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Verbal learning and memory in adolescent cannabis users, alcohol users and non-users

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Abstract

Rationale

Long-term heavy cannabis use can result in memory impairment. Adolescent users may be especially vulnerable to the adverse neurocognitive effects of cannabis.

Objectives and methods

In a cross-sectional and prospective neuropsychological study of 181 adolescents aged 16–20 (mean 18.3 years), we compared performance indices from one of the most widely used measures of learning and memory—the Rey Auditory Verbal Learning Test—between cannabis users (n = 52; mean 2.4 years of use, 14 days/month, median abstinence 20.3 h), alcohol users (n = 67) and non-user controls (n = 62) matched for age, education and premorbid intellectual ability (assessed prospectively), and alcohol consumption for cannabis and alcohol users.

Results

Cannabis users performed significantly worse than alcohol users and non-users on all performance indices. They recalled significantly fewer words overall (p < 0.001), demonstrating impaired learning (p < 0.001), retention (p < 0.001) and retrieval (p < 0.05) (Cohen’s d 0.43–0.84). The degree of impairment was associated with the duration, quantity, frequency and age of onset of cannabis use, but was unrelated to alcohol exposure or other drug use. No gender effects were detected and the findings remained after controlling for premorbid intellectual ability. An earlier age of onset of regular cannabis use was associated with worse memory performance after controlling for extent of exposure to cannabis.

Conclusions

Despite relatively brief exposure, adolescent cannabis users relative to their age-matched counterparts demonstrated similar memory deficits to those reported in adult long-term heavy users. The results indicate that cannabis adversely affects the developing brain and reinforce concerns regarding the impact of early exposure.

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References

  • Allen JP, Litten RZ, Fertig JB, Babor T (1997) A review of research on the Alcohol Use Disorders Identification Test (AUDIT). Alcohol Clin Exp Res 21:613–619

    Article  PubMed  CAS  Google Scholar 

  • Allin M, Khan O, Walshe M, Kontis D, Nosarti C, Barker G, Rifkin L, Murray RMB (2009) Cannabis smoking and white matter in healthy volunteers. Schizophr Bull 35(Suppl 1):201

    Google Scholar 

  • Arnone D, Barrick TR, Chengappa S, Mackay CE, Clark CA, Abou-Saleh MT (2008) Corpus callosum damage in heavy marijuana use: preliminary evidence from diffusion tensor tractography and tract-based spatial statistics. Neuroimage 41:1067–1074

    Article  PubMed  CAS  Google Scholar 

  • Ashtari M, Cervellione K, Cottone J, Ardekani BA, Kumra S (2009) Diffusion abnormalities in adolescents and young adults with a history of heavy cannabis use. J Psychiatr Res 43:189–204

    Article  PubMed  Google Scholar 

  • Barron S, White A, Swartzwelder HS, Bell RL, Rodd ZA, Slawecki CJ, Ehlers CL, Levin ED, Rezvani AH, Spear LP (2005) Adolescent vulnerabilities to chronic alcohol or nicotine exposure: findings from rodent models. Alcohol Clin Exp Res 29:1720–1725

    Article  PubMed  CAS  Google Scholar 

  • Bava S, Frank LR, McQueeny T, Schweinsburg BC, Schweinsburg AD, Tapert SF (2009) Altered white matter microstructure in adolescent substance users. Psychiatry Res Neuroimaging 173:228–237

    Article  Google Scholar 

  • Beck AT, Steer RA, Brown GK (1996) Manual for the beck depression inventory-II. Psychological Corporation, San Antonio

    Google Scholar 

  • Bolla KI, Brown K, Eldreth D, Tate K, Cadet JL (2002) Dose-related neurocognitive effects of marijuana use. Neurology 59:1337–1343

    PubMed  CAS  Google Scholar 

  • Brown SA, Tapert SF, Delis DC, Granholm E (2000) Neurocognitive functioning of adolescents: effects of protracted alcohol use. Alcohol Clin Exp Res 42:164–171

    Article  Google Scholar 

  • Budney AJ, Novy P, Hughes JR (1999) Marijuana withdrawal among adults seeking treatment for marijuana dependence. Addiction 94:1311–1322

