Human laboratory studies on cannabinoids and psychosis

Biological Psychiatry

Volumn 79, Issue 7, 2016, Pages 526-538

  Sherif, Mohamed ^a,b,c   Radhakrishnan, Rajiv ^a,b,c   D'Souza, Deepak Cyril ^a,b,c   Ranganathan, Mohini ^a,b,c  

^a VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

^b Yale University School of Medicine   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cannabinoids; Cannabis; CB1R; Cognition; Dopamine; Experimental; GABA; Glutamate; Laboratory; Psychosis; RCT; Schizophrenia; THC

Indexed keywords

4 AMINOBUTYRIC ACID; AMPHETAMINE; BRAIN DERIVED NEUROTROPHIC FACTOR; CANNABINOID; CANNABINOID RECEPTOR; CANNABINOID RECEPTOR AGONIST; CATECHOL METHYLTRANSFERASE; DOPAMINE TRANSPORTER; ENDOCANNABINOID; GLUTAMIC ACID; KETAMINE; NEU DIFFERENTIATION FACTOR; PROTEIN KINASE B; SALVINORIN A; AKT1 PROTEIN, HUMAN; COMT PROTEIN, HUMAN; DOPAMINE; SLC6A3 PROTEIN, HUMAN;

COGNITION; COGNITIVE DEFECT; DISEASE EXACERBATION; DNA POLYMORPHISM; DOPAMINE METABOLISM; DOPAMINE RELEASE; HUMAN; NEGATIVE SYNDROME; POSITIVE SYNDROME; PRIORITY JOURNAL; PSYCHOPHYSIOLOGY; PSYCHOSIS; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SCHIZOPHRENIA; GENETICS; METABOLISM; PATHOPHYSIOLOGY;

CANNABINOID RECEPTOR AGONISTS; CANNABINOIDS; CATECHOL O-METHYLTRANSFERASE; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; ENDOCANNABINOIDS; HUMANS; PROTO-ONCOGENE PROTEINS C-AKT; PSYCHOSES, SUBSTANCE-INDUCED; RANDOMIZED CONTROLLED TRIALS AS TOPIC; SCHIZOPHRENIA;

EID: 84961801686     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2016.01.011     Document Type: Review

References (138)

1. Carbuto M, Sewell RA, Williams A, Forselius-Bielen K, Braley G, Elander J, et al. (2012): The safety of studies with intravenous Delta (9)-tetrahydrocannabinol in humans, with case histories. Psychopharmacology (Berl) 219:885-896.
2. D'Souza DC, Perry E, MacDougall L, Ammerman Y, Cooper T, Wu YT, et al. (2004): The psychotomimetic effects of intravenous delta- 9-tetrahydrocannabinol in healthy individuals: Implications for psychosis. Neuropsychopharmacology 29:1558-1572.
3. Morrison PD, Stone JM (2011): Synthetic delta-9-tetrahydrocannabinol elicits schizophrenia-like negative symptoms which are distinct from sedation. Hum Psychopharmacol 26:77-80.
4. Morrison PD, Zois V, McKeown DA, Lee TD, Holt DW, Powell JF, et al. (2009): The acute effects of synthetic intravenous Delta9- tetrahydrocannabinol on psychosis, mood and cognitive functioning. Psychol Med 39:1607-1616.
5. Kleinloog D, Liem-Moolenaar M, Jacobs G, Klaassen E, de Kam M, Hijman R, et al. (2012): Does olanzapine inhibit the psychomimetic effects of Delta9-tetrahydrocannabinol? J Psychopharmacol 26: 1307-1316.
6. Liem-Moolenaar M, te Beek ET, de Kam ML, Franson KL, Kahn RS, Hijman R, et al. (2010): Central nervous system effects of haloperidol on THC in healthy male volunteers. J Psychopharmacol 24:1697-1708.
7. D'Souza DC, Braley G, Blaise R, Vendetti M, Oliver S, Pittman B, et al. (2008): Effects of haloperidol on the behavioral, subjective, cognitive, motor, and neuroendocrine effects of Delta-9-tetrahydrocannabinol in humans. Psychopharmacology (Berl) 198:587-603.
8. D'Souza DC, Fridberg DJ, Skosnik PD, Williams A, Roach B, Singh N, et al. (2012): Dose-related modulation of event-related potentials to novel and target stimuli by intravenous Delta(9)-THC in humans. Neuropsychopharmacology 37:1632-1646.
