title: A dynamic deep sleep stage in Drosophila.
abstract: How might one determine whether simple animals such as flies sleep in stages? Sleep in mammals is a dynamic process involving different stages of sleep intensity, and these are typically associated with measurable changes in brain activity (Blake and Gerard, 1937; Rechtschaffen and Kales, 1968; Webb and Agnew, 1971). Evidence for different sleep stages in invertebrates remains elusive, even though it has been well established that many invertebrate species require sleep (Campbell and Tobler, 1984; Hendricks et al., 2000; Shaw et al., 2000; Sauer et al., 2003). Here we used electrophysiology and arousal-testing paradigms to show that the fruit fly, Drosophila melanogaster, transitions between deeper and lighter sleep within extended bouts of inactivity, with deeper sleep intensities after ∼15 and ∼30 min of inactivity. As in mammals, the timing and intensity of these dynamic sleep processes in flies is homeostatically regulated and modulated by behavioral experience. Two molecules linked to synaptic plasticity regulate the intensity of the first deep sleep stage. Optogenetic upregulation of cyclic adenosine monophosphate during the day increases sleep intensity at night, whereas loss of function of a molecule involved in synaptic pruning, the fragile-X mental retardation protein, increases sleep intensity during the day. Our results show that sleep is not homogenous in insects, and suggest that waking behavior and the associated synaptic plasticity mechanisms determine the timing and intensity of deep sleep stages in Drosophila.
authors.affiliation: Queensland Brain Institute, The University of Queensland, St Lucia, Queensland 4072, Australia.
authors.forename: Bart
authors.initials: B
authors.lastname: van Alphen
authors.forename: Melvyn H W
authors.initials: MH
authors.lastname: Yap
authors.forename: Leonie
authors.initials: L
authors.lastname: Kirszenblat
authors.forename: Benjamin
authors.initials: B
authors.lastname: Kottler
authors.forename: Bruno
authors.initials: B
authors.lastname: van Swinderen
mesh_terms: D000262:Adenylyl Cyclases / Q000378:metabolism; D000818:Animals; D030801:Animals, Genetically Modified; D001921:Brain / Q000502:physiology*; D050882:CREB-Binding Protein / Q000378:metabolism; D004330:Drosophila / Q000502:physiology*; D029721:Drosophila Proteins / Q000235:genetics; D051959:ELAV Proteins / Q000235:genetics; D001330:Electronic Data Processing; D005071:Evoked Potentials / Q000235:genetics / Q000502:physiology; D005260:Female; D051860:Fragile X Messenger Ribonucleoprotein 1 / Q000235:genetics; D005786:Gene Expression Regulation / Q000235:genetics; D008124:Locomotion; D008297:Male; D009154:Mutation / Q000235:genetics; D017711:Nonlinear Dynamics; D062308:Optogenetics; D010812:Physical Stimulation; D012684:Sensory Thresholds / Q000502:physiology; D012892:Sleep Deprivation; D012894:Sleep Stages / Q000502:physiology*; D012919:Social Behavior; D018709:Statistics, Nonparametric; D013569:Synapses / Q000378:metabolism; D013997:Time Factors; D014335:Tropomyosin / Q000235:genetics; D014851:Wakefulness
chemical_list: D000262:Adenylyl Cyclases; D050882:CREB-Binding Protein; D029721:Drosophila Proteins; D051959:ELAV Proteins; D051860:Fragile X Messenger Ribonucleoprotein 1; D014335:Tropomyosin; C498009:ELAV protein, Drosophila; C467328:FMR1 protein, Drosophila; C097163:Tm2 protein, Drosophila