Reward Modulation of Hippocampal Subfield Activation during Successful Associative Encoding and Retrieval

Emerging evidence suggests that motivation enhances episodic memory formation through interactions between medial-temporal lobe (MTL) structures and dopaminergic midbrain. In addition, recent theories propose that motivation specifically facilitates hippocampal associative binding processes, resulting in more detailed memories that are readily reinstated from partial input. Here, we used high-resolution fMRI to determine how motivation influences associative encoding and retrieval processes within human MTL subregions and dopaminergic midbrain. Participants intentionally encoded object associations under varying conditions of reward and performed a retrieval task during which studied associations were cued from partial input. Behaviorally, cued recall performance was superior for high-value relative to low-value associations; however, participants differed in the degree to which rewards influenced memory. The magnitude of behavioral reward modulation was associated with reward-related activation changes in dentate gyrus/CA(2,3) during encoding and enhanced functional connectivity between dentate gyrus/CA(2,3) and dopaminergic midbrain during both the encoding and retrieval phases of the task. These findings suggests that, within the hippocampus, reward-based motivation specifically enhances dentate gyrus/CA(2,3) associative encoding mechanisms through interactions with dopaminergic midbrain. Furthermore, within parahippocampal cortex and dopaminergic midbrain regions, activation associated with successful memory formation was modulated by reward across the group. During the retrieval phase, we also observed enhanced activation in hippocampus and dopaminergic midbrain for high-value associations that occurred in the absence of any explicit cues to reward. Collectively, these findings shed light on fundamental mechanisms through which reward impacts associative memory formation and retrieval through facilitation of MTL and ventral tegmental area/substantia nigra processing.