Hostname: page-component-6587cd75c8-67gbf Total loading time: 0 Render date: 2025-04-23T19:30:17.999Z Has data issue: false hasContentIssue false
  • English
  • Français

Neuroimaging in cannabis use: a systematic review of the literature

Published online by Cambridge University Press:  23 July 2009

R. Martín-Santos ,
A. B. Fagundo ,
J. A. Crippa ,
Z. Atakan ,
S. Bhattacharyya ,
P. Allen ,
P. Fusar-Poli ,
S. Borgwardt ,
M. Seal  and
G. F. Busatto
...Show all authors
R. Martín-Santos*
Affiliation:
Section of Neuroimaging, PO67 Division of Psychological Medicine, Institute of Psychiatry, King's College London, UK Neuropsychopharmacology Group, IMIM-Hospital del Mar and Department of Psychiatry; Institute of Neurosciences, Hospital Clinic, IDIBAPS, CIBERSAM, Barcelona, Spain INCT Translational Medicine, Brazil
A. B. Fagundo
Affiliation:
Neuropsychopharmacology Group, IMIM-Hospital del Mar and Department of Psychiatry; Institute of Neurosciences, Hospital Clinic, IDIBAPS, CIBERSAM, Barcelona, Spain Universidad Autónoma de Barcelona, Barcelona, Spain
J. A. Crippa
Affiliation:
Section of Neuroimaging, PO67 Division of Psychological Medicine, Institute of Psychiatry, King's College London, UK INCT Translational Medicine, Brazil Department of Neurosciences and Behaviour, School of Medicine of Riberão Preto, São Paulo University, Brazil
Z. Atakan
Affiliation:
Section of Neuroimaging, PO67 Division of Psychological Medicine, Institute of Psychiatry, King's College London, UK INCT Translational Medicine, Brazil
S. Bhattacharyya
Affiliation:
Section of Neuroimaging, PO67 Division of Psychological Medicine, Institute of Psychiatry, King's College London, UK
P. Allen
Affiliation:
Section of Neuroimaging, PO67 Division of Psychological Medicine, Institute of Psychiatry, King's College London, UK
P. Fusar-Poli
Affiliation:
Section of Neuroimaging, PO67 Division of Psychological Medicine, Institute of Psychiatry, King's College London, UK
S. Borgwardt
Affiliation:
Section of Neuroimaging, PO67 Division of Psychological Medicine, Institute of Psychiatry, King's College London, UK Psychiatric Out-patient Department (SJB), University Hospital Basel, Basel, Switzerland
M. Seal
Affiliation:
Section of Neuroimaging, PO67 Division of Psychological Medicine, Institute of Psychiatry, King's College London, UK Melbourne Neuropsychiatry Centre, The University of Melbourne, Australia
G. F. Busatto
Affiliation:
Department of Psychiatry, School of Medicine, Sao Paulo University, Brazil
P. McGuire
Affiliation:
Section of Neuroimaging, PO67 Division of Psychological Medicine, Institute of Psychiatry, King's College London, UK INCT Translational Medicine, Brazil
*
*Address for correspondence: Dr R. Martín-Santos, Department of Psychiatry, Institute of Neurosciences, Hospital Clinic, IDIBAPS, CIBERSAM, Villarroel, 170, 08036Barcelona, Spain. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

We conducted a systematic review to assess the evidence for specific effects of cannabis on brain structure and function. The review focuses on the cognitive changes associated with acute and chronic use of the drug.

Method

We reviewed literature reporting neuroimaging studies of chronic or acute cannabis use published up until January 2009. The search was conducted using Medline, EMBASE, LILACS and PsycLIT indexing services using the following key words: cannabis, marijuana, delta-9-tetrahydrocannabinol, THC, cannabidiol, CBD, neuroimaging, brain imaging, computerized tomography, CT, magnetic resonance, MRI, single photon emission tomography, SPECT, functional magnetic resonance, fMRI, positron emission tomography, PET, diffusion tensor MRI, DTI-MRI, MRS and spectroscopy.

