Hippocampal Replay Is Not a Simple Function of Experience

Anoopum S. Gupta, Matthijs A.A. van der Meer, David S. Touretzky, A. David Redish

    Research output: Contribution to journalArticlepeer-review

    342 Scopus citations

    Abstract

    Replay of behavioral sequences in the hippocampus during sharp wave ripple complexes (SWRs) provides a potential mechanism for memory consolidation and the learning of knowledge structures. Current hypotheses imply that replay should straightforwardly reflect recent experience. However, we find these hypotheses to be incompatible with the content of replay on a task with two distinct behavioral sequences (A and B). We observed forward and backward replay of B even when rats had been performing A for >10 min. Furthermore, replay of nonlocal sequence B occurred more often when B was infrequently experienced. Neither forward nor backward sequences preferentially represented highly experienced trajectories within a session. Additionally, we observed the construction of never-experienced novel-path sequences. These observations challenge the idea that sequence activation during SWRs is a simple replay of recent experience. Instead, replay reflected all physically available trajectories within the environment, suggesting a potential role in active learning and maintenance of the cognitive map.

    Original languageEnglish (US)
    Pages (from-to)695-705
    Number of pages11
    JournalNeuron
    Volume65
    Issue number5
    DOIs
    StatePublished - Mar 11 2010

    Bibliographical note

    Funding Information:
    We thank Chris Boldt and Adam Steiner for technical assistance, Adam Johnson for comments on a previous version of the manuscript, and the members of the Redish lab for discussion. This work was funded by NIH grant R01 MH-080381, the Pennsylvania Department of Health, and NSF IGERT DGE-0549352.

    Keywords

    • SYSNEURO

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