1932

Abstract

Sleep is essential for proper brain function in mammals and insects. During sleep, animals are disconnected from the external world; they show high arousal thresholds and changed brain activity. Sleep deprivation results in a sleep rebound. Research using the fruit fly, , has helped us understand the genetic and neuronal control of sleep. Genes involved in sleep control code for ion channels, factors influencing neurotransmission and neuromodulation, and proteins involved in the circadian clock. The neurotransmitters/neuromodulators involved in sleep control are GABA, dopamine, acetylcholine, serotonin, and several neuropeptides. Sleep is controlled by the interplay between sleep homeostasis and the circadian clock. Putative sleep-wake centers are located in higher-order brain centers that are indirectly connected to the circadian clock network. The primary function of sleep appears to be the downscaling of synapses that have been built up during wakefulness. Thus, brain homeostasis is maintained and learning and memory are assured.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-020117-043201
2018-01-07
2024-04-13
Loading full text...

Full text loading...

/deliver/fulltext/ento/63/1/annurev-ento-020117-043201.html?itemId=/content/journals/10.1146/annurev-ento-020117-043201&mimeType=html&fmt=ahah

Literature Cited

  1. Afonso DJS, Liu D, Machado DR, Pan H, Jepson JEC. 1.  et al. 2015. TARANIS functions with cyclin A and Cdk1 in a novel arousal center to control sleep in Drosophila. Curr. Biol. 25:1717–26 [Google Scholar]
  2. Agosto J, Choi JC, Parisky KM, Stilwell G, Rosbash M, Griffith LC. 2.  2008. Modulation of GABAA receptor desensitization uncouples sleep onset and maintenance in Drosophila. Nat. Neurosci. 11:354–59 [Google Scholar]
  3. Allebrandt KV, Amin N, Müller-Myhsok B, Esko T, Teder-Laving M. 3.  et al. 2011. A KATP channel gene effect on sleep duration: from genome-wide association studies to function in Drosophila. Mol. Psychiatry 18:122–32 [Google Scholar]
  4. Andersen FS. 4.  1968. Sleep in moths and its dependence on the frequency of stimulation in Anagasta kuehniella. Opusc. Entomol. 33:15–24 [Google Scholar]
  5. Aso Y, Hattori D, Yu Y, Johnston RM, Iyer NA. 5.  et al. 2014. The neuronal architecture of the mushroom body provides a logic for associative learning. eLife 3:e04577 [Google Scholar]
  6. Aso Y, Sitaraman D, Ichinose T, Kaun KR, Vogt K. 6.  et al. 2014. Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila. eLife 3:e04580 [Google Scholar]
  7. Bachleitner W, Kempinger L, Wülbeck C, Rieger D, Helfrich-Förster C. 7.  2007. Moonlight shifts the endogenous clock of Drosophila melanogaster. PNAS 104:93538–43 [Google Scholar]
  8. Barnstedt O, Owald D, Felsenberg J, Brain R, Moszynski JP. 8.  et al. 2016. Memory-relevant mushroom body output synapses are cholinergic. Neuron 89:61237–47 [Google Scholar]
  9. Bellesi M, Bushey D, Chini M, Tononi G, Cirelli C. 9.  2016. Contribution of sleep to the repair of neuronal DNA double-strand breaks: evidence form flies and mice. Sci. Rep. 6:36804 [Google Scholar]
  10. Berry JA, Cervantes-Sandoval I, Chakraborty M, Davis RL. 10.  2015. Sleep facilitates memory by blocking dopamine neuron mediated forgetting. Cell 161:1656–67 [Google Scholar]
  11. Beyaert L, Greggers U, Menzel R. 11.  2012. Honeybees consolidate navigation memory during sleep. J. Exp. Biol. 215:3981–88 [Google Scholar]
  12. Borbély AA. 12.  1982. A two process model of sleep regulation. Hum. Neurobiol. 1:195–204 [Google Scholar]
  13. Bösebeck H, Kaiser W. 13.  1987. Das Verhalten von Honigbienen nach Schlafentzug. In New Frontiers in Brain Research. N Elsner, O Creutzfeldt 206 Stuttgart, Ger: Thieme
