Plasticity in the Vestibulo-Ocular Reflex: A New Hypothesis

The vestibulo-ocular reflex functions to prevent head movements from disturbing retinal images by generating compensatory eye movements to offset the head movements. In the monkey--the species mainly under consideration here--this reflex is machine-like and very effective. In the short-term, the VOR operates as an open-loop control system without the benefit of feedback and its performance is fixed and immutable: No matter what pattern of eye-head coordination the animal uses to view external objects, there is a continuing need for the VOR and it continues to operate; however, should the VOR consistently fail to stabilize the retinal images during head turns, it will gradually undergo long-term adaptive gain changes that restore, that stability. This adaptive capability is ultimately dependent upon vision, and a variety of optical devices that disturb the visual input normally associated with lead turns have been used to induce large changes in the reflex. Insofar as the monkey is concerned, all of the available evidence suggests to us that the modifiable elements underlying these long-term adjustments are located in the brainstem vestibular pathways and not, as previously suggested by others, in the floccular lobes of the cerebellum. However, the flocculus does appear to have an important, inductive role in the adaptive process providing at least part of the error signal guiding the long-term adjustments in the brainstem. In our view, the VOR is a particularly well-defined example of a plastic system and promises to be a most useful model for studying the cellular mechanisms underlying memory and learning the central nervous system.