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Cannabis abuse is associated with decision-making impairment among first-episode patients with schizophrenia-spectrum psychosis

Published online by Cambridge University Press:  16 November 2007

I. Mata ,
J. M. Rodríguez-Sánchez ,
J. M. Pelayo-Terán ,
R. Pérez-Iglesias ,
C. González-Blanch ,
M. Ramírez-Bonilla ,
O. Martínez-García ,
J. L. Vázquez-Barquero  and
B. Crespo-Facorro
I. Mata
Affiliation:
University Hospital Marques de Valdecilla, Department of Psychiatry, School of Medicine, University of Cantabria, Santander, Spain
J. M. Rodríguez-Sánchez
Affiliation:
University Hospital Marques de Valdecilla, Department of Psychiatry, School of Medicine, University of Cantabria, Santander, Spain
J. M. Pelayo-Terán
Affiliation:
University Hospital Marques de Valdecilla, Department of Psychiatry, School of Medicine, University of Cantabria, Santander, Spain
R. Pérez-Iglesias
Affiliation:
University Hospital Marques de Valdecilla, Department of Psychiatry, School of Medicine, University of Cantabria, Santander, Spain
C. González-Blanch
Affiliation:
University Hospital Marques de Valdecilla, Department of Psychiatry, School of Medicine, University of Cantabria, Santander, Spain
M. Ramírez-Bonilla
Affiliation:
University Hospital Marques de Valdecilla, Department of Psychiatry, School of Medicine, University of Cantabria, Santander, Spain
O. Martínez-García
Affiliation:
University Hospital Marques de Valdecilla, Department of Psychiatry, School of Medicine, University of Cantabria, Santander, Spain
J. L. Vázquez-Barquero
Affiliation:
University Hospital Marques de Valdecilla, Department of Psychiatry, School of Medicine, University of Cantabria, Santander, Spain
B. Crespo-Facorro*
Affiliation:
University Hospital Marques de Valdecilla, Department of Psychiatry, School of Medicine, University of Cantabria, Santander, Spain
*
*Address for correspondence: Professor B. Crespo-Facorro, Hospital Universitario Marques de Valdecilla, Department of Psychiatry, Planta 2, edificio 2 de Noviembre, Avda Valdecilla s/n, 39008, Santander, Spain. (Email: [email protected])
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Abstract

Background

Cannabis use appears to be a risk factor for schizophrenia. Moreover, cannabis abusers show impaired decision-making capacities, linked to the orbitofrontal cortex (OFC). Although there is substantial evidence that first-episode schizophrenia patients show impairments in cognitive tasks associated with the dorsolateral prefrontal cortex (DLPFC), it is not clear whether decision making is impaired at schizophrenia onset. In this study, we examined the association between antecedents of cannabis abuse and cognitive impairment in cognitive tasks associated with the DLPFC and the OFC in a sample of first-episode patients with schizophrenia-spectrum disorders.

Method

One hundred and thirty-two patients experiencing their first episode of a schizophrenia-spectrum psychosis were assessed with a cognitive battery including DLPFC-related tasks [backward digits, verbal fluency (FAS) and the Trail Making Test (TMT)] and an OFC-related task [the Iowa Gambling Task (GT)]. Performance on these tasks was compared between patients who had and had not abused cannabis before their psychosis onset.

Results

No differences were observed between the two groups on the performance of any of the DLPFC-related tasks. However, patients who had abused cannabis before their psychosis onset showed a poorer total performance on the gambling task and a lower improvement on the performance of the task compared to no-abusers.

Conclusions

Pre-psychotic cannabis abuse is associated with decision-making impairment, but not working memory and executive function impairment, among first-episode patients with a schizophrenia-spectrum psychosis. Further studies are needed to examine the direction of causality of this impairment; that is, does the impairment make the patients abuse cannabis, or does cannabis abuse cause the impairment?

