Cerebellar plasticity and the automation of first-order rules

Theories of corticocerebellar function propose roles for the cerebellum in automating motor control, a process thought to depend on plasticity in cerebellar circuits that exchange information with the motor cortex. Little is known, however, about automating behaviors beyond the motor domain. The present study tested the hypothesis that cerebellar plasticity also subserves the development of automaticity in behavior based on low-order rules. Human subjects were required to learn two sets of first-order rules in which visual stimuli of different shapes each arbitrarily instructed a particular finger movement. We used event-related functional magnetic resonance imaging to scan subjects while these response rules became increasingly automatic with practice, as assessed with a dual-task procedure. We found that the amplitude of the blood oxygenation level-dependent signal gradually decreased as a function of practice, as responses became increasingly automatic, and that this effect was greater for a set of rules that became automatic rapidly compared with a second set, which became automatic more slowly. These trial-by-trial activity changes occurred in Crus I of cerebellar cortical lobule HVIIA, in which neurons exchange information with the prefrontal cortex rather than the motor cortex. Activity in Crus I was time locked specifically to the processing of these rules, rather than to subsequent actions. The results support the hypothesis that decreases in cerebellar cortical activity underlie the automation of behavior, whether related to motor control and motor cortex or to response rules and prefrontal cortex.