ADAPTATION AND HABITUATION OF THE VESTIBULOOCULAR REFLEX IN INTACT AND INFERIOR OLIVE-LESIONED RATS

The gain of the vestibulo-ocular reflex (VOR) of intact pigmented rats was adaptively modified by training protocols that created a visual-vestibular conflict. For training, head restrained animals were oscillated on a turntable in front of an optokinetic pattern projected onto a cylindrical wall. The optokinetic pattern either moved the same amplitude with the animal ("in-phase": 0.05 Hz +/- 20-degrees/s) or opposite in direction ("out-of-phase": turntable and pattern 0.05 Hz +/- 10-degrees/s each). VOR responses were tested in darkness before and after each 8 min training period for a duration of 40 min. During "out-of-phase" training the gain of compensatory eye movements measured in light was close to 2 from the beginning on and the VOR tested in darkness increased in gain progressively from 0.48 (+/- 0.12) to 0.9 (+/- 0.3; P < 0.05) in 5 out of 7 rats. Two rats did not adapt their VOR gain. Phase values decreased slightly by about 10-degrees. During "in-phase" stimulation compensatory eye movement were almost completely suppressed (gain close to 0) from the beginning on and the VOR tested in darkness decreased gradually in gain from 0.62 (+/- 0.17) to 0.13 (+/- 0.1; P < 0.001) in all 6 trained rats. Phase values decreased in parallel from 151-degrees to 119-degrees (P < 0.01). The effectiveness of the "in-phase" training paradigm in the absence of compensatory eye movements indicates that retinal image slip is the relevant signal for adaptation. In seven rats with histologically verified almost complete inferior olive (IO) lesions (chemically induced at least 45 days prior to training), "out-of-phase" and "in-phase" stimulation evoked compensatory eye movements with gains comparable to those in intact rats. VOR parameters measured in darkness were altered with respect to those of control rats. Gain differed extremely between individuals and phase lag re acceleration was in all IO-lesioned rats larger than in intact rats. The time constant of the VOR in response to table velocity steps was significantly longer (17 s +/- 4) than in intact rats (11 s +/- 3). Training did not alter the gain of the VOR in 5 out of 7 IO-lesioned rats. One rat increased its gain during "out-of-phase" training in the first, but not during a second training session (and not during "in-phase" training) and another rat decreased its gain during "in-phase" training (but not during "out-of-phase" training). These changes in VOR gain might have occurred by chance rather than by learning. The absence of adaptation in IO-lesioned rats can be explained either by the absence of climbing fiber mediated slip signals in the cerebellar cortex or by lesion-induced secondary changes which result in a long-term reduction of the inhibitory efficacy of Purkinje-cells. In the absence of arousing stimuli VOR responses of intact rats exhibit a strong decrement during table oscillations in darkness. Between trials, with the rat at rest, response magnitude recovered spontaneously. Six out of 8 IO-lesioned rats expressed a very similar modification of their VOR gain. These results indicate that the neural mechanisms responsible for adaptive gain decrease during "in-phase" training and those responsible for a gain decrease during short-term habituation are different.