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Neuropsychological Trajectories Associated with Adolescent Alcohol and Cannabis Use: A Prospective 14-Year Study

Published online by Cambridge University Press:  11 December 2019

M. Alejandra Infante
Affiliation:
Department of Psychiatry, University of California San Diego, La Jolla, CA92093, USA
Tam T. Nguyen-Louie
Affiliation:
Cogstate Ltd., New Haven, CT, USA
Matthew Worley
Affiliation:
Department of Psychiatry, University of California San Diego, La Jolla, CA92093, USA
Kelly E. Courtney
Affiliation:
Department of Psychiatry, University of California San Diego, La Jolla, CA92093, USA
Clarisa Coronado
Affiliation:
Department of Psychiatry, University of California San Diego, La Jolla, CA92093, USA
Joanna Jacobus*
Affiliation:
Department of Psychiatry, University of California San Diego, La Jolla, CA92093, USA
*
*Correspondence and reprint requests to: Joanna Jacobus, Department of Psychiatry, University of California San Diego, 9500 Gilman Drive, MC 0405, La Jolla, CA 92093, USA. E-mail: jjacobus@ucsd.edu

Abstract

Objectives:

Alcohol and cannabis remain the substances most widely used by adolescents. Better understanding of the dynamic relationship between trajectories of substance use in relation to neuropsychological functioning is needed. The aim of this study was to examine the different impacts of within- and between-person changes in alcohol and cannabis use on neuropsychological functioning over multiple time points.

Methods:

Hierarchical linear modeling examined the effects of alcohol and cannabis use on neuropsychological functioning over the course of 14 years in a sample of 175 adolescents (aged 12–15 years at baseline).

Results:

Time-specific fluctuations in alcohol use (within-person effect) predicted worse performance across time on the Wechsler Abbreviated Scale of Intelligence Block Design subtest (B = −.05, SE = .02, p = .01). Greater mean levels of percent days of cannabis use across time (between-person effect) were associated with an increased contrast score between Delis–Kaplan Executive Function System Color Word Inhibition and Color Naming conditions (B = .52, SE = .14, p < .0001) and poorer performance over time on Block Design (B = −.08, SE = .04, p = .03). Neither alcohol and/nor cannabis use over time was associated with performance in the verbal memory and processing speed domains.

Conclusions:

Greater cumulative cannabis use over adolescence may be linked to poorer inhibitory control and visuospatial functioning performance, whereas more proximal increases in alcohol consumption during adolescence may drive alcohol-related performance decrements in visuospatial functioning. Results from this prospective study add to the growing body of literature on the impact of alcohol and cannabis use on cognition from adolescent to young adulthood.

Type
Regular Research
Copyright
Copyright © INS. Published by Cambridge University Press, 2019