  14. Burke CJ, Huetteroth W, Owald D, Perisse E, Krashes MJ. 14.  et al. 2012. Layered reward signaling through octopamine and dopamine in Drosophila. Nature 492:7429433–37 [Google Scholar]
  15. Bushey D, Huber R, Tononi G, Cirelli C. 15.  2007. Drosophila hyperkinetic mutants have reduced sleep and impaired memory. J. Neurosci. 27:5384–93 [Google Scholar]
  16. Bushey D, Hughes KA, Tononi G, Cirelli C. 16.  2010. Sleep, aging, and lifespan in Drosophila. BMC Neurosci 11:56 [Google Scholar]
  17. Bushey D, Tononi G, Cirelli C. 17.  2011. Sleep and synaptic homeostasis: structural evidence in Drosophila. Science 332:1576–81 [Google Scholar]
  18. Bushey D, Tononi G, Cirelli C. 18.  2015. Sleep- and wake-dependent changes in neuronal activity and reactivity demonstrated in fly neurons using in vivo calcium imaging. PNAS 112:154785–90 [Google Scholar]
  19. Campbell SS, Tobler I. 19.  1984. Animal sleep: a review of sleep duration across phylogeny. Neurosci. Biobehav. Rev. 8:268–300 [Google Scholar]
  20. Cavanaugh DJ, Geratowski JD, Wooltorton JRA, Spaethling JM, Hector CE. 20.  et al. 2014. Identification of a circadian output circuit for rest: activity rhythms in Drosophila. Cell 157:689–701 [Google Scholar]
  21. Cavanaugh DJ, Vigderman AS, Dean T, Garbe DS, Sehgal A. 21.  2016. The Drosophila circadian clock gates sleep through time-of-day dependent modulation of sleep-promoting neurons. Sleep 39:345–56 [Google Scholar]
  22. Cavey M, Collins B, Bertet C, Blau J. 22.  2016. Circadian rhythms in neuronal activity propagate through output circuits. Nat. Neurosci. 19:587–95 [Google Scholar]
  23. Chen J, Reiher W, Hermann-Luibl C, Sellami A, Cognigni P. 23.  et al. 2016. Allatostatin A signaling in Drosophila regulates feeding and sleep and is modulated by PDF. PLOS Genet 12:9e1006346 [Google Scholar]
  24. Chen W, Shi W, Li L, Zheng Z, Li T. 24.  et al. 2013. Regulation of sleep by the short neuropeptide F (sNPF) in Drosophila melanogaster. Insect Biochem. Mol. Biol. 43:809–19 [Google Scholar]
  25. Chung BY, Kilman VL, Keath JR, Pitman JL, Allada R. 25.  2009. The GABAA receptor RDL acts in peptidergic PDF neurons to promote sleep in Drosophila. Curr. Biol. 19:5386–90 [Google Scholar]
  26. Chung BY, Ro J, Hutter SA, Miller KM, Guduguntla LS, Kondo S, Pletcher SD. 26.  2017. Drosophila Neuropeptide F signaling independently regulates feeding and sleep-wake behavior. Cell Rep 19:2441–50 [Google Scholar]
  27. Cirelli C. 27.  2009. The genetic and molecular regulation of sleep: from fruit flies to humans. Nat. Rev. 10:549–60 [Google Scholar]
  28. Cirelli C, Bushey D, Hill S, Huber R, Kreber R. 28.  et al. 2005. Reduced sleep in Drosophila Shaker mutants. Nature 434:1087–92 [Google Scholar]
  29. Claridge-Chang A, Roorda RD, Vrontou E, Sjulson L, Li H. 29.  et al. 2009. Writing memories with light-addressable reinforcement circuitry. Cell 139:2405–15 [Google Scholar]
  30. Cortelli P, Gambetti P, Montagna P, Lugaresi E. 30.  1999. Fatal familial insomnia: clinical features and molecular genetics. J. Sleep Res. 8:Suppl. 123–29 [Google Scholar]
  31. Crocker A, Sehgal A. 31.  2008. Octopamine regulates sleep in Drosophila through protein kinase A-dependent mechanisms. J. Neurosci. 28:389377–85 [Google Scholar]
  32. Crocker A, Shahidullah M, Levitan IB, Sehgal A. 32.  2010. Identification of a neural circuit that underlies the effects of octopamine on sleep: wake behavior. Neuron 65:670–81 [Google Scholar]
  33. Cros S, Cerda X, Retana J. 33.  1997. Spatial and temporal variations in the activity patterns of Mediterranean ant communities. Ecoscience 4:269–78 [Google Scholar]
