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Accelerated alcohol use across adolescence predicts early adult symptoms of alcohol use disorder via reward-related neural function

Published online by Cambridge University Press:  06 June 2018

Rebecca Waller Open the ORCID record for Rebecca Waller [Opens in a new window] ,
Laura Murray ,
Daniel S. Shaw ,
Erika E. Forbes  and
Luke W. Hyde
Rebecca Waller
Affiliation:
Department of Psychology, University of Michigan, Ann Arbor, USA Department of Psychiatry, University of Michigan, Ann Arbor, USA
Laura Murray
Affiliation:
Department of Psychology, University of Michigan, Ann Arbor, USA
Daniel S. Shaw
Affiliation:
Department of Psychology, University of Pittsburgh, Pittsburgh, USA Center for the Neural Basis of Cognition, University of Pittsburgh, USA
Erika E. Forbes
Affiliation:
Department of Psychology, University of Pittsburgh, Pittsburgh, USA Center for the Neural Basis of Cognition, University of Pittsburgh, USA Department of Psychiatry, University of Pittsburgh Medical Center, Pittsburgh, USA
Luke W. Hyde*
Affiliation:
Department of Psychology, University of Michigan, Ann Arbor, USA Center for Human Growth and Development, University of Michigan, Ann Arbor, USA Survey Research Center of the Institute for Social Research, University of Michigan, Ann Arbor, USA
*
Author for correspondence: Luke W. Hyde, E-mail: lukehyde@umich.edu
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Abstract

Background

Alcohol use is commonly initiated during adolescence, with earlier onset known to increase the risk for alcohol use disorder (AUD). Altered function in neural reward circuitry is thought to increase the risk for AUD. To test the hypothesis that adolescent alcohol misuse primes the brain for alcohol-related psychopathology in early adulthood, we examined whether adolescent alcohol consumption rates predicted reward responsivity in the ventral striatum (VS), and in turn, AUD symptoms in adulthood.

Methods

A total of 139 low income, racially diverse urban males reported on their alcohol use at ages 11, 12, 15, and 17; completed self-reports of personality, psychiatric interviews, and a functional magnetic resonance imaging (fMRI) scan at age 20; and completed a psychiatric interview at age 22. We measured adolescent alcohol use trajectories using latent growth curve modeling and measured neural responses to monetary reward using a VS region of interest. We tested indirect effects of adolescent alcohol use on AUD symptoms at age 22 via VS reward-related reactivity at age 20.

Results

Greater acceleration in adolescent alcohol use predicted increased VS response during reward anticipation at age 20. VS reactivity to reward anticipation at age 20 predicted AUD symptoms at age 22, over and above concurrent symptoms. Accelerated adolescent alcohol use predicted AUD symptoms in early adulthood via greater VS reactivity to reward anticipation.

Conclusions

Prospective findings support a pathway through which adolescent alcohol use increases the risk for AUD in early adulthood by impacting reward-related neural functioning. These results highlight increased VS reward-related reactivity as a biomarker for AUD vulnerability.

Keywords

Adolescencealcohol use disorderfMRIprospectiverewardtrajectory
Type
Original Articles
Information
Psychological Medicine , Volume 49 , Issue 4 , March 2019 , pp. 675 - 684
Copyright
Copyright © Cambridge University Press 2018 