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References

REFERENCES

American Psychiatric Association (2000). Diagnostic and Statistical Manual of Mental Disorders (4th ed., text revision). Washington, DC: American Psychiatric Association.Google Scholar
Barber, A.D., Caffo, B.S., Pekar, J.J., & Mostofsky, S.H. (2013). Developmental changes in within- and between-network connectivity between late childhood and adulthood. Neuropsychologia, 51, 156167. doi: 10.1016/j.neuropsychologia.2012.11.011CrossRefGoogle ScholarPubMed
Behan, B., Connolly, C.G., Datwani, S., Doucet, M., Ivanovic, J., Morioka, R., Stone, A., Watts, R., Smyth, B., & Garavan, H. (2014). Response inhibition and elevated parietal-cerebellar correlations in chronic adolescent cannabis users. Neuropharmacology, 84, 131137. doi: 10.1016/j.neuropharm.2013.05.027CrossRefGoogle ScholarPubMed
Blest-Hopley, G., Giampietro, V., & Bhattacharyya, S. (2019). Regular cannabis use is associated with altered activation of central executive and default mode networks even after prolonged abstinence in adolescent users: results from a complementary meta-analysis. Neuroscience & Biobehavioral Reviews, 96, 4555. doi: 10.1016/j.neubiorev.2018.10.026CrossRefGoogle ScholarPubMed
Brown, L.A., Brockmole, J.R., Gow, A.J., & Deary, I.J. (2012). Processing speed and visuospatial executive function predict visual working memory ability in older adults. Experimental Aging Research, 38, 119. doi: 10.1080/0361073X.2012.636722CrossRefGoogle ScholarPubMed
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, 427438. doi: 10.15288/jsa.1998.59.427CrossRefGoogle ScholarPubMed
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, 164171.CrossRefGoogle ScholarPubMed
Brumback, T.Y., Worley, M., Nguyen-Louie, T.T., Squeglia, L.M., Jacobus, J., & Tapert, S.F. (2016). Neural predictors of alcohol use and psychopathology symptoms in adolescents. Development and Psychopathology, 28, 12091216. doi: 10.1017/s0954579416000766CrossRefGoogle ScholarPubMed
Crean, R.D., Crane, N.A., & Mason, B.J. (2011). An evidence based review of acute and long-term effects of cannabis use on executive cognitive functions. Journal of Addiction Medicine, 5, 18. doi: 10.1097/ADM.0b013e31820c23faCrossRefGoogle ScholarPubMed
Curran, P.J. & Bauer, D.J. (2011). The disaggregation of within-person and between-person effects in longitudinal models of change. Annual Review of Psychology, 62, 583619. doi: 10.1146/annurev.psych.093008.100356CrossRefGoogle ScholarPubMed
Dahlgren, M.K., Sagar, K.A., Racine, M.T., Dreman, M.W., & Gruber, S.A. (2016). Marijuana use predicts cognitive performance on tasks of executive function. Journal of Studies on Alcohol and Drugs, 77, 298308.CrossRefGoogle ScholarPubMed
Delis, D.C., Kaplan, E., & Kramer, J.H. (2001). The Delis-Kaplan Executive Function System: Examiner’s Manual. San Antonio, TX: The Psychological Corporation.Google Scholar
Delis, D.C., Kramer, J.H., Kaplan, E., & Ober, B.A. (1994). Manual for the California Verbal Learning Test–Children’s Version. San Antonio, TX: The Psychological Corporation.Google Scholar
Ernst, M. (2014). The triadic model perspective for the study of adolescent motivated behavior. Brain Cognition, 89, 104111. doi: 10.1016/j.bandc.2014.01.006CrossRefGoogle Scholar
Ferrett, H.L., Carey, P.D., Thomas, K.G., Tapert, S.F., & Fein, G. (2010). Neuropsychological performance of South African treatment-naïve adolescents with alcohol dependence. Drug and Alcohol Dependence, 110, 814. doi: 10.1016/j.drugalcdep.2010.01.019CrossRefGoogle ScholarPubMed
