, Volume 210, Issue 3, pp 429–438 | Cite as

Effects of marijuana on visuospatial working memory: an fMRI study in young adults

  • Andra M. Smith
  • Carmelinda A. Longo
  • Peter A. Fried
  • Matthew J. Hogan
  • Ian Cameron
Original Investigation



The effects of marijuana use on visuospatial working memory were investigated in 19–21-year-olds using functional magnetic resonance imaging (fMRI).


Participants were members of the Ottawa Prenatal Prospective Study, a longitudinal study that collected a unique body of information on participants from infancy to young adulthood including: prenatal drug history, detailed cognitive/behavioral performance, and current and past drug usage. This information allowed for the measurement of an unprecedented number of potentially confounding drug exposure variables including: prenatal marijuana, nicotine, alcohol, and caffeine exposure and offspring alcohol, marijuana, and nicotine use. Ten marijuana users and 14 nonusing controls performed a visuospatial 2-back task while fMRI blood oxygen level-dependent response was examined.


Despite similar task performance, marijuana users had significantly greater activation in the inferior and middle frontal gyri, regions of the brain normally associated with visuospatial working memory. Marijuana users also had greater activation in the right superior temporal gyrus, a region of the brain not typically associated with visuospatial working memory tasks.


These results suggest that marijuana use leads to altered neural functioning during visuospatial working memory after controlling for other prenatal and current drug use. This alteration appears to be compensated for by the recruitment of blood flow in additional brain regions. It is possible that this compensation may not be sufficient in more real-life situations where this type of processing is required and thus deficits may be observed. Awareness of these neural physiological effects of marijuana in youth is critical.


Visuospatial working memory Marijuana Executive functioning Functional magnetic resonance imaging 


Acknowledgments, Disclosure and Conflict of Interest

The manuscript is dedicated to the memory of Barbara Watkinson—a truly dedicated and inspiring researcher. The authors would like to acknowledge the excellent work of The Ottawa Hospital MRI technologists that assisted with this research. The authors would also like to thank the OPPS research associates, Heather Lintell, Robert Gray, and the always cooperative OPPS offspring. The research was funded through an Ontario Research and Development Challenge Fund grant. The authors do not have a financial relationship with the organization that sponsored the research. The authors also have full control of all primary data and agree to allow Psychopharmacology to review the data if requested. All experimentation complies with the current laws of Canada.


