IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-37736-x.html
   My bibliography  Save this article

Hippocampal sharp wave ripples underlie stress susceptibility in male mice

Author

Listed:
  • Nahoko Kuga

    (The University of Tokyo
    Tohoku University)

  • Ryota Nakayama

    (The University of Tokyo)

  • Shota Morikawa

    (The University of Tokyo)

  • Haruya Yagishita

    (The University of Tokyo
    Tohoku University)

  • Daichi Konno

    (The University of Tokyo
    The University of Tokyo)

  • Hiromi Shiozaki

    (Tohoku University)

  • Natsumi Honjoya

    (Tohoku University)

  • Yuji Ikegaya

    (The University of Tokyo
    Center for Information and Neural Networks, 1-4 Yamadaoka, Suita City
    Institute for AI and Beyond, The University of Tokyo)

  • Takuya Sasaki

    (The University of Tokyo
    Tohoku University)

Abstract

The ventral hippocampus (vHC) is a core brain region for emotional memory. Here, we examined how the vHC regulates stress susceptibility from the level of gene expression to neuronal population dynamics in male mice. Transcriptome analysis of samples from stress-naïve mice revealed that intrinsic calbindin (Calb1) expression in the vHC is associated with susceptibility to social defeat stress. Mice with Calb1 gene knockdown in the vHC exhibited increased stress resilience and failed to show the increase in the poststress ventral hippocampal sharp wave ripple (SWR) rate. Poststress vHC SWRs triggered synchronous reactivation of stress memory-encoding neuronal ensembles and facilitated information transfer to the amygdala. Suppression of poststress vHC SWRs by real-time feedback stimulation or walking prevented social behavior deficits. Taken together, our results demonstrate that internal reactivation of memories of negative stressful episodes supported by ventral hippocampal SWRs serves as a crucial neurophysiological substrate for determining stress susceptibility.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37736-x
    DOI: 10.1038/s41467-023-37736-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-37736-x
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-37736-x?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. Sunil Kumar & Rainbo Hultman & Dalton Hughes & Nadine Michel & Brittany M. Katz & Kafui Dzirasa, 2014. "Prefrontal cortex reactivity underlies trait vulnerability to chronic social defeat stress," Nature Communications, Nature, vol. 5(1), pages 1-9, December.
    2. Rosemary C. Bagot & Eric M. Parise & Catherine J. Peña & Hong-Xing Zhang & Ian Maze & Dipesh Chaudhury & Brianna Persaud & Roger Cachope & Carlos A. Bolaños-Guzmán & Joseph F. Cheer & Karl Deisseroth , 2015. "Ventral hippocampal afferents to the nucleus accumbens regulate susceptibility to depression," Nature Communications, Nature, vol. 6(1), pages 1-9, 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. Vaishnav Krishnan & Eric J. Nestler, 2008. "The molecular neurobiology of depression," Nature, Nature, vol. 455(7215), pages 894-902, October.
    5. Christoph Anacker & Victor M. Luna & Gregory S. Stevens & Amira Millette & Ryan Shores & Jessica C. Jimenez & Briana Chen & René Hen, 2018. "Hippocampal neurogenesis confers stress resilience by inhibiting the ventral dentate gyrus," Nature, Nature, vol. 559(7712), pages 98-102, July.
    6. Avishek Adhikari & Talia N. Lerner & Joel Finkelstein & Sally Pak & Joshua H. Jennings & Thomas J. Davidson & Emily Ferenczi & Lisa A. Gunaydin & Julie J. Mirzabekov & Li Ye & Sung-Yon Kim & Anna Lei , 2015. "Basomedial amygdala mediates top-down control of anxiety and fear," Nature, Nature, vol. 527(7577), pages 179-185, November.
    7. Rosemary C. Bagot & Eric M. Parise & Catherine J. Peña & Hong-Xing Zhang & Ian Maze & Dipesh Chaudhury & Brianna Persaud & Roger Cachope & Carlos A. Bolaños-Guzmán & Joseph F. Cheer & Karl Deisseroth , 2015. "Correction: Corrigendum: Ventral hippocampal afferents to the nucleus accumbens regulate susceptibility to depression," Nature Communications, Nature, vol. 6(1), pages 1-1, November.