Fontes, M.A., Bolla, K.I., Cunha, P.J., Almeida, P.P., Jungerman, F., Laranjeira, R.R., Bressan, R.A., & Lacerda, A.L. (2011). Cannabis use before age 15 and subsequent executive functioning. British Journal of Psychiatry, 198, 442447. doi: 10.1192/bjp.bp.110.077479CrossRefGoogle ScholarPubMed
Giancola, P.R., Mezzich, A.C., & Tarter, R.E. (1998). Disruptive, delinquent and aggressive behavior in female adolescents with a psychoactive substance use disorder: relation to executive cognitive functioning. Journal of Studies on Alcohol, 59, 560567.CrossRefGoogle ScholarPubMed
Giancola, P.R. & Parker, A.M. (2001). A six-year prospective study of pathways toward drug use in adolescent boys with and without a family history of a substance use disorder. Journal of Studies on Alcohol, 62, 166178.CrossRefGoogle ScholarPubMed
Gil-Hernandez, S., Mateos, P., Porras, C., Garcia-Gomez, R., Navarro, E., & Garcia-Moreno, L.M. (2017). Alcohol binge drinking and executive functioning during adolescent brain development. Frontiers in Psychology, 8, 1638. doi: 10.3389/fpsyg.2017.01638CrossRefGoogle ScholarPubMed
Gonzalez, R., Pacheco-Colón, I., Duperrouzel, J.C., & Hawes, S.W. (2017). Does cannabis use cause declines in neuropsychological functioning? A review of longitudinal studies. Journal of the International Neuropsychological Society, 23, 893902. doi: 10.1017/S1355617717000789CrossRefGoogle ScholarPubMed
Green, A., Garrick, T., Sheedy, D., Blake, H., Shores, E.A., & Harper, C. (2010). The effect of moderate to heavy alcohol consumption on neuropsychological performance as measured by the repeatable battery for the assessment of neuropsychological status. Alcoholism: Clinical and Experimental Research, 34, 443450. doi: 10.1111/j.1530-0277.2009.01108.xCrossRefGoogle ScholarPubMed
Groth-Marnat, G. & Teal, M. (2000). Block design as a measure of everyday spatial ability: a study of ecological ability. Perceptual & Motor Skills, 90, 522526.CrossRefGoogle ScholarPubMed
Gruber, S.A., Dahlgren, M.K., Sagar, K.A., Gönenc, A., & Killgore, W.D. (2012). Age of onset of marijuana use impacts inhibitory processing. Neuroscience Letters, 511, 8994. doi: 10.1016/j.neulet.2012.01.039CrossRefGoogle ScholarPubMed
Gruber, S.A. & Yurgelun-Todd, D.A. (2005). Neuroimaging of marijuana smokers during inhibitory processing: a pilot investigation. Cognitive Brain Research, 23, 107118. doi: 10.1016/j.cogbrainres.2005.02.016CrossRefGoogle ScholarPubMed
Hollingshead, A.B. (1965). Two-Factor Index of Social Position. New Haven, CT: Yale University Press.Google Scholar
Jackson, N.J., Isen, J.D., Khoddam, R., Irons, D., Tuvblad, C., Iacono, W.G., McGue, M., Raine, A., & Baker, L.A. (2016). Impact of adolescent marijuana use on intelligence: results from two longitudinal twin studies. Proceedings of the National Academy of Sciences of the United States of America, 113, E500508. doi: 10.1073/pnas.1516648113CrossRefGoogle ScholarPubMed
Jacobus, J., Squeglia, L.M., Infante, M.A., Castro, N., Brumback, T., Meruelo, A.D., & Tapert, S.F. (2015). Neuropsychological performance in adolescent marijuana users with co-occurring alcohol use: a three-year longitudinal study. Neuropsychology, 29, 829843. doi: 10.1037/neu0000203CrossRefGoogle ScholarPubMed
Jacobus, J. & Tapert, S.F. (2014). Effects of cannabis on the adolescent brain. Current Pharmaceutical Design, 20, 21862193.CrossRefGoogle ScholarPubMed
