Discrete, unilateral, electrolytic lesions of the dorsal cap of the inferior olive were made in rabbits in an attempt to assess the effect on eye movements of removal of a visual climbing fiber input to the flocculus. The position of the lesioning electrode within the dorsal cap was adjusted on the basis of the field potential evoked by flash stimulation of the contralateral eye. Electrophysiological and anatomical evidence confirmed that the microlesions of the dorsal cap destroyed 10-80% of olivary cells, but caused only slight damage to the olivocerebellar pathway originating from the contralateral dorsal cap. The immediate effect of the microlesions was a spontaneous, conjugate drift of the eyes of the side contralateral to the lesion. The effects of the microlesions on eye movements were further examined using reflexes evoked by vestibular and optokinetic stimulation. Postoperatively, the vestibuloocular reflex (VOR) gain was not modified, but there was a marked VOR velocity bias to the contralateral side. This velocity bias was most pronounced at low stimulus frequencies (0.02-0.05 Hz, ±10°) and was minimal at stimulus frequences above 0.5 Hz. Monocular, sinusoidal optokinetic stimulation with a large contrast-rich visual target evokes, in normal rabbits a conjugate asymmetric following response with a higher eye velocity for target movement from posterior to anterior. Following damage to the dorsal cap, the asymmetry of this optokinetic reflex was reversed when the target was presented to the eye contralateral to the lesion. With monocular, constant-velocity optokinetic stimulation delivered to the contralateral eye, the optokinetic gain for movement in the posterior to anterior direction was decreased. These data suggest that visual climbing fibers are part of a feedback loop that reduces retinal slip of low velocity. The relatively low discharge rate of climbing fibers would seem appropriate to encode continuously retinal slip of low velocity and to influence low-velocity eye movements.
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