Abstract representation of prospective reward in the hippocampus

Abstract

Motivation enhances memory by increasing hippocampal engagement during encoding. However, whether such increased hippocampal activation reflects encoding of the value of highly rewarding events per se is less understood. Here, we tested in humans whether hippocampus represents abstract reward value, independent of perceptual content, using a monetary incentive encoding task with a novel manipulation. During functional MRI scanning, men and women studied object pairs, each preceded by a monetary reward cue indicating the amount of money they would receive if they successfully remembered the object pair at test. Reward cues varied on both the level of reward (penny, dime, and dollar) and visual form (picture or word) across trials to dissociate hippocampal responses to reward value from those reflecting the perceptual properties of the cues. Behaviorally, participants remembered pairs associated with the high reward (dollar) more often than pairs associated with lower rewards. Neural pattern similarity analysis revealed that hippocampal and parahippocampal cortex activation patterns discriminated between cues of different value irrespective of their visual form, and that hippocampal discrimination of value was most pronounced in participants who showed the greatest behavioral sensitivity to reward. Strikingly, hippocampal patterns were most distinct for reward cues that differed in value but had similar visual appearance, consistent with theoretical proposals of hippocampal pattern differentiation of competing representations. Our data illustrate how contextual representations within the hippocampus go beyond space and time to include information about the motivational salience of events, with hippocampal reward coding tracking the motivational impact on later memory. SIGNIFICANCE STATEMENT Motivation, such as the promise of future rewards, enhances hippocampal engagement during encoding and promotes successful retention of events associated with valuable rewards. However, whether the hippocampus explicitly encodes reward value, dissociable from sensory information, is unclear. Here, we show that the hippocampus forms abstract representation of valuable rewards, encoding conceptual rather than perceptual information about the motivational context of individual events. Reward representation within hippocampus is associated with preferential retention of high-value events in memory. Furthermore, we show that hippocampal pattern differentiation serves to emphasize differences between visually similar events with distinct motivational salience. Collectively, these findings indicate that hippocampal contextual representations allow individuals to distinguish the motivational value of events, leading to prioritized encoding of significant memories.

Publication
The Journal of Neuroscience