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. 2012 Dec 7;28(6):746–758. doi: 10.1007/s12264-012-1285-8

Sleep alterations in mammals: Did aquatic conditions inhibit rapid eye movement sleep?

Vibha Madan 1, Sushil K Jha 1,✉
PMCID: PMC5561822  PMID: 23225315

Abstract

Sleep has been studied widely in mammals and to some extent in other vertebrates. Higher vertebrates such as birds and mammals have evolved an inimitable rapid eye movement (REM) sleep state. During REM sleep, postural muscles become atonic and the temperature regulating machinery remains suspended. Although REM sleep is present in almost all the terrestrial mammals, the aquatic mammals have either radically reduced or completely eliminated REM sleep. Further, we found a significant negative correlation between REM sleep and the adaptation of the organism to live on land or in water. The amount of REM sleep is highest in terrestrial mammals, significantly reduced in semi-aquatic mammals and completely absent or negligible in aquatic mammals. The aquatic mammals are obligate swimmers and have to surface at regular intervals for air. Also, these animals live in thermally challenging environments, where the conductive heat loss is approximately ∼90 times greater than air. Therefore, they have to be moving most of the time. As an adaptation, they have evolved unihemispheric sleep, during which they can rove as well as rest. A condition that immobilizes muscle activity and suspends the thermoregulatory machinery, as happens during REM sleep, is not suitable for these animals. It is possible that, in accord with Darwin’s theory, aquatic mammals might have abolished REM sleep with time. In this review, we discuss the possibility of the intrinsic role of aquatic conditions in the elimination of REM sleep in the aquatic mammals.

Keywords: aquatic mammals, aquatic adaptation, mammalian sleep, phylogenetic evolution

References

  • [1].Zepelin H., Siegel J.M., Tobler I. Mammalian Sleep. In: Kryger M.H., Roth T., Dement W.C., editors. Principles and Practice of Sleep Medicine. Philadelphia: WB Saunders Company; 2005. pp. 91–100. [Google Scholar]
  • [2].Rattenborg N.C. Evolution of slow-wave sleep and palliopallial connectivity in mammals and birds: a hypothesis. Brain Res Bull. 2006;69:20–29. doi: 10.1016/j.brainresbull.2005.11.002. [DOI] [PubMed] [Google Scholar]
  • [3].Gonzalez J., Gamundi A., Rial R., Nicolau M.C., de Vera L., Pereda E. Nonlinear, fractal, and spectral analysis of the EEG of lizard, Gallotia galloti. Am J Physiol. 1999;277:R86–93. doi: 10.1152/ajpregu.1999.277.1.R86. [DOI] [PubMed] [Google Scholar]
  • [4].Lazarev S.G. Electroencephalographic analysis of wakefulness and the primary form of sleep in the frog, Rana temporaria. Zh Evol Biokhim Fiziol. 1978;14:379–384. [PubMed] [Google Scholar]
  • [5].Nitz D.A., van Swinderen B., Tononi G., Greenspan R.J. Electrophysiological correlates of rest and activity in Drosophila melanogaster. Curr Biol. 2002;12:1934–1940. doi: 10.1016/S0960-9822(02)01300-3. [DOI] [PubMed] [Google Scholar]
  • [6].Ramon F., Hernandez-Falcon J., Nguyen B., Bullock T.H. Slow wave sleep in crayfish. Proc Natl Acad Sci U S A. 2004;101:11857–11861. doi: 10.1073/pnas.0402015101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [7].Hartse K.M. Sleep in insects and non-mammalian vertebrates. In: Kryger M.H., Roth T., Dement W.C., editors. Principles and Practice of Sleep Medicine. Philadelphia: WB Saunders Company; 1989. pp. 64–73. [Google Scholar]
