Effects of acute oral Δ9-tetrahydrocannabinol and standardized cannabis extract on the auditory P300 event-related potential in healthy volunteers

European Neuropsychopharmacology

Volumn 18, Issue 8, 2008, Pages 569-577

  Roser, Patrik ^a   Juckel, Georg ^a   Rentzsch, Johannes ^b   Nadulski, Thomas ^b   Gallinat, Jürgen ^b   Stadelmann, Andreas M ^b  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Attention; Cannabinoids; Event related potentials; P300; Schizophrenia

Indexed keywords

11 HYDROXYDRONABINOL; CANNABIDIOL; DRONABINOL; PLACEBO; TETRAHYDROCANNABINOLIC ACID;

ADULT; ARTICLE; ATTENTION; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CROSSOVER PROCEDURE; DOUBLE BLIND PROCEDURE; DRUG BLOOD LEVEL; EVOKED AUDITORY P300 RESPONSE; EVOKED AUDITORY RESPONSE; FEMALE; HUMAN; HUMAN EXPERIMENT; LATENT PERIOD; MALE; NEUROMODULATION; NORMAL HUMAN; PRIORITY JOURNAL; RESPONSE TIME; SCHIZOPHRENIA; TASK PERFORMANCE; WORKING MEMORY;

ACOUSTIC STIMULATION; ADMINISTRATION, ORAL; ADULT; CANNABIDIOL; CANNABIS; DOUBLE-BLIND METHOD; ELECTROENCEPHALOGRAPHY; EVENT-RELATED POTENTIALS, P300; EVOKED POTENTIALS, AUDITORY; FEMALE; HUMANS; MALE; MULTIVARIATE ANALYSIS; PROSPECTIVE STUDIES; PSYCHOPHYSICS; PSYCHOTROPIC DRUGS; REACTION TIME; TETRAHYDROCANNABINOL;

EID: 45849137820     PISSN: 0924977X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.euroneuro.2008.04.008     Document Type: Article

References (96)

1. Andreasson S., Allebeck P., Engstrom A., and Rydberg U. Cannabis and schizophrenia. A longitudinal study of Swedish conscripts. Lancet 2 (1987) 1483-1486
2. Arseneault L., Cannon M., Poulton R., Murray R., Caspi A., and Moffitt T.E. Cannabis use in adolescence and risk for adult psychosis: longitudinal prospective study. Brit. Med. J. 325 (2002) 1212-1213
3. Bisogno T., Hanus L., De Petrocelis L., Tehilibon S., Ponde D.E., Brandi I., Moriello A.S., Davies J.B., Mechoulam R., and Di Marzo V. Molecular targets for cannabidiol and its synthetic analogues: effect on vanilloid VR1 receptors and on the cellular uptake and enzymatic hydrolysis of anandamide. Br. J. Pharmacol. 134 (2001) 845-852
4. Blackwood D.H., Whalley L.J., Christie J.E., Blackburn I.M., St Chair D.M., and McInnes A. Changes in auditory P3 event-related potential in schizophrenia and depression. Br. J. Psychiatry 150 (1987) 154-160
5. Bolla K.I., Brown K., Eldreth D., Tate K., and Cadet J.L. Dose-related neurocognitive effects pf marijuana use. Neurology 59 (2002) 1337-1343
6. Bond A., and Lader M. The use of analogue scales in rating subjective feelings. Br. J. Med. Psychol. 47 (1974) 211-218
7. Bosi D.C., Hallak J.E.C., Dursun S.M., Deakin J.F.W., and Zuardi A.W. Effects of cannabidiol on (s)-ketamine-induced psychopathology in healthy volunteers. J. Psychopharmacol. 17 Suppl. (2003) A55
8. Braff D.L. Information processing and attention dysfunction in schizophrenia. Schizophr. Bull. 19 (1993) 233-259
9. Bramon E., Rabe-Hesketh S., Sham P.C., Murray R.M., and Frangou S. Meta-analysis of the P300 and P50 waveforms in schizophrenia. Schizophr. Res. 70 (2004) 315-329
