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J Neurophysiol 100: 1320-1331, 2008. First published June 25, 2008; doi:10.1152/jn.90492.2008
0022-3077/08 $8.00

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Doing Without Learning: Stimulation of the Frontal Eye Fields and Floccular Complex Does Not Instruct Motor Learning in Smooth Pursuit Eye Movements

Howard Hughes Medical Institute, W. M. Keck Foundation Center for Integrative Neuroscience, Department of Physiology, University of California, San Francisco, California

Submitted 21 April 2008; accepted in final form 20 June 2008

Under natural conditions, motor learning is instructed by sensory feedback. We have asked whether sensory signals that indicate motor errors are necessary to instruct learning or if the motor signals related to movements normally driven by sensory error signals would be sufficient. We measured eye movements in trained rhesus monkeys while employing electrical microstimulation of the floccular complex of the cerebellum and the smooth eye movement region of the frontal eye fields to alter ongoing pursuit eye movements. Repeated electrical stimulation at fixed times after the onset of target motion and pursuit failed to cause any learning that was retained beyond the time period used to instruct learning. Learning was not uncovered when the target was stabilized with respect to the moving eye to prevent competition between instructive signals created by electrical stimulation and visual image motion signals evoked when stimulation drove the eye away from the tracking target. We suggest that signals emanating from motor-related structures in the pursuit circuit do not instruct learning. Instead, instructive sensory error signals seem to be necessary.