Supplementation of the Human Vestibulo-Ocular Reflex by Visual Fixation and Smooth Pursuit

In studies over the past 30 years, D.A. Robinson and colleagues established that the dynamic characteristics of smooth pursuit eye movements (SP) are different at the onset from those at the cessation of the response. They proposed that cessation of SP was due to a separate fixation system. During head movements, both fixation and SP may contribute to gaze stabilization. We investigated the relative contributions of fixation and SP to the “visually enhanced” vestibulo-ocular reflex (VVOR) using a paradigm requiring a transition from VVOR to combined eye-head tracking (CEHT). We found, in four normal subjects, that ringing typical of SP generally did not occur during VVOR, but that it often appeared after the transition to CEHT. The findings were different in two patients with absent peripheral vestibular function; ringing typical of SP occurred always during VVOR but disappeared during the onset of CEHT. These results can be explained by a model in which an internal representation of target velocity serves as input to parallel SP and fixation systems, and as the determinant of which of the two systems will provide the command signal. Interpretation of our data using this model indicates that either fixation or SP systems may “visually enhance” the VOR, depending on the magnitude of retinal error velocity that remains after vestibular eye movements have been generated.