Inluence of eye motion on adaptive modifications of the vestibulo-ocular reflex in the rat

While sustained retinal slip is assumed to be the basic conditioning stimulus in adaptive modifications of the vestibulo-ocular reflex (VOR) gain, several observations suggest that eye motion-related signals might also be involved. We oscillated pigmented rats over periods of 20 min around the vertical axis, at 0.3 Hz and 20°/s peak velocity, in different retinal slip and/or eye motion conditions in order to modify their VOR gain. The positions of both eyes were recorded by means of a phase-detection coil system with the head restrained. The main findings came from the comparison of two basic conditions - including their respective controls - in which one or both eyes were reversibly immobilised by threads sutured to the eyes. In the first condition the animals were rotated in the light with one eye immobilised and the other eye free to move but covered. Rotation in the light in this open-loop condition immediately elicited high-gain compensatory eye movements of the non-impeded, covered eye. At the end of this training procedure, the VOR gain increased by 42.3%. In the second condition, both eyes were immobilised and one eye was covered. The result was an increase in the VOR gain of 26.3%. These two conditions were similar as to the visuo-vestibular drive during the exposure, but different as to the resulting - and allowed - eye motion, showing that the condition where the larger eye movements occurred yielded the larger VOR gain change. Our data support the idea proposed by Collewijn and Grootendorst (1979, p. 779) and Collewijn (1981, p. 146) that "[retinal] slip and eye movements seem to be relevant signals for the adaptation of the rabbit's visuo-vestibular oculomotor reflexes". Our data also suggest that sensory information related to eye movements, more likely than efference copy, is the coding signal for eye movement which combines with the retinal slip signal to generate adaptive changes of the VOR.