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Decoding a neural circuit controlling global animal state in C. elegans

  1. Patrick Laurent
  2. Zoltan Soltesz
  3. Geoff Nelson
  4. Changchun Chen
  5. Fausto Arellano-Carbajal
  6. Emmanuel Levy
  7. Mario de Bono  Is a corresponding author
  1. Laboratory of Molecular Biology, United Kingdom
  2. Universidad Autonoma de Queretaro, United Kingdom
  3. Weizmann Institute of Science, Israel
Research Article
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Cite this article as: eLife 2015;4:e04241 doi: 10.7554/eLife.04241

Abstract

Brains organize behavior and physiology to optimize the response to threats or opportunities. We dissect how 21% O2, an indicator of surface exposure, reprograms C. elegans' global state, inducing sustained locomotory arousal and altering expression of neuropeptides, metabolic enzymes, and other non-neural genes. The URX O2-sensing neurons drive arousal at 21% O2 by tonically activating the RMG interneurons. Stimulating RMG is sufficient to switch behavioral state. Ablating the ASH, ADL or ASK sensory neurons connected to RMG by gap junctions does not disrupt arousal. However, disrupting cation currents in these neurons curtails RMG neurosecretion and arousal. RMG signals high O2 by peptidergic secretion. Neuropeptide reporters reveal neural circuit state, as neurosecretion stimulates neuropeptide expression. Neural imaging in unrestrained animals shows that URX and RMG encode O2 concentration rather than behavior, while the activity of downstream interneurons such as AVB and AIY reflect both O2 levels and the behavior being executed.

Article and author information

Author details

  1. Patrick Laurent

    Laboratory of Molecular Biology, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Zoltan Soltesz

    Laboratory of Molecular Biology, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Geoff Nelson

    Laboratory of Molecular Biology, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Changchun Chen

    Laboratory of Molecular Biology, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Fausto Arellano-Carbajal

    School of Natural Science, Universidad Autonoma de Queretaro, Santiago de Querétaro, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Emmanuel Levy

    Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
  7. Mario de Bono

    Laboratory of Molecular Biology, Cambridge, United Kingdom
    For correspondence
    debono@mrc-lmb.cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Graeme W Davis, University of California, San Francisco, United States

Publication history

  1. Received: August 4, 2014
  2. Accepted: March 10, 2015
  3. Accepted Manuscript published: March 11, 2015 (version 1)
  4. Version of Record published: May 22, 2015 (version 2)

Copyright

© 2015, Laurent et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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