Unraveling the Evolutionary Determinants of Sleep

Current Biology

Volumn 26, Issue 20, 2016, Pages R1073-R1087

  Joiner, William J ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b San Diego   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; EVOLUTION; INVERTEBRATE; PHYSIOLOGY; SLEEP; VERTEBRATE;

ANIMALS; BIOLOGICAL EVOLUTION; INVERTEBRATES; SLEEP; VERTEBRATES;

EID: 84994703292     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2016.08.068     Document Type: Review

References (210)

1. 1 Basner, M., Rao, H., Goel, N., Dinges, D.F., Sleep deprivation and neurobehavioral dynamics. Curr. Opin. Neurobiol. 23 (2013), 854–863.
2. 2 Gottlieb, D.J., Punjabi, N.M., Newman, A.B., Resnick, H.E., Redline, S., Baldwin, C.M., Nieto, F.J., Association of sleep time with diabetes mellitus and impaired glucose tolerance. Arch. Intern. Med. 165 (2005), 863–867.
3. 3 Gujar, N., Yoo, S.S., Hu, P., Walker, M.P., Sleep deprivation amplifies reactivity of brain reward networks, biasing the appraisal of positive emotional experiences. J. Neurosci. 31 (2011), 4466–4474.
4. 4 Irwin, M.R., Opp, M.R., Sleep-health: reciprocal regulation of sleep and innate immunity. Neuropsychopharmacology, 2016, 10.1038/npp.2016.148.
5. 5 Rechtschaffen, A., Gilliland, M.A., Bergmann, B.M., Winter, J.B., Physiological correlates of prolonged sleep deprivation in rats. Science 221 (1983), 182–184.
6. 6 Roehrs, T., Hyde, M., Blaisdell, B., Greenwald, M., Roth, T., Sleep loss and REM sleep loss are hyperalgesic. Sleep 29 (2006), 145–151.
7. 7 Schuh-Hofer, S., Wodarski, R., Pfau, D.B., Caspani, O., Magerl, W., Kennedy, J.D., Treede, R.D., One night of total sleep deprivation promotes a state of generalized hyperalgesia: a surrogate pain model to study the relationship of insomnia and pain. Pain 154 (2013), 1613–1621.
8. 8 Tobaldini, E., Costantino, G., Solbiati, M., Cogliati, C., Kara, T., Nobili, L., Montano, N., Sleep, sleep deprivation, autonomic nervous system and cardiovascular diseases. Neurosci. Biobehav. Rev., 2016, 10.1016/j.neubiorev.2016.07.004.
9. 9 Yoo, S.S., Gujar, N., Hu, P., Jolesz, F.A., Walker, M.P., The human emotional brain without sleep–a prefrontal amygdala disconnect. Curr. Biol. 17 (2007), R877–R878.
10. 10 Campbell, S.S., Tobler, I., Animal sleep: a review of sleep duration across phylogeny. Neurosci. Biobehav. Rev. 8 (1984), 269–300.
11. 11 Campbell, I.G., EEG recording and analysis for sleep research. Curr. Protoc. Neurosci., Chapter 10, 2009 Unit10 12.
12. 12 Massimini, M., Ferrarelli, F., Huber, R., Esser, S.K., Singh, H., Tononi, G., Breakdown of cortical effective connectivity during sleep. Science 309 (2005), 2228–2232.
13. 13 Amzica, F., Steriade, M., Electrophysiological correlates of sleep delta waves. Electroencephalogr. Clin. Neurophysiol. 107 (1998), 69–83.
14. 14 Borbely, A.A., A two process model of sleep regulation. Hum. Neurobiol. 1 (1982), 195–204.
15. 15 Daan, S., Beersma, D.G., Borbely, A.A., Timing of human sleep: recovery process gated by a circadian pacemaker. Am. J. Physiol. 246 (1984), R161–R183.
16. 16 Vetrivelan, R., Fuller, P.M., Tong, Q., Lu, J., Medullary circuitry regulating rapid eye movement sleep and motor atonia. J. Neurosci. 29 (2009), 9361–9369.
17. 17 Hendricks, J.C., Finn, S.M., Panckeri, K.A., Chavkin, J., Williams, J.A., Sehgal, A., Pack, A.I., Rest in Drosophila is a sleep-like state. Neuron 25 (2000), 129–138.
18. 18 Shaw, P.J., Cirelli, C., Greenspan, R.J., Tononi, G., Correlates of sleep and waking in Drosophila melanogaster. Science 287 (2000), 1834–1837.
19. 19 Donlea, J.M., Pimentel, D., Miesenbock, G., Neuronal machinery of sleep homeostasis in Drosophila. Neuron 81 (2014), 860–872.
20. 20 Raizen, D.M., Zimmerman, J.E., Maycock, M.H., Ta, U.D., You, Y.J., Sundaram, M.V., Pack, A.I., Lethargus is a Caenorhabditis elegans sleep-like state. Nature 451 (2008), 569–572.
21. 21 Cho, J.Y., Sternberg, P.W., Multilevel modulation of a sensory motor circuit during C. elegans sleep and arousal. Cell 156 (2014), 249–260.
22. 22 Turek, M., Besseling, J., Spies, J.P., Konig, S., Bringmann, H., Sleep-active neuron specification and sleep induction require FLP-11 neuropeptides to systemically induce sleep. Elife, 5, 2016, 10.7554/eLife.12499.
23. 23 Ramon, F., Hernandez-Falcon, J., Nguyen, B., Bullock, T.H., Slow wave sleep in crayfish. Proc. Natl. Acad. Sci. USA 101 (2004), 11857–11861.
24. 24 Vorster, A.P., Krishnan, H.C., Cirelli, C., Lyons, L.C., Characterization of sleep in Aplysia californica. Sleep 37 (2014), 1453–1463.
25. 25 Zhdanova, I.V., Wang, S.Y., Leclair, O.U., Danilova, N.P., Melatonin promotes sleep-like state in zebrafish. Brain Res. 903 (2001), 263–268.
