Decoding locomotion from population neural activity in moving C. elegans

Abstract

We investigated the neural representation of locomotion in the nematode C. elegans by recording population calcium activity during movement. We report that population activity more accurately decodes locomotion than any single neuron. Relevant signals are distributed across neurons with diverse tunings to locomotion. Two largely distinct subpopulations are informative for decoding velocity and curvature, and different neurons’ activities contribute features relevant for different aspects of a behavior or different instances of a behavioral motif. To validate our measurements, we labeled neurons AVAL and AVAR and found that their activity exhibited expected transients during backward locomotion. Finally, we compared population activity during movement and immobilization. Immobilization alters the correlation structure of neural activity and its dynamics. Some neurons positively correlated with AVA during movement become negatively correlated during immobilization and vice versa. This work provides needed experimental measurements that inform and constrain ongoing efforts to understand population dynamics underlying locomotion in C. elegans.

Data availability

Data associated with this manuscript has been deposited in a publicly accessible repository hosted by the Open Science Foundation at DOI:10.17605/OSF.IO/DPR3H

The following data sets were generated

Article and author information

Author details

  1. Kelsey M Hallinen

    Department of Physics, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4081-6699
  2. Ross Dempsey

    Department of Physics, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Monika Scholz

    CAESER, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2186-410X
  4. Xinwei Yu

    Department of Physics, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Ashley Linder

    Princeton Neuroscience Institute, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Francesco Randi

    Department of Physics, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Anuj Kumar Sharma Ph.D.

    Department of Physics, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5061-9731
  8. Joshua W Shaevitz

    Lewis-Sigler Institute of Integrative Genomics, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8809-4723
  9. Andrew Michael Leifer

    Department of Physics and Princeton Neuroscience Institute, Princeton University, Princeton, United States
    For correspondence
    leifer@princeton.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5362-5093

Funding

National Science Foundation (IOS-1845137)

  • Andrew Michael Leifer

National Science Foundation (PHY-1734030)

  • Joshua W Shaevitz
  • Andrew Michael Leifer

National Institutes of Health (MH065214)

  • Ashley Linder

Simons Foundation (324285)

  • Andrew Michael Leifer

Swartz Foundation

  • Francesco Randi

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

Reviewing Editor

  1. Ronald L Calabrese, Emory University, United States

Publication history

  1. Preprint posted: October 17, 2018 (view preprint)
  2. Received: December 29, 2020
  3. Accepted: July 26, 2021
  4. Accepted Manuscript published: July 29, 2021 (version 1)
  5. Version of Record published: September 14, 2021 (version 2)

Copyright

© 2021, Hallinen 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. Kelsey M Hallinen
  2. Ross Dempsey
  3. Monika Scholz
  4. Xinwei Yu
  5. Ashley Linder
  6. Francesco Randi
  7. Anuj Kumar Sharma Ph.D.
  8. Joshua W Shaevitz
  9. Andrew Michael Leifer
(2021)
Decoding locomotion from population neural activity in moving C. elegans
eLife 10:e66135.
https://doi.org/10.7554/eLife.66135
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