Advertisement

Alcohol and Drug Use and the Developing Brain

  • Lindsay M. Squeglia
  • Kevin M. Gray
Substance Use and Related Disorders (F Levin and E Dakwar, Section Editors)
Part of the following topical collections:
  1. Topical Collection on Substance Use and Related Disorders

Abstract

Adolescence is an important neurodevelopmental period marked by rapidly escalating rates of alcohol and drug use. Over the past decade, research has attempted to disentangle pre- and post-substance use effects on brain development by using sophisticated longitudinal designs. This review focuses on recent, prospective studies and addresses the following important questions: (1) what neuropsychological and neural features predate adolescent substance use, making youth more vulnerable to engage in heavy alcohol or drug use, and (2) how does heavy alcohol and drug use affect normal neural development and cognitive functioning? Findings suggest that pre-existing neural features that relate to increased substance use during adolescence include poorer neuropsychological functioning on tests of inhibition and working memory, smaller gray and white matter volume, changes in white matter integrity, and altered brain activation during inhibition, working memory, reward, and resting state. After substance use is initiated, alcohol and marijuana use are associated with poorer cognitive functioning on tests of verbal memory, visuospatial functioning, psychomotor speed, working memory, attention, cognitive control, and overall IQ. Heavy alcohol use during adolescence is related to accelerated decreases in gray matter and attenuated increases in white matter volume, as well as increased brain activation during tasks of inhibition and working memory, relative to controls. Larger longitudinal studies with more diverse samples are needed to better understand the interactive effects of alcohol, marijuana, and other substances, as well as the role of sex, co-occurring psychopathology, genetics, sleep, and age of initiation on substance use.

Keywords

Alcohol Marijuana Neural development Substance use Cognitive functioning Neuropsychological testing Magnetic resonance imaging (MRI) Functional MRI (fMRI) 

Notes

Funding Support

The authors wish to acknowledge the funding sources for this work, including NIDA grants K12 DA031794 (Squeglia), U01 DA031779 (Gray), UG1 DA013727—CTN0053 (Gray), and R01 DA038700 (Gray). The funding source had no role other than financial support.

The authors would like to express gratitude to Jack McKee and Lindsay Meredith for their assistance with manuscript preparation.

Compliance with Ethical Standards

Conflict of Interest

Lindsay M. Squeglia and Kevin M. Gray report grants from National Institute on Drug Abuse.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: •• Of major importance

