Reinstatement of cortical outcome representations during higher-order learning

Abstract

Naturalistic learning scenarios are characterized by infrequent experience of external feedback to guide behavior. Higher-order learning mechanisms like second-order conditioning (SOC) may allow stimuli that were never experienced together with reinforcement to acquire motivational value in such environments. Despite its explanatory potential for real-world learning phenomena, surprisingly little is known about the neural mechanism underlying such associative transfer of motivational value in SOC. Here, we used multivariate cross-session, cross-modality searchlight classification on functional magnetic resonance imaging data obtained from healthy humans during SOC. We show that visual first-order conditioned stimuli (CS) reinstate cortical patterns representing previously paired gustatory outcomes in the lateral orbitofrontal cortex (OFC). The same OFC region was found to increase functional coupling with amygdala, anterior hippocampus, and medial OFC during SOC. In the amygdala, neural pattern similarity specifically increased between second-order CS and outcomes from early to late stages of SOC. Our data suggest a mechanism by which value is conferred to stimuli that were never paired with reinforcement.