Keywords

Cannabisdecision-makingIowa Gambling Taskprefrontal cortexschizophrenia
Type
Original Articles
Information
Psychological Medicine , Volume 38 , Issue 9 , September 2008 , pp. 1257 - 1266
Copyright
Copyright © 2007 Cambridge University Press

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References

Andreasen, NC (1984 a). Scale for the Assessment of Negative Symptoms (SANS). University of Iowa: Iowa City, IA.Google Scholar
Andreasen, NC (1984 b). Scale for the Assessment of Positive Symptoms (SAPS). University of Iowa: Iowa City, IA.Google Scholar
Andreasen, NC, O'Leary, DS, Flaum, M, Nopoulos, P, Watkins, GL, Hichwa, RD (1997). Hypofrontality in schizophrenia: distributed dysfunctional circuits in neuroleptic-naïve patients. Lancet 349, 1730–1734.CrossRefGoogle ScholarPubMed
Andreasson, S, Allebeck, P, Engstrom, A, Rydberg, U (1987). Cannabis and schizophrenia. A longitudinal study of Swedish conscripts. Lancet 26, 1483–1486.CrossRefGoogle Scholar
Arbuthnott, K, Frank, J (2000). Trail Making Test, Part B as a measure of executive control: validation using a set-switching paradigm. Journal of Clinical and Experimental Neuropsychology 22, 518–528.CrossRefGoogle ScholarPubMed
Arsenault, L, Cannon, M, Poulton, R, Murray, 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 Scholar
Baddeley, AD (1986). Working Memory. Oxford University Press: Oxford.Google ScholarPubMed
Barch, D, Carter, C, Braver, T, Sabb, F, MacDonald, A, Noll, DC, Cohen, J (2001). Selective deficits in prefrontal cortex function in medication-naïve patients with schizophrenia. Archives of General Psychiatry 58, 280–288.CrossRefGoogle ScholarPubMed
Bechara, A (2004). The role of emotion in decision-making: evidence from neurological patients with orbitofrontal damage. Brain and Cognition 55, 30–40.CrossRefGoogle ScholarPubMed
Bechara, A, Damasio, AR, Damasio, H, Anderson, SW (1994). Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50, 7–15.CrossRefGoogle ScholarPubMed
Bechara, A, Damasio, H, Tranel, D, Anderson, SW (1998). Dissociation of working memory from decision making within the human prefrontal cortex. Journal of Neuroscience 18, 428–437.CrossRefGoogle ScholarPubMed
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, 289–376.CrossRefGoogle ScholarPubMed
Bechara, A, Tranel, D, Damasio, H (2000). Characterization of the decision-making impairment of patients with bilateral lesions of the ventromedial prefrontal cortex. Brain 123, 2189–2202.CrossRefGoogle Scholar
Beninger, RJ, Wasserman, J, Zanibbi, K, Charbonneau, D, Mangels, J, Beninger, BV (2003). Typical and atypical antipsychotic medications differentially affect two nondeclarative memory tasks in schizophrenic patients: a double dissociation. Schizophrenia Research 61, 281–292.CrossRefGoogle ScholarPubMed
Boeka, AG, Lokken, KL (2006). The Iowa Gambling Task as a measure of decision making in women with bulimia nervosa. Journal of the International Neuropsychological Society 12, 741–745.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
Buchanan, RW, Vladat, K, Barta, PE, Pearlson, GD (1998). Structural evaluation of the prefrontal cortex in schizophrenia. American Journal of Psychiatry 155, 1049–1055.CrossRefGoogle ScholarPubMed
Cantwell, R, Brewin, J, Glazebrook, C, Dalkin, T, Fox, R, Medley, I, Harrison, G (1999). Prevalence of substance misuse in first-episode psychosis. British Journal of Psychiatry 174, 150–153.CrossRefGoogle ScholarPubMed
Carey, KB, Carey, MP, Simons, JS (2003). Correlates of substance use disorder among psychiatric outpatients: focus on cognition, social role functioning, and psychiatric status. Journal of Nervous and Mental Disorders 191, 300–308.CrossRefGoogle ScholarPubMed