  1. 1.
    Squeglia LM, Boissoneault J, Van Skike CE, Nixon SJ, Matthews DB. Age-related effects of alcohol from adolescent, adult, and aged populations using human and animal models. Alcohol Clin Exp Res. 2014;38(10):2509–16.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Brown SA, McGue M, Maggs J, Schulenberg J, Hingson R, Swartzwelder S, et al. A developmental perspective on alcohol and youths 16 to 20 years of age. Pediatrics. 2008;121 Suppl 4:S290–310.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    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 Abus. 1997;9:103–10.CrossRefGoogle Scholar
  4. 4.
    Dawson DA, Goldstein RB, Chou SP, Ruan WJ, Grant BF. Age at first drink and the first incidence of adult-onset DSM-IV alcohol use disorders. Alcohol Clin Exp Res. 2008;32(12):2149–60.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Johnston LD, O’Malley PM, Miech RA, Bachman JG, Schulenberg JE. Monitoring the Future national results on adolescent drug use: Overview of key findings, 2014. Ann Arbor: Michigan; 2015.Google Scholar
  6. 6.
    Paus T. Mapping brain maturation and cognitive development during adolescence. Trends Cogn Sci. 2005;9(2):60–8.CrossRefPubMedGoogle Scholar
  7. 7.
    Petanjek Z, Judas M, Simic G, Rasin MR, Uylings HB, Rakic P, et al. Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc Natl Acad Sci U S A. 2011;108(32):13281–6.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Gogtay N, Giedd JN, Lusk L, Hayashi KM, Greenstein D, Vaituzis AC, et al. Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci U S A. 2004;101(21):8174–9.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Raznahan A, Shaw PW, Lerch JP, Clasen LS, Greenstein D, Berman R, et al. Longitudinal four-dimensional mapping of subcortical anatomy in human development. Proc Natl Acad Sci U S A. 2014;111(4):1592–7.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    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(10):859–61.CrossRefPubMedGoogle Scholar
  11. 11.
    Stiles J, Jernigan TL. The basics of brain development. Neuropsychol Rev. 2010;20(4):327–48.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Bava S, Thayer R, Jacobus J, Ward M, Jernigan TL, Tapert SF. Longitudinal characterization of white matter maturation during adolescence. Brain Res. 2010;1327:38–46.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Asato MR, Terwilliger R, Woo J, Luna B. White matter development in adolescence: a DTI study. Cereb Cortex. 2010;20(9):2122–31.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Benes FM. Myelination of cortical-hippocampal relays during late adolescence. Schizophr Bull. 1989;15(4):585–93.CrossRefPubMedGoogle Scholar
  15. 15.
    Simmonds DJ, Hallquist MN, Asato M, Luna B. Developmental stages and sex differences of white matter and behavioral development through adolescence: a longitudinal diffusion tensor imaging (DTI) study. Neuroimage. 2014;92:356–68.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Squeglia LM, Jacobus J, Sorg SF, Jernigan TL, Tapert SF. Early adolescent cortical thinning is related to better neuropsychological performance. J Int Neuropsychol Soc. 2013;19(9):962–70.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Casey BJ, Getz S, Galvan A. The adolescent brain. Dev Rev. 2008;28(1):62–77.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Ernst M, Nelson EE, Jazbec S, McClure EB, Monk CS, Leibenluft E, et al. Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents. Neuroimage. 2005;25(4):1279–91.CrossRefPubMedGoogle Scholar
  19. 19.
    Koob GF, Volkow ND. Neurocircuitry of addiction. Neuropsychopharmacology. 2010;35(1):217–38.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Sturman DA, Moghaddam B. Reduced neuronal inhibition and coordination of adolescent prefrontal cortex during motivated behavior. J Neurosci. 2011;31(4):1471–8.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Somerville LH, Jones RM, Casey BJ. A time of change: behavioral and neural correlates of adolescent sensitivity to appetitive and aversive environmental cues. Brain Cogn. 2010;72(1):124–33.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Squeglia LM, Jacobus J, Tapert SF. The influence of substance use on adolescent brain development. Clin EEG Neurosci. 2009;40(1):31–8.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Squeglia LM, Jacobus J, Tapert SF. The effect of alcohol use on human adolescent brain structures and systems. Handb Clin Neurol. 2014;125:501–10.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Jacobus J, Tapert SF. Neurotoxic effects of alcohol in adolescence. Annu Rev Clin Psychol. 2013;9:703–21.CrossRefPubMedGoogle Scholar
  25. 25.
