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Awake replay of remote experiences in the hippocampus

Nature Neuroscience volume 12, pages 913–918 (2009)Cite this article

Abstract

Hippocampal replay is thought to be essential for the consolidation of event memories in hippocampal-neocortical networks. Replay is present during both sleep and waking behavior, but although sleep replay involves the reactivation of stored representations in the absence of specific sensory inputs, awake replay is thought to depend on sensory input from the current environment. Here, we show that stored representations are reactivated during both waking and sleep replay. We found frequent awake replay of sequences of rat hippocampal place cells from a previous experience. This spatially remote replay was as common as local replay of the current environment and was more robust when the rat had recently been in motion than during extended periods of quiescence. Our results indicate that the hippocampus consistently replays past experiences during brief pauses in waking behavior, suggesting a role for waking replay in memory consolidation and retrieval.

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Figure 1: Overview of experimental design.
Figure 2: Spatially remote awake replay in the rest box.
Figure 3: Replay of environment 1 in the rest box is more robust during awake than quiescent periods.
Figure 4: Robust replay of environment 1 while the rat was located in environment 2.
Figure 5: Local spatial rate and replay initiation for environment 1 replay in environment 2 and the rest box.

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Acknowledgements

We thank M. Brainard, D. Feldman, S. Lisberger, M. Stryker and the members of the Frank laboratory for comments on the manuscript. We also thank T. Davidson for a helpful discussion and M. Carr for help with histology photographs. This work was supported by the John Merck Scholars Program, the McKnight Scholars Program and US National Institutes of Health grants MH077970 and MH080283.

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Authors and Affiliations

  1. W.M. Keck Center for Integrative Neuroscience and Department of Physiology, University of California, San Francisco, California, USA

    Mattias P Karlsson & Loren M Frank

Authors
  1. Mattias P Karlsson
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  2. Loren M Frank
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Contributions

M.P.K. and L.M.F. designed the experimental procedure. M.P.K. carried out all of the data collection and the majority of the analyses. L.M.F. carried out the remaining analyses. M.P.K. and L.M.F. wrote the manuscript.

Corresponding author

Correspondence to Loren M Frank.

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Supplementary Figures 1–15, Supplementary Table 1, Supplementary Results and Supplementary Clusters (PDF 4337 kb)

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Karlsson, M., Frank, L. Awake replay of remote experiences in the hippocampus. Nat Neurosci 12, 913–918 (2009). https://doi.org/10.1038/nn.2344

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