{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,25]],"date-time":"2026-09-25T23:58:49Z","timestamp":1790380729494,"version":"4.1.0"},"reference-count":54,"publisher":"The Company of Biologists","license":[{"start":{"date-parts":[[2018,1,1]],"date-time":"2018-01-01T00:00:00Z","timestamp":1514764800000},"content-version":"am","delay-in-days":0,"URL":"http:\/\/www.biologists.com\/user-licence-1-1\/"}],"funder":[{"DOI":"10.13039\/100001654","name":"Grass Foundation","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100001654","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:p>Sleep is a state of immobility characterized by three key criteria: an increased threshold of arousal, rapid reversal to an alert state, and evidence of homeostatic \u201crebound sleep\u201d in which there is an increase of time spent in this quiescent state following sleep deprivation. Common European cuttlefish, Sepia officinalis, show states of quiescence during which they meet the last two of these three criteria, yet also show spontaneous bursts of arm and eye movements that accompany rapid changes in chromatophore patterns in the skin. Here we report that this rapid-eye movement sleep-like (REMS-like) state is cyclic in nature. Iterations of the REMS-like state last 2.42\u00b10.22 min (\u00b1SE) and alternate with 34.01\u00b11.49 min of the quiescent sleep-like state. These states alternate for durations lasting 176.89\u00b136.71 min. We found clear evidence that this REMS-like state (i) occurs in animals younger than previously reported; (ii) follows an ultradian pattern; (iii) includes intermittent dynamic chromatophore patterning, representing fragments of normal patterning seen in the waking state for a wide range of signaling and camouflage; and (iv) shows variability in the intensity of expression of these skin patterns between and within individuals. These data suggest that cephalopods, which are molluscs with an elaborate brain and complex behavior, possess a sleep-like state that resembles behaviorally the vertebrate REM sleep state, although the exact nature and mechanism of this form of sleep may differ from that of vertebrates.<\/jats:p>","DOI":"10.1242\/jeb.174862","type":"journal-article","created":{"date-parts":[[2018,11,16]],"date-time":"2018-11-16T12:29:44Z","timestamp":1542371384000},"source":"Crossref","is-referenced-by-count":26,"title":["Cyclic nature of the REM sleep-like state in the cuttlefish <i>Sepia officinalis<\/i>"],"prefix":"10.1242","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0237-8539","authenticated-orcid":false,"given":"Teresa L.","family":"Iglesias","sequence":"first","affiliation":[{"name":"Animal Behavior Graduate Group, University of California Davis, Davis, CA, USA"},{"name":"Physics and Biology Unit, Okinawa Institute of Science and Technology, Okinawa, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jean G.","family":"Boal","sequence":"additional","affiliation":[{"name":"Department of Biology, Millersville University, Lancaster, Pennsylvania, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marcos G.","family":"Frank","sequence":"additional","affiliation":[{"name":"College of Medical Sciences, Washington State University, Spokane, WA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jochen","family":"Zeil","sequence":"additional","affiliation":[{"name":"Research School of Biology, The Australian National University, Canberra, ACT, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Roger T.","family":"Hanlon","sequence":"additional","affiliation":[{"name":"Marine Biological Laboratory, Woods Hole, MA, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"237","published-online":{"date-parts":[[2018,1,1]]},"reference":[{"key":"2021042422470644400_JEB174862C1","doi-asserted-by":"publisher","first-page":"192","DOI":"10.2307\/4134557","article-title":"Signaling to the enemy? body pattern expression and its response to external cues during hunting in the cuttlefish Sepia officinalis (Cephalopoda)","volume":"210","author":"Adamo","year":"2006","journal-title":"Biological Bulletin"},{"key":"2021042422470644400_JEB174862C2","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1207\/S15327604JAWS0504_02","article-title":"Octopus senescence: the beginning of the end","volume":"5","author":"Anderson","year":"2002","journal-title":"J. Appl. Anim. Welf. Sci."