    López-Caneda E, Rodríguez Holguín S, Cadaveira F, Corral M, Doallo S. Impact of alcohol use on inhibitory control (and vice versa) during adolescence and young adulthood: A review. Alcohol Alcohol. 2014;49(2):173–81.CrossRefPubMedGoogle Scholar
  26. 26.
    Luna B, Padmanabhan A, O’Hearn K. What has fMRI told us about the development of cognitive control through adolescence? Brain Cogn. 2010;72(1):101–13.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Stevens MC, Kiehl KA, Pearlson GD, Calhoun VD. Functional neural networks underlying response inhibition in adolescents and adults. Behav Brain Res. 2007;181(1):12–22.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Khurana A, Romer D, Betancourt LM, Brodsky NL, Giannetta JM, Hurt H. Working memory ability predicts trajectories of early alcohol use in adolescents: The mediational role of impulsivity. Addiction. 2013;108(3):506–15.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Durston S, Davidson MC, Tottenham N, Galvan A, Spicer J, Fossella JA, et al. A shift from diffuse to focal cortical activity with development. Dev Sci. 2006;9(1):1–8.CrossRefPubMedGoogle Scholar
  30. 30.
    Velanova K, Wheeler ME, Luna B. Maturational changes in anterior cingulate and frontoparietal recruitment support the development of error processing and inhibitory control. Cereb Cortex. 2008;18(11):2505–22.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Norman AL, Pulido C, Squeglia LM, Spadoni AD, Paulus MP, Tapert SF. Neural activation during inhibition predicts initiation of substance use in adolescence. Drug Alcohol Depend. 2011;119(3):216–23.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    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(7513):185–9.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Heitzeg MM, Nigg JT, Hardee JE, Soules M, Steinberg D, Zubieta JK, et al. Left middle frontal gyrus response to inhibitory errors in children prospectively predicts early problem substance use. Drug Alcohol Depend. 2014;141:51–7.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Mahmood OM, Goldenberg D, Thayer R, Migliorini R, Simmons AN, Tapert SF. Adolescents’ fMRI activation to a response inhibition task predicts future substance use. Addict Behav. 2013;38(1):1435–41.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Wetherill RR, Castro N, Squeglia LM, Tapert SF. Atypical neural activity during inhibitory processing in substance-naïve youth who later experience alcohol-induced blackouts. Drug Alcohol Depend. 2013;128(3):243–9.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Squeglia LM, Pulido C, Wetherill RR, Jacobus J, Brown GG, Tapert SF. Brain response to working memory over three years of adolescence: Influence of initiating heavy drinking. J Stud Alcohol Drugs. 2012;73(5):749–60.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Ramage AE, Lin AL, Olvera RL, Fox PT, Williamson DE. Resting-state regional cerebral blood flow during adolescence: Associations with initiation of substance use and prediction of future use disorders. Drug Alcohol Depend. 2015.Google Scholar
  38. 38.
    Schumann G, Loth E, Banaschewski T, Barbot A, Barker G, Büchel C, et al. IMAGEN consortium. The IMAGEN study: Reinforcement-related behaviour in normal brain function and psychopathology. Mol Psychiatry. 2010;15(12):1128–39.CrossRefPubMedGoogle Scholar
  39. 39.
    Cousijn J, Wiers RW, Ridderinkhof KR, van den Brink W, Veltman DJ, Porrino LJ, et al. Individual differences in decision making and reward processing predict changes in cannabis use: A prospective functional magnetic resonance imaging study. Addict Biol. 2013;18(6):1013–23.CrossRefPubMedGoogle Scholar
  40. 40.
    Cheetham A, Allen NB, Whittle S, Simmons JG, Yücel M, Lubman DI. Orbitofrontal volumes in early adolescence predict initiation of cannabis use: A 4-year longitudinal and prospective study. Biol Psychiatry. 2012;71(8):684–92.CrossRefPubMedGoogle Scholar
  41. 41.
    Weiland BJ, Korycinski ST, Soules M, Zubieta JK, Zucker RA, Heitzeg MM. Substance abuse risk in emerging adults associated with smaller frontal gray matter volumes and higher externalizing behaviors. Drug Alcohol Depend. 2014;137:68–75.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Squeglia LM, Rinker DA, Bartsch H, Castro N, Chung Y, Dale AM, et al. Brain volume reductions in adolescent heavy drinkers. Dev Cogn Neurosci. 2014;9:117–25.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Urošević S, Collins P, Muetzel R, Schissel A, Lim K, Luciana M. Effects of reward sensitivity and regional brain volumes on substance use initiation in adolescence. Soc Cogn Affect Neurosci. 2015;10(1):106–13.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Cheetham A, Allen NB, Whittle S, Simmons J, Yücel M, Lubman DI. Volumetric differences in the anterior cingulate cortex prospectively predict alcohol-related problems in adolescence. Psychopharmacology. 2014;231(8):1731–42.CrossRefPubMedGoogle Scholar
