A CEREBELLAR ROLE IN CONTROL OF THE GOLDFISH VESTIBULO-OCULAR REFLEX

Abstract

The vestibulo-ocular reflex (VOR) stabilizes gaze by producing eye movements that compensate for head rotations. VOR gain is defined as eye velocity divided by head velocity. Three types of experiments were performed in goldfish (Carassius auratus) to investigate the cerebellar role in gain control, including cerebellar ablation, microstimulation, and extracellular recording, before and after training.;Cerebellectomy increased the VOR gain. An average gain of 0.86 (+OR-) 0.12 in untrained animals at 1/8 Hz increased to 1.50 (+OR-) 0.36 after cerebellectomy (N = 9). Cerebellectomy almost immediately abolished gain changes previously established by training. Both visual optokinetic reflexes and VOR suppression were unimpaired by cerebellectomy.;Cerebellar microstimulation (1-6 (mu)A) evoked vigorous nystagmus. The stimulated areas may include the normal output to the brainstem vestibular centers. Results indicate activation or inhibition of cerebellar neurons exerting inhibitory control over the ipsilateral vestibular nucleus. Eye movements reversed direction with currents of reversed polarity.;Extracellular unit recording was performed both in the cerebellum and in the brainstem. Four types of activity were distinguished among cerebellar units, described here as eye velocity, velocity-position, molecular layer interneuron, and Purkinje cell units. Some Purkinje cells were discovered to be sensitive to changes in gaze velocity, i.e., modulating peak-to-peak firing during VOR suppression. Six of these Purkinje cells were followed continuously for 30-90 minutes of gain reduction training. Substantial increases in unit sensitivity occurred: unit sensitivity increased by roughly 0.1 ips/deg/sec with each drop of 0.1 in the gain. Phase change were also observed in several units.;These data demonstrate that the goldfish cerebellum strongly influences the functioning of the VOR. Cerebellar neurons are shown to be sensitive to errors in the VOR gain, suggesting a role in measuring the amplitude and direction of necessary longer-term gain changes. Enhanced firing of cerebellar neurons during gain decreases suggests that the cellular events underlying motor learning may take place within the cerebellum. A model is proposed to account for the different responses seen among cerebellar neurons during training.