Reward modulation of medial temporal lobe function during associative encoding and cued recall

Emerging evidence suggests that hippocampal memory processing is modulated by midbrain regions under conditions of reward, resulting in enhanced encoding of episodic information—long-term memory for events. Current theories further suggest that hippocampal subregions may have distinct roles in episodic memory formation, and may be differentially influenced by dopaminergic midbrain inputs. Using high-resolution functional magnetic resonance imaging (fMRI), the present study investigated hippocampal subregional function as well as activation in surrounding medial temporal lobe (MTL) cortex, midbrain, and nucleus accumbens during associative encoding and cued recall under varying conditions of reward. A high-value or low-value monetary cue preceded a pair of objects indicating potential reward for successful retrieval of the association. At test, participants performed cued recall followed by match (correct association) or mismatch (incorrect association) probe decisions and received feedback on their performance. Behaviorally, cued recall performance was superior for pairs preceded by high reward cues at encoding relative to pairs preceded by low reward cues. FMRI analysis revealed regions within hippocampus, parahippocampal cortex, nucleus accumbens, and midbrain showing subsequent memory effects (greater encoding activation for remembered, compared to forgotten associations) and reward effects (greater activation for high-value, compared to low-value associations) during stimulus encoding. Within several of these regions, individual differences in reward-related encoding activation were correlated with the degree of the behavioral reward effect (better memory for high-value compared to low-value object pairs). At retrieval, regions in midbrain and subiculum predicted successful associative recall, and regions within hippocampus, parahippocampal cortex, nucleus accumbens, and midbrain showed reward effects in the absence of explicit reward cues. Within several MTL regions, activation was greater for match than mismatch probes. These findings are consistent with theories suggesting that reward-based motivation influences memory formation through interactions between dopaminergic midbrain and hippocampus.