Habits are characterized by an insensitivity to their consequences and, as such, can be distinguished from goal-directed actions. The neural basis of the development of demonstrably outcome-insensitive habitual actions in humans has not been previously characterized. In this experiment, we show that extensive training on a free-operant task reduces the sensitivity of participants' behavior to a reduction in outcome value. Analysis of functional magnetic resonance imaging data acquired during training revealed a significant increase in task-related cue sensitivity in a right posterior putamen-globus pallidus region as training progressed. These results provide evidence for a shift from goal-directed to habit-based control of instrumental actions in humans, and suggest that cue-driven activation in a specific region of dorsolateral posterior putamen may contribute to the habitual control of behavior in humans.

Research has increasingly implicated the striatum in the processing of reward-related information in both animals and humans. However, it is unclear whether human striatal activation is driven solely by the hedonic properties of rewards or whether such activation is reliant on other factors, such as anticipation of upcoming reward or performance of an action to earn a reward. We used event-related functional magnetic resonance imaging to investigate hemodynamic responses to monetary rewards and punishments in three experiments that made use of an oddball paradigm. We presented reward and punishment displays randomly in time, following an anticipatory cue, or following a button press response. Robust and differential activation of the caudate nucleus occurred only when a perception of contingency existed between the button press response and the outcome. This finding suggests that the caudate is involved in reinforcement of action potentially leading to reward, rather than in processing reward per se.

A popular hypothesis in the social sciences is that humans have social preferences to reduce inequality in outcome distributions because it has a negative impact on their experienced reward. Although there is a large body of behavioural and anthropological evidence consistent with the predictions of these theories, there is no direct neural evidence for the existence of inequality-averse preferences. Such evidence would be especially useful because some behaviours that are consistent with a dislike for unequal outcomes could also be explained by concerns for social image or reciprocity, which do not require a direct aversion towards inequality. Here we use functional MRI to test directly for the existence of inequality-averse social preferences in the human brain. Inequality was created by recruiting pairs of subjects and giving one of them a large monetary endowment. While both subjects evaluated further monetary transfers from the experimenter to themselves and to the other participant, we measured neural responses in the ventral striatum and ventromedial prefrontal cortex, two areas that have been shown to be involved in the valuation of monetary and primary rewards in both social and non-social contexts. Consistent with inequality-averse models of social preferences, we find that activity in these areas was more responsive to transfers to others than to self in the 'high-pay' subject, whereas the activity of the 'low-pay' subject showed the opposite pattern. These results provide direct evidence for the validity of this class of models, and also show that the brain's reward circuitry is sensitive to both advantageous and disadvantageous inequality.

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.