Velocity storage mechanism drives a cerebellar clock for predictive eye velocity control

Predictive motor control is ubiquitously employed in animal kingdom to achieve rapid and precise motor action. In most vertebrates large, moving visual scenes induce an optokinetic response (OKR) control of eye movements to stabilize vision. In goldfish, the OKR was found to be predictive after a prolonged exposure to temporally periodic visual motion. A recent study showed the cerebellum necessary to acquire this predictive OKR (pOKR), but it remained unclear as to whether the cerebellum alone was sufficient. Herein we examined different fish species known to share the basic architecture of cerebellar neuronal circuitry for their ability to acquire pOKR. Carps were shown to acquire pOKR like goldfish while zebrafish and medaka did not, demonstrating the cerebellum alone not to be sufficient. Interestingly, those fish that acquired pOKR were found to exhibit long-lasting optokinetic after nystagmus (OKAN) as opposed to those that didn’t. To directly manipulate OKAN vestibular-neurectomy was performed in goldfish that severely shortened OKAN, but pOKR was acquired comparable to normal animals. These results suggest that the neuronal circuitry producing OKAN, known as the velocity storage mechanism (VSM), is required to acquire pOKR irrespective of OKAN duration. Taken together, we conclude that pOKR is acquired through recurrent cerebellum-brainstem parallel loops in which the cerebellum adjusts VSM signal flow and, in turn, receives appropriately timed eye velocity information to clock visual world motion.