IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38180-7.html
   My bibliography  Save this article

Neural mechanism of acute stress regulation by trace aminergic signalling in the lateral habenula in male mice

Author

Listed:
  • Soo Hyun Yang

    (Korea University)

  • Esther Yang

    (Korea University)

  • Jaekwang Lee

    (Korea Food Research Institute)

  • Jin Yong Kim

    (Korea University)

  • Hyeijung Yoo

    (Korea University)

  • Hyung Sun Park

    (Korea University)

  • Jin Taek Jung

    (Korea University)

  • Dongmin Lee

    (Korea University)

  • Sungkun Chun

    (Jeonbuk National University Medical School)

  • Yong Sang Jo

    (Korea University)

  • Gyeong Hee Pyeon

    (Korea University)

  • Jae-Yong Park

    (Graduate School, Korea University)

  • Hyun Woo Lee

    (Korea University)

  • Hyun Kim

    (Korea University)

Abstract

Stress management is necessary for vertebrate survival. Chronic stress drives depression by excitation of the lateral habenula (LHb), which silences dopaminergic neurons in the ventral tegmental area (VTA) via GABAergic neuronal projection from the rostromedial tegmental nucleus (RMTg). However, the effect of acute stress on this LHb-RMTg-VTA pathway is not clearly understood. Here, we used fluorescent in situ hybridisation and in vivo electrophysiology in mice to show that LHb aromatic l-amino acid decarboxylase-expressing neurons (D-neurons) are activated by acute stressors and suppress RMTg GABAergic neurons via trace aminergic signalling, thus activating VTA dopaminergic neurons. We show that the LHb regulates RMTg GABAergic neurons biphasically under acute stress. This study, carried out on male mice, has elucidated a molecular mechanism in the efferent LHb-RMTg-VTA pathway whereby trace aminergic signalling enables the brain to manage acute stress by preventing the hypoactivity of VTA dopaminergic neurons.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38180-7
    DOI: 10.1038/s41467-023-38180-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38180-7
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-38180-7?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. 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.
    3. Masayuki Matsumoto & Okihide Hikosaka, 2007. "Lateral habenula as a source of negative reward signals in dopamine neurons," Nature, Nature, vol. 447(7148), pages 1111-1115, June.
    4. Yihui Cui & Yan Yang & Zheyi Ni & Yiyan Dong & Guohong Cai & Alexandre Foncelle & Shuangshuang Ma & Kangning Sang & Siyang Tang & Yuezhou Li & Ying Shen & Hugues Berry & Shengxi Wu & Hailan Hu, 2018. "Astroglial Kir4.1 in the lateral habenula drives neuronal bursts in depression," Nature, Nature, vol. 554(7692), pages 323-327, February.
    5. 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.
    6. Paul Leon Brown & Paul D Shepard, 2013. "Lesions of the Fasciculus Retroflexus Alter Footshock-Induced cFos Expression in the Mesopontine Rostromedial Tegmental Area of Rats," PLOS ONE, Public Library of Science, vol. 8(4), pages 1-9, 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. Shannon Trombley & Jackson Powell & Pavithran Guttipatti & Andrew Matamoros & Xiaohui Lin & Tristan O’Harrow & Tobias Steinschaden & Leann Miles & Qin Wang & Shuchao Wang & Jingyun Qiu & Qingyang Li &, 2023. "Glia instruct axon regeneration via a ternary modulation of neuronal calcium channels in Drosophila," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    2. Muran Wang & Peijun Li & Zewen Li & Beatriz S. Silva & Wu Zheng & Zhenghua Xiang & Yan He & Tao Xu & Cristina Cordeiro & Lu Deng & Yuwei Dai & Mengqian Ye & Zhiqing Lin & Jianhong Zhou & Xuzhao Zhou &, 2023. "Lateral septum adenosine A2A receptors control stress-induced depressive-like behaviors via signaling to the hypothalamus and habenula," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    3. Shan Yao & Min-Dong Xu & Ying Wang & Shen-Ting Zhao & Jin Wang & Gui-Fu Chen & Wen-Bing Chen & Jian Liu & Guo-Bin Huang & Wen-Juan Sun & Yan-Yan Zhang & Huan-Li Hou & Lei Li & Xiang-Dong Sun, 2023. "Astrocytic lactate dehydrogenase A regulates neuronal excitability and depressive-like behaviors through lactate homeostasis in mice," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. 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.
