Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-13T02:16:01.231Z Has data issue: false hasContentIssue false
  • English
  • Français

Cannabis affects people differently: inter-subject variation in the psychotogenic effects of Δ9-tetrahydrocannabinol: a functional magnetic resonance imaging study with healthy volunteers

Published online by Cambridge University Press:  01 October 2012

Z. Atakan ,
S. Bhattacharyya ,
P. Allen ,
R. Martín-Santos ,
J. A. Crippa ,
S. J. Borgwardt ,
P. Fusar-Poli ,
M. Seal ,
H. Sallis  and
D. Stahl
...Show all authors
Z. Atakan*
Affiliation:
Section of Neuroimaging, Department of Psychosis Studies, Institute of Psychiatry, King's College London, London, UK
S. Bhattacharyya
Affiliation:
Section of Neuroimaging, Department of Psychosis Studies, Institute of Psychiatry, King's College London, London, UK
P. Allen
Affiliation:
Section of Neuroimaging, Department of Psychosis Studies, Institute of Psychiatry, King's College London, London, UK
R. Martín-Santos
Affiliation:
Institut Municipal Investigació Mèdica IMIM Hospital del Mar, Barcelona, Spain
J. A. Crippa
Affiliation:
Departamento de Neuropsiquiatria e Psicologia Médica, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Brazil
S. J. Borgwardt
Affiliation:
Psychiatric Outpatient Department, University Hospital Basel, Basel, Switzerland
P. Fusar-Poli
Affiliation:
Section of Neuroimaging, Department of Psychosis Studies, Institute of Psychiatry, King's College London, London, UK
M. Seal
Affiliation:
Murdoch Children's Research Institute, The Royal Children's Hospital, Parkville, Australia
H. Sallis
Affiliation:
Department of Biostatistics, Institute of Psychiatry, King's College London, London, UK
D. Stahl
Affiliation:
Department of Biostatistics, Institute of Psychiatry, King's College London, London, UK
A. W. Zuardi
Affiliation:
Departamento de Neuropsiquiatria e Psicologia Médica, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Brazil
K. Rubia
Affiliation:
Section of Developmental Neuropsychology and Neuroimaging, Institute of Psychiatry, King's College London, London, UK
P. McGuire
Affiliation:
Section of Neuroimaging, Department of Psychosis Studies, Institute of Psychiatry, King's College London, London, UK
*
*Address for correspondence: Z. Atakan, M.D., Department of Psychosis Studies, PO67, Section of Neuroimaging, Institute of Psychiatry, King's College London, DeCrespigny Park, London, SE5 8AF, UK. (Email: Zerrin.Atakan@kcl.ac.uk)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Cannabis can induce transient psychotic symptoms, but not all users experience these adverse effects. We compared the neural response to Δ9-tetrahydrocannabinol (THC) in healthy volunteers in whom the drug did or did not induce acute psychotic symptoms.

Method

In a double-blind, placebo-controlled, pseudorandomized design, 21 healthy men with minimal experience of cannabis were given either 10 mg THC or placebo, orally. Behavioural and functional magnetic resonance imaging measures were then recorded whilst they performed a go/no-go task.

Results

The sample was subdivided on the basis of the Positive and Negative Syndrome Scale positive score following administration of THC into transiently psychotic (TP; n = 11) and non-psychotic (NP; n = 10) groups. During the THC condition, TP subjects made more frequent inhibition errors than the NP group and showed differential activation relative to the NP group in the left parahippocampal gyrus, the left and right middle temporal gyri and in the right cerebellum. In these regions, THC had opposite effects on activation relative to placebo in the two groups. The TP group also showed less activation than the NP group in the right middle temporal gyrus and cerebellum, independent of the effects of THC.

Conclusions

In this first demonstration of inter-subject variability in sensitivity to the psychotogenic effects of THC, we found that the presence of acute psychotic symptoms was associated with a differential effect of THC on activation in the ventral and medial temporal cortex and cerebellum, suggesting that these regions mediate the effects of the drug on psychotic symptoms.

Keywords

CerebellumfMRImiddle temporal gyriparahippocampusresponse inhibitionTHC
Type
Original Articles
Information
Psychological Medicine , Volume 43 , Issue 6 , June 2013 , pp. 1255 - 1267
Copyright
Copyright © Cambridge University Press 2012 

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.)

