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• Frequency selective VOR motor learning was confirmed in goldfish as in other model species. • Sharper tuning of frequency selectivity was found in VOR gain-up than gain-down. • Frequency competitive VOR motor learning was possible in goldfish as in primates. • The cerebellum was shown to be necessary for frequency competitive VOR motor learning. • Purkinje cell activities changed with gain-down but not with gain-up during frequency competitive VOR motor learning. Biological motions commonly contain multiple frequency components in which each fundamental has to be adjusted by motor learning to acquire a new motor skill or maintain acquired skills. At times during this motor performance one frequency component needs to be enhanced (gain-up) while another is suppressed (gain-down). This pattern of simultaneous gain-up and -down adjustments at different frequencies is called frequency competitive motor learning. Currently we investigated cerebellar roles in this behavior utilizing the goldfish vestibulo-ocular reflex (VOR). Previously, VOR motor learning was shown in primates to be frequency selective and exhibit frequency competitive motor learning. Here we demonstrate that the goldfish VOR performs frequency competitive motor learning when high and low frequency components are trained to gain-up and gain-down, respectively. However, when the two frequency components were trained in the opposite directions only gain-up component was observed. We also found that cerebellectomy precluded any frequency competitive VOR motor learning. Complementary single unit recordings from vestibulo-cerebellar Purkinje cells revealed changes in firing modulation along with gain-down learning, but not with gain-up learning irrespective of frequency. These results demonstrate that the cerebellum is required for all frequency competitive VOR motor learning and Purkinje cell activity therein is well correlated with all gain-down behaviors independent of frequency. However, frequency competitive gain-up learning requires intact, recursive brainstem/cerebellar pathways. Collectively these findings support the idea that VOR gain-up and gain-down learning utilize separate brainstem/cerebellar circuitry that, in turn, clearly underlies the unique ability of the oculomotor system to deal with multiple frequency components. [ABSTRACT FROM AUTHOR]

Abstract: Compensatory counter-rotations of the eyes provoked by head turns are commonly attributed to the vestibulo-ocular reflex (VOR). A recent study in guinea pigs demonstrates, however, that this assumption is not always valid. During voluntary head turns, guinea pigs make highly accurate compensatory eye movements that occur with zero or even negative latencies with respect to the onset of the provoking head movements. Furthermore, the anticipatory eye movements occur in animals with bilateral peripheral vestibular lesions, thus confirming that they have an extra vestibular origin. This discovery suggests the possibility that anticipatory responses might also occur in other species including humans and non-human primates, but have been overlooked and mistakenly identified as being produced by the VOR. This review will compare primate and guinea pig vestibular physiology in light of these new findings. A unified model of vestibular and cerebellar pathways will be presented that is consistent with current data in primates and guinea pigs. The model is capable of accurately simulating compensatory eye movements to active head turns (anticipatory responses) and to passive head perturbations (VOR induced eye movements) in guinea pigs and in human subjects who use coordinated eye and head movements to shift gaze direction in space. Anticipatory responses provide new evidence and opportunities to study the role of extra vestibular signals in motor control and sensory–motor transformations. Exercises that employ voluntary head turns are frequently used to improve visual stability in patients with vestibular hypofunction. Thus, a deeper understanding of the origin and physiology of anticipatory responses could suggest new translational approaches to rehabilitative training of patients with bilateral vestibular loss. [Copyright &y& Elsevier]