Individual olfactory channels shape distinct parameters of sleep architecture

Abstract

AbstractAcross the animal kingdom, olfactory dysfunction and anosmia have been associated with disruptions in sleep. In the fruit fly Drosophila melanogaster, various studies have demonstrated that broadly inhibiting olfactory receptor neurons (ORNs) similarly disrupts sleep/wake cycles, suggesting that baseline ORN signaling is an integral component of olfactory modulation of sleep. However, due to the diversity of ORNs and combinatorial nature of olfactory processing, many of the cellular and molecular mechanisms by which ORNs modulate sleep remain unclear. In this study, we addressed this gap of knowledge by characterizing the contributions of different ensembles of ORNs, individual ORN types, and a known modulator of ORNs on baseline sleep architecture. We find that the activity of distinct ORN types are important for day and nighttime sleep and heterogeneously shape parameters of sleep architecture. Importantly, the effects of ORN signaling on sleep are adjusted across mating status, suggesting that distinct ORN types are recruited within the context of sleep depending on the demands of the animal. Furthermore, the effects of ORN signaling on sleep are in part shaped by heterogeneous serotonin (5-HT) receptor expression. Together, this work identifies cellular and molecular pathways bridging olfaction and sleep, and helps establish a circuit model that can be used to further characterize the behavioral consequences of sensory dysfunction.