Decoding locomotion from population neural activity in moving C. elegans

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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

(2020) Calcium activity recordings and behaviors assocated wtih the manuscript
Open Science Foundation, DOI: 10.17605/OSF.IO/R5TB3.

https://doi.org/10.17605/OSF.IO/DPR3H

Article and author information

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Kelsey M Hallinen

Department of Physics, Princeton University, Princeton, United States

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The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-4081-6699
Ross Dempsey

Department of Physics, Princeton University, Princeton, United States

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The authors declare that no competing interests exist.
Monika Scholz

CAESER, Bonn, Germany

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The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-2186-410X
Xinwei Yu

Department of Physics, Princeton University, Princeton, United States

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The authors declare that no competing interests exist.
Ashley Linder

Princeton Neuroscience Institute, Princeton University, Princeton, United States

Competing interests
The authors declare that no competing interests exist.
Francesco Randi

Department of Physics, Princeton University, Princeton, United States

Competing interests
The authors declare that no competing interests exist.
Anuj Kumar Sharma Ph.D.

Department of Physics, Princeton University, Princeton, United States

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The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-5061-9731
Joshua W Shaevitz

Lewis-Sigler Institute of Integrative Genomics, Princeton University, Princeton, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-8809-4723
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.

"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.

Copyright

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.