An Array of Descending Visual Interneurons Encoding Self-Motion in Drosophila

The means by which brains transform sensory information into coherent motor actions is poorly understood. In flies, a relatively small set of descending interneurons are responsible for conveying sensory information and higher-order commands from the brain to motor circuits in the ventral nerve cord. Here, we describe three pairs of genetically identified descending interneurons that integrate information from wide-field visual interneurons and project directly to motor centers controlling flight behavior. We measured the physiological responses of these three cells during flight and found that they respond maximally to visual movement corresponding to rotation around three distinct body axes. After characterizing the tuning properties of an array of nine putative upstream visual interneurons, we show that simple linear combinations of their outputs can predict the responses of the three descending cells. Last, we developed a machine vision-tracking system that allows us to monitor multiple motor systems simultaneously and found that each visual descending interneuron class is correlated with a discrete set of motor programs.