  34. Dingl H. 34.  2014. Migration: The Biology of Life on the Move Oxford, UK: Oxford Univ. Press
  35. Dissel S, Angadi L, Kirsenblat K, Suzuki Y, Donlea J. 35.  et al. 2015. Sleep restores behavioral plasticity to Drosophila mutants. Curr. Biol. 25:1270–81 [Google Scholar]
  36. Dissel S, Melnattur K, Shaw PJ. 36.  2015. Sleep, performance, and memory in flies. Curr. Sleep Med. Rep. 1:47–54 [Google Scholar]
  37. Donlea JM, Pimentel D, Miesenböck G. 37.  2014. Neuronal machinery of sleep homeostasis in Drosophila. Neuron 81:860–72 [Google Scholar]
  38. Donlea JM, Ramanan N, Shaw PJ. 38.  2009. Use-dependent plasticity in clock neurons regulates sleep need in Drosophila. Science 324:105–8 [Google Scholar]
  39. Donlea JM, Thimgan MS, Suzuki L, Gottschalk L, Shaw PJ. 39.  2011. Inducing sleep by remote control facilitates memory consolidation in Drosophila. Science 332:1571–76 [Google Scholar]
  40. Dubowy C, Moravcevic K, Yue Z, Wan JY, Van Dongen HPA. 40.  et al. 2016. Genetic dissociation of daily sleep and sleep following thermogenetic sleep deprivation in Drosophila. Sleep 39:1083–95 [Google Scholar]
  41. Dubowy C, Sehgal A. 41.  2017. Circadian rhythms and sleep in Drosophila melanogaster. Genetics 205:1–26 [Google Scholar]
  42. Eck S, Helfrich-Förster C, Rieger D. 42.  2016. The timed depolarization of morning and evening oscillators phase shifts the circadian clock of Drosophila. J. Biol. Rhythms 31:428–42 [Google Scholar]
  43. Fiebrig K. 43.  1912. Schlafende Insekten. Jena Z. Naturwiss. 48:315–64 [Google Scholar]
  44. Flanigan WF Jr. 44.  1972. Behavioral states and electroencephalograms of reptiles. The Sleeping Brain MH Chase 14–18 Los Angeles: Brain Inform. Serv./Brain Res. Inst., UCLA [Google Scholar]
  45. Fogle KJ, Baik LS, Houl JH, Tran TT, Roberts L. 45.  et al. 2015. CRYPTOCHROME-mediated phototransduction by modulation of the potassium ion channel β-subunit redox sensor. PNAS 112:2245–50 [Google Scholar]
  46. Fogle KJ, Parson KG, Dahm NA, Holmes TC. 46.  2011. CRYPTOCHROME is a blue-light sensor that regulates neuronal firing rate. Science 331:1409–13 [Google Scholar]
  47. Foltenyi K, Greenspan RJ, Newport JW. 47.  2007. Activation of EGFR and ERK by rhomboid signaling regulates the consolidation and maintenance of sleep in Drosophila. Nat. Neurosci. 10:1160–67 [Google Scholar]
  48. Fujii S, Krishnan P, Hardin P, Amrein H. 48.  2007. Nocturnal male sex drive in Drosophila. Curr. Biol. 17:3244–51 [Google Scholar]
  49. Ganguly-Fitzgerald I, Donlea J, Shaw PL. 49.  2006. Waking experience affects sleep need in Drosophila. Science 313:1775–81 [Google Scholar]
  50. Gilestro GF, Tononi G, Cirelli C. 50.  2009. Widespread changes in synaptic markers as a function of sleep and wakefulness in Drosophila. Science 324:109–12 [Google Scholar]
  51. Gmeiner F, Kołodziejczyk A, Yoshii T, Rieger D, Nässel DR, Helfrich-Förster C. 51.  2013. GABAB receptors play an essential role in maintaining sleep during the second half of the night in Drosophila melanogaster. J. Exp. Biol. 216:203837–43 [Google Scholar]
  52. Gorczyca MG, Hall JC. 52.  1987. Immunohistochemical localization of choline acetyltransferase during development and in Chats mutants of Drosophila melanogaster. J. Neurosci. 7:51361–69 [Google Scholar]
  53. Guo F, Yu J, Jung HJ, Abruzzi KC, Luo W. 53.  et al. 2016. Circadian neuron feedback controls the Drosophila sleep-activity profile. Nature 536:292–97 [Google Scholar]
  54. Haufe WO. 54.  1962. Ethological and statistical aspects of a quantal response in mosquitoes to environmental stimuli. Behaviour 20:221–41 [Google Scholar]
