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Influences of Age, Sex, and Moderate Alcohol Drinking on the Intrinsic Functional Architecture of Adolescent Brains.

ABSTRACT: The transition from adolescent to adult cognition and emotional control requires neurodevelopmental maturation likely involving intrinsic functional networks (IFNs). Normal neurodevelopment may be vulnerable to disruption from environmental insult such as alcohol consumption commonly initiated during adolescence. To test potential disruption to IFN maturation, we used resting-state functional magnetic resonance imaging (rs-fMRI) in 581 no-to-low alcohol-consuming and 117 moderate-to-high-drinking youth. Functional seed-to-voxel connectivity analysis assessed age, sex, and moderate alcohol drinking on default-mode, executive-control, salience, reward, and emotion networks and tested cognitive and motor coordination correlates of network connectivity. Among no-to-low alcohol-consuming adolescents, executive-control frontolimbicstriatal connectivity was stronger in older than younger adolescents, particularly boys, and predicted better ability in balance, memory, and impulse control. Connectivity patterns in moderate-to-high-drinking youth were tested mainly in late adolescence when drinking was initiated. Implicated was the emotion network with attenuated connectivity to default-mode network regions. Our cross-sectional rs-fMRI findings from this large cohort of adolescents show sexual dimorphism in connectivity and suggest neurodevelopmental rewiring toward stronger and spatially more distributed executive-control networking in older than younger adolescents. Functional network rewiring in moderate-to-high-drinking adolescents may impede maturation of affective and self-reflection systems and obscure maturation of complex social and emotional behaviors.

SUBMITTER: Muller-Oehring EM

PROVIDER: S-EPMC6059181 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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Influences of Age, Sex, and Moderate Alcohol Drinking on the Intrinsic Functional Architecture of Adolescent Brains.

Müller-Oehring Eva M EM Kwon Dongjin D Nagel Bonnie J BJ Sullivan Edith V EV Chu Weiwei W Rohlfing Torsten T Prouty Devin D Nichols B Nolan BN Poline Jean-Baptiste JB Tapert Susan F SF Brown Sandra A SA Cummins Kevin K Brumback Ty T Colrain Ian M IM Baker Fiona C FC De Bellis Michael D MD Voyvodic James T JT Clark Duncan B DB Pfefferbaum Adolf A Pohl Kilian M KM

Cerebral cortex (New York, N.Y. : 1991) 20180301 3

The transition from adolescent to adult cognition and emotional control requires neurodevelopmental maturation likely involving intrinsic functional networks (IFNs). Normal neurodevelopment may be vulnerable to disruption from environmental insult such as alcohol consumption commonly initiated during adolescence. To test potential disruption to IFN maturation, we used resting-state functional magnetic resonance imaging (rs-fMRI) in 581 no-to-low alcohol-consuming and 117 moderate-to-high-drinkin ...[more]

PMID: 28168274

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Project description:Importance:Studies examining the association of low to moderate drinking with various cognitive functions have yielded mixed findings. Objective:To investigate whether associations exist between low to moderate alcohol drinking and cognitive function trajectories or rates of change in cognitive function from middle age to older age among US adults. Design, Setting, and Participants:A prospective cohort study of participants drawn from the Health and Retirement Study (HRS), a nationally representative sample of US adults, with mean (SD) follow-up of 9.1 (3.1) years. In total, 19?887 participants who had their cognitive functions measured in the HRS starting in 1996 through 2008 and who had participated in at least 3 biennial surveys were included. The data analysis was conducted from June to November 2019. Exposures:Alcohol consumption and aging. Main Outcomes and Measures:Trajectories and annual rates of change for the cognitive domains of mental status, word recall, and vocabulary and for the total cognitive score, which was the sum of the mental status and word recall scores. Participants were clustered into 2 cognitive function trajectories for each cognition measure assessed based on their scores at baseline and through at least 3 biennial surveys: a consistently low trajectory (representing low cognitive scores throughout the study period) and a consistently high trajectory (representing high cognitive scores throughout the study period). Results:The mean (SD) age of 19?887 participants was 61.8 (10.2) years, and the majority of the HRS participants were women (11?943 [60.1%]) and of white race/ethnicity (16?950 [85.2%]). Low to moderate drinking (<8 drinks per week for women and <15 drinks per week for men) was significantly associated with a consistently high cognitive function trajectory and a lower rate of cognitive decline. Compared with never drinkers, low to moderate drinkers were less likely to have a consistently low trajectory for total cognitive function (odds ratio [OR], 0.66; 95% CI, 0.59-0.74), mental status (OR, 0.71; 95% CI, 0.63-0.81), word recall (OR, 0.74; 95% CI, 0.69-0.80), and vocabulary (OR, 0.64; 95% CI, 0.56-0.74) (all P?<?.001). In addition, low to moderate drinking was associated with decreased annual rates of total cognitive function decline (? coefficient, 0.04; 95% CI, 0.02-0.07; P?=?.002), mental status (? coefficient, 0.02; 95% CI, 0.01-0.03; P?=?.002), word recall (? coefficient, 0.02; 95% CI, 0.01-0.04; P?=?.01), and vocabulary (? coefficient, 0.01; 95% CI, 0.00-0.03; P?=?.08). A significant racial/ethnic difference was observed for trajectories of mental status (P?=?.02 for interaction), in which low to moderate drinking was associated with lower odds of having a consistently low trajectory for white participants (OR, 0.65; 95% CI, 0.56-0.75) but not for black participants (OR, 1.02; 95% CI, 0.74-1.39). Finally, the dosage of alcohol consumed had a U-shaped association with all cognitive function domains for all participants, with an optimal dose of 10 to 14 drinks per week. Conclusions and relevance:These findings suggested that low to moderate alcohol drinking was associated with better global cognition scores, and these associations appeared stronger for white participants than for black participants. Studies examining the mechanisms underlying the association between alcohol drinking and cognition in middle-aged or older adults are needed.

