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

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  • Athira Athira
  • Daniel Dondorp
  • Jerneja Rudolf
  • Olivia Peytral
  • Marios Chatzigeorgiou

Abstract

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.

Suggested Citation

  • Athira Athira & Daniel Dondorp & Jerneja Rudolf & Olivia Peytral & Marios Chatzigeorgiou, 2022. "Comprehensive analysis of locomotion dynamics in the protochordate Ciona intestinalis reveals how neuromodulators flexibly shape its behavioral repertoire," PLOS Biology, Public Library of Science, vol. 20(8), pages 1-44, August.
  • Handle: RePEc:plo:pbio00:3001744
    DOI: 10.1371/journal.pbio.3001744
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    References listed on IDEAS

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    1. Greg J Stephens & Bethany Johnson-Kerner & William Bialek & William S Ryu, 2008. "Dimensionality and Dynamics in the Behavior of C. elegans," PLOS Computational Biology, Public Library of Science, vol. 4(4), pages 1-10, April.
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