26. 26 Naumann, E.A., Kampff, A.R., Prober, D.A., Schier, A.F., Engert, F., Monitoring neural activity with bioluminescence during natural behavior. Nat. Neurosci. 13 (2010), 513–520.
27. 27 Kryger, M.H., Roth, T., Dement, W.C., Principles and Practice of Sleep Medicine. 5th Edition, 2011, St. Louis, Mo., Elsevier/Saunders.
28. 28 Seidner, G., Robinson, J.E., Wu, M., Worden, K., Masek, P., Roberts, S.W., Keene, A.C., Joiner, W.J., Identification of neurons with a privileged role in sleep homeostasis in Drosophila melanogaster. Curr. Biol. 25 (2015), 2928–2938.
29. 29 Siegel, J.M., Clues to the functions of mammalian sleep. Nature 437 (2005), 1264–1271.
30. 30 Rattenborg, N.C., Amlaner, C.J., Lima, S.L., Behavioral, neurophysiological and evolutionary perspectives on unihemispheric sleep. Neurosci. Biobehav. Rev. 24 (2000), 817–842.
31. 31 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. 32 (2008), 1451–1484.
32. 32 Rattenborg, N.C., Voirin, B., Cruz, S.M., Tisdale, R., Dell'Omo, G., Lipp, H.P., Wikelski, M., Vyssotski, A.L., Evidence that birds sleep in mid-flight. Nat. Commun., 7, 2016, 12468.
33. 33 Rattenborg, N.C., Mandt, B.H., Obermeyer, W.H., Winsauer, P.J., Huber, R., Wikelski, M., Benca, R.M., Migratory sleeplessness in the white-crowned sparrow (Zonotrichia leucophrys gambelii). PLoS Biol., 2, 2004, E212.
34. 34 Lesku, J.A., Rattenborg, N.C., Valcu, M., Vyssotski, A.L., Kuhn, S., Kuemmeth, F., Heidrich, W., Kempenaers, B., Adaptive sleep loss in polygynous pectoral sandpipers. Science 337 (2012), 1654–1658.
35. 35 Ridgway, S., Carder, D., Finneran, J., Keogh, M., Kamolnick, T., Todd, M., Goldblatt, A., Dolphin continuous auditory vigilance for five days. J. Exp. Biol. 209 (2006), 3621–3628.
36. 36 Ridgway, S., Keogh, M., Carder, D., Finneran, J., Kamolnick, T., Todd, M., Goldblatt, A., Dolphins maintain cognitive performance during 72 to 120 hours of continuous auditory vigilance. J. Exp. Biol. 212 (2009), 1519–1527.
37. 37 Lyamin, O., Pryaslova, J., Lance, V., Siegel, J., Animal behaviour: continuous activity in cetaceans after birth. Nature, 435, 2005, 1177.
38. 38 Gnone, G., Moriconi, T., Gambini, G., Sleep behaviour: activity and sleep in dolphins. Nature 441 (2006), E10–E11 discussion E11.
39. 39 Sekiguchi, Y., Arai, K., Kohshima, S., Sleep behaviour: sleep in continuously active dolphins. Nature 441 (2006), E9–E10 discussion E11.
40. 40 Deurveilher, S., Rusak, B., Semba, K., Time-of-day modulation of homeostatic and allostatic sleep responses to chronic sleep restriction in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 302 (2012), R1411–R1425.
41. 41 Juster, R.P., McEwen, B.S., Sleep and chronic stress: new directions for allostatic load research. Sleep Med. 16 (2015), 7–8.
42. 42 Kim, Y., Laposky, A.D., Bergmann, B.M., Turek, F.W., Repeated sleep restriction in rats leads to homeostatic and allostatic responses during recovery sleep. Proc. Natl. Acad. Sci. USA 104 (2007), 10697–10702.
43. 43 Rechtschaffen, A., Bergmann, B.M., Gilliland, M.A., Bauer, K., Effects of method, duration, and sleep stage on rebounds from sleep deprivation in the rat. Sleep 22 (1999), 11–31.
44. 44 Parmeggiani, P.L., Thermoregulation and sleep. Front. Biosci. 8 (2003), s557–s567.
45. 45 Prudom, A.E., Klemm, W.R., Electrographic correlates of sleep behavior in a primitive mammal, the armadillo Dasypus novemcinctus. Physiol. Behav. 10 (1973), 275–282.
46. 46 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. 10 (2001), 219–228.
47. 47 Tobler, I., Behavioral sleep in the Asian elephant in captivity. Sleep 15 (1992), 1–12.
48. 48 Lesku, J.A., Roth, T.C. 2nd, Amlaner, C.J., Lima, S.L., A phylogenetic analysis of sleep architecture in mammals: the integration of anatomy, physiology, and ecology. Am. Nat. 168 (2006), 441–453.
49. 49 Lesku, J.A., Roth, T.C., Rattenborg, N.C., Amlaner, C.J., Lima, S.L., Phylogenetics and the correlates of mammalian sleep: a reappraisal. Sleep Med. Rev. 12 (2008), 229–244.
50. 50 Capellini, I., Nunn, C.L., McNamara, P., Preston, B.T., Barton, R.A., Energetic constraints, not predation, influence the evolution of sleep patterning in mammals. Funct. Ecol. 22 (2008), 847–853.
51. 51 Capellini, I., Barton, R.A., McNamara, P., Preston, B.T., Nunn, C.L., Phylogenetic analysis of the ecology and evolution of mammalian sleep. Evolution 62 (2008), 1764–1776.
52. 52 Benson-Amram, S., Dantzer, B., Stricker, G., Swanson, E.M., Holekamp, K.E., Brain size predicts problem-solving ability in mammalian carnivores. Proc. Natl. Acad. Sci. USA 113 (2016), 2532–2537.