9. Bhattacharyya S, Atakan Z, Martin-Santos R, Crippa JA, Kambeitz J, Malhi S, et al. (2015): Impairment of inhibitory control processing related to acute psychotomimetic effects of cannabis. Eur Neuropsychopharmacol 25:26-37.
10. Bhattacharyya S, Crippa JA, 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.
11. Bhattacharyya S, Fusar-Poli P, Borgwardt S, Martin-Santos R, Nosarti C, O'Carroll C, et al. (2009): Modulation of mediotemporal and ventrostriatal function in humans by Delta9-tetrahydrocannabinol: A neural basis for the effects of Cannabis sativa on learning and psychosis. Arch Gen Psychiatry 66:442-451.
12. Bhattacharyya S, Morrison PD, Fusar-Poli P, Martin-Santos R, Borgwardt S, Winton-Brown T, et al. (2010): Opposite effects of delta-9-tetrahydrocannabinol and cannabidiol on human brain function and psychopathology. Neuropsychopharmacology 35:764-774.
13. Freeman D, Dunn G, Murray RM, Evans N, Lister R, Antley A, et al. (2015): How cannabis causes paranoia: Using the intravenous administration of 9-tetrahydrocannabinol (THC) to identify key cognitive mechanisms leading to paranoia. Schizophr Bull 41: 391-399.
14. Leweke FM, Schneider U, Radwan M, Schmidt E, Emrich HM (2000): Different effects of nabilone and cannabidiol on binocular depth inversion in Man. Pharmacol Biochem Behav 66:175-181.
15. Leweke FM, Schneider U, Thies M, Munte TF, Emrich HM (1999): Effects of synthetic delta9-tetrahydrocannabinol on binocular depth inversion of natural and artificial objects in man. Psychopharmacology (Berl) 142:230-235.
16. Koethe D, Gerth CW, Neatby MA, Haensel A, Thies M, Schneider U, et al. (2006): Disturbances of visual information processing in early states of psychosis and experimental delta-9-tetrahydrocannabinol altered states of consciousness. Schizophr Res 88:142-150.
17. Emrich HM, Weber MM, Wendl A, Zihl J, von Meyer L, Hanisch W (1991): Reduced binocular depth inversion as an indicator of cannabis-induced censorship impairment. Pharmacol Biochem Behav 40:689-690.
18. Krystal JH, Perry E, Gueorguieva R, Belger A, Madonick S, Abi- Dargham A, et al. (2005): Comparative and interactive human psychopharmacologic effects of ketamine and amphetamine: Implications for glutamatergic and dopaminergic model psychoses and cognitive function. Arch Gen Psychiatry 62:985-994.
19. Ranganathan M, Schnakenberg A, Skosnik PD, Cohen BM, Pittman B, Sewell RA, et al. (2012): Dose-related behavioral, subjective, endocrine, and psychophysiological effects of the kappa opioid agonist salvinorin A in humans. Biol Psychiatry 72:871-879.
20. Iseger TA, Bossong MG (2015): A systematic review of the antipsychotic properties of cannabidiol in humans. Schizophr Res 162: 153-161.
21. Englund A, Morrison PD, Nottage J, Hague D, Kane F, Bonaccorso S, et al. (2013): Cannabidiol inhibits THC-elicited paranoid symptoms and hippocampal-dependent memory impairment. J Psychopharmacol. 27:19-27.
22. Fusar-Poli P, Crippa JA, Bhattacharyya S, Borgwardt SJ, Allen P, Martin-Santos R, et al. (2009): Distinct effects of delta9-tetrahydrocannabinol and cannabidiol on neural activation during emotional processing. Arch Gen Psychiatry 66:95-105.
23. Ranganathan M, D'Souza DC (2006): The acute effects of cannabinoids on memory in humans: A review. Psychopharmacology (Berl) 188:425-444.
24. Miller LL, McFarland D, Cornett TL, Brightwell D (1977): Marijuana and memory impairment: Effect on free recall and recognition memory. Pharmacol Biochem Behav 7:99-103.
25. Marks DF, MacAvoy MG (1989): Divided attention performance in cannabis users and non-users following alcohol and cannabis separately and in combination. Psychopharmacology 99: 397-401.
26. Leweke M, Kampmann C, Radwan M, Dietrich DE, Johannes S, Emrich HM, et al. (1998): The effects of tetrahydrocannabinol on the recognition of emotionally charged words: An analysis using eventrelated brain potentials. Neuropsychobiology 37:104-111.
