Like the mammalian visual cortex, the fly visual system is organized into retinotopic columns. A widely accepted biophysical model for computing visual motion, the elementary motion detector proposed nearly 50 years ago posits a temporal correlation of spatially separated visual inputs implemented across neighboring retinotopic visual columns. Whereas the inputs are defined, the neural substrate for motion computation remains enigmatic. Indeed, it is not known where in the visual processing hierarchy the computation occurs. Here, we combine genetic manipulations with a novel high-throughput dynamic behavioral analysis system to dissect visual circuits required for directional optomotor responses. An enhancer trap screen of synapse-inactivated neural circuits revealed one particularly striking phenotype, which is completely insensitive to motion yet displays fully intact fast phototaxis, indicating that these animals are generally capable of seeing and walking but are unable to respond to motion stimuli. The enhancer circuit is localized within the first optic relay and strongly labels the only columnar interneuron known to interact with neighboring columns both in the lamina and medulla, spatial synaptic interactions that correspond with the two dominant axes of elementary motion detectors on the retinal lattice.