Adaptive modification of central vestibular neurons in response to visual stimulation through reversing prisms

Abstract

The response of vestibular nuclear neurons (Vn) to natural vestibular stimulation was recorded in alert cats that had undergone visual modification of their vestibulo-ocular reflex (VOR) through the use of visual reversing prisms. Forced rotation of the animals with visual input through the reversing prisms produced a reduction in gain of the VOR to about 1/3 of control value over about 4-5 h. As a comparative control, responses of additional Vn were recorded from the same cats and from similar anatomical locations, but with the animal possessing a normal VOR unmodified by the reversing prisms. Responses were recorded from presumed axon terminations of vestibular nuclear neurons within or closely adjacent to the abducens nucleus with the animals in both VOR behavioral states. By careful comparison of the population responses recorded from Vn in both VOR states, a number of conclusions about the possible neural changes underlying visual modification of the VOR were reached. Resting rates of Vn were not modified during VOR adaptation nor were the modulations of the whole population of Vn reduced to 1/3 of normal value to correspond to the change produced in VOR. Instead, a selective modification of a subset of Vn occurred. The modulations of high-gain type II neurons and lag type 1 neurons were significantly reduced. This change was accompanied by a drastic modification in the phases of the type II units from a population almost entirely in phase with contralateral head velocity in the normal animals to a population in which individual units showed phase leads or lags up to 90.degree. displaced from contralateral velocity in the lowered-gain VOR animals. The changes observed in type I neurons and Vn axons projecting to the abducens nucleus is in accord with the idea that adaptive changes in floccular Purkinje cells discharge, induced by visual input through the reversing prisms, lead to a decrease in the modulation of inhibitory Vn projecting to the abducens nuclei, and thus to a plastic change in VOR gain. The changes observed in type II neurons, especially the large modifications of phase, require additional assumptions about adaptive modification of floccular dynamics and/or specific projection of floccular Purkinje cell output to type II vestibular neurons or a new hypothesis that the adaptive changes occur outside the cerebellum.