Dissociating Valence of Outcome from Behavioral Control in Human Orbital and Ventral Prefrontal Cortices

Abstract

The precise role of orbitofrontal cortex (OFC) in affective processing is still debated. One view suggests OFC represents stimulus reward value and supports learning and relearning of stimulus-reward associations. An alternate view implicates OFC in behavioral control after rewarding or punishing feedback. To discriminate between these possibilities, we used event-related functional magnetic resonance imaging in subjects performing a reversal task in which, on each trial, selection of the correct stimulus led to a 70% probability of receiving a monetary reward and a 30% probability of obtaining a monetary punishment. The incorrect stimulus had the reverse contingency. In one condition (choice), subjects had to choose which stimulus to select and switch their response to the other stimulus once contingencies had changed. In another condition (imperative), subjects had simply to track the currently rewarded stimulus. In some regions of OFC and medial prefrontal cortex, activity was related to valence of outcome, whereas in adjacent areas activity was associated with behavioral choice, signaling maintenance of the current response strategy on a subsequent trial. Caudolateral OFC-anterior insula was activated by punishing feedback preceding a switch in stimulus in both the choice and imperative conditions, indicating a possible role for this region in signaling a change in reward contingencies. These results suggest functional heterogeneity within the OFC, with a role for this region in representing stimulus-reward values, signaling changes in reinforcement contingencies and in behavioral control.