IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-52727-2.html
   My bibliography  Save this article

Excitation-inhibition imbalance in medial preoptic area circuits underlies chronic stress-induced depression-like states

Author

Listed:
  • Can Tao

    (University of Southern California)

  • Guang-Wei Zhang

    (University of Southern California)

  • Wen-Jian Sun

    (University of Southern California)

  • Junxiang J. Huang

    (University of Southern California
    University of Southern California)

  • Li I. Zhang

    (University of Southern California
    University of Southern California)

  • Huizhong Whit Tao

    (University of Southern California
    University of Southern California)

Abstract

Dysregulation of brain homeostasis is associated with neuropsychiatric conditions such as major depressive disorder. However, underlying neural-circuit mechanisms remain not well-understood. We show in mice that chronic restraint stress (CRS) and social defeat stress (SDS) are both associated with disruption of excitation (E)-inhibition (I) balance, with increased E/I ratios, in medial preoptic area (MPOA) circuits, but through affecting different neuronal types. CRS results in elevated activity in glutamatergic neurons, and their suppression mitigates CRS-induced depressive-like behaviors. Paraventricular hypothalamic input to these neurons contributes to induction but not expression of depressive-like behaviors. Their projections to ventral tegmental area and periaqueductal gray/dorsal raphe suppress midbrain dopaminergic and serotonergic activity, respectively, and mediate expression of divergent depressive-like symptoms. By contrast, SDS results in reduced activity of GABAergic neurons, and their activation alleviates SDS-induced depressive-like behaviors. Thus, E/I imbalance with relatively increased excitation in MPOA circuits may be a general mechanism underlying depression caused by different etiological factors.

