IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38685-1.html
   My bibliography  Save this article

Multisite regulation integrates multimodal context in sensory circuits to control persistent behavioral states in C. elegans

Author

Listed:
  • Saurabh Thapliyal

    (University of Fribourg)

  • Isabel Beets

    (Department of Biology, KU Leuven)

  • Dominique A. Glauser

    (University of Fribourg)

Abstract

Maintaining or shifting between behavioral states according to context is essential for animals to implement fitness-promoting strategies. How the integration of internal state, past experience and sensory inputs orchestrates persistent multidimensional behavioral changes remains poorly understood. Here, we show that C. elegans integrates environmental temperature and food availability over different timescales to engage in persistent dwelling, scanning, global or glocal search strategies matching thermoregulatory and feeding needs. Transition between states, in each case, involves regulating multiple processes including AFD or FLP tonic sensory neurons activity, neuropeptide expression and downstream circuit responsiveness. State-specific FLP-6 or FLP-5 neuropeptide signaling acts on a distributed set of inhibitory GPCR(s) to promote scanning or glocal search, respectively, bypassing dopamine and glutamate-dependent behavioral state control. Integration of multimodal context via multisite regulation in sensory circuits might represent a conserved regulatory logic for a flexible prioritization on the valence of multiple inputs when operating persistent behavioral state transitions.

Suggested Citation

  • Saurabh Thapliyal & Isabel Beets & Dominique A. Glauser, 2023. "Multisite regulation integrates multimodal context in sensory circuits to control persistent behavioral states in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38685-1
    DOI: 10.1038/s41467-023-38685-1
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38685-1
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-38685-1?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. David M. Raizen & John E. Zimmerman & Matthew H. Maycock & Uyen D. Ta & Young-jai You & Meera V. Sundaram & Allan I. Pack, 2008. "Erratum: Lethargus is a Caenorhabditis elegans sleep-like state," Nature, Nature, vol. 453(7197), pages 952-952, June.
    2. Paul J. Shaw & Giulio Tononi & Ralph J. Greenspan & Donald F. Robinson, 2002. "Stress response genes protect against lethal effects of sleep deprivation in Drosophila," Nature, Nature, vol. 417(6886), pages 287-291, May.
    3. Thomas Gallagher & Theresa Bjorness & Robert Greene & Young-Jai You & Leon Avery, 2013. "The Geometry of Locomotive Behavioral States in C. elegans," PLOS ONE, Public Library of Science, vol. 8(3), pages 1-19, March.
    4. Lisa C. Schild & Dominique A. Glauser, 2013. "Dynamic switching between escape and avoidance regimes reduces Caenorhabditis elegans exposure to noxious heat," Nature Communications, Nature, vol. 4(1), pages 1-11, October.
    5. Yong S. Jo & Vijay Mohan K. Namboodiri & Garret D. Stuber & Larry S. Zweifel, 2020. "Persistent activation of central amygdala CRF neurons helps drive the immediate fear extinction deficit," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    6. Raoul Belzeaux & Victor Gorgievski & Laura M. Fiori & Juan Pablo Lopez & Julien Grenier & Rixing Lin & Corina Nagy & El Chérif Ibrahim & Eduardo Gascon & Philippe Courtet & Stéphane Richard-Devantoy &, 2020. "GPR56/ADGRG1 is associated with response to antidepressant treatment," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    7. Ping Liu & Bojun Chen & Zhao-Wen Wang, 2020. "GABAergic motor neurons bias locomotor decision-making in C. elegans," Nature Communications, Nature, vol. 11(1), pages 1-19, December.
    8. Jesse M. Gray & David S. Karow & Hang Lu & Andy J. Chang & Jennifer S. Chang & Ronald E. Ellis & Michael A. Marletta & Cornelia I. Bargmann, 2004. "Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue," Nature, Nature, vol. 430(6997), pages 317-322, July.
    9. David M. Raizen & John E. Zimmerman & Matthew H. Maycock & Uyen D. Ta & Young-jai You & Meera V. Sundaram & Allan I. Pack, 2008. "Lethargus is a Caenorhabditis elegans sleep-like state," Nature, Nature, vol. 451(7178), pages 569-572, January.
    10. Céline N Martineau & André E X Brown & Patrick Laurent, 2020. "Multidimensional phenotyping predicts lifespan and quantifies health in Caenorhabditis elegans," PLOS Computational Biology, Public Library of Science, vol. 16(7), pages 1-14, July.
    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. Drew Benjamin Sinha & Zachary Scott Pincus, 2022. "High temporal resolution measurements of movement reveal novel early-life physiological decline in C. elegans," PLOS ONE, Public Library of Science, vol. 17(2), pages 1-17, February.
    2. Yael Korem & Pablo Szekely & Yuval Hart & Hila Sheftel & Jean Hausser & Avi Mayo & Michael E Rothenberg & Tomer Kalisky & Uri Alon, 2015. "Geometry of the Gene Expression Space of Individual Cells," PLOS Computational Biology, Public Library of Science, vol. 11(7), pages 1-27, July.
    3. Amelie C. F. Bergs & Jana F. Liewald & Silvia Rodriguez-Rozada & Qiang Liu & Christin Wirt & Artur Bessel & Nadja Zeitzschel & Hilal Durmaz & Adrianna Nozownik & Holger Dill & Maëlle Jospin & Johannes, 2023. "All-optical closed-loop voltage clamp for precise control of muscles and neurons in live animals," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    4. Xu Zhan & Chao Chen & Longgang Niu & Xinran Du & Ying Lei & Rui Dan & Zhao-Wen Wang & Ping Liu, 2023. "Locomotion modulates olfactory learning through proprioception in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    5. Chenxi Lin & Yuxin Shan & Zhongyi Wang & Hui Peng & Rong Li & Pingzhou Wang & Junyan He & Weiwei Shen & Zhengxing Wu & Min Guo, 2024. "Molecular and circuit mechanisms underlying avoidance of rapid cooling stimuli in C. elegans," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    6. Matthew T. Birnie & Annabel K. Short & Gregory B. Carvalho & Lara Taniguchi & Benjamin G. Gunn & Aidan L. Pham & Christy A. Itoga & Xiangmin Xu & Lulu Y. Chen & Stephen V. Mahler & Yuncai Chen & Talli, 2023. "Stress-induced plasticity of a CRH/GABA projection disrupts reward behaviors in mice," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    7. Yan-Ying Wang & Wei-Wei Ma & I-Feng Peng, 2020. "Screening of sleep assisting drug candidates with a Drosophila model," PLOS ONE, Public Library of Science, vol. 15(7), pages 1-17, July.
    8. Kan Xie & Helmut Fuchs & Enzo Scifo & Dan Liu & Ahmad Aziz & Juan Antonio Aguilar-Pimentel & Oana Veronica Amarie & Lore Becker & Patricia da Silva-Buttkus & Julia Calzada-Wack & Yi-Li Cho & Yushuang , 2022. "Deep phenotyping and lifetime trajectories reveal limited effects of longevity regulators on the aging process in C57BL/6J mice," Nature Communications, Nature, vol. 13(1), pages 1-29, 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_s41467-023-38685-1. 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.