  55. Hausl-Hofstätter U. 55.  2008. Beobachtungen an nachtruhenden Hymenopteren in der Umgebung von Mali Lošinj, Kroatien (Anthophoridae, Andrenidae, Eumenidae, Scoliidae, Ichneumonidae). Joanna Zool 10:101–21 [Google Scholar]
  56. Haynes PR, Christmann BL, Griffith LC. 56.  2015. A single pair of neurons links sleep to memory consolidation in Drosophila melanogaster. eLife 4:e03868 [Google Scholar]
  57. Heisenberg M. 57.  1998. What do the mushroom bodies do for the insect brain? An introduction. Learn. Mem. 5:1–10 [Google Scholar]
  58. Helfrich-Förster C. 58.  2004. The circadian clock in the brain: a structural and functional comparison between mammals and insects. J. Comp. Physiol. A 190:601–13 [Google Scholar]
  59. Helfrich-Förster C. 59.  2014. From neurogenetic studies in the fly brain to a concept in circadian biology. J. Neurogenet. 28:3–4329–47 [Google Scholar]
  60. Helfrich-Förster C, Stengl M, Homberg U. 60.  1998. Organization of the circadian system in insects. Chronobiol. Int. 15:6567–94 [Google Scholar]
  61. Helfrich-Förster C, Wulf J, de Belle S. 61.  2002. Mushroom body influence on locomotor activity and circadian rhythms in Drosophila melanogaster. J. Neurogenet. 16:73–109 [Google Scholar]
  62. Hendricks JC, Finn SM, Panckeri KA, Chavkin J, Williams JA. 62.  et al. 2000. Rest in Drosophila is a sleep-like state. Neuron 25:129–38 [Google Scholar]
  63. Hendricks JC, Lu S, Kume K, Yin JC, Yang Z, Sehgal A. 63.  2003. Gender dimorphism in the role of cycle (BMAL1) in rest, rest regulation, and longevity in Drosophila melanogaster. J. Biol. Rhythms 18:12–25 [Google Scholar]
  64. Huber F. 64.  1960. Untersuchungen über die Funktion des Zentralnervensystems und insbesondere des Gehirns bei der Fortbewegung und der Lauterzeugung der Grille. Z. Vergl. Physiol. 44:60–132 [Google Scholar]
  65. Huber F. 65.  1965. Neural integration (central nervous system). The Physiology of Insecta IV M Rockstein 333–406 New York: Academic [Google Scholar]
  66. Joiner WJ, Crocker A, White BH, Sehgal A. 66.  2006. Sleep in Drosophila is regulated by adult mushroom bodies. Nature 441:757–60 [Google Scholar]
  67. Kaiser W. 67.  1985. Comparative neurobiology of sleep—the honeybee model. Sleep ‘84 WP Koella, E Riither, H Schulz 225–27 Stuttgart, Ger: Fischer [Google Scholar]
  68. Kaiser W. 68.  1988. Busy bees need rest, too. Behavioural and electromyographical sleep signs in honeybees. J. Comp. Physiol. A 163:565–84 [Google Scholar]
  69. Kaiser W. 69.  1995. Rest at night in some solitary bees—a comparison with the sleep-like state of honey bees. Apidologie 26:213–30 [Google Scholar]
  70. Kaiser W, Steiner-Kaiser J. 70.  1983. Neuronal correlates of sleep, wakefulness and arousal in a diurnal insect. Nature 301:707–9 [Google Scholar]
  71. Kaiser W, Weber T, Orro D, Miroschinikow A. 71.  2013. Oxygen supply of the heart and electrocardiogram potentials with reversed polarity in sleeping and resting honey bees. Apidologie 45:73–87 [Google Scholar]
  72. Keene AC, Duboué ER, McDonald DM, Dus M, Suh GS. 72.  et al. 2010. Clock and cycle limit starvation-induced sleep loss in Drosophila. Curr. Biol. 20:1209–15 [Google Scholar]
  73. Klein BA, Klein A, Wray MK, Mueller UG, Seeley TD. 73.  2010. Sleep deprivation impairs precision of waggle dance signaling in honey bees. PNAS 107:22705–9 [Google Scholar]
  74. Koh K, Evans JM, Hendricks JC, Sehgal AA. 74.  2006. A Drosophila model for age-associated changes in sleep:wake cycles. PNAS 103:13843–47 [Google Scholar]
  75. Koh K, Joiner WJ, Wu MN, Yue Z, Smith CJ, Sehgal A. 75.  2008. Identification of SLEEPLESS, a sleep-promoting factor. Science 321:5887372–76 [Google Scholar]
