IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-35634-2.html
   My bibliography  Save this article

Parabrachial-to-parasubthalamic nucleus pathway mediates fear-induced suppression of feeding in male mice

Author

Listed:
  • Takashi Nagashima

    (The Jikei University School of Medicine)

  • Suguru Tohyama

    (The Jikei University School of Medicine)

  • Kaori Mikami

    (The Jikei University School of Medicine)

  • Masashi Nagase

    (The Jikei University School of Medicine)

  • Mieko Morishima

    (The Jikei University School of Medicine)

  • Atsushi Kasai

    (Graduate School of Pharmaceutical Sciences, Osaka University)

  • Hitoshi Hashimoto

    (Graduate School of Pharmaceutical Sciences, Osaka University
    Hamamatsu University School of Medicine, Chiba University, and University of Fukui
    Osaka University
    Osaka University)

  • Ayako M. Watabe

    (The Jikei University School of Medicine)

Abstract

Feeding behavior is adaptively regulated by external and internal environment, such that feeding is suppressed when animals experience pain, sickness, or fear. While the lateral parabrachial nucleus (lPB) plays key roles in nociception and stress, neuronal pathways involved in feeding suppression induced by fear are not fully explored. Here, we investigate the parasubthalamic nucleus (PSTN), located in the lateral hypothalamus and critically involved in feeding behaviors, as a target of lPB projection neurons. Optogenetic activation of lPB-PSTN terminals in male mice promote avoidance behaviors, aversive learning, and suppressed feeding. Inactivation of the PSTN and lPB-PSTN pathway reduces fear-induced feeding suppression. Activation of PSTN neurons expressing pituitary adenylate cyclase-activating polypeptide (PACAP), a neuropeptide enriched in the PSTN, is sufficient for inducing avoidance behaviors and feeding suppression. Blockade of PACAP receptors impaires aversive learning induced by lPB-PSTN photomanipulation. These findings indicate that lPB-PSTN pathway plays a pivotal role in fear-induced feeding suppression.

