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Off-line replay maintains declarative memories in a model of hippocampal-neocortical interactions

Abstract

During sleep, neural activity in the hippocampus and neocortex seems to recapitulate aspects of its earlier, awake form. This replay may be a substrate for the consolidation of long-term declarative memories, whereby they become independent of the hippocampus and are stored in neocortex. In contrast to storage, other crucial facets of competent long-term memory, such as maintenance of access to stored traces and preservation of their correct interpretation, have received little attention. We investigate long-term episodic and semantic memory in a theoretical model of neocortical-hippocampal interaction. We find that, in the absence of regular hippocampal reactivation, even supposedly consolidated episodic memories are fragile in the face of cortical semantic plasticity. Replay allows access to episodes stored in the hippocampus to be maintained, by keeping them in appropriate register with changing neocortical representations. Hippocampal storage and replay also has a constructive role in the recall of structured, semantic information.

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Figure 1: Model architecture.
Figure 2: Replay transfers episodic memories to neocortex.
Figure 3: Episodic memories stored in neocortex are extinguished by subsequent semantic training.
Figure 4: Replay protects episodic memories against representational change.
Figure 5: Analysis of the reasons why episodic recall breaks down in Figure 4a.
Figure 6: Hippocampal replay and recall aid the acquisition and consolidation of semantic information.
Figure 7: Neocortical plasticity during replay maintains semantic memory.

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Acknowledgements

We thank S. Becker, N. Burgess, M. Lengyel, J.L. McClelland and A.D. Wagner for their extensive comments on earlier drafts. Funding was from the Hungarian Academy of Sciences (S.K.) and the Gatsby Charitable Foundation (S.K. and P.D.).

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Correspondence to Szabolcs Káli.

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Káli, S., Dayan, P. Off-line replay maintains declarative memories in a model of hippocampal-neocortical interactions. Nat Neurosci 7, 286–294 (2004). https://doi.org/10.1038/nn1202

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