Whole-organism behavioral profiling reveals a role for dopamine in state-dependent motor program coupling in C. elegans

  1. Nathan Cermak
  2. Stephanie K Yu
  3. Rebekah Clark
  4. Yung-Chi Huang
  5. Saba N Baskoylu
  6. Steven Flavell  Is a corresponding author
  1. Massachusetts Institute of Technology, United States

Abstract

Animal behaviors are commonly organized into long-lasting states that coordinately impact the generation of diverse motor outputs such as feeding, locomotion, and grooming. However, the neural mechanisms that coordinate these diverse motor programs remain poorly understood. Here, we examine how the distinct motor programs of the nematode C. elegans are coupled together across behavioral states. We describe a new imaging platform that permits automated, simultaneous quantification of each of the main C. elegans motor programs over hours or days. Analysis of these whole-organism behavioral profiles shows that the motor programs coordinately change as animals switch behavioral states. Utilizing genetics, optogenetics, and calcium imaging, we identify a new role for dopamine in coupling locomotion and egg-laying together across states. These results provide new insights into how the diverse motor programs throughout an organism are coordinated and suggest that neuromodulators like dopamine can couple motor circuits together in a state-dependent manner.

Data availability

Data have been uploaded to Dryad (doi:10.5061/dryad.t4b8gthzf) and are publicly available

The following data sets were generated

Article and author information

Author details

  1. Nathan Cermak

    Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Stephanie K Yu

    Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Rebekah Clark

    Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Yung-Chi Huang

    Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Saba N Baskoylu

    Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Steven Flavell

    Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, United States
    For correspondence
    flavell@mit.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9464-1877

Funding

National Science Foundation (IOS 1845663)

  • Steven Flavell

National Science Foundation (DUE 1845663)

  • Steven Flavell

National Institutes of Health (NS104892)

  • Steven Flavell

JPB Foundation (PIIF,PNDRF)

  • Steven Flavell

Brain and Behavior Research Foundation (NARSAD Young Investigator)

  • Steven Flavell

JPB Foundation (Picower Fellows Award)

  • Yung-Chi Huang

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, Research Institute of Molecular Pathology, Vienna Biocenter and University of Vienna, Austria

Version history

  1. Received: March 20, 2020
  2. Accepted: June 7, 2020
  3. Accepted Manuscript published: June 8, 2020 (version 1)
  4. Version of Record published: July 9, 2020 (version 2)

Copyright

© 2020, Cermak 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. Nathan Cermak
  2. Stephanie K Yu
  3. Rebekah Clark
  4. Yung-Chi Huang
  5. Saba N Baskoylu
  6. Steven Flavell
(2020)
Whole-organism behavioral profiling reveals a role for dopamine in state-dependent motor program coupling in C. elegans
eLife 9:e57093.
https://doi.org/10.7554/eLife.57093

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https://doi.org/10.7554/eLife.57093

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