10. Bramon E., McDonald C., Croft R.J., Landau S., Filbey F., Gruzelier J.H., Sham P.C., Frangou S., and Murray R.M. Is the P300 wave an endophenotype for schizophrenia? A meta-analysis and a family study. NeuroImage 27 (2005) 960-968
11. Breivogel C.S., Griffin G., Di Marzo V., and Martin B.R. Evidence for a new G protein-coupled cannabinoid receptor in mouse brain. Mol. Pharmacol. 60 (2001) 155-163
12. Dean B., Sundram S., Bradbury R., Scarr E., and Copolov D. Studies on [3H]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 103 (2001) 9-15
13. Devane W.A., Hanus L., Breuer A., Pertwee R.G., Stevenson L.A., Griffin G., Gibson D., Mandelbaum A., Etinger A., and Mechoulam R. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258 (1992) 1946-1949
14. Duncan C.C. Event-related brain potentials: a window on information processing in schizophrenia. Schizophr. Bull. 14 (1988) 199-203
15. Ehrenreich H., Rinn T., Kunert H.J., Moeller M.R., Poser W., Schilling L., Gigerenzer G., and Hoehe M.R. Specific attentional dysfunction in adults following early start of cannabis use. Psychopharmacology 142 (1999) 295-301
16. Emrich H.M., Leweke F.M., and Schneider U. Towards a cannabinoid hypothesis of schizophrenia: cognitive impairments due to dysregulation of the endogenous cannabinoid system. Pharmacol. Biochem. Behav. 56 (1997) 803-807
17. Ferraro L., Tomasini M.C., Gessa G.L., Bebe B.W., Tanganelli S., and Antonelli T. The cannabinoid receptor agonist WIN 55,212-2 regulates glutamate transmission in rat cerebral cortex: an in vivo and in vitro study. Cereb. Cortex 11 (2001) 728-733
18. Ford J.M. Schizophrenia: the broken P300 and beyond. Psychophysiology 36 (1999) 667-682
19. Ford J.M., White P.M., Csernansky J.G., Faustman W.O., Roth W.T., and Pfefferbaum A. ERPs in schizophrenia: effects of antipsychotic medication. Biol. Psychiatry 36 (1994) 153-170
20. Frodl-Bauch T., Bottlender R., and Hegerl U. Neurochemical substrates and neuroanatomical generators of the event-related P300. Neuropsychobiology 40 (1999) 86-94
21. Gallinat J., Riedel M., Juckel G., Sokullu S., Frodl T., Moukhtieva R., Mavrogiorgou P., Nissle S., Müller N., Danker-Hopfe H., and Hegerl U. P300 and symptom improvement in schizophrenia. Psychopharmacology 158 (2001) 55-65
22. Gallinat J., Mulert C., Bajbouj M., Herrmann W.M., Schunter J., Senkowski D., Moukhtieva R., Kronfeldt D., and Winterer G. Frontal and temporal dysfunction of auditory stimulus processing in schizophrenia. NeuroImage 17 (2002) 110-127
23. Gangadhar B.N., Ancy J., Janakiramaiah N., and Umapathy C. P300 amplitude in non-bipolar, melancholic depression. J. Affect. Disord. 28 (1993) 57-60
24. Grotenhermen F. Pharmacokinetics and pharmacodynamics of cannabinoids. Clin. Pharmacokinet. 42 (2003) 327-360
25. Grotenhermen F. Cannabinoids. Curr. Drug. Targets. C.N.S. Neurol. Disord. 4 (2005) 507-530
26. Halgren E., Squires N.K., Wilson C.L., Rohrbaugh J.W., Babb T.L., and Crandall P.H. Endogenous potentials generated in the human hippocampal formation and amygdala by infrequent events. Science 210 (1980) 803-805