53. 53 Kotrschal, A., Rogell, B., Bundsen, A., Svensson, B., Zajitschek, S., Brannstrom, I., Immler, S., Maklakov, A.A., Kolm, N., Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain. Curr. Biol. 23 (2013), 168–171.
54. 54 Reader, S.M., Hager, Y., Laland, K.N., The evolution of primate general and cultural intelligence. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366 (2011), 1017–1027.
55. 55 Walker, M.P., Stickgold, R., Sleep-dependent learning and memory consolidation. Neuron 44 (2004), 121–133.
56. 56 Diekelmann, S., Wilhelm, I., Born, J., The whats and whens of sleep-dependent memory consolidation. Sleep Med. Rev. 13 (2009), 309–321.
57. 57 Rasch, B., Born, J., About sleep's role in memory. Physiol. Rev. 93 (2013), 681–766.
58. 58 Siegel, J.M., The REM sleep-memory consolidation hypothesis. Science 294 (2001), 1058–1063.
59. 59 Vertes, R.P., Memory consolidation in sleep; dream or reality. Neuron 44 (2004), 135–148.
60. 60 Boyce, R., Glasgow, S.D., Williams, S., Adamantidis, A., Causal evidence for the role of REM sleep theta rhythm in contextual memory consolidation. Science 352 (2016), 812–816.
61. 61 Siegel, J.M., Rogawski, M.A., A function for REM sleep: regulation of noradrenergic receptor sensitivity. Brain Res. 472 (1988), 213–233.
62. 62 Rechtschaffen, A., Current perspectives on the function of sleep. Perspect. Biol. Med. 41 (1998), 359–390.
63. 63 Roffwarg, H.P., Muzio, J.N., Dement, W.C., Ontogenetic development of the human sleep-dream cycle. Science 152 (1966), 604–619.
64. 64 Kayser, M.S., Yue, Z., Sehgal, A., A critical period of sleep for development of courtship circuitry and behavior in Drosophila. Science 344 (2014), 269–274.
65. 65 Trojanowski, N.F., Raizen, D.M., Call it worm sleep. Trends Neurosci. 39 (2016), 54–62.
66. 66 Cirelli, C., Tononi, G., Cortical development, electroencephalogram rhythms, and the sleep/wake cycle. Biol. Psychiatry. 77 (2015), 1071–1078.
67. 67 Zepelin, H., Rechtschaffen, A., Mammalian sleep, longevity, and energy metabolism. Brain Behav. Evol. 10 (1974), 425–470.
68. 68 Buchsbaum, M.S., Gillin, J.C., Wu, J., Hazlett, E., Sicotte, N., Dupont, R.M., Bunney, W.E. Jr., Regional cerebral glucose metabolic rate in human sleep assessed by positron emission tomography. Life Sci. 45 (1989), 1349–1356.
69. 69 Kennedy, C., Gillin, J.C., Mendelson, W., Suda, S., Miyaoka, M., Ito, M., Nakamura, R.K., Storch, F.I., Pettigrew, K., Mishkin, M., et al. Local cerebral glucose utilization in non-rapid eye movement sleep. Nature 297 (1982), 325–327.
70. 70 Maquet, P., Dive, D., Salmon, E., Sadzot, B., Franco, G., Poirrier, R., von Frenckell, R., Franck, G., Cerebral glucose utilization during sleep-wake cycle in man determined by positron emission tomography and [18F]2-fluoro-2-deoxy-D-glucose method. Brain Res. 513 (1990), 136–143.
71. 71 Nofzinger, E.A., Buysse, D.J., Miewald, J.M., Meltzer, C.C., Price, J.C., Sembrat, R.C., Ombao, H., Reynolds, C.F., Monk, T.H., Hall, M., et al. Human regional cerebral glucose metabolism during non-rapid eye movement sleep in relation to waking. Brain 125 (2002), 1105–1115.
72. 72 Wisor, J.P., Rempe, M.J., Schmidt, M.A., Moore, M.E., Clegern, W.C., Sleep slow-wave activity regulates cerebral glycolytic metabolism. Cereb. Cortex. 23 (2013), 1978–1987.
73. 73 Berger, R.J., Phillips, N.H., Energy conservation and sleep. Behav. Brain Res. 69 (1995), 65–73.
74. 74 Xie, L., Kang, H., Xu, Q., Chen, M.J., Liao, Y., Thiyagarajan, M., O'Donnell, J., Christensen, D.J., Nicholson, C., Iliff, J.J., et al. Sleep drives metabolite clearance from the adult brain. Science 342 (2013), 373–377.
75. 75 Herculano-Houzel, S., Decreasing sleep requirement with increasing numbers of neurons as a driver for bigger brains and bodies in mammalian evolution. Proc. Biol. Sci., 282, 2015, 20151853.
76. 76 Voirin, B., Scriba, M.F., Martinez-Gonzalez, D., Vyssotski, A.L., Wikelski, M., Rattenborg, N.C., Ecology and neurophysiology of sleep in two wild sloth species. Sleep 37 (2014), 753–761.
77. 77 McDonough, C.M., Loughry, W.J., Influences on activity patterns in a population of nine-banded armadillos. J. Mammal. 78 (1997), 932–941.
78. 78 Siegel, J.M., Sleep viewed as a state of adaptive inactivity. Nat. Rev. Neurosci. 10 (2009), 747–753.
79. 79 Schmidt, M.H., The energy allocation function of sleep: a unifying theory of sleep, torpor, and continuous wakefulness. Neurosci. Biobehav. Rev. 47 (2014), 122–153.
80. 80 Blumberg, M.S., Gall, A.J., Todd, W.D., The development of sleep-wake rhythms and the search for elemental circuits in the infant brain. Behav. Neurosci. 128 (2014), 250–263.
81. 81 Brooks, P.L., Peever, J., A temporally controlled inhibitory drive coordinates twitch movements during REM sleep. Curr. Biol. 26 (2016), 1177–1182.
