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Heavy Alcohol Use, Marijuana Use, and Concomitant Use by Adolescents Are Associated with Unique and Shared Cognitive Decrements

Published online by Cambridge University Press:  22 September 2014

Jennifer L. Winward ,
Karen L. Hanson ,
Susan F. Tapert  and
Sandra A. Brown
Jennifer L. Winward
Affiliation:
Department of Psychology, University of California, San Diego, La Jolla, California
Karen L. Hanson
Affiliation:
Department of Psychiatry, University of California, San Diego, La Jolla, California VA Center of Excellence for Stress and Mental Health, San Diego, California Veterans Affairs San Diego Healthcare System, San Diego, California
Susan F. Tapert
Affiliation:
Department of Psychiatry, University of California, San Diego, La Jolla, California Veterans Affairs San Diego Healthcare System, San Diego, California
Sandra A. Brown*
Affiliation:
Department of Psychology, University of California, San Diego, La Jolla, California Department of Psychiatry, University of California, San Diego, La Jolla, California
*
Correspondence and reprint requests to: Sandra A. Brown, University of California, San Diego, 9500 Gilman Drive (MC 0043), La Jolla, CA 92093-0043. E-mail: sandrabrown@ucsd.edu
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Abstract

To assess recovery of cognitive effects, we investigated neuropsychological performance after 1 month of monitored abstinence in teens with histories of heavy episodic drinking, protracted marijuana use, or concomitant use of alcohol and marijuana. Adolescents (ages 16–18 years) with histories of heavy episodic drinking (HED; n=24), marijuana use (MJ; n=20), both heavy alcohol and marijuana use (HED+MJ; n=29), and socio-demographically similar control teens (CON; n=55) completed a neuropsychological battery following 4 weeks of monitored abstinence. Groups were similar on 5th grade standardized test scores, suggesting comparable academic functioning before onset of substance use. Relative to CON, HED showed poorer cognitive flexibility (p=.006), verbal recall (p=.024), semantic clustering (p=.011), and reading skills (p=.018). MJ performed worse than CON on inhibition task accuracy (p=.015), cued verbal memory (p=.031), and psychomotor speed (p=.027). Similar to HED youth, HED+MJ showed differences relative to CON on cognitive flexibility (p=.024) and verbal recall (p=.049). As with MJ teens, HED+MJ showed poorer task accuracy (p=.020). Unique to the HED+MJ group was poorer working memory (p=.012) relative to CON. For all substance using participants, worse performance across domains correlated with more lifetime use of alcohol and of marijuana, more withdrawal symptoms from alcohol, and earlier age of onset of marijuana use (ps<.05). Heavy alcohol use, marijuana use, and concomitant use of both substances during adolescence appear to be associated with decrements in cognitive functioning, and each substance (or combination of substances) may be linked to poorer performance in specific cognitive domains (JINS, 2014, 20, 784–795).

Keywords

Neuropsychological performanceAlcoholMarijuanaExecutive functioningMemoryLanguage
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 20 , Issue 8 , September 2014 , pp. 784 - 795
Copyright
Copyright © The International Neuropsychological Society 2014 

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References

REFERENCES

Achenbach, T.M., & Ruffle, T.M. (2000). The Child Behavior Checklist and related forms for assessing behavioral/emotional problems and competencies. Pediatric Review, 21(8), 265–271.Google Scholar
Anderson, K.G., Ramo, D.E., Cummins, K., & Brown, S.A. (2010). Alcohol and drug involvement after adolescent treatment and functioning during emerging adulthood. Drug and Alcohol Dependence, 107(2-3), 171–181.Google Scholar
