1. We investigated cells in the middle temporal visual area (MT) and the medial superior temporal area (MST) that discharged during smooth pursuit of a dim target in an otherwise dark room. For each of these pursuit cells we determined whether the response during pursuit originated from visual stimulation of the retina by the pursuit target or from an extraretinal input related to the pursuit movement itself. We distinguished between these alternatives by removing the visual motion stimulus during pursuit either by blinking off the visual target briefly or by stabilizing the target on the retina. 2. In the foveal representation of MT (MTf), we found that pursuit cells usually decreased their rate of discharge during a blink or during stabilization of the visual target. The pursuit response of these cells depends on visual stimulation of the retina by the pursuit target. 3. In a dorsal-medial region of MST (MSTd), cells continued to respond during pursuit despite a blink or stabilization of the pursuit target. The pursuit response of these cells is dependent on an extraretinal input. 4. In a lateral-anterior region of MST (MST1), we found both types of pursuit cells; some, like those in MTf, were dependent on visual inputs whereas others, like those in MSTd, received an extraretinal input. 5. We observed a relationship between pursuit responses and passive visual responses. MST cells whose pursuit responses were attributable to extraretinal inputs tended to respond preferentially to large-field random-dot patterns. Some cells that preferred small spots also had an extraretinal input. 6. For 92% of the pursuit cells we studied, the pursuit response began after onset of the pursuit eye movement. A visual response preceding onset of the eye movement could be observed in many of these cells if the initial motion of the target occurred within the visual receptive field of the cell and in its preferred direction. In contrast to the pursuit response, however, this visual response was not dependent on execution of the pursuit movement. 7. For the remaining 8% of the pursuit cells, the pursuit discharge began before initiation of the pursuit eye movement. This occurred even though the initial motion of the target was outside the receptive field as mapped during fixation trials. Our data suggest, however, that such responses may be attributable to an expansion of the receptive field that accompanies enhanced visual responses.(ABSTRACT TRUNCATED AT 400 WORDS)