Inferring the direction of image motion is a fundamental component of visual computation and essential for visually guided behavior. In the retina, the direction of image motion is computed in four cardinal directions, but it is not known at which circuit location along the flow of visual information the cardinal direction selectivity first appears. We recorded the concerted activity of the neuronal circuit elements of single direction-selective (DS) retinal ganglion cells at subcellular resolution by combining GCaMP3-functionalized transsynaptic viral tracing and two-photon imaging. While the visually evoked activity of the dendritic segments of the DS cells were direction selective, direction-selective activity was absent in the axon terminals of bipolar cells. Furthermore, the glutamate input to DS cells, recorded using a genetically encoded glutamate sensor, also lacked direction selectivity. Therefore, the first stage in which extraction of a cardinal motion direction occurs is the dendrites of DS cells. •Dendritic segments of ON direction-selective cells are direction selective•Type-5 bipolar cells are connected to ON direction-selective cells•Activity of bipolar cell axon terminals is not selective for motion direction•Concerted activity within the circuit of a single ON direction-selective cell Yonehara et al. record the concerted activity of the circuit elements of single direction-selective retinal ganglion cells at subcellular resolution. The first stage in which extraction of a cardinal motion direction occurs is the dendrites of the ganglion cell.