Association of Gray Matter and Personality Development With Increased Drunkenness Frequency During Adolescence

TY - JOUR

T1 - Association of Gray Matter and Personality Development With Increased Drunkenness Frequency During Adolescence

AU - Robert, Gabriel H

AU - Luo, Qiang

AU - Yu, Tao

AU - Chu, Congying

AU - Ing, Alex

AU - Jia, Tianye

AU - Papadopoulos Orfanos, Dimitri

AU - Burke-Quinlan, Erin

AU - Desrivières, Sylvane

AU - Ruggeri, Barbara

AU - Spechler, Philip

AU - Chaarani, Bader

AU - Tay, Nicole

AU - Banaschewski, Tobias

AU - Bokde, Arun L W

AU - Bromberg, Uli

AU - Flor, Herta

AU - Frouin, Vincent

AU - Gowland, Penny

AU - Heinz, Andreas

AU - Ittermann, Bernd

AU - Martinot, Jean-Luc

AU - Paillère Martinot, Marie-Laure

AU - Nees, Frauke

AU - Poustka, Luise

AU - Smolka, Michael N

AU - Vetter, Nora C

AU - Walter, Henrik

AU - Whelan, Robert

AU - Conrod, Patricia

AU - Barker, Ted

AU - Garavan, Hugh

AU - Schumann, Gunter

AU - IMAGEN Consortium

PY - 2020/4/1

Y1 - 2020/4/1

N2 - Importance: Alcohol abuse correlates with gray matter development in adolescents, but the directionality of this association remains unknown.Objective: To investigate the directionality of the association between gray matter development and increase in frequency of drunkenness among adolescents.Design, Setting, and Participants: This cohort study analyzed participants of IMAGEN, a multicenter brain imaging study of healthy adolescents in 8 European sites in Germany (Mannheim, Dresden, Berlin, and Hamburg), the United Kingdom (London and Nottingham), Ireland (Dublin), and France (Paris). Data from the second follow-up used in the present study were acquired from January 1, 2013, to December 31, 2016, and these data were analyzed from January 1, 2016, to March 31, 2018. Analyses were controlled for sex, site, socioeconomic status, family history of alcohol dependency, puberty score, negative life events, personality, cognition, and polygenic risk scores. Personality and frequency of drunkenness were assessed at age 14 years (baseline), 16 years (first follow-up), and 19 years (second follow-up). Structural brain imaging scans were acquired at baseline and second follow-up time points.Main Outcomes and Measures: Increases in drunkenness frequency were measured by latent growth modeling, a voxelwise hierarchical linear model was used to observe gray matter volume, and tensor-based morphometry was used for gray matter development. The hypotheses were formulated before the data analyses.Results: A total of 726 adolescents (mean [SD] age at baseline, 14.4 [0.38] years; 418 [58%] female) were included. The increase in drunkenness frequency was associated with accelerated gray matter atrophy in the left posterior temporal cortex (peak: t1,710 = -5.8; familywise error (FWE)-corrected P = 7.2 × 10-5; cluster: 6297 voxels; P = 2.7 × 10-5), right posterior temporal cortex (cluster: 2070 voxels; FWE-corrected P = .01), and left prefrontal cortex (peak: t1,710 = -5.2; FWE-corrected P = 2 × 10-3; cluster: 10 624 voxels; P = 1.9 × 10-7). According to causal bayesian network analyses, 73% of the networks showed directionality from gray matter development to drunkenness increase as confirmed by accelerated gray matter atrophy in late bingers compared with sober controls (n = 20 vs 60; β = 1.25; 95% CI, -2.15 to -0.46; t1,70 = 0.3; P = .004), the association of drunkenness increase with gray matter volume at age 14 years (β = 0.23; 95% CI, 0.01-0.46; t1,584 = 2; P = .04), the association between gray matter atrophy and alcohol drinking units (β = -0.0033; 95% CI, -6 × 10-3 to -5 × 10-4; t1,509 = -2.4; P = .02) and drunkenness frequency at age 23 years (β = -0.16; 95% CI, -0.28 to -0.03; t1,533 = -2.5; P = .01), and the linear exposure-response curve stratified by gray matter atrophy and not by increase in frequency of drunkenness.Conclusions and Relevance: This study found that gray matter development and impulsivity were associated with increased frequency of drunkenness by sex. These results suggest that neurotoxicity-related gray matter atrophy should be interpreted with caution.

