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

• Published in: Current biology 2016-04, Vol.26 (7), p.882-892
• Main Authors: Parisky, Katherine M., Agosto Rivera, José L., Donelson, Nathan C., Kotecha, Sejal, Griffith, Leslie C.
• Format: Article
• Language: English
• Subjects: Animals; Circadian Clocks; CLOCK Proteins - metabolism; Drosophila melanogaster - physiology; Drosophila Proteins - metabolism; Light; Models, Animal; Period Circadian Proteins - metabolism; Sleep; Temperature; Up-Regulation
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2016.02.011

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 pro-arousal 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. •Ambient temperature changes the stereotypic sleep profile in Drosophila•Homeostatic rebound sleep is a critical component of the response to heat•Cycling light coordinates the temperature responses of daytime and nighttime sleep•Temperature is integrated with light cycle by a LNv-DN1p clock subcircuit Why do we sleep more during the day and less at night when it is hot? Parisky et al. show that the reorganization of sleep by increased ambient temperature in Drosophila is controlled by a coordinated interaction of light, the clock, and homeostatic processes. This allows animals to alter the timing of sleep while preserving its approximate amount.