Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Investigation
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

Objectives

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

Methods

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.

Results

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.

Conclusions

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aguirre GK, Detre JA, Alsop DC, D’Esposito M (1996) The parahippocampus subserves topographical learning in man. Cereb Cortex 6:823–829

    Article  CAS  PubMed  Google Scholar 

  • American Psychiatric Association (1994) Diagnostic and statistical manual of mental disorders-fourth edition (DSM-IV). American Psychiatric Association, Washington

    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 

  • Bacon W (1997) NIMH-computerized diagnostic interview schedule for children-version IV (C-DISC 4). Columbia University, New York

    Google Scholar 

  • Baddeley A (1999) Essentials of human memory. Psychology Press

  • 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  PubMed  Google Scholar 

  • 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 5:49–62

    Article  CAS  PubMed  Google Scholar 

  • 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 8:743–752

    Article  CAS  PubMed  Google Scholar 

  • Chang L, Chronicle EP (2007) Functional imaging studies in cannabis users. The Neuroscientist 13:422–432

    Article  PubMed  Google Scholar 

  • Chang L, Yakupov R, Cloak C, Ernst T (2006) Marijuana use is associated with a reorganized visual-attention network and cerebellar hypoactivation. Brain 129:1096–1112

    Article  CAS  PubMed  Google Scholar 

  • 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 386:604–608

    Article  CAS  PubMed  Google Scholar 

  • Costa PT Jr, McCrae RR (1989) NEO PI professional manual. Psychological Assessment Resources, Odessa

    Google Scholar 

  • 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 117–142

    Google Scholar 

  • 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 7:1–13

    Article  Google Scholar 

  • 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 34:605–613

    CAS  PubMed  Google Scholar 

  • Fried PA (2002a) Conceptual issues in behavioral teratology and their application in determining long-term sequelae of prenatal marihuana exposure. J Child Psychol Psychiatry 43:81–102

    Article  CAS  PubMed  Google Scholar 

  • 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–102S

    CAS  PubMed  Google Scholar 

  • 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 6:323–343

    Article  CAS  PubMed  Google Scholar 

  • 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 20:293–306

    Article  CAS  PubMed  Google Scholar 

  • 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 25:427–436

    Article  CAS  PubMed  Google Scholar 

  • Friston KJ, Ashburner J, Poline JB, Frith CD, Heather JD, Frackowiak RSJ (1995) Spatial realignment and normalization of images. Hum Brain Mapp 2:165–189

    Article  Google Scholar 

  • Fuster JM (1997) The PFC: anatomy, physiology and the neuropsychology of the frontal lobe. Raven Press, New York

    Google Scholar 

  • 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 131:3006–3018

    Article  PubMed  Google Scholar 

  • Goyette CH, Conners CK, Ulrich RF (1978) Normative data on revised Conners’ parent and teacher rating scales. J Abnorm Child Psychol 6:221–236

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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 87:1932–1936

    Article  CAS  PubMed  Google Scholar 

  • Ilan AR, Smith ME, Gevins A (2004) Effects of marijuana on neurophysiological signals of working and episodic memory. Psychopharmacology 176:214–222

    Article  CAS  PubMed  Google Scholar 

  • 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 193:557–556

    Article  CAS  PubMed  Google Scholar 

  • Luks T, Simpson G, Feiwell R, Miller W (2002) Evidence for anterior cingulate cortex involvement in monitoring preparatory attentional set. Neuroimage 17:792–802

    Article  PubMed  Google Scholar 

  • 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 176:239–247

    Article  CAS  PubMed  Google Scholar 

  • 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 10:61–76

    Article  CAS  PubMed  Google Scholar 

  • Maguire EA, Mummery CJ, Buchel C (2000) Patterns of hippocampal-cortical interaction dissociate temporal lobe memory subsystems. Hippocampus 10:475–482

    Article  CAS  PubMed  Google Scholar 

  • Mechoulam R, Gaoni Y (1967) The absolute configuration of delta-1-tetrahydrocannabinol, the major active constitute of hashish. Tetrahedron Lett 12:1109–1111

    Article  CAS  PubMed  Google Scholar 

  • 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 27:823–839

    Article  PubMed  Google Scholar 

  • 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 14:7–20

    Article  CAS  PubMed  Google Scholar 

  • 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 10:1211–1216

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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 139:339–349

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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 163:40–51

    Article  PubMed  Google Scholar 

  • Shipman SL, Astur RS (2008) Factors affecting the hippocampal BOLD response during spatial memory. Behav Brain Res 187:433–441

    Article  PubMed  Google Scholar 

  • 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 28:286–295

    Article  CAS  PubMed  Google Scholar 

  • 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 28:1577–1586

    Article  PubMed  Google Scholar 

  • United Nations Office on Drugs and Crime, (2007) World Drug Report

  • Wechsler D (1997) Weshsler adult intelligence scale, 3rd edn. The Psychology Corporation, San Antonio

    Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Department of Psychology, University of Ottawa, Ottawa, ON, K1N 6N5, Canada

    Andra M. Smith & Carmelinda A. Longo

  2. Department of Psychology, Carleton University, Ottawa, ON, K1S 5B6, Canada

    Peter A. Fried

  3. Department of Diagnostic Imaging, The Ottawa Hospital, Ottawa, ON, K1H 8L6, Canada

    Matthew J. Hogan & Ian Cameron

  4. Ottawa Health Research Institute, Ottawa, ON, K1H 8M6, Canada

    Matthew J. Hogan & Ian Cameron

Authors
  1. Andra M. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carmelinda A. Longo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter A. Fried
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Matthew J. Hogan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ian Cameron
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andra M. Smith.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Smith, A.M., Longo, C.A., Fried, P.A. et al. Effects of marijuana on visuospatial working memory: an fMRI study in young adults. Psychopharmacology 210, 429–438 (2010). https://doi.org/10.1007/s00213-010-1841-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-010-1841-8

Keywords

Search

Navigation