  • [8].Roth T.C., 2nd, Lesku J.A., Amlaner C.J., Lima S.L. A phylogenetic analysis of the correlates of sleep in birds. J Sleep Res. 2006;15:395–402. doi: 10.1111/j.1365-2869.2006.00559.x. [DOI] [PubMed] [Google Scholar]
  • [9].Cirelli C. The genetic and molecular regulation of sleep: from fruit flies to humans. Nat Rev Neurosci. 2009;10:549–560. doi: 10.1038/nrn2683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [10].Cirelli C., Tononi G. Is sleep essential? PLoS Biol. 2008;6:e216. doi: 10.1371/journal.pbio.0060216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [11].Lesku J.A., Meyer L.C., Fuller A., Maloney S.K., Dell’Omo G., Vyssotski A.L., et al. Ostriches sleep like platypuses. PLoS One. 2011;6:e23203. doi: 10.1371/journal.pone.0023203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [12].Siegel J.M., Manger P.R., Nienhuis R., Fahringer H.M., Shalita T., Pettigrew J.D. Sleep in the platypus. Neuroscience. 1999;91:391–400. doi: 10.1016/S0306-4522(98)00588-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [13].van Twyver H., Allison T. Sleep in the opossum Didelphis marsupialis. Electroencephalogr Clin Neurophysiol. 1970;29:181–189. doi: 10.1016/0013-4694(70)90121-5. [DOI] [PubMed] [Google Scholar]
  • [14].Jha S.K., Coleman T., Frank M.G. Sleep and sleep regulation in the ferret (Mustela putorius furo) Behav Brain Res. 2006;172:106–113. doi: 10.1016/j.bbr.2006.05.001. [DOI] [PubMed] [Google Scholar]
  • [15].Flanigan W.F., Jr. Sleep and wakefulness in iguanid lizards, Ctenosaura pectinata and Iguana iguana. Brain Behav Evol. 1973;8:401–436. doi: 10.1159/000124366. [DOI] [PubMed] [Google Scholar]
  • [16].Aserinsky E., Kleitman N. Regularly occurring periods of eye motility, and concomitant phenomena, during sleep. Science. 1953;118:273–274. doi: 10.1126/science.118.3062.273. [DOI] [PubMed] [Google Scholar]
  • [17].Aserinsky E., Kleitman N. Regularly occurring periods of eye motility, and concomitant phenomena, during sleep. 1953. J Neuropsychiatry Clin Neurosci. 2003;15:454–455. doi: 10.1176/appi.neuropsych.15.4.454. [DOI] [PubMed] [Google Scholar]
  • [18].Aserinsky E., Kleitman N. Two types of ocular motility occurring in sleep. J Appl Physiol. 1955;8:1–10. doi: 10.1152/jappl.1955.8.1.1. [DOI] [PubMed] [Google Scholar]
  • [19].Dement W., Kleitman N. Cyclic variations in EEG during sleep and their relation to eye movements, body motility, and dreaming. Electroencephalogr Clin Neurophysiol. 1957;9:673–690. doi: 10.1016/0013-4694(57)90088-3. [DOI] [PubMed] [Google Scholar]
  • [20].Dement W. The occurrence of low voltage, fast, electroencephalogram patterns during behavioral sleep in the cat. Electroencephalogr Clin Neurophysiol. 1958;10:291–296. doi: 10.1016/0013-4694(58)90037-3. [DOI] [PubMed] [Google Scholar]
  • [21].Jouvet M., Michel F., Courjon J. Sur un stade d’activité électrique cérébrale rapide au cours du sommeil physiologique. C R Soc Biol. 1959;153:1024–1028. [Google Scholar]
  • [22].Sawyer C.H., Kawakami M. Characteristics of behavioral and electroencephalographic after-reactions to copulation and vaginal stimulation in the female rabbit. Endocrinology. 1959;65:622–630. doi: 10.1210/endo-65-4-622. [DOI] [PubMed] [Google Scholar]
  • [23].Shimazono Y., Horie T., Yanagisawa Y., Hori N., Chikazawa S., Shozuka K. The correlation of the rhythmic waves of the hippocampus with the behaviors of dogs. Neurologia. 1960;2:82–88. [Google Scholar]
