Cerebellar role in adaptation of the goldfish vestibuloocular reflex

1. The time course of eye velocity responses elicited by head velocity steps was compared in normal, adapted, and cerebellectomized goldfish. Vestibuloocular reflex (VOR) adaptation was induced by combined visual and vestibular stimulation that altered the ratio of eye to head velocity (VOR gain) toward values either higher or lower than the control amplitude. The velocity step consisted of alternating periods of head rotation at a constant velocity of 16 degrees/s zero-to-peak around the vertical axis. 2. The VOR produced by head velocity steps consisted of an early acceleration-related component, the dynamic response, separated from a sustained period of constant velocity, the plateau, by a sag that occurred around 125-150 ms. Latency of the VOR averaged 18 ms for the adducting eye and 20 ms for abducting eye independent of the initial VOR gain. Adapted dynamic VOR responses diverged from the control records at the earliest detectable latency after both high and low VOR gain training. This result demonstrates modification in the shortest latency brain stem VOR pathway, presumably, the three-neuron reflex arc. 3. After acute cerebellectomy the adapted dynamic response was unaltered for approximately 50 ms in the low-gain and 70 ms in the high-gain VOR states. Not less than 30% of the altered velocity was retained throughout the remaining dynamic and sustained component. These results demonstrate that the vestibulocerebellum is not necessary for the maintenance of the earliest adapted eye velocity. Hence brain stem pathways are sufficient for the expression of the modified VOR. 4. Purkinje cells identified by simple and complex spikes were recorded extracellularly in the area of the vestibulocerebellum, where electrical stimulation produced conjugate ipsiversive horizontal eye movements. Independent eye and head velocity sensitivities were determined in response to visual world motion and VOR suppression, respectively. The two signals either added, canceled, or were both present in Purkinje cells throughout the range of eye velocity induced by vertical axis visual-vestibular stimulation. 5. Latency of Purkinje cell discharge to either a vestibular or visual velocity step exhibited means of 43 and 70 ms, respectively.(ABSTRACT TRUNCATED AT 400 WORDS)