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References

Aharoni, E, Vincent, GM, Harenski, CL, Calhoun, VD, Sinnott-Armstrong, W, Gazzaniga, MS and Kiehl, KA (2013) Neuroprediction of future rearrest. Proceedings of the National Academy of Sciences 110, 6223–6228.Google Scholar
Association, AP (2000) Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition (DSM-IV). Washington, DC: American Psychiatric Association.Google Scholar
Association, AP (2013) Diagnostic and Statistical Manual of Mental Disorders (DSM-5®). Washington, DC: American Psychiatric Association.Google Scholar
Beck, A, Schlagenhauf, F, Wüstenberg, T, Hein, J, Kienast, T, Kahnt, T, Schmack, K, Hägele, C, Knutson, B and Heinz, A (2009) Ventral striatal activation during reward anticipation correlates with impulsivity in alcoholics. Biological Psychiatry 66, 734–742.Google Scholar
Becker, A, Kirsch, M, Gerchen, MF, Kiefer, F and Kirsch, P (2017) Striatal activation and frontostriatal connectivity during non-drug reward anticipation in alcohol dependence. Addiction Biology 22, 833–843.Google Scholar
Bush, K, Kivlahan, DR, McDonell, MB, Fihn, SD and Bradley, KA (1998) The AUDIT alcohol consumption questions (AUDIT-C): an effective brief screening test for problem drinking. Archives of Internal Medicine 158, 1789–1795.Google Scholar
Cahalan, D, Cisin, I and Crossley, H (1969) American Drinking Practices. New Brunswick, NJ: Center of Alcohol Studies, Rutgers University.Google Scholar
Casey, B and Jones, RM (2010) Neurobiology of the adolescent brain and behavior: implications for substance use disorders. Journal of the American Academy of Child & Adolescent Psychiatry 49, 1189–1201.Google Scholar
Casey, BJ, Jones, RM and Somerville, LH (2011) Braking and accelerating of the adolescent brain. Journal of Research on Adolescence 21, 21–33.Google Scholar
Chassin, L, Flora, DB and King, KM (2004) Trajectories of alcohol and drug use and dependence from adolescence to adulthood: the effects of familial alcoholism and personality. Journal of Abnormal Psychology 113, 483–498.Google Scholar
Cohen, MX, Young, J, Baek, J-M, Kessler, C and Ranganath, C (2005) Individual differences in extraversion and dopamine genetics predict neural reward responses. Cognitive Brain Research 25, 851–861.Google Scholar
Compton, WM, Conway, KP, Stinson, FS, Colliver, JD and Grant, BF (2005) Prevalence, correlates, and comorbidity of DSM-IV antisocial personality syndromes and alcohol and specific drug use disorders in the United States: results from the national epidemiologic survey on alcohol and related conditions. The Journal of Clinical Psychiatry 66, 677–685.Google Scholar
Conrod, PJ and Nikolaou, K (2016) Annual research review: on the developmental neuropsychology of substance use disorders. Journal of Child Psychology and Psychiatry 57, 371–394.Google Scholar
Costa, PT and McCrae, RR (1997) Stability and change in personality assessment: the revised NEO personality inventory in the year 2000. Journal of Personality Assessment 68, 86–94.Google Scholar
Deserno, L, Beck, A, Huys, QJ, Lorenz, RC, Buchert, R, Buchholz, HG, Plotkin, M, Kumakara, Y, Cumming, P and Heinze, HJ (2015) Chronic alcohol intake abolishes the relationship between dopamine synthesis capacity and learning signals in the ventral striatum. European Journal of Neuroscience 41, 477–486.Google Scholar
Dienes, Z and Mclatchie, N (2018) Four reasons to prefer Bayesian analyses over significance testing. Psychonomic Bulletin & Review 25, 207–218.Google Scholar
Doremus-Fitzwater, TL, Varlinskaya, EI and Spear, LP (2010) Motivational systems in adolescence: possible implications for age differences in substance abuse and other risk-taking behaviors. Brain and Cognition 72, 114–123.Google Scholar
