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Biasing the content of hippocampal replay during sleep

Abstract

The hippocampus is essential for encoding self-experienced events into memory. During sleep, neural activity in the hippocampus related to a recent experience has been observed to spontaneously reoccur, and this 'replay' has been postulated to be important for memory consolidation. Task-related cues can enhance memory consolidation when presented during a post-training sleep session, and, if memories are consolidated by hippocampal replay, a specific enhancement for this replay should be observed. To test this, we trained rats on an auditory-spatial association task while recording from neuronal ensembles in the hippocampus. We found that, during sleep, a task-related auditory cue biased reactivation events toward replaying the spatial memory associated with that cue. These results indicate that sleep replay can be manipulated by external stimulation and provide further evidence for the role of hippocampal replay in memory consolidation.

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Figure 1: Behavioral task.
Figure 2: Hippocampal activity during behavior and sleep (rat 1, session 2).
Figure 3: Place cell responses during sleep reactivation events.
Figure 4: Rate bias during sleep reactivation events.
Figure 5: Rate bias during awake reactivation events.
Figure 6: Temporal dynamics of sound-evoked reactivation bias.
Figure 7: Bias in Bayesian decoded position during sleep reactivation events.

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Acknowledgements

We thank M. Fee, H. Tanila and members of the Wilson laboratory for their helpful comments and suggestions. We would also like to thank C. Varela, J. Yamamoto, J. Siegle, E. Kuo, A. Hussain and E. Molina for technical assistance. This work was supported by a Merck Award/Helen Hay Whitney Postdoctoral Fellowship (D.B.), a Charles King Trust Postdoctoral Fellowship (D.B.), US National Institutes of Health grants 1-K99-DC012321-01 (D.B.) and 5R01MH061976 (M.A.W.).

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D.B. designed the experiment, and collected and analyzed the data. D.B. and M.A.W. co-wrote the manuscript. M.A.W. supervised the experiment.

Corresponding author

Correspondence to Daniel Bendor.

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The authors declare no competing financial interests.

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Bendor, D., Wilson, M. Biasing the content of hippocampal replay during sleep. Nat Neurosci 15, 1439–1444 (2012). https://doi.org/10.1038/nn.3203

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