Visual-vestibular interactions to maintain gaze stabilization

The vestibulo-ocular reflex (VOR) and vision act in conjunction to generate eye rotations to compensate for head movements and maintain gaze stability during locomotion. This research investigated the nature of this vestibulo-visual interaction. The first hypothesis tested was whether linear superposition of VOR and smooth-pursuit eye movements could account for the observed responses to head rotation. Subjects were rotated at 0.2--3.5 Hz while viewing stationary targets through a retinal image stabilization device that required eye movements to be twice as large as head rotation to maintain gaze stability. Even at 3.5 Hz, vision influenced the response because the gain of compensatory eye movements was greater while viewing through the device than while attempting to fixate the remembered location of the target in darkness. Further quantitative analysis showed that the linear superposition hypothesis was unable to predict the smooth-pursuit contribution to compensatory eye movements during head rotation at frequencies >2.0 Hz. Therefore, the next part of the project was to investigate nonlinear visual-vestibular interactions. The strategy used was to examine whether eye movements made in response to visual stimuli improved the gain of the VOR response to subsequent transient head rotations. The main observations were that if subjects viewed a stationary target prior to and during head rotation, the initial VOR gain was ∼0.8. However, if subjects made visually guided movements (smooth-pursuit, saccades or eye-head tracking) prior to head rotation, initial VOR gain was ∼1.0. This "priming" effect only occurred if the prior eye movement was in the same plane as the head rotation that followed. In conclusion, the visual contribution to the eye movements that compensate for high frequency or unpredictable head rotations, can be explained by an increase in the internal gain of the vestibular response by a previous, visually mediated gaze shift. A possible site for the "priming" is at the level of the velocity inputs to the neural integrator where gaze-shifting commands and vestibular signals converge.