References

Arseneault, L, Cannon, M, Murray, R, Poulton, R, Caspi, A, Moffitt, TE (2002). Cannabis use in adolescence and risk for adult psychosis: longitudinal prospective study. British Medical Journal 325, 1212–1213.CrossRefGoogle ScholarPubMed
Battisti, RA, Roodenrys, S, Johnstone, SJ, Pesa, N, Hermens, DF, Solowij, N (2010 a). Chronic cannabis users show altered neurophysiological functioning on Stroop task conflict resolution. Psychopharmacology 212, 613–624.CrossRefGoogle ScholarPubMed
Battisti, RA, Roodenrys, S, Johnstone, SJ, Respondek, C, Hermens, DF, Solowij, N (2010 b). Chronic use of cannabis and poor neural efficiency in verbal memory ability. Psychopharmacology 209, 319–330.CrossRefGoogle ScholarPubMed
Bhattacharyya, S, Atakan, Z, Martín-Santos, R, Crippa, JA, Kambeitz, J, Prata, D, Williams, S, Brammer, M, Collier, DA, McGuire, PK (2012 a). Preliminary report of biological basis of sensitivity to the effects of cannabis on psychosis: AKT1 and DAT1 genotype modulates the effects of Δ-9-tetrahydrocannabinol on midbrain and striatal function. Molecular Psychiatry. Published online 31 January 2012. doi:10.3390/v3071210.CrossRefGoogle Scholar
Bhattacharyya, S, Crippa, JA, Allen, P, Martín-Santos, R, Borgwardt, S, Fusar-Poli, P, Rubia, K, Kambeitz, J, O'Carroll, C, Seal, ML, Giampietro, V, Brammer, M, Zuardi, AW, Atakan, Z, McGuire, PK (2012 b). Induction of psychosis by Δ9-tetrahydrocannabinol reflects modulation of prefrontal and striatal function during attentional salience processing. Archives of General Psychiatry 69, 27–36.CrossRefGoogle ScholarPubMed
Bhattacharyya, S, Fusar-Poli, P, Borgwardt, S, Martín-Santos, R, Nosarti, C, O'Carroll, C, Allen, P, Seal, ML, Fletcher, PC, Crippa, JA, Giampietro, V, Mechelli, A, Atakan, Z, McGuire, P (2009). Modulation of mediotemporal and ventrostriatal function in humans by Δ9-tetrahydrocannabinol: a neural basis for the effects of Cannabis sativa on learning and psychosis. Archives of General Psychiatry 66, 442–451.CrossRefGoogle ScholarPubMed
Bhattacharyya, S, Morrison, PD, Fusar-Poli, P, Martín-Santos, R, Borgwardt, S, Winton-Brown, T, Nosarti, C, O'Carroll, CM, Seal, M, Allen, P, Mehta, MA, Stone, JM, Tunstall, N, Giampietro, V, Kapur, S, Murray, RM, Zuardi, AW, Crippa, JA, Atakan, Z, McGuire, P (2010). Opposite effects of Δ-9-tetrahydrocannabinol and cannabidiol on human brain function and psychopathology. Neuropsychopharmacology 35, 764–774.CrossRefGoogle ScholarPubMed
Borgwardt, SJ, Allen, P, Bhattacharyya, S, Fusar-Poli, P, Crippa, JA, Seal, ML, Fraccaro, V, Atakan, Z, Martín-Santos, R, O'Carroll, C, Rubia, K, McGuire, PK (2008). Neural basis of Δ-9-tetrahydrocannabinol and cannabidiol: effects during response inhibition. Biological Psychiatry 64, 966–973.CrossRefGoogle ScholarPubMed
Brammer, MJ, Bullmore, ET, Simmons, A, Williams, SCR, Grasby, PM, Howard, RJ, Woodruff, PWR, Rabe-Hesketh, S (1997). Generic brain activation mapping in fMRI: a non-parametric approach. Magnetic Resonance Imaging 15, 763–770.CrossRefGoogle Scholar
Bullmore, ET, Suckling, J, Overmeyer, S, Rabe-Hesketh, S, Taylor, E, Brammer, MJ (1999). Global, voxel and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE Transactions on Medical Imaging 18, 32–42.CrossRefGoogle ScholarPubMed
Cascini, F, Aiello, C, Di Tanna, G (2011). Increasing delta-9-tetrahydrocannabinol (Δ-9-THC) content in herbal cannabis over time: systematic review and meta-analysis. Current Drug Abuse Reviews 5, 32–40.CrossRefGoogle Scholar
