Susceptibility of the adolescent brain to cannabinoids: Long-term hippocampal effects and relevance to schizophrenia

Translational Psychiatry

Volumn 2, Issue , 2012, Pages

  Gleason, K A ^a   Birnbaum, S G ^a   Shukla, A ^a   Ghose, S ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

adolescence; cannabis; endocannabinoid; hippocampus; mGluR5

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; ACYLGLYCEROL LIPASE; CANNABINOID; ENDOCANNABINOID; FATTY ACID AMIDASE; LIPOPROTEIN LIPASE; METABOTROPIC RECEPTOR 5; BENZOXAZINE DERIVATIVE; CANNABINOID 1 RECEPTOR; METABOTROPIC RECEPTOR; MORPHOLINE DERIVATIVE; NAPHTHALENE DERIVATIVE;

ADOLESCENT; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; CONTROLLED STUDY; FEAR; HIPPOCAMPUS; LEARNING DISORDER; LOCOMOTION; MOUSE; NONHUMAN; PREPULSE INHIBITION; PROTEIN EXPRESSION; SCHIZOPHRENIA; SENSORY GATING; SIGNAL TRANSDUCTION; SOCIAL INTERACTION; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; CHEMICALLY INDUCED DISORDER; CONDITIONING; DISEASE MODEL; DISEASE PREDISPOSITION; DRUG EFFECT; INHIBITION (PSYCHOLOGY); PATHOPHYSIOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; BENZOXAZINES; CANNABINOIDS; CONDITIONING (PSYCHOLOGY); DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; FEAR; HIPPOCAMPUS; INHIBITION (PSYCHOLOGY); MICE; MICE, INBRED C57BL; MORPHOLINES; NAPHTHALENES; RECEPTOR, CANNABINOID, CB1; RECEPTORS, METABOTROPIC GLUTAMATE; SCHIZOPHRENIA;

EID: 84870786096     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2012.122     Document Type: Article

References (94)

1. Substance Abuse and Mental Health Services Administration Results from the 2010 National Survey on Drug Use and Health. Summary of National Findings: Rockville, MD, 2011.
2. Johnston LD, O'Malley PM, Bachman JG, Schulenberg JE. "Marijuana use continues to rise among U. S. teens, while alcohol use hits historic lows". University of Michigan News Service: Ann Arbor, MI, Retrieved 05/10/12ww. monitoringthefuture. org, 2011.
3. Andreasson S, Allebeck P, Engstrom A, Rydberg U. Cannabis and schizophrenia. A longitudinal study of Swedish conscripts. Lancet 1987; 2: 1483-1486.
4. Arseneault L, Cannon M, Poulton R, Murray R, Caspi A, Moffitt TE. Cannabis use in adolescence and risk for adult psychosis: longitudinal prospective study. BMJ 2002; 325: 1212-1213. (Pubitemid 35398785)
5. van Os J, Bak M, Hanssen M, Bijl RV, de Graaf R, Verdoux H. Cannabis use and psychosis: a longitudinal population-based study. Am J Epidemiol 2002; 156: 319-327. (Pubitemid 34857999)
6. Zammit S, Allebeck P, Andreasson S, Lundberg I, Lewis G. Self reported cannabis use as a risk factor for schizophrenia in Swedish conscripts of 1969: historical cohort study. BMJ 2002; 325: 1199.
7. Henquet C, Krabbendam L, Spauwen J, Kaplan C, Lieb R, Wittchen HU et al. Prospective cohort study of cannabis use, predisposition for psychosis, and psychotic symptoms in young people. BMJ 2005; 330: 11.
