The interaction of visual, vestibular and extra-retinal mechanisms in the control of head and gaze during head-free pursuit

The ability to co-ordinate the eyes and head when tracking moving objects is important for survival. Tracking with eyes alone is controlled by both visually dependent and extra-retinal mechanisms, the latter sustaining eye movement during target extinction. We investigated how the extra-retinal component develops at the beginning of randomised responses during head-free pursuit and how it interacts with the vestibulo-ocular reflex (VOR). Subjects viewed horizontal step-ramp stimuli which occurred in pairs of identical velocity; velocity was randomised between pairs, ranging from ±5 to 40 deg s−1. In the first of each pair (short-ramp extinction) the target was visible for only 150 ms. In the second (initial extinction), after a randomised fixation period, the target was extinguished at motion onset, remaining invisible for 750 ms before reappearing for the last 200 ms of motion. Subjects used motion information acquired in the short-ramp extinction presentation to track the target from the start of unseen motion in the initial extinction presentation, using extra-retinal drive to generate smooth gaze and head movements scaled to target velocity. Gaze velocity rose more slowly than when visually driven, but had similar temporal development in head-free and head-fixed conditions. The difference in eye-in-head velocity between head-fixed and head-free conditions was closely related to head velocity throughout its trajectory, implying that extra-retinal drive was responsible for countermanding the VOR in the absence of vision. Thus, the VOR apparently remained active during head-free pursuit with near-unity gain. Evidence also emerged that head movements are not directly controlled by visual input, but by internal estimation mechanisms similar to those controlling gaze.