Cerebellar lesions impair context-dependent adaptation of reaching movements in primates

To produce accurate movements when conditions change suddenly, the brain must be capable of learning multiple versions of a given motor task and must be able to access the appropriate program using sensory information linked to the context of the movement. The neural basis for context-dependent motor learning is uncertain, but the cerebellum is thought to play a fundamental role. In this study, we examined the effect of lesions of the dorsal vermal and paravermal cerebellar cortex on the adaptation of reaching movements produced by modified visual feedback and accessed with a visual cue. Two rhesus monkeys were trained to point to targets displayed on a video monitor while viewing monocularly with either eye. During the experimental sessions, visual information received by one eye (the "modified" eye) was displaced horizontally, while the information received by the other ("normal") eye remained unaltered. In the first set of experiments (noncontextual paradigm), the animals pointed to targets while viewing with the modified eye. This paradigm resulted in a gradual improvement in pointing accuracy when viewing with that eye, but also produced a shift in pointing responses of equivalent size when viewing with the normal eye. In the second set of experiments (contextual paradigm), the animals alternated six blocks of reaches while viewing monocularly with the modified eye with six blocks viewing with the normal eye. This paradigm improved the pointing accuracy when viewing with the modified eye, but produced only a small shift in pointing responses when viewing with the normal eye. After the dorsal vermal and paravermal cerebellar cortex were resected, no change occurred in the pattern of adaptation produced by the noncontextual paradigm. The contextual paradigm, however, no longer selectively adapted pointing responses for each eye, but rather produced a pointing shift of equivalent size when viewing with either eye. The results indicate that pointing responses can be differentially adapted for each viewing eye, which is a form of context-dependent motor learning. This capability was lost after focal lesions of the dorsal vermal and paravermal cerebellar cortex, suggesting that these regions of cerebellar cortex are required to learn or store multiple representations of a movement, or to retrieve the appropriate motor program in a given sensory context.