    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. Robert N. Fetcho & Baila S. Hall & David J. Estrin & Alexander P. Walsh & Peter J. Schuette & Jesse Kaminsky & Ashna Singh & Jacob Roshgodal & Charlotte C. Bavley & Viraj Nadkarni & Susan Antigua & Th, 2023. "Regulation of social interaction in mice by a frontostriatal circuit modulated by established hierarchical relationships," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Eun-Hwa Lee & Jin-Young Park & Hye-Jin Kwon & Pyung-Lim Han, 2021. "Repeated exposure with short-term behavioral stress resolves pre-existing stress-induced depressive-like behavior in mice," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    3. Irene Serra & Julio Esparza & Laura Delgado & Cristina Martín-Monteagudo & Margalida Puigròs & Petar Podlesniy & Ramón Trullás & Marta Navarrete, 2022. "Ca2+-modulated photoactivatable imaging reveals neuron-astrocyte glutamatergic circuitries within the nucleus accumbens," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    4. Bob Bramson & Sjoerd Meijer & Annelies Nuland & Ivan Toni & Karin Roelofs, 2023. "Anxious individuals shift emotion control from lateral frontal pole to dorsolateral prefrontal cortex," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    5. 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.
    6. Dragan Glavaš & Irena Pavela Banai, 2024. "Physical Activity and Mental Health of Employed Adults: Mediation and Moderation Effects of Beliefs in the Benefits of Physical Activity," IJERPH, MDPI, vol. 21(7), pages 1-11, June.
    7. Jia Luo & Changfa Tang & Xiaobin Chen & Zhanbing Ren & Honglin Qu & Rong Chen & Zhen Tong, 2020. "Impacts of Aerobic Exercise on Depression-Like Behaviors in Chronic Unpredictable Mild Stress Mice and Related Factors in the AMPK/PGC-1α Pathway," IJERPH, MDPI, vol. 17(6), pages 1-12, March.
    8. Joana Mendes Duarte & Robin Nguyen & Marios Kyprou & Kaizhen Li & Anastasija Milentijevic & Carlo Cerquetella & Thomas Forro & Stéphane Ciocchi, 2024. "Hippocampal contextualization of social rewards in mice," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    9. Thomas H. Lee & Malegaddi Devaki & Douglas A. Formolo & Julia M. Rosa & Andy S. K. Cheng & Suk-Yu Yau, 2023. "Effects of Voluntary Wheel Running Exercise on Chemotherapy-Impaired Cognitive and Motor Performance in Mice," IJERPH, MDPI, vol. 20(7), pages 1-17, April.
    10. Rui Dang & An Liu & Yu Zhou & Xingcan Li & Miao Wu & Kun Cao & Yanghong Meng & Haiwang Zhang & Guangming Gan & Wei Xie & Zhengping Jia, 2024. "Astrocytic neuroligin 3 regulates social memory and synaptic plasticity through adenosine signaling in male mice," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    11. 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.
    12. Shaoqiang Han & Qian Cui & Ruiping Zheng & Shuying Li & Bingqian Zhou & Keke Fang & Wei Sheng & Baohong Wen & Liang Liu & Yarui Wei & Huafu Chen & Yuan Chen & Jingliang Cheng & Yong Zhang, 2023. "Parsing altered gray matter morphology of depression using a framework integrating the normative model and non-negative matrix factorization," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    13. Ayelet M. Rosenberg & Manish Saggar & Anna S. Monzel & Jack Devine & Peter Rogu & Aaron Limoges & Alex Junker & Carmen Sandi & Eugene V. Mosharov & Dani Dumitriu & Christoph Anacker & Martin Picard, 2023. "Brain mitochondrial diversity and network organization predict anxiety-like behavior in male mice," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    14. Carole Morel & Sarah E. Montgomery & Long Li & Romain Durand-de Cuttoli & Emily M. Teichman & Barbara Juarez & Nikos Tzavaras & Stacy M. Ku & Meghan E. Flanigan & Min Cai & Jessica J. Walsh & Scott J., 2022. "Midbrain projection to the basolateral amygdala encodes anxiety-like but not depression-like behaviors," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    15. 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.
    16. M. Agustina Frechou & Sunaina S. Martin & Kelsey D. McDermott & Evan A. Huaman & Şölen Gökhan & Wolfgang A. Tomé & Ruben Coen-Cagli & J. Tiago Gonçalves, 2024. "Adult neurogenesis improves spatial information encoding in the mouse hippocampus," Nature Communications, Nature, vol. 15(1), pages 1-14, 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_s41467-023-37736-x. 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.