  1. Aguirre GK, Detre JA, Alsop DC, D’Esposito M (1996) The parahippocampus subserves topographical learning in man. Cereb Cortex 6:823–829CrossRefPubMedGoogle Scholar
  2. American Psychiatric Association (1994) Diagnostic and statistical manual of mental disorders-fourth edition (DSM-IV). American Psychiatric Association, WashingtonGoogle Scholar
  3. 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 43:189–204CrossRefPubMedGoogle Scholar
  4. Bacon W (1997) NIMH-computerized diagnostic interview schedule for children-version IV (C-DISC 4). Columbia University, New YorkGoogle Scholar
  5. Baddeley A (1999) Essentials of human memory. Psychology PressGoogle 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 173:228–237CrossRefPubMedGoogle Scholar
  7. Braver TS, Cohen JD, Nystrom LE, Jonides J, Smith EE, Noll DC (1997) A parametric study of prefrontal cortex involvement in human working memory. Neuroimage 5:49–62CrossRefPubMedGoogle Scholar
  8. Carlson S, Martinkauppi S, Rama P, Salli E, Korvenoja A, Aronen HJ (1998) Distribution of cortical activation during visuospatial n-back tasks as revealed by functional magnetic resonance imaging. Cereb Cortex 8:743–752CrossRefPubMedGoogle Scholar
  9. Chang L, Chronicle EP (2007) Functional imaging studies in cannabis users. The Neuroscientist 13:422–432CrossRefPubMedGoogle Scholar
  10. Chang L, Yakupov R, Cloak C, Ernst T (2006) Marijuana use is associated with a reorganized visual-attention network and cerebellar hypoactivation. Brain 129:1096–1112CrossRefPubMedGoogle Scholar
  11. Cohen JD, Perlstein WM, Braver TS, Nystrom LE, Noll DC, Jonides J, Smith EE (1997) Temporal dynamics of brain activation during a working memory task. Nature 386:604–608CrossRefPubMedGoogle Scholar
  12. Costa PT Jr, McCrae RR (1989) NEO PI professional manual. Psychological Assessment Resources, OdessaGoogle Scholar
  13. Denkla MB (1993) Measurement of executive functioning. In: Lyon GR (ed) Frames of reference for the assessment of learning disabilities: new views on measurement issues. Paul Brookes, Baltimore, pp 117–142Google Scholar
  14. D’Esposito M, Aguirre GK, Zarahn E, Ballard D, Shin RK, Lease J (1998) Functional MRI studies of spatial and nonspatial working memory. Cogn Brain Res 7:1–13CrossRefGoogle Scholar
  15. Devane WA, Dysarz FA III, Johnson MR, Melvin LS, Howlett AC (1988) Determination and characterization of a cannabinoid receptor in a rat brain. Mol Pharmacol 34:605–613PubMedGoogle Scholar
  16. Fried PA (2002a) Conceptual issues in behavioral teratology and their application in determining long-term sequelae of prenatal marihuana exposure. J Child Psychol Psychiatry 43:81–102CrossRefPubMedGoogle Scholar
  17. Fried PA (2002b) Adolescents prenatally exposed to marijuana: examination of facets of complex behaviors and comparison with the influence of in utero cigarettes. J Clin Pharmacol 42:97S–102SPubMedGoogle Scholar
  18. Fried PA, Watkinson B, Grant A, Knights RK (1980) Changing patterns of soft drug use prior to and during pregnancy: a prospective study. Drug Alcohol Depend 6:323–343CrossRefPubMedGoogle Scholar
  19. Fried PA, Watkinson B, Gray R (1998) Differential effects on cognitive functioning in 9–12-year-olds prenatally exposed to cigarettes and marihuana. Neurotoxicol Teratol 20:293–306CrossRefPubMedGoogle Scholar
  20. Fried PA, Watkinson B, Gray R (2003) Differential effects on cognitive functioning in 13–16-year-olds prenatally exposed to cigarettes and marihuana. Neurotoxicol Teratol 25:427–436CrossRefPubMedGoogle Scholar
  21. Friston KJ, Ashburner J, Poline JB, Frith CD, Heather JD, Frackowiak RSJ (1995) Spatial realignment and normalization of images. Hum Brain Mapp 2:165–189CrossRefGoogle Scholar
  22. Fuster JM (1997) The PFC: anatomy, physiology and the neuropsychology of the frontal lobe. Raven Press, New YorkGoogle Scholar
  23. Glikmann-Johnston Y, Saling MM, Chen J, Cooper KA, Beare RJ, Reutens DC (2008) Structural and functional correlates of unilateral mesial temporal lobe spatial memory impairment. Brain 131:3006–3018CrossRefPubMedGoogle Scholar
  24. Goyette CH, Conners CK, Ulrich RF (1978) Normative data on revised Conners’ parent and teacher rating scales. J Abnorm Child Psychol 6:221–236CrossRefPubMedGoogle Scholar
  25. Harvey MA, Sellman JD, Portier RJ, Frampton CM (2007) The relationship between non-acute adolescent cannabis use and cognition. Drug Alcohol Rev 26:309–319CrossRefPubMedGoogle Scholar
