Stimulus-outcome learnability differentially activates anterior cingulate and hippocampus at feedback processing

Abstract

Memory systems are known to be influenced by feedback and error processing, but it is not well known what aspects of outcome contingencies are related to different memory systems. Here we use the Rescorla-Wagner model to estimate prediction errors in an fMRI study of stimulus-outcome association learning. The conditional probabilities of outcomes for a given stimulus are manipulated so that associations are either learnable or unlearnable (pseudorandom). The delay between stimulus and outcome is jittered so that we can separately compare activity for either stimulus processing or feedback processing. We find that hippocampus and anterior cingulate are differentially active primarily at feedback processing: Learnable associations are correlated with significantly more hippocampal activity and significantly less anterior cingulate activity than unlearnable associations. We also find that positive prediction errors modulate feedback processing in the midbrain for both types of associations. We suggest that learnable associations use more declarative memory, unlearnable associations involve more uncertainty monitoring, and, in both kinds of associations, positive prediction errors provide a reinforcement signal. © 2009 Cold Spring Harbor Laboratory Press.