Dissociating hippocampal and striatal contributions to sequential prediction learning

Behavior may be generated on the basis of many different kinds of learned contingencies. For instance, responses could be guided by the direct association between a stimulus and response, or by sequential stimulus-stimulus relationships (as in model-based reinforcement learning or goal-directed actions). However, the neural architecture underlying sequential predictive learning is not well understood, in part because it is difficult to isolate its effect on choice behavior. To track such learning more directly, we examined reaction times (RTs) in a probabilistic sequential picture identification task in healthy individuals. We used computational learning models to isolate trial-by-trial effects of two distinct learning processes in behavior, and used these as signatures to analyse the separate neural substrates of each process. RTs were best explained via the combination of two delta rule learning processes with different learning rates. To examine neural manifestations of these learning processes, we used functional magnetic resonance imaging to seek correlates of time-series related to expectancy or surprise. We observed such correlates in two regions, hippocampus and striatum. By estimating the learning rates best explaining each signal, we verified that they were uniquely associated with one of the two distinct processes identified behaviorally. These differential correlates suggest that complementary anticipatory functions drive each region's effect on behavior. Our results provide novel insights as to the quantitative computational distinctions between medial temporal and basal ganglia learning networks and enable experiments that exploit trial-by-trial measurement of the unique contributions of both hippocampus and striatum to response behavior.