Activity of the Substantia Nigra pars Reticulata During Saccade Adaptation.

Abstract

When movements become inaccurate, the resultant error induces motor adaptation to improve accuracy. This error-based motor learning is regarded as a cerebellar function. However, the influence of the other brain areas on adaptation is poorly understood. During saccade adaptation, a type of error-based motor learning, the superior colliculus (SC) sends a post-saccadic error signal to the cerebellum to drive adaptation. Since the SC is directly inhibited by the substantia nigra pars reticulata (SNr), we hypothesized that the SNr might influence saccade adaptation by affecting the SC error signal. In fact, previous studies indicated that the SNr encodes motivation and motivation influences saccade adaptation. In this study, we first established that the SNr projects to the rostral SC, where small error signals are generated, in non-human primates. Then, we examined SNr activity while the animal underwent adaptation. SNr neurons paused their activity in association with the error. This pause was shallower and delayed compared to those of no-error trial saccades. The pause at the end of the adaptation was shallower and delayed compared to that at the beginning of the adaptation. The change in the inter-trial interval, an indicator of motivation, and adaptation speed had a positive correlation with the changes in the error-related pause. These results suggest that 1: the SNr exhibits a unique activity pattern during the error interval, 2: SNr activity increases during adaptation, consistent with the decrease in SC activity, and 3: motivational decay during the adaptation session might increase SNr activity and influence the adaptation speed.Significance StatementMovements impaired due to stroke, injury, or aging recover gradually. To repair an inaccurate movement, the brain measures the error of the movement and changes the movement to minimize the error. This process is called motor adaptation. Although it has been established that the cerebellum plays an essential role in this adaptation, the influence of the other brain areas on the adaptation process is not well defined. The observation that motivation levels influence adaptation led us to suspect that the basal ganglia may influence adaptation. Here, we reveal the substantia nigra pars reticulata activity changes during saccade adaptation in monkeys and suggest how the basal ganglia influence the error signal.