Topographic and directional organization of visual motion inputs for the initiation of horizontal and vertical smooth-pursuit eye movements in monkeys.

1. The goal of our study was to determine the properties of the visual inputs for pursuit eye movements. In a previous study we presented horizontal target motion along the horizontal meridian and showed that targets were more effective if they moved across the center of the visual field. We have now analyzed the topographic weighting of the inputs for pursuit in greater detail, using targets that moved in all directions and across a wide area of the visual field. 2. Monkeys were rewarded for tracking targets that started at 48 positions in the visual field. The initial positions were spaced equally around 4 circles that were centered at the position of fixation and had radii of 3, 6, 9, and 12 degrees. Targets moved horizontally or vertically at 30 degrees/s. We measured the smooth eye acceleration in the first 80 ms after the initiation of pursuit, before there had been time for visual feedback to affect the position or velocity of the retinal images from the target. 3. For both horizontal and vertical target motion, there were major differences between the early and late intervals in the first 80 ms of pursuit. In the first 20 ms eye acceleration was largely independent of initial target position. In later intervals eye acceleration decreased sharply as a function of initial target eccentricity. The later intervals also showed a pronounced toward/away asymmetry such that the initiation of pursuit was more vigorous for target motion toward than for motion away from the horizontal or vertical meridian. 4. Comparison of the topographic organization of the middle temporal visual area (MT) with our data on pursuit suggests that the topography of cortical maps is smoothed when the visual signals are transmitted to the pursuit system. For example, the superior visual hemifield is underrepresented in cortical motion processing areas, but target motion in the superior and inferior visual hemifields is equally effective for the initiation of pursuit. 5. We investigated the directional organization of the visual inputs for pursuit by presenting targets that started at 6 degrees eccentric and moved in 16 different directions. Horizontal target motion always evoked larger eye accelerations than did vertical target motion. Target motion in oblique directions evoked intermediate values of eye acceleration. 6. Our data show two classes of variation in pursuit performance. First, some subjects showed ideosyncratic variations that were restricted to one hemifield or one direction of target motion. We attribute these variations to differences among subjects in the physiology of visual pathways.(ABSTRACT TRUNCATED AT 400 WORDS)