An fMRI study of neuronal activation in schizophrenia patients with and without previous cannabis use

Frontiers in Psychiatry

Volumn 3, Issue OCT, 2012, Pages

  Løberg, Else Marie ^a,b   Nygård, Merethe ^a   Berle, Jan Oystein ^b   Johnsen, Erik ^a,b   Kroken, Rune A ^b   Jørgensen, Hugo A ^a   Hugdahl, Kenneth ^a,b  

^a UNIVERSITY OF BERGEN   (Norway)

^b HAUKELAND UNIVERSITY HOSPITAL   (Norway)

Author keywords

Brain activation; Cannabis; Cognitive control; Default mode network; Dichotic listening; Effort mode network; fMRI; Schizophrenia

Indexed keywords

CANNABIS;

ADULT; ANTERIOR CINGULATE; ARTICLE; ATTENTION; AUDITORY STIMULATION; BRAIN RADIOGRAPHY; BRAIN REGION; CEREBELLUM CORTEX; CLINICAL ARTICLE; DICHOTIC LISTENING; DOWN REGULATION; ELECTROENCEPHALOGRAM; EXECUTIVE FUNCTION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; MALE; MIDDLE FRONTAL GYRUS; MIDDLE TEMPORAL GYRUS; NERVE CELL NETWORK; ON OFF PHENOMENON; ONSET AGE; ORBITAL CORTEX; POSTCENTRAL GYRUS; POSTERIOR CINGULATE; SCHIZOPHRENIA; SUPERIOR TEMPORAL GYRUS; SUPPLEMENTARY MOTOR AREA; UPREGULATION;

EID: 84870760077     PISSN: None     EISSN: 16640640     Source Type: Journal    
DOI: 10.3389/fpsyt.2012.00094     Document Type: Article

References (72)