27. Hooker WD, Jones RT (1987): Increased susceptibility to memory intrusions and the Stroop interference effect during acute marijuana intoxication. Psychopharmacology 91:20-24.
28. Hart CL, van Gorp W, Haney M, Foltin RW, Fischman MW (2001): Effects of acute smoked marijuana on complex cognitive performance. Neuropsychopharmacology 25:757-765.
29. Heishman SJ, Huestis MA, Henningfield JE, Cone EJ (1990): Acute and residual effects of marijuana: Profiles of plasma THC levels, physiological, subjective, and performance measures. Pharmacol Biochem Behav 37:561-565.
30. Lichtman AH, Varvel SA, Martin BR (2002): Endocannabinoids in cognition and dependence. Prostaglandins Leukot Essent Fatty Acids 66:269-285.
31. Wilson RI, Nicoll RA (2002): Endocannabinoid signaling in the brain. Science 296:678-682.
32. D'Souza DC, Abi-Saab WM, 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.
33. Hunault CC, Mensinga TT, Bocker KB, Schipper CM, Kruidenier M, Leenders ME, et al. (2009): Cognitive and psychomotor effects in males after smoking a combination of tobacco and cannabis containing up to 69 mg delta-9-tetrahydrocannabinol (THC). Psychopharmacology (Berl) 204:85-94.
34. Bocker KB, Hunault CC, Gerritsen J, Kruidenier M, Mensinga TT, Kenemans JL (2010): Cannabinoid modulations of resting state EEG theta power and working memory are correlated in humans. J Cogn Neurosci 22:1906-1916.
35. Ilan AB, Smith ME, Gevins A (2004): Effects of marijuana on neurophysiological signals of working and episodic memory. Psychopharmacology (Berl) 176:214-222.
36. Ilan AB, Gevins A, Coleman M, Elsohly MA, de Wit H (2005): Neurophysiological and subjective profile of marijuana with varying concentrations of cannabinoids. Behav Pharmacol 16: 487-496.
37. D'Souza DC, Ranganathan M, Braley G, Gueorguieva R, Zimolo Z, Cooper T, et al. (2008): Blunted psychotomimetic and amnestic effects of delta-9-tetrahydrocannabinol in frequent users of cannabis. Neuropsychopharmacology 33:2505-2516.
38. Ballard ME, de Wit H (2011): Combined effects of acute, very-lowdose ethanol and delta(9)-tetrahydrocannabinol in healthy human volunteers. Pharmacol Biochem Behav 97:627-631.
39. Curran HV, Brignell C, Fletcher S, Middleton P, Henry J (2002): Cognitive and subjective dose-response effects of acute oral Delta 9-tetrahydrocannabinol (THC) in infrequent cannabis users. Psychopharmacology (Berl) 164:61-70.
40. Polich J, Criado JR (2006): Neuropsychology and neuropharmacology of P3a and P3b. Int J Psychophysiol 60:172-185.
41. Turetsky BI, Calkins ME, Light GA, Olincy A, Radant AD, Swerdlow NR (2007): Neurophysiological endophenotypes of schizophrenia: The viability of selected candidate measures. Schizophr Bull 33: 69-94.
42. Jeon YW, Polich J (2003): Meta-analysis of P300 and schizophrenia: Patients, paradigms, and practical implications. Psychophysiology 40:684-701.
43. Bramon E, McDonald C, Croft RJ, Landau S, Filbey F, Gruzelier JH, et al. (2005): Is the P300 wave an endophenotype for schizophrenia? A meta-analysis and a family study. Neuroimage 27:960-968.
44. Solowij N, Michie PT (2007): Cannabis and cognitive dysfunction: Parallels with endophenotypes of schizophrenia? J Psychiatry Neurosci 32:30-52.
45. Bramon E, Rabe-Hesketh S, Sham P, Murray RM, Frangou S (2004): Meta-analysis of the P300 and P50 waveforms in schizophrenia. Schizophr Res 70:315-329.
46. Roser P, Juckel G, Rentzsch J, Nadulski T, Gallinat J, Stadelmann AM (2008): Effects of acute oral Delta9-tetrahydrocannabinol and standardized cannabis extract on the auditory P300 event-related potential in healthy volunteers. Eur Neuropsychopharmacol 18: 569-577.
47. Naatanen R, Alho K (1995): Generators of electrical and magnetic mismatch responses in humans. Brain Topogr 7:315-320.
48. Rinne T, Alho K, Ilmoniemi RJ, Virtanen J, Naatanen R (2000): Separate time behaviors of the temporal and frontal mismatch negativity sources. Neuroimage 12:14-19.
