A conserved neuropeptide system links head and body motor circuits to enable adaptive behavior

  1. Shankar Ramachandran
  2. Navonil Banerjee
  3. Raja Bhattacharya
  4. Michele L Lemons
  5. Jeremy Florman
  6. Christopher M Lambert
  7. Denis Touroutine
  8. Kellianne Alexander
  9. Liliane Schoofs
  10. Mark J Alkema
  11. Isabel Beets
  12. Michael M Francis  Is a corresponding author
  1. University of Massachusetts Medical School, United States
  2. Assumption University, United States
  3. University of Massachusetts Chan Medical School, United States
  4. University of Leuven (KU Leuven), Belgium

Abstract

Neuromodulators promote adaptive behaviors that are often complex and involve concerted activity changes across circuits that are often not physically connected. It is not well understood how neuromodulatory systems accomplish these tasks. Here we show that the C. elegans NLP-12 neuropeptide system shapes responses to food availability by modulating the activity of head and body wall motor neurons through alternate G-protein coupled receptor (GPCR) targets, CKR-1 and CKR-2. We show ckr-2 deletion reduces body bend depth during movement under basal conditions. We demonstrate CKR-1 is a functional NLP-12 receptor and define its expression in the nervous system. In contrast to basal locomotion, biased CKR-1 GPCR stimulation of head motor neurons promotes turning during local searching. Deletion of ckr-1 reduces head neuron activity and diminishes turning while specific ckr-1 overexpression or head neuron activation promote turning. Thus, our studies suggest locomotor responses to changing food availability are regulated through conditional NLP-12 stimulation of head or body wall motor circuits.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files; source data files are provided as supplemental files.

Article and author information

Author details

  1. Shankar Ramachandran

    Neurobiology, University of Massachusetts Medical School, Worcester, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Navonil Banerjee

    Department of Neurobiology, University of Massachusetts Medical School, Worcester, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Raja Bhattacharya

    Department of Neurobiology, University of Massachusetts Medical School, Worcester, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Michele L Lemons

    Biological and Physical Sciences, Assumption University, Worcester, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8459-4130
  5. Jeremy Florman

    Neurobiology, University of Massachusetts Medical School, Worcester, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7578-3511
  6. Christopher M Lambert

    Neurobiology, University of Massachusetts Medical School, Worcester, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Denis Touroutine

    Department of Neurobiology, University of Massachusetts Medical School, Worcester, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Kellianne Alexander

    University of Massachusetts Chan Medical School, Worcester, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Liliane Schoofs

    University of Leuven (KU Leuven), Leuven, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  10. Mark J Alkema

    Department of Neurobiology, University of Massachusetts Medical School, Worcester, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1311-5179
  11. Isabel Beets

    University of Leuven (KU Leuven), Leuven, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  12. Michael M Francis

    University of Massachusetts Chan Medical School, Worcester, United States
    For correspondence
    michael.francis@umassmed.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8076-6668

Funding

NIH (R21NS093492)

  • Michael M Francis

European Research Council (340318)

  • Isabel Beets

Research Foundation Flanders Grant (G0C0618N)

  • Isabel Beets

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Manuel Zimmer, University of Vienna, Austria

Version history

  1. Preprint posted: April 28, 2020 (view preprint)
  2. Received: June 28, 2021
  3. Accepted: November 11, 2021
  4. Accepted Manuscript published: November 12, 2021 (version 1)
  5. Version of Record published: November 26, 2021 (version 2)

Copyright

© 2021, Ramachandran 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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  1. Shankar Ramachandran
  2. Navonil Banerjee
  3. Raja Bhattacharya
  4. Michele L Lemons
  5. Jeremy Florman
  6. Christopher M Lambert
  7. Denis Touroutine
  8. Kellianne Alexander
  9. Liliane Schoofs
  10. Mark J Alkema
  11. Isabel Beets
  12. Michael M Francis
(2021)
A conserved neuropeptide system links head and body motor circuits to enable adaptive behavior
eLife 10:e71747.
https://doi.org/10.7554/eLife.71747

Share this article

https://doi.org/10.7554/eLife.71747

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