Peripheral visual circuits perform paradigmatic computations such as motion processing. However, our understanding of the necessary and sufficient roles of individual cell types, their interactions, and the molecules that underpin their specific activity patterns remains limited. Our work combines genetic manipulations of both neural activity and molecular function with in vivo imaging of calcium and voltage signals to unravel circuit mechanisms using the Drosophila visual system as a model. Our results reveal that the algorithms used to detect visual motion in flies and humans are fundamentally similar.