IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38338-3.html
   My bibliography  Save this article

Dynamic and stable hippocampal representations of social identity and reward expectation support associative social memory in male mice

Author

Listed:
  • Eunji Kong

    (Institute for Basic Science
    Korea Advanced Institute of Science and Technology
    Korea Advanced Institute of Science and Technology)

  • Kyu-Hee Lee

    (Institute for Basic Science)

  • Jongrok Do

    (Institute for Basic Science
    Korea Advanced Institute of Science and Technology)

  • Pilhan Kim

    (Korea Advanced Institute of Science and Technology
    Korea Advanced Institute of Science and Technology)

  • Doyun Lee

    (Institute for Basic Science)

Abstract

Recognizing an individual and retrieving and updating the value information assigned to the individual are fundamental abilities for establishing social relationships. To understand the neural mechanisms underlying the association between social identity and reward value, we developed Go-NoGo social discrimination paradigms that required male subject mice to distinguish between familiar mice based on their individually unique characteristics and associate them with reward availability. We found that mice could discriminate individual conspecifics through a brief nose-to-nose investigation, and this ability depended on the dorsal hippocampus. Two-photon calcium imaging revealed that dorsal CA1 hippocampal neurons represented reward expectation during social, but not non-social tasks, and these activities were maintained over days regardless of the identity of the associated mouse. Furthermore, a dynamically changing subset of hippocampal CA1 neurons discriminated between individual mice with high accuracy. Our findings suggest that the neuronal activities in CA1 provide possible neural substrates for associative social memory.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38338-3
    DOI: 10.1038/s41467-023-38338-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38338-3
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-38338-3?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Edward H. Nieh & Manuel Schottdorf & Nicolas W. Freeman & Ryan J. Low & Sam Lewallen & Sue Ann Koay & Lucas Pinto & Jeffrey L. Gauthier & Carlos D. Brody & David W. Tank, 2021. "Geometry of abstract learned knowledge in the hippocampus," Nature, Nature, vol. 595(7865), pages 80-84, July.
    2. 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.
    3. Torcato Meira & Felix Leroy & Eric W. Buss & Azahara Oliva & Jung Park & Steven A. Siegelbaum, 2018. "A hippocampal circuit linking dorsal CA2 to ventral CA1 critical for social memory dynamics," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    4. Frederick L. Hitti & Steven A. Siegelbaum, 2014. "The hippocampal CA2 region is essential for social memory," Nature, Nature, vol. 508(7494), pages 88-92, April.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. 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.
    3. 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.
    4. P. Dylan Rich & Stephan Yves Thiberge & Benjamin B. Scott & Caiying Guo & D. Gowanlock R. Tervo & Carlos D. Brody & Alla Y. Karpova & Nathaniel D. Daw & David W. Tank, 2024. "Magnetic voluntary head-fixation in transgenic rats enables lifespan imaging of hippocampal neurons," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    5. 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.
    6. Nicole Eichert & Jordan DeKraker & Amy F. D. Howard & Istvan N. Huszar & Silei Zhu & Jérôme Sallet & Karla L. Miller & Rogier B. Mars & Saad Jbabdi & Boris C. Bernhardt, 2024. "Hippocampal connectivity patterns echo macroscale cortical evolution in the primate brain," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    7. Yuto Hasegawa & Juhyun Kim & Gianluca Ursini & Yan Jouroukhin & Xiaolei Zhu & Yu Miyahara & Feiyi Xiong & Samskruthi Madireddy & Mizuho Obayashi & Beat Lutz & Akira Sawa & Solange P. Brown & Mikhail V, 2023. "Microglial cannabinoid receptor type 1 mediates social memory deficits in mice produced by adolescent THC exposure and 16p11.2 duplication," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    8. 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.
    9. David Wolf & Renée Hartig & Yi Zhuo & Max F. Scheller & Mirko Articus & Marcel Moor & Valery Grinevich & Christiane Linster & Eleonora Russo & Wolfgang Weber-Fahr & Jonathan R. Reinwald & Wolfgang Kel, 2024. "Oxytocin induces the formation of distinctive cortical representations and cognitions biased toward familiar mice," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    10. Eleanor Spens & Neil Burgess, 2024. "A generative model of memory construction and consolidation," Nature Human Behaviour, Nature, vol. 8(3), pages 526-543, March.
    11. Owen Y. Chao & Salil Saurav Pathak & Hao Zhang & George J. Augustine & Jason M. Christie & Chikako Kikuchi & Hiroki Taniguchi & Yi-Mei Yang, 2023. "Social memory deficit caused by dysregulation of the cerebellar vermis," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    12. Chinnakkaruppan Adaikkan & Justin Joseph & Georgios Foustoukos & Jun Wang & Denis Polygalov & Roman Boehringer & Steven J. Middleton & Arthur J. Y. Huang & Li-Huei Tsai & Thomas J. McHugh, 2024. "Silencing CA1 pyramidal cells output reveals the role of feedback inhibition in hippocampal oscillations," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    13. 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.
    14. Biao Zhang & Shuqin Zhang & Shihua Zhang, 2024. "Whole brain alignment of spatial transcriptomics between humans and mice with BrainAlign," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    15. Huixin Lin & Jingfeng Zhou, 2024. "Hippocampal and orbitofrontal neurons contribute to complementary aspects of associative structure," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    16. Nahoko Kuga & Ryota Nakayama & Shota Morikawa & Haruya Yagishita & Daichi Konno & Hiromi Shiozaki & Natsumi Honjoya & Yuji Ikegaya & Takuya Sasaki, 2023. "Hippocampal sharp wave ripples underlie stress susceptibility in male mice," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    17. Joanna C. Chang & Matthew G. Perich & Lee E. Miller & Juan A. Gallego & Claudia Clopath, 2024. "De novo motor learning creates structure in neural activity that shapes adaptation," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    18. Ian Cone & Claudia Clopath, 2024. "Latent representations in hippocampal network model co-evolve with behavioral exploration of task structure," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    19. Changyuan Yang & Sai Ma & Qinkai Han, 2023. "Unified discriminant manifold learning for rotating machinery fault diagnosis," Journal of Intelligent Manufacturing, Springer, vol. 34(8), pages 3483-3494, December.
    20. Zihao Chen & Yechao Han & Zheng Ma & Xinnian Wang & Surui Xu & Yong Tang & Alexei L. Vyssotski & Bailu Si & Yang Zhan, 2024. "A prefrontal-thalamic circuit encodes social information for social recognition," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38338-3. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.