Visual information in the retina is processed via two pathways: ON and OFF pathways that originate from ON and OFF bipolar cells. The differences in the receptors that mediate signal transmission from photoreceptors imply that the response speed to light signals differs between ON and OFF pathways. We studied the initial optokinetic responses (OKRs) of mice using two-frame motion stimuli presented with interstimulus intervals (ISIs) to understand functional difference of these pathways. When two successive image frames were presented with an ISI, observers often perceived motion in the opposite direction of the actual shift. This directional reversal results from the biphasic nature of the temporal filters in visual systems whose characteristics can be estimated from the dependence on ISIs. We examined the dependence on ISIs in the OKRs of TRPM1-/- mice, whose ON bipolar cells are dysfunctional, as well as in those of wild-type control mice. Wild type and TRPM1-/- mice showed comparable OKRs in the veridical direction when no ISI was present. Both types of mice showed OKRs that decreased and eventually reversed as the ISI increased, but with a directional reversal at a shorter ISI in TRPM1-/- than wild-type mice. In addition, the temporal filters of TRPM1-/- mice estimated from dependence on ISIs were tuned for higher frequencies, suggesting that compared with wild-type mice, the visual system of TRPM1-/- mice responds to light signals with faster dynamics. We conclude that the ON and OFF pathways contribute to initial OKRs by providing visual signals processed with different temporal resolutions.