Whereas positive feedback is both rewarding and informative, negative feedback can be construed as either punishing (because it is indicative of poor performance) or informative (because it may lead to goal attainment). In this neuroimaging experiment, we highlighted the informational value of negative feedback by intermixing trials with and without feedback. When performance feedback is expected, positive feedback triggers an increase in striatal activity, whereas negative feedback elicits a decrease in striatal activity. We predicted that, in contrast, when feedback receipt is unpredictable, the striatal response to negative feedback would increase. Participants performed a paired-associate learning task during fMRI scanning. In one condition (“blocked feedback”), the receipt of feedback was predictable—participants knew whether or not they would receive feedback for their responses. In another condition (“mixed feedback”), the receipt of feedback was unpredictable—on a random 50% of trials, participants received feedback, and they otherwise received no feedback. Negative feedback in the mixed feedback condition elicited more striatal activity than negative feedback in the blocked feedback condition. In contrast, feedback omission evoked more striatal activity when feedback delivery was expected, compared to when it was unpredictable. This pattern emerged from an increase in caudate activity in response to negative feedback in the mixed feedback condition and a decrease in ventral striatal activity in response to no feedback in this condition. These results suggest that, by emphasizing the informational value of negative feedback, an unpredictable feedback context alters the striatal response to negative feedback and to the omission of feedback.

Adults have difficulty discriminating nonnative phonetic contrasts, but under certain circumstances training can lead to improvement in this ability. Despite the ubiquitous use of performance feedback in training paradigms in this and many other domains, the mechanisms by which feedback affects learning are not well understood. In this event-related functional magnetic resonance imaging study, we examined how performance feedback is processed during perceptual learning. Thirteen Japanese speakers for whom the English phonemes [r] and [l] were nondistinct performed an identification task of the words “road” and “load” that has been shown to be effective in inducing learning only when performance feedback is present. Each subject performed alternating runs of training with and without feedback, followed by performance of a card-guessing task with monetary reward and punishment outcomes. We found that the caudate nucleus was more robustly activated bilaterally when performing the perceptual identification task with feedback than without feedback, and the right caudate nucleus also showed a differential response to positive and negative feedback. Moreover, using a within-subjects design, we found that the caudate nucleus also showed a similar activation pattern to monetary reward and punishment outcomes in the card-guessing task. These results demonstrate that the caudate responds to positive and negative feedback during learning in a manner analogous to its processing of extrinsic affective reinforcers and indicate that this region may be a critical moderator of the influence of feedback on learning. These findings impact our broader understanding of the mechanisms underlying nondeclarative learning and language acquisition.