IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-52466-4.html
   My bibliography  Save this article

Distinct ventral hippocampal inhibitory microcircuits regulating anxiety and fear behaviors

Author

Listed:
  • Kaizhen Li

    (University of Bern)

  • Konstantinos Koukoutselos

    (University of Bern)

  • Masanori Sakaguchi

    (University of Tsukuba)

  • Stéphane Ciocchi

    (University of Bern)

Abstract

In emotion research, anxiety and fear have always been interconnected, sharing overlapping brain structures and neural circuitry. Recent investigations, however, have unveiled parallel long-range projection pathways originating from the ventral hippocampus, shedding light on their distinct roles in anxiety and fear. Yet, the mechanisms governing the emergence of projection-specific activity patterns to mediate different negative emotions remain elusive. Here, we show a division of labor in local GABAergic inhibitory microcircuits of the ventral hippocampus, orchestrating the activity of subpopulations of pyramidal neurons to shape anxiety and fear behaviors in mice. These findings offer a comprehensive insight into how distinct inhibitory microcircuits are dynamically engaged to encode different emotional states.

Suggested Citation

  • Kaizhen Li & Konstantinos Koukoutselos & Masanori Sakaguchi & Stéphane Ciocchi, 2024. "Distinct ventral hippocampal inhibitory microcircuits regulating anxiety and fear behaviors," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52466-4
    DOI: 10.1038/s41467-024-52466-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-52466-4
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-52466-4?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. Jessica C. Jimenez & Jack E. Berry & Sean C. Lim & Samantha K. Ong & Mazen A. Kheirbek & Rene Hen, 2020. "Contextual fear memory retrieval by correlated ensembles of ventral CA1 neurons," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    2. Denise J. Cai & Daniel Aharoni & Tristan Shuman & Justin Shobe & Jeremy Biane & Weilin Song & Brandon Wei & Michael Veshkini & Mimi La-Vu & Jerry Lou & Sergio E. Flores & Isaac Kim & Yoshitake Sano & , 2016. "A shared neural ensemble links distinct contextual memories encoded close in time," Nature, Nature, vol. 534(7605), pages 115-118, June.
    3. Woong Bin Kim & Jun-Hyeong Cho, 2020. "Encoding of contextual fear memory in hippocampal–amygdala circuit," Nature Communications, Nature, vol. 11(1), pages 1-22, December.
    4. Hyun-Jae Pi & Balázs Hangya & Duda Kvitsiani & Joshua I. Sanders & Z. Josh Huang & Adam Kepecs, 2013. "Cortical interneurons that specialize in disinhibitory control," Nature, Nature, vol. 503(7477), pages 521-524, November.
    5. Sanja Mikulovic & Carlos Ernesto Restrepo & Samer Siwani & Pavol Bauer & Stefano Pupe & Adriano B. L. Tort & Klas Kullander & Richardson N. Leão, 2018. "Ventral hippocampal OLM cells control type 2 theta oscillations and response to predator odor," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    6. Candela Sánchez-Bellot & Rawan AlSubaie & Karyna Mishchanchuk & Ryan W. S. Wee & Andrew F. MacAskill, 2022. "Two opposing hippocampus to prefrontal cortex pathways for the control of approach and avoidance behaviour," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    7. Kay M. Tye & Rohit Prakash & Sung-Yon Kim & Lief E. Fenno & Logan Grosenick & Hosniya Zarabi & Kimberly R. Thompson & Viviana Gradinaru & Charu Ramakrishnan & Karl Deisseroth, 2011. "Amygdala circuitry mediating reversible and bidirectional control of anxiety," Nature, Nature, vol. 471(7338), pages 358-362, March.
    8. Benjamin F. Grewe & Jan Gründemann & Lacey J. Kitch & Jerome A. Lecoq & Jones G. Parker & Jesse D. Marshall & Margaret C. Larkin & Pablo E. Jercog & Francois Grenier & Jin Zhong Li & Andreas Lüthi & M, 2017. "Neural ensemble dynamics underlying a long-term associative memory," Nature, Nature, vol. 543(7647), pages 670-675, March.
    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. Masakazu Agetsuma & Issei Sato & Yasuhiro R. Tanaka & Luis Carrillo-Reid & Atsushi Kasai & Atsushi Noritake & Yoshiyuki Arai & Miki Yoshitomo & Takashi Inagaki & Hiroshi Yukawa & Hitoshi Hashimoto & J, 2023. "Activity-dependent organization of prefrontal hub-networks for associative learning and signal transformation," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    2. Anna J. Bowen & Y. Waterlily Huang & Jane Y. Chen & Jordan L. Pauli & Carlos A. Campos & Richard D. Palmiter, 2023. "Topographic representation of current and future threats in the mouse nociceptive amygdala," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Sorinel A Oprisan & Xandre Clementsmith & Tamas Tompa & Antonieta Lavin, 2019. "Dopamine receptor antagonists effects on low-dimensional attractors of local field potentials in optogenetic mice," PLOS ONE, Public Library of Science, vol. 14(10), pages 1-39, October.
