Effects of delaying binge drinking on adolescent brain development: a longitudinal neuroimaging study

Josiane Bourque1,2, Travis E. Baker3, Alain Dagher4, Alan C. Evans4, Hugh Garavan5, Marco Leyton6,7,4, Jean R. Séguin1,2, Robert Pihl7, Patricia J. Conrod1,2
1Department of Psychiatry, Faculty of Medicine, University of Montreal, Montreal, Canada
2Centre de recherche, CHU Sainte-Justine, Montreal, Canada
3Center for Molecular and Behavioural Neuroscience, Rutgers University, Newark, USA
4Montreal Neurological Institute, McGill University, Montreal, Canada
5Department of Psychiatry, University of Vermont, Burlington, USA
6Department of Psychiatry, McGill University, Montréal, Canada
7Department of Psychology, McGill University, Montréal, Canada

Tóm tắt

Onset of alcohol use by 14 relative to 21 years of age strongly predicts elevated risk for severe alcohol use problems, with 27% versus 4% of individuals exhibiting alcohol dependence within 10 years of onset. What remains unclear is whether this early alcohol use (i) is a marker for later problems, reflected as a pre-existing developmental predisposition, (ii) causes global neural atrophy or (iii) specifically disturbs neuro-maturational processes implicated in addiction, such as executive functions or reward processing. Since our group has demonstrated that a novel intervention program targeting personality traits associated with adolescent alcohol use can prevent the uptake of drinking and binge drinking by 40 to 60%, a crucial question is whether prevention of early onset alcohol misuse will protect adolescent neurodevelopment and which domains of neurodevelopment can be protected. A subsample of 120 youth at high risk for substance misuse and 30 low-risk youth will be recruited from the Co-Venture trial (Montreal, Canada) to take part in this 5-year follow-up neuroimaging study. The Co-Venture trial is a community-based cluster-randomised trial evaluating the effectiveness of school-based personality-targeted interventions on substance use and cognitive outcomes involving approximately 3800 Grade 7 youths. Half of the 120 high-risk participants will have received the preventative intervention program. Cognitive tasks and structural and functional neuroimaging scans will be conducted at baseline, and at 24- and 48-month follow-up. Two functional paradigms will be used: the Stop-Signal Task to measure motor inhibitory control and a modified version of the Monetary Incentive Delay Task to evaluate reward processing. The expected results should help identify biological vulnerability factors, and quantify the consequences of early alcohol abuse as well as the benefits of early intervention using brain metrics.

Từ khóa


Tài liệu tham khảo

Hingson RW, Heeren T, Winter MR. Age at drinking onset and alcohol dependence: age at onset, duration, and severity. Arch Pediatr Adolesc Med. 2006;160:739–46. Giedd JN. Structural magnetic resonance imaging of the adolescent brain. Ann N Y Acad Sci. 2004;1021:77–85. Shaw P, Kabani NJ, Lerch JP, Eckstrand K, Lenroot R, Gogtay N, et al. Neurodevelopmental trajectories of the human cerebral cortex. J Neurosci. 2008;28:3586–94. Sowell ER, Thompson PM, Holmes CJ, Jernigan TL, Toga AW. In vivo evidence for post-adolescent brain maturation in frontal and striatal regions. Nat Neurosci. 1999;2:859–61. Casey BJ, Tottenham N, Liston C, Durston S. Imaging the developing brain: what have we learned about cognitive development? Trends Cogn Sci. 2005;9:104–10. Olesen PJ, Nagy Z, Westerberg H, Klingberg T. Combined analysis of DTI and fMRI data reveals a joint maturation of white and grey matter in a fronto-parietal network. Brain Res Cogn Brain Res. 2003;18:48–57. Shulman EP, Smith AR, Silva K, Icenogle G, Duell N, Chein J, et al. The dual systems model: review, reappraisal, and reaffirmation. Dev Cogn Neurosci. 