  • [24].Weitzmann E.D. A note on the EEG and eye movements during behavioral sleep in monkeys. Electroencephalogr Clin Neurophysiol. 1961;17:376–381. [Google Scholar]
  • [25].Michel F., Klein M., Jouvet M., Valatx J.L. Etude polygraphique du sommeil chez le Rat. C R Soc Biol. 1961;155:2389–2392. [Google Scholar]
  • [26].Weiss T., Fifkova E. Sleep cycles in mice. Physiol Bohemoslov. 1964;13:242–245. [PubMed] [Google Scholar]
  • [27].Gottesmann C. The golden age of rapid eye movement sleep discoveries. 1. Lucretius—1964. Prog Neurobiol. 2001;65:211–287. doi: 10.1016/S0301-0082(01)00014-4. [DOI] [PubMed] [Google Scholar]
  • [28].Ookawa T., Gotoh J. Electroencephalographic study of chickens: Periodic recurrence of low voltage and fast waves during behavioral sleep. Poultry Sci. 1964;43:1603–1604. doi: 10.3382/ps.0431603. [DOI] [Google Scholar]
  • [29].Klein M., Michel F., Jouvet M. Etude polygraphique du sommeil chez les oiseaux. C R Soc Biol (Paris) 1964;158:99–103. [PubMed] [Google Scholar]
  • [30].Rojas-Ramirez J.A., Tauber E.S. Paradoxical sleep in two species of avian predator (Falconiformes) Science. 1970;167:1754–1755. doi: 10.1126/science.167.3926.1754. [DOI] [PubMed] [Google Scholar]
  • [31].Tradardi V. Sleep in the pigeon. Arch Ital Biol. 1966;104:516–521. [PubMed] [Google Scholar]
  • [32].Van Twyver H., Allison T. A polygraphic and behavioral study of sleep in the pigeon (Columba livia) Exp Neurol. 1972;35:138–153. doi: 10.1016/0014-4886(72)90065-9. [DOI] [PubMed] [Google Scholar]
  • [33].Walker J.M., Berger R.J. Sleep in the domestic pigeon (Columba livia) Behav Biol. 1972;7:195–203. doi: 10.1016/S0091-6773(72)80199-8. [DOI] [PubMed] [Google Scholar]
  • [34].Amlaner C.J., Ball N.J. Avian sleep. In: Kryger M.H., Roth T., Dement W.C., editors. Principles and Practice of Sleep Medicine. Philadelphia: W.B. Saunders Company; 1994. pp. 81–94. [Google Scholar]
  • [35].Huntley A.C., Friedmann J.K., Cohen H.B. Sleep in an Iguanid lizard, Dipsosaurus dorsalis. Sleep Res. 1977;6:104. [Google Scholar]
  • [36].Goldman A.S. Evolution of the mammary gland defense system and the ontogeny of the immune system. J Mammary Gland Biol Neoplasia. 2002;7:277–289. doi: 10.1023/A:1022852700266. [DOI] [PubMed] [Google Scholar]
  • [37].Allison T., Van Twyver H., Goff W.R. Electrophysiological studies of the echidna, Tachyglossus aculeatus. I. Waking and sleep. Arch Ital Biol. 1972;110:145–184. [PubMed] [Google Scholar]
  • [38].Nicol S.C., Andersen N.A., Phillips N.H., Berger R.J. The echidna manifests typical characteristics of rapid eye movement sleep. Neurosci Lett. 2000;283:49–52. doi: 10.1016/S0304-3940(00)00922-8. [DOI] [PubMed] [Google Scholar]
  • [39].Ruckebusch Y. The relevance of drowsiness in the circadian cycle of farm animals. Anim Behav. 1972;20:637–643. doi: 10.1016/S0003-3472(72)80136-2. [DOI] [PubMed] [Google Scholar]
  • [40].Bell F.R., Itabisashi T. The electroencephalogram of sheep and goats with special reference to rumination. Physiol Behav. 1973;11:503–514. doi: 10.1016/0031-9384(73)90037-1. [DOI] [PubMed] [Google Scholar]
  • [41].Affanni J.M., Cervino C.O., Marcos H.J. Absence of penile erections during paradoxical sleep. Peculiar penile events during wakefulness and slow wave sleep in the armadillo. J Sleep Res. 2001;10:219–228. doi: 10.1046/j.1365-2869.2001.00259.x. [DOI] [PubMed] [Google Scholar]
