Normal and adapted visuooculomotor reflexes in goldfish.

Under normal physiological conditions, whole field visual motion generally occurs in response to either active or passive self-motion. In the laboratory, selective movement of the visual surround produces an optokinetic response (OKR) that acts primarily to support the vestibuloocular reflex (VOR). During visual world motion, however, the OKR can be viewed as operating independently over frequency and amplitude ranges insufficient for vestibular activation. The goal of the present study was to characterize this isolated behavior of the OKR in goldfish as an essential step for studying central neuronal correlates of visual-vestibular interactions and the mechanisms underlying oculomotor adaptation. After presentation of either binocular sinusoidal or step visual stimuli, conjugate eye movements were elicited with an amplitude and phase profile similar to that of other vertebrates. An early and a delayed component were measured with different dynamics that could be altered independently by visual training. The ensuing visuomotor plasticity was robust and exhibited five major characteristics. First, the gain of both early and delayed components of the OKR increased > 100%. Second, eye velocity decreased 0.5-2.0 s before the change in direction of stimulus velocity. Third, on lengthening the duration of a constant velocity visual stimulus (e.g., from 8 to 16 s), eye velocity decreased toward 0 degrees/s. This behavior was correlated with the direction and period as opposed to the frequency of the visual stimulus ("period tuning"). Fourth, visual stimulus training increased VOR eye velocity with a ratio of 0.6 to 1 to that measured for the OKR. Fifth, the OKR adaptation, eye velocity consistently oscillated in a conjugate, symmetrical fashion at 2.4 Hz in the light, whereas in the dark, a rhythmical low-amplitude eye velocity occurred at the visual training frequency. We conclude that the frequency and amplitude of visual stimuli for eliciting the goldfish OKR are well suited for complementing the VOR. Unlike most mammals, OKR adaptive modifications significantly alter VOR gain, whereas the effects of VOR training are much less on OKR gain. These observations suggest that both distributed circuits and discrete neuronal populations control visuo- and vestibulomotor performance. Finally, the existence of a rhythmic, "period tuned" visuomotor behavior provides a unique opportunity to examine the neuronal mechanisms of adaptive plasticity.