49. Perez VB, Woods SW, Roach BJ, Ford JM, McGlashan TH, Srihari VH, et al. (2013): Automatic auditory processing deficits in schizophrenia and clinical high-risk patients: Forecasting psychosis risk with mismatch negativity. Biol Psychiatry 75:459-469.
50. Pesa N, Hermens DF, Battisti RA, Kaur M, Hickie IB, Solowij N (2012): Delayed preattentional functioning in early psychosis patients with cannabis use. Psychopharmacology (Berl) 222:507-518.
51. Juckel G, Roser P, Nadulski T, Stadelmann AM, Gallinat J (2007): Acute effects of Delta9-tetrahydrocannabinol and standardized cannabis extract on the auditory evoked mismatch negativity. Schizophr Res 97:109-117.
52. Rentzsch J, Penzhorn A, Kernbichler K, Plockl D, Gomez-Carrillo de Castro A, Gallinat J, et al. (2007): Differential impact of heavy cannabis use on sensory gating in schizophrenic patients and otherwise healthy controls. Exp Neurol 205:241-249.
53. de Wilde OM, Bour LJ, Dingemans PM, Koelman JH, Linszen DH (2007): A meta-analysis of P50 studies in patients with schizophrenia and relatives: Differences in methodology between research groups. Schizophr Res 97:137-151.
54. Patterson JV, Hetrick WP, Boutros NN, Jin Y, Sandman C, Stern H, et al. (2008): P50 sensory gating ratios in schizophrenics and controls: A review and data analysis. Psychiatry Res 158: 226-247.
55. Patrick G, Straumanis JJ, Struve FA, Fitz-Gerald MJ, Leavitt J, Manno JE (1999): Reduced P50 auditory gating response in psychiatrically normal chronic marihuana users: A pilot study. Biol Psychiatry 45:1307-1312.
56. Patrick G, Struve FA (2000): Reduction of auditory P50 gating response in marihuana users: Further supporting data. Clin Electroencephalogr 31:88-93.
57. Uhlhaas PJ, Roux F, Rodriguez E, Rotarska-Jagiela A, Singer W (2010): Neural synchrony and the development of cortical networks. Trends Cogn Sci 14:72-80.
58. Uhlhaas PJ, Singer W (2010): Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci 11:100-113.
59. Uhlhaas PJ, Haenschel C, Nikolić D, Singer W (2008): The role of oscillations and synchrony in cortical networks and their putative relevance for the pathophysiology of schizophrenia. Schizophr Bull 34:927-943.
60. Hajos N, Katona I, Naiem SS, Mackie K, Ledent C, Mody I, et al. (2000): Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur J Neurosci 12:3239-3249.
61. Hajos M, Hoffmann WE, Kocsis B (2008): Activation of cannabinoid- 1 receptors disrupts sensory gating and neuronal oscillation: Relevance to schizophrenia. Biol Psychiatry 63:1075-1083.
62. Sales-Carbonell C, Rueda-Orozco PE, Soria-Gomez E, Buzsaki G, Marsicano G, Robbe D (2013): Striatal GABAergic and cortical glutamatergic neurons mediate contrasting effects of cannabinoids on cortical network synchrony. Proc Natl Acad Sci U S A 110:719-724.
63. Cortes-Briones J, Skosnik PD, Mathalon D, Cahill J, Pittman B, Williams A, et al. (2015): Delta(9)-THC disrupts gamma (gamma)- band neural oscillations in humans. Neuropsychopharmacology 40: 2124-2134.
64. Morrison PD, Nottage J, Stone JM, Bhattacharyya S, Tunstall N, Brenneisen R, et al. (2011): Disruption of frontal theta coherence by Delta9-tetrahydrocannabinol is associated with positive psychotic symptoms. Neuropsychopharmacology 36:827-836.
65. Skosnik PD, Krishnan GP, Vohs JL, O'Donnell BF (2006): The effect of cannabis use and gender on the visual steady state evoked potential. Clin Neurophysiol 117:144-156.
66. Edwards CR, Skosnik PD, Steinmetz AB, O'Donnell BF, Hetrick WP (2009): Sensory gating impairments in heavy cannabis users are associated with altered neural oscillations. Behav Neurosci 123: 894-904.
67. Skosnik PD, D'Souza DC, Steinmetz AB, Edwards CR, Vollmer JM, Hetrick WP, et al. (2012): The effect of chronic cannabinoids on broadband EEG neural oscillations in humans. Neuropsychopharmacology 37:2184-2193.
