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Animals rely on rapid sensorimotor processing to detect and respond to visual stimuli in their environment, yet how sensorimotor networks are organized to generate appropriate behaviors remains unclear. Here, we identify a bilateral pair of descending neurons (DNs), DNp03, as a hub for collision avoidance in flying flies. DNp03 receives visual information related to looming objects approaching on a collision course and connects directly and indirectly to motor neurons of the wings and neck, enabling the coordinated banked turn and head stabilization maneuvers of a rapid saccade. Although DNp03 can drive saccade-like behavior when optogenetically activated, naturalistic looming-evoked saccade behavior relies on a network of interconnected DNs that can partially compensate for DNp03 in its absence. The connectivity of this hierarchical network suggests DNp03 operates in parallel with two additional DN hubs that directly recruit subservient DNs to reinforce and expand behavioral outputs. We also find competition between the saccade network and descending pathways for landing behavior, where direct inhibitory connections from DNp03 reduce the likelihood a fly decides to land on, rather than turn away from, a looming object. Altogether, we provide a detailed mapping of one key sensorimotor pathway from visual inputs to motor outputs to demonstrate how even rapid, innate sensorimotor transformations rely on complex networks. These findings reveal intricate interconnectivity and hierarchy in descending pathways, a strategy that may represent a general principle of motor control across species. 

Abstract In most complex nervous systems there is a clear anatomical separation between the nerve cord, which contains most of the final motor outputs necessary for behaviour, and the brain. In insects, the neck connective is both a physical and information bottleneck connecting the brain and the ventral nerve cord (VNC, spinal cord analogue) and comprises diverse populations of descending (DN), ascending (AN) and sensory ascending neurons, which are crucial for sensorimotor signalling and control. Integrating three separate EM datasets, we now provide a complete connectomic description of the ascending and descending neurons of the female nervous system ofDrosophilaand compare them with neurons of the male nerve cord. Proofread neuronal reconstructions have been matched across hemispheres, datasets and sexes. Crucially, we have also matched 51% of DN cell types to light level data defining specific driver lines as well as classifying all ascending populations. We use these results to reveal the general architecture, tracts, neuropil innervation and connectivity of neck connective neurons. We observe connected chains of descending and ascending neurons spanning the neck, which may subserve motor sequences. We provide a complete description of sexually dimorphic DN and AN populations, with detailed analysis of circuits implicated in sex-related behaviours, including female ovipositor extrusion (DNp13), male courtship (DNa12/aSP22) and song production (AN hemilineage 08B). Our work represents the first EM-level circuit analyses spanning the entire central nervous system of an adult animal.