A half-center oscillator regulates sleep pressure

Abstract

Abstract Changes in oscillatory neural dynamics reflect—but may not necessarily determine—transitions between sleep stages and variations in sleep pressure. Here we show that sleep-control neurons innervating the dorsal fan-shaped body of Drosophila (dFBNs) produce slow-wave activity (SWA) that is causally linked to sleep. The dFBN ensemble contains bistable cells whose membrane voltages oscillate between hyperpolarized DOWN and depolarized UP states. The oscillations rely on interhemispheric competition of two half-centers connected by inhibitory glutamatergic synapses. dFBN-restricted interference with glutamate release disrupts SWA and baseline as well as rebound sleep, whereas the optogenetic replay of SWA induces sleep. dFBNs generate SWA throughout the sleep–wake cycle (despite mutual antagonism with arousing dopaminergic neurons) and adjust its power to sleep need via sleep history-dependent increases in excitability and homeostatic synaptic depression. The oscillatory format permits a continuous encoding of sleep pressure but requires mechanisms that convert the amplitude-modulated signal into binary sleep–wake states.