},{"key":"2021042422470644400_JEB174862C3","doi-asserted-by":"publisher","first-page":"590","DOI":"10.1016\/j.tree.2016.05.004","article-title":"Sleep ecophysiology: integrating neuroscience and ecology","volume":"31","author":"Aulsebrook","year":"2016","journal-title":"Trends Ecol. Evol."},{"key":"2021042422470644400_JEB174862C4","doi-asserted-by":"publisher","first-page":"1","DOI":"10.18637\/jss.v067.i01","article-title":"Fitting linear mixed-effects models using lme4","volume":"67","author":"Bates","year":"2015","journal-title":"J. Stat. Softw."},{"key":"2021042422470644400_JEB174862C5","doi-asserted-by":"publisher","first-page":"120","DOI":"10.1016\/j.neubiorev.2014.07.019","article-title":"An in depth view of avian sleep","volume":"50","author":"Beckers","year":"2015","journal-title":"Neurosci. Biobehav. Rev."},{"key":"2021042422470644400_JEB174862C6","doi-asserted-by":"publisher","first-page":"355","DOI":"10.1016\/j.bbr.2006.05.009","article-title":"Brain and behavioural evidence for rest-activity cycles in Octopus vulgaris","volume":"172","author":"Brown","year":"2006","journal-title":"Behav. Brain Res."},{"key":"2021042422470644400_JEB174862C7","author":"Burnham","year":"2013","journal-title":"Model Selection and Inference: A Practical Information-Theoretic Approach"},{"key":"2021042422470644400_JEB174862C8","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1242\/jeb.030247","article-title":"Mottle camouflage patterns in cuttlefish: quantitative characterization and visual background stimuli that evoke them","volume":"213","author":"Chiao","year":"2009","journal-title":"J. Exp. Biol."},{"key":"2021042422470644400_JEB174862C9","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1016\/0006-8993(92)90802-G","article-title":"Behavioural and neurohistological changes in aging Sepia","volume":"574","author":"Chichery","year":"1992","journal-title":"Brain Res."},{"key":"2021042422470644400_JEB174862C10","doi-asserted-by":"publisher","first-page":"373","DOI":"10.1007\/s12264-013-1313-3","article-title":"Call it sleep \u2013 what animals without backbones can tell us about the phylogeny of intrinsically generated neuromotor rhythms during early development","volume":"29","author":"Corner","year":"2013","journal-title":"Neurosci. Bull."},{"key":"2021042422470644400_JEB174862C11","doi-asserted-by":"publisher","first-page":"e1500105","DOI":"10.1126\/sciadv.1500105","article-title":"Rapid eye movement sleep promotes cortical plasticity in the developing brain","volume":"1","author":"Dumoulin Bridi","year":"2015","journal-title":"Sci. Adv."},{"key":"2021042422470644400_JEB174862C12","doi-asserted-by":"publisher","first-page":"e38125","DOI":"10.1371\/journal.pone.0038125","article-title":"A preliminary analysis of sleep-like states in the cuttlefish Sepia officinalis","volume":"7","author":"Frank","year":"2012","journal-title":"PLoS ONE"},{"key":"2021042422470644400_JEB174862C13","doi-asserted-by":"publisher","first-page":"24","DOI":"10.18637\/jss.v031.i07","article-title":"Computing and visualizing dynamic time warping alignments in r: the dtw package","volume":"31","author":"Giorgino","year":"2009","journal-title":"2009"},{"key":"2021042422470644400_JEB174862C14","doi-asserted-by":"publisher","first-page":"1","DOI":"10.18637\/jss.v022.i07","article-title":"The ecodist package for dissimilarity-based analysis of ecological data","volume":"22","author":"Goslee","year":"2007","journal-title":"J. Stat. Softw."