Positive reward prediction errors strengthen incidental memory encoding

Abstract

The dopamine system is thought to provide a reward prediction error signal that facilitates reinforcement learning and reward-based choice in corticostriatal circuits. While it is believed that similar prediction error signals are also provided to temporal lobe memory systems, the impact of such signals on episodic memory encoding has not been fully characterized. Here we develop an incidental memory paradigm that allows us to 1) estimate the influence of reward prediction errors on the formation of episodic memories, 2) dissociate this influence from other factors such as surprise and uncertainty, 3) test the degree to which this influence depends on temporal correspondence between prediction error and memoranda presentation, and 4) determine the extent to which this influence is consolidation-dependent. We find that when choosing to gamble for potential rewards during a primary decision making task, people encode incidental memoranda more strongly even though they are not aware that their memory will be subsequently probed. Moreover, this strengthened encoding scales with the reward prediction error, and not overall reward, experienced selectively at the time of memoranda presentation (and not before or after). Finally, this strengthened encoding is identifiable within a few minutes and is not substantially enhanced after twenty-four hours, indicating that it is not consolidation-dependent. These results suggest a computationally and temporally specific role for putative dopaminergic reward prediction error signaling in memory formation.