  45. 45.
    Jacobus J, Thayer RE, Trim RS, Bava S, Frank LR, Tapert SF. White matter integrity, substance use, and risk taking in adolescence. Psychol Addict Behav. 2013;27(2):431–42.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Brown SA, Brumback T, Tomlinson K, Cummins K, Thompson WK, Nagel BJ, De Bellis MD, Hooper SR, Clark DB, Chung T, Hasler BP, Colrain IM, Baker FB, Prouty D, Pfefferbaum A, Sullivan EV, Pohl KM, Rohlfing T, Nichols BN, Chu W, Tapert SF. The National Consortium on Alcohol and NeuroDevelopment in Adolescence (NCANDA): A multi-site study of adolescent development and substance use. Journal of Studies on Alcohol and Drugs. in press.Google Scholar
  47. 47.
    Latvala A, Rose RJ, Pulkkinen L, Dick DM, Korhonen T, Kaprio J. Drinking, smoking, and educational achievement: Cross-lagged associations from adolescence to adulthood. Drug Alcohol Depend. 2014;137:106–13.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Nguyen-Louie TT, Castro N, Matt GE, Squeglia LM, Brumback T, Tapert SF. Effects of emerging alcohol and marijuana use behaviors on adolescents’ neuropsychological functioning over four years. Journal of Studies on Alcohol and Drugs. in press.Google Scholar
  49. 49.
    Hanson KL, Cummins K, Tapert SF, Brown SA. Changes in neuropsychological functioning over 10 years following adolescent substance abuse treatment. Psychol Addict Behav. 2011;25(1):127–42.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Hanson KL, Medina KL, Padula CB, Tapert SF, Brown SA. Impact of adolescent alcohol and drug use on neuropsychological functioning in young adulthood: 10-year outcomes. J Child Adolesc Subst Abuse. 2011;20(2):135–54.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Winward JL, Hanson KL, Tapert SF, Brown SA. Heavy alcohol use, marijuana use, and concomitant use by adolescents are associated with unique and shared cognitive decrements. J Int Neuropsychol Soc. 2014;20(8):784–95.CrossRefPubMedGoogle Scholar
  52. 52.••
    Jacobus J, Squeglia LM, Infante MA, Castro N, Brumback T, Meruelo AD, Tapert SF. Neuropsychological performance in adolescent marijuana users with co-occurring alcohol use: A three-year longitudinal study. Neuropsychology. 2015;29(6):829–43. This study examined neuropsychological functioning in a large sample of adolescent heavy marijuana and alcohol users over three years and found that substance use negatively affected domains of complex attention, memory, processing speed, and visuospatial functioning, with earlier age of marijuana use onset associated with poorer outcomes on tests of attention and executive functioning. Google Scholar
  53. 53.
    Randolph K, Turull P, Margolis A, Tau G. Cannabis and cognitive systems in adolescents. Adolesc Psychiatry. 2013;3(2):135–47.CrossRefGoogle Scholar
  54. 54.••
    Meier MH, Caspi A, Ambler A, Harrington H, Houts R, Keefe RS, et al. Persistent cannabis users show neuropsychological decline from childhood to midlife. Proc Natl Acad Sci U S A. 2012;109:E2657–64. This study showed that, in a large longitudinal birth cohort from New Zealand, persistent adolescent-onset marijuana use was associated with neuropsychological decline broadly across domains of functioning. For the heaviest users, marijuana use was associated with an IQ decline of more than 5 points.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Jackson NJ, Isen JD, Khoddam R, Irons D, Tuvblad C, Iacono WG, et al. Impact of adolescent marijuana use on intelligence: Results from two longitudinal twin studies. Proceedings of the National Academy of Sciences: PNAS; 2016.Google Scholar
  56. 56.
    Hanson KL, Winward JL, Schweinsburg AD, Medina KL, Brown SA, Tapert SF. Longitudinal study of cognition among adolescent marijuana users over three weeks of abstinence. Addict Behav. 2010;35(11):970–6.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Winward JL, Hanson KL, Bekman NM, Tapert SF, Brown SA. Adolescent heavy episodic drinking: neurocognitive functioning during early abstinence. J Int Neuropsychol Soc. 2014;20(2):218–29.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Roten A, Baker NL, Gray KM. Cognitive performance in a placebo-controlled pharmacotherapy trial for youth with marijuana dependence. Addict Behav. 2015;45:119–23.CrossRefPubMedGoogle Scholar
  59. 59.••