Ashtari, M., Avants, B., Cyckowski, L., Cervellione, K.L., Roofeh, D., Cook, P., & Kumra, S. (2011). Medial temporal structures and memory functioning in adolescents with heavy cannabis use. Journal of Psychiatry Research, 45, 1055–1066.Google Scholar
Barbey, A.K., Koenigs, M., & Grafman, J. (2013). Dorsolateral prefrontal contributions to human working memory. Cortex, 49(5), 1195–1205.Google Scholar
Benes, F.M., Turtle, M., Khan, Y., & Farol, P. (1994). Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood. Archives of General Psychiatry, 51(6), 477–484.CrossRefGoogle ScholarPubMed
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological), 57(1), 289–300.Google Scholar
Brown, S., Anderson, K., Schulte, M., Sintov, N., & Frissell, K. (2005). Facilitating youth self change through school based intervention. Addictive Behaviors, 30(9), 1797–1810.Google Scholar
Brown, S.A., McGue, M., Maggs, J., Schulenberg, J., Hingson, R., Swartzwelder, S., & Murphy, S. (2008). A developmental perspective on alcohol and youths 16 to 20 years of age. Pediatrics, 121(Suppl. 4), S290–S310.Google Scholar
Brown, S.A., Myers, M.G., Lippke, L., Tapert, S.F., Stewart, D.G., & Vik, P.W. (1998). Psychometric evaluation of the Customary Drinking and Drug Use Record (CDDR): A measure of adolescent alcohol and drug involvement. Journal of Studies on Alcohol, 59(4), 427–438.Google Scholar
Brown, S.A., & Tapert, S.F. (2004). Adolescence and the trajectory of alcohol use: Basic to clinical studies. Annals of the New York Academy of Sciences, 1021, 234–244.Google Scholar
Brown, S.A., Tapert, S.F., Granholm, E., & Delis, D.C. (2000). Neurocognitive functioning of adolescents: Effects of protracted alcohol use. Alcoholism: Clinical and Experimental Research, 24, 164–171.CrossRefGoogle ScholarPubMed
Brown, S.A., Vik, P.W., & Creamer, V.A. (1989). Characteristics of relapse following adolescent substance abuse treatment. Addictive Behaviors, 14, 291–300.Google Scholar
Cha, Y.M., White, A.M., Kuhn, C.M., Wilson, W.A., & Swartzwelder, H.S. (2006). Differential effects of delta9-THC on learning in adolescent and adult rats. Pharmacology, Biochemistry, and Behavior, 83, 448–455.Google Scholar
Churchwell, J.C., Lopez-Larson, M., & Yurgelun-Todd, D.A. (2010). Altered frontal cortical volume and decision making in adolescent cannabis users. Frontiers in Psychology, 1, 225.Google Scholar
Cousijn, J., Wiers, R.W., Ridderinkhof, K.R., van den Brink, W., Veltman, D.J., & Goudrian, A.E. (2012). Grey matter alterations associated with cannabis use: Results of a VBM study in heavy cannabis users and healthy controls. Neuroimage, 59, 3845–3851.Google Scholar
Crews, F.T., Braun, C.J., Hoplight, B., Switzer, R.C. III, & Knapp, D.J. (2000). Binge ethanol consumption causes differential brain damage in young adolescent rats compared with adult rats. Alcoholism: Clinical and Experimental Research, 24(11), 1712–1723.CrossRefGoogle ScholarPubMed
De Bellis, M.D., Clark, D.B., Beers, S.R., Soloff, P.H., Boring, A.M., Hall, J., & Keshavan, M.S. (2000). Hippocampal volume in adolescent-onset alcohol use disorders. American Journal of Psychiatry, 157(5), 737–744.Google Scholar
De Bellis, M.D., Narasimhan, A., Thatcher, D.L., Keshavan, M.S., Soloff, P., & Clark, D.B. (2005). Prefrontal cortex, thalamus, and cerebellar volumes in adolescents and young adults with adolescent onset alcohol use disorders and co-morbid mental disorders. Alcoholism: Clinical and Experimental Research, 29, 1590–1600.Google Scholar
Delis, D.C., Kaplan, E., & Kramer, J.H. (2001). Manual for the Delis-Kaplan Executive Function System (D-KEFS). San Antonio, TX: Psychological Corp.Google Scholar