Caspi, A, Moffitt, TE, Cannon, M, McClay, J, Murray, R, Harrington, H, Taylor, A, Arseneault, L, Williams, B, Braithwaite, A, Poulton, R, Craig, IW (2005). Moderation of the effect of adolescent-onset cannabis use on adult psychosis by a functional polymorphism in the catechol-O-methyltransferase gene: longitudinal evidence of a gene × environment interaction. Biological Psychiatry 57, 1117–1127.CrossRefGoogle Scholar
Chambers, CD, Garavan, , Bellgrove, MA (2009). Insights into the neural basis of response inhibition from cognitive and clinical neuroscience. Neuroscience and Biobehavioural Reviews 33, 631–646.CrossRefGoogle ScholarPubMed
Chesher, GB, Bird, KD, Jackson, DM, Perrignon, A, Starmer, GA (1990). The effects of orally administered delta 9-tetrahydrocannabinol in man on mood and performance measures: a dose–response study. Pharmacology, Biochemistry and Behavior 35, 861–864.CrossRefGoogle Scholar
Curran, HV, Brignell, C, Fletcher, S, Middleton, P, Henry, J (2002). Cognitive subjective dose–response effects of acute oral Δ9-tetrahydrocannabinol (THC) in infrequent cannabis users. Psychopharmacology 164, 61–70.CrossRefGoogle ScholarPubMed
Degenhardt, L, Coffey, C, Carlin, JB, Swift, W, Moore, E, Patton, GC (2010). Outcomes of occasional cannabis use in adolescence: 10-year follow-up study in Victoria, Australia. British Journal of Psychiatry 196, 290–295.CrossRefGoogle ScholarPubMed
D'Souza, DC, Perry, E, MacDougall, L, Ammerman, Y, Cooper, TB, Wu, YT, Braley, G, Gueorguieva, R, Krystal, JH (2004). The psychotomimetic effects of intravenous delta-9-tetrahydrocannabinol in healthy individuals: implications for psychosis. Neuropsychopharmacology 29, 1558–1572.CrossRefGoogle ScholarPubMed
D'Souza, DC, Sewell, RA, Ranganathan, M (2009). Cannabis and psychosis/schizophrenia: human studies. European Archives of Clinical Neurosciences 259, 413–431.Google ScholarPubMed
Enticott, PG, Ogloff, JR, Bradshaw, JL (2008). Response inhibition and impulsivity in schizophrenia. Psychiatry Research 157, 251–254.CrossRefGoogle ScholarPubMed
Fleck, DE, Kotwal, R, Eliassen, JC, Lamy, M, DelBello, MP, Adler, CM, Durling, M, Cerullo, MA, Strakowski, SM (2011). Preliminary evidence for increased frontosubcortical activation on a motor impulsivity task in mixed episode bipolar disorder. Journal of Affective Disorders 133, 333–339.CrossRefGoogle ScholarPubMed
Fusar-Poli, P, Broome, MR, Matthiasson, P, Woolley, JB, Johns, LC, Tabraham, P, Bramon, E, Valmaggia, L, William, SC, McGuire, P (2010). Spatial working memory in individuals at high risk for psychosis: longitudinal fMRI study. Schizophrenia Research 123, 45–52.CrossRefGoogle ScholarPubMed
Fusar-Poli, P, Crippa, JA, Bhattacharyya, S, Borgwardt, SJ, Allen, P, Martín-Santos, R, Seal, M, Surguladze, SA, O'Carroll, C, Atakan, Z, Zuardi, AW, McGuire, PK (2009). Distinct effects of Δ9-tetrahydrocannabinol and cannabidiol on neural activation during emotional processing. Archives of General Psychiatry 66, 95–105.CrossRefGoogle ScholarPubMed
Fusar-Poli, P, Radua, J, McGuire, P, Borgwardt, S (2011). Neuroanatomical maps of psychosis onset: voxel-wise meta-analysis of antipsychotic-naïve VBM studies. Schizophrenia Bulletin. Published online 17 November 2011. doi:10.1093/schbul/sbr134.Google ScholarPubMed
Gray, KM, Hart, CL, Christie, DK, Upadhyaya, HP (2008). Tolerability and effects of oral Δ9-tetrahydrocannabinol in older adolescents with marijuana use disorders. Pharmacology, Biochemistry and Behavior 91, 67–70.CrossRefGoogle ScholarPubMed
Green, B, Kavanagh, D, Young, R (2003). Being stoned: a review of self-reported cannabis effects. Drug and Alcohol Review 22, 453–460.CrossRefGoogle ScholarPubMed
