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Replay of rule-learning related neural patterns in the prefrontal cortex during sleep

Nature Neuroscience volume 12, pages 919926 (2009) | Download Citation

Abstract

Slow-wave sleep (SWS) is important for memory consolidation. During sleep, neural patterns reflecting previously acquired information are replayed. One possible reason for this is that such replay exchanges information between hippocampus and neocortex, supporting consolidation. We recorded neuron ensembles in the rat medial prefrontal cortex (mPFC) to study memory trace reactivation during SWS following learning and execution of cross-modal strategy shifts. In general, reactivation of learning-related patterns occurred in distinct, highly synchronized transient bouts, mostly simultaneous with hippocampal sharp wave/ripple complexes (SPWRs), when hippocampal ensemble reactivation and cortico-hippocampal interaction is enhanced. During sleep following learning of a new rule, mPFC neural patterns that appeared during response selection replayed prominently, coincident with hippocampal SPWRs. This was learning dependent, as the patterns appeared only after rule acquisition. Therefore, learning, or the resulting reliable reward, influenced which patterns were most strongly encoded and successively reactivated in the hippocampal/prefrontal network.

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Acknowledgements

We thank P. Tierney for valuable discussions and help with the surgical procedures, J.-M. Deniau, Y. Gioanni, A.-M. Thierry, M.B. Zugaro, M. Cencini and A. Aubry for interesting discussions, S. Doutremer for histology, D. Hopkins and N. Quenech'du for the anatomical reconstructions, V. Douchamps for help with the experiments, K. Gothard, K. Hoffman and A. Treves for critical readings of an earlier version of the manuscript, and A Berthoz for support throughout the project. This work was supported by Fondation Fyssen (F.P.B.), Fondation pour la Recherche Medicale (A.P.), and European Community contracts FP6-IST 027819 (Integrating Cognition, Emotion and Autonomy), FP6-IST-027140 (Bayesian Approach to Cognitive Systems) and FP6-IST-027017 (NeuroProbes).

Author information

Affiliations

  1. Laboratoire de Physiologie de la Perception et de l'Action, Collège de France, Centre National de la Recherche Scientifique, Paris, France.

    • Adrien Peyrache
    • , Mehdi Khamassi
    • , Karim Benchenane
    • , Sidney I Wiener
    •  & Francesco P Battaglia
  2. Institut des Systèmes Intelligents et de Robotique, Université Pierre et Marie Curie – Paris 6, Centre National de la Recherche Scientifique, Paris, France.

    • Mehdi Khamassi
  3. Center for Neuroscience, Swammerdam Institute for Life Sciences, Faculty of Science, Universiteit van Amsterdam, Amsterdam, The Netherlands.

    • Francesco P Battaglia

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Contributions

S.I.W., F.P.B. and M.K. designed the experiment, F.P.B., M.K. and A.P. performed the experiments, A.P., F.P.B. and K.B. designed the analysis techniques, A.P. analyzed the data, and F.P.B., A.P. and S.I.W. wrote the paper.

Corresponding author

Correspondence to Sidney I Wiener.

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DOI

https://doi.org/10.1038/nn.2337

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