  • [42].Siegel J.M. Clues to the functions of mammalian sleep. Nature. 2005;437:1264–1271. doi: 10.1038/nature04285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [43].Siegel J.M. Do all animals sleep? Trends Neurosci. 2008;31:208–213. doi: 10.1016/j.tins.2008.02.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [44].Lyamin O., Oleksenko A.I., Sevostiyanov V.F., Nazarenko E.A., Mukhametov L.M. Behavioral sleep in captive sea otters. Aquatic Mammals. 2000;26:132–136. [Google Scholar]
  • [45].Lyamin O.I., Chetyrbok I.S. Unilateral EEG activation during sleep in the Cape fur seal, Arctocephalus pusillus. Neurosci Lett. 1992;143:263–266. doi: 10.1016/0304-3940(92)90279-G. [DOI] [PubMed] [Google Scholar]
  • [46].Lyamin O.I., Mukhametov L.M., Chetyrbok I.S., Vassiliev A.V. Sleep and wakefulness in the southern sea lion. Behav Brain Res. 2002;128:129–138. doi: 10.1016/S0166-4328(01)00317-5. [DOI] [PubMed] [Google Scholar]
  • [47].Lyamin O.I., Kosenko P.O., Vyssotski A.L., Lapierre J.L., Siegel J.M., Mukhametov L.M. Study of sleep in a walrus. Dokl Biol Sci. 2012;444:188–191. doi: 10.1134/S0012496612030143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [48].Pryaslova J.P., Lyamin O.I., Siegel J.M., Mukhametov L.M. Behavioral sleep in the walrus. Behav Brain Res. 2009;201:80–87. doi: 10.1016/j.bbr.2009.01.033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [49].Mukhametov L.M., Supin A., Poliakova I.G. Sleep of Caspian seals. Zh Vyssh Nerv Deiat Im I P Pavlova. 1984;34:259–264. [PubMed] [Google Scholar]
  • [50].Lyamin O.I. Sleep in the harp seal (Pagophilus groenlandica). Comparison of sleep on land and in water. J Sleep Res. 1993;2:170–174. doi: 10.1111/j.1365-2869.1993.tb00082.x. [DOI] [PubMed] [Google Scholar]
  • [51].Castellini M.A., Milsom W.K., Berger R.J., Costa D.P., Jones D.R., Castellini J.M., et al. Patterns of respiration and heart rate during wakefulness and sleep in elephant seal pups. Am J Physiol. 1994;266:R863–869. doi: 10.1152/ajpregu.1994.266.3.R863. [DOI] [PubMed] [Google Scholar]
  • [52].Ridgway S.H., Harrison R.J., Joyce P.L. Sleep and cardiac rhythm in the gray seal. Science. 1975;187:553–555. doi: 10.1126/science.163484. [DOI] [PubMed] [Google Scholar]
  • [53].Mukhametov L.M., Liamin O.I., Poliakova I.G. Sleep and wakefulness in Callorhinus ursinus. Zh Vyssh Nerv Deiat Im I P Pavlova. 1984;34:465–471. [PubMed] [Google Scholar]
  • [54].Mukhametov L.M., Lyamin O., Polyakova I.G. Interhemispheric asynchrony of the sleep EEG in northern fur seal. Experientia. 1985;41:1034–1035. doi: 10.1007/BF01952128. [DOI] [PubMed] [Google Scholar]
  • [55].Lyamin O., Mukhametov L.M. Organization of sleep in the northern fur seal. In: Sokolov V.E., Aristov A.A., Lisitzina T.U., editors. The Northern Fur Seal. Systematic, Morphology, Ecology, Behavior. Moscow: Nauka; 1998. pp. 280–302. [Google Scholar]
  • [56].Lyamin O.I., Manger P.R., Ridgway S.H., Mukhametov L.M., Siegel J.M. Cetacean sleep: an unusual form of mammalian sleep. Neurosci Biobehav Rev. 2008;32:1451–1484. doi: 10.1016/j.neubiorev.2008.05.023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [57].Lilly J.C. Animals in the aquatic environments: adaptations of mammals to the ocean. In: Dill D.B., editor. Handbook of Physiology-Environment. Washington DC: American Physiology Society; 1964. pp. 741–747. [Google Scholar]
  • [58].Mukhametov L.M., Supin A. An EEG study of different behavioral states of freely moving dolphins. Zh Vyssh Nerv Deiat Im I P Pavlova. 1975;25:396–401. [PubMed] [Google Scholar]
  • [59].Shurley J.T., Serafetinides E.A., Brooks R.E., Elsner R., Kenney D.W. Sleep in Cetaceans: The pilot whale, Globicephala scammoni. Psychophysiology (abstract) 1969;6:230. [Google Scholar]
