Getting ahead of oneself: anticipation and the vestibulo-ocular reflex

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.