68. Winterer G, Weinberger DR (2003): Cortical signal-to-noise ratio: Insight into the pathophysiology and genetics of schizophrenia. Clin Neurosci Res 3:55-66.
69. Winterer G, Coppola R, Goldberg TE, Egan MF, Jones DW, Sanchez CE, et al. (2004): Prefrontal broadband noise, working memory, and genetic risk for schizophrenia. Am J Psychiatry 161:490-500.
70. Yang GJ, Murray JD, Repovs G, Cole MW, Savic A, Glasser MF, et al. (2014): Altered global brain signal in schizophrenia. Proc Natl Acad Sci U S A 111:7438-7443.
71. Cortes-Briones JA, Cahill JD, Skosnik PD, Mathalon DH, Williams A, Sewell RA, et al. (2015): The psychosis-like effects of delta-tetrahydrocannabinol are associated with increased cortical noise in healthy humans. Biol Psychiatry 78:805-813.
72. van Os J, Bak M, Hanssen M, Bijl RV, de Graaf R, Verdoux H (2002): Cannabis use and psychosis: A longitudinal population-based study. Am J Epidemiol 156:319-327.
73. Henquet C, Krabbendam L, Spauwen J, Kaplan C, Lieb R, Wittchen HU, et al. (2005): Prospective cohort study of cannabis use, predisposition for psychosis, and psychotic symptoms in young people. BMJ 330:11.
74. Henquet C, Rosa A, Krabbendam L, Papiol S, Fananas L, Drukker M, et al. (2006): An experimental study of catechol-O-methyltransferase Val(158)Met moderation of delta-9-tetrahydrocannabinol-induced effects on psychosis and cognition. Neuropsychopharmacology 31: 2748-2757.
75. Papaleo F, Crawley JN, Song J, Lipska BK, Pickel J, Weinberger DR, et al. (2008): Genetic dissection of the role of catechol-O-methyltransferase in cognition and stress reactivity in mice. J Neurosci 28: 8709-8723.
76. Pelayo-Teran JM, Perez-Iglesias R, Mata I, Carrasco-Marin E, Vazquez-Barquero JL, Crespo-Facorro B (2010): Catechol-O-methyltransferase (COMT) Val158Met variations and cannabis use in firstepisode non-affective psychosis: clinical-onset implications. Psychiatry Res 179:291-296.
77. Caspi A, Moffitt TE, Cannon M, McClay J, Murray R, Harrington H, et al. (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 X environment interaction. Biol Psychiatry 57:1117-1127.
78. Kantrowitz JT, Nolan KA, Sen S, Simen AA, Lachman HM, Bowers MB Jr (2009): Adolescent cannabis use, psychosis and catechol-Omethyltransferase genotype in African Americans and Caucasians. Psychiatr Q 80:213-218.
79. Zammit S, Spurlock G, Williams H, Norton N, Williams N, O'Donovan MC, et al. (2007): Genotype effects of CHRNA7, CNR1 and COMT in schizophrenia: Interactions with tobacco and cannabis use. Br J Psychiatry 191:402-407.
80. Talkowski ME, Kirov G, Bamne M, Georgieva L, Torres G, Mansour H, et al. (2008): A network of dopaminergic gene variations implicated as risk factors for schizophrenia. Hum Mol Genet 17:747-758.
81. Bhattacharyya S, Atakan Z, Martin-Santos R, Crippa JA, Kambeitz J, Prata D, et al. (2012): Preliminary report of biological basis of sensitivity to the effects of cannabis on psychosis: AKT1 and DAT1 genotype modulates the effects of delta-9-tetrahydrocannabinol on midbrain and striatal function. Mol Psychiatry 17: 1152-1155.
82. Thiselton DL, Vladimirov VI, Kuo PH, McClay J, Wormley B, Fanous A, et al. (2008): AKT1 is associated with schizophrenia across multiple symptom dimensions in the Irish study of high density schizophrenia families. Biol Psychiatry 63:449-457.
83. Emamian ES, Hall D, Birnbaum MJ, Karayiorgou M, Gogos JA (2004): Convergent evidence for impaired AKT1-GSK3beta signaling in schizophrenia. Nat Genet 36:131-137.
84. 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. Arch Gen Psychiatry 68:148-157.
85. Di Forti M, Iyegbe C, Sallis H, Kolliakou A, Falcone MA, Paparelli A, et al. (2012): Confirmation that the AKT1 (rs2494732) genotype influences the risk of psychosis in cannabis users. Biol Psychiatry 72:811-816.