Results

Sixty-six studies were identified, of which 41 met the inclusion criteria. Thirty-three were functional (SPECT/PET/fMRI) and eight structural (volumetric/DTI) imaging studies. The high degree of heterogeneity across studies precluded a meta-analysis. The functional studies suggest that resting global and prefrontal blood flow are lower in cannabis users than in controls. The results from the activation studies using a cognitive task are inconsistent because of the heterogeneity of the methods used. Studies of acute administration of THC or marijuana report increased resting activity and activation of the frontal and anterior cingulate cortex during cognitive tasks. Only three of the structural imaging studies found differences between users and controls.

Conclusions

Functional neuroimaging studies suggest a modulation of global and prefrontal metabolism both during the resting state and after the administration of THC/marijuana cigarettes. Minimal evidence of major effects of cannabis on brain structure has been reported.

Keywords

Brain effectcannabisCBDcognitive taskscognitionmarijuananeuroimagingsystematic reviewTHC
Type
Review Article
Information
Psychological Medicine , Volume 40 , Issue 3 , March 2010 , pp. 383 - 398
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Aasly, J, Storsaeter, O, Nilsen, G, Smevik, O, Rinck, P (1993). Minor structural brain changes in young drug abusers. A magnetic resonance study. Acta Neurologica Scandinavica 87, 210–214.CrossRefGoogle ScholarPubMed
Amen, DG, Waugh, M (1998). High resolution brain SPECT imaging of marijuana smokers with AD/HD. Journal of Psychoactive Drugs 30, 209–214.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Arseneault, L, Cannon, M, Witton, J, Murray, RM (2004). Causal association between cannabis and psychosis: examination of the evidence. British Journal of Psychiatry 184, 110–117.CrossRefGoogle ScholarPubMed
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. Journal of Psychiatric Research 43, 189–204.CrossRefGoogle Scholar
Bechara, A, Dolan, S, Denburg, N, Hindes, A, Anderson, SW, Nathan, PE (2001). Decision-making deficits, linked to a dysfunctional ventromedial prefrontal cortex, revealed in alcohol and stimulant abusers. Neuropsychologia 39, 376–389.CrossRefGoogle ScholarPubMed
Berger, A, Posner, MI (2000). Pathologies of brain attentional networks. Neuroscience and Biobehavioral Reviews 24, 3–5.CrossRefGoogle ScholarPubMed
Block, RI, O'Leary, DS, Ehrhardt, JC, Augustinack, JC, Ghoneim, MM, Arndt, S, Hall, JA (2000 a). Effects of frequent marijuana use on brain tissue volume and composition. Neuroreport 11, 491–496.CrossRefGoogle ScholarPubMed
Block, RI, O'Leary, DS, Hichwa, RD, Augustinack, JC, Boles Ponto, LL, Ghoneim, MM, Arndt, S, Hurtig, RR, Watkins, GL, Hall, JA, Nathan, PE, Andreasen, NC (2002). Effects of frequent marijuana use on memory-related regional cerebral blood flow. Pharmacology, Biochemistry, and Behavior 72, 237–250.CrossRefGoogle ScholarPubMed
Block, RI, O'Leary, DS, Hichwa, RD, Augustinack, JC, Ponto, LL, Ghoneim, MM, Arndt, S, Ehrhardt, JC, Hurtig, RR, Watkins, GL, Hall, JA, Nathan, PE, Andreasen, NC (2000 b). Cerebellar hypoactivity in frequent marijuana users. Neuroreport 11, 749–753.CrossRefGoogle ScholarPubMed