Delis, D.C., Kramer, J.H., Kaplan, E., & Ober, B.A. (2000). Manual for the California Verbal Learning Test, 2nd edition (CVLT-II). San Antonio, TX: Psychological Corp.Google Scholar
Ernst, M., Grant, S.J., London, E.D., Contoreggi, C.S., Kimes, A.S., & Spurgeon, L. (2003). Decision making in adolescents with behavior disorders and adults with substance abuse. American Journal of Psychiatry, 160(1), 33–40.Google Scholar
Fryer, S.L., Frank, L.R., Spadoni, A.D., Theilmann, R.J., Nagel, B.J., Schweinsburg, A.D., & Tapert, S.F. (2008). Microstructural integrity of the corpus callosum linked with neuropsychological performance in adolescents. Brain and Cognition, 67, 225–233.Google Scholar
Giancola, P.R., & Mezzich, A.C. (2000). Neuropsychological deficits in female adolescents with a substance use disorder: Better accounted for by conduct disorder? Journal of Studies on Alcohol, 61(6), 809–817.Google Scholar
Giancola, P.R., & Moss, H.B. (1998). Executive cognitive functioning in alcohol use disorders. Recent Developments in Alcoholism, 14, 227–251.CrossRefGoogle ScholarPubMed
Giancola, P.R., Shoal, G.D., & Mezzich, A.C. (2001). Constructive thinking, executive functioning, antisocial behavior, and drug use involvement in adolescent females with a substance use disorder. Experimental and Clinical Psychopharmacology, 9(2), 215–227.Google Scholar
Giedd, J.N., Blumenthal, J., Jeffries, N.O., Castellanos, F.X., Liu, H., Zijdenbos, A., & Rapoport, J.L. (1999). Brain development during childhood and adolescence: A longitudinal MRI study. Nature Neuroscience, 2, 861–863.CrossRefGoogle ScholarPubMed
Gogtay, N., Giedd, J.N., Lusk, L., Hayashi, K.M., Greenstein, D., Vaituzis, A.C., & Thompson, P.M. (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(21), 8174–8179.Google Scholar
Goudriaan, A.E., Grekin, E.R., & Sher, K.J. (2007). Decision making and binge drinking: A longitudinal study. Alcoholism: Clinical and Experimental Research, 31(6), 928–938.Google Scholar
Hamilton, M. (1996). The Hamilton Rating Scale for Depression. New York: Springer-Verlag.Google Scholar
Hansen, H.H., Krutz, B., Sifringer, M., Stefovska, V., Bittigau, P., Pragst, F., & Ikonomidou, C. (2008). Cannabinoids enhance susceptibility of immature brain to ethanol neurotoxicity. Annals of Neurology, 64, 42–52.Google Scholar
Hanson, K.L., Medina, K.L., Padula, C.B., Tapert, S.F., & Brown, S.A. (2011). Impact of adolescent alcohol and drug use on neuropsychological functioning in young adulthood: 10-year outcomes. Journal of Child & Adolescent Substance Abuse, 20(2), 135–154.Google Scholar
Hanson, K.L., Winward, J.L., Schweinsburg, A.D., Medina, K.L., Brown, S.A., & Tapert, S.F. (2010). Longitudinal study of cognition among adolescent marijuana users over three weeks of abstinence. Addictive Behaviors, 35(11), 970–976.Google Scholar
Harvey, M.A., Sellman, J.D., Porter, R.J., & Frampton, C.M. (2007). The relationship between non-acute adolescent cannabis use and cognition. Drug and Alcohol Review, 26, 309–319.Google Scholar
Hollingshead, A.B. (1965). Two-factor index of social position . New Haven, CT: Yale University Press.Google Scholar
Jernigan, T.L., & Gamst, A.C. (2005). Changes in volume with age: Consistency and interpretation of observed effects. Neurobiology of Aging, 26(9), 1271–1274.CrossRefGoogle ScholarPubMed
Johnston, L.D., O’Malley, P.M., Miech, R.A., Bachman, J.G., & Schulenberg, J.E. (2014). Monitoring the future national results on drug use: 1975-2013: Overview, key findings on adolescent drug use. Ann Arbor, MI: Institute for Social Research, The University of Michigan.Google Scholar
