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Psychopharmacology

, Volume 216, Issue 1, pp 131–144 | Cite as

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

  • Nadia SolowijEmail author
  • Katy A. Jones
  • Megan E. Rozman
  • Sasha M. Davis
  • Joseph Ciarrochi
  • Patrick C. L. Heaven
  • Dan I. Lubman
  • Murat Yücel
Original Investigation

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.

Keywords

Adolescence Alcohol Cannabis Cognition Marijuana Verbal memory 

Notes

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.

Supplementary material

213_2011_2203_MOESM1_ESM.doc (105 kb)
Esm 1 Verbal learning and memory in adolescent cannabis users, alcohol users and non-users. (DOC 105 kb)

References

  1. 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 21:613–619PubMedCrossRefGoogle Scholar
  2. 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):201Google Scholar
  3. 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 41:1067–1074PubMedCrossRefGoogle Scholar
  4. 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 43:189–204PubMedCrossRefGoogle Scholar
  5. 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 29:1720–1725PubMedCrossRefGoogle Scholar
  6. Bava S, Frank LR, McQueeny T, Schweinsburg BC, Schweinsburg AD, Tapert SF (2009) Altered white matter microstructure in adolescent substance users. Psychiatry Res Neuroimaging 173:228–237CrossRefGoogle Scholar
  7. Beck AT, Steer RA, Brown GK (1996) Manual for the beck depression inventory-II. Psychological Corporation, San AntonioGoogle Scholar
  8. Bolla KI, Brown K, Eldreth D, Tate K, Cadet JL (2002) Dose-related neurocognitive effects of marijuana use. Neurology 59:1337–1343PubMedGoogle Scholar
  9. Brown SA, Tapert SF, Delis DC, Granholm E (2000) Neurocognitive functioning of adolescents: effects of protracted alcohol use. Alcohol Clin Exp Res 42:164–171CrossRefGoogle Scholar
  10. Budney AJ, Novy P, Hughes JR (1999) Marijuana withdrawal among adults seeking treatment for marijuana dependence. Addiction 94:1311–1322PubMedCrossRefGoogle Scholar
  11. 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 83:448–455PubMedCrossRefGoogle Scholar
  12. Ciarrochi J, Heaven PC (2008) Learned social hopelessness: the role of explanatory style in predicting social support during adolescence. J Child Psychol Psychiatry 49:1279–1286PubMedCrossRefGoogle Scholar
  13. Consroe P, Carlini EA, Zwicker AP, Lacerda LA (1979) Interaction of cannabidiol and alcohol in humans. Psychopharmacology 66:45–50PubMedCrossRefGoogle Scholar
  14. Copeland J, Swift W (2009) Cannabis use disorder: epidemiology and management. Int Rev Psychiatry 21:96–103PubMedCrossRefGoogle Scholar
  15. Croft RJ, Mackay AJ, Mills ATD, Gruzelier JGH (2001) The relative contributions of ecstasy and cannabis to cognitive impairment. Psychopharmacology 153:373–379PubMedCrossRefGoogle Scholar
  16. 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 157:737–744PubMedCrossRefGoogle Scholar
  17. 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 24:421–426PubMedCrossRefGoogle Scholar
  18. 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:e141PubMedCrossRefGoogle Scholar
  19. 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 142:295–301PubMedCrossRefGoogle Scholar
  20. 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, LuxembourgGoogle Scholar
  21. 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 53:1051–1057PubMedGoogle Scholar
  22. 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 64:42–52PubMedCrossRefGoogle Scholar
  23. Harvey MA, Sellman JD, Porter RJ, Frampton CM (2007) The relationship between non-acute adolescent cannabis use and cognition. Drug Alcohol Rev 26:309–319PubMedCrossRefGoogle Scholar
  24. Huestegge L, Radach R, Kunert HJ, Heller D (2002) Visual search in long-term cannabis users with early age of onset. Prog Brain Res 140:377–394PubMedCrossRefGoogle Scholar
  25. Huestis MA, Cone EJ (2004) Relationship of Δ9-tetrahydrocannabinol concentrations in oral fluid and plasma after controlled administration of smoked cannabis. J Anal Toxicol 28:394–399PubMedGoogle Scholar
  26. Jacobsen LK, Mencl WE, Westerveld M, Pugh KR (2004) Impact of cannabis use on brain function in adolescents. Ann N Y Acad Sci 1021:384–390PubMedCrossRefGoogle Scholar
  27. 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 61:31–40PubMedCrossRefGoogle Scholar
  28. Jacobus J, Bava S, Cohen-Zion M, Mahmood O, Tapert SF (2009) Functional consequences of marijuana use in adolescents. Pharmacol Biochem Behav 92:559–565PubMedCrossRefGoogle Scholar
  29. 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, BethesdaGoogle Scholar
  30. 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 48:95–101PubMedCrossRefGoogle Scholar
  31. 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 32:959–956PubMedCrossRefGoogle Scholar
  32. 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 163:119–125PubMedCrossRefGoogle Scholar
  33. Lezak MD, Howieson DB, Loring DW (2004) Neuropsychological assessment, 4th edn. Oxford University Press, OxfordGoogle Scholar
  34. Lubman DI, Yücel M, Hall W (2007) Substance use and the adolescent brain: a toxic combination? J Psychopharmacol 21:792–794PubMedCrossRefGoogle Scholar
