Cargando…

A Quantitative Analysis of Locomotor Patterns in Developing C. elegans

Adult animals display robust locomotion, yet the timeline and mechanisms of how juvenile animals acquire coordinated movements and how these movements evolve during development are not well understood. Recent advances in quantitative behavioral analyses have paved the way for investigating complex n...

Descripción completa

Detalles Bibliográficos
Autores principales: Hassinan, Cera W., Sterrett, Scott C., Summy, Brennan, Khera, Arnav, Wang, Angie, Bai, Jihong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10274735/
https://www.ncbi.nlm.nih.gov/pubmed/37333370
http://dx.doi.org/10.1101/2023.06.03.543584
_version_ 1785059788163383296
author Hassinan, Cera W.
Sterrett, Scott C.
Summy, Brennan
Khera, Arnav
Wang, Angie
Bai, Jihong
author_facet Hassinan, Cera W.
Sterrett, Scott C.
Summy, Brennan
Khera, Arnav
Wang, Angie
Bai, Jihong
author_sort Hassinan, Cera W.
collection PubMed
description Adult animals display robust locomotion, yet the timeline and mechanisms of how juvenile animals acquire coordinated movements and how these movements evolve during development are not well understood. Recent advances in quantitative behavioral analyses have paved the way for investigating complex natural behaviors like locomotion. In this study, we tracked the swimming and crawling behaviors of the nematode Caenorhabditis elegans from postembryonic development through to adulthood. Our principal component analyses revealed that adult C. elegans swimming is low dimensional, suggesting that a small number of distinct postures, or eigenworms, account for most of the variance in the body shapes that constitute swimming behavior. Additionally, we found that crawling behavior in adult C. elegans is similarly low dimensional, corroborating previous studies. However, our analysis revealed that swimming and crawling are distinct gaits in adult animals, clearly distinguishable within the eigenworm space. Remarkably, young L1 larvae are capable of producing the postural shapes for swimming and crawling seen in adults, despite frequent instances of uncoordinated body movements. In contrast, late L1 larvae exhibit robust coordination of locomotion, while many neurons crucial for adult locomotion are still under development. In conclusion, this study establishes a comprehensive quantitative behavioral framework for understanding the neural basis of locomotor development, including distinct gaits such as swimming and crawling in C. elegans.
format Online
Article
Text
id pubmed-10274735
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Cold Spring Harbor Laboratory
record_format MEDLINE/PubMed
spelling pubmed-102747352023-06-17 A Quantitative Analysis of Locomotor Patterns in Developing C. elegans Hassinan, Cera W. Sterrett, Scott C. Summy, Brennan Khera, Arnav Wang, Angie Bai, Jihong bioRxiv Article Adult animals display robust locomotion, yet the timeline and mechanisms of how juvenile animals acquire coordinated movements and how these movements evolve during development are not well understood. Recent advances in quantitative behavioral analyses have paved the way for investigating complex natural behaviors like locomotion. In this study, we tracked the swimming and crawling behaviors of the nematode Caenorhabditis elegans from postembryonic development through to adulthood. Our principal component analyses revealed that adult C. elegans swimming is low dimensional, suggesting that a small number of distinct postures, or eigenworms, account for most of the variance in the body shapes that constitute swimming behavior. Additionally, we found that crawling behavior in adult C. elegans is similarly low dimensional, corroborating previous studies. However, our analysis revealed that swimming and crawling are distinct gaits in adult animals, clearly distinguishable within the eigenworm space. Remarkably, young L1 larvae are capable of producing the postural shapes for swimming and crawling seen in adults, despite frequent instances of uncoordinated body movements. In contrast, late L1 larvae exhibit robust coordination of locomotion, while many neurons crucial for adult locomotion are still under development. In conclusion, this study establishes a comprehensive quantitative behavioral framework for understanding the neural basis of locomotor development, including distinct gaits such as swimming and crawling in C. elegans. Cold Spring Harbor Laboratory 2023-06-06 /pmc/articles/PMC10274735/ /pubmed/37333370 http://dx.doi.org/10.1101/2023.06.03.543584 Text en https://creativecommons.org/licenses/by-nd/4.0/This work is licensed under a Creative Commons Attribution-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, and only so long as attribution is given to the creator. The license allows for commercial use.
spellingShingle Article
Hassinan, Cera W.
Sterrett, Scott C.
Summy, Brennan
Khera, Arnav
Wang, Angie
Bai, Jihong
A Quantitative Analysis of Locomotor Patterns in Developing C. elegans
title A Quantitative Analysis of Locomotor Patterns in Developing C. elegans
title_full A Quantitative Analysis of Locomotor Patterns in Developing C. elegans
title_fullStr A Quantitative Analysis of Locomotor Patterns in Developing C. elegans
title_full_unstemmed A Quantitative Analysis of Locomotor Patterns in Developing C. elegans
title_short A Quantitative Analysis of Locomotor Patterns in Developing C. elegans
title_sort quantitative analysis of locomotor patterns in developing c. elegans
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10274735/
https://www.ncbi.nlm.nih.gov/pubmed/37333370
http://dx.doi.org/10.1101/2023.06.03.543584
work_keys_str_mv AT hassinanceraw aquantitativeanalysisoflocomotorpatternsindevelopingcelegans
AT sterrettscottc aquantitativeanalysisoflocomotorpatternsindevelopingcelegans
AT summybrennan aquantitativeanalysisoflocomotorpatternsindevelopingcelegans
AT kheraarnav aquantitativeanalysisoflocomotorpatternsindevelopingcelegans
AT wangangie aquantitativeanalysisoflocomotorpatternsindevelopingcelegans
AT baijihong aquantitativeanalysisoflocomotorpatternsindevelopingcelegans
AT hassinanceraw quantitativeanalysisoflocomotorpatternsindevelopingcelegans
AT sterrettscottc quantitativeanalysisoflocomotorpatternsindevelopingcelegans
AT summybrennan quantitativeanalysisoflocomotorpatternsindevelopingcelegans
AT kheraarnav quantitativeanalysisoflocomotorpatternsindevelopingcelegans
AT wangangie quantitativeanalysisoflocomotorpatternsindevelopingcelegans
AT baijihong quantitativeanalysisoflocomotorpatternsindevelopingcelegans