Mahmood, O.M., Jacobus, J., Bava, S., Scarlett, A., & Tapert, S.F. (2010). Learning and memory performance in adolescent users of alcohol and marijuana: Interactive effects. Journal of Studies on Alcohol and Drugs, 71, 885–894.Google Scholar
McGue, M., Iacono, W.G., Legrand, L.N., & Elkins, I. (2001). Origins and consequences of age at first drink. II. Familial risk and heritability. Alcoholism: Clinical and Experimental Research, 25(8), 1166–1173.CrossRefGoogle ScholarPubMed
McQueeny, T., Schweinsburg, B.C., Schweinsburg, A.D., Jacobus, J., Bava, S., & Frank, L.R. (2009). Altered white matter integrity in adolescent binge drinkers. Alcoholism: Clinical and Experimental Research, 33(7), 1278–1285.CrossRefGoogle ScholarPubMed
Medina, K.L., Hanson, K.L., Schweinsburg, A.D., Cohen-Zion, M., Nagel, B.J., & Tapert, S.F. (2007). Neuropsychological functioning in adolescent marijuana users: Subtle deficits detectable after a month of abstinence. Journal of the International Neuropsychological Society, 13, 807–820.Google Scholar
Medina, K.L., McQueeny, T., Nagel, B.J., Hanson, K.L., Schweinsburg, A.D., & Tapert, S.F. (2008). Prefrontal cortex volumes in adolescents with alcohol use disorders: Unique gender effects. Alcoholism: Clinical and Experimental Research, 32, 386–394.Google Scholar
Medina, K.L., Nagel, B.J., & Tapert, S.F. (2010). Abnormal cerebellar morphometry in abstinent adolescent marijuana users. Psychiatry Research, 182, 152–159.Google Scholar
Miller, W.R., & Rollnick, S. (1991). Motivational interviewing: Preparing people to change addictive behavior. New York: Guilford Press.Google Scholar
Millsaps, C.L., Azrin, R.L., & Mittenberg, W. (1994). Neuropsychological effects of chronic cannabis use on the memory and intelligence of adolescence. Journal of Child & Adolescent Substance Abuse, 3, 47–54.CrossRefGoogle Scholar
Moss, H.B., Kirisci, L., Gordon, H.W., & Tarter, R.E. (1994). A neuropsychologic profile of adolescent alcoholics. Alcoholism: Clinical and Experimental Research, 18, 159–163.Google Scholar
Nagel, B.J., Barlett, V.C., Schweinsburg, A.D., & Tapert, S.F. (2005). Neuropsychological predictors of BOLD response during a spatial working memory task in adolescents: What can performance tell us about fMRI response patterns? Journal of Clinical and Experimental Neuropsychology, 27(7), 823–839.Google Scholar
Nagel, B.J., Schweinsburg, A.D., Phan, V., & Tapert, S.F. (2005). Reduced hippocampal volume among adolescents with alcohol use disorders without psychiatric comorbidity. Psychiatry Research, 139(3), 181–190.Google Scholar
National Institute on Alcohol Abuse and Alcoholism. (2002). High-risk drinking in college: What we know and what we need to learn Final Report of the Panel on Contexts and Consequences, Task Force of the National Advisory Council on Alcohol Abuse and Alcoholism. Bethesda, MD: Department of Health and Human Service.Google Scholar
Nixon, S.J., Tivis, R., Ceballos, N., Varner, J.L., & Rohrbaugh, J. (2002). Neurophysiological efficiency in male and female alcoholics. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 26(5), 919–927.Google Scholar
Osterrieth, P.A. (1944). Le test de copie d’une figure complexe. Archives of Psychology, 30, 206–356.Google Scholar
Paus, T., Zijdenbos, A., Worsley, K., Collins, D.L., Blumenthal, J., Giedd, J.N., & Evans, A.C. (1999). Structural maturation of neural pathways in children and adolescents: In vivo study. Science, 283(5409), 1908–1911.Google Scholar
Pfefferbaum, A., Mathalon, D.H., Sullivan, E.V., Rawles, J.M., Zipursky, R.B., & Lim, K.O. (1994). A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. Archives of Neurology, 51, 874–887.Google Scholar
