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, biomechanics^2,3 and aerodynamics underlying asynchronous flight^4,5, 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.

昆虫不同步飞行是最普遍的动物运动形式之一，被超过 600,000 种动物使用。尽管对异步飞行背后的运动模式¹、生物力学^2,3和空气动力学^4,5有深刻的见解，但中央模式生成 (CPG) 神经网络的架构和功能仍不清楚。在此，基于包括电生理学、光生理学、果蝇属在内的实验-理论方法通过遗传学和数学建模，我们确定了具有意想不到特性的微型电路解决方案。CPG 网络由通过电突触互连的运动神经元组成，与学说相反，电突触产生的网络活动会及时展开，而不是跨神经元同步。实验和数学证据支持网络去同步化的通用机制，该机制依赖于耦合神经元的弱电突触和特定兴奋性动力学。在小型网络中，电突触可以同步或去同步网络活动，具体取决于神经元内在动力学和离子通道组成。在异步飞行 CPG 中，这种机制将无模式的前运动输入转化为具有固定细胞激活序列的刻板神经元放电，确保稳定的翼拍功率，正如我们所展示的，在多个物种中是保守的。我们的研究结果证明了电突触在神经回路动态控制中具有更广泛的功能多样性，并强调了在连接组学中检测电突触的相关性。