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Hippocampal signatures of awake targeted memory reactivation

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Abstract

Dominant theories of episodic memory propose that a key mechanism of memory consolidation is replay—a process, whereby neural patterns of activation during learning are reinstated during offline post-learning periods. Here, we tested whether key signatures of replay defined by studies in rodents, such as recapitulation of specific memory traces, as well as sequences, are apparent in humans during post-encoding memory reactivation. Thirty participants underwent functional imaging that consisted of interleaved encoding and rest periods. During an offline period of wakeful rest, we biased reactivation towards some memories by presenting sound cues that had previously been associated with particular stimulus sequences. Results showed that targeted hippocampal reactivation was biased towards cued memory sequences and that reactivation signatures preserved the temporal order of particular sequences. Importantly, the biased reactivation was related to differences in subsequent memory, suggesting that preferential reactivation may be a mechanism by which specific memory traces can be strengthened for enhanced subsequent memory retrieval.

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Acknowledgements

We would like to thank Drs. Feroze Mohamed and Chris Conklin for assistance with pulse sequence development, Drs. Charan Ranganath, Anthony Wagner, Jason Chein, and Vinod Venkatraman for helpful advice and commentary on early versions of this manuscript.

Funding

This work was supported by a National Institute of Mental Health Grant to I.R.O. [R01 MH091113] and a Temple University Dissertation Completion Grant to K.H.A. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institute of Mental Health or the National Institutes of Health.

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Correspondence to Kylie H. Alm.

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The authors declare that they have no conflicts of interest.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Informed consent was obtained from all individual participants included in the study.

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Alm, K.H., Ngo, C.T. & Olson, I.R. Hippocampal signatures of awake targeted memory reactivation. Brain Struct Funct 224, 713–726 (2019). https://doi.org/10.1007/s00429-018-1790-2

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  • DOI: https://doi.org/10.1007/s00429-018-1790-2

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