Three-dimensional vestibuloocular reflex of the monkey: Optimal retinal image stabilization versus Listing's law

If the rotational vestibuloocular reflex (VOR) were to achieve optimal reti nal image stabilization during head rotations in three-dimensional space, i t must turn the eye around the same axis as the head, with equal velocity b ut in the opposite direction. This optimal VOR strategy implies that the po sition of the eye in the orbit must not affect the VOR. However, if the VOR were to follow Listing's law, then the slow-phase eye rotation axis should tilt as a function of current eye position. We trained animals to fixate v isual targets placed straight ahead or 20 degrees up, down, left or right w hile being oscillated in yaw, pitch, and roll at 0.5-4 Hz, either with or w ithout a full-field visual background. Our main result was that the visuall y assisted VOR of normal monkeys invariantly rotated the eye around the sam e axis as the head during yaw, pitch, and roll (optimal VOR). In the absenc e of a visual background, eccentric eye positions evoked small axis tilts o f slow phases in normal animals. Under the same visual condition, a promine nt effect of eye position was found during roll but not during pitch or yaw in animals with low torsional and vertical gains following plugging of the vertical semicircular canals. This result was in accordance with a model i ncorporating a specific compromise between an optimal VOR and a VOR that pe rfectly obeys Listing's law. We conclude that the visually assisted VOR of the normal monkey optimally stabilizes foveal as well as peripheral retinal images. The finding of optimal VOR performance challenges a dominant role of plant mechanics and supports the notion of noncommutative operations in the oculomotor control system.