    Squeglia LM, Tapert SF, Sullivan EV, Jacobus J, Meloy MJ, Rohlfing T, et al. Brain development in heavy-drinking adolescents. Am J Psychiatr. 2015;172(6):531–42. This study used the largest neuroimaging sample size with the longest follow-up to date to examine neural volume trajectories in adolescent heavy drinkers compared to non-using youth. Findings suggest that heavy alcohol use during adolescence is associated with interruptions in both gray and white matter development.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Luciana M, Collins PF, Muetzel RL, Lim KO. Effects of alcohol use initiation on brain structure in typically developing adolescents. Am J Drug Alcohol Abuse. 2013;39(6):345–55.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Pfefferbaum A, Lim KO, Zipursky RB, Mathalon DH, Rosenbloom MJ, Lane B, et al. Brain gray and white matter volume loss accelerates with aging in chronic alcoholics: A quantitative MRI study. Alcohol Clin Exp Res. 1992;16(6):1078–89.CrossRefPubMedGoogle Scholar
  62. 62.
    Pfefferbaum A, Mathalon DH, Sullivan EV, Rawles JM, Zipursky RB, Lim KO. A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. Arch Neurol. 1994;51(9):874–87.CrossRefPubMedGoogle Scholar
  63. 63.
    Pfefferbaum A, Rohlfing T, Rosenbloom MJ, Chu W, Colrain IM, Sullivan EV. Variation in longitudinal trajectories of regional brain volumes of healthy men and women (ages 10 to 85 years) measured with atlas-based parcellation of MRI. NeuroImage. 2013;65:176–93.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Jacobus J, Squeglia LM, Meruelo AD, Castro N, Brumback T, Giedd JN, Tapert SF. Cortical thickness in adolescent marijuana and alcohol users: A three-year prospective study from adolescence to young adulthood. Dev Cogn Neurosci. 2015;16:101–9. Google Scholar
  65. 65.
    Jacobus J, Squeglia LM, Sorg SF, Nguyen-Louie TT, Tapert SF. Cortical thickness and neurocognition in adolescent marijuana and alcohol users following 28 days of monitored abstinence. J Stud Alcohol Drugs. 2014;75(5):729–43.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Shollenbarger SG, Price J, Wieser J, Lisdahl K. Poorer frontolimbic white matter integrity is associated with chronic cannabis use, FAAH genotype, and increased depressive and apathy symptoms in adolescents and young adults. NeuroImage Clinical. 2015;8:117–1125.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Wilson S, Malone SM, Thomas KM, Iacono WG. Adolescent drinking and brain morphometry: A co-twin control analysis. Dev Cogn Neurosci. 2015;16:130–8.Google Scholar
  68. 68.
    Groenman AP, Greven CU, van Donkelaar MM, Schellekens A, van Hulzen K, Rommelse N, et al. Dopamine and serotonin genetic risk scores predicting substance and nicotine use in attention deficit/hyperactivity disorder. Addict Biol. 2015.Google Scholar
  69. 69.
    Gruber SA, Dahlgren MK, Sagar KA, Gönenç A, Lukas SE. Worth the wait: Effects of age of onset of marijuana use on white matter and impulsivity. Psychopharmacology. 2014;231(8):1455–65.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Baker ST, Yücel M, Fornito A, Allen NB, Lubman DI. A systematic review of diffusion weighted MRI studies of white matter microstructure in adolescent substance users. Neurosci Biobehav Rev. 2013;37(8):1713–23.CrossRefPubMedGoogle Scholar
  71. 71.
    Bava S, Jacobus J, Thayer RE, Tapert SF. Longitudinal changes in white matter integrity among adolescent substance users. Alcohol Clin Exp Res. 2013;37 Suppl 1:E181–9.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Jacobus J, Squeglia LM, Bava S, Tapert SF. White matter characterization of adolescent binge drinking with and without co-occurring marijuana use: A 3-year investigation. Psychiatry Res. 2013;214(3):374–81.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Jacobus J, Squeglia LM, Infante MA, Bava S, Tapert SF. White matter integrity pre- and post marijuana and alcohol initiation in adolescence. Brain Sci. 2013;3(1):396–414.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Epstein KA, Kumra S. White matter fractional anisotropy over two time points in early onset schizophrenia and adolescent cannabis use disorder: A naturalistic diffusion tensor imaging study. Psychiatry Res. 2015;232(1):34–41.CrossRefPubMedGoogle Scholar
  75. 75.
    Wetherill RR, Squeglia LM, Yang TT, Tapert SF. A longitudinal examination of adolescent response inhibition: neural differences before and after the initiation of heavy drinking. Psychopharmacology. 2013.Google Scholar
  76. 76.
    Berns GS, Moore S, Capra CM. Adolescent engagement in dangerous behaviors is associated with increased white matter maturity of frontal cortex. PLoS ONE. 2009;4(8), e6773.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Li Q, Sun J, Guo L, Zang Y, Feng Z, Huang X, et al. Increased fractional anisotropy in white matter of the right frontal region in children with attention-deficit/hyperactivity disorder: A diffusion tensor imaging study. Neuroendocrinol Lett. 2010;31(6):747–53.PubMedGoogle Scholar
  78. 78.
