Sleep pressure after sleep deprivation in flies can be counteracted by raising their sexual arousal

Regulation of sleep homeostasis by sexual arousal. Esteban J Beckwith et al. eLife 2017;6:e27445 doi: 10.7554/eLife.27445

Abstract: In all animals, sleep pressure is under continuous tight regulation. It is universally accepted that this regulation arises from a two-process model, integrating both a circadian and a homeostatic controller. Here we explore the role of environmental social signals as a third, parallel controller of sleep homeostasis and sleep pressure. We show that, in Drosophila melanogaster males, sleep pressure after sleep deprivation can be counteracted by raising their sexual arousal, either by engaging the flies with prolonged courtship activity or merely by exposing them to female pheromones.

---
Finally, to investigate whether mere sexual arousal is responsible for this effect, we used flies mutant in the TDC2 gene, that possess lower levels of tyramine and octopamine (Crocker and Sehgal, 2008) and were previously shown to court male as well as female flies (Huang et al., 2016). We hypothesised that if these flies are sexually aroused by both male and female partners, they should then respond with a suppression of sleep rebound to both conditions of social interaction. This was what we observed indeed (Figure 8D,E). In flies with a bi-sexual orientation, both MF and MM interaction lead to a strong suppression of sleep rebound.

[...] migratory birds and cetaceans were reported to have the ability to suppress sleep at certain important periods of their lives, namely during migration or immediately after giving birth (Fuchs et al., 2009; Lyamin et al., 2005; Rattenborg et al., 2004); flies, similarly, were shown to lack sleep rebound after starvation-induced sleep deprivation (Thimgan et al., 2010) or after induction of sleep deprivation through specific neuronal clusters (Seidner et al., 2015). Perhaps even more fitting with our findings is the observation that male pectoral sandpipers, a type of Arctic bird, can forego sleep in favour of courtship during the three weeks time window of female fertility (Lesku et al., 2012). It appears, therefore, that animals are able to balance sleep needs with other, various, biological drives. It would be interesting to see whether these drives act to suppress sleep through a common regulatory circuit. Rebound sleep has always been considered one of the most important features of sleep itself. Together with the reported death by sleep deprivation, it is frequently used in support of the hypothesis that sleep is not an accessory phenomenon but a basic need of the organism (Cirelli and Tononi, 2008). Understanding the regulation of rebound sleep, therefore, may be crucial to understanding the very function of sleep. Interestingly, in our paradigm rebound sleep is not postponed, but rather eliminated. Moreover, on rebound day, the sleep architecture of sexually aroused male flies does not seem to be affected: the sleep bout numbers appear to be similar to their mock control counterparts, while the length of sleep bouts is, if anything, slightly reduced (Figure 1 – figure supplement 1).