Visual contribution to the high-frequency human angular vestibulo-ocular reflex

Abstract

The vestibulo-ocular reflex (VOR) acts to maintain images stable on the retina by rotating the eyes in exactly the opposite direction, but with equal magnitude, to head velocity. When viewing a near target, this reflex has an increased response to compensate for the translation of the eyes relative to the target that acts to reduce retinal image slip. Previous studies have shown that retinal velocity error provides an important visual feedback signal to increase the low-frequency (<1 Hz) VOR response during near viewing. We sought to determine whether initial eye position and retinal image position error could provide enough information to substantially increase the high-frequency VOR gain (eye velocity/head velocity) during near viewing. Ten human subjects were tested using the scleral search coil technique during horizontal head impulses under different lighting conditions (constant dark, strobe light at 0.5, 1, 2, 4, 10, 15 Hz, constant light) while viewing near (9.5 ± 1.3 cm) and far (104 cm) targets. Our results showed that the VOR gain increased during near viewing compared to far viewing, even during constant dark. For the near target, there was an increase in VOR gain with increasing strobe frequency from 1.17 ± 0.17 in constant dark to 1.36 ± 0.27 in constant light, a 21 ± 9 % increase. For the far target, strobe frequency had no effect. Presentation order of strobe frequency (i.e. 0.5-15 vs. 15-0.5 Hz) did not affect the gain, but it did affect the vergence angle (angle between the two eye's lines of sight). The VOR gain and vergence angles were constant during each trial. Our findings show that a retinal position error signal helps increase the vergence angle and could be invoking vestibular adaptation mechanisms to increase the high-frequency VOR response during near viewing. This is in contrast to the low-frequency VOR that depends more on retinal velocity error and predictive adaptation mechanisms.