Rice, J.P., Reich, T., Bucholz, K.K., Neuman, R.J., Fishman, R., Rochberg, N., & Begleiter, H. (1995). Comparison of direct interview and family history diagnoses of alcohol dependence. Alcoholism: Clinical and Experimental Research, 19(4), 1018–1023.Google Scholar
Roehrs, T., Beare, D., Zorick, F., & Roth, T. (1994). Sleepiness and ethanol effects on simulated driving. Alcoholism: Clinical and Experimental Research, 18, 154–158.Google Scholar
Rubino, T., Realini, N., Braida, D., Guidi, S., Capurro, V., Vigano, D., & Parolaro, D. (2009). Changes in hippocampal morphology and neuroplasticity induced by adolescent THC treatment are associated with cognitive impairment in adulthood. Hippocampus, 19, 763–772.Google Scholar
Schneider, M., & Koch, M. (2003). Chronic pubertal, but not adult chronic cannabinoid treatment impairs sensorimotor gating, recognition memory, and the performance in a progressive ratio task in adult rats. Neuropsychopharmacology, 28, 1760–1769.Google Scholar
Schneider, M., Schomig, E., & Leweke, F.M. (2008). Acute and chronic cannabinoid treatment differentially affects recognition memory and social behavior in pubertal and adult rats. Addiction Biology, 13, 345–357.Google Scholar
Schwartz, R.H., Gruenewald, P.J., Klitzner, M., & Fedio, P. (1989). Short-term memory impairment in cannabis-dependent adolescents. American Journal of Diseases of Children, 143, 1214–1219.Google Scholar
Schweinsburg, A.D., Schweinsburg, B.C., Cheung, E.H., Brown, G.G., Brown, S.A., & Tapert, S.F. (2005). fMRI response to spatial working memory in adolescents with comorbid marijuana and alcohol use disorders. Drug and Alcohol Dependence, 79(2), 201–210.Google Scholar
Shaffer, D., Fisher, P., Lucas, C.P., Dulcan, M.K., & Schwab-Stone, M.E. (2000). NIMH Diagnostic Interview Schedule for Children Version IV (NIMH DISC-IV): Description, differences from previous versions, and reliability of some common diagnoses. Journal of the American Academy of Child and Adolescent Psychiatry, 39(1), 28–38.Google Scholar
Sher, K.J., Martin, E.D., Wood, P.K., & Rutledge, P.C. (1997). Alcohol use disorders and neuropsychological functioning in first-year undergraduates. Experimental and Clinical Psychopharmacology, 5(3), 304–315.CrossRefGoogle ScholarPubMed
Silveri, M.M., & Spear, L.P. (1998). Decreased sensitivity to the hypnotic effects of ethanol early in ontogeny. Alcoholism: Clinical and Experimental Research, 22(3), 670–676.Google Scholar
Slawecki, C.J. (2002). Altered EEG responses to ethanol in adult rats exposed to ethanol during adolescence. Alcoholism: Clinical and Experimental Research, 26(2), 246–254.Google Scholar
Slawecki, C.J., Betancourt, M., Cole, M., & Ehlers, C.L. (2001). Periadolescent alcohol exposure has lasting effects on adult neurophysiological function in rats. Developmental Brain Research, 128(1), 63–72.Google Scholar
Slawecki, C.J., & Roth, J. (2004). Comparison of the onset of hypoactivity and anxiety-like behavior during alcohol withdrawal in adolescent and adult rats. Alcoholism: Clinical and Experimental Research, 28(4), 598–607.Google Scholar
Sobell, L.C., & Sobell, M.B. (1992). Timeline follow-back: A technique for assessing self-reported alcohol consumption. In R.Z. Litten & J.P. Allen (Eds.), Measuring alcohol consumption: Psychosocial and biochemical methods. (pp. 41–72). Totowa, NJ: Humana Press.Google Scholar
Solowij, N., Jones, K.A., Rozman, M.E., Davis, S.M., Ciarrochi, J., Heaven, P.C., & Yucel, M. (2011). Verbal learning and memory in adolescent cannabis users, alcohol users, and non-users. Psychopharmacology (Berl), 216, 131–144.Google Scholar
Sowell, E.R., Delis, D., Stiles, J., & Jernigan, T.L. (2001). Improved memory functioning and frontal lobe maturation between childhood and adolescence: A structural MRI study. Journal of the International Neuropsychological Society, 7(3), 312–322.Google Scholar
