Recurrent Circuitry for Balancing Sleep Need and Sleep

• Published in: Neuron (Cambridge, Mass.) Mass.), 2018-01, Vol.97 (2), p.378-389.e4
• Main Authors: Donlea, Jeffrey M., Pimentel, Diogo, Talbot, Clifford B., Kempf, Anissa, Omoto, Jaison J., Hartenstein, Volker, Miesenböck, Gero
• Format: Article
• Language: English
• Subjects: Animals; arousal; Brain - physiology; central complex; Circadian Rhythm; Drosophila; Drosophila melanogaster; Drosophila melanogaster - physiology; Drosophila Proteins - genetics; Drosophila Proteins - physiology; ellipsoid body; Excitatory Postsynaptic Potentials - physiology; fan-shaped body; Female; Homeostasis; Insect Hormones - physiology; Insects; Interneurons - physiology; Light; Locomotion - radiation effects; Male; Membrane Potentials; Memory; Nerve Tissue Proteins - physiology; Neurons; Neurons - physiology; Neuropeptides; Optogenetics; Receptors, G-Protein-Coupled - genetics; Receptors, G-Protein-Coupled - physiology; Receptors, Neuropeptide - genetics; Receptors, Neuropeptide - physiology; Recombinant Fusion Proteins - metabolism; relaxation oscillator; Sleep; Sleep - physiology; Sleep deprivation; sleep homeostasis; sleep pressure; Vision, Ocular
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2017.12.016

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. [Display omitted] •Sleep-promoting dFB neurons inhibit helicon cells of the central complex•Helicon cells transmit visual signals to R2 ring neurons and gate locomotion•Neurons generating sleep need and sleep-inducing neurons are recurrently connected•A unified mechanism accounts for sensory, motor, and homeostatic features of sleep Neurons encoding sleep need and sleep-inducing neurons are recurrently connected. A crucial link in the circuit is necessary for visually guided movements but inhibited during sleep. A unified mechanism can thus account for sensory, motor, and homeostatic aspects of sleep.