In the mouse retina, there are two distinct groups of direction-selective ganglion cells, ON and ON–OFF, that detect movement of visual images. To understand the roles of these cells in controlling eye movements, we studied the optokinetic responses (OKRs) of mutant mice with dysfunctional ON-bipolar cells that have a functional obstruction of transmission to ON direction-selective ganglion cells. Experiments were carried out to examine the initial and late phases of OKRs. The initial phase was examined by measurement of eye velocity using stimuli of sinusoidal grating patterns of various spatiotemporal frequencies that moved for 0.5 s. The mutant mice showed significant initial OKRs, although the range of spatiotemporal frequencies that elicited these OKRs was limited and the response magnitude was weaker than that in wild-type mice. To examine the late phase of the OKRs, the same visual patterns were moved for 30 s to induce alternating slow and quick eye movements (optokinetic nystagmus) and the slow-phase eye velocity was measured. Wild-type mice showed significant late OKRs with a stimulus in an appropriate range of spatiotemporal frequencies (0.0625–0.25 cycles/°, 0.75–3.0 Hz, 3–48°/s), but mutant mice did not show late OKRs in response to the same visual stimuli. The results suggest that two groups of direction-selective ganglion cells play different roles in OKRs: ON direction-selective ganglion cells contribute to both initial and late OKRs, whereas ON–OFF direction-selective ganglion cells contribute to OKRs only transiently.