Weissbourd, Brandon and Momose, Tsuyoshi and Nair, Aditya and Kennedy, Ann and Hunt, Bridgett and Anderson, David J. (2021) A genetically tractable jellyfish model for systems and evolutionary neuroscience. Cell, 184 (24). pp. 5854-5868. ISSN 0092-8674. PMCID PMC8629132. doi:10.1016/j.cell.2021.10.021. https://resolver.caltech.edu/CaltechAUTHORS:20201129-234567890
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Abstract
Jellyfish are radially symmetric organisms without a brain that arose more than 500 million years ago. They achieve organismal behaviors through coordinated interactions between autonomously functioning body parts. Jellyfish neurons have been studied electrophysiologically, but not at the systems level. We introduce Clytia hemisphaerica as a transparent, genetically tractable jellyfish model for systems and evolutionary neuroscience. We generate stable F₁ transgenic lines for cell-type-specific conditional ablation and whole-organism GCaMP imaging. Using these tools and computational analyses, we find that an apparently diffuse network of RFamide-expressing umbrellar neurons is functionally subdivided into a series of spatially localized subassemblies whose synchronous activation controls directional food transfer from the tentacles to the mouth. These data reveal an unanticipated degree of structured neural organization in this species. Clytia affords a platform for systems-level studies of neural function, behavior, and evolution within a clade of marine organisms with growing ecological and economic importance.
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| Additional Information: | © 2021 Elsevier. Received 23 February 2021, Revised 30 August 2021, Accepted 19 October 2021, Available online 24 November 2021. We thank the Marine Resources Center of the MBL (Woods Hole, MA) and J. Malamy for an introduction to Clytia; E. Houliston and R. Copley for Clytia resources and advice; M.D.C. Lamadrid for illustrations; S. Ekker for Tol2 reagents; J. Williams for software; A. Collazo for imaging support; and J. Parker, D. Prober, and Anderson lab members for feedback. We thank the CRBM/Service Aquario (FR 3761; EMBRC-France, managed by ANR-10-INBS-0002) for support. This work was supported by the Caltech Center for Evolutionary Science, the Whitman Center of the MBL, the Life Sciences Research Foundation (to B.W.), NINDS (K99NS119749 to B.W.), and NIMH (K99MH117264 to A.K.). Content is the authors’ sole responsibility and not that of NIH. T.M. was supported by ANR (ANR-17-CE13-0016, i-MMEJ) and ASSEMBLE Plus JRA3 (EU Horizon 2020 No. 730984). A.N. was supported by a Scholarship from the Agency of Science, Technology and Research, Singapore. D.J.A. is an Investigator of the Howard Hughes Medical Institute. Author contributions: B.W. and D.J.A. conceived of the project and wrote the manuscript with input from T.M., A.N., A.K., and B.H. B.W., D.J.A., and B.H. designed and performed histology, behavior, and imaging experiments. B.W., D.J.A., and T.M. designed and performed experiments establishing transgenesis. B.W., A.N., and A.K. analyzed the data. A.N. performed NMF/ICA, subspace, and GLM analyses. A.K. generated the neural network models. The authors declare no competing interests. Data and code availability: • Source data reported in this paper will be shared by the lead contact upon request. • Code used for analyses in this paper will be shared by the lead contact upon request. • Any additional information required to reanalyze the data reported in this paper is available from the lead contact upon request. | ||||||||||||||||||||||||
| Group: | Tianqiao and Chrissy Chen Institute for Neuroscience | ||||||||||||||||||||||||
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| Subject Keywords: | neuroscience; imaging; GCaMP; Clytia; cnidarian; neuropeptide; behavior; transgenesis; jellyfish; nerve net | ||||||||||||||||||||||||
| Issue or Number: | 24 | ||||||||||||||||||||||||
| PubMed Central ID: | PMC8629132 | ||||||||||||||||||||||||
| DOI: | 10.1016/j.cell.2021.10.021 | ||||||||||||||||||||||||
| Record Number: | CaltechAUTHORS:20201129-234567890 | ||||||||||||||||||||||||
| Persistent URL: | https://resolver.caltech.edu/CaltechAUTHORS:20201129-234567890 | ||||||||||||||||||||||||
| Official Citation: | Brandon Weissbourd, Tsuyoshi Momose, Aditya Nair, Ann Kennedy, Bridgett Hunt, David J. Anderson, A genetically tractable jellyfish model for systems and evolutionary neuroscience, Cell, Volume 184, Issue 24, 2021, Pages 5854-5868.e20, ISSN 0092-8674, https://doi.org/10.1016/j.cell.2021.10.021. | ||||||||||||||||||||||||
| Usage Policy: | No commercial reproduction, distribution, display or performance rights in this work are provided. | ||||||||||||||||||||||||
| ID Code: | 112062 | ||||||||||||||||||||||||
| Collection: | CaltechAUTHORS | ||||||||||||||||||||||||
| Deposited By: | George Porter | ||||||||||||||||||||||||
| Deposited On: | 29 Nov 2021 08:59 | ||||||||||||||||||||||||
| Last Modified: | 10 Dec 2021 20:55 |
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