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The Jellyfish Cassiopea Exhibits a Sleep-like State

Nath, Ravi D. and Bedbrook, Claire N. and Abrams, Michael J. and Basinger, Ty and Bois, Justin S. and Prober, David A. and Sternberg, Paul W. and Gradinaru, Viviana and Goentoro, Lea (2017) The Jellyfish Cassiopea Exhibits a Sleep-like State. Current Biology, 27 (19). pp. 2984-2990. ISSN 0960-9822. PMCID PMC5653286. https://resolver.caltech.edu/CaltechAUTHORS:20170921-075913502

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Abstract

Do all animals sleep? Sleep has been observed in many vertebrates, and there is a growing body of evidence for sleep-like states in arthropods and nematodes. Here we show that sleep is also present in Cnidaria, an earlier-branching metazoan lineage. Cnidaria and Ctenophora are the first metazoan phyla to evolve tissue-level organization and differentiated cell types, such as neurons and muscle. In Cnidaria, neurons are organized into a non-centralized radially symmetric nerve net that nevertheless shares fundamental properties with the vertebrate nervous system: action potentials, synaptic transmission, neuropeptides, and neurotransmitters . It was reported that cnidarian soft corals and box jellyfish exhibit periods of quiescence, a pre-requisite for sleep-like states, prompting us to ask whether sleep is present in Cnidaria. Within Cnidaria, the upside-down jellyfish Cassiopea spp. displays a quantifiable pulsing behavior, allowing us to perform long-term behavioral tracking. Monitoring of Cassiopea pulsing activity for consecutive days and nights revealed behavioral quiescence at night that is rapidly reversible, as well as a delayed response to stimulation in the quiescent state. When deprived of nighttime quiescence, Cassiopea exhibited decreased activity and reduced responsiveness to a sensory stimulus during the subsequent day, consistent with homeostatic regulation of the quiescent state. Together, these results indicate that Cassiopea has a sleep-like state, supporting the hypothesis that sleep arose early in the metazoan lineage, prior to the emergence of a centralized nervous system.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.cub.2017.08.014DOIArticle
http://www.sciencedirect.com/science/article/pii/S0960982217310230PublisherArticle
https://github.com/GradinaruLab/JellyfishRelated ItemCode used for tracking jellyfish activity and analysis
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5653286/PubMed CentralArticle
ORCID:
AuthorORCID
Bedbrook, Claire N.0000-0003-3973-598X
Bois, Justin S.0000-0001-7137-8746
Prober, David A.0000-0002-7371-4675
Sternberg, Paul W.0000-0002-7699-0173
Gradinaru, Viviana0000-0001-5868-348X
Goentoro, Lea0000-0002-3904-0195
Additional Information:© 2017 Elsevier. Received 30 April 2017, Revised 17 July 2017, Accepted 4 August 2017, Available online 21 September 2017. Published: September 21, 2017. We thank Chris Blair from the National Aquarium, MD; Monica Medina and Aki Ohdera from Pennsylvania State University, PA; and Wyatt Patry from the Monterey Bay Aquarium, CA, for generously supplying Cassiopea medusa and polyps and Dr. John Bedbrook for critical reading of the manuscript. We thank Kiersten Darrow and Michael Schaadt of the Cabrillo Marine Aquarium, CA, for input on husbandry. We thank http://dryades.units.it/jelly for an image of Cassiopea (CC 3.01 NC-BY-SA) that was adapted in Figure 3 and Figure S1. This work was supported by the NIH Director’s New Innovator Award/PECASE (IDP20D017782-01; to V.G.), the James S. McDonnell Foundation for Complex Systems Science (220020365; to L.G.), the NIMH under a Ruth L. Kirschstein National Research Service Award (F31MH102913; to C.N.B.), the NINDS under a Ruth L. Kirschstein National Research Service Award (F31NS100519; to R.D.N.), a National Science Foundation Graduate Research Fellowship (1144469; to M.J.A.), and an NIH training grant (T32GM007616; to C.N.B. and R.D.N.). V.G. is a Heritage Principal Investigator supported by the Heritage Medical Research Institute; P.W.S. is an investigator with the HHMI (047-101), which supported this research. Data and Software Availability: Code used for tracking jellyfish activity and analysis is available at https://github.com/GradinaruLab/Jellyfish. Author Contributions: R.D.N., C.N.B., and M.J.A. conceived the project. V.G., P.W.S., and L.G. oversaw the project. R.D.N., C.N.B., and M.J.A. performed experiments and data analysis. R.D.N., C.N.B., M.J.A., and T.B. conceptualized, designed, and built experimental setups. C.N.B. and R.D.N. wrote image-processing and data-analysis scripts with J.S.B.’s oversight. D.A.P. provided input on experimental design. R.D.N., C.N.B., and M.J.A. wrote the paper with input from J.S.B., D.A.P., V.G., P.W.S., and L.G.
Group:Heritage Medical Research Institute, Tianqiao and Chrissy Chen Institute for Neuroscience
Funders:
Funding AgencyGrant Number
NIHIDP20D017782-01
James S. McDonnell Foundation220020365
NIH Predoctoral FellowshipF31MH102913
NIH Predoctoral FellowshipF31NS100519
NSF Graduate Research FellowshipDGE-1144469
NIH Predoctoral FellowshipT32GM007616
Heritage Medical Research InstituteUNSPECIFIED
Howard Hughes Medical Institute (HHMI)047-101
Subject Keywords:evolution of sleep; sleep; Cnidaria; jellyfish; Cassiopea
Issue or Number:19
PubMed Central ID:PMC5653286
Record Number:CaltechAUTHORS:20170921-075913502
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20170921-075913502
Official Citation:Ravi D. Nath, Claire N. Bedbrook, Michael J. Abrams, Ty Basinger, Justin S. Bois, David A. Prober, Paul W. Sternberg, Viviana Gradinaru, Lea Goentoro, The Jellyfish Cassiopea Exhibits a Sleep-like State, In Current Biology, Volume 27, Issue 19, 2017, Pages 2984-2990.e3, ISSN 0960-9822, https://doi.org/10.1016/j.cub.2017.08.014. (http://www.sciencedirect.com/science/article/pii/S0960982217310230)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:81662
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:21 Sep 2017 16:19
Last Modified:14 Oct 2019 17:42

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