},{"key":"2021042422470644400_JEB174862C15","doi-asserted-by":"publisher","first-page":"e0171903","DOI":"10.1371\/journal.pone.0171903","article-title":"Inactivity\/sleep in two wild free-roaming African elephant matriarchs\u2013Does large body size make elephants the shortest mammalian sleepers?","volume":"12","author":"Gravett","year":"2017","journal-title":"PLOS ONE"},{"key":"2021042422470644400_JEB174862C16","doi-asserted-by":"publisher","first-page":"437","DOI":"10.1098\/rstb.1988.0087","article-title":"Adaptive coloration in young cuttlefish (Sepia-officinalis L) - the morphology and development of body patterns and their relation to behavior","volume":"320","author":"Hanlon","year":"1988","journal-title":"Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci."},{"key":"2021042422470644400_JEB174862C17","doi-asserted-by":"crossref","DOI":"10.1017\/9780511843600","volume-title":"Cephalopod Behaviour","author":"Hanlon","year":"2018","edition":"2nd edn"},{"key":"2021042422470644400_JEB174862C18","doi-asserted-by":"publisher","first-page":"429","DOI":"10.1098\/rstb.2008.0270","article-title":"Cephalopod dynamic camouflage: bridging the continuum between background matching and disruptive coloration","volume":"364","author":"Hanlon","year":"2009","journal-title":"Philos. Trans. R. Soc. B Biol. Sci."},{"key":"2021042422470644400_JEB174862C19","doi-asserted-by":"publisher","first-page":"793","DOI":"10.1017\/S0140525X00003976","article-title":"Dreaming and the brain: toward a cognitive neuroscience of conscious states","volume":"23","author":"Hobson","year":"2000","journal-title":"Behav. Brain Sci."},{"key":"2021042422470644400_JEB174862C20","doi-asserted-by":"publisher","first-page":"707","DOI":"10.1038\/301707a0","article-title":"Neuronal correlates of sleep, wakefulness and arousal in a diurnal insect","volume":"301","author":"Kaiser","year":"1983","journal-title":"Nature"},{"key":"2021042422470644400_JEB174862C21","doi-asserted-by":"publisher","first-page":"959","DOI":"10.1098\/rspb.2005.3395","article-title":"Symmetrical crypsis and asymmetrical signalling in the cuttlefish Sepia officinalis","volume":"273","author":"Langridge","year":"2006","journal-title":"Proc. R. Soc. B"},{"key":"2021042422470644400_JEB174862C22","doi-asserted-by":"publisher","first-page":"R1044","DOI":"10.1016\/j.cub.2007.10.028","article-title":"Selective signalling by cuttlefish to predators","volume":"17","author":"Langridge","year":"2007","journal-title":"Curr. Biol."},{"key":"2021042422470644400_JEB174862C23","doi-asserted-by":"publisher","first-page":"R12","DOI":"10.1016\/j.cub.2013.10.005","article-title":"Avian sleep","volume":"24","author":"Lesku","year":"2014","journal-title":"Curr. Biol."},{"key":"2021042422470644400_JEB174862C24","doi-asserted-by":"publisher","first-page":"441","DOI":"10.1086\/506973","article-title":"A phylogenetic analysis of sleep architecture in mammals: the integration of anatomy, physiology, and ecology","volume":"168","author":"Lesku","year":"2006","journal-title":"Am. Nat."},{"key":"2021042422470644400_JEB174862C25","doi-asserted-by":"publisher","first-page":"e23203","DOI":"10.1371\/journal.pone.0023203","article-title":"Ostriches sleep like platypuses","volume":"6","author":"Lesku","year":"2011","journal-title":"PLoS ONE"},{"key":"2021042422470644400_JEB174862C26","doi-asserted-by":"publisher","first-page":"e2005982","DOI":"10.1371\/journal.pbio.2005982","article-title":"Partial homologies between sleep states in lizards, mammals, and birds suggest a complex evolution of sleep states in amniotes","volume":"16","author":"Libourel","year":"2018","journal-title":"PLoS Biol."},{"key":"2021042422470644400_JEB174862C27","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1016\/S0896-6273(01)00186-6","article-title":"Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep","volume":"29","author":"Louie","year":"2001","journal-title":"Neuron"},{"key":"2021042422470644400_JEB174862C28","doi-asserted-by":"publisher","first-page":"9081","DOI":"10.1073\/pnas.0703452105","article-title":"Mammalian-like features of sleep structure in zebra finches","volume":"105","author":"Low","year":"2008","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2021042422470644400_JEB174862C29","doi-asserted-by":"publisher","first-page":"188","DOI":"10.1134\/S0012496612030143","article-title":"Study of sleep in a walrus","volume":"444","author":"Lyamin","year":"2012","journal-title":"Dokl. Biol. Sci."