Behavioral and genetic features of sleep ontogeny in Drosophila

Abstract

The fruit fly Drosophila melanogaster, like most organisms, exhibits increased sleep amount and depth in young compared to mature animals. While the fly has emerged as a powerful model for studying sleep during development, qualitative behavioral features of sleep ontogeny and its genetic control are poorly understood. Here we find that, in addition to increased sleep time and intensity, young flies sleep with less place preference than mature adults, and, like mammals, exhibit more motor twitches during sleep. In addition, we show that ontogenetic changes in sleep amount, twitch, and place preference are preserved across sleep mutants with lesions in distinct molecular pathways. Our results demonstrate that sleep ontogeny is characterized by multifaceted behavioral changes, including quantitative and qualitative alterations to sleep as animals mature. Further, the preservation of sleep ontogenetic changes despite mutations that alter sleep time suggests independent genetic control mechanisms for sleep maturation.

Pdm3 directs sleep circuit development to control sleep maturation

“…More broadly, there are no known genes that regulate sleep ontogenetic change. We previously found that all studied short and long-sleeping Drosophila mutants sleep more when young (Dilley et al, 2018). Thus, genes regulating sleep ontogenetic change are likely distinct from 50 those that control sleep duration.…”

“…Across species, sleep amounts are highest in early life and decrease as animals mature (Kayser and Biron, 2016;Roffwarg et al, 1966). Increasing evidence suggests early life sleep may represent a distinct behavioral state, uniquely evolved for the needs of a developing nervous system (Blumberg, 2015;Clawson et al, 2016;Dilley et al, 2018;35 Frank, 2011). In humans, childhood sleep disturbances portend later neurocognitive deficits, possibly because sleep loss impinges on neural circuit formation (Kotagal, 2015;O'Brien, 2009).…”

“…Although mechanisms controlling mature adult sleep have been uncovered (Allada et al, 2017), the regulation of early life sleep remains poorly understood. 40 Like other animals, the fruit fly, Drosophila melanogaster, exhibits increased sleep duration in young adulthood that tapers with maturity (Dilley et al, 2018;Kayser et al, 2014;Shaw et al, 2000). At the circuit level, activity of wake-promoting dopaminergic (DA) neurons increases as flies mature, exerting greater inhibitory influence on the sleep-promoting dorsal fan shaped body (dFSB) (Donlea et al, 2014; 45 Kayser et al, 2014;Liu et al, 2012;Ueno et al, 2012).…”

Identification of a molecular basis for the juvenile sleep state

“…Across species, sleep amounts are highest in early life and decrease as animals mature (Kayser and Biron, 2016;Roffwarg et al, 1966). Increasing evidence suggests early life sleep may represent a distinct behavioral state, uniquely evolved for the needs of a developing nervous system (Blumberg, 2015;Clawson et al, 2016;Dilley et al, 2018;Frank, 2011). In humans, childhood sleep disturbances portend later neurocognitive deficits, possibly because sleep loss impinges on neural circuit formation (Kotagal, 2015;O'Brien, 2009).…”

“…Like other animals, the fruit fly, Drosophila melanogaster, exhibits increased sleep duration in young adulthood that tapers with maturity (Dilley et al, 2018;Kayser et al, 2014;Shaw et al, 2000). At the circuit level, activity of wake-promoting dopaminergic (DA) neurons increases as flies mature, exerting greater inhibitory influence on the sleep-promoting dorsal fan shaped body (dFSB) (Donlea et al, 2014;Kayser et al, 2014;Liu et al, 2012;Ueno et al, 2012).…”