1. We investigated the influence of visual experience upon vestibular compensation in monkeys. Two paradigms were used to elicit vestibular adaptation: artificially imposed motion of images upon the retina during head rotation and unilateral labyrinthectomy. Two groups of animals were investigated: monkeys that underwent a bilateral occipital lobectomy and intact monkeys without a cortical lesion. Occipital lobectomy alone caused only a minor change in the vestibuloocular reflex (VOR); the gain (eye vel/head vel) decreased slightly (10-15%) for high speeds of rotation (180-300°/s). 2. In response to a 4-h period of continuous oscillation of the head (0.25 Hz, 30°/s) with the visual scene made to move in phase with the head (0x viewing) or out of phase with the head (x2 viewing), intact monkeys showed an average 40% decrease or increase, respectively, of the VOR gain measured in darkness. After occipital lobectomy this adaptive capability was diminished, primarily for increasing the VOR gain after x2 viewing (42% preop to 13% postop). 3. Unilateral labyrinthectomy in either occipital-lobectomized or in otherwise intact monkeys led to a static imbalance with initial (18- to 20-h postlesion) values of spontaneous nystagmus of 22-62°/s measured in darkness and to a dynamic disturbance with an ~50% decrease of VOR gain. Compensation for both abnormalities was studied in three groups of animals: previously occipital-lobectomized monkeys kept in the light after labyrinthectomy, intact monkeys kept in the light after labyrinthectomy, and intact monkeys kept in the dark for 4 days after labyrinthectomy and then exposed to light. Spontaneous nystagmus disappeared at the same rate in each group of animals. VOR gain increased in the intact monkeys kept in the light after labyrinthectomy but not in the intact monkeys kept in the dark after labyrinthectomy until they were exposed to light. The occipital-lobectomized monkeys showed some recovery of VOR gain (~25-40%), but only at low speeds of rotation (30-60°/s). Occipital lobectomy performed in monkeys after they had already compensated for a labyrinthectomy caused the VOR gain to drop to values ~0.5 but without any recurrence of spontaneous nystagmus. 4. Our results indicate that visual experience after labyrinthectomy is essential for recovery of VOR gain but not for resolution of spontaneous nystagmus. Furthermore, geniculostriate pathways play a major role in providing information about high velocities of retinal image motion that is necessary for the acquisition of VOR gain adaptation. In addition the maintenance of VOR gain adaptation depends on the presence of the posterior cerebral hemispheres. Finally, the residual vestibular adaptive capabilities shown by occipital-lobectomized monkeys paralleled the degree to which the velocity-storage, slow buildup component of their optokinetic nystagmus (as reflected in optokinetic afternystagmus) was preserved. Both optokinetic afternystagmus and vestibular adaptation were best when the velocity of image motion on the retina was low.
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