Integration of sleep homeostasis and navigation in Drosophila

Author summary In Drosophila, sleep and navigation are largely disconnected fields, even though the same brain structures and connected neural circuits are important for the two different functionalities. Motivated by experimental results from both fields as well as the connectome, we use theoretical modeling to describe the coupled dynamics of homeostatic sleep and navigation circuits in the central complex of Drosophila. The resulting model can incorporate and explain several experimental findings about sleep and navigation in flies and mice. The model is based on a ring attractor network which is combined with plasticity rules that change between sleep and wake phases and shows autonomous dynamics during sleep, reminiscent of observations in the head direction system of mice. During sleep, the brain undergoes dynamic and structural changes. In Drosophila, such changes have been observed in the central complex, a brain area important for sleep control and navigation. The connectivity of the central complex raises the question about how navigation, and specifically the head direction system, can operate in the face of sleep related plasticity. To address this question, we develop a model that integrates sleep homeostasis and head direction. We show that by introducing plasticity, the head direction system can function in a stable way by balancing plasticity in connected circuits that encode sleep pressure. With increasing sleep pressure, the head direction system nevertheless becomes unstable and a sleep phase with a different plasticity mechanism is introduced to reset network connectivity. The proposed integration of sleep homeostasis and head direction circuits captures features of their neural dynamics observed in flies and mice.