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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
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    References listed on IDEAS

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    1. 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.
    2. 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.
    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. 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.
    5. Vaishnav Krishnan & Eric J. Nestler, 2008. "The molecular neurobiology of depression," Nature, Nature, vol. 455(7215), pages 894-902, October.
    6. 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.
    7. 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.
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