Bolla, KI, Brown, K, Eldreth, D, Tate, K, Cadet, JL (2002). Dose-related neurocognitive effects of marijuana use. Neurology 59, 1337–1343.CrossRefGoogle ScholarPubMed
Bolla, KI, Eldreth, DA, Matochik, JA, Cadet, JL (2005). Neural substrates of faulty decision-making in abstinent marijuana users. Neuroimage 26, 480–492.CrossRefGoogle ScholarPubMed
Borgwardt, SJ, Allen, P, Bhattacharyya, S, Fusar-Poli, P, Crippa, JA, Seal, ML, Fraccaro, V, Atakan, Z, Martin-Santos, R, O'Carroll, C, Rubia, K, McGuire, PK (2008). Neural basis of Δ-9-tetrahydrocannabinol (THC) and cannabidiol (CBD): effects during response inhibition. Biological Psychiatry 64, 966–973.CrossRefGoogle ScholarPubMed
Bossong, MG, van Berckel, BN, Boellaard, R, Zuurman, L, Schuit, RC, Windhorst, AD, van Gerven, JM, Ramsey, NF, Lammertsma, AA, Kahn, RS (2009). Delta 9-tetrahydrocannabinol induces dopamine release in the human striatum. Neuropsychopharmacology 34, 759–766.CrossRefGoogle ScholarPubMed
Campbell, AM, Evans, M, Thomson, JL, Williams, MJ (1971). Cerebral atrophy in young cannabis smokers. Lancet 2, 1219–1224.CrossRefGoogle ScholarPubMed
Chang, L, Chronicle, EP (2007). Functional imaging studies in cannabis users. Neuroscientist 13, 422–432.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Co, BT, Goodwin, DW, Gado, M, Mikhael, M, Hill, SY (1977). Absence of cerebral atrophy in chronic cannabis users. Evaluation by computerized transaxial tomography. Journal of the American Medical Association 237, 1229–1230.CrossRefGoogle ScholarPubMed
Crippa, JA, Lacerda, AL, Amaro, E, Busatto, FG, Zuardi, AW, Bressan, RA (2005). Brain effects of cannabis – neuroimaging findings [in Portuguese]. Revista Brasileira de Psiquiatria 27, 70–78.CrossRefGoogle ScholarPubMed
Crippa, JA, Zuardi, AW, Garrido, GE, Wichert-Ana, L, Guarnieri, R, Ferrari, L, Azevedo-Marques, PM, Hallack, JE, McGuire, PK, Filho Busatto, G (2004). Effects of cannabidiol (CBD) on regional cerebral blood flow. Neuropsychopharmacology 29, 417–426.CrossRefGoogle ScholarPubMed
DeLisi, LE (2008). The effect of cannabis on the brain: can it cause brain anomalies that lead to increased risk for schizophrenia? Current Opinion in Psychiatry 21, 140–150.CrossRefGoogle ScholarPubMed
DeLisi, LE, Bertisch, HC, Szulc, KU, Majcher, M, Brown, K, Bappal, A, Ardekani, BA (2006). A preliminary DTI study showing no brain structural change associated with adolescent cannabis use. Harm Reduction Journal 3, 17.CrossRefGoogle ScholarPubMed
Eldreth, DA, Matochik, JA, Cadet, JL, Bolla, KI (2004). Abnormal brain activity in prefrontal brain regions in abstinent marijuana users. Neuroimage 23, 914–920.CrossRefGoogle ScholarPubMed
Freund, TF, Katona, I, Piomelli, D (2003). Role of endogenous cannabinoids in synaptic signaling. Physiological Reviews 83, 1017–1066.CrossRefGoogle ScholarPubMed
Fusar-Poli, P, Crippa, JA, Bhattacharyya, S, Borgwardt, SJ, Allen, P, Martin-Santos, R, Seal, M, Surguladze, SA, O'Carrol, C, Atakan, Z, Zuardi, AW, McGuire, PK (2009). Distinct effects of (delta)9-tetrahydrocannabinol and cannabidiol on neural activation during emotional processing. Archives of General Psychiatry 66, 95–105.CrossRefGoogle ScholarPubMed