Grotenhermen, F (2003). Pharmacokinetics and pharmacodynamics of cannabinoids. Clinical Pharmacokinetics 42, 327–360.CrossRefGoogle 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
Hayasaka, S, Nichols, TE (2003). Validating cluster size inference: random field and permutation methods. Neuroimage 20, 2343–2356.CrossRefGoogle ScholarPubMed
Henquet, C, Krabbendam, L, Spauwen, J, Kaplan, C, Lieb, R, Wittchen, HU, van Os, J (2004). Prospective cohort study of cannabis use, predisposition for psychosis, and psychotic symptoms in young people. British Medical Journal 330, 11–14.CrossRefGoogle ScholarPubMed
Hester, R, Nestor, L, Garavan, H (2009). Impaired error awareness and anterior cingulate cortex hypoactivity in chronic cannabis users. Neuropsychopharmacology 4, 2450–2458.CrossRefGoogle Scholar
Honea, R, Crow, TJ, Passingham, D, Mackay, CE (2005). Regional deficits in brain volume in schizophrenia: a meta-analysis of voxel-based morphometry studies. American Journal of Psychiatry 162, 2233–2245.CrossRefGoogle ScholarPubMed
Honey, GD, Corlett, PR, Absolam, AR, Lee, M, Pomarol-Clotet, E, Murray, GK, McKenna, PJ, Bullmore, ET, Menon, DK, Fletcher, PC (2008). Individual differences in psychotic effects of ketamine are predicted by brain function measure under placebo. Journal of Neuroscience 28, 6295–7303.CrossRefGoogle ScholarPubMed
Huddy, VC, Aron, AR, Harrison, M, Barnes, TR, Robbins, TW, Joyce, EM (2009). Impaired conscious and preserved unconscious inhibitory processing in recent onset schizophrenia. Psychological Medicine 39, 907–916.CrossRefGoogle ScholarPubMed
Hughes, ME, Fulham, WR, Johnston, PK, Michie, PT (2012). Stop-signal response inhibition in schizophrenia: behavioural, event-related potential and functional neuroimaging data. Biological Psychiatry 89, 220–231.CrossRefGoogle ScholarPubMed
Jardri, R, Pouchet, A, Pins, D, Thomas, P (2011). Cortical activations during auditory verbal hallucinations in schizophrenia: a coordinate-based meta-analysis. American Journal of Psychiatry 168, 73–81.CrossRefGoogle ScholarPubMed
Kay, SR, Fiszbein, A, Opler, LA (1987). The Positive and Negative Syndrome Scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261–276.CrossRefGoogle ScholarPubMed
Kiehl, KA, Smith, AM, Hare, RD, Liddle, PF (2000). An event-related potential investigation of response inhibition in schizophrenia and psychopathy. Biological Psychiatry 48, 210–221.CrossRefGoogle ScholarPubMed
Lemberger, L, Axelrod, J, Kopin, IJ (1971). Metabolism disposition of Δ9-tetrahydrocannabinol in man. Pharmacological Review 23, 371–380.Google ScholarPubMed
Lorenzetti, V, Lubman, DI, Whittle, S, Solowij, N, Yucel, M (2010). Structural MRI findings in long-term cannabis users: what do we know? Substance Use and Misuse 45, 1787–1808.CrossRefGoogle ScholarPubMed
Martín-Santos, R, Fagundo, AB, Crippa, JA, Atakan, Z, Bhattacharyya, S, Allen, P, Fusar-Poli, P, Borgwardt, S, Seal, M, Busatto, GF, McGuire, P (2010). Neuroimaging in cannabis use: a systematic review of the literature. Psychological Medicine 40, 383–398.CrossRefGoogle ScholarPubMed
Marvel, CL, Turner, BM, O'Leary, DS, Johnson, HJ, Pierson, RK, Pnoto, LL, Andreasen, NC (2007). The neural correlates of implicit sequence learning in schizophrenia. Neuropsychology 21, 761–777.CrossRefGoogle ScholarPubMed
McDonald, B, Highley, JR, Walker, MA, Herron, BM, Cooper, SJ, Esiri, MM, Crow, TJ (2000). Anomalous asymmetry of fusiform and parahippocampal gyrus gray matter in schizophrenia: a postmortem study. American Journal of Psychiatry 157, 40–47.CrossRefGoogle ScholarPubMed
