Impairment of inhibitory control processing related to acute psychotomimetic effects of cannabis

European Neuropsychopharmacology

Volumn 25, Issue 1, 2015, Pages 26-37

  Bhattacharyya, Sagnik ^a   Atakan, Z ^a   Martin Santos, R ^b   Crippa, J A ^c   Kambeitz, J ^a,d   Malhi, S ^a   Giampietro, V ^a   Williams, S ^a   Brammer, M ^a   Rubia, K ^a   Collier, D A ^a   McGuire, P K ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b HOSPITAL CLÍNIC   (Spain)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d UNIVERSITY OF MUNICH   (Germany)

Author keywords

Cannabis; Functional MRI; Inferior frontal gyrus; Psychotic symptoms; Response inhibition; THC

Indexed keywords

CANNABIS; DRONABINOL; ILLICIT DRUG; PSYCHEDELIC AGENT; OXYGEN;

ADDICTION SEVERITY INDEX; ANXIETY; AREA UNDER THE CURVE; ARTICLE; BRAIN REGION; CANNABIS USE; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CROSSOVER PROCEDURE; DISEASE SEVERITY; DOUBLE BLIND PROCEDURE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INHIBITION (PSYCHOLOGY); INTOXICATION; MALE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; POSITIVE AND NEGATIVE SYNDROME SCALE; SEDATION; THINKING IMPAIRMENT; BLOOD; BRAIN; CHEMICALLY INDUCED; CHI SQUARE DISTRIBUTION; DECISION MAKING; DRUG EFFECTS; FEMALE; IMAGE PROCESSING; LEARNING DISORDER; PSYCHOLOGICAL RATING SCALE; RANDOMIZED CONTROLLED TRIAL; STATISTICS; TIME; VASCULARIZATION; VISUAL ANALOG SCALE;

AREA UNDER CURVE; BRAIN; CHI-SQUARE DISTRIBUTION; CROSS-OVER STUDIES; DECISION MAKING; DOUBLE-BLIND METHOD; DRONABINOL; FEMALE; HALLUCINOGENS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INHIBITION (PSYCHOLOGY); LEARNING DISORDERS; MALE; OXYGEN; PSYCHIATRIC STATUS RATING SCALES; STATISTICS AS TOPIC; TIME FACTORS; VISUAL ANALOG SCALE;

EID: 84920599438     PISSN: 0924977X     EISSN: 18737862     Source Type: Journal    
DOI: 10.1016/j.euroneuro.2014.11.018     Document Type: Article

References (50)