Johnston, L.D., Miech, R.A., O’Malley, P.M., Bachman, J.G., Schulenberg, J.E., & Patrick, M.E. (2019). Monitoring the Future National Survey Results on Drug Use 1975-2018. Ann Arbor: Institute for Social Research, University of Michigan.Google Scholar
Kundu, P., Benson, B.E., Rosen, D., Frangou, S., Leibenluft, E., Luh, W.M., Bandettini, P.A., Pine, D.S., & Ernst, M. (2018). The integration of functional brain activity from adolescence to adulthood. The Journal of Neuroscience, 38, 35593570.CrossRefGoogle Scholar
Lezak, M.D., Howieson, D.B., & Loring, D.W. (2004). Neuropsychological Assessment (4th ed.). Oxford, UK: Oxford University Press.Google Scholar
Lisdahl, K.M. & Price, J.S. (2012). Increased marijuana use and gender predict poorer cognitive functioning in adolescents and emerging adults. Journal of the International Neuropsychological Society, 18, 678688. doi: 10.1017/S1355617712000276CrossRefGoogle ScholarPubMed
Luciana, M., Bjork, J.M., Nagel, B.J., Barch, D.M., Gonzalez, R., Nixon, S.J., & Banich, M.T. (2018). Adolescent neurocognitive development and impacts of substance use: overview of the adolescent brain cognitive development (ABCD) baseline neurocognition battery. Developmental Cognitive Neuroscience, 32, 6779. doi: 10.1016/j.dcn.2018.02.006CrossRefGoogle ScholarPubMed
Lyons, M.J., Bar, J.L., Panizzon, M.S., Toomey, R., Eisen, S., Xian, H., & Tsuang, M.T. (2004). Neuropsychological consequences of regular marijuana use: a twin study. Psychological Medicine, 34, 12391250.CrossRefGoogle ScholarPubMed
Mathias, C.W., Blumenthal, T.D., Dawes, M.A., Liguori, A., Richard, D.M., Bray, B., Tong, W., & Dougherty, D.M. (2011). Failure to sustain prepulse inhibition in adolescent marijuana users. Drug and Alcohol Dependence, 116, 110116. doi: 10.1016/j.drugalcdep.2010.11.020CrossRefGoogle 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, 807820. doi: 10.1017/s1355617707071032CrossRefGoogle ScholarPubMed
Meier, M.H., Caspi, A., Ambler, A., Harrington, H., Houts, R., Keefe, R.S., McDonald, K., Ward, A., Poulton, R., & Moffitt, T.E. (2012). Persistent cannabis users show neuropsychological decline from childhood to midlife. Proceedings of the National Academy of Sciences of the United States of America, 109, E26572664. doi: 10.1073/pnas.1206820109CrossRefGoogle ScholarPubMed
Meier, M.H., Caspi, A., Danese, A., Fisher, H.L., Houts, R.Arseneault, L., Moffitt, T.E. (2018). Associations between adolescent cannabis use and neuropsychological decline: a longitudinal co-twin control study. Addiction. 113(2):257265. doi: 10.1111/add.13946CrossRefGoogle ScholarPubMed
Meruelo, A.D., Castro, N., Cota, C.I., & Tapert, S.F. (2017). Cannabis and alcohol use, and the developing brain. Behavioural Brain Research, 325, 4450. doi: 10.1016/j.bbr.2017.02.025CrossRefGoogle ScholarPubMed
Nguyen-Louie, T.T., Castro, N., Matt, G.E., Squeglia, L.M., Brumback, T., & Tapert, S.F. (2015). Effects of emerging alcohol and marijuana use behaviors on adolescents’ neuropsychological functioning over four years. Journal of Studies on Alcohol and Drugs, 76, 738748. doi: 10.15288/jsad.2015.76.738CrossRefGoogle ScholarPubMed
Nguyen-Louie, T.T., Matt, G.E., Jacobus, J., Li, I., Cota, C., Castro, N., & Tapert, S.F. (2017). Earlier alcohol use onset predicts poorer neuropsychological functioning in young adults. Alcoholism: Clinical and Experimental Research, 41, 20822092. doi: 10.1111/acer.13503CrossRefGoogle ScholarPubMed