Cavallaro, R, Cavedini, P, Mistretta, P, Bassi, T, Angelone, SM, Ubbiali, A, Bellodi, L (2003). Basal-corticofrontal circuits in schizophrenia and obsessive-compulsive disorder: a controlled double dissociation study. Biological Psychiatry 54, 437–443.CrossRefGoogle ScholarPubMed
Crespo-Facorro, B, Kim, JJ, Andreasen, NC, O'Leary, DS, Magnotta, V (2000). Regional frontal abnormalities in schizophrenia: a quantitative gray matter volume and cortical surface size study. Biological Psychiatry 48, 110–119.CrossRefGoogle ScholarPubMed
Crespo-Facorro, B, Kim, JJ, Andreasen, NC, O'Leary, DS, Wiser, AK, Bailey, JM, Harris, G, Magnotta, VA (1999). Human frontal cortex: an MRI-based parcellation method. Neuroimage 10, 500–519.CrossRefGoogle ScholarPubMed
Crespo-Facorro, B, Perez-Inglesias, R, Ramirez-Bonilla, ML, Martinez-Garcia, O, Llorca, J, Vazquez-Barquero, JL (2006). A practical clinical trial comparing haloperidol, risperidone and olanzapine for the acute treatment of first-episode nonaffective psychosis. Journal of Clinical Psychiatry 67, 1511–1521.CrossRefGoogle ScholarPubMed
Evans, CEY, Bowman, CH, Turnbull, OH (2005). Subjective awareness of the Iowa Gambling Task: the key role of emotional experience in schizophrenia. Journal of Clinical and Experimental Neuropsychology 27, 656–664.CrossRefGoogle ScholarPubMed
Fried, PA, Watkinson, B, Gray, R (2005). Neurocognitive consequences of marihuana – a comparison with pre-drug performance. Neurotoxicology and Teratology 27, 231–239.CrossRefGoogle ScholarPubMed
Fuster, JM (1997). The Prefrontal Cortex: Anatomy, Physiology and Neuropsychology of the Frontal Lobe, 3rd edn.Raven: New York.Google Scholar
Glahn, DC, Ragland, JD, Abramoff, A, Barrett, J, Laird, AR, Bearden, CE, Velligan, DI (2005). Beyond hypofrontality: a quantitative meta-analysis of functional neuroimaging studies of working memory in schizophrenia. Human Brain Mapping 25, 60–69.CrossRefGoogle ScholarPubMed
Goldman-Rakic, PS (1996). Regional and cellular fractionation of working memory. Proceedings of the National Academy of Sciences USA 93, 13473–13480.CrossRefGoogle Scholar
Goldstein, JM, Goodman, JM, Seidman, LJ, Kennedy, DN, Makris, N, Lee, H, Tourville, J, Caviness, VS Jr., Faraone, SV, Tsuang, MT (1999). Cortical abnormalities in schizophrenia identified by structural magnetic resonance imaging. Archives of General Psychiatry 56, 537–547.CrossRefGoogle ScholarPubMed
Grant, I, Gonzalez, R, Carey, C, Natarajan, L (2001). Long-term neurocognitive consequences of marijuana: a meta-analytic study. In National Institute on Drug Abuse Workshop on Clinical Consequences of Marijuana, August 2001, Rockville, MD (www.nida.nih.gov/MeetSum/marijuanaabstracts.html). Accessed 12 October 2006.Google Scholar
Grant, S, Contoreggi, C, London, ED (2000). Drug abusers show impaired performance in a laboratory test of decision making. Neuropsychologia 38, 1180–1187.CrossRefGoogle Scholar
Grant, S, London, ED, Neulin, DB, Villemagne, VL, Liu, X, Contoreggi, C, Phillips, RL, Kimes, AS, Margolin, A (1996). Activation of memory circuits during cue-elicited cocaine craving. Proceedings of the National Academy of Sciences USA 93, 12040–12045.CrossRefGoogle Scholar
Green, MF (1996). What are the functional consequences of neurocognitive deficits in schizophrenia? American Journal of Psychiatry 153, 321–330.Google ScholarPubMed
HaalandVØ, Landrø NI VØ, Landrø NI (2007). Decision making as measured with the Iowa Gambling Task in patients with borderline personality disorder. Journal of the International Neuropsychological Society 13, 699–703.CrossRefGoogle ScholarPubMed
Henquet, C, Murray, R, Linszen, D, van Os, J (2005). The environment and schizophrenia: the role of cannabis use. Schizophrenia Bulletin 31, 608–612.CrossRefGoogle ScholarPubMed
