The effect of reward-based motivation on associative memory processing in the medial temporal lobes

Abstract

What determines whether an experience is encoded to memory? One factor is reward-based motivation: we are more likely to remember information if we believe it will lead to future rewards. Memory critically depends on the integrity of the medial temporal lobes (MTL). Notably, the MTL is comprised of subregions that are hypothesized to serve different functions in memory and may be differentially influenced by reward. The present research examines how reward-based motivation influences associative memory processing within MTL subregions of the human brain. In two high-resolution functional magnetic resonance imaging (fMRI) studies, a high-value or low-value monetary cue preceded a pair of objects indicating potential reward for successful retrieval of the association on a later memory test. Memory was enhanced for pairs preceded by high-value compared to low-value reward cues, however participants differed in the degree to which reward value influenced memory. In fMRI Study 1, the behavioral effect of reward on memory was associated with reward-related activation changes in hippocampal subregions dentate gyrus/CA₂,₃ and enhanced connectivity between dentate gyrus/CA₂,₃ and reward-related midbrain regions during encoding and retrieval. In fMRI Study 2, patterns of MTL activations represented reward context, showing greater consistency among events of the same reward value than among events of different reward values. Successful memory formation was associated with enhanced hippocampal reward representations during the anticipatory cue phase prior to object pair encoding. During object pair encoding, the degree of reward representation in hippocampus and more specifically dentate gyrus/CA₂,₃ was associated with individual differences in the behavioral effect of reward on memory. Finally, a series of behavioral studies demonstrate that during motivated learning, associative memory accuracy increases monotonically with increasing reward value, and may be enhanced when participants must maintain information about reward cues in short-term memory prior to encoding. These findings indicate that reward-based motivation enhances associative memory processing specifically within dentate gyrus/CA₂,₃ through interactions with reward-related midbrain regions. Furthermore, these results suggest that associative memory may be facilitated when information about reward context is incorporated into stored memory representations. Collectively, these findings shed light on fundamental mechanisms through which reward impacts associative memory.