86. van Winkel R, van Beveren NJ, Simons C & Genetic Risk and Outcome of Psychosis (GROUP) Investigators. (2011): AKT1 moderation of cannabis-induced cognitive alterations in psychotic disorder. Neuropsychopharmacology 36:2529-2537.
87. Boucher AA, Arnold JC, Duffy L, Schofield PR, Micheau J, Karl T (2007): Heterozygous neuregulin 1 mice are more sensitive to the behavioural effects of Delta9-tetrahydrocannabinol. Psychopharmacology (Berl) 192:325-336.
88. Decoster J, van Os J, Kenis G, Henquet C, Peuskens J, De Hert M, et al. (2011): Age at onset of psychotic disorder: Cannabis, BDNF Val66Met, and sex-specific models of gene-environment interaction. Am J Med Genet B Neuropsychiatr Genet 156B:363-369.
89. Ho BC, Wassink TH, Ziebell S, Andreasen NC (2011): Cannabinoid receptor 1 gene polymorphisms and marijuana misuse interactions on white matter and cognitive deficits in schizophrenia. Schizophr Res 128:66-75.
90. Stokes PR, Mehta MA, Curran HV, Breen G, Grasby PM (2009): Can recreational doses of THC produce significant dopamine release in the human striatum? Neuroimage 48:186-190.
91. Barkus E, Morrison PD, Vuletic D, Dickson JC, Ell PJ, Pilowsky LS, et al. (2011): Does intravenous Delta9-tetrahydrocannabinol increase dopamine release? A SPET study. J Psychopharmacol 25:1462-1468.
92. Bossong MG, vanBerckel BN, Boellaard R, Zuurman L, Schuit RC, Windhorst AD, et al. (2009): Delta 9-tetrahydrocannabinol induces dopamine release in the human striatum. Neuropsychopharmacology 34:759-766.
93. Bossong MG, Mehta MA, van Berckel BN, Howes OD, Kahn RS, Stokes PR (2015): Further human evidence for striatal dopamine release induced by administration of 9-tetrahydrocannabinol (THC): Selectivity to limbic striatum. Psychopharmacology (Berl) 232: 2723-2729.
94. Kuepper R, Ceccarini J, Lataster J, van Os J, van Kroonenburgh M, van Gerven JM, et al. (2013): Delta-9-tetrahydrocannabinol-induced dopamine release as a function of psychosis risk: 18F-fallypride positron emission tomography study. PLoS One, 8, e70378.
95. Glass M, Felder CC (1997): Concurrent stimulation of cannabinoid CB1 and dopamine D2 receptors augments cAMP accumulation in striatal neurons: Evidence for a Gs linkage to the CB1 receptor. J Neurosci 17:5327-5333.
96. Munoz-Arenas G, Paz-Bermudez F, Baez-Cordero A, Caballero- Floran R, Gonzalez-Hernandez B, Floran B, et al. (2015): Cannabinoid CB1 receptors activation and coactivation with D2 receptors modulate GABAergic neurotransmission in the globus pallidus and increase motor asymmetry. Synapse 69:103-114.
97. Fitzgerald ML, Shobin E, Pickel VM (2012): Cannabinoid modulation of the dopaminergic circuitry: Implications for limbic and striatal output. Prog Neuropsychopharmacol Biol Psychiatry 38:21-29.
98. Prescot AP, Renshaw PF, Yurgelun-Todd DA (2013): Gamma-amino butyric acid and glutamate abnormalities in adolescent chronic marijuana smokers. Drug Alcohol Depend 129:232-239.
99. Kano M (2014): Control of synaptic function by endocannabinoidmediated retrograde signaling. Proc Jpn Acad Ser B Phys Biol Sci 90:235-250.
100. Li Q, Yan H, Wilson WA, Swartzwelder HS (2010): Modulation of NMDA and AMPA-mediated synaptic transmission by CB1 receptors in frontal cortical pyramidal cells. Brain Res 1342:127-137.
101. Hampson RE, Miller F, Palchik G, Deadwyler SA (2011): Cannabinoid receptor activation modifies NMDA receptor mediated release of intracellular calcium: Implications for endocannabinoid control of hippocampal neural plasticity. Neuropharmacology 60:944-952.
102. Gonzalez-Burgos G, Lewis DA (2012): NMDA receptor hypofunction, parvalbumin-positive neurons, and cortical gamma oscillations in schizophrenia. Schizophr Bull 38:950-957.