Gonzalez, R (2007). Acute and non-acute effects of cannabis on brain functioning and neuropsychological performance. Neuropsychology Review 17, 347–361.CrossRefGoogle ScholarPubMed
Gorelick, DA, Heishman, SJ (2006). Methods for clinical research involving cannabis administration. Methods in Molecular Medicine 123, 235–253.Google ScholarPubMed
Gruber, SA, Yurgelun-Todd, DA (2005). Neuroimaging of marijuana smokers during inhibitory processing: a pilot investigation. Brain Research. Cognitive Brain Research 23, 107–118.CrossRefGoogle ScholarPubMed
Hall, W, Solowij, N (1998). Adverse effects of cannabis. Lancet 352, 1611–1616.CrossRefGoogle ScholarPubMed
Hannerz, J, Hindmarsh, T (1983). Neurological and neuroradiological examination of chronic cannabis smokers. Annals of Neurology 13, 207–210.CrossRefGoogle ScholarPubMed
Hermann, D, Sartorius, A, Welzel, H, Walter, S, Skopp, G, Ende, G, Mann, K (2007). Dorsolateral prefrontal cortex N-acetylaspartate/total creatine (NAA/tCr) loss in male recreational cannabis users. Biological Psychiatry 61, 1281–1289.CrossRefGoogle ScholarPubMed
Hirst, RA, Lambert, DG, Notcutt, WG (1998). Pharmacology and potential therapeutic uses of cannabis. British Journal of Anaesthesia 81, 77–84.CrossRefGoogle ScholarPubMed
Hollister, LE (1986). Health aspects of cannabis. Pharmacological Reviews 38, 1–20.Google ScholarPubMed
Jacobsen, LK, Mencl, WE, Westerveld, M, Pugh, KR (2004). Impact of cannabis use on brain function in adolescents. Annals of the New York Academy of Sciences 1021, 384–390.CrossRefGoogle ScholarPubMed
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. Biological Psychiatry 61, 31–40.CrossRefGoogle ScholarPubMed
Jager, G, Kahn, RS, Van Den Brink, W, Van Ree, JM, Ramsey, NF (2006). Long-term effects of frequent cannabis use on working memory and attention: an fMRI study. Psychopharmacology (Berlin) 185, 358–368.CrossRefGoogle ScholarPubMed
Jager, G, Van Hell, HH, De Win, MM, Kahn, RS, Van Den Brink, W, Van Ree, JM, Ramsey, NF (2007). Effects of frequent cannabis use on hippocampal activity during an associative memory task. Journal of the European College of Neuropsychopharmacology 17, 289–297.CrossRefGoogle ScholarPubMed
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 (Berlin) 176, 239–247.CrossRefGoogle ScholarPubMed
Kuehnle, J, Mendelson, JH, Davis, KR, New, PF (1977). Computed tomographic examination of heavy marijuana smokers. Journal of the American Medical Association 237, 1231–1232.CrossRefGoogle ScholarPubMed
Li, CS, Milivojevic, V, Constable, RT, Sinha, R (2005). Recent cannabis abuse decreased stress-induced BOLD signals in the frontal and cingulate cortices of cocaine dependent individuals. Psychiatry Research 140, 271–280.CrossRefGoogle ScholarPubMed
Lundqvist, T (2005). Cognitive consequences of cannabis use: comparison with abuse of stimulants and heroin with regard to attention, memory and executive functions. Pharmacology, Biochemistry, and Behavior 81, 319–330.CrossRefGoogle ScholarPubMed
Lundqvist, T, Jonsson, S, Warkentin, S (2001). Frontal lobe dysfunction in long-term cannabis users. Neurotoxicology and Teratology 23, 437–443.CrossRefGoogle ScholarPubMed
Mathew, RJ, Tant, S, Burger, C (1986). Regional cerebral blood flow in marijuana smokers. British Journal of Addiction 81, 567–571.CrossRefGoogle ScholarPubMed