82. 82 Scharf, M.T., Naidoo, N., Zimmerman, J.E., Pack, A.I., The energy hypothesis of sleep revisited. Prog. Neurobiol. 86 (2008), 264–280.
83. 83 Haddad, G.G., Does the brain gain back energy during sleep? But what does it mean?. Sleep 34 (2011), 835–836.
84. 84 Jones, S.G., Paletz, E.M., Obermeyer, W.H., Hannan, C.T., Benca, R.M., Seasonal influences on sleep and executive function in the migratory White-crowned Sparrow (Zonotrichia leucophrys gambelii). BMC Neurosci., 11, 2010, 87.
85. 85 Abel, T., Havekes, R., Saletin, J.M., Walker, M.P., Sleep, plasticity and memory from molecules to whole-brain networks. Curr. Biol. 23 (2013), R774–R788.
86. 86 Buzsaki, G., Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning. Hippocampus 25 (2015), 1073–1188.
87. 87 Wilson, M.A., McNaughton, B.L., Reactivation of hippocampal ensemble memories during sleep. Science 265 (1994), 676–679.
88. 88 Davidson, T.J., Kloosterman, F., Wilson, M.A., Hippocampal replay of extended experience. Neuron 63 (2009), 497–507.
89. 89 Schwindel, C.D., McNaughton, B.L., Hippocampal-cortical interactions and the dynamics of memory trace reactivation. Prog. Brain Res. 193 (2011), 163–177.
90. 90 Sadowski, J.H., Jones, M.W., Mellor, J.R., Sharp-wave ripples orchestrate the induction of synaptic plasticity during reactivation of place cell firing patterns in the hippocampus. Cell Rep. 14 (2016), 1916–1929.
91. 91 Maingret, N., Girardeau, G., Todorova, R., Goutierre, M., Zugaro, M., Hippocampo-cortical coupling mediates memory consolidation during sleep. Nat. Neurosci. 19 (2016), 959–964.
92. 92 Aeschbach, D., Cutler, A.J., Ronda, J.M., A role for non-rapid-eye-movement sleep homeostasis in perceptual learning. J. Neurosci. 28 (2008), 2766–2772.
93. 93 Landsness, E.C., Crupi, D., Hulse, B.K., Peterson, M.J., Huber, R., Ansari, H., Coen, M., Cirelli, C., Benca, R.M., Ghilardi, M.F., et al. Sleep-dependent improvement in visuomotor learning: a causal role for slow waves. Sleep 32 (2009), 1273–1284.
94. 94 Marshall, L., Helgadottir, H., Molle, M., Born, J., Boosting slow oscillations during sleep potentiates memory. Nature 444 (2006), 610–613.
95. 95 Girardeau, G., Benchenane, K., Wiener, S.I., Buzsaki, G., Zugaro, M.B., Selective suppression of hippocampal ripples impairs spatial memory. Nat. Neurosci. 12 (2009), 1222–1223.
96. 96 Li, Y., Zhou, Z., Zhang, X., Tong, H., Li, P., Zhang, Z.C., Jia, Z., Xie, W., Han, J., Drosophila neuroligin 4 regulates sleep through modulating GABA transmission. J. Neurosci. 33 (2013), 15545–15554.
97. 97 Dissel, S., Melnattur, K., Shaw, P.J., Sleep, performance, and memory in flies. Curr. Sleep Med. Rep. 1 (2015), 47–54.
98. 98 Donlea, J.M., Thimgan, M.S., Suzuki, Y., Gottschalk, L., Shaw, P.J., Inducing sleep by remote control facilitates memory consolidation in Drosophila. Science 332 (2011), 1571–1576.
99. 99 Tononi, G., Cirelli, C., Sleep and synaptic homeostasis: a hypothesis. Brain Res. Bull. 62 (2003), 143–150.
100. 100 Tononi, G., Cirelli, C., Sleep function and synaptic homeostasis. Sleep Med. Rev. 10 (2006), 49–62.
101. 101 Tononi, G., Cirelli, C., Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron 81 (2014), 12–34.
102. 102 Vyazovskiy, V.V., Cirelli, C., Pfister-Genskow, M., Faraguna, U., Tononi, G., Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nat. Neurosci. 11 (2008), 200–208.
103. 103 Huber, R., Ghilardi, M.F., Massimini, M., Tononi, G., Local sleep and learning. Nature 430 (2004), 78–81.
104. 104 Donlea, J.M., Ramanan, N., Shaw, P.J., Use-dependent plasticity in clock neurons regulates sleep need in Drosophila. Science 324 (2009), 105–108.
105. 105 Gilestro, G.F., Tononi, G., Cirelli, C., Widespread changes in synaptic markers as a function of sleep and wakefulness in Drosophila. Science 324 (2009), 109–112.
106. 106 Bushey, D., Tononi, G., Cirelli, C., Sleep and synaptic homeostasis: structural evidence in Drosophila. Science 332 (2011), 1576–1581.
107. 107 Robinson, J.E., Paluch, J., Dickman, D.K., Joiner, W.J., ADAR-mediated RNA editing suppresses sleep by acting as a brake on glutamatergic synaptic plasticity. Nat. Commun., 7, 2016, 10512.
108. 108 Aton, S.J., Seibt, J., Dumoulin, M., Jha, S.K., Steinmetz, N., Coleman, T., Naidoo, N., Frank, M.G., Mechanisms of sleep-dependent consolidation of cortical plasticity. Neuron 61 (2009), 454–466.
109. 109 Frank, M.G., Erasing synapses in sleep: is it time to be SHY?. Neural Plast., 2012, 2012, 264378.
110. 110 Cirelli, C., Cellular consequences of sleep deprivation in the brain. Sleep Med. Rev. 10 (2006), 307–321.
111. 111 Mackiewicz, M., Zimmerman, J.E., Shockley, K.R., Churchill, G.A., Pack, A.I., What are microarrays teaching us about sleep?. Trends Mol. Med. 15 (2009), 79–87.
