Distributed midbrain responses signal the content of positive identity prediction errors

Abstract

Recent work across species has shown that midbrain dopamine neurons signal not only errors in the prediction of reward value but also in the prediction of value-neutral sensory features. To support learning of associative structures in downstream areas, identity prediction errors (iPEs) should signal specific information about the mis-predicted outcome. Here, we used pattern-based analysis of functional magnetic resonance imaging (fMRI) data acquired during reversal learning to characterize the information content of iPE responses in the human midbrain. We find that fMRI responses to value-neutral identity errors contain information about the identity of the unexpectedly received reward (positive iPE+) but not about the identity of the omitted reward (negative iPE−). Exploratory analyses revealed representations of iPE− in the dorsomedial prefrontal cortex. These results demonstrate that ensemble midbrain responses to value-neutral identity errors convey information about the identity of unexpectedly received outcomes, which could shape the formation of novel stimulus-outcome associations that constitute cognitive maps.