Cerebral correlates of salient prediction error for different rewards and punishments

Abstract

Learning to predict rewarding and aversive outcomes is based on the comparison between predicted and actual outcomes (prediction error: PE). Recent electrophysiological studies reported that during a Pavlovian procedure some dopamine neurons code a classical PE signal while a larger population of dopaminergic neurons reflect a "salient" prediction error (SPE) signal, being excited both by unpredictable aversive events and by rewards. Yet, it is still unclear whether specific human brain structures receiving afferents from dopaminergic neurons code a SPE and whether this signal depends upon reinforcer type. Here, we used a model-based functional magnetic resonance imaging approach implementing a reinforcement learning model to compute the PE while subjects underwent a Pavlovian conditioning procedure with 2 types of rewards (pleasant juice and monetary gain) and 2 types of punishments (aversive juice and aversive picture). The results revealed that activity of a brain network composed of the striatum, anterior insula, and anterior cingulate cortex covaried with a SPE for appetitive and aversive juice. Moreover, amygdala activity correlated with a SPE for these 2 reinforcers and for aversive pictures. These results provide insights into the neurobiological mechanisms underlying the ability to learn stimuli-rewards and stimuli-punishments contingencies, by demonstrating that the network reflecting the SPE depends upon reinforcement's type. © The Author 2012. Published by Oxford University Press. All rights reserved.