Nguyen-Louie, T.T., Simmons, A.N., Squeglia, L.M., Alejandra Infante, M., Schacht, J.P., & Tapert, S.F. (2018). Earlier alcohol use onset prospectively predicts changes in functional connectivity. Psychopharmacology (Berl), 235, 10411054. doi: 10.1007/s00213-017-4821-4CrossRefGoogle ScholarPubMed
Nguyen-Louie, T.T., Tracas, A., Squeglia, L.M., Matt, G.E., Eberson-Shumate, S., & Tapert, S.F. (2016). Learning and memory in adolescent moderate, binge, and extreme-binge drinkers. Alcoholism: Clinical and Experimental Research, 40, 18951904. doi: 10.1111/acer.13160CrossRefGoogle ScholarPubMed
Parada, M., Corral, M., Mota, N., Crego, A., Rodríguez Holguín, S., & Cadaveira, F. (2012). Executive functioning and alcohol binge drinking in university students. Addictive Behaviors, 37, 167172. doi: 10.1016/j.addbeh.2011.09.015CrossRefGoogle ScholarPubMed
Rubia, K. (2013). Functional brain imaging across development. European Child & Adolescent Psychiatry, 22, 719731. doi: 10.1007/s00787-012-0291-8CrossRefGoogle ScholarPubMed
Rubia, K., Smith, A.B., Taylor, E., & Brammer, M. (2007). Linear age-correlated functional development of right inferior fronto-striato-cerebellar networks during response inhibition and anterior cingulate during error-related processes. Human Brain Mapping, 28, 11631177. doi: 10.1002/hbm.20347CrossRefGoogle ScholarPubMed
Scott, J.C., Slomiak, S.T., Jones, J.D., Rosen, A.F.G., Moore, T.M., & Gur, R.C. (2018). Association of cannabis with cognitive functioning in adolescents and young adults: a systematic review and meta-analysis. JAMA Psychiatry, 75, 585595. doi: 10.1001/jamapsychiatry.2018.0335CrossRefGoogle Scholar
Selya, A.S., Rose, J.S., Dierker, L.C., Hedeker, D., & Mermelstein, R.J. (2012). A practical guide to calculating Cohen’s f2, a measure of local effect size, from PROC MIXED. Frontiers in Psychology, 3, article 111.CrossRefGoogle Scholar
Sneider, J.T., Cohen-Gilbert, J.E., Crowley, D.J., Paul, M.D., & Silveri, M.M. (2013). Differential effects of binge drinking on learning and memory in emerging adults. Journal of Addiction Research and Therapy, Suppl 7. doi: 10.4172/2155-6105.s7-006CrossRefGoogle Scholar
Solowij, N., Jones, K.A., Rozman, M.E., Davis, S.M., Ciarrochi, J., Heaven, P.C., Lubman, D.I., & Yücel, M. (2011). Verbal learning and memory in adolescent cannabis users, alcohol users and non-users. Psychopharmacology (Berl), 216, 131144. doi: 10.1007/s00213-011-2203-xCrossRefGoogle ScholarPubMed
Solowij, N., Jones, K.A., Rozman, M.E., Davis, S.M., Ciarrochi, J., Heaven, P.C., Pesa, N., Lubman, D.I., & Yucel, M. (2012). Reflection impulsivity in adolescent cannabis users: a comparison with alcohol-using and non-substance-using adolescents. Psychopharmacology (Berl), 219, 575586. doi: 10.1007/s00213-011-2486-yCrossRefGoogle ScholarPubMed
Spear, L.P. (2000). The adolescent brain and age-related behavioral manifestations. Neuroscience & Biobehavioral Reviews, 24, 417463.CrossRefGoogle ScholarPubMed
Squeglia, L.M., Jacobus, J., & Tapert, S.F. (2009). The influence of substance use on adolescent brain development. Clinical EEG and Neuroscience, 40, 3138. doi: 10.1177/155005940904000110CrossRefGoogle ScholarPubMed
Squeglia, L.M., Schweinsburg, A.D., Pulido, C., & Tapert, S.F. (2011). Adolescent binge drinking linked to abnormal spatial working memory brain activation: differential gender effects. Alcoholism: Clinical and Experimental Research, 35, 18311841. doi: 10.1111/j.1530-0277.2011.01527.xCrossRefGoogle ScholarPubMed
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, 715722. doi: 10.1037/a0016516CrossRefGoogle ScholarPubMed
