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Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus

Nature volume 394, pages 891–894 (1998)Cite this article

Abstract

Experience-dependent long-lasting increases in excitatory synaptic transmission in the hippocampus are believed to underlie certain types of memory1,2,3. Whereas stimulation of hippocampal pathways in freely moving rats can readily elicit a long-term potentiation (LTP) of transmission that may last for weeks, previous studies have failed to detect persistent increases in synaptic efficacy after hippocampus-mediated learning4,5,6. As changes in synaptic efficacy are contingent on the history of plasticity at the synapses7, we have examined the effect of experience-dependent hippocampal activation on transmission after the induction of LTP. We show that exploration of a new, non-stressful environment rapidly induces a complete and persistent reversal ofthe expression of high-frequency stimulation-induced early-phase LTP in the CA1 area of the hippocampus, without affecting baseline transmission in a control pathway. LTP expression is not affected by exploration of familiar environments. We found that spatial exploration affected LTP within a defined time window because neither the induction of LTP nor the maintenance of long-established LTP was blocked. The discovery of a novelty-induced reversal of LTP expression provides strong evidence that extensive long-lasting decreases in synaptic efficacy may act in tandem with enhancements at selected synapses to allow the detection and storage of new information by the hippocampus.

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Figure 1: Exploration of a novel environment rapidly reverses LTP.
Figure 2: Exploration of a familiar environment fails to affect LTP persistence.
Figure 3: Time window for the effect of novelty exploration on LTP.

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Acknowledgements

This research was supported by the Health Research Board of Ireland, the European Union DGXII and the Wellcome Trust. We thank W. K. Cullen and J. Wu for assistance.

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Authors and Affiliations

  1. Department of Pharmacology and Therapeutics, Dublin, 2, Ireland

    Lin Xu & Michael J. Rowan

  2. Department of Physiology, Trinity College, Dublin, 2, Ireland

    Roger Anwyl

  3. Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, The People's Republic of China

    Lin Xu

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  1. Lin Xu
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  2. Roger Anwyl
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  3. Michael J. Rowan
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Xu, L., Anwyl, R. & Rowan, M. Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus. Nature 394, 891–894 (1998). https://doi.org/10.1038/29783

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