Hutton, SB, Murphy, FC, Joyce, EM, Rogers, RD, Cuthbert, I, Barnes, TRE, McKenna, PJ, Sahakian, BJ, Robbins, TW (2002). Decision making deficits in patients with first-episode and chronic schizophrenia. Schizophrenia Research 55, 249–257.CrossRefGoogle ScholarPubMed
Hutton, SB, Puri, BK, Duncan, LJ, Robbins, TW, Barnes, TRE, Joyce, EM (1998). Executive function in first episode schizophrenia. Psychological Medicine 28, 463–473.CrossRefGoogle ScholarPubMed
Jentsch, JD, Verrico, CD, Le, D, Roth, RH (1998). Repeated exposure to Δ9-tetrahydrocannabinol reduces prefrontal cortical dopamine metabolism in the rat. Neuroscience Letters 246, 169–172.CrossRefGoogle ScholarPubMed
Jockers-Scherübl, MC, Wolf, T, Radzei, N, Schlattmann, P, Rentzsch, J, Gomez-Carrillo de Castro, A, Kühl, K-P (2007). Cannabis induces different cognitive changes in schizophrenic patients and in healthy controls. Progress in Neuropsychopharmacology and Biological Psychiatry 31, 1054–1063.CrossRefGoogle ScholarPubMed
Jollant, F, Bellivier, F, Leboyer, M, Astruc, B, Torres, S, Verdier, R, Castelnau, D, Malafosse, A, Courtet, P (2005). Impaired decision making in suicide attempters. American Journal of Psychiatry 162, 304–310.CrossRefGoogle ScholarPubMed
Joyal, CC, Halle, P, Lapierre, D, Hodgins, S (2003). Drug abuse and/or dependence and better neuropsychological performance in patients with schizophrenia. Schizophrenia Research 63, 297–299.CrossRefGoogle ScholarPubMed
Kester, HM, Sevy, S, Yechiam, E, Burdick, KE, Cervellione, KL, Kumra, S (2006). Decision-making impairments in adolescents with early-onset schizophrenia. Schizophrenia Research 85, 113–123.CrossRefGoogle ScholarPubMed
Lee, J, Park, S (2005). Working memory impairments in schizophrenia: a meta-analysis. Journal of Abnormal Psychology 114, 599–611.CrossRefGoogle ScholarPubMed
Lezak, MD (1995). Neuropsychological Assessment, 3rd edn. Oxford University Press: New York.Google Scholar
London, ED, Ernst, M, Grant, S, Bonson, K, Weinstein, A (2000). Orbital cortex and human drug abuse: functional imaging. Cerebral Cortex 10, 334–342.CrossRefGoogle ScholarPubMed
Mazas, CA, Finn, PR, Steinmetz, JE (2000). Decision-making biases, antisocial personality, and early onset alcoholism. Alcoholism: Clinical and Experimental Research 24, 1036–1040.Google ScholarPubMed
McCleery, A, Addington, J, Addington, D (2006). Substance misuse and cognitive functioning in early psychosis: a 2 year follow-up. Schizophrenia Research 88, 187–191.CrossRefGoogle ScholarPubMed
Mintzer, MZ, Stitzer, ML (2002). Cognitive impairment in methadone maintenance patients. Drug and Alcohol Dependence 67, 41–51.CrossRefGoogle ScholarPubMed
Ohnuma, T, Kimura, M, Takahashi, T, Iwamoto, M, Arai, H (1997). A magnetic resonance imaging study in first-episode disorganized-type patients with schizophrenia. Psychiatry and Clinical Neuroscience 52, 9–15.CrossRefGoogle Scholar
Öngür, D, Price, JL (2000). The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cerebral Cortex 10, 206–219.CrossRefGoogle ScholarPubMed
Pope, HG Jr, Gruber, AJ, Hudson, JI, Huestis, MA, Yurgelun-Todd, D (2001). Neuropsychological performance in long-term cannabis users. Archives of General Psychiatry 58, 909–915.CrossRefGoogle ScholarPubMed
Potvin, S, Briand, C, Prouteau, A, Bouchard, R-H, Lipp, O, Lalonde, P, Nicole, L, Lesage, A, Stip, E (2005). CANTAB explicit memory is less impaired in addicted schizophrenia patients. Brain Cognition 59, 38–42.CrossRefGoogle ScholarPubMed
Quednow, BB, Kuhn, KU, Hoppe, C, Westheide, J, Maier, W, Daum, I, Wagner, M (2006). Elevated impulsivity and impaired decision-making cognition in heavy users of MDMA (‘ecstasy’). Psychopharmacology (Berlin) 20, 1–14.Google Scholar
