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.
An animal's need to sleep grows with time spent awake and decays again during sleep. In the brain, a homeostatic process or signal has been proposed to represent sleep need, steadily increasing during wakefulness and gradually decreasing during sleep. However, such dynamics of a sleep homeostat, capturing the changing need to sleep in real time depending on behavior, has so far not been observed in identified cells.
Here, using a system that we developed for monitoring calcium activity over multiple days in head-fixed, walking fruit flies, we find that a class of glia in the fly brain, called ensheathing glia, shows dynamics expected of a sleep homeostat. Calcium levels in these cells - monitored in a central brain area important for memory, navigation and sleep - integrate activity during wakefulness, reset during sleep, and saturate under sleep deprivation. Optogenetic activation of ensheathing glia induces sleep consistent with charging of the homeostat.
The dynamics of the sleep homeostat, observed in glia of different brain compartments with similar but distinct dynamics, agree with conceptual model expectations. Ensheathing glia therefore act as a system for sleep control distributed across brain areas. The structural arrangement of these glia suggests that sleep homeostasis differentially impacts large ensembles of cells at the same time.
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