Rewards or penalties become informative only when contingent on an immediately preceding response. Our goal was to determine if the brain responds differently to motivational events depending on whether they provide feedback with the contingencies effective for learning. Event-related fMRI data were obtained from 22 volunteers performing a visuomotor categorical task. In learning-condition trials, participants learned by trial and error to make left or right responses to letter cues (16 consonants). Monetary rewards (+500) or penalties (-500) were given as feedback (learning feedback). In random-condition trials, cues (4 vowels) appeared right or left of the display center, and participants were instructed to respond with the appropriate hand. However, rewards or penalties (random feedback) were given randomly (50⁄50%) regardless of the correctness of response. Feedback-associated BOLD responses were analyzed with ANOVA [trial type (learning vs. random) x feedback type (reward vs. penalty)] using SPM8 (voxel-wise FWE p < .001). The right caudate nucleus and right cerebellum showed activation, whereas the left parahippocampus and other regions as the default mode network showed deactivation, both greater for learning trials than random trials. Activations associated with reward feedback did not differ between the two trial types for any brain region. For penalty, both learning-penalty and random-penalty enhanced activity in the left insular cortex, but not the right. The left insula, however, as well as the left dorsolateral prefrontal cortex and dorsomedial prefrontal cortex/dorsal anterior cingulate cortex, showed much greater responses for learning-penalty than for random-penalty. These findings suggest that learning-penalty plays a critical role in learning, unlike rewards or random-penalty, probably not only due to its evoking of aversive emotional responses, but also because of error-detection processing, either of which might lead to changes in planning or strategy.