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Published February 23, 2021 | Submitted + Supplemental Material
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Functional modules within a distributed neural network control feeding in a model medusa


Jellyfish are free-swimming, radially symmetric organisms with complex behaviors that arise from coordinated interactions between distinct, autonomously functioning body parts. This behavioral complexity evolved without a corresponding cephalization of the nervous system. The systems-level neural mechanisms through which such decentralized control is achieved remain unclear. Here, we address this question using the jellyfish, Clytia, and present it as a new neuroscience model. We describe a coordinated, asymmetric behavior in which food is passed from the umbrellar margin to the central mouth via directed margin folding. Using newly developed transgenic jellyfish lines to ablate or image specific neuronal subpopulations, we find, unexpectedly, that margin folding reflects the local activation of neural subnetworks that tile the umbrella. Modeling suggests that this structured ensemble activity emerges from sparse, local connectivity rules. These findings reveal how an organismal behavior can emerge from local interactions between functional modules in the absence of a central brain.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license. This version posted February 23, 2021. We thank J. Malamy, E. Houliston, R. Copley, J. Costello, S. Colin, and members of L. Goentoro's Laboratory, particularly T. Basinger, for assistance establishing Clytia at Caltech and performing initial experiments. We thank J. Malamy for first introducing B.W. and D.J.A to Clytia, X. Da and X. Wang for technical assistance, G. Mancuso for administrative assistance, C. Chiu for laboratory management, S. Ekker and C. Daby for assistance and reagents while establishing the Tol2 system, A. Collazo and the Caltech Biological Imaging Facility for imaging assistance, T. Chari, J. Gehring, and L. Pachter for scRNAseq analysis, and J. DeGiorgis who captured Supplemental Video 2. We thank E. Houliston, J. Parker, D. Prober, T. Karigo, G. Mountoufaris, Y. Ouadah, S. Stagkourakis, A. Vinograd, and B. Yang for feedback on the manuscript. This work was supported in part by the Caltech Center for Evolutionary Science, the Whitman Center of the Marine Biological Laboratory in Woods Hole, MA, a Howard Hughes Medical Institute Fellowship of the Life Sciences Research Foundation (to B.W.), the National Institute Of Neurological Disorders and Stroke of the National Institutes of Health under Award Number K99NS119749 (to B.W.), and by the National Institute Of Mental Health of the National Institutes of Health under Award Number K99MH117264 (to A.K.). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. We thank the CRBM Villefranche (FR 3761) for marine facilities, biological resources, and a travel grant to B.W., which is supported by EMBRC-France, whose French state funds are managed by the ANR within the Investments of the Future program under reference ANR-10-INBS-02. T.M was supported by Agence Nationale de la Recherche (ANR), ANR-17-CE13-0016 (i-MMEJ). A. N. is supported by a National Science 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, and 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.

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Submitted - 2021.02.22.432372v1.full.pdf

Supplemental Material - media-10.mov

Supplemental Material - media-2.mov

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Supplemental Material - media-7.mov

Supplemental Material - media-8.avi

Supplemental Material - media-9.mov


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August 20, 2023
December 22, 2023