112. 112 Mongrain, V., Hernandez, S.A., Pradervand, S., Dorsaz, S., Curie, T., Hagiwara, G., Gip, P., Heller, H.C., Franken, P., Separating the contribution of glucocorticoids and wakefulness to the molecular and electrophysiological correlates of sleep homeostasis. Sleep 33 (2010), 1147–1157.
113. 113 Hobson, J.A., Sleep is of the brain, by the brain and for the brain. Nature 437 (2005), 1254–1256.
114. 114 Born, J., Wilhelm, I., System consolidation of memory during sleep. Psychol. Res. 76 (2012), 192–203.
115. 115 Diekelmann, S., Born, J., The memory function of sleep. Nat. Rev. Neurosci. 11 (2010), 114–126.
116. 116 Berry, J.A., Cervantes-Sandoval, I., Chakraborty, M., Davis, R.L., Sleep facilitates memory by blocking dopamine neuron-mediated forgetting. Cell 161 (2015), 1656–1667.
117. 117 Haynes, P.R., Christmann, B.L., Griffith, L.C., A single pair of neurons links sleep to memory consolidation in Drosophila melanogaster. Elife, 4, 2015, 10.7554/eLife.03868.
118. 118 Dissel, S., Angadi, V., Kirszenblat, L., Suzuki, Y., Donlea, J., Klose, M., Koch, Z., English, D., Winsky-Sommerer, R., van Swinderen, B., et al. Sleep restores behavioral plasticity to Drosophila mutants. Curr. Biol. 25 (2015), 1270–1281.
119. 119 Anafi, R.C., Pellegrino, R., Shockley, K.R., Romer, M., Tufik, S., Pack, A.I., Sleep is not just for the brain: transcriptional responses to sleep in peripheral tissues. BMC Genomics., 14, 2013, 362.
120. 120 Maret, S., Dorsaz, S., Gurcel, L., Pradervand, S., Petit, B., Pfister, C., Hagenbuchle, O., O'Hara, B.F., Franken, P., Tafti, M., Homer1a is a core brain molecular correlate of sleep loss. Proc. Natl. Acad. Sci. USA 104 (2007), 20090–20095.
121. 121 Everson, C.A., Laatsch, C.D., Hogg, N., Antioxidant defense responses to sleep loss and sleep recovery. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288 (2005), R374–R383.
122. 122 Everson, C.A., Thalacker, C.D., Hogg, N., Phagocyte migration and cellular stress induced in liver, lung, and intestine during sleep loss and sleep recovery. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295 (2008), R2067–R2074.
123. 123 Driver, R.J., Lamb, A.L., Wyner, A.J., Raizen, D.M., DAF-16/FOXO regulates homeostasis of essential sleep-like behavior during larval transitions in C. elegans. Curr. Biol. 23 (2013), 501–506.
124. 124 Maret, S., Faraguna, U., Nelson, A.B., Cirelli, C., Tononi, G., Sleep and waking modulate spine turnover in the adolescent mouse cortex. Nat. Neurosci. 14 (2011), 1418–1420.
125. 125 Yang, G., Lai, C.S., Cichon, J., Ma, L., Li, W., Gan, W.B., Sleep promotes branch-specific formation of dendritic spines after learning. Science 344 (2014), 1173–1178.
126. 126 Sehgal, A., Mignot, E., Genetics of sleep and sleep disorders. Cell 146 (2011), 194–207.
127. 127 Agosto, J., Choi, J.C., Parisky, K.M., Stilwell, G., Rosbash, M., Griffith, L.C., Modulation of GABAA receptor desensitization uncouples sleep onset and maintenance in Drosophila. Nat. Neurosci. 11 (2008), 354–359.
128. 128 Parisky, K.M., Agosto, J., Pulver, S.R., Shang, Y., Kuklin, E., Hodge, J.J., Kang, K., Liu, X., Garrity, P.A., Rosbash, M., et al. PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit. Neuron 60 (2008), 672–682.
129. 129 Cirelli, C., Bushey, D., Hill, S., Huber, R., Kreber, R., Ganetzky, B., Tononi, G., Reduced sleep in Drosophila Shaker mutants. Nature 434 (2005), 1087–1092.
130. 130 Yelin-Bekerman, L., Elbaz, I., Diber, A., Dahary, D., Gibbs-Bar, L., Alon, S., Lerer-Goldshtein, T., Appelbaum, L., Hypocretin neuron-specific transcriptome profiling identifies the sleep modulator Kcnh4a. Elife, 4, 2015, e08638.
131. 131 Douglas, C.L., Vyazovskiy, V., Southard, T., Chiu, S.Y., Messing, A., Tononi, G., Cirelli, C., Sleep in Kcna2 knockout mice. BMC Biol., 5, 2007, 42.
132. 132 Winsky-Sommerer, R., Role of GABAA receptors in the physiology and pharmacology of sleep. Eur. J. Neurosci. 29 (2009), 1779–1794.
133. 133 Espinosa, F., Marks, G., Heintz, N., Joho, R.H., Increased motor drive and sleep loss in mice lacking Kv3-type potassium channels. Genes Brain Behav. 3 (2004), 90–100.
134. 134 El Helou, J., Belanger-Nelson, E., Freyburger, M., Dorsaz, S., Curie, T., La Spada, F., Gaudreault, P.O., Beaumont, E., Pouliot, P., Lesage, F., et al. Neuroligin-1 links neuronal activity to sleep-wake regulation. Proc. Natl. Acad. Sci. USA 110 (2013), 9974–9979.
135. 135 Wu, M.N., Joiner, W.J., Dean, T., Yue, Z., Smith, C.J., Chen, D., Hoshi, T., Sehgal, A., Koh, K., SLEEPLESS, a Ly-6/neurotoxin family member, regulates the levels, localization and activity of Shaker. Nat. Neurosci. 13 (2010), 69–75.