  76. Kramer A, Yang FC, Snodgrass P, Li X, Scammell TE. 76.  et al. 2001. Regulation of daily locomotor activity and sleep by hypothalamic EGF receptor signaling. Science 294:55512511–15 [Google Scholar]
  77. Kula-Eversole E, Nagoshi E, Shang Y, Rodriguez J, Allada R. 77.  2010. Surprising gene expression patterns within and between PDF-containing circadian neurons in Drosophila. PNAS 107:13497–502 [Google Scholar]
  78. Kume K, Kume S, Park SK, Hirsh J, Jackson FR. 78.  2005. Dopamine is a regulator of arousal in the fruit fly. J. Neurosci. 25:7377–84 [Google Scholar]
  79. Kunst M, Hughes ME, Raccuglia D, Felix M, Li M. 79.  et al. 2014. Calcitonin gene-related peptide neurons mediate sleep specific circadian output in Drosophila. Curr. Biol. 24:2652–64 [Google Scholar]
  80. Lebestky T, Chang JS, Dankert H, Zelnik L, Kim YC. 80.  et al. 2009. Two different forms of arousal in Drosophila are oppositely regulated by the dopamine D1 receptor ortholog DopR via distinct neural circuits. Neuron 64:522–36 [Google Scholar]
  81. Lee G, Park JH. 81.  2004. Hemolymph sugar homeostasis and starvation-induced hyperactivity affected by genetic manipulations of the adipokinetic hormone-encoding gene in Drosophila melanogaster. Genetics 167:311–23 [Google Scholar]
  82. Li X, Yu F, Guo A. 82.  2009. Sleep deprivation specifically impairs short-term olfactory memory in Drosophila. Sleep 32:1417–24 [Google Scholar]
  83. Liu Q, Liu S, Kodama MR, Driscoll MR, Wu MN. 83.  2012. Two dopaminergic neurons signal to the dorsal fan-shaped body to promote wakefulness in Drosophila. Curr. Biol. 22:2114–23 [Google Scholar]
  84. Liu S, Lamaze A, Liu Q, Tabuchi M, Yang Y. 84.  et al. 2014. WIDE AWAKE mediates the circadian timing of sleep onset. Neuron 82:151–66 [Google Scholar]
  85. Liu S, Liu Q, Tabuchi M, Wu MN. 85.  2016. Sleep drive is encoded by neural plastic changes in a dedicated circuit. Cell 165:1347–60 [Google Scholar]
  86. Maguire SE, Rhoades S, Chen W-F, Sengupta A, Yue Z. 86.  et al. 2015. Independent effects of GABA transaminase (GABAT) on metabolic and sleep homeostasis. J. Biol. Chem. 290:20407–16 [Google Scholar]
  87. Martelli C, Pech U, Kobbenbring S, Pauls D, Bahl B. 87.  et al. 2017. SIFamide translates hunger signals into appetitive and feeding behavior in Drosophila. Cell Rep 20:464–78 [Google Scholar]
  88. Martin J-R, Heisenberg M. 88.  1998. Mushroom bodies suppress locomotor activity in Drosophila melanogaster. Learn. Mem. 5:179–91 [Google Scholar]
  89. Muraro N, Ceriani MF. 89.  2015. Acetylcholine from visual circuits modulates the activity of arousal neurons in Drosophila. J. Neurosci. 35:5016315–27 [Google Scholar]
  90. Murphy KR, Deshpande SA, Yurgel ME, Quinn JP, Weissbach JL. 90.  et al. 2016. Postprandial sleep mechanics in Drosophila. eLife 5:e19334 [Google Scholar]
  91. Nitz DA, van Swinderen B, Tononi G, Greenspan RJ. 91.  2002. Electrophysiological correlates of rest and activity in Drosophila melanogaster. Curr. Biol. 12:1934–40 [Google Scholar]
  92. Ofstad TA, Zuker CS, Reiser MB. 92.  2011. Visual place learning in Drosophila melanogaster. Nature 474:203–9 [Google Scholar]
  93. Owald D, Waddell S. 93.  2015. Olfactory learning skews mushroom body output pathways to steer behavioral choice in Drosophila. Curr. Opin. Neurobiol. 35:178–84 [Google Scholar]
  94. Parisky KM, Agosto J, Pulver SR, Shang Y, Kuklin E. 94.  et al. 2008. PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit. Neuron 60:672–82 [Google Scholar]
  95. Parisky KM, Agosto Rivera JL, Donelson NC, Kotecha S, Griffith LC. 95.  2016. Reorganization of sleep by temperature in Drosophila requires light, the homeostat, and the circadian clock. Curr. Biol. 26:882–92 [Google Scholar]
