INTRODUCTION Fundamental circuit features of the mouse visual system emerge before the onset of vision, allowing the mouse to perceive objects and detect visual motion immediately upon eye opening. How the mouse visual system achieves self-organization by the time of eye opening without structured external sensory input is not well understood. In the absence of sensory drive, the developing retina generates spontaneous activity in the form of propagating waves. Past work has shown that spontaneous retinal waves provide the correlated activity necessary to refine the development of gross topographic maps in downstream visual areas, such as retinotopy and eye-specific segregation, but it is unclear whether waves also convey information that instructs the development of higher-order visual response properties, such as direction selectivity, at eye opening. RATIONALE Spontaneous retinal waves exhibit stereotyped changing spatiotemporal patterns throughout development. To characterize the spatiotemporal properties of waves during development, we used one-photon wide-field calcium imaging of retinal axons projecting to the superior colliculus in awake neonatal mice. We identified a consistent propagation bias that occurred during a transient developmental window shortly before eye opening. Using quantitative analysis, we investigated whether the directionally biased retinal waves conveyed ethological information relevant to future visual inputs. To understand the origin of directional retinal waves, we used pharmacological, optogenetic, and genetic strategies to identify the retinal circuitry underlying the propagation bias. Finally, to evaluate the role of directional retinal waves in visual system development, we used pharmacological and genetic strategies to chronically manipulate wave directionality and used two-photon calcium imaging to measure responses to visual motion in the midbrain superior colliculus immediately after eye opening. RESULTS We found that spontaneous retinal waves in mice exhibit a distinct propagation bias in the temporal-to-nasal direction during a transient window of development (postnatal day 8 to day 11). The spatial geometry of directional wave flow aligns strongly with the optic flow pattern generated by forward self-motion, a dominant natural optic flow pattern after eye opening. We identified an intrinsic asymmetry in the retinal circuit that enforced the wave propagation bias involving the same circuit elements necessary for motion detection in the adult retina, specifically asymmetric inhibition from starburst amacrine cells through γ-aminobutyric acid type A (GABA A ) receptors. Finally, manipulation of directional retinal waves, through either the chronic delivery of gabazine to block GABAergic inhibition or the starburst amacrine cell–specific mutation of the FRMD7 gene, impaired the development of responses to visual motion in superior colliculus neurons downstream of the retina. CONCLUSION Our results show that spontaneous activity in the developing retina prior to vision onset is structured to convey essential information for the development of visual response properties before the onset of visual experience. Spontaneous retinal waves simulate future optic flow patterns produced by forward motion through space, due to an asymmetric retinal circuit that has an evolutionarily conserved link with motion detection circuitry in the mature retina. Furthermore, the ethologically relevant information relayed by directional retinal waves enhances the development of higher-order visual function in the downstream visual system prior to eye opening. These findings provide insight into the activity-dependent mechanisms that regulate the self-organization of brain circuits before sensory experience begins.