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Neural basis of reward anticipation and its genetic determinants.

ABSTRACT: Dysfunctional reward processing is implicated in various mental disorders, including attention deficit hyperactivity disorder (ADHD) and addictions. Such impairments might involve different components of the reward process, including brain activity during reward anticipation. We examined brain nodes engaged by reward anticipation in 1,544 adolescents and identified a network containing a core striatal node and cortical nodes facilitating outcome prediction and response preparation. Distinct nodes and functional connections were preferentially associated with either adolescent hyperactivity or alcohol consumption, thus conveying specificity of reward processing to clinically relevant behavior. We observed associations between the striatal node, hyperactivity, and the vacuolar protein sorting-associated protein 4A (VPS4A) gene in humans, and the causal role of Vps4 for hyperactivity was validated in Drosophila Our data provide a neurobehavioral model explaining the heterogeneity of reward-related behaviors and generate a hypothesis accounting for their enduring nature.

SUBMITTER: Jia T

PROVIDER: S-EPMC4833244 | biostudies-literature | 2016 Apr

REPOSITORIES: biostudies-literature

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Neural basis of reward anticipation and its genetic determinants.

Jia Tianye T Macare Christine C Desrivières Sylvane S Gonzalez Dante A DA Tao Chenyang C Ji Xiaoxi X Ruggeri Barbara B Nees Frauke F Banaschewski Tobias T Barker Gareth J GJ Bokde Arun L W AL Bromberg Uli U Büchel Christian C Conrod Patricia J PJ Dove Rachel R Frouin Vincent V Gallinat Jürgen J Garavan Hugh H Gowland Penny A PA Heinz Andreas A Ittermann Bernd B Lathrop Mark M Lemaitre Hervé H Martinot Jean-Luc JL Paus Tomáš T Pausova Zdenka Z Poline Jean-Baptiste JB Rietschel Marcella M Robbins Trevor T Smolka Michael N MN Müller Christian P CP Feng Jianfeng J Rothenfluh Adrian A Flor Herta H Schumann Gunter G

Proceedings of the National Academy of Sciences of the United States of America 20160321 14

Dysfunctional reward processing is implicated in various mental disorders, including attention deficit hyperactivity disorder (ADHD) and addictions. Such impairments might involve different components of the reward process, including brain activity during reward anticipation. We examined brain nodes engaged by reward anticipation in 1,544 adolescents and identified a network containing a core striatal node and cortical nodes facilitating outcome prediction and response preparation. Distinct node ...[more]

PMID: 27001827

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Project description:Background: Microorganisms in the human intestine (i.e. the gut microbiome) have an increasingly recognized impact on human health, including brain functioning. Attention-deficit/hyperactivity disorder (ADHD) is a neurodevelopmental disorder associated with abnormalities in dopamine neurotransmission and deficits in reward processing and its underlying neuro-circuitry including the ventral striatum. The microbiome might contribute to ADHD etiology via the gut-brain axis. In this pilot study, we investigated potential differences in the microbiome between ADHD cases and undiagnosed controls, as well as its relation to neural reward processing.Methods: We used 16S rRNA marker gene sequencing (16S) to identify bacterial taxa and their predicted gene functions in 19 ADHD and 77 control participants. Using functional magnetic resonance imaging (fMRI), we interrogated the effect of observed microbiome differences in neural reward responses in a subset of 28 participants, independent of diagnosis.Results: For the first time, we describe gut microbial makeup of adolescents and adults diagnosed with ADHD. We found that the relative abundance of several bacterial taxa differed between cases and controls, albeit marginally significant. A nominal increase in the Bifidobacterium genus was observed in ADHD cases. In a hypothesis-driven approach, we found that the observed increase was linked to significantly enhanced 16S-based predicted bacterial gene functionality encoding cyclohexadienyl dehydratase in cases relative to controls. This enzyme is involved in the synthesis of phenylalanine, a precursor of dopamine. Increased relative abundance of this functionality was significantly associated with decreased ventral striatal fMRI responses during reward anticipation, independent of ADHD diagnosis and age.Conclusions: Our results show increases in gut microbiome predicted function of dopamine precursor synthesis between ADHD cases and controls. This increase in microbiome function relates to decreased neural responses to reward anticipation. Decreased neural reward anticipation constitutes one of the hallmarks of ADHD.

Dataset Information

Neural basis of reward anticipation and its genetic determinants.

Publications

Neural basis of reward anticipation and its genetic determinants.

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