    Article  PubMed  CAS  Google Scholar 

  • Cha YM, White AM, Kuhn CM, Wilson WA, Swartzwelder HS (2006) Differential effects of delta9-THC on learning in adolescent and adult rats. Pharmacol Biochem Behav 83:448–455

    Article  PubMed  CAS  Google Scholar 

  • Ciarrochi J, Heaven PC (2008) Learned social hopelessness: the role of explanatory style in predicting social support during adolescence. J Child Psychol Psychiatry 49:1279–1286

    Article  PubMed  Google Scholar 

  • Consroe P, Carlini EA, Zwicker AP, Lacerda LA (1979) Interaction of cannabidiol and alcohol in humans. Psychopharmacology 66:45–50

    Article  PubMed  CAS  Google Scholar 

  • Copeland J, Swift W (2009) Cannabis use disorder: epidemiology and management. Int Rev Psychiatry 21:96–103

    Article  PubMed  Google Scholar 

  • Croft RJ, Mackay AJ, Mills ATD, Gruzelier JGH (2001) The relative contributions of ecstasy and cannabis to cognitive impairment. Psychopharmacology 153:373–379

    Article  PubMed  CAS  Google Scholar 

  • De Bellis MD, Clark DB, Beers SR, Soloff PH, Boring AM, Hall J, Kersh A, Keshavan MS (2000) Hippocampal volume in adolescent-onset alcohol use disorders. Am J Psychiatry 157:737–744

    Article  PubMed  Google Scholar 

  • Degenhardt L, Lynskey M, Hall W (2000) Cohort trends in the age of initiation of drug use in Australia. Aust N Z J Public Health 24:421–426

    Article  PubMed  CAS  Google Scholar 

  • Degenhardt L, Chiu WT, Sampson N, Kessler RC, Anthony JC, Angermeyer M, Bruffaerts R, de Girolamo G, Gureje O, Huang Y, Karam A, Kostyuchenko S, Lepine JP, Mora MEM, Neumark Y, Ormel JH, Pinto-Meza A, Posada-Villa J, Stein DJ, Takeshima T, Wells JE (2008) Toward a global view of alcohol, tobacco, cannabis, and cocaine use: findings from the WHO World Mental Health Surveys. PLoS Med 5:e141

    Article  PubMed  Google Scholar 

  • Ehrenreich H, Rinn T, Kunert HJ, Moeller MR, Poser W, Schilling L, Gigerenzer G, Hoehe MR (1999) Specific attentional dysfunction in adults following early start of cannabis use. Psychopharmacology 142:295–301

    Article  PubMed  CAS  Google Scholar 

  • European Monitoring Centre for Drugs and Drug Addiction (EMCDDA) (2009) The state of the drugs problem in Europe: Annual Report 2009. Publications Office of the European Union, Luxembourg

    Google Scholar 

  • Fletcher JM, Page B, Francis DJ, Copeland K, Naus MJ, Davis CM, Morris R, Krauskopf D, Satz P (1996) Cognitive correlates of long-term cannabis use in Costa Rican men. Arch Gen Psychiatry 53:1051–1057

    PubMed  CAS  Google Scholar 

  • Hansen HH, Krutz B, Sifringer M, Stefovska V, Bittigau P, Pragst F, Marsicano G, Lutz B, Ikonomidou C (2008) Cannabinoids enhance susceptibility of immature brain to ethanol neurotoxicity. Ann Neurol 64:42–52

    Article  PubMed  CAS  Google Scholar 

  • Harvey MA, Sellman JD, Porter RJ, Frampton CM (2007) The relationship between non-acute adolescent cannabis use and cognition. Drug Alcohol Rev 26:309–319

    Article  PubMed  Google Scholar 

  • Huestegge L, Radach R, Kunert HJ, Heller D (2002) Visual search in long-term cannabis users with early age of onset. Prog Brain Res 140:377–394

    Article  PubMed  Google Scholar 

  • Huestis MA, Cone EJ (2004) Relationship of Δ9-tetrahydrocannabinol concentrations in oral fluid and plasma after controlled administration of smoked cannabis. J Anal Toxicol 28:394–399