136. 136 Chiu, C.N., Rihel, J., Lee, D.A., Singh, C., Mosser, E.A., Chen, S., Sapin, V., Pham, U., Engle, J., Niles, B.J., et al. A zebrafish genetic screen identifies Neuromedin U as a regulator of sleep/wake states. Neuron 89 (2016), 842–856.
137. 137 Hanada, R., Nakazato, M., Murakami, N., Sakihara, S., Yoshimatsu, H., Toshinai, K., Hanada, T., Suda, T., Kangawa, K., Matsukura, S., et al. A role for neuromedin U in stress response. Biochem. Biophys. Res. Commun. 289 (2001), 225–228.
138. 138 Li, J., Hu, Z., de Lecea, L., The hypocretins/orexins: integrators of multiple physiological functions. Br. J. Pharmacol. 171 (2014), 332–350.
139. 139 Semjonous, N.M., Smith, K.L., Parkinson, J.R., Gunner, D.J., Liu, Y.L., Murphy, K.G., Ghatei, M.A., Bloom, S.R., Small, C.J., Coordinated changes in energy intake and expenditure following hypothalamic administration of neuropeptides involved in energy balance. Int. J. Obes. (Lond) 33 (2009), 775–785.
140. 140 Ramanathan, L., Gulyani, S., Nienhuis, R., Siegel, J.M., Sleep deprivation decreases superoxide dismutase activity in rat hippocampus and brainstem. Neuroreport 13 (2002), 1387–1390.
141. 141 Naidoo, N., Giang, W., Galante, R.J., Pack, A.I., Sleep deprivation induces the unfolded protein response in mouse cerebral cortex. J. Neurochem. 92 (2005), 1150–1157.
142. 142 Naidoo, N., Casiano, V., Cater, J., Zimmerman, J., Pack, A.I., A role for the molecular chaperone protein BiP/GRP78 in Drosophila sleep homeostasis. Sleep 30 (2007), 557–565.
143. 143 Shaw, P.J., Tononi, G., Greenspan, R.J., Robinson, D.F., Stress response genes protect against lethal effects of sleep deprivation in Drosophila. Nature 417 (2002), 287–291.
144. 144 Krueger, J.M., The role of cytokines in sleep regulation. Curr. Pharm. Des. 14 (2008), 3408–3416.
145. 145 Imeri, L., Opp, M.R., How (and why) the immune system makes us sleep. Nat. Rev. Neurosci. 10 (2009), 199–210.
146. 146 Kuo, T.H., Pike, D.H., Beizaeipour, Z., Williams, J.A., Sleep triggered by an immune response in Drosophila is regulated by the circadian clock and requires the NFkappaB Relish. BMC Neurosci., 11, 2010, 17.
147. 147 Hendricks, J.C., Lu, S., Kume, K., Yin, J.C., Yang, Z., Sehgal, A., Gender dimorphism in the role of cycle (BMAL1) in rest, rest regulation, and longevity in Drosophila melanogaster. J. Biol. Rhythms 18 (2003), 12–25.
148. 148 Laposky, A., Easton, A., Dugovic, C., Walisser, J., Bradfield, C., Turek, F., Deletion of the mammalian circadian clock gene BMAL1/Mop3 alters baseline sleep architecture and the response to sleep deprivation. Sleep 28 (2005), 395–409.
149. 149 Naylor, E., Bergmann, B.M., Krauski, K., Zee, P.C., Takahashi, J.S., Vitaterna, M.H., Turek, F.W., The circadian clock mutation alters sleep homeostasis in the mouse. J. Neurosci. 20 (2000), 8138–8143.
150. 150 He, Y., Jones, C.R., Fujiki, N., Xu, Y., Guo, B., Holder, J.L. Jr., Rossner, M.J., Nishino, S., Fu, Y.H., The transcriptional repressor DEC2 regulates sleep length in mammals. Science 325 (2009), 866–870.
151. 151 Renier, C., Faraco, J.H., Bourgin, P., Motley, T., Bonaventure, P., Rosa, F., Mignot, E., Genomic and functional conservation of sedative-hypnotic targets in the zebrafish. Pharmacogenet. Genomics 17 (2007), 237–253.
152. 152 Maximino, C., Lima, M.G., Olivera, K.R., Picanco-Diniz, D.L., Herculano, A.M., Adenosine A1, but not A2, receptor blockade increases anxiety and arousal in Zebrafish. Basic Clin. Pharmacol. Toxicol. 109 (2011), 203–207.
153. 153 Nishimura, Y., Okabe, S., Sasagawa, S., Murakami, S., Ashikawa, Y., Yuge, M., Kawaguchi, K., Kawase, R., Tanaka, T., Pharmacological profiling of zebrafish behavior using chemical and genetic classification of sleep-wake modifiers. Front Pharmacol., 6, 2015, 257.
154. 154 Allada, R., Nash, H.A., Drosophila melanogaster as a model for study of general anesthesia: the quantitative response to clinical anesthetics and alkanes. Anesth. Analg. 77 (1993), 19–26.
155. 155 Joiner, W.J., Friedman, E.B., Hung, H.T., Koh, K., Sowcik, M., Sehgal, A., Kelz, M.B., Genetic and anatomical basis of the barrier separating wakefulness and anesthetic-induced unresponsiveness. PLoS Genet., 9, 2013, e1003605.
156. 156 Pace-Schott, E.F., Hobson, J.A., The neurobiology of sleep: genetics, cellular physiology and subcortical networks. Nat. Rev. Neurosci. 3 (2002), 591–605.
157. 157 Brown, R.E., Basheer, R., McKenna, J.T., Strecker, R.E., McCarley, R.W., Control of sleep and wakefulness. Physiol. Rev. 92 (2012), 1087–1187.
158. 158 Alam, M.A., Kumar, S., McGinty, D., Alam, M.N., Szymusiak, R., Neuronal activity in the preoptic hypothalamus during sleep deprivation and recovery sleep. J. Neurophysiol. 111 (2014), 287–299.
159. 159 Jones, B.E., Hassani, O.K., The role of Hcrt/Orx and MCH neurons in sleep-wake state regulation. Sleep 36 (2013), 1769–1772.