},{"key":"2021042422470644400_JEB174862C30","doi-asserted-by":"publisher","first-page":"2000","DOI":"10.1016\/j.cub.2018.05.022","article-title":"Fur seals suppress REM sleep for very long periods without subsequent rebound","volume":"28","author":"Lyamin","year":"2018","journal-title":"Curr. Biol."},{"key":"2021042422470644400_JEB174862C31","doi-asserted-by":"publisher","first-page":"140","DOI":"10.1111\/j.1365-2869.2008.00636.x","article-title":"Increased EEG spectral power density during sleep following short-term sleep deprivation in pigeons (Columba livia): evidence for avian sleep homeostasis","volume":"17","author":"Martinez-Gonzalez","year":"2008","journal-title":"J. Sleep Res."},{"key":"2021042422470644400_JEB174862C32","doi-asserted-by":"publisher","first-page":"221","DOI":"10.2147\/NSS.S71970","article-title":"Unihemispheric sleep and asymmetrical sleep: behavioral, neurophysiological, and functional perspectives","volume":"8","author":"Mascetti","year":"2016","journal-title":"Nat. Sci. Sleep"},{"key":"2021042422470644400_JEB174862C33","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1017\/CBO9780511921179.010","article-title":"A systems-level approach to human REM sleep","volume-title":"Rapid Eye Movement Sleep: Regulation and Function","author":"Matarazzo","year":"2011"},{"key":"2021042422470644400_JEB174862C34","first-page":"185","article-title":"Behavioral sleep in Octopus vulgaris","volume":"61","author":"Meisel","year":"2011","journal-title":"Vie Et Milieu-Life and Environment"},{"key":"2021042422470644400_JEB174862C35","doi-asserted-by":"publisher","first-page":"473","DOI":"10.1017\/S1464793101005772","article-title":"Cephalopod chromatophores: neurobiology and natural history","volume":"76","author":"Messenger","year":"2001","journal-title":"Biol. Rev."},{"key":"2021042422470644400_JEB174862C36","first-page":"567","article-title":"Relationships between phenomena of paradoxical sleep and their counterparts in wakefulness","volume":"39","author":"Morrison","year":"1979","journal-title":"Acta Neurobiol. Exp. (Wars.)"},{"key":"2021042422470644400_JEB174862C37","doi-asserted-by":"publisher","first-page":"2984","DOI":"10.1016\/j.cub.2017.08.014","article-title":"The jellyfish Cassiopea exhibits a sleep-like state","volume":"27","author":"Nath","year":"2017","journal-title":"Curr. Biol."},{"key":"2021042422470644400_JEB174862C38","volume-title":"The Brains and Lives of Cephalopods","author":"Nixon","year":"2003"},{"key":"2021042422470644400_JEB174862C39","doi-asserted-by":"publisher","first-page":"559","DOI":"10.1016\/S1568-1637(02)00014-4","article-title":"Senescence, sleep, and circadian rhythms","volume":"1","author":"Pandi-Perumal","year":"2002","journal-title":"Ageing Res. Rev."},{"key":"2021042422470644400_JEB174862C40","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1093\/bioinformatics\/btg412","article-title":"APE: analyses of phylogenetics and evolution in R language","volume":"20","author":"Paradis","year":"2004","journal-title":"Bioinformatics"},{"key":"2021042422470644400_JEB174862C41","doi-asserted-by":"publisher","first-page":"80","DOI":"10.1016\/j.bbr.2009.01.033","article-title":"Behavioral sleep in the walrus","volume":"201","author":"Pryaslova","year":"2009","journal-title":"Behav. Brain Res."