    PubMed  CAS  Google Scholar 

  • Jacobsen LK, Mencl WE, Westerveld M, Pugh KR (2004) Impact of cannabis use on brain function in adolescents. Ann N Y Acad Sci 1021:384–390

    Article  PubMed  Google Scholar 

  • Jacobsen LK, Pugh KR, Constable RT, Westerveld M, Mencl WE (2007) Functional correlates of verbal memory deficits emerging during nicotine withdrawal in abstinent adolescent cannabis users. Biol Psychiatry 61:31–40

    Article  PubMed  CAS  Google Scholar 

  • Jacobus J, Bava S, Cohen-Zion M, Mahmood O, Tapert SF (2009) Functional consequences of marijuana use in adolescents. Pharmacol Biochem Behav 92:559–565

    Article  PubMed  CAS  Google Scholar 

  • Johnston LD, O’Malley PM, Bachman JG, Schulenberg JE (2010) Monitoring the Future national results on adolescent drug use: overview of key findings, 2009. NIH Publication. National Institute on Drug Abuse, Bethesda

    Google Scholar 

  • Kempel P, Lampe K, Parnefjord R, Hennig J, Kunert HJ (2003) Auditory-evoked potentials and selective attention: different ways to information processing in cannabis users and controls. Neuropsychobiology 48:95–101

    Article  PubMed  CAS  Google Scholar 

  • Kessler RC, Andrews G, Colpe LJ, Hiripi E, Mroczek DK, Normand SLT, Walters EE, Zaslavsky AM (2002) Short screening scales to monitor population prevalences and trends in non-specific psychological distress. Psychol Med 32:959–956

    Article  PubMed  CAS  Google Scholar 

  • Kuntsche E, Simons-Morton B, Fotiou A, ter Bogt T, Kokkevi A (2009) Decrease in adolescent cannabis use from 2002 to 2006 and links to evenings out with friends in 31 European and North American countries and regions. Arch Pediatr Adolesc Med 163:119–125

    Article  PubMed  Google Scholar 

  • Lezak MD, Howieson DB, Loring DW (2004) Neuropsychological assessment, 4th edn. Oxford University Press, Oxford

    Google Scholar 

  • Lubman DI, Yücel M, Hall W (2007) Substance use and the adolescent brain: a toxic combination? J Psychopharmacol 21:792–794

    Article  PubMed  Google Scholar 

  • Lynskey M, Hall W (2000) The effects of adolescent cannabis use on educational attainment: a review. Addiction 95:1621–1630

    Article  PubMed  CAS  Google Scholar 

  • Martin CA, Kelly TH, Rayens MK, Brogli BR, Brenzel A, Smith WJ, Omar HA (2002) Sensation seeking, puberty and nicotine, alcohol and marijuana use in adolescence. J Am Acad Child Adolesc Psychiatry 41:1495–502

    Article  PubMed  Google Scholar 

  • Martin G, Copeland J, Gates P, Gilmour S (2006) The severity of dependence scale (SDS) in an adolescent population of cannabis users: reliability, validity and diagnostic cut-off. Drug Alcohol Depend 83:90–93

    Article  PubMed  Google Scholar 

  • Mata I, Perez-Iglesias R, Roiz-Santiañez R, Tordesillas-Gutierrez D, Pazos A, Gutierrez A, Vazquez-Barquero JL, Crespo-Facorro B (2010) Gyrification brain abnormalities associated with adolescence and early-adulthood cannabis use. Brain Res 1317:297–304

    Article  PubMed  CAS  Google Scholar 

  • Medina KL, Schweinsburg AD, Cohen-Zion M, Nagel BJ, Tapert SF (2007) Effects of alcohol and combined marijuana and alcohol use during adolescence on hippocampal volume and asymmetry. Neurotoxicol Teratol 29:141–152

    Article  PubMed  CAS  Google Scholar 

  • Messinis L, Kyprianidou A, Malefaki S, Papathansopoulos P (2006) Neuropsychological deficits in long-term frequent cannabis users. Neurology 66:737–739

    Article  PubMed  Google Scholar 

  • Monti PM, Miranda R, Nixon K, Sher KJ, Swartzwelder HS, Tapert SF, White A, Crews FT (2005) Adolescence: booze, brains, and behavior. Alcohol Clin Exp Res 29:207–220

