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

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.

SUBMITTER: Aberg KC

PROVIDER: S-EPMC7156375 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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

Aberg Kristoffer Carl KC Kramer Emily Elizabeth EE Schwartz Sophie S

Nature communications 20200414 1

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), a ...[more]

PMID: 32286275

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Project description:Most cigarette smokers who wish to quit too often relapse within the first few days of abstinence, primarily due to the aversive aspects of the nicotine withdrawal syndrome (NWS), which remains poorly understood. Considerable research has suggested that the dorsal anterior cingulate cortex (dACC) plays a key role in nicotine dependence, with its functional connections between other brain regions altered as a function of trait addiction and state withdrawal. The flow of information between dACC and fronto-striatal regions is secured through different pathways, the vast majority of which are glutamatergic. As such, we investigated dACC activity using resting state functional connectivity (rsFC) with functional magnetic resonance imaging (fMRI) and glutamate (Glu) concentration with magnetic resonance spectroscopy (MRS). We also investigated the changes in adenosine levels in plasma during withdrawal as a surrogate for brain adenosine, which plays a role in fine-tuning synaptic glutamate transmission. Using a double-blind, placebo-controlled, randomized crossover design, nontreatment seeking smoking participants (N = 30) completed two imaging sessions, one while nicotine sated and another after 36 h nicotine abstinence. We observed reduced dACC Glu (P = 0.029) along with a significant reduction in plasma adenosine (P = 0.03) and adenosine monophosphate (AMP; P < 0.0001) concentrations during nicotine withdrawal in comparison with nicotine sated state. This withdrawal state manipulation also led to an increase in rsFC strength (P < 0.05) between dACC and several frontal cortical regions, including left superior frontal gyrus (LSFG), and right middle frontal gyrus (RMFG). Moreover, the state-trait changes in dACC Glu and rsFC strength between the dACC and both SFG and MFG were positively correlated (P = 0.012, and P = 0.007, respectively). Finally, the change in circuit strength between dACC and LSFG was negatively correlated with the change in withdrawal symptom manifestations as measured by the Wisconsin Smoking Withdrawal Scale (P = 0.04) and Tobacco Craving Questionnaire (P = 0.014). These multimodal imaging-behavioral findings reveal the complex cascade of changes induced by acute nicotine deprivation and call for further investigation into the potential utility of adenosine- and glutamate-signaling as novel therapeutic targets to treat the NWS.

Dataset Information

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

Publications

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

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