Response selection versus feedback analysis in conditional visuo-motor learning

Abstract

Conditional associative sensori-motor learning (i.e. the acquisition of specific arbitrary sensori-motor mappings) involves several processes that depend upon the integrity of the fronto-striatal system. The specific role of the different components of the fronto-striatal system in this type of learning is still unclear and was examined in the present functional Magnetic Resonance Imaging (fMRI) study in humans. The subjects had to learn by trial and error arbitrary associations between visual stimuli and motor responses in an experimental paradigm designed to dissociate between the neuronal substrates specifically involved in the selection of the appropriate response and in the analysis of the feedback obtained during the learning and post-learning periods. First, the results demonstrate that the dorsal premotor (PMd) cortex is the critical structure for the acquisition and execution of arbitrary mappings of visual stimuli to motor responses. Second, they reveal an important shift in activation from the cognitive fronto-striatal network (involving the caudate nucleus, the dorsolateral prefrontal cortex, and the PMd) to the motor fronto-striatal network (involving the putamen and the PMd) as we move from initial learning of sensori-motor relations to the post-learning selection of the responses. Finally, they show that feedback processing, but not response selection, increased activity in the anterior cingulate and orbitofrontal cortical regions, demonstrating the selective involvement of these limbic frontal regions in the processing of the consequences of a given action. Altogether our data suggest that, in conditional visuo-motor learning, the associations are critically regulated by the dorsal premotor cortex and the striatum, with additional brain areas contributing to specific aspects of the learning and performance of such associations.