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

Abstract

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.

Cerebellar Purkinje cell activity drives motor learning

“…Purkinje cells encode information that could, in principle, be used to guide the induction of plasticity 6,7 , and several models have suggested a role for Purkinje cell activity in guiding the acquisition or consolidation of motor memory 5,8,9 . However, causal evidence that Purkinje cell activity can induce learning in vivo has been lacking; previous attempts to induce learning by activating Purkinje cells with electrical stimulation of the cerebellar cortex were unsuccessful 10,11 . Thus, we harnessed the cell-type specificity of optogenetics and the power of the well-characterized vestibulo-ocular reflex (VOR) to determine whether Purkinje cell activity can drive the induction of learned changes in behavior.…”