2016;17:103–17. Steinberg L, Albert D, Cauffman E, Banich M, Graham S, Woolard J. Age differences in sensation seeking and impulsivity as indexed by behavior and self-report: evidence for a dual systems model. Dev Psychol. 2008;44:1764–78. Rubia K, Overmeyer S, Taylor E, Brammer M, Williams SC, Simmons A, et al. Functional frontalisation with age: mapping neurodevelopmental trajectories with fMRI. Neurosci Biobehav Rev. 2000;24:13–9. Rubia K, Smith AB, Woolley J, Nosarti C, Heyman I, Taylor E, et al. Progressive increase of frontostriatal brain activation from childhood to adulthood during event-related tasks of cognitive control. Hum Brain Mapp. 2006;27:973–93. Qu Y, Galvan A, Fuligni AJ, Lieberman MD, Telzer EH. Longitudinal changes in prefrontal cortex activation underlie declines in adolescent risk taking. J Neurosci. 2015;35:11308–14. Brown SA, Tapert SF, Granholm E, Delis DC. Neurocognitive functioning of adolescents: effects of protracted alcohol use. Alcohol Clin Exp Res. 2000;24:164–71. Tapert SF, Brown SA. Neuropsychological correlates of adolescent substance abuse: four-year outcomes. J Int Neuropsychol Soc. 1999;5:481–93. Tapert SF, Granholm E, Leedy NG, Brown SA. Substance use and withdrawal: neuropsychological functioning over 8 years in youth. J Int Neuropsychol Soc. 2002;8:873–83. De Bellis MD, Clark DB, Beers SR, Soloff PH, Boring AM, Hall J, et al. Hippocampal volume in adolescent-onset alcohol use disorders. Am J Psychiatry. 2000;157:737–44. Tapert SF, Cheung EH, Brown GG, Frank LR, Paulus MP, Schweinsburg AD, et al. Neural response to alcohol stimuli in adolescents with alcohol use disorder. Arch Gen Psychiatry. 2003;60:727–35. Caldwell LC, Schweinsburg AD, Nagel BJ, Barlett VC, Brown SA, Tapert SF. Gender and adolescent alcohol use disorders on BOLD (blood oxygen level dependent) response to spatial working memory. Alcohol Alcohol. 2005;40:194–200. Kirisci L, Tarter RE, Reynolds M, Vanyukov M. Individual differences in childhood neurobehavior disinhibition predict decision to desist substance use during adolescence and substance use disorder in young adulthood: a prospective study. Addict Behav. 2006;31:686–96. Rubia K, Smith AB, Brammer MJ, Taylor E. Temporal lobe dysfunction in medication-naive boys with attention-deficit/hyperactivity disorder during attention allocation and its relation to response variability. Biol Psychiatry. 2007;62:999–1006. Harden PW, Pihl RO. Cognitive function, cardiovascular reactivity, and behavior in boys at high risk for alcoholism. J Abnorm Psychol. 1995;104:94. Oosterlaan J, Logan GD, Sergeant JA. Response inhibition in AD/HD, CD, comorbid AD/HD+ CD, anxious, and control children: a meta-analysis of studies with the stop task. J Child Psychol Psychiatry. 1998;39:411–25. Peterson JB, Finn PR, Pihl RO. Cognitive dysfunction and the inherited predisposition to alcoholism. J Stud Alcohol Drugs. 1992;53:154. Sonuga-Barke EJ, Dalen L, Daley D, Remington B. Are planning, working memory, and inhibition associated with individual differences in preschool ADHD symptoms? Dev Neuropsychol. 2002;21:255–72. Schilling C, Kühn S, Romanowski A, Banaschewski T, Barbot A, Barker GJ, et al. Common structural correlates of trait impulsiveness and perceptual reasoning in adolescence. Hum Brain Mapp. 2013;34:374–83. Castellanos-Ryan N, Struve M, Whelan R, Banaschewski T, Barker GJ, Bokde AL, et al. Neural and cognitive correlates of the common and specific variance across externalizing problems in young adolescence. Am J Psychiatry. 2014;171:1310–19. Tapert SF, Brown SA. Substance dependence, family history of alcohol dependence and neuropsychological functioning in adolescence. Addiction. 2000;95:1043–53. Zuckerman M. Behavioral expressions and biosocial bases of sensation seeking. Cambridge: Cambridge University Press; 1994. Arnett JJ. Sensation seeking, aggressiveness, and adolescent reckless behavior. Personal Individ Differ. 