Duncan, TE and Duncan, SC (1995) Modeling the processes of development via latent variable growth curve methodology. Structural Equation Modeling: A Multidisciplinary Journal 2, 187–213.Google Scholar
Duncan, TE, Duncan, SC and Hops, H (1994) The effects of family cohesiveness and peer encouragement on the development of adolescent alcohol use: a cohort-sequential approach to the analysis of longitudinal data. Journal of Studies on Alcohol 55, 588–599.Google Scholar
Elliott, DS, Huizinga, D and Menard, S (2012) Multiple Problem Youth: Delinquency, Substance use, and Mental Health Problems. Springer Science & Business Media, New York, NY, USA.Google Scholar
Ewing, SWF, Sakhardande, A and Blakemore, S-J (2014) The effect of alcohol consumption on the adolescent brain: a systematic review of MRI and fMRI studies of alcohol-using youth. NeuroImage: Clinical 5, 420–437.Google Scholar
First, MB, Gibbon, M, Spitzer, RL, Benjamin, LS and Williams, JB (1997) Structured Clinical Interview for DSM-IV Axis II Personality Disorders: SCID-II. American Psychiatric Press, Washington, DC.Google Scholar
First, MB, Spitzer, RL, Gibbon, M and Williams, JB (1995) Structured Clinical Interview for DSM-IV Axis I Disorders. New York: New York State Psychiatric Institute.Google Scholar
Forbes, EE, Rodriguez, EE, Musselman, S and Narendran, R (2014) Prefrontal response and frontostriatal functional connectivity to monetary reward in abstinent alcohol-dependent young adults. PLoS ONE 9, e94640.Google Scholar
Goddings, A-L, Mills, KL, Clasen, LS, Giedd, JN, Viner, RM and Blakemore, S-J (2014) The influence of puberty on subcortical brain development. Neuroimage 88, 242–251.Google Scholar
Gogtay, N, Giedd, JN, Lusk, L, Hayashi, KM, Greenstein, D, Vaituzis, AC, Nugent, TF, Herman, DH, Clasen, LS and Toga, AW (2004) Dynamic mapping of human cortical development during childhood through early adulthood. Proceedings of the National Academy of Sciences of the United States of America 101, 8174–8179.Google Scholar
Grant, BF, Goldstein, RB, Saha, TD, Chou, SP, Jung, J, Zhang, H, Pickering, RP, Ruan, WJ, Smith, SM and Huang, B (2015) Epidemiology of DSM-5 alcohol use disorder: results from the national epidemiologic survey on alcohol and related conditions III. JAMA Psychiatry 72, 757–766.Google Scholar
Grant, BF, Stinson, FS, Dawson, DA, Chou, SP, Dufour, MC, Compton, W, Pickering, RP and Kaplan, K (2004) Prevalence and co-occurrence of substance use disorders and independentmood and anxiety disorders: results from the national epidemiologic survey on alcohol and relatedconditions. Archives of General Psychiatry 61, 807–816.Google Scholar
Grimm, KJ, Ram, N and Hamagami, F (2011) Nonlinear growth curves in developmental research. Child Development 82, 1357–1371.Google Scholar
Haber, SN and Knutson, B (2010) The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35, 4–26.Google Scholar
Hasin, DS, Goodwin, RD, Stinson, FS and Grant, BF (2005) Epidemiology of major depressive disorder: results from the national epidemiologic survey on alcoholism and related conditions. Archives of General Psychiatry 62, 1097–1106.Google Scholar
Hasler, BP, Dahl, RE, Holm, SM, Jakubcak, JL, Ryan, ND, Silk, JS, Phillips, ML and Forbes, EE (2012) Weekend–weekday advances in sleep timing are associated with altered reward-related brain function in healthy adolescents. Biological Psychology 91, 334–341.Google Scholar
Heitzeg, MM, Cope, LM, Martz, ME and Hardee, JE (2015) Neuroimaging risk markers for substance abuse: recent findings on inhibitory control and reward system functioning. Current Addiction Reports 2, 91–103.Google Scholar
Heitzeg, MM, Nigg, JT, Yau, W-YW, Zucker, RA and Zubieta, J-K (2010) Striatal dysfunction marks preexisting risk and medial prefrontal dysfunction is related to problem drinking in children of alcoholics. Biological Psychiatry 68, 287–295.Google Scholar