McGuire, PK, Jones, P, Harvey, I, Williams, M, McGuffin, P, Murray, RM (1995). Morbid risk of schizophrenia for relatives of patients with cannabis-associated psychosis. Schizophrenia Research 15, 277–281.CrossRefGoogle ScholarPubMed
Mechelli, A, Fusar-Poli, P, Papagni, SA, Tognin, S, Kambeitz, J, Fu, C, Picchioni, M, Walshe, M, Toulopoulou, T, Bramon, E, Murray, R, McGuire, P (2012). Genetic vulnerability to psychosis and cortical function: epistatic effects between DAAO and G72. Current Pharmacological Design 18, 510–517.Google ScholarPubMed
Meijer, JH, Schmitz, N, Nieman, DH, Becker, HE, van Amelsvoort, TA, Dingemans, PM, Linszen, DH, de Haan, L (2011). Semantic fluency deficits and reduced grey matter before transition to psychosis: a voxelwise correlational analysis. Psychiatry Research 194, 1–6.CrossRefGoogle ScholarPubMed
Moore, THM, Zammit, S, Lingford-Hughes, A, Barnes, TRE, Jones, PB, Burke, M, Lewis, G (2007). Cannabis use and risk of psychotic or affective mental health outcomes: a systematic review. Lancet 370, 319–328.CrossRefGoogle ScholarPubMed
Morrison, PD, Zois, V, McKeown, DA, Lee, TD, Holt, DW, Powell, JF, Kapur, S, Murray, RM (2009). The acute effects of synthetic intravenous Δ9-tetrahydrocannabinol on psychosis, mood and cognitive functioning. Psychological Medicine 39, 1607–1616.CrossRefGoogle ScholarPubMed
Ohlsson, A, Lindgren, JE, Wahlen, A, Agurell, S, Hollister, LE, Gillespie, HK (1980). Plasma delta-9 tetrahydrocannabinol concentrations clinical effects after oral intravenous administration smoking. Clinical Pharmacology and Therapeutics 28, 409–416.CrossRefGoogle ScholarPubMed
Peters, BD, de Koning, P, Dingemans, P, Becker, H, Linszen, DH, de Haan, L (2009). Subjective effects of cannabis before the first psychotic episode. Australian and New Zealand Journal of Psychiatry 43, 1155–1162.CrossRefGoogle ScholarPubMed
Rabe-Hesketh, S, Bullmore, ET, Brammer, MJ (1997). The analysis of functional magnetic resonance images. Statistical Methods in Medical Research 6, 215–237.CrossRefGoogle ScholarPubMed
Ramaekers, JG, Kauert, G, Theunissen, EL, Toennes, SW, Moeller, MR (2009). Neurocognitive performance during acute THC intoxication in heavy and occasional cannabis users. Journal of Psychopharmacology 23, 266–277.CrossRefGoogle ScholarPubMed
Roberts, GM, Garavan, H (2010). Evidence of increased activation underlying cognitive control in ecstasy and cannabis users. Neuroimage 15, 429–435.CrossRefGoogle Scholar
Rubia, K, Russell, T, Bullmore, ET, Soni, W, Brammer, MJ, Simmons, A, Taylor, E, Andrew, C, Giampietro, V, Sharma, T (2001 a). An fMRI study of reduced left prefrontal activation in schizophrenia during normal inhibitory function. Schizophrenia Research 52, 47–55.CrossRefGoogle ScholarPubMed
Rubia, K, Russell, T, Overmeyer, S, Brammer, MJ, Bullmore, ET, Sharma, T, Simmons, A, William, SC, Giampetro, V, Andrew, CM, Taylor, E (2001 b). Mapping motor inhibition: conjunctive brain activations across different versions of go/no-go and stop tasks. Neuroimage 13, 250–261.CrossRefGoogle ScholarPubMed
Rubia, K, Smith, AB, Brammer, MJ, Taylor, E (2007). Temporal lobe dysfunction in medication-naïve boys with attention-deficit/hyperactivity disorder during attention allocation and its relation to response variability. Biological Psychiatry 62, 999–1006.CrossRefGoogle ScholarPubMed
Simmonds, DJ, Pekar, JJ, Mostofsky, SH (2008). Meta-analysis of go/no-go tasks demonstrating that fMRI activation associated with response inhibition task is task-dependent. Neuropsychologia 46, 224–232.CrossRefGoogle ScholarPubMed