27. Hajos N., Ledent C., and Freund T.F. Novel cannabinoid-sensitive receptor mediates inhibition of glutamatergic synaptic transmission in the hippocampus. Neuroscience 106 (2001) 1-4
28. Herkenham M., Lynn A.B., Little M.D., Johnson M.R., Melvin L.S., de Costa B.R., and Rice K.C. Cannabinoid receptor localization in brain. Proc. Natl. Acad. Sci. U.S.A. 87 (1990) 1932-1936
29. Hesselbrock V., Begleiter H., Porjesz B., O'Connor S., and Bauer L. P300 event-related potential amplitude as an endophenotype of alcoholism - evidence from the collaborative study on the genetics of alcoholism. J. Biomed. Sci. 8 (2001) 77-82
30. Ilan A.B., Gevins A., Coleman M., ElSohly M.A., and de Wit H. Neurophysiological and subjective profile of marijuana with varying concentrations of cannabinoids. Behav. Pharmacol. 16 (2005) 487-496
31. Iversen L. Cannabis and the brain. Brain 126 (2003) 1252-1270
32. Jager G., Van Hell H.H., De Win M.M., Kahn R.S., Van Den Brink W., Van Ree J.M., and Ramsey N.F. Effects of frequent cannabis use on hippocampal activity during an associative memory task. Eur. Neuropsychopharmacol. 17 (2007) 289-297
33. Jeon Y.W., and Polich J. P300 asymmetry in schizophrenia: a meta-analysis. Psychiatry Res. 104 (2001) 61-74
34. Jeon Y.W., and Polich J. Meta-analysis of P300 and schizophrenia: paradigms, and practical implications. Psychophysiology 40 (2003) 684-701
35. Johns A. Psychiatric effects of cannabis. Br. J. Psychiatry 178 (2001) 116-122
36. Johnson J.P., Muhleman D., MacMurray J., Gade R., Verde R., Ask M., Kelley J., and Comings D.E. Association between the cannabinoid receptor gene (CNR1) and the P300 event-related potential. Mol. Psychiatry 2 (1997) 169-171
37. Juckel G., Müller-Schubert A., Gaebel W., and Hegerl U. Residual symptoms and P300 in schizophrenic outpatients. Psychiatry Res. 65 (1996) 23-32
38. Juckel G., Roser P., Nadulski T., Stadelmann A.M., and Gallinat J. Acute effects of delta-9-tetrahydrocannabinol and standardized cannabis extract on the auditory evoked mismatch negativity. Schizophr. Res. 97 (2007) 109-117
39. Kempel P., Lampe K., Parnefjord R., Hennig J., and Kunert H.J. Auditory-evoked potentials and selective attention: different ways of information processing in cannabis users and controls. Neuropsychobiology 48 (2003) 95-101
40. Kiehl K.A., Laurens K.R., Duty T.L., Forster B.B., and Liddle P.F. Neural sources involved in auditory target detection and novelty processing: an event-related fMRI study. Psychophysiology 38 (2001) 133-142
41. Leweke F.M., Giuffrida A., Wurster U., Emrich H.M., and Piomelli D. Elevated endogenous cannabinoids in schizophrenia. Neuroreport 10 (1999) 1665-1669
42. Leweke F.M., Schneider U., Radwan M., Schmidt E., and Emrich H.M. Different effects of nabilone and cannabidiol on binocular depth inversion in man. Pharmacol. Biochem. Behav. 66 (2000) 175-181
43. Leweke F.M., Gerth C.W., and Klosterkötter J. Cannabis-associated psychosis: current status of research. C.N.S. Drugs 18 (2004) 895-910
