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Hippocampal CA2 sharp-wave ripples reactivate and promote social memory

Author

Listed:
  • Azahara Oliva

    (The Kavli Institute for Brain Science, Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University)

  • Antonio Fernández-Ruiz

    (New York University)

  • Felix Leroy

    (The Kavli Institute for Brain Science, Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University)

  • Steven A. Siegelbaum

    (The Kavli Institute for Brain Science, Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University
    Columbia University)

Abstract

The consolidation of spatial memory depends on the reactivation (‘replay’) of hippocampal place cells that were active during recent behaviour. Such reactivation is observed during sharp-wave ripples (SWRs)—synchronous oscillatory electrical events that occur during non-rapid-eye-movement (non-REM) sleep1–8 and whose disruption impairs spatial memory3,5,6,8. Although the hippocampus also encodes a wide range of non-spatial forms of declarative memory, it is not yet known whether SWRs are necessary for such memories. Moreover, although SWRs can arise from either the CA3 or the CA2 region of the hippocampus7,9, the relative importance of SWRs from these regions for memory consolidation is unknown. Here we examine the role of SWRs during the consolidation of social memory—the ability of an animal to recognize and remember a member of the same species—focusing on CA2 because of its essential role in social memory10–12. We find that ensembles of CA2 pyramidal neurons that are active during social exploration of previously unknown conspecifics are reactivated during SWRs. Notably, disruption or enhancement of CA2 SWRs suppresses or prolongs social memory, respectively. Thus, SWR-mediated reactivation of hippocampal firing related to recent experience appears to be a general mechanism for binding spatial, temporal and sensory information into high-order memory representations, including social memory.

Suggested Citation

  • Azahara Oliva & Antonio Fernández-Ruiz & Felix Leroy & Steven A. Siegelbaum, 2020. "Hippocampal CA2 sharp-wave ripples reactivate and promote social memory," Nature, Nature, vol. 587(7833), pages 264-269, November.
  • Handle: RePEc:nat:nature:v:587:y:2020:i:7833:d:10.1038_s41586-020-2758-y
    DOI: 10.1038/s41586-020-2758-y
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    Citations

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    Cited by:

    1. Myung Chung & Katsutoshi Imanaka & Ziyan Huang & Akiyuki Watarai & Mu-Yun Wang & Kentaro Tao & Hirotaka Ejima & Tomomi Aida & Guoping Feng & Teruhiro Okuyama, 2024. "Conditional knockout of Shank3 in the ventral CA1 by quantitative in vivo genome-editing impairs social memory in mice," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    2. Rodrigo Ordoñez Sierra & Lizeth Katherine Pedraza & Lívia Barcsai & Andrea Pejin & Qun Li & Gábor Kozák & Yuichi Takeuchi & Anett J. Nagy & Magor L. Lőrincz & Orrin Devinsky & György Buzsáki & Antal B, 2023. "Closed-loop brain stimulation augments fear extinction in male rats," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. Hefei Guan & Steven J. Middleton & Takafumi Inoue & Thomas J. McHugh, 2021. "Lateralization of CA1 assemblies in the absence of CA3 input," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    4. Asako Noguchi & Roman Huszár & Shota Morikawa & György Buzsáki & Yuji Ikegaya, 2022. "Inhibition allocates spikes during hippocampal ripples," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    5. Elise C. Cope & Samantha H. Wang & Renée C. Waters & Isha R. Gore & Betsy Vasquez & Blake J. Laham & Elizabeth Gould, 2023. "Activation of the CA2-ventral CA1 pathway reverses social discrimination dysfunction in Shank3B knockout mice," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    6. Tansel Baran Yasar & Peter Gombkoto & Alexei L. Vyssotski & Angeliki D. Vavladeli & Christopher M. Lewis & Bifeng Wu & Linus Meienberg & Valter Lundegardh & Fritjof Helmchen & Wolfger von der Behrens , 2024. "Months-long tracking of neuronal ensembles spanning multiple brain areas with Ultra-Flexible Tentacle Electrodes," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    7. Eunji Kong & Kyu-Hee Lee & Jongrok Do & Pilhan Kim & Doyun Lee, 2023. "Dynamic and stable hippocampal representations of social identity and reward expectation support associative social memory in male mice," Nature Communications, Nature, vol. 14(1), pages 1-20, December.

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