1. To determine the potential role of the primate accessory optic system (AOS) in optokinetic and smooth-pursuit eye movements, we recorded the activity of 110 single units in a subdivision of the AOS, the lateral terminal nucleus (LTN), in five alert rhesus macaques. All monkeys were trained to fixate a stationary target spot during visual testing and to track a small spot moving in a variety of visual environments. 2. LTN units formed a continuum of types ranging from purely visual to purely oculomotor. Visual units (50%) responded best for large-field (70 x 50 degrees), moving visual stimuli and had no response associated with smooth-pursuit eye movement; some responded during smooth pursuit in the dark, but the response disappeared if the target was briefly extinguished, indicating that their smooth-pursuit-related response reflected activation of a parafoveal receptive field. Eye movement and visual units (36%) responded both for large, moving visual stimuli and during smooth-pursuit eye movements made in the dark. Eye movement units (14%) discharged during smooth-pursuit or other eye movements but showed no evidence of visual sensitivity. 3. Essentially all (98%) LTN units were direction selective, responding preferentially during vertical background and/or smooth-pursuit movement. The vast majority (88%) preferred upward background and/or eye movement. During periodic movement of the large-field visual background while the animal fixated, their firing rates were modulated above and below rather high resting rates. Although LTN units typically responded best to movement of large-field stimuli, some also responded well to small moving stimuli (0.25 degrees diam). 4. LTN units could be separated into two populations according to their dependence on visual stimulus velocity. For periodic triangle wave stimuli, both types had velocity thresholds less than 3 degrees/s. As stimulus velocity increased above threshold, the activity of one type reached peak firing rates over a very narrow velocity range and remained nearly at peak firing for velocities from approximately 4-80 degrees/s. The firing rates of the other type exhibited velocity tuning in which the firing rate peaked at an average preferred velocity of 13 degrees/s and decreased for higher velocities. 5. A close examination of firing rates to sinusoidal background stimuli revealed that both unit types exhibited unusual behaviors at the extremes of stimulus velocity.(ABSTRACT TRUNCATED AT 400 WORDS)