Suggested Citation

  • Takashi Nagashima & Suguru Tohyama & Kaori Mikami & Masashi Nagase & Mieko Morishima & Atsushi Kasai & Hitoshi Hashimoto & Ayako M. Watabe, 2022. "Parabrachial-to-parasubthalamic nucleus pathway mediates fear-induced suppression of feeding in male mice," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35634-2
    DOI: 10.1038/s41467-022-35634-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-35634-2
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-35634-2?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. Hikari Tanaka & Hidenori Homma & Kyota Fujita & Kanoh Kondo & Shingo Yamada & Xiaocen Jin & Masaaki Waragai & Gaku Ohtomo & Atsushi Iwata & Kazuhiko Tagawa & Naoki Atsuta & Masahisa Katsuno & Naoki To, 2020. "YAP-dependent necrosis occurs in early stages of Alzheimer’s disease and regulates mouse model pathology," Nature Communications, Nature, vol. 11(1), pages 1-22, December.
    2. Yong Wang & JungMin Kim & Matthew B. Schmit & Tiffany S. Cho & Caohui Fang & Haijiang Cai, 2019. "A bed nucleus of stria terminalis microcircuit regulating inflammation-associated modulation of feeding," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    3. Kerry J. Ressler & Kristina B. Mercer & Bekh Bradley & Tanja Jovanovic & Amy Mahan & Kimberly Kerley & Seth D. Norrholm & Varun Kilaru & Alicia K. Smith & Amanda J. Myers & Manuel Ramirez & Anzhelika , 2011. "Post-traumatic stress disorder is associated with PACAP and the PAC1 receptor," Nature, Nature, vol. 470(7335), pages 492-497, February.
    4. Ed S. Lein & Michael J. Hawrylycz & Nancy Ao & Mikael Ayres & Amy Bensinger & Amy Bernard & Andrew F. Boe & Mark S. Boguski & Kevin S. Brockway & Emi J. Byrnes & Lin Chen & Li Chen & Tsuey-Ming Chen &, 2007. "Genome-wide atlas of gene expression in the adult mouse brain," Nature, Nature, vol. 445(7124), pages 168-176, January.
    5. Carlos A. Campos & Anna J. Bowen & Carolyn W. Roman & Richard D. Palmiter, 2018. "Encoding of danger by parabrachial CGRP neurons," Nature, Nature, vol. 555(7698), pages 617-622, March.
    6. Michael J. Krashes & Bhavik P. Shah & Joseph C. Madara & David P. Olson & David E. Strochlic & Alastair S. Garfield & Linh Vong & Hongjuan Pei & Mitsuko Watabe-Uchida & Naoshige Uchida & Stephen D. Li, 2014. "An excitatory paraventricular nucleus to AgRP neuron circuit that drives hunger," Nature, Nature, vol. 507(7491), pages 238-242, March.
    7. Matthew E. Carter & Marta E. Soden & Larry S. Zweifel & Richard D. Palmiter, 2013. "Genetic identification of a neural circuit that suppresses appetite," Nature, Nature, vol. 503(7474), pages 111-114, November.
    8. Kerry J. Ressler & Kristina B. Mercer & Bekh Bradley & Tanja Jovanovic & Amy Mahan & Kimberly Kerley & Seth D. Norrholm & Varun Kilaru & Alicia K. Smith & Amanda J. Myers & Manuel Ramirez & Anzhelika , 2011. "Post-traumatic stress disorder is associated with PACAP and the PAC1 receptor," Nature, Nature, vol. 477(7362), pages 120-120, September.
    9. Deniz Atasoy & J. Nicholas Betley & Helen H. Su & Scott M. Sternson, 2012. "Deconstruction of a neural circuit for hunger," Nature, Nature, vol. 488(7410), pages 172-177, August.
    10. Dominic A. Evans & A. Vanessa Stempel & Ruben Vale & Sabine Ruehle & Yaara Lefler & Tiago Branco, 2018. "A synaptic threshold mechanism for computing escape decisions," Nature, Nature, vol. 558(7711), pages 590-594, June.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Qin Wang & Rui-Yue Sun & Jia-Xue Hu & Yan-Hui Sun & Chun-Yue Li & Huiqian Huang & Hao Wang & Xiao-Ming Li, 2024. "Hypothalamic-hindbrain circuit for consumption-induced fear regulation," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

