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Comprehensive analysis of locomotion dynamics in the protochordate Ciona intestinalis reveals how neuromodulators flexibly shape its behavioral repertoire

Vertebrate nervous systems can generate a remarkable diversity of behaviors. However, our understanding of how behaviors may have evolved in the chordate lineage is limited by the lack of neuroethological studies leveraging our closest invertebrate relatives. Here, we combine high-throughput video a...

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Autores principales: Athira, Athira, Dondorp, Daniel, Rudolf, Jerneja, Peytral, Olivia, Chatzigeorgiou, Marios
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9352054/
https://www.ncbi.nlm.nih.gov/pubmed/35925898
http://dx.doi.org/10.1371/journal.pbio.3001744
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author Athira, Athira
Dondorp, Daniel
Rudolf, Jerneja
Peytral, Olivia
Chatzigeorgiou, Marios
author_facet Athira, Athira
Dondorp, Daniel
Rudolf, Jerneja
Peytral, Olivia
Chatzigeorgiou, Marios
author_sort Athira, Athira
collection PubMed
description Vertebrate nervous systems can generate a remarkable diversity of behaviors. However, our understanding of how behaviors may have evolved in the chordate lineage is limited by the lack of neuroethological studies leveraging our closest invertebrate relatives. Here, we combine high-throughput video acquisition with pharmacological perturbations of bioamine signaling to systematically reveal the global structure of the motor behavioral repertoire in the Ciona intestinalis larvae. Most of Ciona’s postural variance can be captured by 6 basic shapes, which we term “eigencionas.” Motif analysis of postural time series revealed numerous stereotyped behavioral maneuvers including “startle-like” and “beat-and-glide.” Employing computational modeling of swimming dynamics and spatiotemporal embedding of postural features revealed that behavioral differences are generated at the levels of motor modules and the transitions between, which may in part be modulated by bioamines. Finally, we show that flexible motor module usage gives rise to diverse behaviors in response to different light stimuli.
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spelling pubmed-93520542022-08-05 Comprehensive analysis of locomotion dynamics in the protochordate Ciona intestinalis reveals how neuromodulators flexibly shape its behavioral repertoire Athira, Athira Dondorp, Daniel Rudolf, Jerneja Peytral, Olivia Chatzigeorgiou, Marios PLoS Biol Research Article Vertebrate nervous systems can generate a remarkable diversity of behaviors. However, our understanding of how behaviors may have evolved in the chordate lineage is limited by the lack of neuroethological studies leveraging our closest invertebrate relatives. Here, we combine high-throughput video acquisition with pharmacological perturbations of bioamine signaling to systematically reveal the global structure of the motor behavioral repertoire in the Ciona intestinalis larvae. Most of Ciona’s postural variance can be captured by 6 basic shapes, which we term “eigencionas.” Motif analysis of postural time series revealed numerous stereotyped behavioral maneuvers including “startle-like” and “beat-and-glide.” Employing computational modeling of swimming dynamics and spatiotemporal embedding of postural features revealed that behavioral differences are generated at the levels of motor modules and the transitions between, which may in part be modulated by bioamines. Finally, we show that flexible motor module usage gives rise to diverse behaviors in response to different light stimuli. Public Library of Science 2022-08-04 /pmc/articles/PMC9352054/ /pubmed/35925898 http://dx.doi.org/10.1371/journal.pbio.3001744 Text en © 2022 Athira 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
Athira, Athira
Dondorp, Daniel
Rudolf, Jerneja
Peytral, Olivia
Chatzigeorgiou, Marios
Comprehensive analysis of locomotion dynamics in the protochordate Ciona intestinalis reveals how neuromodulators flexibly shape its behavioral repertoire
title Comprehensive analysis of locomotion dynamics in the protochordate Ciona intestinalis reveals how neuromodulators flexibly shape its behavioral repertoire
title_full Comprehensive analysis of locomotion dynamics in the protochordate Ciona intestinalis reveals how neuromodulators flexibly shape its behavioral repertoire
title_fullStr Comprehensive analysis of locomotion dynamics in the protochordate Ciona intestinalis reveals how neuromodulators flexibly shape its behavioral repertoire
title_full_unstemmed Comprehensive analysis of locomotion dynamics in the protochordate Ciona intestinalis reveals how neuromodulators flexibly shape its behavioral repertoire
title_short Comprehensive analysis of locomotion dynamics in the protochordate Ciona intestinalis reveals how neuromodulators flexibly shape its behavioral repertoire
title_sort comprehensive analysis of locomotion dynamics in the protochordate ciona intestinalis reveals how neuromodulators flexibly shape its behavioral repertoire
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9352054/
https://www.ncbi.nlm.nih.gov/pubmed/35925898
http://dx.doi.org/10.1371/journal.pbio.3001744
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