    5. 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.
    6. Francis Kei Masuda & Emily A. Aery Jones & Yanjun Sun & Lisa M. Giocomo, 2023. "Ketamine evoked disruption of entorhinal and hippocampal spatial maps," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    7. 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.
    8. 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.
    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. Hiroyuki Kawai & Youcef Bouchekioua & Naoya Nishitani & Kazuhei Niitani & Shoma Izumi & Hinako Morishita & Chihiro Andoh & Yuma Nagai & Masashi Koda & Masako Hagiwara & Koji Toda & Hisashi Shirakawa &, 2022. "Median raphe serotonergic neurons projecting to the interpeduncular nucleus control preference and aversion," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    12. 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.
    13. Yun-Feng Zhang & Jialiang Wu & Yingqi Wang & Natalie L. Johnson & Janardhan P. Bhattarai & Guanqing Li & Wenqiang Wang & Camilo Guevara & Hannah Shoenhard & Marc V. Fuccillo & Daniel W. Wesson & Mingh, 2023. "Ventral striatal islands of Calleja neurons bidirectionally mediate depression-like behaviors in mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    14. Tommaso Ianni & Sedona N. Ewbank & Marjorie R. Levinstein & Matine M. Azadian & Reece C. Budinich & Michael Michaelides & Raag D. Airan, 2024. "Sex dependence of opioid-mediated responses to subanesthetic ketamine in rats," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    15. Andrew Jo & Sercan Deniz & Jian Xu & Robert M. Duvoisin & Steven H. DeVries & Yongling Zhu, 2023. "A sign-inverted receptive field of inhibitory interneurons provides a pathway for ON-OFF interactions in the retina," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    16. Maggie W. Waung & Kayla A. Maanum & Thomas J. Cirino & Joseph R. Driscoll & Chris O’Brien & Svetlana Bryant & Kasra A. Mansourian & Marisela Morales & David J. Barker & Elyssa B. Margolis, 2022. "A diencephalic circuit in rats for opioid analgesia but not positive reinforcement," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    17. Danijela Bataveljic & Helena Pivonkova & Vidian de Concini & Betty Hébert & Pascal Ezan & Sylvain Briault & Alexis-Pierre Bemelmans & Jacques Pichon & Arnaud Menuet & Nathalie Rouach, 2024. "Astroglial Kir4.1 potassium channel deficit drives neuronal hyperexcitability and behavioral defects in Fragile X syndrome mouse model," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    18. Robert C Wilson & Matthew R Nassar & Joshua I Gold, 2013. "A Mixture of Delta-Rules Approximation to Bayesian Inference in Change-Point Problems," PLOS Computational Biology, Public Library of Science, vol. 9(7), pages 1-18, July.
    19. Wang, Xianjun & Gu, Huaguang & Jia, Yanbing, 2023. "Nonlinear mechanism for enhanced and reduced bursting activity respectively induced by fast and slow excitatory autapse," Chaos, Solitons & Fractals, Elsevier, vol. 166(C).
    20. Robyn Mary Brown & Jennifer Lynn Short & Andrew John Lawrence, 2010. "Identification of Brain Nuclei Implicated in Cocaine-Primed Reinstatement of Conditioned Place Preference: A Behaviour Dissociable from Sensitization," PLOS ONE, Public Library of Science, vol. 5(12), pages 1-13, 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_s41467-023-38180-7. 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.