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Decoding locomotion from population neural activity in moving C. elegans

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 tuni...

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Detalles Bibliográficos
Autores principales: Hallinen, Kelsey M, Dempsey, Ross, Scholz, Monika, Yu, Xinwei, Linder, Ashley, Randi, Francesco, Sharma, Anuj K, Shaevitz, Joshua W, Leifer, Andrew M
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8439659/
https://www.ncbi.nlm.nih.gov/pubmed/34323218
http://dx.doi.org/10.7554/eLife.66135
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author Hallinen, Kelsey M
Dempsey, Ross
Scholz, Monika
Yu, Xinwei
Linder, Ashley
Randi, Francesco
Sharma, Anuj K
Shaevitz, Joshua W
Leifer, Andrew M
author_facet Hallinen, Kelsey M
Dempsey, Ross
Scholz, Monika
Yu, Xinwei
Linder, Ashley
Randi, Francesco
Sharma, Anuj K
Shaevitz, Joshua W
Leifer, Andrew M
author_sort Hallinen, Kelsey M
collection PubMed
description 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.
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spelling pubmed-84396592021-09-15 Decoding locomotion from population neural activity in moving C. elegans Hallinen, Kelsey M Dempsey, Ross Scholz, Monika Yu, Xinwei Linder, Ashley Randi, Francesco Sharma, Anuj K Shaevitz, Joshua W Leifer, Andrew M eLife Neuroscience 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. eLife Sciences Publications, Ltd 2021-07-29 /pmc/articles/PMC8439659/ /pubmed/34323218 http://dx.doi.org/10.7554/eLife.66135 Text en © 2021, Hallinen et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Hallinen, Kelsey M
Dempsey, Ross
Scholz, Monika
Yu, Xinwei
Linder, Ashley
Randi, Francesco
Sharma, Anuj K
Shaevitz, Joshua W
Leifer, Andrew M
Decoding locomotion from population neural activity in moving C. elegans
title Decoding locomotion from population neural activity in moving C. elegans
title_full Decoding locomotion from population neural activity in moving C. elegans
title_fullStr Decoding locomotion from population neural activity in moving C. elegans
title_full_unstemmed Decoding locomotion from population neural activity in moving C. elegans
title_short Decoding locomotion from population neural activity in moving C. elegans
title_sort decoding locomotion from population neural activity in moving c. elegans
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8439659/
https://www.ncbi.nlm.nih.gov/pubmed/34323218
http://dx.doi.org/10.7554/eLife.66135
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