    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. E. R. Velasco & A. Florido & Á Flores & E. Senabre & A. Gomez-Gomez & A. Torres & A. Roca & S. Norrholm & E. L. Newman & P. Das & R. A. Ross & A. Lori & O. J. Pozo & K. J. Ressler & L. L. Garcia-Estev, 2022. "PACAP-PAC1R modulates fear extinction via the ventromedial hypothalamus," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Devin Rocks & Mamta Shukla & Laila Ouldibbat & Silvia C. Finnemann & Achyuth Kalluchi & M. Jordan Rowley & Marija Kundakovic, 2022. "Sex-specific multi-level 3D genome dynamics in the mouse brain," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. Mingming Xing & Yang Li & Yuqi Zhang & Juemou Zhou & Danting Ma & Mengqi Zhang & Minglei Tang & Ting Ouyang & Fumiao Zhang & Xiaofeng Shi & Jianyuan Sun & Zuxin Chen & Weiping J. Zhang & Shuli Zhang &, 2024. "Paraventricular hypothalamic RUVBL2 neurons suppress appetite by enhancing excitatory synaptic transmission in distinct neurocircuits," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    4. 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.
    5. Morgan Heinzelmann & Jessica Gill, 2013. "Epigenetic Mechanisms Shape the Biological Response to Trauma and Risk for PTSD: A Critical Review," Nursing Research and Practice, Hindawi, vol. 2013, pages 1-10, April.
    6. Joseph W. Arthurs & Anna J. Bowen & Richard D. Palmiter & Nathan A. Baertsch, 2023. "Parabrachial tachykinin1-expressing neurons involved in state-dependent breathing control," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    7. Sekun Park & Anqi Zhu & Feng Cao & Richard D. Palmiter, 2024. "Parabrachial Calca neurons mediate second-order conditioning," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    8. S. Vickovic & B. Lötstedt & J. Klughammer & S. Mages & Å Segerstolpe & O. Rozenblatt-Rosen & A. Regev, 2022. "SM-Omics is an automated platform for high-throughput spatial multi-omics," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    9. Suma Chinta & Scott R. Pluta, 2023. "Neural mechanisms for the localization of unexpected external motion," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    10. Clément Solié & Alessandro Contestabile & Pedro Espinosa & Stefano Musardo & Sebastiano Bariselli & Chieko Huber & Alan Carleton & Camilla Bellone, 2022. "Superior Colliculus to VTA pathway controls orienting response and influences social interaction in mice," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    11. Xiaocen Jin & Hikari Tanaka & Meihua Jin & Kyota Fujita & Hidenori Homma & Maiko Inotsume & Huang Yong & Kenichi Umeda & Noriyuki Kodera & Toshio Ando & Hitoshi Okazawa, 2023. "PQBP5/NOL10 maintains and anchors the nucleolus under physiological and osmotic stress conditions," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    12. Jacob D Davidson & Ahmed El Hady, 2019. "Foraging as an evidence accumulation process," PLOS Computational Biology, Public Library of Science, vol. 15(7), pages 1-25, July.
    13. Léa J. Becker & Clémentine Fillinger & Robin Waegaert & Sarah H. Journée & Pierre Hener & Beyza Ayazgok & Muris Humo & Meltem Karatas & Maxime Thouaye & Mithil Gaikwad & Laetitia Degiorgis & Marie des, 2023. "The basolateral amygdala-anterior cingulate pathway contributes to depression-like behaviors and comorbidity with chronic pain behaviors in male mice," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    14. Ami Ritter & Shlomi Habusha & Lior Givon & Shahaf Edut & Oded Klavir, 2024. "Prefrontal control of superior colliculus modulates innate escape behavior following adversity," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    15. Wei Liu & Xu Liao & Ziye Luo & Yi Yang & Mai Chan Lau & Yuling Jiao & Xingjie Shi & Weiwei Zhai & Hongkai Ji & Joe Yeong & Jin Liu, 2023. "Probabilistic embedding, clustering, and alignment for integrating spatial transcriptomics data with PRECAST," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    16. Tingting Bo & Jie Li & Ganlu Hu & Ge Zhang & Wei Wang & Qian Lv & Shaoling Zhao & Junjie Ma & Meng Qin & Xiaohui Yao & Meiyun Wang & Guang-Zhong Wang & Zheng Wang, 2023. "Brain-wide and cell-specific transcriptomic insights into MRI-derived cortical morphology in macaque monkeys," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    17. Benjamin L. Walker & Qing Nie, 2023. "NeST: nested hierarchical structure identification in spatial transcriptomic data," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    18. Vincent Bazinet & Justine Y. Hansen & Reinder Vos de Wael & Boris C. Bernhardt & Martijn P. Heuvel & Bratislav Misic, 2023. "Assortative mixing in micro-architecturally annotated brain connectomes," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    19. Xiaomeng Wan & Jiashun Xiao & Sindy Sing Ting Tam & Mingxuan Cai & Ryohichi Sugimura & Yang Wang & Xiang Wan & Zhixiang Lin & Angela Ruohao Wu & Can Yang, 2023. "Integrating spatial and single-cell transcriptomics data using deep generative models with SpatialScope," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    20. Maxime Brunner & David Lopez-Rodriguez & Judith Estrada-Meza & Rafik Dali & Antoine Rohrbach & Tamara Deglise & Andrea Messina & Bernard Thorens & Federico Santoni & Fanny Langlet, 2024. "Fasting induces metabolic switches and spatial redistributions of lipid processing and neuronal interactions in tanycytes," Nature Communications, Nature, vol. 15(1), pages 1-19, 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:13:y:2022:i:1:d:10.1038_s41467-022-35634-2. 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.