    Sarkar S, Craig MC, Catani M, Dell’acqua F, Fahy T, Deeley Q, et al. Frontotemporal white-matter microstructural abnormalities in adolescents with conduct disorder: a diffusion tensor imaging study. Psychol Med. 2013;43(2):401–11.CrossRefPubMedGoogle Scholar
  79. 79.
    Stoodley CJ, Schmahmann JD. Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex. 2010;46(7):831–44.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Cservenka A, Jones SA. Nagel BJ. Developmental Cognitive Neuroscience: Reduced cerebellar brain activity during reward processing in adolescent binge drinkers; 2015.Google Scholar
  81. 81.
    Jacobus J, Goldenberg D, Wierenga CE, Tolentino NJ, Liu TT, Tapert SF. Altered cerebral blood flow and neurocognitive correlates in adolescent cannabis users. Psychopharmacology. 2012;222(4):675–84.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Brumback T, Squeglia LM, Jacobus J, Pulido C, Tapert SF, Brown SA. Adolescent heavy drinkers’ amplified brain responses to alcohol cues decrease over one month of abstinence. Addict Behav. 2015;46:45–52.CrossRefPubMedGoogle Scholar
  83. 83.
    Squeglia LM, Spadoni AD, Infante MA, Myers MG, Tapert SF. Initiating moderate to heavy alcohol use predicts changes in neuropsychological functioning for adolescent girls and boys. Psychol Addict Behav. 2009;23(4):715–22.CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Squeglia LM, Schweinsburg AD, Pulido C, Tapert SF. Adolescent binge drinking linked to abnormal spatial working memory brain activation: differential gender effects. Alcohol Clin Exp Res. 2011;35(10):1831–41.CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Squeglia LM, Sorg SF, Schweinsburg AD, Wetherill RR, Pulido C, Tapert SF. Binge drinking differentially affects adolescent male and female brain morphometry. Psychopharmacology. 2012;220(3):529–39.CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Thatcher DL, Pajtek S, Chung T, Terwilliger RA, Clark DB. Gender differences in the relationship between white matter organization and adolescent substance use disorders. Drug Alcohol Depend. 2010;110(1-2):55–61.CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Schweinsburg AD, Schweinsburg BC, Cheung EH, Brown GG, Brown SA, Tapert SF. fMRI response to spatial working memory in adolescents with comorbid marijuana and alcohol use disorders. Drug Alcohol Depend. 2005;79:201–10.CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Schweinsburg AD, Schweinsburg BC, Nagel BJ, Eyler LT, Tapert SF. Neural correlates of verbal learning in adolescent alcohol and marijuana users. Addiction. 2011;106(3):564–73.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    De Bellis MD, Wang L, Bergman SR, Yaxley RH, Hooper SR, Huettel SA. Neural mechanisms of risky decision-making and reward response in adolescent onset cannabis use disorder. Drug Alcohol Depend. 2013;133(1):134–45.CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Houck JM, Bryan AD, Feldstein Ewing SW. Functional connectivity and cannabis use in high-risk adolescents. Am J Drug Alcohol Abuse. 2013;39(6):414–23.CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Orr C, Morioka R, Behan B, Datwani S, Doucet M, Ivanovic J, et al. Altered resting-state connectivity in adolescent cannabis users. Am J Drug Alcohol Abuse. 2013;39(6):372–81.CrossRefPubMedGoogle Scholar
  92. 92.
    Jager G, Block RI, Luijten M, Ramsey NF. Cannabis use and memory brain function in adolescent boys: a cross-sectional multicenter functional magnetic resonance imaging study. J Am Acad Child Adolesc Psychiatry. 2010;49(6):561–72.PubMedPubMedCentralGoogle Scholar
  93. 93.
    Cousijn J, Vingerhoets WA, Koenders L, de Haan L, van den Brink W, Wiers RW, et al. Relationship between working-memory network function and substance use: a 3-year longitudinal fMRI study in heavy cannabis users and controls. Addict Biol. 2014;19(2):282–93.CrossRefPubMedGoogle Scholar
  94. 94.
    Chadwick B, Miller ML, Hurd YL. Cannabis use during adolescent development: susceptibility to psychiatric illness. Front Psychiatr. 2013;4:129.CrossRefGoogle Scholar
  95. 95.
    Hasler BP, Sitnick SL, Shaw DS, Forbes EE. An altered neural response to reward may contribute to alcohol problems among late adolescents with an evening chronotype. Psychiatry Res. 2013;214(3):357–64.CrossRefPubMedGoogle Scholar
  96. 96.
    Lopez-Larson MP, Bogorodzki P, Rogowska J, McGlade E, King JB, Terry J, et al. Altered prefrontal and insular cortical thickness in adolescent marijuana users. Behav Brain Res. 2011;220(1):164–72.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Addiction Sciences Division, Department of Psychiatry and Behavioral SciencesMedical University of South CarolinaCharlestonUSA
  2. 2.Child and Adolescent Psychiatry Division, Department of Psychiatry and Behavioral SciencesMedical University of South CarolinaCharlestonUSA

Personalised recommendations