Foveal versus full-field visual stabilization strategies for translational and rotational head movements

Because we view the world from a constantly shifting platform when our head and body move in space, vestibular and visuomotor reflexes are critical to maintain visual acuity. In contrast to the phylogenetically old rotational vestibulo-ocular reflex (RVOR), it has been proposed that the translational vestibulo-ocular reflex (TVOR) represents a newly developed vestibular-driven mechanism that is important for foveal vision and stereopsis. To investigate the hypothesis that the function of the TVOR is indeed related to foveal (as opposed to full-field) image stabilization, we compared the three-dimensional ocular kinematics during lateral translation and rotational movements with those during pursuit of a small moving target in four rhesus monkeys. Specifically, we tested whether TVOR rotation axes tilt with eye position as in visually driven systems such as pursuit, or whether they stay relatively fixed in the head as in the RVOR. We found a significant dependence of three-dimensional eye velocity on eye position that was independent of viewing distance and viewing conditions (full-field, single target, or complete darkness). The slopes for this eye-position dependence averaged 0.7 +/- 0.07 for the TVOR, compared with 0.6 +/- 0.07 for visually guided pursuit eye movements and 0.18 +/- 0.09 for the RVOR. Because the torsional tilt versus vertical gaze slopes during translation were slightly higher than those during pursuit, three-dimensional eye movements during translation could partly reflect a compromise between the two different solutions for foveal gaze control, that of Listing's law and minimum velocity strategies. These results with respect to three-dimensional kinematics provide additional support for a functional difference in the two vestibular-driven mechanisms for visual stability during rotations and translations and establish clearly the functional goal of the TVOR as that for foveal visual acuity.