The voltage-gated potassium channel Shaker promotes sleep via thermosensitive GABA transmission

Abstract

Genes and neural circuits coordinately regulate sleep homeostasis. However, it remains elusive how these endogenous factors shape animal sleep in response to environmental changes. Here, we found that Shaker (Sh)-expressing GABAergic neurons projecting onto dorsal fan-shaped body (dFSB) constitute a neural pathway important for temperature-adaptive sleep behaviors in Drosophila. Loss of Sh function potently suppressed sleep at low temperature whereas light and high temperature cooperatively gated Sh effects on sleep. RNA interference-mediated depletion of Sh expression in GABAergic neurons partially phenocopied Sh mutants. Moreover, trans-heterozygous mutations that decrease GABA transmission rescued Sh mutant sleep. Transgenic mapping further revealed that the ionotropic GABA receptor, Resistant to dieldrin (Rdl), in dFSB neurons acts downstream of Sh and antagonizes the sleep-promoting effects of Sh. In fact, Rdl inhibited the intracellular cAMP signaling of constitutively active dopaminergic synapses on dFSB neurons at low temperature. On the other hand, high temperature silenced GABAergic synapses onto dFSB neurons, thereby potentiating the wake-promoting dopamine transmission. We propose that temperature-dependent switching between these two synaptic transmission modalities may adaptively tune the neural property of dFSB neurons to temperature shifts and reorganize sleep architecture for the benefit of animal fitness.