Suggested Citation

  • Can Tao & Guang-Wei Zhang & Wen-Jian Sun & Junxiang J. Huang & Li I. Zhang & Huizhong Whit Tao, 2024. "Excitation-inhibition imbalance in medial preoptic area circuits underlies chronic stress-induced depression-like states," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-52727-2
    DOI: 10.1038/s41467-024-52727-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-52727-2
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-52727-2?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. Dipesh Chaudhury & Jessica J. Walsh & Allyson K. Friedman & Barbara Juarez & Stacy M. Ku & Ja Wook Koo & Deveroux Ferguson & Hsing-Chen Tsai & Lisa Pomeranz & Daniel J. Christoffel & Alexander R. Nect, 2013. "Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons," Nature, Nature, vol. 493(7433), pages 532-536, January.
    2. Shinjae Chung & Franz Weber & Peng Zhong & Chan Lek Tan & Thuc Nghi Nguyen & Kevin T. Beier & Nikolai Hörmann & Wei-Cheng Chang & Zhe Zhang & Johnny Phong Do & Shenqin Yao & Michael J. Krashes & Bosil, 2017. "Identification of preoptic sleep neurons using retrograde labelling and gene profiling," Nature, Nature, vol. 545(7655), pages 477-481, May.
    3. Ofer Yizhar & Lief E. Fenno & Matthias Prigge & Franziska Schneider & Thomas J. Davidson & Daniel J. O’Shea & Vikaas S. Sohal & Inbal Goshen & Joel Finkelstein & Jeanne T. Paz & Katja Stehfest & Roman, 2011. "Neocortical excitation/inhibition balance in information processing and social dysfunction," Nature, Nature, vol. 477(7363), pages 171-178, September.
    4. Yi-Chao Wei & Shao-Ran Wang & Zhuo-Lei Jiao & Wen Zhang & Jun-Kai Lin & Xing-Yu Li & Shuai-Shuai Li & Xin Zhang & Xiao-Hong Xu, 2018. "Medial preoptic area in mice is capable of mediating sexually dimorphic behaviors regardless of gender," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    5. Johannes Kohl & Benedicte M. Babayan & Nimrod D. Rubinstein & Anita E. Autry & Brenda Marin-Rodriguez & Vikrant Kapoor & Kazunari Miyamishi & Larry S. Zweifel & Liqun Luo & Naoshige Uchida & Catherine, 2018. "Functional circuit architecture underlying parental behaviour," Nature, Nature, vol. 556(7701), pages 326-331, April.
    6. Zheng Wu & Anita E. Autry & Joseph F. Bergan & Mitsuko Watabe-Uchida & Catherine G. Dulac, 2014. "Galanin neurons in the medial preoptic area govern parental behaviour," Nature, Nature, vol. 509(7500), pages 325-330, May.
    7. Steve Ramirez & Xu Liu & Christopher J. MacDonald & Anthony Moffa & Joanne Zhou & Roger L. Redondo & Susumu Tonegawa, 2015. "Activating positive memory engrams suppresses depression-like behaviour," Nature, Nature, vol. 522(7556), pages 335-339, June.
    8. Yan Yang & Yihui Cui & Kangning Sang & Yiyan Dong & Zheyi Ni & Shuangshuang Ma & Hailan Hu, 2018. "Ketamine blocks bursting in the lateral habenula to rapidly relieve depression," Nature, Nature, vol. 554(7692), pages 317-322, February.
    9. Zhong Li & Bo Peng & Junxiang J. Huang & Yuan Zhang & Michelle B. Seo & Qi Fang & Guang-Wei Zhang & Xiaohui Zhang & Li I. Zhang & Huizhong Whit Tao, 2023. "Enhancement and contextual modulation of visuospatial processing by thalamocollicular projections from ventral lateral geniculate nucleus," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    10. Zhong Li & Jin-Xing Wei & Guang-Wei Zhang & Junxiang J. Huang & Brian Zingg & Xiyue Wang & Huizhong W. Tao & Li I. Zhang, 2021. "Corticostriatal control of defense behavior in mice induced by auditory looming cues," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    11. Li Shen & Guang-Wei Zhang & Can Tao & Michelle B. Seo & Nicole K. Zhang & Junxiang J. Huang & Li I. Zhang & Huizhong W. Tao, 2022. "A bottom-up reward pathway mediated by somatostatin neurons in the medial septum complex underlying appetitive learning," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    12. Kay M. Tye & Julie J. Mirzabekov & Melissa R. Warden & Emily A. Ferenczi & Hsing-Chen Tsai & Joel Finkelstein & Sung-Yon Kim & Avishek Adhikari & Kimberly R. Thompson & Aaron S. Andalman & Lisa A. Gun, 2013. "Dopamine neurons modulate neural encoding and expression of depression-related behaviour," Nature, Nature, vol. 493(7433), pages 537-541, January.
    13. Long Mei & Rongzhen Yan & Luping Yin & Regina M. Sullivan & Dayu Lin, 2023. "Antagonistic circuits mediating infanticide and maternal care in female mice," Nature, Nature, vol. 618(7967), pages 1006-1016, June.
    14. Melissa R. Warden & Aslihan Selimbeyoglu & Julie J. Mirzabekov & Maisie Lo & Kimberly R. Thompson & Sung-Yon Kim & Avishek Adhikari & Kay M. Tye & Loren M. Frank & Karl Deisseroth, 2012. "A prefrontal cortex–brainstem neuronal projection that controls response to behavioural challenge," Nature, Nature, vol. 492(7429), pages 428-432, December.
    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. Soo Hyun Yang & Esther Yang & Jaekwang Lee & Jin Yong Kim & Hyeijung Yoo & Hyung Sun Park & Jin Taek Jung & Dongmin Lee & Sungkun Chun & Yong Sang Jo & Gyeong Hee Pyeon & Jae-Yong Park & Hyun Woo Lee , 2023. "Neural mechanism of acute stress regulation by trace aminergic signalling in the lateral habenula in male mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Jeroen P. H. Verharen & Johannes W. Jong & Yichen Zhu & Stephan Lammel, 2023. "A computational analysis of mouse behavior in the sucrose preference test," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. Qingtao Sun & Jianping Zhang & Anan Li & Mei Yao & Guangcai Liu & Siqi Chen & Yue Luo & Zhi Wang & Hui Gong & Xiangning Li & Qingming Luo, 2022. "Acetylcholine deficiency disrupts extratelencephalic projection neurons in the prefrontal cortex in a mouse model of Alzheimer’s disease," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    4. 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.
