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Networks of Causal Linkage Between Eigenmodes Characterize Behavioral Dynamics of Caenorhabditis elegans

Behavioral phenotyping of model organisms has played an important role in unravelling the complexities of animal behavior. Techniques for classifying behavior often rely on easily identified changes in posture and motion. However, such approaches are likely to miss complex behaviors that cannot be r...

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Autores principales: Saberski, Erik, Bock, Antonia K., Goodridge, Rachel, Agarwal, Vitul, Lorimer, Tom, Rifkin, Scott A., Sugihara, George
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8494368/
https://www.ncbi.nlm.nih.gov/pubmed/34506477
http://dx.doi.org/10.1371/journal.pcbi.1009329
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author Saberski, Erik
Bock, Antonia K.
Goodridge, Rachel
Agarwal, Vitul
Lorimer, Tom
Rifkin, Scott A.
Sugihara, George
author_facet Saberski, Erik
Bock, Antonia K.
Goodridge, Rachel
Agarwal, Vitul
Lorimer, Tom
Rifkin, Scott A.
Sugihara, George
author_sort Saberski, Erik
collection PubMed
description Behavioral phenotyping of model organisms has played an important role in unravelling the complexities of animal behavior. Techniques for classifying behavior often rely on easily identified changes in posture and motion. However, such approaches are likely to miss complex behaviors that cannot be readily distinguished by eye (e.g., behaviors produced by high dimensional dynamics). To explore this issue, we focus on the model organism Caenorhabditis elegans, where behaviors have been extensively recorded and classified. Using a dynamical systems lens, we identify high dimensional, nonlinear causal relationships between four basic shapes that describe worm motion (eigenmodes, also called “eigenworms”). We find relationships between all pairs of eigenmodes, but the timescales of the interactions vary between pairs and across individuals. Using these varying timescales, we create “interaction profiles” to represent an individual’s behavioral dynamics. As desired, these profiles are able to distinguish well-known behavioral states: i.e., the profiles for foraging individuals are distinct from those of individuals exhibiting an escape response. More importantly, we find that interaction profiles can distinguish high dimensional behaviors among divergent mutant strains that were previously classified as phenotypically similar. Specifically, we find it is able to detect phenotypic behavioral differences not previously identified in strains related to dysfunction of hermaphrodite-specific neurons.
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spelling pubmed-84943682021-10-07 Networks of Causal Linkage Between Eigenmodes Characterize Behavioral Dynamics of Caenorhabditis elegans Saberski, Erik Bock, Antonia K. Goodridge, Rachel Agarwal, Vitul Lorimer, Tom Rifkin, Scott A. Sugihara, George PLoS Comput Biol Research Article Behavioral phenotyping of model organisms has played an important role in unravelling the complexities of animal behavior. Techniques for classifying behavior often rely on easily identified changes in posture and motion. However, such approaches are likely to miss complex behaviors that cannot be readily distinguished by eye (e.g., behaviors produced by high dimensional dynamics). To explore this issue, we focus on the model organism Caenorhabditis elegans, where behaviors have been extensively recorded and classified. Using a dynamical systems lens, we identify high dimensional, nonlinear causal relationships between four basic shapes that describe worm motion (eigenmodes, also called “eigenworms”). We find relationships between all pairs of eigenmodes, but the timescales of the interactions vary between pairs and across individuals. Using these varying timescales, we create “interaction profiles” to represent an individual’s behavioral dynamics. As desired, these profiles are able to distinguish well-known behavioral states: i.e., the profiles for foraging individuals are distinct from those of individuals exhibiting an escape response. More importantly, we find that interaction profiles can distinguish high dimensional behaviors among divergent mutant strains that were previously classified as phenotypically similar. Specifically, we find it is able to detect phenotypic behavioral differences not previously identified in strains related to dysfunction of hermaphrodite-specific neurons. Public Library of Science 2021-09-10 /pmc/articles/PMC8494368/ /pubmed/34506477 http://dx.doi.org/10.1371/journal.pcbi.1009329 Text en © 2021 Saberski et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Saberski, Erik
Bock, Antonia K.
Goodridge, Rachel
Agarwal, Vitul
Lorimer, Tom
Rifkin, Scott A.
Sugihara, George
Networks of Causal Linkage Between Eigenmodes Characterize Behavioral Dynamics of Caenorhabditis elegans
title Networks of Causal Linkage Between Eigenmodes Characterize Behavioral Dynamics of Caenorhabditis elegans
title_full Networks of Causal Linkage Between Eigenmodes Characterize Behavioral Dynamics of Caenorhabditis elegans
title_fullStr Networks of Causal Linkage Between Eigenmodes Characterize Behavioral Dynamics of Caenorhabditis elegans
title_full_unstemmed Networks of Causal Linkage Between Eigenmodes Characterize Behavioral Dynamics of Caenorhabditis elegans
title_short Networks of Causal Linkage Between Eigenmodes Characterize Behavioral Dynamics of Caenorhabditis elegans
title_sort networks of causal linkage between eigenmodes characterize behavioral dynamics of caenorhabditis elegans
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8494368/
https://www.ncbi.nlm.nih.gov/pubmed/34506477
http://dx.doi.org/10.1371/journal.pcbi.1009329
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