160. 160 Luppi, P.H., Peyron, C., Fort, P., Not a single but multiple populations of GABAergic neurons control sleep. Sleep Med. Rev., 2016, 10.1016/j.smrv.2016.03.002.
161. 161 Xu, M., Chung, S., Zhang, S., Zhong, P., Ma, C., Chang, W.C., Weissbourd, B., Sakai, N., Luo, L., Nishino, S., et al. Basal forebrain circuit for sleep-wake control. Nat. Neurosci. 18 (2015), 1641–1647.
162. 162 Lu, J., Greco, M.A., Shiromani, P., Saper, C.B., Effect of lesions of the ventrolateral preoptic nucleus on NREM and REM sleep. J. Neurosci. 20 (2000), 3830–3842.
163. 163 Chiu, C.N., Prober, D.A., Regulation of zebrafish sleep and arousal states: current and prospective approaches. Front. Neural Circuits, 7, 2013, 58.
164. 164 Singh, A., Subhashini, N., Sharma, S., Mallick, B.N., Involvement of the alpha1-adrenoceptor in sleep-waking and sleep loss-induced anxiety behavior in zebrafish. Neuroscience 245 (2013), 136–147.
165. 165 Singh, C., Oikonomou, G., Prober, D.A., Norepinephrine is required to promote wakefulness and for hypocretin-induced arousal in zebrafish. Elife, 4, 2015, e07000.
166. 166 Parker, M.O., Brock, A.J., Walton, R.T., Brennan, C.H., The role of zebrafish (Danio rerio) in dissecting the genetics and neural circuits of executive function. Front. Neural Circuits, 7, 2013, 63.
167. 167 Sundvik, M., Kudo, H., Toivonen, P., Rozov, S., Chen, Y.C., Panula, P., The histaminergic system regulates wakefulness and orexin/hypocretin neuron development via histamine receptor H1 in zebrafish. FASEB J. 25 (2011), 4338–4347.
168. 168 Liu, Q., Liu, S., Kodama, L., Driscoll, M.R., Wu, M.N., Two dopaminergic neurons signal to the dorsal fan-shaped body to promote wakefulness in Drosophila. Curr. Biol. 22 (2012), 2114–2123.
169. 169 Yuan, Q., Joiner, W.J., Sehgal, A., A sleep-promoting role for the Drosophila serotonin receptor 1A. Curr. Biol. 16 (2006), 1051–1062.
170. 170 Pooryasin, A., Fiala, A., Identified serotonin-releasing neurons induce behavioral quiescence and suppress mating in Drosophila. J. Neurosci. 35 (2015), 12792–12812.
171. 171 Sheeba, V., Fogle, K.J., Kaneko, M., Rashid, S., Chou, Y.T., Sharma, V.K., Holmes, T.C., Large ventral lateral neurons modulate arousal and sleep in Drosophila. Curr. Biol. 18 (2008), 1537–1545.
172. 172 Joiner, W.J., Crocker, A., White, B.H., Sehgal, A., Sleep in Drosophila is regulated by adult mushroom bodies. Nature 441 (2006), 757–760.
173. 173 Pitman, J.L., McGill, J.J., Keegan, K.P., Allada, R., A dynamic role for the mushroom bodies in promoting sleep in Drosophila. Nature 441 (2006), 753–756.
174. 174 Sitaraman, D., Aso, Y., Jin, X., Chen, N., Felix, M., Rubin, G.M., Nitabach, M.N., Propagation of homeostatic sleep signals by segregated synaptic microcircuits of the Drosophila mushroom body. Curr. Biol. 25 (2015), 2915–2927.
175. 175 Schwarz, J., Lewandrowski, I., Bringmann, H., Reduced activity of a sensory neuron during a sleep-like state in Caenorhabditis elegans. Curr. Biol. 21 (2011), R983–R984.
176. 176 Saper, C.B., Scammell, T.E., Lu, J., Hypothalamic regulation of sleep and circadian rhythms. Nature 437 (2005), 1257–1263.
177. 177 Dauvilliers, Y., Arnulf, I., Mignot, E., Narcolepsy with cataplexy. Lancet 369 (2007), 499–511.
178. 178 Friedman, E.B., Sun, Y., Moore, J.T., Hung, H.T., Meng, Q.C., Perera, P., Joiner, W.J., Thomas, S.A., Eckenhoff, R.G., Sehgal, A., et al. A conserved behavioral state barrier impedes transitions between anesthetic-induced unconsciousness and wakefulness: evidence for neural inertia. PLoS One, 5, 2010, e11903.
179. 179 Davis, C.J., Clinton, J.M., Jewett, K.A., Zielinski, M.R., Krueger, J.M., Delta wave power: an independent sleep phenotype or epiphenomenon?. J. Clin. Sleep Med. 7 (2011), S16–S18.
180. 180 Qiu, M.H., Chen, M.C., Lu, J., Cortical neuronal activity does not regulate sleep homeostasis. Neuroscience 297 (2015), 211–218.
181. 181 Benington, J.H., Heller, H.C., Restoration of brain energy metabolism as the function of sleep. Prog. Neurobiol. 45 (1995), 347–360.
182. 182 Porkka-Heiskanen, T., Strecker, R.E., Thakkar, M., Bjorkum, A.A., Greene, R.W., McCarley, R.W., Adenosine: a mediator of the sleep-inducing effects of prolonged wakefulness. Science 276 (1997), 1265–1268.
183. 183 Bjorness, T.E., Greene, R.W., Adenosine and sleep. Curr. Neuropharmacol. 7 (2009), 238–245.
184. 184 Bjorness, T.E., Kelly, C.L., Gao, T., Poffenberger, V., Greene, R.W., Control and function of the homeostatic sleep response by adenosine A1 receptors. J. Neurosci. 29 (2009), 1267–1276.