Hu, LT and Bentler, PM (1999) Cutoff criteria for fit indexes in covariance structure analysis: conventional criteria versus new alternatives. Structural Equation Modeling: A Multidisciplinary Journal 6, 1–55.Google Scholar
Hyde, LW, Byrd, AL, Votruba-Drzal, E, Hariri, AR and Manuck, SB (2014) Amygdala reactivity and negative emotionality: divergent correlates of antisocial personality and psychopathy traits in a community sample. Journal of Abnormal Psychology 123, 214–224.Google Scholar
Jeffreys, H (1998) The Theory of Probability. Oxford: OUP.Google Scholar
Johnston, LD, O'Malley, PM, Bachman, JG, Schulenberg, JE, Patrick, ME and Miech, RA (2015) National Survey Results Monitoring The Future. In http://citeseerx.ist.psu.edu/viewdoc/citations?doi=10.1.1.719.6081.Google Scholar
Kaufman, J, Birmaher, B, Brent, D, Rao, U, Flynn, C, Moreci, P, Williamson, D and Ryan, N (1997) Schedule for affective disorders and schizophrenia for school-age children-present and lifetime version (K-SADS-PL): initial reliability and validity data. Journal of the American Academy of Child & Adolescent Psychiatry 36, 980–988.Google Scholar
Kriegeskorte, N, Simmons, WK, Bellgowan, PS and Baker, CI (2009) Circular analysis in systems neuroscience: the dangers of double dipping. Nature Neuroscience 12, 535–540.Google Scholar
Kuntsche, E, Knibbe, R, Gmel, G and Engels, R (2006) Who drinks and why? A review of socio-demographic, personality, and contextual issues behind the drinking motives in young people. Addictive Behaviors 31, 1844–1857.Google Scholar
Kushner, MG, Abrams, K and Borchardt, C (2000) The relationship between anxiety disorders and alcohol use disorders: a review of major perspectives and findings. Clinical Psychology Review 20, 149–171.Google Scholar
Mattson, WI, Hyde, LW, Shaw, DS, Forbes, EE and Monk, CS (2016) Clinical neuroprediction: Amygdala reactivity predicts depressive symptoms 2 years later. Social Cognitive and Affective Neuroscience 11, 892–898.Google Scholar
Miech, R, Johnston, L, O'Malley, P, Bachman, J and Schulenberg, J (2015) Monitoring The Future National Survey Results On Drug Use, 1975–2014, Volume I. Ann Arbor: Secondary School Students, Institute for Social Research. http://monitoringthefutureorg/pubshtml-monographs.Google Scholar
Moss, HB, Chen, CM and Yi, H-Y (2014) Early adolescent patterns of alcohol, cigarettes, and marijuana polysubstance use and young adult substance use outcomes in a nationally representative sample. Drug and Alcohol Dependence 136, 51–62.Google Scholar
Murray, L, Shaw, DS, Forbes, EE and Hyde, LW (2017) Reward-related neural correlates of antisocial behavior and callous-unemotional traits in young men. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging 2, 346–354.Google Scholar
Muthén, LK and Muthén, BO (2014) Mplus User's Guide, 7th Edn. Los Angeles, CA: Muthén & Muthén.Google Scholar
Nichols, T, Brett, M, Andersson, J, Wager, T and Poline, J-B (2005) Valid conjunction inference with the minimum statistic. Neuroimage 25, 653–660.Google Scholar
Nikolova, YS, Knodt, AR, Radtke, SR and Hariri, AR (2016) Divergent responses of the amygdala and ventral striatum predict stress-related problem drinking in young adults: possible differential markers of affective and impulsive pathways of risk for alcohol use disorder. Molecular Psychiatry 21, 348–356.Google Scholar
Nusslock, R, Almeida, JR, Forbes, EE, Versace, A, Frank, E, Labarbara, EJ, Klein, CR and Phillips, ML (2012) Waiting to win: elevated striatal and orbitofrontal cortical activity during reward anticipation in euthymic bipolar disorder adults. Bipolar Disorders 14, 249–260.Google Scholar
Patton, JH and Stanford, MS (1995) Factor structure of the Barratt impulsiveness scale. Journal of Clinical Psychology 51, 768–774.Google Scholar