Mathew, RJ, Wilson, WH (1993). Acute changes in cerebral blood flow after smoking marijuana. Life Sciences 52, 757–767.CrossRefGoogle ScholarPubMed
Mathew, RJ, Wilson, WH, Chiu, NY, Turkington, TG, DeGrado, TR, Coleman, RE (1999). Regional cerebral blood flow and depersonalization after tetrahydrocannabinol administration. Acta Psychiatrica Scandinavica 100, 67–75.CrossRefGoogle ScholarPubMed
Mathew, RJ, Wilson, WH, Coleman, RE, Turkington, TG, DeGrado, TR (1997). Marijuana intoxication and brain activation in marijuana smokers. Life Sciences 60, 2075–2089.CrossRefGoogle ScholarPubMed
Mathew, RJ, Wilson, WH, Humphreys, DF, Lowe, JV, Wiethe, KE (1992 a). Regional cerebral blood flow after marijuana smoking. Journal of Cerebral Blood Flow and Metabolism 12, 750–758.CrossRefGoogle ScholarPubMed
Mathew, RJ, Wilson, WH, Humphreys, DF, Lowe, JV, Wiethe, KE (1992 b). Changes in middle cerebral artery velocity after marijuana. Biological Psychiatry 32, 164–169.CrossRefGoogle ScholarPubMed
Mathew, RJ, Wilson, WH, Tant, SR (1989). Acute changes in cerebral blood flow associated with marijuana smoking. Acta Psychiatrica Scandinavica 79, 118–128.CrossRefGoogle ScholarPubMed
Mathew, RJ, Wilson, WH, Turkington, TG, Coleman, RE (1998). Cerebellar activity and disturbed time sense after THC. Brain Research 797, 183–189.CrossRefGoogle ScholarPubMed
Mathew, RJ, Wilson, WH, Turkington, TG, Hawk, TC, Coleman, RE, DeGrado, TR, Provenzale, J (2002). Time course of tetrahydrocannabinol-induced changes in regional cerebral blood flow measured with positron emission tomography. Psychiatry Research 116, 173–185.CrossRefGoogle ScholarPubMed
Matochik, JA, Eldreth, DA, Cadet, JL, Bolla, KI (2005). Altered brain tissue composition in heavy marijuana users. Drug and Alcohol Dependence 77, 23–30.CrossRefGoogle ScholarPubMed
Murphy, K, Dixon, V, LaGrave, K, Kaufman, J, Risinger, R, Bloom, A, Garavan, H (2006). A validation of event-related FMRI comparisons between users of cocaine, nicotine, or cannabis and control subjects. American Journal of Psychiatry 163, 1245–1251.CrossRefGoogle ScholarPubMed
Nestor, L, Roberts, G, Garavan, H, Hester, R (2008). Deficits in learning and memory: parahippocampal hyperactivity and frontocortical hypoactivity in cannabis users. Neuroimage 40, 1328–1339.CrossRefGoogle ScholarPubMed
O'Leary, DS, Block, RI, Flaum, M, Schultz, SK, Boles Ponto, LL, Watkins, GL, Hurtig, RR, Andreasen, NC, Hichwa, RD (2000). Acute marijuana effects on rCBF and cognition: a PET study. Neuroreport 11, 3835–3841.CrossRefGoogle ScholarPubMed
O'Leary, DS, Block, RI, Koeppel, JA, Flaum, M, Schultz, SK, Andreasen, NC, Ponto, LB, Watkins, GL, Hurtig, RR, Hichwa, RD (2002). Effects of smoking marijuana on brain perfusion and cognition. Neuropsychopharmacology 26, 802–816.CrossRefGoogle ScholarPubMed
O'Leary, D, Block, RI, Koeppel, JA, Schultz, SK, Magnotta, VA, Boles Ponto, L, Watkins, FL, Hichwa, RD (2007). Effects of smoking marijuana on focal attention and brain flow. Human Psychopharmacology 22, 135–148.CrossRefGoogle Scholar
O'Leary, DS, Block, RI, Turner, BM, Koeppel, J, Magnotta, VA, Ponto, LB, Watkins, GL, Hichwa, RD, Andreasen, NC (2003). Marijuana alters the human cerebellar clock. Neuroreport 14, 1145–1151.CrossRefGoogle ScholarPubMed