Project description:The objective of this study was to determine changes in gene expression within the extended amygdala following binge-like alcohol drinking by adolescent alcohol-preferring (P) rats. Starting at 28 days of age, P rats were given concurrent access to 15 and 30 % ethanol for 3 one-h sessions for 5 consecutive days each week until they were 49 days old. Rats were killed by decapitation 3 h after the first ethanol access session on the 15th day of drinking. RNA was prepared from micropunch samples of the nucleus accumbens shell (Acb-sh) and central nucleus of the amygdala (CeA). Ethanol intakes were 2.5 to 3.0 g/kg/session. There were 154 and 182 unique named genes that significantly differed (FDR = 0.2) between the water and ethanol group in the Acb-sh and CeA, respectively. Gene Ontology (GO) analyses indicated that adolescent binge drinking produced changes in the in biological processes involved in cell proliferation and regulation of cellular structure in the Acb-sh, and in neuron projection and positive regulation of cellular organization in the CeA. Ingenuity Pathway Analysis indicated that, in the Acb-sh, there were several major intracellular signaling pathways (e.g., cAMP-mediated and protein kinase A signaling pathways) altered by adolescent drinking, with 3-fold more genes up-regulated than down-regulated in the alcohol group. The cAMP-mediated signaling system was also up-regulated in the CeA of the alcohol group. Weighted gene co-expression network analysis (WGCNA) indicated significant G-protein coupled receptor signaling and transmembrane receptor protein kinase signaling categories in the Acb-sh and CeA, respectively. Overall, the results of this study indicated that binge-like alcohol drinking by adolescent P rats is differentially altering the expression of genes in the Acb-sh and CeA, some of which are involved in intracellular signaling pathways and may produce long-term changes in neuronal function. Differences in gene expression in the central nucleus of the amygdala (CeA) were compared in two groups of alcohol-preferring (P) rats, one given water only and the other given access to 15 & 30% ethanol during adolescence.

Project description:The objective of this study was to determine changes in gene expression within the extended amygdala following binge-like alcohol drinking by adolescent alcohol-preferring (P) rats. Starting at 28 days of age, P rats were given concurrent access to 15 and 30 % ethanol for 3 one-h sessions for 5 consecutive days each week until they were 49 days old. Rats were killed by decapitation 3 h after the first ethanol access session on the 15th day of drinking. RNA was prepared from micropunch samples of the nucleus accumbens shell (Acb-sh) and central nucleus of the amygdala (CeA). Ethanol intakes were 2.5 ‚Äì 3.0 g/kg/session. There were 154 and 182 unique named genes that significantly differed (FDR = 0.2) between the water and ethanol group in the Acb-sh and CeA, respectively. Gene Ontology (GO) analyses indicated that adolescent binge drinking produced changes in the in biological processes involved in cell proliferation and regulation of cellular structure in the Acb-sh, and in neuron projection and positive regulation of cellular organization in the CeA. Ingenuity Pathway Analysis indicated that, in the Acb-sh, there were several major intracellular signaling pathways (e.g., cAMP-mediated and protein kinase A signaling pathways) altered by adolescent drinking, with 3-fold more genes up-regulated than down-regulated in the alcohol group. The cAMP-mediated signaling system was also up-regulated in the CeA of the alcohol group. Weighted gene co-expression network analysis (WGCNA) indicated significant G-protein coupled receptor signaling and transmembrane receptor protein kinase signaling categories in the Acb-sh and CeA, respectively. Overall, the results of this study indicated that binge-like alcohol drinking by adolescent P rats is differentially altering the expression of genes in the Acb-sh and CeA, some of which are involved in intracellular signaling pathways and may produce long-term changes in neuronal function. Differences in gene expression in brain nucleus accumbens shell (Acb-sh) were compared in two groups of alcohol-preferring (P) rats, one given water only and the other given access to 15 & 30% ethanol during adolescence.

Dataset Information

Influences of Age, Sex, and Moderate Alcohol Drinking on the Intrinsic Functional Architecture of Adolescent Brains.

Publications

Influences of Age, Sex, and Moderate Alcohol Drinking on the Intrinsic Functional Architecture of Adolescent Brains.

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