  96. Park S, Sonn JY, Oh Y, Lim C, Choe J. 96.  2014. SIFamide and SIFamide receptor define a novel neuropeptide signaling to promote sleep in Drosophila. Mol. Cells 37:295–301 [Google Scholar]
  97. Pfeiffer K, Homberg U. 97.  2014. Organization and functional roles of the central complex in the insect brain. Annu. Rev. Entomol. 59:165–84 [Google Scholar]
  98. Pimentel D, Donlea JM, Talbot CB, Song SM, Thurston AJ, Miesenböck G. 98.  2016. Operation of a homeostatic sleep switch. Nature 536:333–37 [Google Scholar]
  99. Pirron H. 99.  1913. Le Problème Physiologique du Sommeil Paris: Masson
  100. Pitman JL, McGill JJ, Keegan KP, Allada R. 100.  2006. A dynamic role for the mushroom bodies in promoting sleep in Drosophila. Nature 441:753–56 [Google Scholar]
  101. Ramón F, Hernándes-Falcón J, Nguyen B, Bullock TH. 101.  2004. Slow wave sleep in crayfish. PNAS 101:11857–61 [Google Scholar]
  102. Rechtschaffen A, Bergmann BM, Everson CA, Kushida CA, Gilliland MA. 102.  1989. Sleep deprivation in the rat: X. Integration and discussion of the findings. Sleep 12:68–87 [Google Scholar]
  103. Reischig T, Stengl M. 103.  2003. Ultrastructure of pigment-dispersing hormone-immunoreactive neurons in a three-dimensional model of the accessory medulla of the cockroach Leucophaea maderae. Cell Tissue Res 314:3421–35 [Google Scholar]
  104. Riemensperger T, Isabel G, Coulom H, Neuser K, Seugnet L. 104.  et al. 2011. Behavioral consequences of dopamine deficiency in the Drosophila central nervous system. PNAS 108:834–39 [Google Scholar]
  105. Rodríguez-Sosa L, Calderón-Rosete G, Ortega-Cambranis A, De-Miguel FF. 105.  2017. Octopamine cyclic release and its modulation of visual sensitivity in crayfish. Comp. Biochem. Physiol. A 203:83–90 [Google Scholar]
  106. Saper CB, Fuller PM, Pedersen NP, Lu J, Scammell TE. 106.  2010. Sleep state switching. Neuron 68:1023–42 [Google Scholar]
  107. Saper CB, Scammell TE, Lu J. 107.  2005. Hypothalamic regulation of sleep and circadian rhythms. Nature 437:1257–63 [Google Scholar]
  108. Sauer S, Hermann E, Kaiser W. 108.  2004. Sleep deprivation in honey bees. J. Sleep Res. 13:145–52 [Google Scholar]
  109. Schendzielorz T, Schirmer K, Stolte P, Stengl M. 109.  2015. Octopamine regulates antennal sensory neurons via daytime-dependent changes in cAMP and IP3 levels in the hawkmoth Manduca sexta. PLOS ONE 9:9e0121230 [Google Scholar]
  110. Schlichting M, Menegazzi P, Lelito KR, Yao Z, Buhl E. 110.  et al. 2016. A neural network underlying circadian entrainment and photoperiodic adjustment of sleep and activity in Drosophila. J. Neurosci. 36:9084–96 [Google Scholar]
  111. Schulze H. 111.  1924. Über die Fühlerhaltung von Habrobracon jugl. Ash. (Braconidae); zugleich ein Beitrag zur Sinnesphysiologie und Psychologie dieser Schlupfwespe. Zool. Anz. 61:122–34 [Google Scholar]
  112. Schwaerzel M, Monastirioti M, Scholz H, Friggi-Grelin F, Birman S, Heisenberg M. 112.  2003. Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J. Neurosci. 23:3310495–502 [Google Scholar]
  113. Seidner G, Robinson JE, Wu M, Worden R, Masek P. 113.  et al. 2015. Identification of neurons with a privileged role in sleep homeostasis in Drosophila melanogaster. Curr. Biol. 25:2928–38 [Google Scholar]
  114. Seugnet L, Suzuki L, Donlea JM, Gottschalk L, Shaw PJ. 114.  2011. Sleep deprivation during early-adult development results in long-lasting learning deficits in adult Drosophila. Sleep 34:137–46 [Google Scholar]