44. Leweke F.M., Koethe D., Gerth C.W., Nolden B.M., Mauss C., Schreiber D., Hänsel A., Neatby M.A., Juelicher A., and Klosterkötter J. Cannabidiol as an antipsychotic: a double-blind, controlled clinical trial on cannabidiol vs amisulpride in acute schizophrenia (2005), 2005 Symposium on the Cannabinoids, Burlington, Vermont
45. Long L.E., Malone D.T., and Taylor D.A. Cannabidiol reverses MK-801-induced disruption of prepulse inhibition in mice. Neuropsychopharmacology 31 (2006) 795-803
46. Lundqvist T. Cognitive consequences of cannabis use: comparison with abuse of stimulants and heroin with regard to attention, memory and executive functions. Pharmacol. Biochem. Behav. 81 (2005) 319-330
47. Martinez-Arevalo M.J., Calcedo-Ordonez A., and Varo-Prieto J.R. Cannabis consumption as a prognostic factor in schizophrenia. Br. J. Psychiatry 164 (1994) 679-681
48. Matsuda L.A., Lolait S.J., Brownstein M.J., Young A.C., and Bonner T.I. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346 (1990) 561-564
49. McCarley R.W., Shenton M.E., O'Donnell B.F., Faux S.F., Kikinis R., Nestor P.G., and Jolesz F.A. Auditory P300 abnormalities and left posterior superior temporal gyrus volume reduction in schizophrenia. Arch. Gen. Psychiatry 50 (1993) 190-197
50. Mechoulam R., and Gaoni Y. A total synthesis of delta-1-tetrahydrocannabinol, the active constituent of hashish. J. Am. Chem. Soc. 87 (1965) 3273-3275
51. Mechoulam R., Parker L.A., and Gallily R. Cannabidiol: an overview of some pharmacological aspects. J. Clin. Pharmacol. 42 (2002) 11S-19S
52. Miller P., Lawrie S.M., Hodges A., Clafferty R., Cosway R., and Johnstone E.C. Genetic liability, illicit drug use, life stress and psychotic symptoms: preliminary findings from the Edinburgh study of people at high risk for schizophrenia. Soc. Psychiatry Psychiatr. Epidemiol. 36 (2001) 338-342
53. Monory K., Tzavara E.T., Lexime J., Ledent C., Parmentier M., Borsodi A., and Hanoune J. Novel, not adenylyl cyclase coupled cannabinoid binding site in cerebellum of mice. Biochem. Biophys. Res. Commun. 292 (2002) 231-235
54. Moreira F.A., and Guimaraes F.S. Cannabidiol inhibits the hyperlocomotion induced by psychotomimetics drugs in mice. Eur. J. Pharmacol. 512 (2005) 199-205
55. Mulert C., Pogarell O., Juckel G., Rujescu D., Giegling I., Rupp D., Mavrogiorgou P., Bussfeld P., Gallinat J., Möller H.J., and Hegerl U. The neural basis of the P300 potential. Focus on the time-course of the underlying cortical generators. Eur. Arch. Psychiatry Clin. Neurosci. 254 (2004) 190-198
56. Munro S., Thomas K.L., and Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature 365 (1993) 61-65
57. Nadulski T., Sporkert F., Schnelle M., Stadelmann A.M., Roser P., Schefter T., and Pragst F. Simultaneous and sensitive analysis of THC, 11-OH-THC, THC-COOH, CBD and CBN by GC-MS in plasma after oral application of small doses of THC and cannabis extract. J. Anal. Toxicol. 29 (2005) 782-789
58. 9-tetrahydrocannabinol (THC) after oral application of THC verses standardized cannabis extract. Ther. Drug Monit. 27 (2005) 799-810
