Insect asynchronous flight is one of the most prevalent forms of animal locomotion used by more than 600,000 species. Despite profound insights into the motor patterns1, biomechanics2,3 and aerodynamics underlying asynchronous flight4,5, the architecture and function of the central-pattern-generating (CPG) neural network remain unclear. Here, on the basis of an experiment–theory approach including electrophysiology, optophysiology, Drosophila genetics and mathematical modelling, we identify a miniaturized circuit solution with unexpected properties. The CPG network consists of motoneurons interconnected by electrical synapses that, in contrast to doctrine, produce network activity splayed out in time instead of synchronized across neurons. Experimental and mathematical evidence support a generic mechanism for network desynchronization that relies on weak electrical synapses and specific excitability dynamics of the coupled neurons. In small networks, electrical synapses can synchronize or desynchronize network activity, depending on the neuron-intrinsic dynamics and ion channel composition. In the asynchronous flight CPG, this mechanism translates unpatterned premotor input into stereotyped neuronal firing with fixed sequences of cell activation that ensure stable wingbeat power and, as we show, is conserved across multiple species. Our findings prove a wider functional versatility of electrical synapses in the dynamic control of neural circuits and highlight the relevance of detecting electrical synapses in connectomics.
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.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
10624 S. Eastern Ave., Ste. A-614
Henderson, NV 89052, USA
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.