},{"key":"2021042422470644400_JEB174862C42","doi-asserted-by":"publisher","first-page":"569","DOI":"10.1038\/nature06535","article-title":"Lethargus is a Caenorhabditis elegans sleep-like state","volume":"451","author":"Raizen","year":"2008","journal-title":"Nature"},{"key":"2021042422470644400_JEB174862C43","doi-asserted-by":"publisher","first-page":"11857","DOI":"10.1073\/pnas.0402015101","article-title":"Slow wave sleep in crayfish","volume":"101","author":"Ramon","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2021042422470644400_JEB174862C44","doi-asserted-by":"publisher","first-page":"12468","DOI":"10.1038\/ncomms12468","article-title":"Evidence that birds sleep in mid-flight","volume":"7","author":"Rattenborg","year":"2016","journal-title":"Nat. Commun."},{"key":"2021042422470644400_JEB174862C45","author":"Sarda-Espinosa","year":"2016"},{"key":"2021042422470644400_JEB174862C46","doi-asserted-by":"publisher","first-page":"1834","DOI":"10.1126\/science.287.5459.1834","article-title":"Correlates of sleep and waking in Drosophila melanogaster","volume":"287","author":"Shaw","year":"2000","journal-title":"Science"},{"key":"2021042422470644400_JEB174862C47","doi-asserted-by":"publisher","first-page":"590","DOI":"10.1126\/science.aaf3621","article-title":"Slow waves, sharp waves, ripples, and REM in sleeping dragons","volume":"352","author":"Shein-Idelson","year":"2016","journal-title":"Science"},{"key":"2021042422470644400_JEB174862C48","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1016\/0166-4328(95)00023-M","article-title":"Phylogeny and the function of REM sleep","volume":"69","author":"Siegel","year":"1995","journal-title":"Behav. Brain Res."},{"key":"2021042422470644400_JEB174862C49","doi-asserted-by":"publisher","first-page":"208","DOI":"10.1016\/j.tins.2008.02.001","article-title":"Do all animals sleep?","volume":"31","author":"Siegel","year":"2008","journal-title":"Trends Neurosci."},{"key":"2021042422470644400_JEB174862C50","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1086\/BBLv225n3p161","article-title":"Defensive responses of cuttlefish to different teleost predators","volume":"225","author":"Staudinger","year":"2013","journal-title":"Biol. Bull."},{"key":"2021042422470644400_JEB174862C51","volume-title":"The Neuroscience of Sleep","author":"Stickgold","year":"2010"},{"key":"2021042422470644400_JEB174862C52","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1007\/978-1-4614-7599-6_2","article-title":"Evolution and comparative physiology of sleep in animals","volume-title":"Clinical Physiology of Sleep","author":"Tobler","year":"1988"},{"key":"2021042422470644400_JEB174862C53","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1016\/0166-4328(95)00025-o","article-title":"Is sleep fundamentally different between mammalian-species?","volume":"69","author":"Tobler","year":"1995","journal-title":"Behav. Brain Res."},{"key":"2021042422470644400_JEB174862C54","doi-asserted-by":"publisher","first-page":"195","DOI":"10.1016\/S0091-6773(72)80199-8","article-title":"Sleep in the domestic pigeon (Columba livia)","volume":"7","author":"Walker","year":"1972","journal-title":"Behav. Biol."}],"container-title":["Journal of Experimental Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/syndication.highwire.org\/content\/doi\/10.1242\/jeb.174862","content-type":"unspecified","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/jeb\/article-pdf\/doi\/10.1242\/jeb.174862\/1908287\/jeb174862.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/jeb\/article-pdf\/doi\/10.1242\/jeb.174862\/2041604\/jeb_174862v1.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/jeb\/article-pdf\/doi\/10.1242\/jeb.174862\/2041604\/jeb_174862v1.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,5,18]],"date-time":"2021-05-18T19:15:12Z","timestamp":1621365312000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/jeb\/article\/doi\/10.1242\/jeb.174862\/262916\/Cyclic-nature-of-the-REM-sleep-like-state-in-the"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,1,1]]},"references-count":54,"URL":"https:\/\/doi.org\/10.1242\/jeb.174862","relation":{},"ISSN":["1477-9145","0022-0949"],"issn-type":[{"value":"1477-9145","type":"electronic"},{"value":"0022-0949","type":"print"}],"subject":[],"published":{"date-parts":[[2018,1,1]]},"article-number":"jeb.174862"}}