8. Caspi A, Moffitt TE, Cannon M, McClay J, Murray R, Harrington H et al. 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 X environment interaction. Biol Psychiatry 2005; 57: 1117-1127. (Pubitemid 40615773)
9. Moore TH, Zammit S, Lingford-Hughes A, Barnes TR, Jones PB, Burke M et al. Cannabis use and risk of psychotic or affective mental health outcomes: a systematic review. Lancet 2007; 370: 319-328. (Pubitemid 47094993)
10. Kim J, Alger BE. Inhibition of cyclooxygenase-2 potentiates retrograde endocannabinoid effects in hippocampus. Nat Neurosci 2004; 7: 697-698. (Pubitemid 38859050)
11. Makara JK, Mor M, Fegley D, Szabo SI, Kathuria S, Astarita G et al. Selective inhibition of 2-AG hydrolysis enhances endocannabinoid signaling in hippocampus. Nat Neurosci 2005; 8: 1139-1141. (Pubitemid 43348129)
12. Hashimotodani Y, Ohno-Shosaku T, Kano M. Presynaptic monoacylglycerol lipase activity determines basal endocannabinoid tone and terminates retrograde endocannabinoid signaling in the hippocampus. J Neurosci 2007; 27: 1211-1219. (Pubitemid 46203330)
13. Ligresti A, Cascio MG, Di Marzo V. Endocannabinoid metabolic pathways and enzymes. Curr Drug Targets CNS Neurol Disord 2005; 4: 615-623. (Pubitemid 41782623)
14. Irving AJ, Coutts AA, Harvey J, Rae MG, Mackie K, Bewick GS et al. Functional expression of cell surface cannabinoid CB(1) receptors on presynaptic inhibitory terminals in cultured rat hippocampal neurons. Neuroscience 2000; 98: 253-262. (Pubitemid 30347287)
15. Katona I, Sperlagh B, Sik A, Kafalvi A, Vizi ES, Mackie K et al. Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 1999; 19: 4544-4558. (Pubitemid 29241104)
16. Eggan SM, Melchitzky DS, Sesack SR, Fish KN, Lewis DA. Relationship of cannabinoid CB1 receptor and cholecystokinin immunoreactivity in monkey dorsolateral prefrontal cortex. Neuroscience 169: 1651-1661.
17. Spano MS, Ellgren M, Wang X, Hurd YL. Prenatal cannabis exposure increases heroin seeking with allostatic changes in limbic enkephalin systems in adulthood. Biol Psychiatry 2007; 61: 554-563. (Pubitemid 46185333)
18. Rubino T, Realini N, Braida D, Alberio T, Capurro V, Vigano D et al. The depressive phenotype induced in adult female rats by adolescent exposure to THC is associated with cognitive impairment and altered neuroplasticity in the prefrontal cortex. Neurotox Res 2009; 15: 291-302.
19. Schneider M, Koch M. Chronic pubertal, but not adult chronic cannabinoid treatment impairs sensorimotor gating, recognition memory, and the performance in a progressive ratio task in adult rats. Neuropsychopharmacology 2003; 28: 1760-1769. (Pubitemid 41070841)
20. Schneider M, Koch M. The effect of chronic peripubertal cannabinoid treatment on deficient object recognition memory in rats after neonatal mPFC lesion. Eur Neuropsychopharmacol 2007; 17: 180-186. (Pubitemid 44779191)
21. Wegener N, Koch M. Behavioural disturbances and altered Fos protein expression in adult rats after chronic pubertal cannabinoid treatment. Brain Res 2009; 1253: 81-91.
22. Ellgren M, Spano SM, Hurd YL. Adolescent cannabis exposure alters opiate intake and opioid limbic neuronal populations in adult rats. Neuropsychopharmacology 2007; 32: 607-615.
23. Eggan SM, Stoyak SR, Verrico CD, Lewis DA. Cannabinoid CB1 receptor immunoreactivity in the prefrontal cortex: comparison of schizophrenia and major depressive disorder. Neuropsychopharmacology Sep 35: 2060-2071.
24. Dean B, Sundram S, Bradbury R, Scarr E, Copolov D. Studies on [3 H]CP-55940 binding in the human central nervous system: regional specific changes in density of cannabinoid-1 receptors associated with schizophrenia and cannabis use. Neuroscience 2001; 103: 9-15. (Pubitemid 32304342)
25. Zavitsanou K, Garrick T, Huang XF. Selective antagonist [3 H]SR141716A binding to cannabinoid CB1 receptors is increased in the anterior cingulate cortex in schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 2004; 28: 355-360. (Pubitemid 38130143)
26. Koethe D, Llenos IC, Dulay JR, Hoyer C, Torrey EF, Leweke FM et al. Expression of CB1 cannabinoid receptor in the anterior cingulate cortex in schizophrenia, bipolar disorder, and major depression. J Neural Transm 2007; 114: 1055-1063. (Pubitemid 47106441)
27. Lu YM, Jia Z, Janus C, Henderson JT, Gerlai R, Wojtowicz JM et al. Mice lacking metabotropic glutamate receptor 5 show impaired learning and reduced CA1 long-term potentiation (LTP) but normal CA3 LTP. J Neurosci 1997; 17: 5196-5205. (Pubitemid 27263833)
28. Xu J, Zhu Y, Contractor A, Heinemann SF. mGluR5 has a critical role in inhibitory learning. J Neurosci 2009; 29: 3676-3684.