1996;20:693–702. Comeau N, Stewart SH, Loba P. The relations of trait anxiety, anxiety sensitivity, and sensation seeking to adolescents’ motivations for alcohol, cigarette, and marijuana use. Addict Behav. 2001;26:803–25. Cooper ML, Frone MR, Russell M, Mudar P. Drinking to regulate positive and negative emotions: a motivational model of alcohol use. J Pers Soc Psychol. 1995;69:990. Schall M, Kemeny A, Maltzman I. Factors associated with alcohol use in university students. J Stud Alcohol Drugs. 1992;53:122. Castellanos-Ryan N, Rubia K, Conrod PJ. Response inhibition and reward response bias mediate the predictive relationships between impulsivity and sensation seeking and common and unique variance in conduct disorder and substance misuse. Alcohol Clin Exp Res. 2011;35:140–55. Mahu IT, Doucet C, O’Leary-Barrett M, Conrod PJ. Can cannabis use be prevented by targeting personality risk in schools? Twenty-four-month outcome of the adventure trial on cannabis use: a cluster-randomized controlled trial. Addiction. 2015;110:1625–33. Conrod PJ, Castellanos N, Mackie C. Personality-targeted interventions delay the growth of adolescent drinking and binge drinking. J Child Psychol Psychiatry. 2008;49:181–90. Conrod PJ, Castellanos-Ryan N, Strang J. Brief, personality-targeted coping skills interventions and survival as a non-drug user over a 2-year period during adolescence. Arch Gen Psychiatry. 2010;67:85–93. Woicik PA, Stewart SH, Pihl RO, Conrod PJ. The substance use risk profile scale: a scale measuring traits linked to reinforcement-specific substance use profiles. Addict Behav. 2009;34:1042–55. Stewart SH, Devine H. Relations between personality and drinking motives in young adults. Personal Individ Differ. 2000;29:495–511. O’Leary-Barrett M, Mackie CJ, Castellanos-Ryan N, Al-Khudhairy N, Conrod PJ. Personality-targeted interventions delay uptake of drinking and decrease risk of alcohol-related problems when delivered by teachers. J Am Acad Child Adolesc Psychiatry. 2010;49:954–63. e1. Conrod PJ, Stewart SH, Comeau N, Maclean AM. Efficacy of cognitive-behavioral interventions targeting personality risk factors for youth alcohol misuse. J Clin Child Adolesc Psychol. 2006;35:550–63. Conrod PJ, O’Leary-Barrett M, Newton N, Topper L, Castellanos-Ryan N, Mackie C, et al. Effectiveness of a selective, personality-targeted prevention program for adolescent alcohol use and misuse: a cluster randomized controlled trial. JAMA Psychiat. 2013;70:334–42. Conrod PJ. Personality-targeted interventions for adolescence substance misuse. Curr Addict Rep. 2016;3:426–36. Whelan R, Watts R, Orr CA, Althoff RR, Artiges E, Banaschewski T, et al. Neuropsychosocial profiles of current and future adolescent alcohol misusers. Nature. 2014;512:185–9. Donohue B, Azrin NH, Strada MJ, Silver NC, Teichner G, Murphy H. Psychometric evaluation of self- and collateral timeline follow-back reports of drug and alcohol use in a sample of drug-abusing and conduct-disordered adolescents and their parents. Psychol Addict Behav. 2004;18:184–9. Sobell LC, Maisto SA, Sobell MB, Cooper AM. Reliability of alcohol abusers’ self-reports of drinking behavior. Behav Res Ther. 1979;17:157–60. Stroop JR. Studies of interference in serial verbal reactions. J Exp Psychol. 1935;18:643–62. Petrides M, Milner B. Deficits on subject-ordered tasks after frontal- and temporal-lobe lesions in man. Neuropsychologia. 1982;20:249–62. Kirchner WK. Age differences in short-term retention of rapidly changing information. J Exp Psychol. 1958;55:352–8. Cohen MJ. Children memory scale (CMS). San Antonio: The Psychological Corporation; 1997. Lejuez CW, Read JP, Kahler CW, Richards JB, Ramsey SE, Stuart GL, et al. Evaluation of a behavioral measure of risk taking: the Balloon Analogue Risk Task (BART). J Exp Psychol Appl. 2002;8:75–84. Wechsler D. Wechsler Intelligence Scale for Children. 