Spielberger, C.D., Gorsuch, R.L., & Lushene, R.E. (1970). Manual for the State-Trait Anxiety Inventory. Palo Alto, CA: Consulting Psychologists Press.Google Scholar
Squeglia, L.M., Spadoni, A.D., Infante, M.A., Myers, M.G., & Tapert, S.F. (2009). Initiating moderate to heavy alcohol use predicts changes in neuropsychological functioning for adolescent girls and boys. Psychology of Addictive Behaviors, 23(4), 715–722.Google Scholar
Stewart, D.G., & Brown, S.A. (1995). Withdrawal and dependency symptoms among adolescent alcohol and drug abusers. Addiction, 90, 627–635.Google Scholar
Stiglick, A., & Kalant, H. (1982). Learning impairment in the radial arm maze following prolonged cannabis treatment in rats. Psychopharmacology, 77(2), 117–123.CrossRefGoogle ScholarPubMed
Tapert, S.F., Brown, G.G., Kindermann, S., Cheung, E.H., Frank, L.R., & Brown, S.A. (2001). fMRI measurement of brain dysfunction in alcohol-dependent young women. Alcoholism: Clinical and Experimental Research, 25, 236–245.Google Scholar
Tapert, S.F., & Brown, S.A. (1999). Neuropsychological correlates of adolescent substance abuse: Four year outcomes. Journal of the International Neuropsychological Society, 5(6), 481–493.Google Scholar
Tapert, S.F., Granholm, E., Leedy, N.G., & Brown, S.A. (2002). Substance use and withdrawal: Neuropsychological functioning over 8 years in youth. Journal of the International Neuropsychological Society, 8(7), 873–883.Google Scholar
Tapert, S.F., Schweinsburg, A.D., Barlett, V.C., Brown, S.A., Frank, L.R., Brown, G.G., & Meloy, M.J. (2004). Blood oxygen level dependent response and spatial working memory in adolescents with alcohol use disorders. Alcoholism: Clinical and Experimental Research, 28(10), 1577–1586.Google Scholar
Tapert, S.F., Schweinsburg, A.D., Drummond, S.P.A., Paulus, M.P., Brown, S.A., Yang, T.T., & Frank, L.R. (2007). Functional MRI of inhibitory processing in abstinent adolescent marijuana users. Psychopharmacology (Berl), 194, 173–183.Google Scholar
Ward, R.J., Colivicchi, M.A., Allen, R., Schol, F., Lallemand, F., de Witte, P., & Dexter, D. (2009). Neuro-inflammation induced in the hippocampus of 'binge drinking' rats may be mediated by elevated extracellular glutamate content. Journal of Neurochemistry, 111(5), 1119–1128.Google Scholar
Wechsler, D. (1997). Manual for the Wechsler Adult Intelligence Scale-III. San Antonio, TX: Psychological Corp.Google Scholar
Wechsler, D. (1999). Wechsler Abbreviated Scale of Intelligence. San Antonio, TX: Psychological Corp.Google Scholar
Weissenborn, R., & Duka, T. (2003). Acute alcohol effects on cognitive function in social drinkers: Their relationship to drinking habits. Psychopharmacology (Berl), 165, 306–312.Google Scholar
White, A.M., Ghia, A.J., Levin, E.D., & Swartzwelder, H.S. (2000). Binge pattern ethanol exposure in adolescent and adult rats: Differential impact on subsequent responsiveness to ethanol. Alcoholism, Clinical and Experimental Research, 24(8), 1251–1256.Google Scholar
Wilkinson, G.S., & Robertson, G.J. (2006). The Wide Range Achievement Test-4 administration manual. Lutz, FL: Psychological Assessment Resources.Google Scholar
Winward, J.L., Hanson, K.L., Bekman, N.M., Tapert, S.F., & Brown, S.A. (2014). Adolescent heavy episodic drinking: Neurocognitive functioning during early abstinence. Journal of the International Neuropsychological Society, 20, 218–229.Google Scholar
Yucel, M., Zalesky, A., Takagi, M., Bora, E., Fornito, A., Ditchfield, M., & Lubman, D.I. (2010). White-matter abnormalities in adolescents with long-term inhalant and cannabis use: A diffusion magnetic resonance imaging study. Journal of Psychiatry and Neuroscience, 35(6), 409–412.Google Scholar