Gap junctions desynchronize a neural circuit to stabilize insect flight

Abstract

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.

Qualitative switches in single-neuron spike dynamics on neuromorphic hardware: implementation, impact on network synchronization and relevance for plasticity

“…Spike statistics of a small network of all-to-all coupled neurons consequently differ depending on single-neuron dynamics. We showcase this by implementing a CPG network of four neurons that exhibit the same changes in network synchrony upon the alteration of V reset as the Drosophila wing motor circuit [12] (figure 1) shows upon genetic manipulations of intrinsic neuron parameters.…”

“…The mechanism of desynchronizing small networks via neurons that operate close to the SNL point is potentially shared across many flying insects [12] and provides an interesting example how cellular properties (and not just network connectivity) shape network and, consequently, animal behaviour. In terms of neuromorphic applications, such a small and resource-efficient biological CPG can serve as a role model for robotic locomotion control.…”

“…Firstly, the synapses on the chip are implementations of an exponential synapse model, mimicking the action of very fast chemical synapses. In the biological fly circuit, the neurons are instead coupled via gap junctions [12], which are ion channels spanning the membranes of two neurons to form a direct electrical conductance between them. In principle, gap junction coupling on the BrainScaleS-2 chip can be emulated via the available resistance linking originally designed for emulating multi-compartment neurons.…”

“…To demonstrate this, we draw inspiration from a small CPG network in the Drosophila wing motor system. In this system, neuron-intrinsic properties have recently been shown to be crucial to the network synchronization state that allows the animal to fly stably [12]. Specifically, the neurons in this network innervate the muscle that is responsible for the wing down-stroke and thus control the frequency of the wingbeat.…”

“…These periods produce high and low wingbeat frequencies respectively, and thus result in less stable flight (figure 1, left). Recently, it has been shown that the mechanism that generates the splayed-out state for stable flight relies on a particular spike-generating dynamics [12]. When the properties of the cell membrane were genetically manipulated to change the spiking dynamics, in-phase synchrony (i.e.…”