29. Wang H, Westin L, Nong Y, Birnbaum S, Bendor J, Brismar H et al. Norbin is an endogenous regulator of metabotropic glutamate receptor 5 signaling. Science 2009; 326: 1554-1557.
30. Swerdlow NR, Shoemaker JM, Platten A, Pitcher L, Goins J, Auerbach PP. Heritable differences in the dopaminergic regulation of sensorimotor gating. I. Apomorphine effects on startle gating in albino and hooded outbred rat strains and their F1 and N2 progeny. Psychopharmacology (Berl) 2004; 174: 441-451. (Pubitemid 39119334)
31. Herkenham M, Lynn AB, Little MD, Johnson MR, Melvin LS, de Costa BR et al. Cannabinoid receptor localization in brain. Proc Natl Acad Sci USA 1990; 87: 1932-1936.
32. Lichtman AH, Dimen KR, Martin BR. Systemic or intrahippocampal cannabinoid administration impairs spatial memory in rats. Psychopharmacology (Berl) 1995; 119: 282-290.
33. Robbe D, Montgomery SM, Thome A, Rueda-Orozco PE, McNaughton BL, Buzsaki G. Cannabinoids reveal importance of spike timing coordination in hippocampal function. Nat Neurosci 2006; 9: 1526-1533. (Pubitemid 44862661)
34. Egashira N, Mishima K, Iwasaki K, Fujiwara M. Intracerebral microinjections of delta 9-tetrahydrocannabinol: search for the impairment of spatial memory in the eight-arm radial maze in rats. Brain Res 2002; 952: 239-245.
35. Lawston J, Borella A, Robinson JK, Whitaker-Azmitia PM. Changes in hippocampal morphology following chronic treatment with the synthetic cannabinoid WIN 55, 212-2. Brain Res 2000; 877: 407-410.
36. Tagliaferro P, Javier Ramos A, Onaivi ES, Evrard SG, Lujilde J, Brusco A. Neuronal cytoskeleton and synaptic densities are altered after a chronic treatment with the cannabinoid receptor agonist WIN 55, 212-2. Brain Res 2006; 1085: 163-176.
37. Squire LR. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 1992; 99: 195-231.
38. Gabrieli JD. Cognitive neuroscience of human memory. Annu Rev Psychol 1998; 49: 87-115. (Pubitemid 128491769)
39. Eichenbaum HE CN. From Conditioning to Conscious Recollection: Memory Systems of the Brain. Oxford University Press: New York, 2001.
40. Keefe RS, Silverman JM, Mohs RC, Siever LJ, Harvey PD, Friedman L et al. Eye tracking, attention, and schizotypal symptoms in nonpsychotic relatives of patients with schizophrenia. Arch Gen Psychiatry 1997; 54: 169-176. (Pubitemid 27074305)
41. Ragland JD, Cools R, Frank M, Pizzagalli DA, Preston A, Ranganath C et al. CNTRICS final task selection: long-term memory. Schizophr Bull 2009; 35: 197-212.
42. Stone M, Gabrieli JD, Stebbins GT, Sullivan EV. Working and strategic memory deficits in schizophrenia. Neuropsychology 1998; 12: 278-288. (Pubitemid 28188868)
43. Weiss AP, Goff D, Schacter DL, Ditman T, Freudenreich O, Henderson D et al. Fronto-hippocampal function during temporal context monitoring in schizophrenia. Biol Psychiatry 2006; 60: 1268-1277. (Pubitemid 44693542)
44. Shohamy D, Mihalakos P, Chin R, Thomas B, Wagner AD, Tamminga C. Learning and generalization in schizophrenia: effects of disease and antipsychotic drug treatment. Biol Psychiatry 67: 926-932.
