Nighttime sleep promotes mechanosensory habituation in Drosophila

Abstract

Sleep is a highly conserved behaviour that facilitates episodic, procedural, and/or associative modes of memory across species 1-3, a process hypothesised to involve structural downscaling of synapses potentiated during waking episodes 4-6. Habituation, an ancient form of non-associative memory in which repetition of a stimulus leads to diminishing behavioural responses, is considered a prerequisite for such complex forms of learning 7,8. Yet whether sleep also influences the capacity of organisms to habituate is poorly understood. Here we examine this question using the fruit fly, Drosophila. We describe an automated system that yields long-term analogue measurements of habituation to mechanosensory stimuli in adult flies. Using this platform, we find that Drosophila lacking neuronal calcium sensor Neurocalcin - which exhibit reduced sleep specifically during the night 9 - display impaired mechanosensory habituation during the day. Mimicking a method used to treat insomnia 10, we show that compressing nighttime duration both restores consolidated night sleep and renormalises habituation in Neurocalcin mutants. Conversely, in wild type flies without sleep deficits, decreasing night length reduces total night sleep and disrupts daytime habituation. In wild type flies, exposure to longer nights - which increases overall night sleep - enhances synaptic downscaling in sensory circuits. Strikingly, this effect is abolished in Neurocalcin mutants, which do not exhibit increased sleep under these conditions. Collectively, our findings reveal a role for nighttime sleep in facilitating habituation and suggest that this may occur by promoting synaptic downscaling.