103. Sanchez-Blazquez P, Rodriguez-Munoz M, Vicente-Sanchez A, Garzon J (2013): Cannabinoid receptors couple to NMDA receptors to reduce the production of NO and the mobilization of zinc induced by glutamate. Antioxid Redox Signal 19:1766-1782.
104. Vicente-Sanchez A, Sanchez-Blazquez P, Rodriguez-Munoz M, Garzon J (2013): HINT1 protein cooperates with cannabinoid 1 receptor to negatively regulate glutamate NMDA receptor activity. Mol Brain 6:42.
105. Sanchez-Blazquez P, Rodriguez-Munoz M, Garzon J (2014): The cannabinoid receptor 1 associates with NMDA receptors to produce glutamatergic hypofunction: Implications in psychosis and schizophrenia. Front Pharmacol 4:169.
106. Radhakrishnan R, Skosnik PD, Cortes-Briones J, Sewell RA, Carbuto M, Schnakenberg A, et al. (2015): GABA deficits enhance the psychotomimetic effects of delta(9)-THC. Neuropsychopharmacology 40:2047-2056.
107. Eggan SM, Melchitzky DS, Sesack SR, Fish KN, Lewis DA (2010): Relationship of cannabinoid CB1 receptor and cholecystokinin immunoreactivity in monkey dorsolateral prefrontal cortex. Neuroscience 169:1651-1661.
108. Bartos M, Elgueta C (2012): Functional characteristics of parvalbumin- and cholecystokinin-expressing basket cells. J Physiol 590: 669-681.
109. Klausberger T, Marton LF, O'Neill J, Huck JH, Dalezios Y, Fuentealba P, et al. (2005): Complementary roles of cholecystokinin- and parvalbumin-expressing GABAergic neurons in hippocampal network oscillations. J Neurosci 25:9782-9793.
110. Farkas I, Kallo I, Deli L, Vida B, Hrabovszky E, Fekete C, et al. (2010): Retrograde endocannabinoid signaling reduces GABAergic synaptic transmission to gonadotropin-releasing hormone neurons. Endocrinology 151:5818-5829.
111. Curley AA, Lewis DA (2012): Cortical basket cell dysfunction in schizophrenia. J Physiol 590:715-724.
112. Lewis DA, Hashimoto T, Volk DW (2005): Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6:312-324.
113. Volk DW, Lewis DA (2015): The role of endocannabinoid signaling in cortical inhibitory neuron dysfunction in schizophrenia [published online ahead of print Jun 19]. Biol Psychiatry.
114. Wang XJ, Krystal JH (2014): Computational psychiatry. Neuron 84: 638-654.
115. Rall W, Shepherd GM (1968): Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in olfactory bulb. J Neurophysiol 31:884-915.
116. Lytton WW, Sejnowski TJ (1991): Simulations of cortical pyramidal neurons synchronized by inhibitory interneurons. J Neurophysiol 66: 1059-1079.
117. Gupta S, Ranganathan M, D'Souza DC (2016): The early identification of psychosis: Can lessons be learnt from cardiac stress testing? Psychopharmacology (Berl) 233:19-37.
118. Zuurman L, Roy C, Schoemaker RC, Hazekamp A, den Hartigh J, Bender JC, et al. (2008): Effect of intrapulmonary tetrahydrocannabinol administration in humans. J Psychopharmacol 22:707-716.
119. Bossong MG, Jansma JM, van Hell HH, Jager G, Oudman E, Saliasi E, et al. (2012): Effects of delta9-tetrahydrocannabinol on human working memory function. Biol Psychiatry 71:693-699.
120. Bossong MG, Jager G, van Hell HH, Zuurman L, Jansma JM, Mehta MA, et al. (2012): Effects of Delta9-tetrahydrocannabinol administration on human encoding and recall memory function: A pharmacological FMRI study. J Cogn Neurosci 24:588-599.
121. Klumpers LE, Cole DM, Khalili-Mahani N, Soeter RP, Te Beek ET, Rombouts SA, et al. (2012): Manipulating brain connectivity with delta(9)-tetrahydrocannabinol: A pharmacological resting state FMRI study. Neuroimage 63:1701-1711.
122. Klumpers LE, Fridberg M, de Kam ML, Little PB, Jensen NO, Kleinloog HD, et al. (2013): Peripheral selectivity of the novel cannabinoid receptor antagonist TM38837 in healthy subjects. Br J Clin Pharmacol 76:846-857.
