Hippocampal CA2 sharp-wave ripples reactivate and promote social memory
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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) sleep 1-8 and whose disruption impairs spatial memory 3,5,6,8. 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 hippocampus 7,9, 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 memory 10-12. 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.
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The dorsal CA2 is the key centre for encoding, consolidation and recall phases of social memory.
“The dorsal CA2 is the key centre for encoding, consolidation and recall phases of social memory [125–128].”
From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [127]
In “Dorsal CA2 is needed for social memory” (page unavailable), silencing dorsal CA2 during learning disrupted social memory, supporting its role in encoding. The Discussion and “Social memory requires CA2 SWRs” support a role in consolidation. “CA2 SWRs replay social memory” reports reactivation during recall, but does not establish that dorsal CA2 is a key centre required for the recall phase. (LLM, conf=0.84)
Experimental — accuracy not yet measuredRipples induced optogenetically in CA2 neurons following encoding of a social memory task enhanced recall 24 h later.
“In a recent study, ripples induced optogenetically in CA2 neurons following encoding of a social memory task enhanced recall 24 h later.194”
From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [194]
Processing of social information by dorsal CA2, possibly in the form of sharp-wave ripples, is relayed to ventral CA1 that in turn influences downstream limbic structures including the nucleus accumbens and medial prefrontal cortex.
“This processing of social information by dorsal CA2, possibly in the form of sharp-wave ripples [86], is then relayed to ventral CA1 that in turn influences downstream limbic structures including the NAc and mPFC.”
From Neural circuits regulating prosocial behaviors (2023) · cites this paper as [86]
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Self-citation
- Authors
- Oliva, A., Fernández-Ruiz, A., Leroy, F., & Siegelbaum, S. A.
- Affiliations
- Mortimer B. Zuckerman Mind Brain Behavior Institute (US)
- Corresponding author
- Oliva, Azahara
- Siegelbaum, Steven A.
- Venue
- Nature
- Published
- 2020-09-23
- Volume
- 587
- Issue
- 7833
- Pages
- 264-269
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC7666067
- OpenAlex
- W3087859979
- Cited by
- 268
- References
- 55
- Citations by year
- 2026: 40 · 2025: 49 · 2024: 39 · 2023: 61 · 2022: 48 · 2021: 28 · 2020: 2
- FWCI
- 18.66
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Locations
- Nature (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- Funders
- Wellcome Trust
- National Institutes of Health (2r01mh104602-11)
- National Institute of Mental Health (R01-MH104602, R01MH106629, K99MH122582, K99MH120343, R00MH122582, R01MH140009)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- sharp-wave ripples, hippocampal CA2, social memory, memory consolidation, neural reactivation, NREM sleep, pyramidal neurons, spatial memory
- MeSH terms
- Memory Consolidation, Social Interaction, Animals, Male, Memory, Mice, Inbred C57BL, Mental Recall, Sleep, Pyramidal Cells, Mice, CA2 Region, Hippocampal, Optogenetics
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