45. Titone D, Ditman T, Holzman PS, Eichenbaum H, Levy DL. Transitive inference in schizophrenia: impairments in relational memory organization. Schizophr Res 2004; 68: 235-247. (Pubitemid 38526146)
46. Aleman A, Hijman R, de Haan EH, Kahn RS. Memory impairment in schizophrenia: a metaanalysis. Am J Psychiatry 1999; 156: 1358-1366.
47. Danion JM, Rizzo L, Bruant A. Functional mechanisms underlying impaired recognition memory and conscious awareness in patients with schizophrenia. Arch Gen Psychiatry 1999; 56: 639-644.
48. Achim AM, Bertrand MC, Sutton H, Montoya A, Czechowska Y, Malla AK et al. Selective abnormal modulation of hippocampal activity during memory formation in first-episode psychosis. Arch Gen Psychiatry 2007; 64: 999-1014. (Pubitemid 47360845)
49. Heckers S, Zalesak M, Weiss AP, Ditman T, Titone D. Hippocampal activation during transitive inference in humans. Hippocampus 2004; 14: 153-162. (Pubitemid 38477102)
50. Leube DT, Rapp A, Buchkremer G, Bartels M, Kircher TT, Erb M et al. Hippocampal dysfunction during episodic memory encoding in patients with schizophrenia-an fMRI study. Schizophr Res 2003; 64: 83-85. (Pubitemid 37153353)
51. O'Shea M, McGregor IS, Mallet PE. Repeated cannabinoid exposure during perinatal, adolescent or early adult ages produces similar longlasting deficits in object recognition and reduced social interaction in rats. J Psychopharmacol 2006; 20: 611-621. (Pubitemid 44315859)
52. O'Shea M, Singh ME, McGregor IS, Mallet PE. Chronic cannabinoid exposure produces lasting memory impairment and increased anxiety in adolescent but not adult rats. J Psychopharmacol 2004; 18: 502-508. (Pubitemid 39665118)
53. Quinn HR, Matsumoto I, Callaghan PD, Long LE, Arnold JC, Gunasekaran N et al. Adolescent rats find repeated Delta(9)-THC less aversive than adult rats but display greater residual cognitive deficits and changes in hippocampal protein expression following exposure. Neuropsychopharmacology 2008; 33: 1113-1126. (Pubitemid 351367534)
54. Wise LE, Thorpe AJ, Lichtman AH. Hippocampal CB(1) receptors mediate the memory impairing effects of Delta(9)-tetrahydrocannabinol. Neuropsychopharmacology 2009; 34: 2072-2080.
55. Broadbent NJ, Gaskin S, Squire LR, Clark RE. Object recognition memory and the rodent hippocampus. Learn Mem Jan 17: 5-11.
56. Nadel L, Hardt O. The spatial brain. Neuropsychology 2004; 18: 473-476. (Pubitemid 38944383)
57. Gray L, van den Buuse M, Scarr E, Dean B, Hannan AJ. Clozapine reverses schizophrenia-related behaviours in the metabotropic glutamate receptor 5 knockout mouse: association with N-methyl-D-aspartic acid receptor up-regulation. Int J Neuropsychopharmacol 2009; 12: 45-60.
58. Homayoun H, Stefani MR, Adams BW, Tamagan GD, Moghaddam B. Functional interaction between NMDA and mGlu5 receptors: effects on working memory, instrumental learning, motor behaviors, and dopamine release. Neuropsychopharmacology 2004; 29: 1259-1269. (Pubitemid 38780649)
59. Kinney GG, O'Brien JA, Lemaire W, Burno M, Bickel DJ, Clements MK et al. A novel selective positive allosteric modulator of metabotropic glutamate receptor subtype 5 has in vivo activity and antipsychotic-like effects in rat behavioral models. J Pharmacol Exp Ther 2005; 313: 199-206. (Pubitemid 40411343)
60. Chan MH, Chiu PH, Sou JH, Chen HH. Attenuation of ketamine-evoked behavioral responses by mGluR5 positive modulators in mice. Psychopharmacology (Berl) 2008; 198: 141-148.
