Interplay between midbrain and dorsal anterior cingulate regions arbitrates lingering reward effects on memory encoding

Kristoffer Carl Aberg,Sophie Schwartz,Emily Elizabeth Kramer

doi:10.1038/s41467-020-15542-z

Abstract

Rewarding events enhance memory encoding via dopaminergic influences on hippocampal plasticity. Phasic dopamine release depends on immediate reward magnitude, but presumably also on tonic dopamine levels, which may vary as a function of the average accumulation of reward over time. Using model-based fMRI in combination with a novel associative memory task, we show that immediate reward magnitude exerts a monotonically increasing influence on the nucleus accumbens, ventral tegmental area (VTA), and hippocampal activity during encoding, and enhances memory. By contrast, average reward levels modulate feedback-related responses in the VTA and hippocampus in a non-linear (inverted U-shape) fashion, with similar effects on memory performance. Additionally, the dorsal anterior cingulate cortex (dACC) monotonically tracks average reward levels, while VTA-dACC functional connectivity is non-linearly modulated (inverted U-shape) by average reward. We propose that the dACC computes the net behavioral impact of average reward and relays this information to memory circuitry via the VTA.

Highlights

Rewarding events enhance memory encoding via dopaminergic influences on hippocampal plasticity
It is currently unclear whether these effects of dopamine on memory formation relate to changes in ventral tegmental area (VTA) function and/or in other brain regions involved in memory formation and motivation, such as the HC and the nucleus accumbens (NAcc)
We predict that immediate reward magnitude and average reward levels during encoding engage brain regions involved in reward processing and motivation and memory formation, and account for variance in subsequently tested memory performance

Summary

Introduction

Rewarding events enhance memory encoding via dopaminergic influences on hippocampal plasticity. Reward-related information has priority in memory, as evidenced by studies reporting better memory for information presented in trials where a large reward was presented or anticipated (as compared with smaller or no reward)[1,2,3,4,5,6,7,8] Rewarding events, such as reward feedbacks or cues predictive of reward, initiate phasic dopamine release from the ventral tegmental area (VTA)[9,10], a midbrain region with dopaminergic projections to the hippocampus (HC). Increased levels of dopamine enhance memory encoding only up to a certain point, after which additional dopamine may become detrimental for memory encoding[27,28] It is currently unclear whether these effects of dopamine on memory formation relate to changes in VTA function and/or in other brain regions involved in memory formation and motivation, such as the HC and the nucleus accumbens (NAcc). Because the brain loci enabling a non-linear effect of dopamine on episodic memory formation are unclear, we make no specific predictions regarding a differential neuronal representation of linear versus nonlinear effects of immediate and average reward

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Conclusion