Reorganization of Sleep by Temperature in Drosophila Requires Light, the Homeostat, and the Circadian Clock

Abstract

SUMMARY Increasing ambient temperature reorganizes the Drosophila sleep pattern in a way similar to the human response to heat, increasing daytime sleep while decreasing nighttime sleep. Mutation of core circadian genes blocks the immediate increase in daytime sleep, but not the heat-stimulated decrease in nighttime sleep, when animals are in a light:dark cycle. The ability of per01 flies to increase daytime sleep in light:dark can be rescued by expression of PER in either LNv or DN1p clock cells and does not require rescue of locomotor rhythms. Prolonged heat exposure engages the homeostat to maintain daytime sleep in the face of nighttime sleep loss. In constant darkness, all genotypes show an immediate decrease in sleep in response to temperature shift during the subjective day, implying that the absence of light input uncovers a clock-independent proarousal effect of increased temperature. Interestingly, the effects of temperature on nighttime sleep are blunted in constant darkness and in cryOUT mutants in light:dark, suggesting that they are dependent on the presence of light the previous day. In contrast, flies of all genotypes kept in constant light sleep more at all times of day in response to high temperature, indicating that the presence of light can invert the normal nighttime response to increased temperature. The effect of temperature on sleep thus reflects coordinated regulation by light, the homeostat, and components of the clock, allowing animals to reorganize sleep patterns in response to high temperature with rough preservation of the total amount of sleep.

A Genetic Screen To Assess Dopamine Receptor (DopR1) Dependent Sleep Regulation inDrosophila

“…Furthermore, distinctly different levels of cocaine-induced activity observed for wild-type animals during the day (low induced activity) vs. night (high induced activity) suggests potential separability between day and night that is nevertheless dependent in part on DopR function and may support spatially distinct circuits (Lebestky et al 2009). Given the separability of day and night circadian oscillators (Grima et al 2004; Stoleru et al 2004) and the differential expression of arousal activities in the day and night (Ishimoto et al 2012; Parisky et al 2016), this data identifies a requirement for DopR in the mushroom body for daytime sleep and arousal regulation. Future immunohistochemical and double mutant analyses with DopR and previously identified day sleep modulators, such as sex peptide (Isaac et al 2010), Ecdysone receptor, and DTS-3 (Ishimoto et al 2012), may also be informative in better understanding the network of molecules involved in day sleep regulation.…”

“…Sleep in Drosophila can be divided into multiple behavioral dimensions for investigation of potentially separable aspects of sleep behavior, such as onset of sleep, duration, number of sleep bouts, and average duration of individual sleep bouts. Furthermore, both genetic and environmental factors, such as temperature and light, can differentially affect parameters of Drosophila sleep in the day vs. night period (Ishimoto et al 2012; Parisky et al 2016). …”

Temporal calcium profiling of specific circadian neurons in freely moving flies

“…S3). It would be interesting to assay the E cell pattern at 29°C, which causes a more nocturnal activity pattern (34). Would the E cell and gDN1 Tric-LUC patterns also change?…”

Modulation of light-driven arousal by LIM-homeodomain transcription factor Apterous in large PDF-positive lateral neurons of the Drosophila brain

“…Drosophila sleep is modulated by external signals (e.g., light and temperature) and internal signals (e.g., circadian clock, sleep pressure, and hunger)163738. Since the induction of arousal is determined by the balance between external and internal impacts, neural mechanisms, which positively and negatively regulate arousal level, are required for keeping the suitable quality and/or quantity of sleep/wake behaviors.…”