185. 185 Huang, Z.L., Qu, W.M., Eguchi, N., Chen, J.F., Schwarzschild, M.A., Fredholm, B.B., Urade, Y., Hayaishi, O., Adenosine A2A, but not A1, receptors mediate the arousal effect of caffeine. Nat. Neurosci. 8 (2005), 858–859.
186. 186 Wu, M.N., Ho, K., Crocker, A., Yue, Z., Koh, K., Sehgal, A., The effects of caffeine on sleep in Drosophila require PKA activity, but not the adenosine receptor. J. Neurosci. 29 (2009), 11029–11037.
187. 187 Franken, P., Chollet, D., Tafti, M., The homeostatic regulation of sleep need is under genetic control. J. Neurosci. 21 (2001), 2610–2621.
188. 188 Liu, S., Liu, Q., Tabuchi, M., Wu, M.N., Sleep drive is encoded by neural plastic changes in a dedicated circuit. Cell 165 (2016), 1347–1360.
189. 189 Morairty, S.R., Dittrich, L., Pasumarthi, R.K., Valladao, D., Heiss, J.E., Gerashchenko, D., Kilduff, T.S., A role for cortical nNOS/NK1 neurons in coupling homeostatic sleep drive to EEG slow wave activity. Proc. Natl. Acad. Sci. USA 110 (2013), 20272–20277.
190. 190 Vyazovskiy, V.V., Olcese, U., Hanlon, E.C., Nir, Y., Cirelli, C., Tononi, G., Local sleep in awake rats. Nature 472 (2011), 443–447.
191. 191 Hinard, V., Mikhail, C., Pradervand, S., Curie, T., Houtkooper, R.H., Auwerx, J., Franken, P., Tafti, M., Key electrophysiological, molecular, and metabolic signatures of sleep and wakefulness revealed in primary cortical cultures. J. Neurosci. 32 (2012), 12506–12517.
192. 192 Rial, R.V., Akaarir, M., Gamundi, A., Nicolau, C., Garau, C., Aparicio, S., Tejada, S., Gene, L., Gonzalez, J., De Vera, L.M., et al. Evolution of wakefulness, sleep and hibernation: from reptiles to mammals. Neurosci. Biobehav. Rev. 34 (2010), 1144–1160.
193. 193 Shein-Idelson, M., Ondracek, J.M., Liaw, H.P., Reiter, S., Laurent, G., Slow waves, sharp waves, ripples, and REM in sleeping dragons. Science 352 (2016), 590–595.
194. 194 Villablanca, J.R., Counterpointing the functional role of the forebrain and of the brainstem in the control of the sleep-waking system. J. Sleep Res. 13 (2004), 179–208.
195. 195 Hayashi, Y., Kashiwagi, M., Yasuda, K., Ando, R., Kanuka, M., Sakai, K., Itohara, S., Cells of a common developmental origin regulate REM/non-REM sleep and wakefulness in mice. Science 350 (2015), 957–961.
196. 196 Dugas-Ford, J., Rowell, J.J., Ragsdale, C.W., Cell-type homologies and the origins of the neocortex. Proc. Natl. Acad. Sci. USA 109 (2012), 16974–16979.
197. 197 Karten, H.J., Neocortical evolution: neuronal circuits arise independently of lamination. Curr. Biol. 23 (2013), R12–R15.
198. 198 Karten, H.J., Vertebrate brains and evolutionary connectomics: on the origins of the mammalian ‘neocortex’. Philos. Trans. R. Soc. Lond. B Biol. Sci., 370, 2015.
199. 199 David, F., Schmiedt, J.T., Taylor, H.L., Orban, G., Di Giovanni, G., Uebele, V.N., Renger, J.J., Lambert, R.C., Leresche, N., Crunelli, V., Essential thalamic contribution to slow waves of natural sleep. J. Neurosci. 33 (2013), 19599–19610.
200. 200 Lemieux, M., Chen, J.Y., Lonjers, P., Bazhenov, M., Timofeev, I., The impact of cortical deafferentation on the neocortical slow oscillation. J. Neurosci. 34 (2014), 5689–5703.
201. 201 Mueller, T., What is the Thalamus in Zebrafish?. Front. Neurosci., 6, 2012, 64.
202. 202 Arnason, B.B., Thornorsteinsson, H., Karlsson, K.A.E., Absence of rapid eye movements during sleep in adult zebrafish. Behav. Brain Res. 291 (2015), 189–194.
203. 203 Stopfer, M., Central processing in the mushroom bodies. Curr. Opin. Insect Sci. 6 (2014), 99–103.
204. 204 Tomer, R., Denes, A.S., Tessmar-Raible, K., Arendt, D., Profiling by image registration reveals common origin of annelid mushroom bodies and vertebrate pallium. Cell 142 (2010), 800–809.
205. 205 Stopfer, M., Bhagavan, S., Smith, B.H., Laurent, G., Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390 (1997), 70–74.
206. 206 Zwaka, H., Bartels, R., Gora, J., Franck, V., Culo, A., Gotsch, M., Menzel, R., Context odor presentation during sleep enhances memory in honeybees. Curr. Biol. 25 (2015), 2869–2874.
207. 207 Seymour, J.E., Carrette, T.J., Sutherland, P.A., Do box jellyfish sleep at night?. Med. J. Aust., 181, 2004, 707.
208. 208 Watanabe, H., Fujisawa, T., Holstein, T.W., Cnidarians and the evolutionary origin of the nervous system. Dev. Growth Differ. 51 (2009), 167–183.
209. 209 Hiragaki, S., Suzuki, T., Mohamed, A.A., Takeda, M., Structures and functions of insect arylalkylamine N-acetyltransferase (iaaNAT); a key enzyme for physiological and behavioral switch in arthropods. Front. Physiol., 6, 2015, 113.
210. 210 Ureta-Vidal, A., Ettwiller, L., Birney, E., Comparative genomics: genome-wide analysis in metazoan eukaryotes. Nat. Rev. Genet. 4 (2003), 251–262.