  • [60].Mukhametov L.M., Oleksenko A.I., Poliakova I.G. Quantification of ECoG stages of sleep in the bottlenose dolphin. Neurophysiology. 1988;20:532–538. doi: 10.1007/BF02198450. [DOI] [PubMed] [Google Scholar]
  • [61].Mukhametov L.M., Poliakova I.G. Electroencephalographic study of sleep in Sea of Azov porpoises. Zh Vyssh Nerv Deiat Im I P Pavlova. 1981;31:333–339. [PubMed] [Google Scholar]
  • [62].Mukhametov L.M. Unihemispheric slow-wave sleep in the Amazonian dolphin, Inia geoffrensis. Neurosci Lett. 1987;79:128–132. doi: 10.1016/0304-3940(87)90684-7. [DOI] [PubMed] [Google Scholar]
  • [63].Lyamin O.I., Mukhametov L.M., Siegel J.M., Nazarenko E.A., Polyakova I.G., Shpak O.V. Unihemispheric slow wave sleep and the state of the eyes in a white whale. Behav Brain Res. 2002;129:125–129. doi: 10.1016/S0166-4328(01)00346-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [64].Mukhametov L.M., Lyamin O.I., Chetyrbok I.S., Vassilyev A.A., Diaz R.P. Sleep in an Amazonian manatee, Trichechus inunguis. Experientia. 1992;48:417–419. doi: 10.1007/BF01923447. [DOI] [PubMed] [Google Scholar]
  • [65].Zepelin H. Mammalian sleep. In: Dement W.C., editor. Principles and Practice of Sleep Medicin. Philadelphia: Saunderes Company; 1989. pp. 30–49. [Google Scholar]
  • [66].Rechtschaffen A., Bergmann B.M. Sleep deprivation in the rat: an update of the 1989 paper. Sleep. 2002;25:18–24. doi: 10.1093/sleep/25.1.18. [DOI] [PubMed] [Google Scholar]
  • [67].Mallick B.N., Siegel J.M., Fahringer H. Changes in pontine unit activity with REM sleep deprivation. Brain Res. 1990;515:94–98. doi: 10.1016/0006-8993(90)90581-U. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [68].Newman S.M., Paletz E.M., Rattenborg N.C., Obermeyer W.H., Benca R.M. Sleep deprivation in the pigeon using the Disk-Over-Water method. Physiol Behav. 2008;93:50–58. doi: 10.1016/j.physbeh.2007.07.012. [DOI] [PubMed] [Google Scholar]
  • [69].Machado R.B., Hipolide D.C., Benedito-Silva A.A., Tufik S. Sleep deprivation induced by the modified multiple platform technique: quantification of sleep loss and recovery. Brain Res. 2004;1004:45–51. doi: 10.1016/j.brainres.2004.01.019. [DOI] [PubMed] [Google Scholar]
  • [70].Jha S.K., Brennan F.X., Pawlyk A.C., Ross R.J., Morrison A.R. REM sleep: a sensitive index of fear conditioning in rats. Eur J Neurosci. 2005;21:1077–1080. doi: 10.1111/j.1460-9568.2005.03920.x. [DOI] [PubMed] [Google Scholar]
  • [71].Parmeggiani P.L. Physiologic regulation in sleep. In: Kryger M.H., Roth T., Dement W., editors. Principles and Practice of Sleep Medicine. Philadelphia: Elsevier Saunders; 2005. pp. 154–168. [Google Scholar]
  • [72].Chase M.H., Morales F.R. Controls of motoneurons during sleep. In: Kryger M.H., Roth T., Dement W., editors. Principles and Practice of Sleep Medicine. Philadelphia: Elsevier Saunders; 2005. pp. 154–168. [Google Scholar]
  • [73].Lyamin O., Pryaslova J., Lance V., Siegel J. Animal behaviour: continuous activity in cetaceans after birth. Nature. 2005;435:1177. doi: 10.1038/4351177a. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [74].Walker J.M., Berger R.J. The ontogenesis of sleep states, thermogenesis, and thermoregulation in the Virginia opossum. Dev Psychobiol. 1980;13:443–454. doi: 10.1002/dev.420130502. [DOI] [PubMed] [Google Scholar]
  • [75].Affanni J. Observations on the sleep of some South American marsupials and edentates. Perspect Brain Sci. 1972;1:21–23. [Google Scholar]