Pertwee, RG, Ross, RA (2002). Cannabinoid receptors and their ligands. Prostaglandins, Leukotrienes and Essential Fatty Acids 66, 101–121.CrossRefGoogle ScholarPubMed
Phan, KL, Angstadt, M, Golden, J, Onyewuenyi, I, Popovska, A, de Wit, H (2008). Cannabinoid modulation of amygdala reactivity to social signals of threat in humans. Journal of Neuroscience 28, 2313–2319.CrossRefGoogle ScholarPubMed
Pillay, SS, Rogowska, J, Kanayama, G, Jon, DI, Gruber, S, Simpson, N, Cherayil, M, Pope, HG, Yurgelun-Todd, DA (2004). Neurophysiology of motor function following cannabis discontinuation in chronic cannabis smokers: an fMRI study. Drug and Alcohol Dependence 76, 261–271.CrossRefGoogle ScholarPubMed
Quickfall, J, Crockford, D (2006). Brain neuroimaging in cannabis use: a review. Journal of Neuropsychiatry and Clinical Neuroscience 18, 318–332.CrossRefGoogle ScholarPubMed
Ranganathan, M, D'Souza, DC (2006). The acute effects of cannabinoids on memory in humans: a review. Psychopharmacology (Berlin) 188, 425–444.CrossRefGoogle ScholarPubMed
Roser, P, Vollenweider, FX, Kawohl, W (2008). Potential antipsychotic properties of central cannabinoid (CB(1)) receptor antagonists. World Journal of Biological Psychiatry 7, 1–12.Google Scholar
Rypma, B, D'Esposito, M (2000). Isolating the neural mechanisms of age-related changes in human working memory. Nature Neuroscience 3, 509–515.CrossRefGoogle ScholarPubMed
Schneider, M (2008). Puberty as a highly vulnerable development period for the consequences of cannabis exposure. Addiction Biology 13, 253–263.CrossRefGoogle ScholarPubMed
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 and Alcohol Dependence 79, 201–210.CrossRefGoogle ScholarPubMed
Sevy, S, Smith, GS, Ma, Y, Dhawan, V, Chaly, T, Kingsley, PB, Kumra, S, Abdelmessih, S, Eidelberg, D (2008). Cerebral glucose metabolism and D2/D3 receptor availability in young adults with cannabis dependence measured with positron emission tomography. Psychopharmacology (Berlin) 197, 549–556.CrossRefGoogle ScholarPubMed
Sneider, JT, Pope, HG Jr., Silveri, MM, Simpson, NS, Gruber, SA, Yurgelun-Todd, DA (2006). Altered regional blood volume in chronic cannabis smokers. Experimental and Clinical Psychopharmacology 14, 422–428.CrossRefGoogle ScholarPubMed
Sneider, JT, Pope, HG Jr., Silveri, MM, Simpson, NS, Gruber, SA, Yurgelun-Todd, DA (2008). Differences in regional blood volume during a 28-day period of abstinence in chronic cannabis smokers. European Neuropsychopharmacology 18, 612–619.CrossRefGoogle ScholarPubMed
Solowij, N, Stephens, RS, Roffman, RA, Babor, T, Kadden, R, Miller, M, Christiansen, K, McRee, B, Vendetti, J (2002). Cognitive functioning of long-term heavy cannabis users seeking treatment. Journal of the American Medical Association 287, 1123–1131.CrossRefGoogle ScholarPubMed
Tunving, K, Thulin, SO, Risberg, J, Warkentin, S (1986). Regional cerebral blood flow in long-term heavy cannabis use. Psychiatry Research 17, 15–21.CrossRefGoogle ScholarPubMed
Tzilos, GK, Cintron, CB, Wood, JB, Simpson, NS, Young, AD, Pope, HG Jr., Yurgelun-Todd, DA (2005). Lack of hippocampal volume change in long-term heavy cannabis users. American Journal on Addictions 14, 64–72.CrossRefGoogle ScholarPubMed
Vernon, PA (1983). Speed of information processing and general intelligence. Intelligence 7, 53–70.CrossRefGoogle Scholar
