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The Journal of Neuroscience, October 29, 2003, 23(30):9742-9751

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Behavioral/Systems/Cognitive
Cerebellar Signatures of Vestibulo-Ocular Reflex Motor Learning

Pablo M. Blazquez,¹ Yutaka Hirata,³ Shane A. Heiney,¹ Andrea M. Green,² and Stephen M. Highstein¹

Departments of ¹Otolaryngology and ²Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110, and ³Department of Electronic Engineering, Chubu University College of Engineering, Kasugai 487 8501, Japan

The vestibulo-ocular reflex (VOR) comprises an outstanding system to perform studies that probe possible cerebellar roles in motor learning. Novel VOR gains can be induced (learned) by the wearing of minifying or magnifying lenses, and learning requires the presence of the cerebellum. Previously, it was shown that Purkinje cells change their head velocity sensitivities with learning and that this change was thought to be inappropriate to be causal for the changed behavior. We now demonstrate that Purkinje cells also change their eye position, eye velocity, and head velocity sensitivities after learning. These combined changes at the Purkinje cell level contribute to a net modulation that is appropriate to support the new VOR gains. Importantly, the changes in the eye position parameter, reported for the first time, suggest the involvement of the neuronal integrator pathways in VOR learning. We provide evidence that all of these changes are necessary for VOR behavior and can explain learning deficits after cerebellar removal.

Key words: cerebellum; VOR; learning; primate; Purkinje cell; primate

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Received June 17, 2003; revised August 10, 2003; accepted September 2, 2003.

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