Visual vestibular interaction: vestibulo-ocular reflex suppression with head-fixed target fixation

Abstract

In order to maintain clear vision, the images on the retina must remain reasonably stable. Head movements are generally dealt with successfully by counterrotation of the eyes induced by the combined actions of the vestibulo-ocular reflex (VOR) and the opto-kinetic reflex. We have studied how, in humans, the VOR gain (VORG) is modulated to provide appropriate eye movements in two situations: 1. fixation of a stationary object of the visual space while the head moves. This requires a visuo-vestibulo-ocular reaction to induce eye movements opposite in direction, and equal in velocity to head movements, and 2. fixation of an object moving with the head. Here, the visuo-vestibulo-ocular reaction should be totally suppressed. These two situations were compared to a basic condition in which, to induce "pure" VOR, the subjects (Ss) in darkness were not allowed a visual target. Eye movements were recorded in seated Ss during constant amplitude sinusoidal and pulse-like passive rotations applied around the vertical axis. Subjects were in total darkness (DARK condition) and performing mental arithmetic. Alternatively, they were provided with a small target, either stationary with respect to earth (earth-fixed target: EFT), or moving with them (chair-fixed-target: CFT). The sinusoidal rotation experiment was used as baseline for the ensuing experiments and yielded control data in agreement with the literature. In particular, rotation in the dark showed a VORG of 0.6. With, for example, 0.8 s passive pulse rotations, typical responses in all three visual conditions were rigorously identical during the first 150 to 180 ms. They showed a delay of about 16 ms of the eye behind the head with no significant difference between passive whole-body and passive head-alone rotations. In all conditions, once the eyes had started to move, a rapid increase in eye velocity was observed during 75 to 80 ms, after which, the average VORG was 0.9 +/- 0.15. During the following 50 to 100 ms, the gain remained around 0.9 in all three conditions. Beyond 180 ms, the VORG remained around 0.9 in DARK, increased slowly towards 1 or decreased towards zero in the EFT and CFT conditions, respectively. The time-course of these later events suggests that visual tracking mechanisms came into play to reduce retinal slip through smooth pursuit. Sinusoidal rotations, extensively used in VOR studies, do not seem to be a satisfactory stimulus to rapidly and precisely characterize VOR function, particularly in pathological cases. Our data suggest that rapid transient rotations are more appropriate.