    5. Jing Huang & Weijun Huang & Junzhe Yi & Yiwen Deng & Ruijie Li & Jieying Chen & Jiahao Shi & Yuan Qiu & Tao Wang & Xiaoyong Chen & Xiaoran Zhang & Andy Peng Xiang, 2023. "Mesenchymal stromal cells alleviate depressive and anxiety-like behaviors via a lung vagal-to-brain axis in male mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    6. Weiping Dai & Mengqian Yang & Pei Xia & Chuan Xiao & Shuying Huang & Zhan Zhang & Xin Cheng & Wenchang Li & Jian Jin & Jingyun Zhang & Binghuo Wu & Yingying Zhang & Pei-hui Wu & Yangyang Lin & Wen Wu , 2022. "A functional role of meningeal lymphatics in sex difference of stress susceptibility in mice," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    7. Zhong Li & Bo Peng & Junxiang J. Huang & Yuan Zhang & Michelle B. Seo & Qi Fang & Guang-Wei Zhang & Xiaohui Zhang & Li I. Zhang & Huizhong Whit Tao, 2023. "Enhancement and contextual modulation of visuospatial processing by thalamocollicular projections from ventral lateral geniculate nucleus," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    8. Elyashiv Zangen & Shira Hadar & Christopher Lawrence & Mustafa Obeid & Hala Rasras & Ella Hanzin & Ori Aslan & Eyal Zur & Nadav Schulcz & Daniel Cohen-Hatab & Yona Samama & Sarah Nir & Yi Li & Irina D, 2024. "Prefrontal cortex neurons encode ambient light intensity differentially across regions and layers," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    9. Radhika Rawat & Elif Tunc-Ozcan & Tammy L. McGuire & Chian-Yu Peng & John A. Kessler, 2022. "Ketamine activates adult-born immature granule neurons to rapidly alleviate depression-like behaviors in mice," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    10. 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.
    11. Shuancheng Ren & Cai Zhang & Faguo Yue & Jinxiang Tang & Wei Zhang & Yue Zheng & Yuanyuan Fang & Na Wang & Zhenbo Song & Zehui Zhang & Xiaolong Zhang & Han Qin & Yaling Wang & Jianxia Xia & Chenggang , 2024. "A midbrain GABAergic circuit constrains wakefulness in a mouse model of stress," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    12. Alexandre Castonguay & Sébastien Thomas & Frédéric Lesage & Christian Casanova, 2014. "Repetitive and Retinotopically Restricted Activation of the Dorsal Lateral Geniculate Nucleus with Optogenetics," PLOS ONE, Public Library of Science, vol. 9(4), pages 1-8, April.
    13. Giulia Faini & Dimitrii Tanese & Clément Molinier & Cécile Telliez & Massilia Hamdani & Francois Blot & Christophe Tourain & Vincent Sars & Filippo Bene & Benoît C. Forget & Emiliano Ronzitti & Valent, 2023. "Ultrafast light targeting for high-throughput precise control of neuronal networks," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    14. Brandon W. Hughes & Jessica L. Huebschman & Evgeny Tsvetkov & Benjamin M. Siemsen & Kirsten K. Snyder & Rose Marie Akiki & Daniel J. Wood & Rachel D. Penrod & Michael D. Scofield & Stefano Berto & Mak, 2024. "NPAS4 supports cocaine-conditioned cues in rodents by controlling the cell type-specific activation balance in the nucleus accumbens," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    15. Jun Wang & Qian Yang & Xue Liu & Jie Li & Ya-Lan Wen & Yuzheng Hu & Tian-Le Xu & Shumin Duan & Han Xu, 2024. "The basal forebrain to lateral habenula circuitry mediates social behavioral maladaptation," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    16. Grace Png & Andrei Barysenka & Linda Repetto & Pau Navarro & Xia Shen & Maik Pietzner & Eleanor Wheeler & Nicholas J. Wareham & Claudia Langenberg & Emmanouil Tsafantakis & Maria Karaleftheri & George, 2021. "Mapping the serum proteome to neurological diseases using whole genome sequencing," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    17. Gregory Lepeu & Ellen Maren & Kristina Slabeva & Cecilia Friedrichs-Maeder & Markus Fuchs & Werner J. Z’Graggen & Claudio Pollo & Kaspar A. Schindler & Antoine Adamantidis & Timothée Proix & Maxime O., 2024. "The critical dynamics of hippocampal seizures," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    18. Pan Xu & Yuanlei Yue & Juntao Su & Xiaoqian Sun & Hongfei Du & Zhichao Liu & Rahul Simha & Jianhui Zhou & Chen Zeng & Hui Lu, 2022. "Pattern decorrelation in the mouse medial prefrontal cortex enables social preference and requires MeCP2," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    19. Yu-Jun Wang & Gui-Ying Zan & Cenglin Xu & Xue-Ping Li & Xuelian Shu & Song-Yu Yao & Xiao-Shan Xu & Xiaoyun Qiu & Yexiang Chen & Kai Jin & Qi-Xin Zhou & Jia-Yu Ye & Yi Wang & Lin Xu & Zhong Chen & Jing, 2023. "The claustrum-prelimbic cortex circuit through dynorphin/κ-opioid receptor signaling underlies depression-like behaviors associated with social stress etiology," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    20. Zhang, Xu & Min, Fuhong & Dou, Yiping & Xu, Yeyin, 2023. "Bifurcation analysis of a modified FitzHugh-Nagumo neuron with electric field," Chaos, Solitons & Fractals, Elsevier, vol. 170(C).

    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_s41467-024-52727-2. 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.