Integration of sleep homeostasis and navigation in Drosophila

Abstract

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.

Coherent multi-level network oscillations create neural filters to favor quiescence over navigation in Drosophila

“…With increasing sleep need GABAergic R5 neurons increase their presynaptic weight (Liu et al, 2016), which tilts the head direction system to more inhibition. While similar interactions have recently been proposed as part of a theoretical model (Flores-Valle et al, 2021), we here provide experimental evidence for this, demonstrating that rhythmic R5 activity hyperpolarizes the head direction system to suppress spontaneous events ( Fig. 6 ).…”

“…At the level of the central complex it has become clear that the dorsal fan-shaped body (dFSB) encodes a sleep switch (Donlea et al, 2009; Pimentel et al, 2016) that interacts with ExR1/helicon cells, which process visual information and gate locomotion, positioning this network as an ideal candidate for balancing arousal and sleep (Donlea et al, 2018). Moreover, helicon cells interact with the R5 network, which based on its connectivity likely can engage in both navigation and sleep regulation (Flores-Valle et al, 2021). We recently discovered that in the R5 circuit, network-specific synchronization generating compound SWA arises over the day to integrate circadian and homeostatic sleep drive, tilting flies towards sleep or maintaining it to ensure adequate sleep quality (Raccuglia et al, 2019).…”

“…Moreover, helicon cells interact with the R5 network, which based on its connectivity likely can engage in both navigation and sleep regulation (Flores-Valle et al, 2021). We recently discovered that in the R5 circuit, network-specific synchronization generating compound SWA arises over the day to integrate circadian and homeostatic sleep drive, tilting flies towards sleep or maintaining it to ensure adequate sleep quality (Raccuglia et al, 2019).…”

Dynamics of sleep and feeding homeostasis inDrosophilaglia and neurons

“…In Drosophila , a number of cell types and brain regions have been found to be important for sleep. Neural substrates for sleep regulation circuits as postulated by the two-process model have been investigated in the ellipsoid body (EB) and fan-shaped body (FB) of the central complex 14, 19–21, 26, 27 , an area in the center of the fly brain also important for memory and navigation 28 . Sleep depriving flies for 6 21 or 12 19 hours led to an increase of activity in calcium or electrophysiology recordings in brain explants, consistent with the behavior of a homeostat.…”

“…A side view of the fly was recorded with a camera at 10 Hz with a resolution of 640 × 480 during the whole experiment, which was used later for behavior classification. The VR, implemented as described 27,73 displayed a dark stripe on a bright background using a blue laser (488 nm), which was switched off 14/37 during the night for 12 hours. The VR night and day cycle was synchronized to the day and night cycle used in the fly incubator before the experiment.…”