Sleep-promoting neurons in the dorsal fan-shaped body (dFB) of Drosophila are integral to sleep homeostasis, but how these cells impose sleep on the organism is unknown. We report that dFB neurons communicate via inhibitory transmitters, including allatostatin-A (AstA), with interneurons connecting the superior arch with the ellipsoid body of the central complex. These "helicon cells" express the galanin receptor homolog AstA-R1, respond to visual input, gate locomotion, and are inhibited by AstA, suggesting that dFB neurons promote rest by suppressing visually guided movement. Sleep changes caused by enhanced or diminished allatostatinergic transmission from dFB neurons and by inhibition or optogenetic stimulation of helicon cells support this notion. Helicon cells provide excitation to R2 neurons of the ellipsoid body, whose activity-dependent plasticity signals rising sleep pressure to the dFB. By virtue of this autoregulatory loop, dFB-mediated inhibition interrupts processes that incur a sleep debt, allowing restorative sleep to rebalance the books. VIDEO ABSTRACT.
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Drosophila melanogaster, arousal, central complex, ellipsoid body, fan-shaped body, relaxation oscillator, sleep homeostasis, sleep pressure, Animals, Brain, Circadian Rhythm, Drosophila Proteins, Drosophila melanogaster, Excitatory Postsynaptic Potentials, Female, Homeostasis, Insect Hormones, Interneurons, Light, Locomotion, Male, Membrane Potentials, Nerve Tissue Proteins, Neurons, Optogenetics, Receptors, G-Protein-Coupled, Receptors, Neuropeptide, Recombinant Fusion Proteins, Sleep, Vision, Ocular