Cerebellar Nodulectomy Impairs Spatial Memory of Vestibular and Optokinetic Stimulation in Rabbits

Natural vestibular and optokinetic stimulation were used to investigate the possible role of the cerebellar nodulus in the regulation and modification of reflexive eye movements in rabbits. The nodulus and folium 9d of the uvula were destroyed by surgical aspiration. Before and after nodulectomy the vertical and horizontal vestibuloocular reflexes (VVOR, HVOR) were measured during sinusoidal vestibular stimulation about the longitudinal (roll) and vertical (yaw) axes. Although the gain of the HVOR (GHVOR = peak eye movement velocity/peak head velocity) was not affected by the nodulectomy, the gain of the VVOR (GVVOR) was reduced. The gains of the vertical and horizontal optokinetic reflexes (GVOKR, GHOKR) were measured during monocular, sinusoidal optokinetic stimulation (OKS) about the longitudinal and vertical axes. Following nodulectomy, there was no reduction in GVOKR or GHOKR. Long-term binocular OKS was used to generate optokinetic afternystagmus, OKAN II, that lasts for hours. After OKAN II was induced, rabbits were subjected to static pitch and roll, to determine how the plane and velocity of OKAN II is influenced by a changing vestibular environment. During static pitch, OKAN II slow phase remained aligned with earth-horizontal. This was true for normal and nodulectomized rabbits. During static roll, OKAN II remained aligned with earth-horizontal in normal rabbits. During static roll in nodulectomized rabbits, OKAN II slow phase developed a centripetal vertical drift. We examined the suppression and recovery of GVVOR following exposure to conflicting vertical OKS for 10–30 min. This vestibular-optokinetic conflict reduced GVVOR in both normal and nodulectomized rabbits. The time course of recovery of GVVOR after conflicting OKS was the same before and after nodulectomy. In normal rabbits, the head pitch angle, at which peak OKAN II velocity occurred, corresponded to the head pitch angle maintained during long-term OKS. If the head was maintained in a “pitched-up” or “pitched-down” orientation during long-term OKS, the subsequently measured OKAN II peak velocity occurred at the same orientation. This was not true for nodulectomized rabbits, who had OKAN II peak velocities at head pitch angles independent of those maintained during long-term OKS. We conclude that the nodulus participates in the regulation of compensatory reflexive movements. The nodulus also influences “remembered” head position in space derived from previous optokinetic and vestibular stimulation.

Signals used to compute errors in monkey vestibuloocular reflex: possible role of flocculus

Adaptive changes were induced in the vestibuloocular reflex (VOR) of monkeys by oscillating them while they viewed the visual scene through optical devices (“spectacles”) that required changes in the amplitude of eye movement during head turns. The “gain” of the VOR (eye velocity divided by head velocity) during sinusoidal oscillation in darkness underwent gradual changes that were appropriate to reduce the motion of images on the retina during the adapting procedures. Bilateral ablation of the flocculus and ventral paraflocculus caused a complete and enduring loss of the ability to undergo adaptive changes in the VOR. Partial lesions caused a substantial but incomplete loss of the adaptive capability. We conclude that the flocculus is necessary for adaptive changes in the monkey's VOR. Further experiments in normal animals determined the types of stimuli that were necessary and/or sufficient to cause changes in VOR gain. Full-field visual stimulation was not necessary to induce adaptive changes in the VOR. Monkeys tracked a small spot in conditions that elicited the same combination of eye and head movements seen during passive oscillation with spectacles. The gain of the VOR showed changes 50-70% as large as those produced by the same duration of oscillation with spectacles. Since the effective tracking conditions cause a consistent correlation of floccular output with vestibular inputs, these data are compatible with our previous suggestion that the flocculus may provide signals used by the central nervous system to compute errors in the gain of the VOR. Prolonged sinusoidal optokinetic stimulation with the head stationary caused only a slight increase in VOR gain. Left-right reversal of vision and eye movement during sinusoidal vestibular oscillation caused decreases in VOR gain. In rabbits, both of these stimulus conditions produced large increases in the gain of the VOR, which implied that eye velocity signals were used instead of vestibular inputs to compute errors in the VOR. Our different results argue that vestibular signals are necessary for computing errors in VOR gain in the monkey. The species difference may reflect the additional role that smooth pursuit eye movements play in stabilizing gaze during head turns in monkeys.