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...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2022-08-01
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| Series: | PLoS Biology |
| Online Access: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9352054/?tool=EBI |
| _version_ | 1811343953215094784 |
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| author | Athira Athira Daniel Dondorp Jerneja Rudolf Olivia Peytral Marios Chatzigeorgiou |
| author_facet | Athira Athira Daniel Dondorp Jerneja Rudolf Olivia Peytral Marios Chatzigeorgiou |
| author_sort | Athira Athira |
| collection | DOAJ |
| 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. Vertebrate nervous systems can generate a remarkable diversity of behaviors, but how did these evolve in the chordate lineage? A study of the protochordate Ciona intestinalis reveals novel insights into how a simple chordate brain uses neuromodulators to control its behavioral repertoire. |
| first_indexed | 2024-04-13T19:39:07Z |
| format | Article |
| id | doaj.art-c71b1e8d0a3a4bab9242fa6785678594 |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-04-13T19:39:07Z |
| publishDate | 2022-08-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-c71b1e8d0a3a4bab9242fa67856785942022-12-22T02:32:57ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852022-08-01208Comprehensive analysis of locomotion dynamics in the protochordate Ciona intestinalis reveals how neuromodulators flexibly shape its behavioral repertoireAthira AthiraDaniel DondorpJerneja RudolfOlivia PeytralMarios ChatzigeorgiouVertebrate 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. Vertebrate nervous systems can generate a remarkable diversity of behaviors, but how did these evolve in the chordate lineage? A study of the protochordate Ciona intestinalis reveals novel insights into how a simple chordate brain uses neuromodulators to control its behavioral repertoire.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9352054/?tool=EBI |
| spellingShingle | Athira Athira Daniel Dondorp Jerneja Rudolf Olivia Peytral Marios Chatzigeorgiou Comprehensive analysis of locomotion dynamics in the protochordate Ciona intestinalis reveals how neuromodulators flexibly shape its behavioral repertoire PLoS Biology |
| 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 |
| url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9352054/?tool=EBI |
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