Short- and long-term modifications of vestibulo-ocular response dynamics following unilateral vestibular nerve lesions in the cat

Abstract

The dynamics of the horizontal vestibuloocular reflex (VOR) were determined in the dark prior to and at various time periods after unilateral removal of the vestibular nerve. One chronic group, consisting of cats that were operated at the age of 6 weeks or as adults, was studied 10.5 to 22 months later; an adult-operated group was measured 1–244 days postoperatively (p.o.). Between measurements cats were kept in a normal environment. In control animals the VOR gain was close to unity only up to certain stimulus velocities which varied amongst cats; thereafter a sharp drop in gain occurred probably due to saturation of central and peripheral neuronal responses. Therefore, VOR gains in lesioned animals were compared to the control responses yielding high gain. It is only at these small stimulus amplitudes that the two labyrinths maximally interact and, therefore, one would expect the largest changes. The gain was computed after correction for the ocular imbalance induced by the lesion. Immediately after the lesion a drop in gain to stimulations in both directions was noted; the reduction was larger for the VOR evoked on rotation to the lesioned side. Contrary to control animals, no partial response saturation occurred in lesioned animals but, following rotation to the lesioned side, complete saturation was noted with larger stimuli. Ocular balance was greatly improved within the first 3–4 days p.o. as indicated by the strong reduction of nystagmus. The time course of p.o. adaptive gain changes could be divided into three stages: in the initial stage (1–5 days p.o.) no improvement was visible; between p.o. days 5–10 one group of cats showed an abrupt increase in gain while it remained low in others. Response symmetry showed no consistent change in either group; the 3rd stage starting p.o. day 10 and extending throughout the observation period (22 months) is characterized by slowly developing changes reducing significantly response asymmetry. The incremental gain was higher in the young than in the adult-operated chronic cats. Compared to controls the phase plot of the VOR of lesioned animals shows a parallel shift of ca. 10 ° towards larger lead over the frequency range tested (0.05–1.0 Hz) independent of direction of rotation or p.o. stages. All lesioned animals showed a clear failure to hold eye position in the dark even in the chronic stage; a drift with an exponentially decreasing velocity of ca. 2–4 °/s was typical. The direction of the drift could be to the lesioned as well as to the intact side. The eyes seem to approach a new null point which is shifted towards the lesioned side. In conclusion on data show that while ocular balance recovers quite well and fast after unilateral lesions the VOR dynamics show some adaptive plasticity but also significant long-term deficits when measured in the dark and with the head fixed. Obviously, the striking recovery observed in the freely moving animal must be aided by other sensory systems.