Separate Neural Substrates in the Human Cerebellum for Sensory-motor Adaptation of Reactive and of Scanning Voluntary Saccades

Abstract

Sensory-motor adaptation processes are critically involved in maintaining accurate motor behavior throughout life. Yet their underlying neural substrates and task-dependency bases are still poorly understood. We address these issues here by studying adaptation of saccadic eye movements, a well-established model of sensory-motor plasticity. The cerebellum plays a major role in saccadic adaptation but it has not yet been investigated whether this role can account for the known specificity of adaptation to the saccade type (e.g., reactive versus voluntary). Two patients with focal lesions in different parts of the cerebellum were tested using the double-step target paradigm. Each patient was submitted to two separate sessions: one for reactive saccades (RS) triggered by the sudden appearance of a visual target and the second for scanning voluntary saccades (SVS) performed when exploring a more complex scene. We found that a medial cerebellar lesion impaired adaptation of reactive—but not of voluntary—saccades, whereas a lateral lesion affected adaptation of scanning voluntary saccades, but not of reactive saccades. These findings provide the first evidence of an involvement of the lateral cerebellum in saccadic adaptation, and extend the demonstrated role of the cerebellum in RS adaptation to adaptation of SVS. The double dissociation of adaptive abilities is also consistent with our previous hypothesis of the involvement in saccadic adaptation of partially separated cerebellar areas specific to the reactive or voluntary task (Alahyane et al. Brain Res 1135:107–121 (2007)).