Insect asynchronous flight requires neural circuit de-synchronization by electrical synapses

Abstract

Despite profound mechanistic insight into motor pattern generation, for asynchronous insect flight - the most prevalent form of flight employed by >600.000 species - architecture and function of the underlying central pattern generating (CPG) neural network remain elusive. Combining electro- and optophysiology, Drosophila genetics, and mathematical modelling, we uncover a miniaturized circuit solution of motoneurons interconnected by electrical synapses that, contrary to doctrine, serve to de-synchronize network activity. This minimal gap-junctional motoneuron network suffices to translate unpatterned premotor input into stereotyped firing sequences which are conserved across species and generate stable wingbeat power. Mechanistically, network de-synchronization requires weak electrical coupling in conjunction with specific postsynaptic excitability dynamics, revealing an unexpected, generic feature in the control of neural circuit dynamics by electrical synapses. One Sentence SummaryElectrical synapses de-synchronize neural network firing to enable stable wingbeat power during insect flight.