AB - Importance: Alcohol abuse correlates with gray matter development in adolescents, but the directionality of this association remains unknown.Objective: To investigate the directionality of the association between gray matter development and increase in frequency of drunkenness among adolescents.Design, Setting, and Participants: This cohort study analyzed participants of IMAGEN, a multicenter brain imaging study of healthy adolescents in 8 European sites in Germany (Mannheim, Dresden, Berlin, and Hamburg), the United Kingdom (London and Nottingham), Ireland (Dublin), and France (Paris). Data from the second follow-up used in the present study were acquired from January 1, 2013, to December 31, 2016, and these data were analyzed from January 1, 2016, to March 31, 2018. Analyses were controlled for sex, site, socioeconomic status, family history of alcohol dependency, puberty score, negative life events, personality, cognition, and polygenic risk scores. Personality and frequency of drunkenness were assessed at age 14 years (baseline), 16 years (first follow-up), and 19 years (second follow-up). Structural brain imaging scans were acquired at baseline and second follow-up time points.Main Outcomes and Measures: Increases in drunkenness frequency were measured by latent growth modeling, a voxelwise hierarchical linear model was used to observe gray matter volume, and tensor-based morphometry was used for gray matter development. The hypotheses were formulated before the data analyses.Results: A total of 726 adolescents (mean [SD] age at baseline, 14.4 [0.38] years; 418 [58%] female) were included. The increase in drunkenness frequency was associated with accelerated gray matter atrophy in the left posterior temporal cortex (peak: t1,710 = -5.8; familywise error (FWE)-corrected P = 7.2 × 10-5; cluster: 6297 voxels; P = 2.7 × 10-5), right posterior temporal cortex (cluster: 2070 voxels; FWE-corrected P = .01), and left prefrontal cortex (peak: t1,710 = -5.2; FWE-corrected P = 2 × 10-3; cluster: 10 624 voxels; P = 1.9 × 10-7). According to causal bayesian network analyses, 73% of the networks showed directionality from gray matter development to drunkenness increase as confirmed by accelerated gray matter atrophy in late bingers compared with sober controls (n = 20 vs 60; β = 1.25; 95% CI, -2.15 to -0.46; t1,70 = 0.3; P = .004), the association of drunkenness increase with gray matter volume at age 14 years (β = 0.23; 95% CI, 0.01-0.46; t1,584 = 2; P = .04), the association between gray matter atrophy and alcohol drinking units (β = -0.0033; 95% CI, -6 × 10-3 to -5 × 10-4; t1,509 = -2.4; P = .02) and drunkenness frequency at age 23 years (β = -0.16; 95% CI, -0.28 to -0.03; t1,533 = -2.5; P = .01), and the linear exposure-response curve stratified by gray matter atrophy and not by increase in frequency of drunkenness.Conclusions and Relevance: This study found that gray matter development and impulsivity were associated with increased frequency of drunkenness by sex. These results suggest that neurotoxicity-related gray matter atrophy should be interpreted with caution.

KW - Adolescent

KW - Adolescent Development

KW - Alcoholic Intoxication/epidemiology

KW - Female

KW - Frontal Lobe/growth & development

KW - Gray Matter/growth & development

KW - Humans

KW - Impulsive Behavior

KW - Male

KW - Personality Development

KW - Risk Factors

KW - Sex Factors

KW - Temporal Lobe/growth & development

KW - Young Adult

U2 - 10.1001/jamapsychiatry.2019.4063

DO - 10.1001/jamapsychiatry.2019.4063

M3 - SCORING: Journal article

C2 - 31851304

VL - 77

SP - 409

EP - 419

JO - JAMA PSYCHIAT

JF - JAMA PSYCHIAT

SN - 2168-622X

IS - 4

ER -