61. Noetzel MJ, Rook JM, Vinson PN, Cho HP, Days E, Zhou Y et al. Functional impact of allosteric agonist activity of selective positive allosteric modulators of metabotropic glutamate receptor subtype 5 in regulating central nervous system function. Mol Pharmacol Feb 81: 120-133.
62. Ellgren M, Artmann A, Tkalych O, Gupta A, Hansen HS, Hansen SH et al. Dynamic changes of the endogenous cannabinoid and opioid mesocorticolimbic systems during adolescence: THC effects. Eur Neuropsychopharmacol 2008; 18: 826-834.
63. Rubino T, Guidali C, Vigano D, Realini N, Valenti M, Massi P et al. CB1 receptor stimulation in specific brain areas differently modulate anxiety-related behaviour. Neuropharmacology 2008; 54: 151-160. (Pubitemid 350299412)
64. Chadwick B, Saylor AJ, Lopez HH. Adolescent cannabinoid exposure attenuates adult female sexual motivation but does not alter adulthood CB(1)R expression or estrous cyclicity. Pharmacol Biochem Behav 2011; 100: 157-164.
65. Hirvonen J, Goodwin RS, Li CT, Terry GE, Zoghbi SS, Morse C et al. Reversible and regionally selective downregulation of brain cannabinoid CB(1) receptors in chronic daily cannabis smokers. Mol Psychiatry 2012; 17: 642-649.
66. Moore NL, Greenleaf AL, Acheson SK, Wilson WA, Swartzwelder HS, Kuhn CM. Role of cannabinoid receptor type 1 desensitization in greater tetrahydrocannabinol impairment of memory in adolescent rats. J Pharmacol Exp Ther 2010; 335: 294-301.
67. Renthal W, Nestler EJ. Epigenetic mechanisms in drug addiction. Trends Mol Med 2008; 14: 341-350.
68. Levenson JM, O'Riordan KJ, Brown KD, Trinh MA, Molfese DL, Sweatt JD. Regulation of histone acetylation during memory formation in the hippocampus. J Biol Chem 2004; 279: 40545-40559. (Pubitemid 39287646)
69. Mackie K. Signaling via CNS cannabinoid receptors. Mol Cell Endocrinol 2008; 286 (1-2 Suppl 1): S60-S65.
70. Viveros MP, Marco EM, Llorente R, Lopez-Gallardo M. Endocannabinoid system and synaptic plasticity: implications for emotional responses. Neural Plast 2007; 2007: 52908.
71. Katona I, Sperlagh B, Magloczky Z, Santha E, Kofalvi A, Czirjak S et al. GABAergic interneurons are the targets of cannabinoid actions in the human hippocampus. Neuroscience 2000; 100: 797-804.
72. Hill EL, Gallopin T, Ferezou I, Cauli B, Rossier J, Schweitzer P et al. Functional CB1 receptors are broadly expressed in neocortical GABAergic and glutamatergic neurons. J Neurophysiol 2007; 97: 2580-2589. (Pubitemid 46557693)
73. Marsicano G, Lutz B. Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur J Neurosci 1999; 11: 4213-4225. (Pubitemid 30009252)
74. Matsuda LA, Bonner TI, Lolait SJ. Localization of cannabinoid receptor mRNA in rat brain. J Comp Neurol 1993; 327: 535-550. (Pubitemid 23033649)
75. Lewis DA, Hashimoto T, Volk DW. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 2005; 6: 312-324. (Pubitemid 40469985)
76. Heckers S, Stone D, Walsh J, Shick J, Koul P, Benes FM. Differential hippocampal expression of glutamic acid decarboxylase 65 and 67 messenger RNA in bipolar disorder and schizophrenia. Arch Gen Psychiatry 2002; 59: 521-529. (Pubitemid 34602934)
77. Kegeles LS, Mao X, Stanford AD, Girgis R, Ojeil N, Xu X et al. Elevated prefrontal cortex gamma-aminobutyric acid and glutamate-glutamine levels in schizophrenia measured in vivo with proton magnetic resonance spectroscopy. Arch Gen Psychiatry 2012; 69: 449-459.
