Corollary discharge promotes a sustained motor state in a neural circuit for navigation

  1. Ni Ji
  2. Vivek Venkatachalam
  3. Hillary Denise Rodgers
  4. Wesley Hung
  5. Taizo Kawano
  6. Christopher M Clark
  7. Maria Lim
  8. Mark J Alkema  Is a corresponding author
  9. Mei Zhen  Is a corresponding author
  10. Aravinthan DT Samuel  Is a corresponding author
  1. Harvard University, United States
  2. Mount Sinai Hospital, Canada
  3. University of Massachusetts Medical School, United States

Abstract

Animals exhibit behavioral and neural responses that persist on longer time scales than transient or fluctuating stimulus inputs. Here, we report that C. elegans uses feedback from the motor circuit to a sensory processing interneuron to sustain its motor state during thermotactic navigation. By imaging circuit activity in behaving animals, we show that a principal postsynaptic partner of the AFD thermosensory neuron, the AIY interneuron, encodes both temperature and motor state information. By optogenetic and genetic manipulation of this circuit, we demonstrate that the motor state representation in AIY is a corollary discharge signal. RIM, an interneuron that is connected with premotor interneurons, is required for this corollary discharge. Ablation of RIM eliminates the motor representation in AIY, allows thermosensory representations to reach downstream premotor interneurons, and reduces the animal's ability to sustain forward movements during thermotaxis. We propose that feedback from the motor circuit to the sensory processing circuit underlies a positive feedback mechanism to generate persistent neural activity and sustained behavioral patterns in a sensorimotor transformation.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 1-6. Source code has been provided for Figure 7.

Article and author information

Author details

  1. Ni Ji

    Physics, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Vivek Venkatachalam

    Physics, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2414-7416
  3. Hillary Denise Rodgers

    Department of Physics and Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0565-1940
  4. Wesley Hung

    Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Taizo Kawano

    Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  6. Christopher M Clark

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

    Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  8. Mark J Alkema

    Department of Neurobiology, University of Massachusetts Medical School, Worcester, United States
    For correspondence
    mark.alkema@umassmed.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1311-5179
  9. Mei Zhen

    Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Canada
    For correspondence
    meizhen@lunenfeld.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0086-9622
  10. Aravinthan DT Samuel

    Physics, Harvard University, Cambridge, United States
    For correspondence
    samuel@physics.harvard.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1672-8720

Funding

National Institute of Neurological Disorders and Stroke (NS082525-01A1)

  • Aravinthan DT Samuel

National Institute of General Medical Sciences (PO1 GM103770)

  • Aravinthan DT Samuel

National Institute of General Medical Sciences (RO1 GM084491)

  • Mark J Alkema

Burroughs Wellcome Fund

  • Vivek Venkatachalam

Canadian Institutes of Health Research (154274)

  • Mei Zhen

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 27, 2021
  2. Accepted: April 8, 2021
  3. Accepted Manuscript published: April 21, 2021 (version 1)
  4. Accepted Manuscript updated: April 22, 2021 (version 2)
  5. Version of Record published: May 21, 2021 (version 3)

Copyright

© 2021, Ji 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. Ni Ji
  2. Vivek Venkatachalam
  3. Hillary Denise Rodgers
  4. Wesley Hung
  5. Taizo Kawano
  6. Christopher M Clark
  7. Maria Lim
  8. Mark J Alkema
  9. Mei Zhen
  10. Aravinthan DT Samuel
(2021)
Corollary discharge promotes a sustained motor state in a neural circuit for navigation
eLife 10:e68848.
https://doi.org/10.7554/eLife.68848

Share this article

https://doi.org/10.7554/eLife.68848

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