4th ed. San Antonio: The Psychological Corporation; 2003. Schumann G, Loth E, Banaschewski T, Barbot A, Barker G, Buchel C, et al. The IMAGEN study: reinforcement-related behaviour in normal brain function and psychopathology. Mol Psychiatry. 2010;15:1128–39. Knutson B, Adams CM, Fong GW, Hommer D. Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neurosci. 2001;21:RC159. Bjork JM, Knutson B, Fong GW, Caggiano DM, Bennett SM, Hommer DW. Incentive-elicited brain activation in adolescents: similarities and differences from young adults. J Neurosci. 2004;24:1793–802. Peters J, Bromberg U, Schneider S, Brassen S, Menz M, Banaschewski T, et al. Lower ventral striatal activation during reward anticipation in adolescent smokers. Am J Psychiatry. 2011;168:540–9. Schneider S, Peters J, Bromberg U, Brassen S, Miedl SF, Banaschewski T, et al. Risk taking and the adolescent reward system: a potential common link to substance abuse. Am J Psychiatry. 2012;169:39–46. Rubia K, Smith AB, Taylor E, Brammer M. Linear age-correlated functional development of right inferior fronto-striato-cerebellar networks during response inhibition and anterior cingulate during error-related processes. Hum Brain Mapp. 2007;28:1163–77. Rubia K, Smith AB, Brammer MJ, Toone B, Taylor E. Abnormal brain activation during inhibition and error detection in medication-naive adolescents with ADHD. Am J Psychiatry. 2005;162:1067–75. Rubia K, Smith AB, Brammer MJ, Taylor E. Right inferior prefrontal cortex mediates response inhibition while mesial prefrontal cortex is responsible for error detection. Neuroimage. 2003;20:351–8. Rubia K, Russell T, Overmeyer S, Brammer MJ, Bullmore ET, Sharma T, et al. Mapping motor inhibition: conjunctive brain activations across different versions of go/no-go and stop tasks. Neuroimage. 2001;13:250–61. Logan GD, Schachar RJ, Tannock R. Impulsivity and inhibitory control. Psychol Sci. 1997;8:60–4. Cocosco CA, Zijdenbos AP, Evans AC. A fully automatic and robust brain MRI tissue classification method. Med Image Anal. 2003;7:513–27. Zijdenbos AP, Forghani R, Evans AC. Automatic “pipeline” analysis of 3-D MRI data for clinical trials: application to multiple sclerosis. IEEE Trans Med Imaging. 2002;21:1280–91. Kim JS, Singh V, Lee JK, Lerch J, Ad-Dab’bagh Y, MacDonald D, et al. Automated 3-D extraction and evaluation of the inner and outer cortical surfaces using a Laplacian map and partial volume effect classification. Neuroimage. 2005;27:210–21. Lerch JP, Pruessner J, Zijdenbos AP, Collins DL, Teipel SJ, Hampel H, et al. Automated cortical thickness measurements from MRI can accurately separate Alzheimer’s patients from normal elderly controls. Neurobiol Aging. 2008;29:23–30. Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW. Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? Neuroimage. 2007;34:144–55. Powell HW, Parker GJ, Alexander DC, Symms MR, Boulby PA, Wheeler-Kingshott CA, et al. Hemispheric asymmetries in language-related pathways: a combined functional MRI and tractography study. Neuroimage. 2006;32:388–99. Parker GJ, Haroon HA, Wheeler-Kingshott CA. A framework for a streamline-based probabilistic index of connectivity (PICo) using a structural interpretation of MRI diffusion measurements. J Magn Reson Imaging. 2003;18:242–54. Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 2002;17:825–41. Smith SM. Fast robust automated brain extraction. Hum Brain Mapp. 2002;17:143–55. Woolrich MW, Ripley BD, Brady M, Smith SM. Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage. 2001;14:1370–86. Beckmann CF, Jenkinson M, Smith SM. General multilevel linear modeling for group analysis in FMRI. Neuroimage. 2003;20:1052–63. Squeglia LM, Gray KM. Alcohol and drug use and the developing brain. Curr Psychiatry Rep. 2016;18:46. Grant BF, Dawson DA. Age at onset of alcohol use and its association with DSM-IV alcohol abuse and dependence: results from the National Longitudinal Alcohol Epidemiologic Survey. J Subst Abuse. 1997;9:103–10.