1. American Psychiatric Association. (1994). Diagnostic and Statistical Manual of Mental Disorders, 4th Edn. Washington, DC: American Psychiatric Press.
2. Andreasson, S., Allebeck, P., Engstrom, A., and Rydberg, U. (1987). Cannabis and schizophrenia. A longitudinal study of Swedish conscripts. Lancet 2, 1483-1486.
3. Arseneault, L., Cannon, M., Witton, J., and Murray, R. M. (2004). Causal association between cannabis and psychosis: examination of the evidence.Br. J. Psychiatry 184, 110-117.
4. Ashburner, J., and Friston, K. J. (1999). Nonlinear spatial normalization using basis functions. Hum. Brain Mapp. 7, 254-266.
5. Ashtari, M., Avants, B., Cyckowski, L., Cervellione, K. L., Roofeh, D., Cook, P., et al. (2011). Medial temporal structures and memory functions in adolescents with heavy cannabis use. J. Psychiatr. Res. 45, 1055-1066.
6. Bangalore, S. S., Prasad, K. M., Montrose, D. M., Goradia, D. D., Diwadkar, V. A., and Keshavan, M. S. (2008). Cannabis use and brain structural alterations in first episode schizophrenia - a region of interest, voxel based morphometric study. Schizophr. Res. 99, 1-6.
7. Barnes, T. R., Mutsatsa, S. H., Hutton, S. B., Watt, H. C., and Joyce, E. M. (2006). Comorbid substance use and age at onset of schizophrenia. Br. J. Psychiatry 188, 237-242.
8. Bersani, G., Orlandi, V., Gherardelli, S., and Pancheri, P. (2002). Cannabis and neurological soft signs in schizophrenia: absence of relationship and influence on psychopathology. Psychopathology 35, 289-295.
9. Bhattacharyya, S., Crippa, J. A., Allen, P., Martin-Santos, R., Borgwardt, S., Fusar-Poli, P., et al. (2012). Induction of psychosis by Delta9-tetrahydrocannabinol reflects modulation of prefrontal and striatal function during attentional salience processing. Arch. Gen. Psychiatry 69, 27-36.
10. Binder, J. R. (2012). Taskinduced deactivation and the "resting" state. Neuroimage 62, 1086-1091.
11. Birchwood, M., Smith, J., Cochrane, R., Wetton, S., and Copestake, S. (1990). The Social Functioning Scale. The developmentand validationofanew scale of social adjustment for use in family intervention programmes with schizophrenic patients. Br. J. Psychiatry 157, 853-859.
12. Block, R. I., O'Leary, D. S., Ehrhardt, J. C., Augustinack, J. C., Ghoneim, M. M., Arndt, S., et al. (2000). Effects of frequent marijuana use on brain tissue volume and composition. Neuroreport 11, 491-496.
13. Bossong, M. G., Jansma, J. M., Van Hell, H. H., Jager, G., Oudman, E., Saliasi, E., et al. (2012). Effects of delta9-tetrahydrocannabinol on human working memory function. Biol. Psychiatry 71, 693-699.
14. Bossong, M. G., and Niesink, R. J. (2010). Adolescent brain maturation, the endogenous cannabinoid system and the neurobiology of cannabisinduced schizophrenia. Prog. Neurobiol. 92, 370-385.
15. Broyd, S. J., Demanuele, C., Debener, S., Helps,S.K.,James,C. J., and Sonuga-Barke, E. J. (2009). Defaultmode brain dysfunction in mental disorders: a systematic review. Neurosci. Biobehav. Rev. 33, 279-296.
16. Buckner, R. L., Raichle, M. E., Miezin, F. M., and Petersen, S. E. (1996). Functional anatomic studies of memory retrieval for auditory words and visual pictures. J. Neurosci. 16, 6219-6235.
17. Cahn, W., Hulshoff Pol, H. E., Caspers, E.,Van Haren, N. E., Schnack, H. G., and Kahn, R. S. (2004). Cannabis and brain morphology in recentonset schizophrenia. Schizophr. Res. 67, 305-307.
18. Cohen, M., Rasser, P. E., Peck, G., Carr, V. J., Ward, P. B., Thompson, P. M., et al. (2012). Cerebellar greymatter deficits, cannabis use and firstepisode schizophrenia in adolescents and young adults. Int. J. Neuropsychopharmacol. 15, 297-307.