Squeglia, L.M., Tapert, S.F., Sullivan, E.V., Jacobus, J., Meloy, M.J., Rohlfing, T., & Pfefferbaum, A. (2015). Brain development in heavy-drinking adolescents. The American Journal of Psychiatry, 172, 531542. doi: 10.1176/appi.ajp.2015.14101249CrossRefGoogle ScholarPubMed
Statacorp (2007). Stata Statistical Software: Release 10. Statacorp LP, College Station, TX.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, 481493.CrossRefGoogle ScholarPubMed
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, 873883.CrossRefGoogle ScholarPubMed
Tarter, R.E., Mezzich, A.C., Hsieh, Y.C., & Parks, S.M. (1995). Cognitive capacity in female adolescent substance abusers. Drug and Alcohol Dependence, 39, 1521.CrossRefGoogle ScholarPubMed
Thoma, R.J., Monnig, M.A., Lysne, P.A., Ruhl, D.A., Pommy, J.A., Bogenschutz, M., Tonigan, J.S., & Yeo, R.A. (2011). Adolescent substance abuse: the effects of alcohol and marijuana on neuropsychological performance. Alcoholism: Clinical and Experimental Research, 35, 3946. doi: 10.1111/j.1530-0277.2010.01320.xCrossRefGoogle ScholarPubMed
Verdejo-Garcia, A., Rivas-Perez, C., Lopez-Torrecillas, F., & Perez-Garcia, M. (2006). Differential impact of severity of drug use on frontal behavioral symptoms. Addictive Behaviors, 31, 13731382. doi: 10.1016/j.addbeh.2005.11.003CrossRefGoogle ScholarPubMed
Volkow, N.D., Koob, G.F., Croyle, R.T., Bianchi, D.W., Gordon, J.A., Koroshetz, W.J., Pérez-Stable, E.J., Riley, W.T., Bloch, M.H., Conway, K., & Weiss, S.R.B. (2018). The conception of the ABCD study: from substance use to a broad NIH collaboration. Developmental Cognitive Neuroscience, 32, 47. doi: 10.1016/j.dcn.2017.10.002CrossRefGoogle ScholarPubMed
Wechsler, D. (1997). Wechsler Adult Intelligence Scale (3rd ed.). New York: The Psychological Corporation.Google Scholar
Wechsler, D. (1999). Wechsler Abbreviated Scale of Intelligence. San Antonio, TX: The Psychological Corporation.Google Scholar
Wechsler, D. Wechsler Intelligence Scale for Children. 3rd ed. New York, NY: Psychological Corporation; 1991.Google Scholar
Wilson, J., Freeman, T.P., & Mackie, C.J. (2019). Effects of increasing cannabis potency on adolescent health. The Lancet Child & Adolescent Health, 3, 121128. doi: 10.1016/S2352-4642(18)30342-0CrossRefGoogle ScholarPubMed
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, 218229. doi: 10.1017/s1355617713001410CrossRefGoogle ScholarPubMed
Winward, J.L., Hanson, K.L., Tapert, S.F., & Brown, S.A. (2014). Heavy alcohol use, marijuana use, and concomitant use by adolescents are associated with unique and shared cognitive decrements. Journal of the International Neuropsychological Society, 20, 784795. doi: 10.1017/s1355617714000666CrossRefGoogle ScholarPubMed
Worley, M.J., Trim, R.S., Tate, S.R., Roesch, S.C., Myers, M.G., & Brown, S.A. (2014). Self-efficacy and social networks after treatment for alcohol or drug dependence and major depression: disentangling person and time-level effects. Psychology of Addictive Behaviors, 28, 12201229. doi: 10.1037/a0037901CrossRefGoogle ScholarPubMed
Yanes, J.A., Riedel, M.C., Ray, K.L., Kirkland, A.E., Bird, R.T., Boeving, E.R., Reid, M.A., Gonzalez, R., Robinson, J.L., Laird, A.R., & Sutherland, M.T. (2018). Neuroimaging meta-analysis of cannabis use studies reveals convergent functional alterations in brain regions supporting cognitive control and reward processing. Journal of Psychopharmacology, 32, 283295. doi: 10.1177/0269881117744995CrossRefGoogle ScholarPubMed