    4. Panna Hegedüs & Bálint Király & Dániel Schlingloff & Victoria Lyakhova & Anna Velencei & Írisz Szabó & Márton I. Mayer & Zsofia Zelenak & Gábor Nyiri & Balázs Hangya, 2024. "Parvalbumin-expressing basal forebrain neurons mediate learning from negative experience," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    5. 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.
    6. Ren-Wen Han & Zi-Yi Zhang & Chen Jiao & Ze-Yu Hu & Bing-Xing Pan, 2024. "Synergism between two BLA-to-BNST pathways for appropriate expression of anxiety-like behaviors in male mice," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    7. Paul J. Lamothe-Molina & Andreas Franzelin & Lennart Beck & Dong Li & Lea Auksutat & Tim Fieblinger & Laura Laprell & Joachim Alhbeck & Christine E. Gee & Matthias Kneussel & Andreas K. Engel & Claus , 2022. "ΔFosB accumulation in hippocampal granule cells drives cFos pattern separation during spatial learning," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    8. Tristan G. Heintz & Antonio J. Hinojosa & Sina E. Dominiak & Leon Lagnado, 2022. "Opposite forms of adaptation in mouse visual cortex are controlled by distinct inhibitory microcircuits," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    9. Zhiwei Xu & Erez Geron & Luis M. Pérez-Cuesta & Yang Bai & Wen-Biao Gan, 2023. "Generalized extinction of fear memory depends on co-allocation of synaptic plasticity in dendrites," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    10. Nicholas Cole & Matthew Harvey & Dylan Myers-Joseph & Aditya Gilra & Adil G. Khan, 2024. "Prediction-error signals in anterior cingulate cortex drive task-switching," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    11. Mohamad Motaharinia & Kim Gerrow & Roobina Boghozian & Emily White & Sun-Eui Choi & Kerry R. Delaney & Craig E. Brown, 2021. "Longitudinal functional imaging of VIP interneurons reveals sup-population specific effects of stroke that are rescued with chemogenetic therapy," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    12. Akinobu Suzuki & Sakurako Kosugi & Emi Murayama & Eri Sasakawa & Noriaki Ohkawa & Ayumu Konno & Hirokazu Hirai & Kaoru Inokuchi, 2022. "A cortical cell ensemble in the posterior parietal cortex controls past experience-dependent memory updating," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    13. Shiri Shoob & Nadav Buchbinder & Ortal Shinikamin & Or Gold & Halit Baeloha & Tomer Langberg & Daniel Zarhin & Ilana Shapira & Gabriella Braun & Naomi Habib & Inna Slutsky, 2023. "Deep brain stimulation of thalamic nucleus reuniens promotes neuronal and cognitive resilience in an Alzheimer’s disease mouse model," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    14. Robert Legenstein & Wolfgang Maass, 2014. "Ensembles of Spiking Neurons with Noise Support Optimal Probabilistic Inference in a Dynamically Changing Environment," PLOS Computational Biology, Public Library of Science, vol. 10(10), pages 1-27, October.
    15. Thibault Cholvin & Marlene Bartos, 2022. "Hemisphere-specific spatial representation by hippocampal granule cells," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    16. Caio Vaz Rimoli & Claudio Moretti & Fernando Soldevila & Enora Brémont & Cathie Ventalon & Sylvain Gigan, 2024. "Demixing fluorescence time traces transmitted by multimode fibers," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    17. Heather C. Ratigan & Seetha Krishnan & Shai Smith & Mark E. J. Sheffield, 2023. "A thalamic-hippocampal CA1 signal for contextual fear memory suppression, extinction, and discrimination," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    18. Masanori Nomoto & Emi Murayama & Shuntaro Ohno & Reiko Okubo-Suzuki & Shin-ichi Muramatsu & Kaoru Inokuchi, 2022. "Hippocampus as a sorter and reverberatory integrator of sensory inputs," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    19. XiaoYuan Li & XiaoLi Yang & ZhongKui Sun, 2020. "Alpha rhythm slowing in a modified thalamo-cortico-thalamic model related with Alzheimer’s disease," PLOS ONE, Public Library of Science, vol. 15(3), pages 1-22, March.
    20. C. Nicolas & A. Ju & Y. Wu & H. Eldirdiri & S. Delcasso & Y. Couderc & C. Fornari & A. Mitra & L. Supiot & A. Vérité & M. Masson & S. Rodriguez-Rozada & D. Jacky & J. S. Wiegert & A. Beyeler, 2023. "Linking emotional valence and anxiety in a mouse insula-amygdala circuit," Nature Communications, Nature, vol. 14(1), pages 1-18, 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:15:y:2024:i:1:d:10.1038_s41467-024-52466-4. 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.