Smieskova, R, Fusar-Poli, P, Allen, P, Bendfeldt, K, Stieglitz, RD, Drewe, J, Radue, EW, McGuire, PK, Riecher-Rössler, A, Borgwardt, SJ (2010). Neuroimaging predictors of transition to psychosis – a systematic review and meta-analysis. Neuroscience and Biobehavioral Reviews 34, 1207–1222.CrossRefGoogle ScholarPubMed
Stirling, J, Barkus, EJ, Nabosi, L, Irshad, S, Roemer, G, Schreudergoidheijt, B, Lewis, S (2008). Cannabis-induced psychotic-like experiences are predicted by high schizotypy. Confirmation of preliminary results in a large cohort. Psychopathology 41, 371–378.Google ScholarPubMed
Stone, JM, Howes, OD, Egerton, A, Kambeitz, J, Allen, P, Lythgoe, DJ, O'Gorman, RL, McLean, MA, Barker, GJ, McGuire, P (2010). Altered relationship between hippocampal glutamate levels and striatal dopamine function in subjects at ultra high risk of psychosis. Biological Psychiatry 68, 599–602.CrossRefGoogle ScholarPubMed
Tapert, SF, Schweinsburg, AD, Drummond, SPA, Paulus, MP, Brown, SA, Yang, TT, Frank, LR (2007). Functional MRI of inhibitory processing in abstinent adolescent marijuana users. Psychopharmacology 194, 173–183.CrossRefGoogle ScholarPubMed
Thirion, B, Pinel, P, Tucholka, A, Roche, A, Ciuciu, P, Mangin, JF, Poline, JB (2007). Structural analysis of fMRI data revisited: improving the sensitivity and reliability of fMRI group studies. IEEE Transactions on Medical Imaging 26, 1256–1269.CrossRefGoogle ScholarPubMed
Thomas, H (1996). A community survey of adverse effects of cannabis use. Drug and Alcohol Dependence 42, 201–207.CrossRefGoogle ScholarPubMed
Turken, AU, Vuilleumier, P, Mathalon, DH, Swick, D, Ford, JM (2003). Are impairments of action monitoring and executive control true dissociative dysfunctions in patients with schizophrenia? American Journal of Psychiatry 160, 1881–1883.CrossRefGoogle ScholarPubMed
van Winkel, R; Genetic Risk and Outcome of Psychosis (GROUP) Investigators (2011). Family-based analysis of genetic variation underlying psychosis-inducing effects of cannabis: sibling analysis and proband follow-up. Archives of General Psychiatry 68, 148–157.CrossRefGoogle ScholarPubMed
Winton-Brown, TT, Allen, P, Bhattacharrya, S, Borgwardt, SJ, Fusar-Poli, P, Crippa, JA, Seal, M, Martín-Santos, R, Ffytche, D, Zuardi, AW, Atakan, Z, McGuire, PK (2011). Modulation of auditory and visual processing by delta-9-tetrahydrocannabinol and cannabidiol: an fMRI study. Neuropsychopharmacology 36, 1340–1348.CrossRefGoogle ScholarPubMed
Witthaus, H, Kaufmann, C, Bohner, G, Ozgurdal, S, Gudlowski, Y, Gallinat, J, Ruhrmann, S, Brune, M, Heinz, A, Klingebiel, R, Juckel, G (2009). Gray matter abnormalities in subjects at ultra-high risk for schizophrenia and first-episode schizophrenic patients compared to healthy controls. Psychiatry Research 173, 163–169.CrossRefGoogle ScholarPubMed
Wolf, DH, Gur, RC, Valdez, JN, Loughead, J, Elliott, MA, Gur, R, Ragland, JD (2007). Alterations of fronto-temporal connectivity during word encoding in schizophrenia. Psychiatry Research 154, 221–232.CrossRefGoogle ScholarPubMed
Zammit, S, Allebeck, P, Andreasson, S, Lundberg, I, Lewis, G (2002). Self reported cannabis use as a risk factor for schizophrenia in Swedish conscripts of 1969: historical cohort study. British Medical Journal 325, 1199–1201.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Atakan supplementary material

Atakan supplementary material

Download Atakan supplementary material(PDF)
PDF 501.6 KB