19. Dekker, N., Schmitz, N., Peters, B. D., Van Amelsvoort, T. A., Linszen, D. H., and De Haan, L. (2010). Cannabis useand callosal white matter structure and integrity in recentonset schizophrenia. Psychiatry Res. 181, 51-56.
20. DeLisi, L. E. (2008). The effect of cannabis on the brain: can it cause brain anomalies that lead to increased risk for schizophrenia? Curr. Opin. Psychiatry 21, 140-150.
21. DeRosse, P., Kaplan, A., Burdick, K. E., Lencz, T., and Malhotra, A. K. (2010). Cannabis use disorders in schizophrenia: effects on cognition and symptoms. Schizophr. Res. 120, 95-100.
22. D'Souza, D. C., Abi-Saab, W. M., Madonick, S., Forselius-Bielen, K., Doersch, A., Braley, G., et al. (2005). Delta-9-tetrahydrocannabinol effects in schizophrenia: implications for cognition, psychosis, and addiction. Biol. Psychiatry 57, 594-608.
23. Filbey, F. M., Toulopoulou, T., Morris, R. G., Mcdonald, C., Bramon, E., Walshe, M., et al. (2008). Selective attention deficits reflect increased genetic vulnerability to schizophrenia. Schizophr. Res. 101, 169-175.
24. First, M., Spitzer, R., Gobbon, M., and Williams, J. (1995). Structured Clinical Interview for DSM-IV Axis I Disorders, Patient Edition (SCID-P), Version 2. New York: New York State Psychiatric Institute, Biometrics Research.
25. Fox, M. D., and Raichle, M. E. (2007). Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 8, 700-711.
26. Habets, P., Krabbendam, L., Hofman, P., Suckling, J., Oderwald, F., Bullmore, E., et al. (2008). Cognitive performance and grey matter density in psychosis: functional relevance of a structural endophenotype. Neuropsychobiology 58, 128-137.
27. He, Z., Deng, W., Li, M., Chen, Z., Jiang, L., Wang, Q., et al. (2012). Aberrant intrinsic brain activity and cognitive deficit in firstepisode treatmentnaive patients with schizophrenia. Psychol. Med. doi:10.1017/S0033291712001638.
28. Ho, B. C., Wassink, T. H., Ziebell, S., and Andreasen, N. C. (2011). Cannabinoid receptor 1 gene polymorphisms and marijuana misuse interactions on white matter and cognitive deficits in schizophrenia. Schizophr. Res. 128, 66-75.
29. Hugdahl, K., and Andersson, L. (1986). The "forcedattention paradigm" in dichotic listening to CV-syllables: a comparison between adults and children. Cortex 22, 417-432.
30. Hugdahl, K., Løberg,E.M., and Nygård, M. (2009). Left temporal lobe structural and functional abnormality underlying auditory hallucinations in schizophrenia. Front. Neurosci. 3:1. doi:10.3389/neuro.01.001.2009
31. Hugdahl, K., Rund,B. R., Lund, A., Asbjørnsen, A., Egeland, J., Ersland, L., et al. (2004). Brain activation measured with fMRI during a mental arithmetic task in schizophrenia and major depression. Am. J. Psychiatry 161, 286-293.
32. Insel, T. R. (2010). Rethinking schizophrenia. Nature 468, 187-193.
33. Jager, G., Kahn, R. S., Van Den Brink, W., Van Ree, J. M., and Ramsey, N. F. (2006). Long-term effects of frequent cannabis use on working memory and attention: an fMRI study. Psychopharmacology (Berl.) 185, 358-368.
34. James, A., Hough, M., James, S., Win-Mill, L., Burge, L., Nijhawan, S., et al. (2011). Greater white and grey matter changes associated with early cannabis use in adolescentonset schizophrenia (AOS). Schizophr. Res. 128, 91-97.
35. Johnsen, E., Jørgensen, H. A., Kro-Ken, R. A., and Løberg, E. M. (2011). Neurocognitive effectiveness of quetiapine, olanzapine, risperi-done, and ziprasidone: a pragmatic, randomized trial. Eur. Psychiatry. PMID:22153730. [Epub ahead of print].
36. Karlsgodt, K. H., Glahn, D. C., Van Erp, T. G., Therman, S., Huttunen, M., Manninen, M., et al. (2007). The relationship between performance and fMRI signal during working memory in patients with schizophrenia, unaffected cotwins, and control subjects. Schizophr. Res. 89, 191-197.
