Ito, M. A. Rev. Neurosci. 12, 85–102 (1989).

    Article  CAS  Google Scholar 

  5. Montarolo, P. G., Palestini, M. & Strata, P. J. Physiol. 332, 187–202 (1982).

    Article  CAS  Google Scholar 

  6. Kano, M. & Kato, M. Neurosci. Res. 5, 544–556 (1988).

    Article  CAS  Google Scholar 

  7. Hamill, O. P., Marty, A., Neher, E., Sakmann, B. & Sigworth, F. J. Pflügers Arch. 391, 85–100 (1981).

    Article  CAS  Google Scholar 

  8. Edwards, F. A., Konnerth, A., Sakmann, B. & Takahashi, T. Pflügers Arch. 414, 600–612 (1989).

    Article  CAS  Google Scholar 

  9. Konnerth, A., Llano, I. & Armstrong, C. Proc. natn. Acad. Sci. U.S.A. 87, 2662–2665 (1990).

    Article  ADS  CAS  Google Scholar 

  10. Eccles, J. C., Llinas, R. & Sasaki, K. J. Physiol. 182, 268–296 (1966).

    Article  CAS  Google Scholar 

  11. Llinas, R. & Sugimori, M. J. Physiol. 305, 197–213 (1980).

    Article  CAS  Google Scholar 

  12. Llano, I., Marty, A., Armstrong, C. & Konnerth, A. J. Physiol. 424, 183–213 (1991).

    Article  Google Scholar 

  13. Ross, W. N. & Werman, R. J. Physiol. 389, 319–336 (1987).

    Article  CAS  Google Scholar 

  14. Knöpfel, T., Vranesic, I., Staub, C. & Gähwiler, B. H. Eur. J. Neurosci. 3, 343–348 (1991).

    Article  Google Scholar 

  15. Konnerth, A., Dreessen, J. & Augustine, G. J. Proc. natn. Acad. Sci. U.S.A. (in the press).

  16. Llano, I., Dreessen, J., Kano, M. & Konnerth, A. Neuron 7, 577–583 (1991).

    Article  CAS  Google Scholar 

  17. Marchenko, S. M. Brain Res. 546, 355–357 (1991).

    Article  CAS  Google Scholar 

  18. Llano, I., Leresche, N. & Marty, A. Neuron 6, 565–574 (1991).

    Article  CAS  Google Scholar 

  19. Cheun, J. E. & Yeh, H. H. Soc. Neurosci. Abst. 17, 602 (1991).

    Google Scholar 

  20. Inoue, M., Oomura, Y., Yakushiji, T. & Akaike, N. Nature 324, 156–158 (1986).

    Article  ADS  CAS  Google Scholar 

  21. Chen, Q. X., Stelzer, A., Kay, A. R. & Wong, R. K. S. J. Physiol. 420, 207–221 (1990).

    Article  CAS  Google Scholar 

  22. Mulle, C., Choquet, D., Korn, H. & Changeux, J. P. Neuron 8, 135–143 (1992).

    Article  CAS  Google Scholar 

  23. Harrison, N. L. & Lambert, N. A. Neurosci. Lett. 105, 137–142 (1989).

    Article  CAS  Google Scholar 

  24. Porter, N. M., Twyman, R. E., Uhler, M. D. & MacDonald, L. Neuron 5, 789–796 (1990).

    Article  CAS  Google Scholar 

  25. Mouginot, D., Feltz, P. & Schlichter, R. J. Physiol. 427, 109–132 (1991).

    Article  Google Scholar 

  26. Benedetti, F., Montarolo, P. G. & Rabacchi, S. Expl Brain Res. 55, 368–371 (1984).

    Article  CAS  Google Scholar 

  27. Kano, M. & Kato, M. Nature 325, 276–279 (1987).

    Article  ADS  CAS  Google Scholar 

  28. Ito, M. & Karachot, L. NeuroReport 1, 129–132 (1990).

    Article  CAS  Google Scholar 

  29. Linden, D. J., Dickinson, M. H., Smeyne, M. & Connor J. A. Neuron 6, 81–89 (1991).

    Article  Google Scholar 

  30. Edwards, F. A., Konnerth, A. & Sakmann, B. J. Physiol. 430, 213–249 (1990).

    Article  CAS  Google Scholar 

  31. Grynkiewicz, G., Poenie, M. & Tsien, R. Y. J. biol. Chem. 260, 3440–3450 (1985).

    CAS  Google Scholar 

  32. Neher, E. in Neuromuscular Junction (eds Sellin, L. C., Libelius, R. & Thesleff, S.) 65–76 (Elsevier, Amsterdam, 1989).

    Google Scholar 

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Authors and Affiliations

  1. Max-Planck-lnstitut für Biophysikalische Chemie, Am Fassberg, 3400, Göttingen, Germany

    M. Kano, U. Rexhausen, J. Dreessen & A. Konnerth

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  1. M. Kano
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  2. U. Rexhausen
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  3. J. Dreessen
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  4. A. Konnerth
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Kano, M., Rexhausen, U., Dreessen, J. et al. Synaptic excitation produces a long-lasting rebound potentiation of inhibitory synaptic signals in cerebellar Purkinje cells. Nature 356, 601–604 (1992). https://doi.org/10.1038/356601a0

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