78. Arendt M, Rosenberg R, Foldager L, Perto G, Munk-Jorgensen P. . Cannabis-induced psychosis and subsequent schizophrenia-spectrum disorders: follow-up study of 535 incident cases. Br J Psychiatry 2005; 187: 510-515. (Pubitemid 41752739)
79. Barnes TR, Mutsatsa SH, Hutton SB, Watt HC, Joyce EM. Comorbid substance use and age at onset of schizophrenia. Br J Psychiatry 2006; 188: 237-242. (Pubitemid 43341651)
80. Caspari D. Cannabis and schizophrenia: results of a follow-up study. Eur Arch Psychiatry Clin Neurosci 1999; 249: 45-49. (Pubitemid 29366776)
81. Green AI, Tohen MF, Hamer RM, Strakowski SM, Lieberman JA, Glick I et al. First episode schizophrenia-related psychosis and substance use disorders: acute response to olanzapine and haloperidol. Schizophr Res 2004; 66: 125-135. (Pubitemid 38041110)
82. Hambrecht M, Hafner H. Cannabis, vulnerability, and the onset of schizophrenia: an epidemiological perspective. Aust N Z J Psychiatry 2000; 34: 468-475. (Pubitemid 30389416)
83. Degenhardt L, Tennant C, Gilmour S, Schofield D, Nash L, Hall W et al. The temporal dynamics of relationships between cannabis, psychosis and depression among young adults with psychotic disorders: findings from a 10-month prospective study. Psychol Med 2007; 37: 927-934. (Pubitemid 46993593)
84. Grech A, Van Os J, Jones PB, Lewis SW, Murray RM. Cannabis use and outcome of recent onset psychosis. Eur Psychiatry 2005; 20: 349-353. (Pubitemid 40978562)
85. Sevy S, Robinson DG, Holloway S, Alvir JM, Woerner MG, Bilder R et al. Correlates of substance misuse in patients with first-episode schizophrenia and schizoaffective disorder. Acta Psychiatr Scand 2001; 104: 367-374. (Pubitemid 34284785)
86. McCleery A, Addington J, Addington D. Substance misuse and cognitive functioning in early psychosis: a 2 year follow-up. Schizophr Res 2006; 88: 187-191. (Pubitemid 44693239)
87. Kumra S, Thaden E, DeThomas C, Kranzler H. Correlates of substance abuse in adolescents with treatment-refractory schizophrenia and schizoaffective disorder. Schizophr Res 2005; 73: 369-371. (Pubitemid 40093902)
88. Potvin S, Briand C, Prouteau A, Bouchard RH, Lipp O, Lalonde P et al. CANTAB explicit memory is less impaired in addicted schizophrenia patients. Brain Cogn 2005; 59: 38-42. (Pubitemid 41405838)
89. Jockers-Scherubl MC, Wolf T, Radzei N, Schlattmann P, Rentzsch J, Gomez-Carrillo de Castro A et al. Cannabis induces different cognitive changes in schizophrenic patients and in healthy controls. Prog Neuropsychopharmacol Biol Psychiatry 2007; 31: 1054-1063. (Pubitemid 46824020)
90. Schnell T, Koethe D, Daumann J, Gouzoulis-Mayfrank E. The role of cannabis in cognitive functioning of patients with schizophrenia. Psychopharmacology (Berl) 2009; 205: 45-52.
91. Stirling J, White C, Lewis S, Hopkins R, Tantam D, Huddy A et al. Neurocognitive function and outcome in first-episode schizophrenia: a 10-year follow-up of an epidemiological cohort. Schizophr Res 2003; 65: 75-86. (Pubitemid 37434014)
92. Rodriguez-Sanchez JM, Ayesa-Arriola R, Mata I, Moreno-Calle T, Perez-Iglesias R, Gonzalez-Blanch C et al. Cannabis use and cognitive functioning in first-episode schizophrenia patients. Schizophr Res 2010; 124: 142-151.
93. Carey KB, Carey MP, Simons JS. Correlates of substance use disorder among psychiatric outpatients: focus on cognition, social role functioning, and psychiatric status. J Nerv Ment Dis 2003; 191: 300-308. (Pubitemid 36627204)
94. Yucel M, Bora E, Lubman DI, Solowij N, Brewer WJ, Cotton SM et al. 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 2012; 38: 316-330.