ABSTRACTChanges in dendritic morphology in response to activity have long been thought to be a critical component of how neural circuits develop to properly encode sensory information. Here we report the impact of dark-rearing on the dendritic morphology and function of a retinal ganglion cell type, a ventral-preferring direction-selective ganglion cell (vDSGC). vDSGCs have asymmetric dendrites oriented along their preferred direction. We found that, at eye opening, vDSGC dendrites are not yet ventrally oriented, and that, surprisingly, dark-rearing prevents ventral orientation of vDSGC dendrites. Despite their dramatic change in dendritic morphology, vDSGCs in dark-reared mice maintain ventral directional preference. Direction selective tuning in dark-reared mice is mediated by asymmetric inhibition, as observed in vDSGCs of normally reared animals. Hence, we postulate that dendritic form follows proper circuit function, where dendritic orientation is refined over the course of development and is dependent on structured visual experience following eye opening.