  35. Lynskey M, Hall W (2000) The effects of adolescent cannabis use on educational attainment: a review. Addiction 95:1621–1630PubMedCrossRefGoogle Scholar
  36. 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 41:1495–502PubMedCrossRefGoogle Scholar
  37. 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 83:90–93PubMedCrossRefGoogle Scholar
  38. 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 1317:297–304PubMedCrossRefGoogle Scholar
  39. 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 29:141–152PubMedCrossRefGoogle Scholar
  40. Messinis L, Kyprianidou A, Malefaki S, Papathansopoulos P (2006) Neuropsychological deficits in long-term frequent cannabis users. Neurology 66:737–739PubMedCrossRefGoogle Scholar
  41. 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 29:207–220PubMedCrossRefGoogle Scholar
  42. Nagel BJ, Schweinsburg AD, Phan V, Tapert SF (2005) Reduced hippocampal volume among adolescents with alcohol use disorders without psychiatric comorbidity. Psychiatry Res 139:181–190PubMedCrossRefGoogle Scholar
  43. 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 25:289–303PubMedGoogle Scholar
  44. Parrott A, Gouzoulis-Meyfrank E, Rodgers J, Solowij N (2004) Ecstasy/MDMA and cannabis: the complexities of their interactive neuropsychobiological effects. J Psychopharmacology 18:579–582CrossRefGoogle Scholar
  45. Paus T (2005) Mapping brain maturation and cognitive development during adolescence. Trends Cogn Sci 9:60–68PubMedCrossRefGoogle Scholar
  46. Pope HG, Yurgelun-Todd D (1996) The residual cognitive effects of heavy marijuana use in college students. JAMA 275:521–527PubMedCrossRefGoogle Scholar
  47. Pope HG, Gruber AJ, Hudson JI, Heustis MA, Yurgelun-Todd D (2001) Neuropsychological performance in long-term cannabis users. Arch Gen Psychiatry 58:909–915PubMedCrossRefGoogle Scholar
  48. 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 69:303–310PubMedCrossRefGoogle Scholar
  49. Schepis TS, Adinoff B, Rao U (2008) Neurobiological processes in adolescent addictive disorders. Am J Addict 17:6–23PubMedCrossRefGoogle Scholar
  50. Schneider M (2008) Puberty as a highly vulnerable developmental period for the consequences of cannabis exposure. Addict Biol 13:253–263PubMedCrossRefGoogle Scholar
  51. Schwartz RH, Gruenewald PJ, Klitzner M, Fedio P (1989) Short-term memory impairment in cannabis-dependent adolescents. Am J Dis Child 143:1214–1219PubMedGoogle Scholar
  52. 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 79:201–210CrossRefGoogle Scholar
  53. Simon NG, Mattick RP (2002) The impact of regular ecstasy use on memory function. Addiction 97:1523–1529PubMedCrossRefGoogle Scholar
  54. Simons J, Correia CJ, Carey KB (2000) A comparison of motives for marijuana and alcohol use among experienced users. Addict Behav 25:153–160PubMedCrossRefGoogle Scholar
  55. 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 41–72Google Scholar
  56. Solowij N, Battisti R (2008) The chronic effects of cannabis on memory in humans: a review. Curr Drug Abuse Rev 1:81–98PubMedCrossRefGoogle Scholar
  57. Solowij N, Pesa N (2010) Cognitive abnormalities and cannabis use. Rev Bras Psiquiatr 32(Suppl 1):31–40Google Scholar
  58. 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 287:1123–1131PubMedCrossRefGoogle Scholar
  59. 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)Google Scholar
  60. Spielberger CD (1989) State-trait anxiety inventory: a comprehensive bibliography. Consulting Psychologists, Palo AltoGoogle Scholar
  61. Swift W, Copeland J, Hall W (1998) Choosing a diagnostic cut-off for cannabis dependence. Addiction 93:1681–1692PubMedCrossRefGoogle Scholar
  62. Vandrey R, Budney AJ, Kamon JL, Stanger C (2005) Cannabis withdrawal in adolescent treatment seekers. Drug Alcohol Depend 78:205–210PubMedCrossRefGoogle Scholar
  63. 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 19:1–22PubMedCrossRefGoogle Scholar
  64. Yücel M, Lubman DI, Solowij N, Brewer W (2007) Understanding drug addiction: a neuropsychological perspective. Aust NZ J Psychiatry 41:957–969CrossRefGoogle Scholar
  65. 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 65:694–701PubMedCrossRefGoogle Scholar
  66. 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 326–341CrossRefGoogle Scholar
  67. 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 65:409-412Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Nadia Solowij
    • 1
    • 2
    • 3
    Email author
  • Katy A. Jones
    • 1
    • 4
  • Megan E. Rozman
    • 1
  • Sasha M. Davis
    • 1
  • Joseph Ciarrochi
    • 1
    • 2
  • Patrick C. L. Heaven
    • 1
    • 2
  • Dan I. Lubman
    • 4
    • 5
  • Murat Yücel
    • 5
    • 6
  1. 1.School of PsychologyUniversity of WollongongWollongongAustralia
  2. 2.Illawarra Health and Medical Research InstituteUniversity of WollongongWollongongAustralia
  3. 3.Schizophrenia Research InstituteSydneyAustralia
  4. 4.Turning Point Alcohol and Drug CentreEastern Health and Monash UniversityMelbourneAustralia
  5. 5.Orygen Youth Health Research Centre, Centre for Youth Mental HealthUniversity of MelbourneParkvilleAustralia
  6. 6.Melbourne Neuropsychiatry Centre, Department of PsychiatryUniversity of Melbourne and Melbourne HealthMelbourneAustralia

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