    Article  PubMed  Google Scholar 

  • Nagel BJ, Schweinsburg AD, Phan V, Tapert SF (2005) Reduced hippocampal volume among adolescents with alcohol use disorders without psychiatric comorbidity. Psychiatry Res 139:181–190

    Article  PubMed  Google Scholar 

  • Niedbala RS, Kardos KW, Fritch DF, Kardos S, Fries T, Waga J, Robb J, Cone EJ (2001) Detection of marijuana use by oral fluid and urine analysis following single-dose administration of smoked and oral marijuana. J Anal Toxicol 25:289–303

    PubMed  CAS  Google Scholar 

  • Parrott A, Gouzoulis-Meyfrank E, Rodgers J, Solowij N (2004) Ecstasy/MDMA and cannabis: the complexities of their interactive neuropsychobiological effects. J Psychopharmacology 18:579–582

    Article  Google Scholar 

  • Paus T (2005) Mapping brain maturation and cognitive development during adolescence. Trends Cogn Sci 9:60–68

    Article  PubMed  Google Scholar 

  • Pope HG, Yurgelun-Todd D (1996) The residual cognitive effects of heavy marijuana use in college students. JAMA 275:521–527

    Article  PubMed  CAS  Google Scholar 

  • Pope HG, Gruber AJ, Hudson JI, Heustis MA, Yurgelun-Todd D (2001) Neuropsychological performance in long-term cannabis users. Arch Gen Psychiatry 58:909–915

    Article  PubMed  Google Scholar 

  • Pope HG Jr, Gruber AJ, Hudson JI, Cohane G, Huestis MA, Yurgelun-Todd D (2003) Early-onset cannabis use and cognitive deficits: what is the nature of the association? Drug Alcohol Depend 69:303–310

    Article  PubMed  Google Scholar 

  • Schepis TS, Adinoff B, Rao U (2008) Neurobiological processes in adolescent addictive disorders. Am J Addict 17:6–23

    Article  PubMed  Google Scholar 

  • Schneider M (2008) Puberty as a highly vulnerable developmental period for the consequences of cannabis exposure. Addict Biol 13:253–263

    Article  PubMed  Google Scholar 

  • Schwartz RH, Gruenewald PJ, Klitzner M, Fedio P (1989) Short-term memory impairment in cannabis-dependent adolescents. Am J Dis Child 143:1214–1219

    PubMed  CAS  Google Scholar 

  • Schweinsburg AD, Schweinsburg BC, Cheung EH, Brown GG, Brown SA, Tapert SF (2005) fMRI response to spatial working memory in adolescents with comorbid marijuana and alcohol use disorders. Drug Alc Depend 79:201–210

    Article  Google Scholar 

  • Simon NG, Mattick RP (2002) The impact of regular ecstasy use on memory function. Addiction 97:1523–1529

    Article  PubMed  Google Scholar 

  • Simons J, Correia CJ, Carey KB (2000) A comparison of motives for marijuana and alcohol use among experienced users. Addict Behav 25:153–160

    Article  PubMed  CAS  Google Scholar 

  • Sobell LC, Sobell MB (1992) Timeline follow-back: a technique for assessing self-reported alcohol consumption. In: Litten RZ, Allen JP (eds) Measuring alcohol consumption: psychosocial and biochemical methods. Humana, Totowa NJ, pp 41–72

    Google Scholar 

  • Solowij N, Battisti R (2008) The chronic effects of cannabis on memory in humans: a review. Curr Drug Abuse Rev 1:81–98

    Article  PubMed  Google Scholar 

  • Solowij N, Pesa N (2010) Cognitive abnormalities and cannabis use. Rev Bras Psiquiatr 32(Suppl 1):31–40

    Google Scholar 

  • Solowij N, Stephens R, Roffman R, Babor T, Kadden R, Miller M, Christiansen K, McRee B, Vendetti J (2002) Cognitive functioning of long-term heavy cannabis users seeking treatment. JAMA 287:1123–1131

    Article  PubMed  Google Scholar 

  • Solowij N, Yücel M, Respondek C, Whittle S, Lindsay E, Pantelis C, Lubman DI (2011) Cerebellar white matter changes in cannabis users with and without schizophrenia. Psychol Med (in press)

