Regulation of sleep homeostasis by sexual arousal

Why we sleep remains an unresolved mystery of biology. Why do humans have to spend one-third of their lifetime in a status of profound unconsciousness which leaves them vulnerable and endangered? What do we gain from it? We still do not possess an answer to this question but we assume that it must be something tremendously important, also considered that sleep appears to be a necessity not just in humans but in all animals – including fruit flies. A particularly intriguing evolutionary conserved feature of sleep is what we call “sleep homeostasis”, that is: the innate modulation of sleep pressure based on previous sleep amount. If we have a good long nap, we may have a harder time falling asleep at night; conversely, if we pull an all-nighter partying on Sunday night, we are going to have a hard time at the office on the following morning. That is sleep homeostasis.

Is sleep homeostasis an unmodifiable, sovereign need in the animal or can it somehow be suppressed? Previous studies showed that migratory birds may be able to resist the temptation to sleep while flying above the ocean. Similarly, male pectoral sandpipers, a type of Arctic bird, can forego sleep in favour of courtship during the three weeks time window of female fertility. Could we find a similar behaviour in a genetically amenable animal model, like fruit flies?

In a “blind date” experiment, we forced interaction in a restricted space between socially naive, young, male fruit flies and receptive females. The interaction between the two led to an uninterrupted passionate courtship lasting the entire 24 hour period (and to one – and, in some cases, more – events of copulations). Surprisingly, not only did male flies forego sleep when prompted with a receptive female counterpart, but they also suppressed their natural sleep homeostasis and never recovered from the sleep lost courting. In the second set of experiments, we forcefully kept flies awake by employing robots that would automatically disturb the flies whenever they would fall asleep. At the end of the sleep deprivation treatment, flies would normally recover the lost sleep by having an extra nap. However, raising the sexual arousal of male flies by simply exposing them to the female pheromone, abolished their homeostatic need.

Ours is a study on the fundamental biological underpinnings of sleep. Our goal is to show that sleep is not a disconnected, uncontrollable phenomenon but a biological drive that can, in some conditions, be overcome. The study is particularly directed at other researchers and provides an important caveat not to be forgotten when conducting sleep experiments: it is possible to create an internal state in the animal that will heavily affect sleep regulation, without interfering with sleep regulatory circuits. A researcher may be artificially activating neurons that make an animal stressed, anxious, angered, or in love and all of these neurons will ultimately have an effect on sleep. Yet, they shall not be classified directly as “sleep neurons” or we will end up with a false map of where sleep neurons really are.

eLife 2017 Sep 12;6;e27445
Regulation of sleep homeostasis by sexual arousal
Esteban J. Beckwith, Quentin Geissmann, Alice S. French, and Giorgio F. Gilestro

Online published paper

Supplementary Material

Interactive supplementary videos
Supplementary movies as raw dataset

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