123. Klumpers LE, Roy C, Ferron G, Turpault S, Poitiers F, Pinquier JL, et al. (2013): Surinabant, a selective cannabinoid receptor type 1 antagonist, inhibits Delta9-tetrahydrocannabinol-induced central nervous system and heart rate effects in humans. Br J Clin Pharmacol 76:65-77.
124. Bossong MG, Jansma JM, van Hell HH, Jager G, Kahn RS, Ramsey NF (2013): Default mode network in the effects of delta9-tetrahydrocannabinol (THC) on human executive function. PLoS One 8:e70074.
125. Bossong MG, van Hell HH, Jager G, Kahn RS, Ramsey NF, Jansma JM (2013): The endocannabinoid system and emotional processing: A pharmacological fMRI study with 9-tetrahydrocannabinol. Eur Neuropsychopharmacol 23:1687-1697.
126. Jansma JM, van Hell HH, Vanderschuren LJ, Bossong MG, Jager G, Kahn RS, et al. (2013): THC reduces the anticipatory nucleus accumbens response to reward in subjects with a nicotine addiction. Transl Psychiatry 3:e234.
127. Kleinloog D, Rombouts S, Zoethout R, Klumpers L, Niesters M, Khalili-Mahani N, et al. (2015): Subjective effects of ethanol, morphine, delta-tetrahydrocannabinol, and ketamine following a pharmacological challenge are related to functional brain connectivity. Brain Connect 5:641-648.
128. Borgwardt SJ, Allen P, Bhattacharyya S, Fusar-Poli P, Crippa JA, Seal ML, et al. (2008): Neural basis of delta-9-tetrahydrocannabinol and cannabidiol: Effects during response inhibition. Biol Psychiatry 64:966-973.
129. Fusar-Poli P, Allen P, Bhattacharyya S, Crippa JA, Mechelli A, Borgwardt S, et al. (2009): Modulation of effective connectivity during emotional processing by Delta 9-tetrahydrocannabinol and cannabidiol. Int J Neuropsychopharmacol 13:421-432.
130. Hallak JE, Machado-de-Sousa JP, Crippa JA, Sanches RF, Trzesniak C, Chaves C, et al. (2010): Performance of schizophrenic patients in the Stroop Color Word Test and electrodermal responsiveness after acute administration of cannabidiol (CBD). Rev Bras Psiquiatr 32: 56-61.
131. Winton-Brown TT, Allen P, Bhattacharyya S, Borgwardt SJ, Fusar-Poli P, Crippa JA, et al. (2011): Modulation of auditory and visual processing by delta-9-tetrahydrocannabinol and cannabidiol: An FMRI study. Neuropsychopharmacology 36:1340-1348.
132. Ranganathan M, Carbuto M, Braley G, Elander J, Perry E, Pittman B, et al. (2012): Naltrexone does not attenuate the effects of intravenous Delta9-tetrahydrocannabinol in healthy humans. Int J Neuropsychopharmacol 15:1251-1264.
133. Atakan Z, Bhattacharyya S, Allen P, Martin-Santos R, Crippa JA, Borgwardt SJ, et al. (2013): Cannabis affects people differently: Intersubject variation in the psychotogenic effects of Delta9-tetrahydrocannabinol: A functional magnetic resonance imaging study with healthy volunteers. Psychol Med 43:1255-1267.
134. Nottage JF, Stone J, Murray RM, Sumich A, Bramon-Bosch E, Ffytche D, et al. (2015): Delta-9-tetrahydrocannabinol, neural oscillations above 20 Hz and induced acute psychosis. Psychopharmacology (Berl) 232:519-528.
135. Kaufmann RM, Kraft B, Frey R, Winkler D, Weiszenbichler S, Backer C, et al. (2010): Acute psychotropic effects of oral cannabis extract with a defined content of Delta9-tetrahydrocannabinol (THC) in healthy volunteers. Pharmacopsychiatry 43:24-32.
136. Kopell BS, Tinklenberg JR, Hollister LE (1972): Contingent negative variation amplitudes. Marihuana and alcohol. Arch Gen Psychiatry 27:809-811.
137. Stadelmann AM, Juckel G, Arning L, Gallinat J, Epplen JT, Roser P (2011): Association between a cannabinoid receptor gene (CNR1) polymorphism and cannabinoid-induced alterations of the auditory event-related P300 potential. Neurosci Lett 496:60-64.
138. Bhattacharyya S, Falkenberg I, Martin-Santos R, Atakan Z, Crippa JA, Giampietro V, et al. (2015): Cannabinoid modulation of functional connectivity within regions processing attentional salience. Neuropsychopharmacology 40:1343-1352.