  • [76].Elgar M.A., Pagel M.D., Harvey P.H. Sources of variation in mammalian sleep. Animal Behavior. 1990;40:991–995. doi: 10.1016/S0003-3472(05)81006-1. [DOI] [Google Scholar]
  • [77].Zepelin H., Rechtschaffen A. Mammalian sleep, longevity, and energy metabolism. Brain Behav Evol. 1974;10:425–470. doi: 10.1159/000124330. [DOI] [PubMed] [Google Scholar]
  • [78].Prudom A.E., Klemm W.R. Electrographic correlates of sleep behavior in a primitive mammal, the armadillo Dasypus novemcinctus. Physiol Behav. 1973;10:275–282. doi: 10.1016/0031-9384(73)90310-7. [DOI] [PubMed] [Google Scholar]
  • [79].Tobler I., Jaggi K. Sleep and EEG spectra in the Syrian hamster (Mesocricetus auratus) under baseline conditions and following sleep deprivation. J Comp Physiol A. 1987;161:449–459. doi: 10.1007/BF00603970. [DOI] [PubMed] [Google Scholar]
  • [80].Van Twyver H. Sleep patterns of five rodent species. Pysiol Behav. 1969;4:901–905. doi: 10.1016/0031-9384(69)90038-9. [DOI] [Google Scholar]
  • [81].Chepkasov I.E. Daily rhythm of sleep and wakefulness in the arctic ground squirrel Citellus parryi during the summer season. J Evol Biochem Physiol. 1980;17:77–80. [Google Scholar]
  • [82].Ursin R. The two stages of slow wave sleep in the cat and their relation to REM sleep. Brain Res. 1968;11:347–356. doi: 10.1016/0006-8993(68)90030-9. [DOI] [PubMed] [Google Scholar]
  • [83].Karmanova I.G., Maksimuk F.M., Murav’eva L.N., Pastukhov Y.F., Sazonov V.S. Specific features of the cycle ‘wakefulness-sleep’ in the arctic lemming Dicrostonyx torquatus. J Evol Biochem Physiol. 1979;15:190–195. [Google Scholar]
  • [84].Walker J.M., Walker L.E., Harris D.V., Berger R.J. Cessation of thermoregulation during REM sleep in the pocket mouse. Am J Physiol. 1983;244:R114–118. doi: 10.1152/ajpregu.1983.244.1.R114. [DOI] [PubMed] [Google Scholar]
  • [85].Walker J.M., Glotzbach S.F., Berger R.J., Heller H.C. Sleep and hibernation in ground squirrels (Citellus spp): electrophysiological observations. Am J Physiol. 1977;233:R213–221. doi: 10.1152/ajpregu.1977.233.5.R213. [DOI] [PubMed] [Google Scholar]
  • [86].Dijk D.J., Daan S. Sleep EEG spectral analysis in a diurnal rodent: Eutamias sibiricus. J Comp Physiol A. 1989;165:205–215. doi: 10.1007/BF00619195. [DOI] [PubMed] [Google Scholar]
  • [87].Snyder F., Bugbee N., Douthitt T.C. Telemetric studies of 24-hour sleep-waking patterns in some primitive mammals. Psychophysiology. 1972;9:122. [Google Scholar]
  • [88].Tauber E.S., Michel F., Roffwarg H.P. Preliminary note on the sleep and waking cycle in the desert hedgehog (Paraechinus hypomelas) Psychophysiology. 1968;5:201. [Google Scholar]
  • [89].Sakaguchi S., Glotzbach S.F., Heller H.C. Influence of hypothalamic and ambient temperatures on sleep in kangaroo rats. Am J Physiol. 1979;237:R80–88. doi: 10.1152/ajpregu.1979.237.1.R80. [DOI] [PubMed] [Google Scholar]
  • [90].Robert S., Dallaire A. Polygraphic analysis of the sleep-wake states and the REM sleep periodicity in domesticated pigs (Sus scrofa) Physiol Behav. 1986;37:289–293. doi: 10.1016/0031-9384(86)90235-0. [DOI] [PubMed] [Google Scholar]
  • [91].Berger R.J., Walker J.M. A polygraphic study of sleep in the tree shrew (Tupaia glis) Brain Behav Evol. 1972;5:54–69. doi: 10.1159/000123737. [DOI] [PubMed] [Google Scholar]
  • [92].Dallaire A., Ruckebusch Y. Rest-activity cycle and sleep patterns in captive foxes (Vulpes vulpes) Experientia. 1974;30:59–60. doi: 10.1007/BF01921597. [DOI] [Google Scholar]