  115. Seugnet L, Suzuki L, Vine L, Gottschalk L, Shaw PJ. 115.  2008. D1 receptor activation in the mushroom bodies rescues sleep-loss-induced learning impairments in Drosophila. Curr. Biol. 18:1110–17 [Google Scholar]
  116. Shang Y, Donelson NC, Vecsey CG, Guo F, Rosbash M, Griffith LC. 116.  2013. Short neuropeptide F is a sleep-promoting inhibitory modulator. Neuron 80:171–83 [Google Scholar]
  117. Shang Y, Griffith LC, Rosbash M. 117.  2008. Light-arousal and circadian photoreception circuits intersect at the large PDF cells of the Drosophila brain. PNAS 105:19587–94 [Google Scholar]
  118. Shang Y, Haynes P, Pírez N, Harrington KI, Guo F. 118.  et al. 2011. Imaging analysis of clock neurons reveals light buffers the wake-promoting effect of dopamine. Nat. Neurosci. 14:889–95 [Google Scholar]
  119. Shaw PJ, Cirelli C, Greenspan RJ, Tononi G. 119.  2000. Correlates of sleep and waking in Drosophila melanogaster. Science 287:1834–37 [Google Scholar]
  120. Shaw PJ, Tononi G, Greenspan RJ, Robinson DF. 120.  2002. Stress response genes protect against lethal effects of sleep deprivation in Drosophila. Nature 417:287–91 [Google Scholar]
  121. Sheeba VK, Fogle J, Kaneko M, Rashid S, Chou Y-T. 121.  2008. Large ventral lateral neurons modulate arousal and sleep in Drosophila. Curr. Biol. 18:1537–45 [Google Scholar]
  122. Shi M, Yue Z, Kuryatov JM, Lindstrom JM, Sehgal A. 122.  2014. Identification of redeye, a new sleep-regulating protein whose expression is modulated by sleep amount. eLife 3:e01473 [Google Scholar]
  123. Sitaraman D, Aso Y, Jin X, Chen N, Felix M. 123.  et al. 2015. Propagation of homeostatic sleep signals by segregated synaptic microcircuits of the Drosophila mushroom body. Curr. Biol. 25:2915–27 [Google Scholar]
  124. Sitaraman D, Aso Y, Rubin GM, Nitabach MN. 124.  2015. Control of sleep by dopaminergic inputs to the Drosophila mushroom body. Front. Neural. Circuits 9:73 [Google Scholar]
  125. Sokoloff L. 125.  1960. Metabolism of the central nervous system in vivo. Handbook of Physiology III Neurophysiology J Field, HW Magoun 1843–64 Bethesda, MD: Am. Physiol. Soc. [Google Scholar]
  126. Stahl ML, Orr WC, Bollinger C. 126.  1983. Postprandial sleepiness: objective documentation via polysomnography. Sleep 6:129–35 [Google Scholar]
  127. Stengl M, Arendt A. 127.  2016. Peptidergic circadian clock circuits in the Madeira cockroach. Curr. Opin. Neurobiol. 41:44–52 [Google Scholar]
  128. Strauss R. 128.  2002. The central complex and the genetic dissection of locomotor behavior. Curr. Opin. Neurobiol. 12:6633–38 [Google Scholar]
  129. Thimgan MS, Seugnet L, Turk J, Shaw PJ. 129.  2015. Identification of genes associated with resilience/vulnerability to sleep deprivation and starvation in Drosophila. Sleep 38:801–14 [Google Scholar]
  130. Thimgan MS, Suzuki Y, Seugnet L, Gottschalk L, Shaw PJ. 130.  2010. The perilipin homologue, lipid storage droplet 2, regulates sleep homeostasis and prevents learning impairments following sleep loss. PLOS Biol 8:e1000466 [Google Scholar]
  131. Tobler I. 131.  1983. Effect of forced locomotion on the rest-activity cycle of the cockroach. Behav. Brain Res. 8:351–60 [Google Scholar]
  132. Tobler I. 132.  1984. Evolution of the sleep process: a phylogenetic approach. Sleep Mechanisms AA Borbély, JL Valatx 207–26 Berlin: Springer [Google Scholar]
  133. Tobler I. 133.  1985. Deprivation of sleep and rest in vertebrates and invertebrates. Endogenous Sleep Substances and Sleep Regulation S Inoue, AA Borbély 57–66 Utrecht, the Neth.: VNU Sci. Press [Google Scholar]
  134. Tobler I. 134.  1995. Is sleep fundamentally different between mammalian species?. Behav. Brain Res. 69:1–235–41 [Google Scholar]
