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Reactivation of experience-dependent cell assembly patterns in the hippocampus

Abstract

The hippocampus is thought to be involved in episodic memory formation by reactivating traces of waking experience during sleep. Indeed, the joint firing of spatially tuned pyramidal cells encoding nearby places recur during sleep. We found that the sleep cofiring of rat CA1 pyramidal cells encoding similar places increased relative to the sleep session before exploration. This cofiring increase depended on the number of times that cells fired together with short latencies (<50 ms) during exploration, and was strongest between cells representing the most visited places. This is indicative of a Hebbian learning rule in which changes in firing associations between cells are determined by the number of waking coincident firing events. In contrast, cells encoding different locations reduced their cofiring in proportion to the number of times that they fired independently. Together these data indicate that reactivated patterns are shaped by both positive and negative changes in cofiring, which are determined by recent behavior.

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Figure 1: Place-related firing patterns are reactivated during sleep.
Figure 2: PFS predicts sleep cofiring (post) and cofiring change (from pre to post).
Figure 3: Cells that fire together in more frequently visited locations show stronger cofiring in SWR periods.
Figure 4: Ensemble firing patterns during sleep reflect the number of times that cells fire together during exploration.
Figure 5: Average cofiring change as a function of the mean CSI.
Figure 6: Reactivation of CA3-CA1 cell ensembles after exploration in novel environments.

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Acknowledgements

We thank G. Buzsaki, A. Czurko, D. Dupret, T. Klausberger, O. Paulsen, B. Pleydell-Bouverie, O. Potvin and P. Somogyi for their constructive comments on a previous version of the manuscript, and N. Campo-Urriza for the technical assistance. This work was supported by the Medical Research Council. T.J.S. and K.A. are funded by the Wellcome Trust.

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J.O. carried out the data analysis. T.J.S., J.O., J.C. and K.A. conducted the experiments and spike clustering. J.C., J.O. and J.R.H. wrote the manuscript. J.C. supervised the project.

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Correspondence to Jozsef Csicsvari.

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O'Neill, J., Senior, T., Allen, K. et al. Reactivation of experience-dependent cell assembly patterns in the hippocampus. Nat Neurosci 11, 209–215 (2008). https://doi.org/10.1038/nn2037

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