37. Kay, S. R., Opler, L. A., Spitzer, R. L., Williams, J. B. W., Gibbon, M., and First, M. B. (1989). Structured Clinical Interview for DSM-III-R: PANSS Version (SCID-PANSS). New York: Biometrics Research, New York State Psychiatric Institute.
38. Koch, K., Wagner, G., Nenadic, I., Schachtzabel, C., Schultz, C., Roebel, M., et al. (2008). Frontostriatal hypoactivation during correct information retrieval in patients with schizophrenia: an fMRI study. Neuroscience 153, 54-62.
39. Large, M., Sharma, S., Compton, M. T., Slade, T., and Nielssen, O. (2011). Cannabis use and earlier onset of psychosis: a systematic metaanalysis. Arch. Gen. Psychiatry 68, 555-561.
40. Løberg, E. M., and Hugdahl, K. (2009). Cannabis use and cognition in schizophrenia. Front. Hum. Neurosci. 3:53. doi:10.3389/neuro.09.053.2009
41. Løberg, E. M., Hugdahl, K., and Green, M. F. (1999). Hemispheric asymmetry in schizophrenia: a "dual deficits" model. Biol. Psychiatry 45, 76-81.
42. Mannell, M. V., Franco, A. R., Calhoun, V. D., Canive, J. M., Thoma, R. J., and Mayer, A. R. (2010). Resting state and taskinduced deactivation: a methodological comparison in patients with schizophrenia and healthy controls. Hum. Brain Mapp. 31, 424-437.
43. Martin-Santos, R., Fagundo, A. B., Crippa, J. A., Atakan, Z., Bhattacharyya, S., Allen, P., et al. (2010). Neuroimaging in cannabis use: a systematic review of the literature. Psychol. Med. 40, 383-398.
44. Meijer, J. H., Dekker, N., Koeter, M. W., Quee, P. J., Van Beveren, N. J., and Meijer, C. J. (2012). Cannabis and cognitive performance in psychosis: a crosssectional study in patients with non-affective psychotic illness and their unaffected siblings. Psychol. Med. 42, 705-716.
45. Moore, T. H., Zammit, S., Lingford-Hughes, A., Barnes, T. R., Jones, P. B., Burke, M., et al. (2007). Cannabis use and risk of psychotic or affective mental health outcomes: a systematic review. Lancet 370, 319-328.
46. Northoff, G., and Qin, P. (2011). How can the brain's resting state activity generate hallucinations? A "resting state hypothesis" of auditory verbal hallucinations. Schizophr. Res. 127, 202-214.
47. Nygård, M., Eichele, T., Løberg, E. M., Jørgensen, H. A., Johnsen, E., Kroken, R. A., et al. (2012). Patients with schizophrenia fail to up-regulate task-positive and down-regulate task-negative brain networks: an fMRI study using an ICA analysis approach. Front. Hum. Neurosci. 6:149. doi:10.3389/fnhum.2012.00149
48. Pomarol-Clotet, E., Salvador, R., Sarro, S., Gomar, J., Vila, F., Martinez, A., et al. (2008). Failure to deactivate in the prefrontal cortex in schizophrenia: dysfunction of the default mode network? Psychol. Med. 38, 1185-1193.
49. Potvin,S.,Mancini-Marie,A., Fahim, C., Mensour, B., and Stip, E. (2007). Processing of social emotion in patients with schizophrenia and substance use disorder: an fMRI study. Soc. Neurosci. 2, 106-116.
50. Rabin, R. A., Zakzanis, K. K., and George, T. P. (2011). The effects of cannabis use on neurocognition in schizophrenia: a meta-analysis. Schizophr. Res. 128, 111-116.
51. Raczkowski, D., Kalat, J. W., and Nebes, R. (1974). Reliability and validity of some handedness questionnaire items. Neuropsychologia 12, 43-47.
52. Raichle, M. E., Macleod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., and Shulman, G.L. (2001).Adefault mode of brain function. Proc. Natl. Acad. Sci. U.S.A. 98, 676-682.
53. Rais, M., Cahn, W., Van Haren, N., Schnack, H., Caspers, E., Hulshoff Pol, H., et al. (2008). Excessive brain volume loss over time in cannabis-using first-episode schizophrenia patients. Am. J. Psychiatry 165, 490-496.
54. Regier, D. A., Farmer, M. E., Rae, D. S., Locke, B. Z., Keith, S. J., Judd, L. L., et al. (1990). Comorbidity of mental disorders with alcohol and other drug abuse. Results from the Epi-demiologic Catchment Area (ECA) Study. JAMA 264, 2511-2518.