  135. Tobler I, Neuner-Jehle M. 135.  1992. 24-h variation of vigilance in the cockroach Blaberus giganteus. J. Sleep Res. 1:231–39 [Google Scholar]
  136. Tobler I, Stalder J. 136.  1988. Rest in the scorpion—a sleep-like state?. J. Comp. Physiol. A 163:227–35 [Google Scholar]
  137. Tononi G, Cirelli C. 137.  2003. Sleep and synaptic homeostasis: a hypothesis. Brain Res. Bull. 62:143–50 [Google Scholar]
  138. Tononi G, Cirelli C. 138.  2012. Time to be SHY? Some comments on sleep and synaptic homeostasis. Neural Plast 2012:415250 [Google Scholar]
  139. Tononi G, Cirelli C. 139.  2014. Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron 81:12–34 [Google Scholar]
  140. Ueno T, Tomita J, Tanimoto H, Endo K, Ito K. 140.  et al. 2012. Identification of a dopamine pathway that regulates sleep and arousal in Drosophila. Nat. Neurosci. 15:1516–23 [Google Scholar]
  141. Van Alphen B, Yap MHW, Kirszenblat L, Kottler B, van Swinderen B. 141.  2013. A dynamic deep sleep stage in Drosophila. J. Neurosci. 33:166917–27 [Google Scholar]
  142. Van der Vinne V, Riede SJ, Gorter JA, Eijer WG, Sellix MT. 142.  et al. 2014. Cold and hunger induce diurnality in a nocturnal mammal. PNAS 111:4215256–60 [Google Scholar]
  143. Varga AG, Kathman ND, Martin JP, Guo P, Ritzmann RE. 143.  2017. Spatial navigation and the central complex: sensory acquisition, orientation, and motor control. Front. Behav. Neurosci. 11:4 [Google Scholar]
  144. Waddell S, Armstrong JD, Kitamoto T, Kaiser K, Quinn WG. 144.  2000. The amnesiac gene product is expressed in two neurons in the Drosophila brain that are critical for memory. Cell 103:805–13 [Google Scholar]
  145. Westrich P, Westrich L, Müller A. 145.  1992. Beobachtungen zur Nachtruhe der Kraftbiene Biastes emarginatus (Schenck) (Hymenoptera, Apoidea, Anthrophoricae). Linzer Biol. Beitr. 24:13–12 [Google Scholar]
  146. Wicher D, Agricola H-J, Söhler S, Gundel M, Heinemann SH. 146.  et al. 2006. Differential receptor activation by cockroach adipokinetic hormones produces differential effects on ion currents, neuronal activity, and locomotion. J. Neurophysiol. 95:2314–25 [Google Scholar]
  147. Woods IG, Schoppik D, Shi VJ, Zimmerman S, Coleman HA. 147.  et al. 2014. Neuropeptidergic signaling partitions arousal behaviors in zebrafish. J. Neurosci. 34:3142–60 [Google Scholar]
  148. Wu M, Robinson JE, Joiner WJ. 148.  2014. SLEEPLESS is a bifunctional regulator of excitability and cholinergic synaptic transmission. Curr. Biol. 24:621–29 [Google Scholar]
  149. Wu MN, Joiner WJ, Dean Z, Yue CJ, Smith. 149.  et al. 2009. SLEEPNESS, a Ly-6/neurotoxin family member, regulates the levels, localization and activity of Shaker. Nat. Neurosci. 13:69–75 [Google Scholar]
  150. Yasuyama K, Kitamoto T, Salvaterra PM. 150.  1995. Immunocytochemical study of choline acetyltransferase in Drosophila melanogaster: an analysis of cis-regulatory regions controlling expression in the brain of cDNA-transformed flies. J. Comp. Neurol. 361:125–37 [Google Scholar]
  151. Young JM, Armstrong JD. 151.  2010. Structure of the adult central complex in Drosophila: organization of distinct neuronal subsets. J. Comp. Neurol. 13:1525–41 [Google Scholar]
  152. Yuan LL, Chen X. 152.  2004. Diversity of potassium channels in neuronal dendrites. Prog. Neurobiol. 78:374–89 [Google Scholar]
  153. Yuan Q, Joiner WJ, Sehgal A. 153.  2006. A sleep-promoting role for the Drosophila serotonin receptor 1A. Curr. Biol. 16:1051–62 [Google Scholar]
/content/journals/10.1146/annurev-ento-020117-043201
Loading
/content/journals/10.1146/annurev-ento-020117-043201
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error