The Substantia Nigra Pars Reticulata Modulates Error-Based Saccadic Learning in Monkeys

摘要

The basal ganglia have long been considered crucial for associative learning, but whether they also are involved in another type of learning, error-based motor learning, is not clear. Error-based learning has been considered the province of the cerebellum. However, learning to use a robotic arm and saccade adaptation, which use error-based learning, are facilitated by motivation, which is a function of the basal ganglia. Additionally, patients with Parkinson's disease, a basal ganglia deficit, show slower saccade adaptation than age matched controls. To further investigate whether the basal ganglia actually influence error-based learning, we reversibly inactivated the oculomotor portion of the substantia nigra pars reticulata (SNr) in two monkeys and tested saccade adaptation. Here, we show that nigral inactivation affected saccade adaptation. In particular, the inactivation facilitated the amplitude decrease adaptation of ipsiversive saccades. Consistent with previous studies, no effect was seen on the amplitude of the ipsiversive saccades when we did not induce adaptation. Therefore, the facilitated adaptation was not caused by inactivation directly modulating ipsiversive saccades. On the other hand, the kinematics of corrective saccades, which represent error processing, were changed after the inactivation. Thus, our data suggest that the oculomotor SNr assists saccade adaptation by strengthening the error signal. This effect indicates the basal ganglia influence error-based motor learning, a previously unrecognized function.