55. Rodriguez-Sanchez, J. M., Ayesa-Arriola, R., Mata, I., Moreno-Calle, T., Perez-Iglesias, R., Gonzalez-Blanch, C., et al. (2010). Cannabis use and cognitive functioning in first-episode schizophrenia patients. Schizophr. Res. 124, 142-151.
56. Ruiz-Veguilla, M., Gurpegui, M., Barrigon, M. L., Ferrin, M., Marin, E., Rubio, J. L., et al. (2009). Fewer neurological soft signs among first episode psychosis patients with heavy cannabis use. Schizophr. Res. 107, 158-164.
57. Schneider, F. C., Royer, A., Grosselin, A., Pellet, J., Barral, F. G., Laurent, B., et al. (2011). Modulation of the default mode network is task-dependant in chronic schizophrenia patients. Schizophr. Res. 125, 110-117.
58. Shulman, G. L., Fiez, J. A., Corbetta, M., Buckner,R.L., Miezin,F. M.,Raichle, M. E., et al. (1997). Common blood flow changes across visual tasks: II. Decreases in cerebral cortex. J. Cogn. Neurosci. 9, 648-663.
59. Skosnik, P. D., Ranganathan, M., and D'Souza, D. C. (2012). Cannabinoids, working memory, and schizophrenia. Biol. Psychiatry 71, 662-663.
60. Solowij, N., and Michie, P. T. (2007). Cannabis and cognitive dysfunction: parallels with endophenotypes of schizophrenia? J. Psychiatry Neurosci. 32, 30-52.
61. Solowij, N., Yucel, M., Respondek, C., Whittle, S., Lindsay, E., Pantelis, C., et al. (2011). Cerebellar whitematter changes in cannabis users with and without schizophrenia. Psychol. Med. 41, 2349-2359.
62. Stirling, J., Lewis, S., Hopkins, R., and White, C. (2005). Cannabis use prior to first onset psychosis predicts spared neurocognition at 10-year follow-up. Schizophr. Res. 75, 135-137.
63. Szeszko, P. R., Robinson, D. G., Sevy, S., Kumra, S., Rupp, C. I., Betensky, J. D., et al. (2007). Anterior cingulate grey-matter deficits and cannabis use in first-episode schizophrenia. Br. J. Psychiatry 190, 230-236.
64. Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., et al. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15, 273-289.
65. van den Noort, M., Specht, K., Rimol, L. M., Ersland, L., and Hugdahl, K. (2008). A new verbal reports fMRI dichotic listening paradigm for studies of hemispheric asymmetry. Neuroimage 40, 902-911.
66. van Wageningen, H., Jorgensen, H. A., Specht, K., and Hugdahl, K. (2009). Evidence for glutamatergic neurotransmission in cognitive control in an auditory attention task. Neurosci. Lett. 454, 171-175.
67. Whitfield-Gabrieli, S., Thermenos, H. W., Milanovic, S., Tsuang, M. T., Faraone, S. V., Mccarley, R. W., et al. (2009). Hyperactivity and hyper-connectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia. Proc. Natl. Acad. Sci. U.S.A. 106, 1279-1284.
68. WHO.(1992).TheICD-10 Classification of Mental and Behavioral Disorders. Clinical Descriptions and Diagnostic Guidelines. Geneva: World Health Organization.
69. Wobrock, T., Sittinger, H., Behrendt, B., D'Amelio, R., and Falkai, P. (2009). Comorbid substance abuse and brain morphology in recent-onset psychosis. Eur. Arch. Psychiatry Clin. Neurosci. 259, 28-36.
70. Yucel, M., Bora, E., Lubman, D. I., Solowij, N., Brewer, W. J., Cotton, S. M., et al. (2012). The impact of cannabis use on cognitive functioning in patients with schizophrenia: a meta-analysis of existing findings and new data in a first-episode sample. Schizophr. Bull. 38, 316-330.
71. Zammit, S., Allebeck, P., Andreasson, S., Lundberg, I., and Lewis, G. (2002). Self reported cannabis use as a risk factor for schizophrenia in Swedish conscripts of 1969: historical cohort study. BMJ 325, 1199.
72. Zubin, J., and Spring, B. (1977). Vulnerability - a new view of schizophrenia. J. Abnorm. Psychol. 86, 103-124.