59. Noland J.S., Singer L.T., Short E.J., Minnes S., Arendt R.E., Kirchner H.L., and Bearer C. Prenatal drug exposure and selective attention in preschoolers. Neurotoxicol. Teratol. 27 (2005) 429-438
60. O'Donnell B.F., Faux S.F., McCarley R.W., Kimble M.O., Salisbury D.F., Nestor P.G., Kikinis R., Jolesz F.A., and Shenton M.E. Increased rate of P300 latency prolongation with age in schizophrenia. Electrophysiological evidence for a neurodegenerative process. Arch. Gen. Psychiatry 52 (1995) 544-549
61. O'Donnell B.F., Vohs J.L., Hetrick W.P., Carroll C.A., and Shekhar A. Auditory event-related potential abnormalities in bipolar disorder and schizophrenia. Int. J. Psychophysiol. 53 (2004) 45-55
62. Papageorgiou C., Oulis P., Vasios C., Kontopantelis E., Uzunoglu N., Rabavilas A., and Christodoulou G.N. P300 alterations in schizophrenic patients experiencing auditory hallucinations. Eur. Neuropsychopharmacol. 14 (2004) 227-236
63. Patrick G., Straumanis J.J., Struve F.A., Nixon F., Fitz-Gerald M.J., Manno J.E., and Soucair M. Auditory and visual P300 event related potentials are not altered in medically and psychiatrically normal chronic marihuana users. Life Sci. 56 (1995) 2135-2140
64. Pertwee R. The diverse CB1 and CB2 receptor pharmacology of three plant cannabinoids: delta9-tetrahydrocannabinol. cannabidiol and delta9-tetrahydrocannabivarin. Br. J. Pharmacol. 153 (2008) 199-215
65. Petitet F., Jeantaud B., Reibaud M., Imperato A., and Dubroeucq M.C. Complex pharmacology of natural cannabinoids: evidence for partial agonist activity of delta9-tetrahydrocannabinol and antagonist activity of cannabidiol on rat brain cannabinoid receptors. Life Sci. 63 (1998) PL1-PL6
66. Picton T.W. The P300 wave of the human event-related potential. J. Clin. Neurophysiol. 9 (1992) 456-479
67. Pistis M., Ferraro L., Pira L., Flore G., Tanganelli S., Gessa G.L., and Devoto P. Delta(9)-tetrahydrocannabinol decreases extracellular GABA and increases extracellular glutamate and dopamine levels in the rat prefrontal cortex: an in vivo microdialysis study. Brain Res. 948 (2002) 155-158
68. Polich J. P300 in clinical applications: meaning, method, and measurement. Am. J. E.E.G. Tech. 31 (1991) 201-231
69. Polich J., Ladish C., and Bloom F.E. P300 assessment of early Alzheimer's disease. Electroencephalogr. Clin. Neurophysiol. 77 (1990) 179-189
70. Ranganathan M., and D'Souza D.C. The acute effects of cannabinoids on memory in humans: a review. Psychopharmacology 188 (2006) 425-444
71. Rehm J., Room R., Van Den Brink W., and Kraus L. Problematic drug use and drug use disorders in EU countries and Norway: an overview of the epidemiology. Eur. Neuropsychopharmacol. 15 (2005) 389-397
72. Rodriguez de Fonseca F., Del Arco I., Martin-Calderon J.L., Gorriti M.A., and Navarro M. Role of the endogenous cannabinoid system in the regulation of motor activity. Neurobiol. Dis. 5 (1998) 483-501
73. Roser, P., Vollenweider, F.X., Kawohl, W., (in press). Potential antipsychotic properties of central cannabinoid (CB1) receptor antagonists. World J. Biol. Psychiatry. DOI: 10.1080/15622970801908047.