  • [93].Elgar M.A., Pagel M.D., Harvey P.H. Sleep in mammals. Anim Behav. 1988;36:1407–1419. doi: 10.1016/S0003-3472(88)80211-2. [DOI] [Google Scholar]
  • [94].Allison T., Gerber S.D., Breedlove S.M., Dryden G.L. A behavioral and polygraphic study of sleep in the shrews Suncus murinus, Blarina brevicauda, and Cryptotis parva. Behav Biol. 1977;20:354–366. doi: 10.1016/S0091-6773(77)90909-9. [DOI] [PubMed] [Google Scholar]
  • [95].Susic V., Masirevic G. Sleep patterns in the Mongolian gerbil, Meriones unguiculatus. Physiol Behav. 1986;37:257–261. doi: 10.1016/0031-9384(86)90229-5. [DOI] [PubMed] [Google Scholar]
  • [96].Allison T., Van Twyver H. Sleep in the moles, Scalopus aquaticus and Condylura cristata. Exp Neurol. 1970;27:564–578. doi: 10.1016/0014-4886(70)90117-2. [DOI] [PubMed] [Google Scholar]
  • [97].Deboer T., Franken P., Tobler I. Sleep and cortical temperature in the Djungarian hamster under baseline conditions and after sleep deprivation. J Comp Physiol A. 1994;174:145–155. doi: 10.1007/BF00193782. [DOI] [PubMed] [Google Scholar]
  • [98].Meddis R. The evolution of sleep. In: Mayes A., editor. Sleep Mechanisms and Functions. Berkshire: Van Nostrand Renihold; 1983. pp. 57–95. [Google Scholar]
  • [99].Brebbia D.R., Pyne E.T. Environmental hypothermia and cerebral electrical activity in the little brown bat, Myotis lucifugus. Psychophysiology. 1972;9:122. [Google Scholar]
  • [100].Tobler I., Deboer T. Sleep in the blind mole rat Spalax ehrenbergi. Sleep. 2001;24:147–154. [PubMed] [Google Scholar]
  • [101].Ayala-Guerrero F., Vargas-Reyna L., Ramos J.I., Mexicano G. Sleep patterns of the volcano mouse (Neotomodon alstoni alstoni) Physiol Behav. 1998;64:577–580. doi: 10.1016/S0031-9384(98)00081-X. [DOI] [PubMed] [Google Scholar]
  • [102].LoPresti R.W., McGinty D.J. Sleep in the phalanger (Trichosurus vulpecula): an Australian marsupial. Psychophysiology. 1970;7:304. [Google Scholar]
  • [103].McNew J.J., Howe R.C., Adey W.R. The sleep cycle and subcorticalcortical EEG relations to the unrestrained chimpanzee. Electroencephalogr Clin Neurophysiol. 1971;30:489–503. doi: 10.1016/0013-4694(71)90146-5. [DOI] [PubMed] [Google Scholar]
  • [104].Crofts H.S., Wilson S., Muggleton N.G., Nutt D.J., Scott E.A., Pearce P.C. Investigation of the sleep electrocorticogram of the common marmoset (Callithrix jacchus) using radiotelemetry. Clin Neurophysiol. 2001;112:2265–2273. doi: 10.1016/S1388-2457(01)00699-X. [DOI] [PubMed] [Google Scholar]
  • [105].Lucas E.A., Powell E.W. Murphree OD. Baseline sleep-wake patterns in the pointer dog. Physiol Behav. 1977;19:285–291. doi: 10.1016/0031-9384(77)90340-7. [DOI] [PubMed] [Google Scholar]
  • [106].Copley M.P., Jennings D.P., Mitler M.M. A study of continuous forty-eight hour sleep waking recordings in five dogs. Sleep Res. 1976;5:94. [Google Scholar]
  • [107].Leinonen L., Stenberg D. Sleep in Macaca arctoides and the effects of prazosin. Physiol Behav. 1986;37:199–202. doi: 10.1016/0031-9384(86)90221-0. [DOI] [PubMed] [Google Scholar]
  • [108].Barre V., Petter-Rousseaux A. Seasonal variations in sleep-wake cycle in Microcebus murinus. Primates. 1988;29:53–64. doi: 10.1007/BF02380849. [DOI] [Google Scholar]
  • [109].Bert J. Similarities and differences in the sleep of two baboons, Papio hamadryas and Papio papio. Electroenceph Clin Neurophysiol. 1973;39:657–662. doi: 10.1016/0013-4694(75)90079-6. [DOI] [PubMed] [Google Scholar]
