Sleep promotes aversive value coding in Drosophila

Abstract Sleep is a state of reduced behavioural responsiveness to the external world. Lowered arousal is thought to arise from sensory gating in the brain, yet there is compelling evidence that stimuli can still be processed to some degree. Which aspects of sensory information are processed during sleep remains largely unknown. Here, we perform comprehensive recordings of activity from multiple neuron types during sleep and wakefulness in the Drosophila olfactory association center. We find that baseline activity of dopamine neurons (DANs) is distinct between active, rest and sleep states, enabling a decoder to predict when the fly is asleep. Optogenetic inhibition of DANs acutely induces sleep and lowers odor-evoked arousal, suggesting causality between DAN activity and behavior. We then examine odor processing during sleep, and find that whereas coding of odor identity in Kenyon cells (KCs) remains intact, coding of odor value in DANs is altered. Specifically, DANs encoding positive (attractive) and negative (aversive) values change their odor responses in an opposing manner, producing more aversive odor representations during sleep. Consistent with these changes in neural activity, sleeping flies awoken by odors show reduced approach and increased avoidance behaviour. Taken together, our data reveal that the brain does not simply suppress the propagation of sensory signals during sleep; rather, it utilizes different cell types to retain or modify specific aspects of sensory information. The aversive odor evaluation in DANs may have ethological benefits as it suppresses the motivation to pursue attractive odors during sleep and primes defensive action when aroused by the scent of potential dangers.