  • Spielberger CD (1989) State-trait anxiety inventory: a comprehensive bibliography. Consulting Psychologists, Palo Alto

    Google Scholar 

  • Swift W, Copeland J, Hall W (1998) Choosing a diagnostic cut-off for cannabis dependence. Addiction 93:1681–1692

    Article  PubMed  CAS  Google Scholar 

  • Vandrey R, Budney AJ, Kamon JL, Stanger C (2005) Cannabis withdrawal in adolescent treatment seekers. Drug Alcohol Depend 78:205–210

    Article  PubMed  Google Scholar 

  • Wilson W, Mathew R, Turkington T, Hawk T, Coleman RE, Provenzale J (2000) Brain morphological changes and early marijuana use: a magnetic resonance and positron emission tomography study. J Addict Dis 19:1–22

    Article  PubMed  CAS  Google Scholar 

  • Yücel M, Lubman DI, Solowij N, Brewer W (2007) Understanding drug addiction: a neuropsychological perspective. Aust NZ J Psychiatry 41:957–969

    Article  Google Scholar 

  • Yücel M, Solowij N, Respondek C, Whittle S, Fornito A, Pantelis C, Lubman DI (2008) Regional brain abnormalities associated with long-term heavy cannabis use. Arch Gen Psychiatry 65:694–701

    Article  PubMed  Google Scholar 

  • Yücel M, Lubman DI, Solowij N, Brewer WJ (2009) Neurobiological and neuropsychological pathways into substance use and addictive behaviour. In: Wood SJ, Allen NB, Pantelis C (eds) The neuropsychology of mental illness. Cambridge University Press, Cambridge, pp 326–341

    Chapter  Google Scholar 

  • Yücel M, Zalesky A, Takagi MJ, Bora E, Fornito A, Ditchfield M, Egan GF, Pantelis C, Lubman DI (2010) Age-related white-matter abnormalities in long-term inhalant misusing adolescents: a diffusion MRI comparison with cannabis users and drug-naive controls. J Psychiatry Neurosci 65:409-412

    Google Scholar 

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Acknowledgements

This research was supported by grants from the National Health and Medical Research Council of Australia (Grants 459111, 514604) and the Australian Research Council (Grants LP0453853, DP0878925). The authors have full control of the data and the study concept and design, and have no conflicts of interest to declare. Dr Yücel is supported by a National Health and Medical Research Council Clinical Career Development Award (Grant 509345). We thank Dr Peter Leeson and Robert Battisti for assistance with project management.

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Authors and Affiliations

  1. School of Psychology, University of Wollongong, Northfields Ave, Wollongong, NSW, 2522, Australia

    Nadia Solowij, Katy A. Jones, Megan E. Rozman, Sasha M. Davis, Joseph Ciarrochi & Patrick C. L. Heaven

  2. Illawarra Health and Medical Research Institute, University of Wollongong, Wollongong, NSW, 2522, Australia

    Nadia Solowij, Joseph Ciarrochi & Patrick C. L. Heaven

  3. Schizophrenia Research Institute, Sydney, NSW, 2010, Australia

    Nadia Solowij

  4. Turning Point Alcohol and Drug Centre, Eastern Health and Monash University, Melbourne, VIC, 3065, Australia

    Katy A. Jones & Dan I. Lubman

  5. Orygen Youth Health Research Centre, Centre for Youth Mental Health, University of Melbourne, Parkville, VIC, 3052, Australia

    Dan I. Lubman & Murat Yücel

  6. Melbourne Neuropsychiatry Centre, Department of Psychiatry, University of Melbourne and Melbourne Health, Melbourne, VIC, 3053, Australia

    Murat Yücel

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  1. Nadia Solowij
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  2. Katy A. Jones
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  3. Megan E. Rozman
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  4. Sasha M. Davis
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Correspondence to Nadia Solowij.

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Solowij, N., Jones, K.A., Rozman, M.E. et al. Verbal learning and memory in adolescent cannabis users, alcohol users and non-users. Psychopharmacology 216, 131–144 (2011). https://doi.org/10.1007/s00213-011-2203-x

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