  • [110].De Moura Filho A.G., Huggins S.E., Lines S.G. Sleep and waking in the three-toed sloth, Bradypus tridactylus. Comp Biochem Physiol A Comp Physiol. 1983;76:345–355. doi: 10.1016/0300-9629(83)90336-5. [DOI] [PubMed] [Google Scholar]
  • [111].Zhao X., Sun H., Tang Z., Flanders J., Zhang S., Ma Y. Characterization of the sleep architecture in two species of fruit bat. Behav Brain Res. 2010;208:497–501. doi: 10.1016/j.bbr.2009.12.027. [DOI] [PubMed] [Google Scholar]
  • [112].Pivik R.T., Bylsma F.W., Cooper P. Sleep-wakefulness rhythms in the rabbit. Behav Neural Biol. 1986;45:275–286. doi: 10.1016/S0163-1047(86)80016-4. [DOI] [PubMed] [Google Scholar]
  • [113].Gonzalez F.F., Zaplana J., Ruiz de Elvira C., Delgado J.M. Nocturnal and diurnal sleep in Macaca sylvana. Electroencephalogr Clin Neurophysiol. 1979;46:13–28. doi: 10.1016/0013-4694(79)90045-2. [DOI] [PubMed] [Google Scholar]
  • [114].Reite M.L., Rhodes J.M., Kavan E., Adey W.R. Normal sleep patterns in macaque monkey. Arch Neurol. 1965;12:133–144. doi: 10.1001/archneur.1965.00460260023003. [DOI] [PubMed] [Google Scholar]
  • [115].Ibuka N. Ontogenesis of circadian sleep-wakefulness rhythms and developmental changes of sleep in the altricial rat and in the precocial guinea pig. Behav Brain Res. 1984;11:185–196. doi: 10.1016/0166-4328(84)90210-9. [DOI] [PubMed] [Google Scholar]
  • [116].Bert J., Pegram V., Balzamo E. Comparison of sleep between two macaques (Macaca radiata and Macaca mulatta) Fol Primatol. 1972;17:202–208. doi: 10.1159/000155429. [DOI] [PubMed] [Google Scholar]
  • [117].Edgar D.M., Dement W.C., Fuller C.A. Effect of SCN lesions on sleep in squirrel monkeys: evidence for opponent processes in sleep-wake regulation. J Neurosci. 1993;13:1065–1079. doi: 10.1523/JNEUROSCI.13-03-01065.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [118].Balzamo E., Van Beers P., Lagarde D. Scoring of sleep and wakefulness by behavioral analysis from video recordings in rhesus monkeys: comparison with conventional EEG analysis. Electroencephalogr Clin Neurophysiol. 1998;106:206–212. doi: 10.1016/S0013-4694(97)00152-1. [DOI] [PubMed] [Google Scholar]
  • [119].Synder F. Sleep-waking patterns of Hyracoidea. Sleep Res. 1974;3:87. [Google Scholar]
  • [120].Bert J., Collomb H., Martino A. The electroencephalogram of sleep of a pro-simian. Its place in the organization of sleep in primates. Electroencephalogr Clin Neurophysiol. 1967;23:342–350. doi: 10.1016/0013-4694(67)90047-8. [DOI] [PubMed] [Google Scholar]
  • [121].Bert J., Pegram V. The sleep electroencephalogram in Cercopithecinae: Erythrocerbus patas and Cercopithecus aethiops sabaeus. Folia Primatol (Basel) 1969;11:151–159. doi: 10.1159/000155263. [DOI] [PubMed] [Google Scholar]
  • [122].Balzamo E., Vuillon-Caciuttolo G., Petter J.J., Bert J. States of vigilance in two Lemuridae: EEG patterns and organisation obtained using telemetry. Waking Sleeping. 1978;2:237–245. [Google Scholar]
  • [123].Balzamo E. Study of states of vigilance in adult Papio cynocephalus. C R Seances Soc Biol Fil. 1973;167:1168–1172. [PubMed] [Google Scholar]
  • [124].Astic L., Saucier D., Megirian D. Sleep circadian rhythm in rat kangaroo (Potorous apicalis): Effect of food distribution. Physiol Behav. 1979;22:441–446. doi: 10.1016/0031-9384(79)90006-4. [DOI] [PubMed] [Google Scholar]
  • [125].Mendelson W.B. The Octodon degu: a diurnal small mammal for sleep studies. Sleep Res. 1982;11:89. [Google Scholar]

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