Signals used to compute errors in monkey vestibuloocular reflex: possible role of flocculus

Abstract

Adaptive changes were induced in the vestibuloocular reflex (VOR) of monkeys by oscillating them while they viewed the visual scene through optical devices (“spectacles”) that required changes in the amplitude of eye movement during head turns. The “gain” of the VOR (eye velocity divided by head velocity) during sinusoidal oscillation in darkness underwent gradual changes that were appropriate to reduce the motion of images on the retina during the adapting procedures. Bilateral ablation of the flocculus and ventral paraflocculus caused a complete and enduring loss of the ability to undergo adaptive changes in the VOR. Partial lesions caused a substantial but incomplete loss of the adaptive capability. We conclude that the flocculus is necessary for adaptive changes in the monkey's VOR. Further experiments in normal animals determined the types of stimuli that were necessary and/or sufficient to cause changes in VOR gain. Full-field visual stimulation was not necessary to induce adaptive changes in the VOR. Monkeys tracked a small spot in conditions that elicited the same combination of eye and head movements seen during passive oscillation with spectacles. The gain of the VOR showed changes 50-70% as large as those produced by the same duration of oscillation with spectacles. Since the effective tracking conditions cause a consistent correlation of floccular output with vestibular inputs, these data are compatible with our previous suggestion that the flocculus may provide signals used by the central nervous system to compute errors in the gain of the VOR. Prolonged sinusoidal optokinetic stimulation with the head stationary caused only a slight increase in VOR gain. Left-right reversal of vision and eye movement during sinusoidal vestibular oscillation caused decreases in VOR gain. In rabbits, both of these stimulus conditions produced large increases in the gain of the VOR, which implied that eye velocity signals were used instead of vestibular inputs to compute errors in the VOR. Our different results argue that vestibular signals are necessary for computing errors in VOR gain in the monkey. The species difference may reflect the additional role that smooth pursuit eye movements play in stabilizing gaze during head turns in monkeys.