74. Roth W.T., and Cannon F.H. Some features of the auditory event-related response in schizophrenia. Arch. Gen. Psychiatry 27 (1972) 466-471
75. Russo E.B., Burnett A., Hall B., and Parker B.B. Agonistic properties of cannabidiol at 5-HT1a receptors. Neurochem. Res. 30 (2005) 1037-1043
76. Ryberg E., Larsson N., Sjögren S., Hjorth S., Hermansson N.O., Leonova J., Elebring T., Nilsson K., Drmota T., and Greasley P.J. The orphan receptor GPR55 is a novel cannabinoid receptor. Br. J. Pharmacol. 152 (2007) 1092-1101
77. Schwartz R.H. Marijuana: an overview. Pediatr. Clin. North. Am. 34 (1987) 305-317
78. Shen M., and Thayer S.A. Delta9-tetrahydrocannabinol acts as a partial agonist to modulate glutamatergic synaptic transmission between rat hippocampal neurons in culture. Mol. Pharmacol. 55 (1999) 8-13
79. Shen M., Piser T.M., Seybold V.S., and Thayer S.A. Cannabinoid receptor agonists inhibit glutamatergic synaptic transmission in rat hippocampal cultures. J. Neurosci. 16 (1996) 4322-4334
80. Smith M.E., Halgren E., Sokolik M., Baudena P., Musolino A., Liegeois-Chauvel C., and Chauvel P. The intracranial topography of the P3 event-related potential elicited during auditory oddball. Electroencephalogr. Clin. Neurophysiol. 76 (1990) 235-248
81. Solowij N. Cannabis and cognitive functioning (1998), Cambridge University Press, Cambridge
82. Solowij N., Michie P.T., and Fox A.M. Effects of long-term cannabis use on selective attention: an event-related potential study. Pharmacol. Biochem. Behav. 40 (1991) 683-688
83. Solowij N., Michie P.T., and Fox A.M. Differential impairments of selective attention due to frequency and duration of cannabis use. Biol. Psychiatry 37 (1995) 731-739
84. Solowij N., Stephens R.S., Roffman R.A., Babor T., Kadden R., Miller M., Christiansen K., McRee B., and Vendetti J. Cognitive functioning of long-term heavy cannabis users seeking treatment. J.A.M.A. 287 (2002) 1123-1131
85. Stapleton J.M., and Halgren E. Endogenous potentials evoked in simple cognitive tasks: depth components and task correlates. Electroencephalogr. Clin. Neurophysiol. 67 (1987) 44-52
86. Thierry A.M., Tassin J.P., Blanc G., and Glowinski J. Studies on mesocortical dopamine systems. Adv. Biochem. Psychopharmacol. 19 (1978) 205-216
87. Tomasini M.C., Ferraro L., Bebe B.W., Tanganelli S., Cassano T., Cuomo V., and Antonelli T. Delta(9)-tetrahydrocannabinol increases endogenous extracellular glutamate levels in primary cultures of rat cerebral cortex neurons: involvement of CB(1) receptors. J. Neurosci. Res. 68 (2002) 449-453
88. Treffert D.A. Marijuana use in schizophrenia: a clear hazard. Am. J. Psychiatry 135 (1978) 1213-1215
89. Turner W.M., and Tsuang M.T. Impact of substance abuse on the course and outcome of schizophrenia. Schizophr. Bull. 16 (1990) 87-95
90. Umbricht D., Bates J.A., Lieberman J.A., Kane J.M., and Javitt D.C. Electrophysiological indices of automatic and controlled auditory information processing in first-episode, recent-onset and chronic schizophrenia. Biol. Psychiatry 59 (2006) 762-772
91. Van der Stelt O., Lieberman J.A., and Belger A. Auditory P300 in high-risk, recent-onset and chronic schizophrenia. Schizophr. Res. 77 (2005) 309-320
92. Van Os J., Bak M., Hanssen M., Bijl R.V., De Graaf R., and Verdoux H. Cannabis use and psychosis: a longitudinal population-based study. Am. J. Epidemiol. 156 (2002) 19-27
93. Winterer G., Mulert C., Mientus S., Gallinat J., Schlattmann P., Dorn H., and Herrmann W.M. P300 and LORETA: comparison of normal subjects and schizophrenic patients. Brain Topogr. 13 (2001) 299-313
94. Yingling C., and Hosobuchi Y. A subcortical correlate of P300 in man. Electroencephalogr. Clin. Neurophysiol. 59 (1984) 72-76
95. Zavitsanou K., Garrick T., and Huang X.F. Selective antagonist [3H] SR141716A binding to cannabinoid CB1 receptors is increased in the anterior cingulate cortex in schizophrenia. Prog. Neuropsychopharmacol. Biol. Psychiatry 28 (2004) 355-360
96. Zuardi A.W., Crippa J.A.S., Hallak J.E.C., Moreira F.A., and Guimaraes F.S. Cannabidiol, a Cannabis sativa constituent, as an antipsychotic drug. Braz. J. Med. Biol. Res. 39 (2006) 421-429