A Critical Period of Sleep for Development of Courtship Circuitry and Behavior in Drosophila

Overview

Journal Science

Specialty Science

Date 2014 Apr 19

PMID 24744368

Citations 90

Authors

Matthew S Kayser

Zhifeng Yue

Amita Sehgal

Affiliations

Soon will be listed here.

Abstract

Most animals sleep more early in life than in adulthood, but the function of early sleep is not known. Using Drosophila, we found that increased sleep in young flies was associated with an elevated arousal threshold and resistance to sleep deprivation. Excess sleep results from decreased inhibition of a sleep-promoting region by a specific dopaminergic circuit. Experimental hyperactivation of this circuit in young flies results in sleep loss and lasting deficits in adult courtship behaviors. These deficits are accompanied by impaired development of a single olfactory glomerulus, VA1v, which normally displays extensive sleep-dependent growth after eclosion. Our results demonstrate that sleep promotes normal brain development that gives rise to an adult behavior critical for species propagation and suggest that rapidly growing regions of the brain are most susceptible to sleep perturbations early in life.

Citing Articles

Sleep timing in flies from "adolescence" to adulthood.

Domenie E, Cusumano P, Montagnese S, Costa R Fly (Austin). 2025; 19(1):2448022.

PMID: 39773381 PMC: 11702927. DOI: 10.1080/19336934.2024.2448022.

Serotonin acts through multiple cellular targets during an olfactory critical period.

Mallick A, Tan H, Epstein J, Jing Ng C, Cook O, Gaudry Q iScience. 2024; 27(11):111083.

PMID: 39524339 PMC: 11550141. DOI: 10.1016/j.isci.2024.111083.

Developing forebrain synapses are uniquely vulnerable to sleep loss.

Gay S, Chartampila E, Lord J, Grizzard S, Maisashvili T, Ye M Proc Natl Acad Sci U S A. 2024; 121(44):e2407533121.

PMID: 39441640 PMC: 11536182. DOI: 10.1073/pnas.2407533121.

Stem cell-specific ecdysone signaling regulates the development of dorsal fan-shaped body neurons and sleep homeostasis.

Wani A, Chowdhury B, Luong J, Chaya G, Patel K, Isaacman-Beck J Curr Biol. 2024; 34(21):4951-4967.e5.

PMID: 39383867 PMC: 11537841. DOI: 10.1016/j.cub.2024.09.020.

Developmentally Unique Cerebellar Processing Prioritizes Self- over Other-Generated Movements.

Richardson A, Sokoloff G, Blumberg M J Neurosci. 2024; 44(19).

PMID: 38589230 PMC: 11079960. DOI: 10.1523/JNEUROSCI.2345-23.2024.

References

Kitamoto T . Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J Neurobiol. 2001; 47(2):81-92. DOI: 10.1002/neu.1018. View

Wagh D, Rasse T, Asan E, Hofbauer A, Schwenkert I, Durrbeck H . Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron. 2006; 49(6):833-44. DOI: 10.1016/j.neuron.2006.02.008. View

Hendricks J, Finn S, Panckeri K, Chavkin J, Williams J, Sehgal A . Rest in Drosophila is a sleep-like state. Neuron. 2000; 25(1):129-38. DOI: 10.1016/s0896-6273(00)80877-6. View

Frank M . Sleep and developmental plasticity not just for kids. Prog Brain Res. 2011; 193:221-32. DOI: 10.1016/B978-0-444-53839-0.00014-4. View

Hall J . The mating of a fly. Science. 1994; 264(5166):1702-14. DOI: 10.1126/science.8209251. View

Sheng M, Thompson M, Greenberg M . CREB: a Ca(2+)-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science. 1991; 252(5011):1427-30. DOI: 10.1126/science.1646483. View

van der Goes van Naters W, Carlson J . Receptors and neurons for fly odors in Drosophila. Curr Biol. 2007; 17(7):606-12. PMC: 1876700. DOI: 10.1016/j.cub.2007.02.043. View

Dickson B . Wired for sex: the neurobiology of Drosophila mating decisions. Science. 2008; 322(5903):904-9. DOI: 10.1126/science.1159276. View

Seugnet L, Suzuki Y, Donlea J, Gottschalk L, Shaw P . Sleep deprivation during early-adult development results in long-lasting learning deficits in adult Drosophila. Sleep. 2011; 34(2):137-46. PMC: 3022932. DOI: 10.1093/sleep/34.2.137. View

10.

Pfeiffer B, Truman J, Rubin G . Using translational enhancers to increase transgene expression in Drosophila. Proc Natl Acad Sci U S A. 2012; 109(17):6626-31. PMC: 3340069. DOI: 10.1073/pnas.1204520109. View

11.

Astic L, Lacote D . Ontogenesis of the states of sleep in rat, cat, and guinea pig during the first postnatal month. Dev Psychobiol. 1970; 2(4):216-39. DOI: 10.1002/dev.420020407. View

12.

Schechtman V, Harper R, Wilson A, Southall D . Sleep state organization in normal infants and victims of the sudden infant death syndrome. Pediatrics. 1992; 89(5 Pt 1):865-70. View

13.

Crocker A, Shahidullah M, Levitan I, Sehgal A . Identification of a neural circuit that underlies the effects of octopamine on sleep:wake behavior. Neuron. 2010; 65(5):670-81. PMC: 2862355. DOI: 10.1016/j.neuron.2010.01.032. View

14.

Tanenhaus A, Zhang J, Yin J . In vivo circadian oscillation of dCREB2 and NF-κB activity in the Drosophila nervous system. PLoS One. 2012; 7(10):e45130. PMC: 3471920. DOI: 10.1371/journal.pone.0045130. View

15.

Wu M, Koh K, Yue Z, Joiner W, Sehgal A . A genetic screen for sleep and circadian mutants reveals mechanisms underlying regulation of sleep in Drosophila. Sleep. 2008; 31(4):465-72. PMC: 2279757. DOI: 10.1093/sleep/31.4.465. View

16.

Shaw P, Cirelli C, Greenspan R, Tononi G . Correlates of sleep and waking in Drosophila melanogaster. Science. 2000; 287(5459):1834-7. DOI: 10.1126/science.287.5459.1834. View

17.

Kim W, Jan L, Jan Y . A PDF/NPF neuropeptide signaling circuitry of male Drosophila melanogaster controls rival-induced prolonged mating. Neuron. 2013; 80(5):1190-205. PMC: 3867312. DOI: 10.1016/j.neuron.2013.09.034. View

18.

Wang L, Han X, Mehren J, Hiroi M, Billeter J, Miyamoto T . Hierarchical chemosensory regulation of male-male social interactions in Drosophila. Nat Neurosci. 2011; 14(6):757-62. PMC: 3102769. DOI: 10.1038/nn.2800. View

19.

Kondoh Y, Kaneshiro K, Kimura K, Yamamoto D . Evolution of sexual dimorphism in the olfactory brain of Hawaiian Drosophila. Proc Biol Sci. 2003; 270(1519):1005-13. PMC: 1691346. DOI: 10.1098/rspb.2003.2331. View

20.

Yamamoto D, Koganezawa M . Genes and circuits of courtship behaviour in Drosophila males. Nat Rev Neurosci. 2013; 14(10):681-92. DOI: 10.1038/nrn3567. View