Volkow, ND, Fowler, JS, Wang, GJ (2003). The addicted human brain: insights from imaging studies. Journal of Clinical Investigation 111, 1444–1451.CrossRefGoogle ScholarPubMed
Volkow, ND, Gillespie, H, Mullani, N, Tancredi, L, Grant, C, Ivanovic, M, Hollister, L (1991). Cerebellar metabolic activation by delta-9-tetrahydro-cannabinol in human brain: a study with positron emission tomography and 18F-2-fluoro-2-deoxyglucose. Psychiatry Research 40, 69–78.CrossRefGoogle Scholar
Volkow, ND, Gillespie, H, Mullani, N, Tancredi, L, Grant, C, Valentine, A, Hollister, L (1996). Brain glucose metabolism in chronic marijuana users at baseline and during marijuana intoxication. Psychiatry Research 67, 29–38.CrossRefGoogle ScholarPubMed
Voruganti, LN, Slomka, P, Zabel, P, Mattar, A, Awad, AG (2001). Cannabis induced dopamine release: an in-vivo SPECT study. Psychiatry Research 107, 173–177.CrossRefGoogle ScholarPubMed
Voytek, B, Berman, SM, Hassid, BD, Simon, SL, Mandelkern, MA, Brody, AL, Monterosso, J, Ling, W, London, ED (2005). Differences in regional brain metabolism associated with marijuana abuse in methamphetamine abusers. Synapse 57, 113–115.CrossRefGoogle ScholarPubMed
Ward, PB, Solowij, N, Peters, R, Otton, J, Chesher, G, Grenyer, B (2002). An fMRI study of regional brain volumes in long-term cannabis users. Journal of Psychopharmacology 16 (Suppl. 3), A56.Google Scholar
Watson, SJ, Benson, JA Jr., Joy, JE (2000). Marijuana and medicine: assessing the science base: a summary of the 1999 Institute of Medicine report. Archives of General Psychiatry 57, 547–552.CrossRefGoogle Scholar
Weinstein, A, Brickner, O, Lerman, H, Greemland, M, Bloch, M, Lester, H, Chisin, R, Mechoulam, R, Bar-Hamburger, R, Freedman, N, Even-Sapir, E (2008). Brain imaging study of the acute effects of Delta9-tetrahydrocannabinol (THC) on attention and motor coordination in regular users of marijuana. Psychopharmacology (Berlin) 196, 119–131.CrossRefGoogle ScholarPubMed
Wiesbeck, GA, Taeschner, KL (1991). A cerebral computed tomography study of patients with drug-induced psychoses. European Archives of Psychiatry and Clinical Neuroscience 241, 88–90.CrossRefGoogle ScholarPubMed
Williamson, EM, Evans, FJ (2000). Cannabinoids in clinical practice. Drugs 60, 1303–1314.CrossRefGoogle ScholarPubMed
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. Journal of Addictive Diseases 19, 1–22.CrossRefGoogle ScholarPubMed
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. Archives of General Psychiatry 65, 694–701.CrossRefGoogle ScholarPubMed
Yurgelun-Todd, DA, Gruber, SA, Hanson, RA, Baird, AA, Renshaw, PF, Pope, HG (1998). Residual effects of marijuana use: an fMRI study. In Problems of drug dependence. Proceedings of the 60th Annual Scientific Meeting. The College on Problems of Drug Dependence (ed. Harris, L. S.). NIDA Research Monograph 179, 78.Google Scholar
Zuardi, AW (2006). History of cannabis as a medicine: a review. Revista Brasileira de Psiquiatria 28, 153–157.CrossRefGoogle ScholarPubMed
Zuardi, AW, Shirakawa, I, Finkelfarb, E, Karniol, IG (1982). Action of cannabidiol on the anxiety and others effects produced by delta 9-THC in normal subjects. Psychopharmacology (Berlin) 76, 245–250.CrossRefGoogle Scholar