Impairment of saccade adaptation in a patient with a focal thalamic lesion

Abstract

The frequent jumps of the eyeballs—called saccades—imply the need for a constant correction of motor errors. If systematic errors are detected in saccade landing, the saccade amplitude adapts to compensate for the error. In the laboratory, saccade adaptation can be studied by displacing the saccade target. Functional selectivity of adaptation for different saccade types suggests that adaptation occurs at multiple sites in the oculomotor system. Saccade motor learning might be the result of a comparison between a prediction of the saccade landing position and its actual postsaccadic location. To investigate whether a thalamic feedback pathway might carry such a prediction signal, we studied a patient with a lesion in the posterior ventrolateral thalamic nucleus. Saccade adaptation was tested for reactive saccades, which are performed to suddenly appearing targets, and for scanning saccades, which are performed to stationary targets. For reactive saccades, we found a clear impairment in adaptation retention ipsilateral to the lesioned side and a larger-than-normal adaptation on the contralesional side. For scanning saccades, adaptation was intact on both sides and not different from the control group. Our results provide the first lesion evidence that adaptation of reactive and scanning saccades relies on distinct feedback pathways from cerebellum to cortex. They further demonstrate that saccade adaptation in humans is not restricted to the cerebellum but also involves cortical areas. The paradoxically strong adaptation for outward target steps can be explained by stronger reliance on visual targeting errors when prediction error signaling is impaired.