Rehm, J (2011) The risks associated with alcohol use and alcoholism. Alcohol Research & Health: the Journal of the National Institute on Alcohol Abuse and Alcoholism 34, 135.Google Scholar
Robinson, TE and Berridge, KC (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Research Reviews 18, 247–291.Google Scholar
Schramm, NL, Egli, RE and Winder, DG (2002) LTP in the mouse nucleus accumbens is developmentally regulated. Synapse 45, 213–219.Google Scholar
Seeman, P (1987) Dopamine receptors and the dopamine hypothesis of schizophrenia. Synapse 1, 133–152.Google Scholar
Shaw, DS, Hyde, LW and Brennan, LM (2012) Early predictors of boys' antisocial trajectories. Development and Psychopathology 24, 871–888.Google Scholar
Silveri, M and Spear, L (2002) The effects of NMDA and GABAA pharmacological manipulations on ethanol sensitivity in immature and mature animals. Alcoholism: Clinical and Experimental Research 26, 449–456.Google Scholar
Spear, LP (2016) Alcohol consumption in adolescence: a translational perspective. Current Addiction Reports 3, 50–61.Google Scholar
Spear, LP and Swartzwelder, HS (2014) Adolescent alcohol exposure and persistence of adolescent-typical phenotypes into adulthood: a mini-review. Neuroscience & Biobehavioral Reviews 45, 1–8.Google Scholar
Tapert, SF, Schweinsburg, AD, Barlett, VC, Brown, SA, Frank, LR, Brown, GG and Meloy, MJ (2004) Blood oxygen level dependent response and spatial working memory in adolescents with alcohol use disorders. Alcoholism: Clinical and Experimental Research 28, 1577–1586.Google Scholar
Teicher, MH, Andersen, SL and Hostetter, JC (1995) Evidence for dopamine receptor pruning between adolescence and adulthood in striatum but not nucleus accumbens. Developmental Brain Research 89, 167–172.Google Scholar
van Emmerik-van Oortmerssen, K, van de Glind, G, van den Brink, W, Smit, F, Crunelle, CL, Swets, M and Schoevers, RA (2012) Prevalence of attention-deficit hyperactivity disorder in substance use disorder patients: a meta-analysis and meta-regression analysis. Drug and Alcohol Dependence 122, 11–19.Google Scholar
Waller, R, Corral-Frias, N, Vannucci, B, Bogdan, R, Knodt, AR, Hariri, AR and Hyde, LW (2016) An oxytocin receptor polymorphism predicts amygdala reactivity and antisocial behavior in men. Social Cognitive and Affective Neuroscience 11, 1218–1226.Google Scholar
Wetherill, RR, Squeglia, LM, Yang, TT and Tapert, SF (2013) A longitudinal examination of adolescent response inhibition: neural differences before and after the initiation of heavy drinking. Psychopharmacology 230, 663–671.Google Scholar
Wiers, RW, Bartholow, BD, van den Wildenberg, E, Thush, C, Engels, RC, Sher, KJ, Grenard, J, Ames, SL and Stacy, AW (2007) Automatic and controlled processes and the development of addictive behaviors in adolescents: a review and a model. Pharmacology Biochemistry and Behavior 86, 263–283.Google Scholar
Wrase, J, Schlagenhauf, F, Kienast, T, Wüstenberg, T, Bermpohl, F, Kahnt, T, Beck, A, Ströhle, A, Juckel, G and Knutson, B (2007) Dysfunction of reward processing correlates with alcohol craving in detoxified alcoholics. Neuroimage 35, 787–794.Google Scholar
Xiao, L, Bechara, A, Gong, Q, Huang, X, Li, X, Xue, G, Wong, S, Lu, Z-L, Palmer, P and Wei, Y (2013) Abnormal affective decision making revealed in adolescent binge drinkers using a functional magnetic resonance imaging study. Psychology of Addictive Behaviors 27, 443.Google Scholar
Yau, W-YW, Zubieta, J-K, Weiland, BJ, Samudra, PG, Zucker, RA and Heitzeg, MM (2012) Nucleus accumbens response to incentive stimuli anticipation in children of alcoholics: relationships with precursive behavioral risk and lifetime alcohol use. Journal of Neuroscience 32, 2544–2551.Google Scholar
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