Ragland, JD, Gur, RC, Glahn, DC, Censits, DM, Smith, RJ, Lazareth, MG, Alavi, A, Gur, RE (1998). Frontotemporal cerebral blood flow change during executive and declarative memory tasks in schizophrenia: a positron emission tomography study. Neuropsychology 12, 399–413.CrossRefGoogle ScholarPubMed
Ritter, LM, Meador-Woodruff, JH, Dalack, GW (2004). Neurocognitive measures of prefrontal cortical dysfunction in schizophrenia. Schizophrenia Research 68, 65–73.CrossRefGoogle ScholarPubMed
Rodriguez-Sanchez, JM, Crespo-Facorro, B, Perez-Iglesias, R, Gonzalez-Blanch, C, Alvarez, M, Llorca, J, Vazquez-Barquero, JL (2005). Prefrontal cognitive functions in stabilized first-episode patients with schizophrenia spectrum disorders: a dissociation between dorsolateral and orbitofrontal functioning. Schizophrenia Research 77, 279–288.CrossRefGoogle ScholarPubMed
Rogers, RD, Owen, AM, Middleton, HC, Williams, EJ, Pickard, JD, Sahakian, BJ, Robbins, TW (1999 a). Choosing between small, likely rewards and large unlikely rewards activates inferior and orbital prefrontal cortex. Journal of Neuroscience 20, 9029–9038.CrossRefGoogle Scholar
Rogers, RD, Everitt, BJ, Baldacchino, A, Blackshaw, AJ, Swainson, R, Wynne, K, Baker, NB, Hunter, J, Carthy, T, Booker, E, London, M, Deakin, JFW, Sahakian, BJ, Robbins, TW (1999 b). Dissociable deficits in the decision-making cognition of chronic amphetamine abusers, opiate abusers, patients with focal damage to prefrontal cortex, and tryptophan-depleted normal volunteers: evidence for monoaminergic mechanisms. Neuropsychopharmacology 20, 322–339.CrossRefGoogle ScholarPubMed
Saykin, A, Shtasel, DL, Gur, R, Kester, BD, Mozley, L, Stafiniak, P, Gur, RC (1994). Neuropsychological deficits in neuroleptic naïve patients with first episode schizophrenia. Archives of General Psychiatry 51, 123–131.CrossRefGoogle ScholarPubMed
Sevy, S, Robinson, DG, Solloway, S, Alvir, JM, Woerner, MG, Bilder, R, Goldman, R, Lieberman, J, Kane, J (2001). Correlates of substance misuse in patients with first-episode schizophrenia and schizoaffective disorder. Acta Psychiatrica Scandinavica 104, 367–374.CrossRefGoogle ScholarPubMed
Shurman, B, Horan, WP, Nuechterlein, KH (2005). Schizophrenia patients demonstrate a distinctive pattern of decision-making impairment on the Iowa Gambling Task. Schizophrenia Research 72, 215–224.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
Stirling, J, Lewis, S, Hopkins, R, White, C (2005). Cannabis use prior to first onset psychosis predicts spared neurocognition at 10-year follow-up. Schizophrenia Research 75, 135–137.CrossRefGoogle Scholar
Stuss, DT, Benson, DF (1986). The Frontal Lobes. Raven: New York.Google Scholar
Van Snellenberg, JX, Torres, IJ, Thornton, AE (2006). Functional neuroimaging of working memory in schizophrenia: task performance as a moderating variable. Neuropsychology 20, 497–510.CrossRefGoogle ScholarPubMed
Verrico, CD, Jentsch, JD, Roth, RH, Taylor, JR (2004). Repeated, intermittent Δ9-tetrahydrocannabinol administration to rats impairs acquisition and performance of a test of visuospatial divided attention. Neuropsychopharmacology 29, 522–529.CrossRefGoogle ScholarPubMed
Wechsler, D (1999). Weschler Adult Intelligence Scale III. TEA Ediciones: Madrid.Google Scholar
Whitlow, CT, Liguori, A, Livengood, LB, Hart, SL, Mussat-Whitlow, BJ, Lamborn, CM, Laurienti, PJ, Porrino, LJ (2004). Long-term heavy marijuana users make costly decisions on a gambling task. Drug and Alcohol Dependence 76, 107–111.CrossRefGoogle ScholarPubMed
Wilder, KE, Weinberger, DR, Goldberg, TE (1998). Operant conditioning and the orbitofrontal cortex in schizophrenic patients: unexpected evidence for intact functioning. Schizophrenia Research 30, 169–174.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, 1183–1184.CrossRefGoogle ScholarPubMed