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

Abstract

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.

Fig. 1.

Geometrical expectations based on different strategies for image stabilization. A, For FF image stabilization (FF strategy), the axis of rotation of the eye [shown as the arrow indicating eye velocity (EV)] should always remain head-fixed (e.g., head horizontal) and be independent of the direction of gaze.B, For foveal image stabilization, the axis of rotation of the eye is not anchored to the head. According to the LL strategy, the axis of rotation of the eye is neither head-fixed nor eye-fixed, but rather rotates in the same direction of gaze through one-half the angle of gaze (θ/2; half-angle rule). According to the MR strategy, the axis of rotation of the eye remains eye-fixed (i.e., rotates in the same direction and through the same angle as gaze, θ; full-angle rule). Dotted lines represent the head vertical and horizontal directions.

Fig. 2.

Dependence of smooth pursuit and ocular responses during translation on vertical gaze. From top tobottom, Three-dimensional eye position (E_tor,E_ver, andE_hor) and angular velocity (Ω_tor, Ω_ver, Ω_hor) for up, center, and down gaze during 0.5 Hz (± 3°) pursuit and 4 Hz (± 0.25 gm) lateral translation (distance of 32 cm). Tg, Target on and off; H, head motion acceleration. Fast phases have been eliminated.

Fig. 3.

A, Calculated torsional tilt angles of eye velocity as a function of vertical gaze during pursuit, translation, and rotation as the animal followed a target at a distance of 18 cm. Solid lines represent linear regressions;dotted lines illustrate the full- and half-angle rules of three-dimensional kinematics. B, The torsional eye velocity tilt versus vertical gaze angle slopes for the TVOR (solid symbols) and RVOR (open symbols) from four animals (6 eyes) at different viewing distances.Dotted lines illustrate the unity-slope line (diagonal).C, The corresponding zero-intercepts for the TVOR regressions plotted versus the corresponding values for pursuit. Other than the farthest distance (squares), data fall along the unity (dotted) line.