OPINION

A contextual binding theory of episodic memory: systems consolidation reconsidered

Abstract

Episodic memory reflects the ability to recollect the temporal and spatial context of past experiences. Episodic memories depend on the hippocampus but have been proposed to undergo rapid forgetting unless consolidated during offline periods such as sleep to neocortical areas for long-term storage. Here, we propose an alternative to this standard systems consolidation theory (SSCT) — a contextual binding account — in which the hippocampus binds item-related and context-related information. We compare these accounts in light of behavioural, lesion, neuroimaging and sleep studies of episodic memory and contend that forgetting is largely due to contextual interference, episodic memory remains dependent on the hippocampus across time, contextual drift produces post-encoding activity and sleep benefits memory by reducing contextual interference.

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Fig. 1: Results that have historically been taken as evidence in support of systems consolidation theory.

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Acknowledgements

This paper is based on discussions with students and faculty participating in a graduate seminar at the University of California–Davis, including A. Borders, G. Shields, R. Goodrich, M. Ramey, T. Baer, I. Pastor, C. Riddell, M. Sazma, A. McCullough, C. Carrasco, M. Ritchey, D. Ragland, M. Starrett, M. Liang, A. Barnett, Z. Reagh, B. Cohn-Sheehy, J. Crivelli-Decker, W. Reilly, M. Gruber, N. Bouffard, H. Dimsdale-Zucker, J. Wilmot, Y. Ota, K. Puhger and J. Krueger. This work was supported by the US National Eye Institute of the US National Institutes of Health (NIH) under Award Number R01EY025999 (A.P.Y.); NIH/National Institute of Neurological Disorders and Stroke (NINDS) grants NS076856 (A.D.E.) and NS093052 (A.D.E. and A.P.Y.); and NINDS grants R01NS088053 and R21NS101694 (B.J.W.). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.

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Nature Reviews Neuroscience thanks P. Frankland, M. Moscovitch, R. J. Sutherland and the other, anonymous reviewer for their contribution to the peer review of this work.

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Yonelinas, A.P., Ranganath, C., Ekstrom, A.D. et al. A contextual binding theory of episodic memory: systems consolidation reconsidered. Nat Rev Neurosci 20, 364–375 (2019). https://doi.org/10.1038/s41583-019-0150-4

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