Three-dimensional ocular kinematics during eccentric rotations: evidence for functional rather than mechanical constraints

Previous studies have reported that the translational vestibuloocular reflex (TVOR) follows a three-dimensional (3D) kinematic behavior that is more similar to visually guided eye movements, like pursuit, rather than the rotational VOR (RVOR). Accordingly, TVOR rotation axes tilted with eye position toward an eye-fixed reference frame rather than staying relatively fixed in the head like in the RVOR. This difference arises because, contrary to the RVOR where peripheral image stability is functionally important, the TVOR like pursuit and saccades cares to stabilize images on the fovea. During most natural head and body movements, both VORs are simultaneously activated. In the present study, we have investigated in rhesus monkeys the 3D kinematics of the combined VOR during yaw rotation about eccentric axes. The experiments were motivated by and quantitatively compared with the predictions of two distinct hypotheses. According to the first (fixed-rule) hypothesis, an eye-position-dependent torsion is computed downstream of a site for RVOR/TVOR convergence, and the combined VOR axis would tilt through an angle that is proportional to gaze angle and independent of the relative RVOR/TVOR contributions to the total eye movement. This hypothesis would be consistent with the recently postulated mechanical constraints imposed by extraocular muscle pulleys. According to the second (image-stabilization) hypothesis, an eye-position-dependent torsion is computed separately for the RVOR and the TVOR components, implying a processing that takes place upstream of a site for RVOR/TVOR convergence. The latter hypothesis is based on the functional requirement that the 3D kinematics of the combined VOR should be governed by the need to keep images stable on the fovea with slip on the peripheral retina being dependent on the different functional goals of the two VORs. In contrast to the fixed-rule hypothesis, the data demonstrated a variable eye-position-dependent torsion for the combined VOR that was different for synergistic versus antagonistic RVOR/TVOR interactions. Furthermore, not only were the eye-velocity tilt slopes of the combined VOR as much as 10 times larger than what would be expected based on extraocular muscle pulley location, but also eye velocity during antagonistic RVOR/TVOR combinations often tilted opposite to gaze. These results are qualitatively and quantitatively consistent with the image-stabilization hypothesis, suggesting that the eye-position-dependent torsion is computed separately for the RVOR and the TVOR and that the 3D kinematics of the combined VOR are dependent on functional rather than mechanical constraints.