Neural substrates of parallel devaluation-sensitive and devaluation-insensitive Pavlovian learning in humans

Abstract

Pavlovian learning depends on multiple and parallel associations leading to distinct classes of conditioned responses that vary in their flexibility following changes in the value of an associated outcome. Here, we aimed to differentiate brain areas involved in learning and encoding associations that are sensitive to changes in the value of an outcome from those that are not sensitive to such changes. To address this question, we combined a Pavlovian learning task with outcome devaluation, eye-tracking and functional magnetic resonance imaging. We used computational modeling to identify brain regions involved in learning stimulus-reward associations and stimulus-stimulus associations, by testing for brain areas correlating with reward-prediction errors and state-prediction errors, respectively. We found that, contrary to theoretical predictions about reward prediction errors being exclusively model-free, voxels correlating with reward prediction errors in the ventral striatum and subgenual anterior cingulate cortex were sensitive to devaluation. On the other hand, brain areas correlating with state prediction errors were found to be devaluation insensitive. In a supplementary analysis, we distinguished brain regions encoding predictions about outcome taste identity from those involved in encoding predictions about its expected spatial location. A subset of regions involved in taste identity predictions were devaluation sensitive while those involved in encoding predictions about spatial location were devaluation insensitive. These findings provide insights into the role of multiple associative mechanisms in the brain in mediating Pavlovian conditioned behavior - illustrating how distinct neural pathways can in parallel produce both devaluation sensitive and devaluation insensitive behaviors.