  26. Herkenham M, Lynn AB, Little MD, Johnson MR, Melvin LS, de Costa BR, Rice KC (1990) Cannabinoid receptor localization in brain. Proc Natl Acad Sci USA 87:1932–1936CrossRefPubMedGoogle Scholar
  27. Ilan AR, Smith ME, Gevins A (2004) Effects of marijuana on neurophysiological signals of working and episodic memory. Psychopharmacology 176:214–222CrossRefPubMedGoogle Scholar
  28. Jacobsen LK, Mencl WE, Constable RT, Westerveld M, Pugh KR (2007) Impact of smoking abstinence on working memory neurocircuitry in adolescent daily tobacco smokers. Psychopharmacology 193:557–556CrossRefPubMedGoogle Scholar
  29. Luks T, Simpson G, Feiwell R, Miller W (2002) Evidence for anterior cingulate cortex involvement in monitoring preparatory attentional set. Neuroimage 17:792–802CrossRefPubMedGoogle Scholar
  30. Kanayama G, Rogowska J, Pope HG, Gruber SA, Yurgelun-Todd DA (2004) Spatial working memory in heavy cannabis users: a functional magnetic resonance imaging study. Psychopharmacology 176:239–247CrossRefPubMedGoogle Scholar
  31. Maguire EA, Frith CD, Burgess N, Donnett JG, O’Keefe J (1998) Knowing where things are: parahippocampal involvement in encoding object location in virtual large-scale space. J Cogn Neurosci 10:61–76CrossRefPubMedGoogle Scholar
  32. Maguire EA, Mummery CJ, Buchel C (2000) Patterns of hippocampal-cortical interaction dissociate temporal lobe memory subsystems. Hippocampus 10:475–482CrossRefPubMedGoogle Scholar
  33. Mechoulam R, Gaoni Y (1967) The absolute configuration of delta-1-tetrahydrocannabinol, the major active constitute of hashish. Tetrahedron Lett 12:1109–1111CrossRefPubMedGoogle Scholar
  34. Nagel BJ, Barlett VC, Schweinsburg AD, Tapert SF (2005) Neuropsychological predictors of BOLD response during a spatial working memory task in adolescents: what can performance tell us about fMRI response patterns? J Clin Exp Neuropsychol 27:823–839CrossRefPubMedGoogle Scholar
  35. Pfefferbaum A, Desmond JE, Galloway C, Menon V, Glover GH, Sullivan EV (2001) Reorganization of frontal systems used by alcoholics for spatial working memory: an fMRI study. Neuroimage 14:7–20CrossRefPubMedGoogle Scholar
  36. Ploner CJ, Gaymard BM, Rivaud-Pechoux S, Baulac M, Clemenceau S, Severine S, Pierrot-Deseilligny C (2000) Lesions affecting the parahippocampal cortex yield spatial memory deficits in humans. Cereb Cortex 10:1211–1216CrossRefPubMedGoogle Scholar
  37. Pope HG Jr, Gruber AJ, Hudson JI, Huestis MA, Yurgelun-Todd D (2001) Neuropsychological performance in long-term cannabis users. Arch Gen Psychiatry 58:909–915CrossRefPubMedGoogle Scholar
  38. Ricciardi E, Bonino D, Gentili C, Sani L, Pietrini P, Vecchi T (2006) Neural correlates of spatial working memory in humans: a functional magnetic resonance imaging study comparing visual and tactile processes. Neuroscience 139:339–349CrossRefPubMedGoogle Scholar
  39. Schwartz RH, Gruenewald PJ, Klitzer M, Fedio P (1989) Short-term memory impairment in cannabis-dependent adolescents. Am J Dis Child 143:1214–1219PubMedGoogle Scholar
  40. Schweinsburg AD, Nagel BJ, Schweinsburg BC, Park A, Theilmann RJ, Tapert SF (2008) Abstinent adolescent marijuana users show altered fMRI response during spatial working memory. Psychiatry Res: Neuroimaging 163:40–51CrossRefPubMedGoogle Scholar
  41. Shipman SL, Astur RS (2008) Factors affecting the hippocampal BOLD response during spatial memory. Behav Brain Res 187:433–441CrossRefPubMedGoogle Scholar
  42. Smith AM, Fried PA, Hogan MJ, Cameron I (2006) Effects of prenatal marijuana on visuospatial working memory: an fMRI study in young adults. Neurotoxicol Teratol 28:286–295CrossRefPubMedGoogle Scholar
  43. Tapert SF, Schweinsburg AD, Barlett VC, Brown SA, Frank LR, Brown GG, Meloy MJ (2004) Blood oxygen level dependent response and spatial working memory in adolescents with alcohol use disorders. Alcohol Clin Exp Res 28:1577–1586CrossRefPubMedGoogle Scholar
  44. United Nations Office on Drugs and Crime, (2007) World Drug ReportGoogle Scholar
  45. Wechsler D (1997) Weshsler adult intelligence scale, 3rd edn. The Psychology Corporation, San AntonioGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Andra M. Smith
    • 1
  • Carmelinda A. Longo
    • 1
  • Peter A. Fried
    • 2
  • Matthew J. Hogan
    • 3
    • 4
  • Ian Cameron
    • 3
    • 4
  1. 1.Department of PsychologyUniversity of OttawaOttawaCanada
  2. 2.Department of PsychologyCarleton UniversityOttawaCanada
  3. 3.Department of Diagnostic ImagingThe Ottawa HospitalOttawaCanada
  4. 4.Ottawa Health Research InstituteOttawaCanada

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