Parallel contributions of distinct human memory systems during probabilistic learning

Regions within the medial temporal lobe and basal ganglia are thought to subserve distinct memory systems underlying declarative and nondeclarative processes, respectively. One question of interest is how these multiple memory systems interact during learning to contribute to goal directed behavior. While some hypotheses suggest that regions such as the striatum and the hippocampus interact in a competitive manner, alternative views posit that these structures may operate in a parallel manner to facilitate learning. In the current experiment, we probed the functional connectivity between regions in the striatum and hippocampus in the human brain during an event related probabilistic learning task that varied with respect to type of difficulty (easy or hard cues) and type of learning (via feedback or observation). We hypothesized that the hippocampus and striatum would interact in a parallel manner during learning. We identified regions of interest (ROI) in the striatum and hippocampus that showed an effect of cue difficulty during learning and found that such ROIs displayed a similar pattern of blood oxygen level dependent (BOLD) responses, irrespective of learning type, and were functionally correlated as assessed by a Granger causality analysis. Given the connectivity of both structures with dopaminergic midbrain centers, we further applied a reinforcement learning algorithm often used to highlight the role of dopamine in human reward related learning paradigms. Activity in both the striatum and hippocampus positively correlated with a prediction error signal during feedback learning. These results suggest that distinct human memory systems operate in parallel during probabilistic learning, and may act synergistically particularly when a violation of expectation occurs, to jointly contribute to learning and decision making.