1. We have investigated the inhibitory mechanisms modulating the extracellularly recorded responses of ON-OFF directionally selective (DS) ganglion cells of the rabbit retina. Our investigations used both moving spots and apparent motion. The latter was produced by both prolonged light steps, which simulate movement of an edge, and light flashes, which simulate movement of a spot or slit. 2. Within the excitatory receptive-field center of DS ganglion cells, apparent motion with prolonged light steps elicits null-direction inhibition whose strength rises to 90% of maximum in 160 ± 110 ms (7 cells) and then decays slowly, remaining above baseline longer than 2,000 ms for short interslit distances. 3. Prolonged light steps are generally effective for inhibiting any given excitatory receptive-field locus from an ovate-shaped area that extends asymmetrically in the direction that would be previously traversed by null-direction moving objects. This inhibitory area is typically larger than one-half the size of the receptive- field center. The strength of the inhibition is greater at short than long distances within this area. 4. The rise and fall times of the null-direction inhibition elicited by apparent motion using prolonged light steps are somewhat faster at large than short interslit distances. 5. Short light flashes (at sufficiently long interslit delays) elicit inhibition not only from the same asymmetric, ovate-shaped inhibitory field as long steps of light, but also from loci completely surrounding the second slit. This implies that the asymmetric, null-direction-specific inhibition is due to a temporally sustained mechanism. The symmetric inhibition elicited by short flashes may be due to the presence of the antagonistic surround mechanism within the receptive-field center. The apparent absence of this surround inhibition for preferred-direction apparent motion during prolonged light steps may be due to masking by facilitation that is strongly evoked by long steps, but not flashes of light (see accompanying paper). 6. The relatively slow rise time and sustained time course of the inhibition elicited by null- direction apparent motion within the excitatory receptive field center appears to distinguish it from the inhibition elicited by stimulation within the receptive field surround, which has a much faster rise time and more transient time course. However, the sustained, null-direction inhibitory mechanism that can be elicited by prolonged light steps within the excitatory receptive field center extends into the surround on the side of the receptive-field center previously traversed during null-direction motion. 7. The contrast dependency of both the null-direction and the surround inhibition is division-like, rather than subtraction-like. That is, the effect of both types of inhibition is to divide the response-versus-contrast curves by a constant factor rather than to subtract a fixed value. 8. Use of prolonged light steps shows that the interaction between excitation and null- direction inhibition is largely segregated between the ON and the OFF pathways. Thus, for null-direction apparent motion, light onset of the first slit strongly inhibits response to the onset, but generally not the offset, of the second slit. Light offset of the first slit similarly tends to inhibit the response to light offset, but not onset, of the second slit. Thus selectivity for direction of motion appears to be computed independently for light and dark regions of moving objects.