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Reactivations of emotional memory in the hippocampus–amygdala system during sleep

Nature Neuroscience volume 20, pages 16341642 (2017) | Download Citation

Abstract

The consolidation of context-dependent emotional memory requires communication between the hippocampus and the basolateral amygdala (BLA), but the mechanisms of this process are unknown. We recorded neuronal ensembles in the hippocampus and BLA while rats learned the location of an aversive air puff on a linear track, as well as during sleep before and after training. We found coordinated reactivations between the hippocampus and the BLA during non-REM sleep following training. These reactivations peaked during hippocampal sharp wave–ripples (SPW-Rs) and involved a subgroup of BLA cells positively modulated during hippocampal SPW-Rs. Notably, reactivation was stronger for the hippocampus–BLA correlation patterns representing the run direction that involved the air puff than for the 'safe' direction. These findings suggest that consolidation of contextual emotional memory occurs during ripple-reactivation of hippocampus–amygdala circuits.

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Acknowledgements

We thank J. LeDoux, C. Léna, E. Stark, A. Peyrache and L. Roux for comments and discussions on the analyses and manuscript and all the members of the Buzsáki laboratory for their support. This work was supported by the Fondation pour la Recherche Médicale (FRM), the Fyssen Foundation, a Charles H. Revson Senior Fellowship in Biomedical Science (G.G.), NIH MH54671 and MH107396, NS 090583 and the Simons Foundations (G.B.).

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Author notes

    • Ingrid Inema

    Present address: Douglas Institute, McGill University, Montreal, Quebec, Canada.

Affiliations

  1. New York University Neuroscience Institute, New York University, New York, New York, USA.

    • Gabrielle Girardeau
    • , Ingrid Inema
    •  & György Buzsáki
  2. Department of Neurology, Medical Center, New York University, New York, New York, USA.

    • György Buzsáki
  3. Center for Neural Science, New York University, New York, New York, USA.

    • György Buzsáki

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Contributions

G.G. and G.B. designed the study, G.G. and I.I. performed the experiments, G.G. analyzed the data and G.B. and G.G. wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to György Buzsáki.

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DOI

https://doi.org/10.1038/nn.4637