When we make hand movements to visual targets, gaze usually leads hand position by a series of saccades to task-relevant locations. Recent research suggests that the slow smooth pursuit eye movement system may interact with the saccadic system in complex tasks, suggesting that the smooth pursuit system can receive non-retinal input. We hypothesise that a combination of saccades and smooth pursuit guides the hand movements towards a goal in a complex environment, using an internal representation of future trajectories as input to the visuomotor system. This would imply that smooth pursuit leads hand position, which is remarkable, as the general idea is that smooth pursuit is driven by retinal slip. To test this hypothesis, we designed a video-game task in which human subjects used their thumbs to move two cursors to a common goal position while avoiding stationary obstacles. We found that gaze led the cursors by a series of saccades interleaved with ocular fixation or pursuit. Smooth pursuit was correlated with neither cursor position nor cursor velocity. We conclude that a combination of fast and slow eye movements, driven by an internal goal instead of a retinal goal, led the cursor movements, and that both saccades and pursuit are driven by an internal representation of future trajectories of the hand. The lead distance of gaze relative to the hand may reflect a compromise between exploring future hand (cursor) paths and verifying that the cursors move along the desired paths.
We demonstrated that in a natural task involving hand-eye coordination gaze leads hand position by saccades interleaved with ocular fixation or pursuit. Quite remarkably, pursuit is not only driven by retinal slip, but also by an internal goal which may reflect a compromise between exploring a future path and verifying that the hands move along the desired path. This indicates that pursuit is much more flexible than previously thought and shows a clear functional role for such flexibility.