1. Aichert D.S., Wostmann N.M., Costa A., Macare C., Wenig J.R., Moller H.J., Rubia K., Ettinger U. Associations between trait impulsivity and prepotent response inhibition. J. Clin. Exp. Neuropsychol. 2012, 34:1016-1032.
2. Aron A.R., Durston S., Eagle D.M., Logan G.D., Stinear C.M., Stuphorn V. Converging evidence for a fronto-basal-ganglia network for inhibitory control of action and cognition. J. Neurosci. 2007, 27:11860-11864.
3. Bhattacharyya S., Atakan Z., Martin-Santos R., Crippa J.A., Kambeitz J., Prata D., Williams S., Brammer M., Collier D.A., McGuire P.K. 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 2012, 17:1152-1155.
4. Bhattacharyya S., Atakan Z., Martin-Santos R., Crippa J.A., McGuire P.K. Neural mechanisms for the cannabinoid modulation of cognition and affect in man: a critical review of neuroimaging studies. Curr. Pharm. Des. 2012, 18:5045-5054.
5. Bhattacharyya S., Crippa J.A., Allen P., Martin-Santos R., Borgwardt S., Fusar-Poli P., Rubia K., Kambeitz J., O'Carroll C., Seal M.L., Giampietro V., Brammer M., Zuardi A.W., Atakan Z., McGuire P.K. Induction of psychosis by Delta9-tetrahydrocannabinol reflects modulation of prefrontal and striatal function during attentional salience processing. Arch. Gen. Psychiatry 2012, 69:27-36.
6. Bhattacharyya S., Falkenberg I., Martin-Santos R., Atakan Z., Crippa J.A., Giampietro V., Brammer M., McGuire P. Cannabinoid modulation of functional connectivity within regions processing attentional salience. Neuropsychopharmacology 2014.
7. Bhattacharyya S., Fusar-Poli P., Borgwardt S., Martin-Santos R., Nosarti C., O'Carroll C., Allen P., Seal M.L., Fletcher P.C., Crippa J.A., Giampietro V., Mechelli A., Atakan Z., McGuire P. 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 2009, 66:442-451.
8. Bhattacharyya S., Iyegbe C., Atakan Z., Martin-Santos R., Crippa J.A., Xu X., Williams S., Brammer M., Rubia K., Prata D., Collier D.A., McGuire P.K. Protein kinase B (AKT1) genotype mediates sensitivity to cannabis-induced impairments in psychomotor control. Psychol. Med. 2014, 44:3315-3328.
9. Bhattacharyya S., Morrison P.D., Fusar-Poli P., Martin-Santos R., Borgwardt S., Winton-Brown T., Nosarti C., CM O.C., Seal M., Allen P., Mehta M.A., Stone J.M., Tunstall N., Giampietro V., Kapur S., Murray R.M., Zuardi A.W., Crippa J.A., Atakan Z., McGuire P.K. Opposite effects of delta-9-tetrahydrocannabinol and cannabidiol on human brain function and psychopathology. Neuropsychopharmacology 2010, 35:764-774.
10. Borgwardt S.J., Allen P., Bhattacharyya S., Fusar-Poli P., Crippa J.A., Seal M.L., Fraccaro V., Atakan Z., Martin-Santos R., O'Carroll C., Rubia K., McGuire P.K. Neural basis of Delta-9-tetrahydrocannabinol and cannabidiol: effects during response inhibition. Biol. Psychiatry 2008, 64:966-973.
11. Brammer M.J., Bullmore E.T., Simmons A., Williams S.C., Grasby P.M., Howard R.J., Woodruff P.W., Rabe-Hesketh S. Generic brain activation mapping in functional magnetic resonance imaging: a nonparametric approach. Magn. Reson. Imaging 1997, 15:763-770.
12. Bullmore E., Long C., Suckling J., Fadili J., Calvert G., Zelaya F., Carpenter T.A., Brammer M. Colored noise and computational inference in neurophysiological (fMRI) time series analysis: resampling methods in time and wavelet domains. Hum. Brain Mapp. 2001, 12:61-78.
13. Bullmore E.T., Suckling J., Overmeyer S., Rabe-Hesketh S., Taylor E., Brammer M.J. Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE Trans. Med. Imaging 1999, 18:32-42.
14. Costa A., Riedel M., Pogarell O., Menzel-Zelnitschek F., Schwarz M., Reiser M., Moller H.J., Rubia K., Meindl T., Ettinger U. Methylphenidate effects on neural activity during response inhibition in healthy humans. Cereb. Cortex 2013, 23:1179-1189.
15. Coyle J.L., Fuller A., McKee V., Nelson J. Comparison of copper imine and amine podates: geometric consequences of podand size and donor type. Acta Crystallogr., Sect. C: Cryst. Struct. Commun. 2006, 62:m472-476.
16. Criaud M., Boulinguez P. Have we been asking the right questions when assessing response inhibition in Go/No-Go tasks with fMRI? A meta-analysis and critical review. Neurosci. Biobehav. Rev. 2013, 37:11-23.
17. Dale A.M. Optimal experimental design for event-related fMRI. Hum. Brain Mapp. 1999, 8:109-114.
18. Eldreth D.A., Matochik J.A., Cadet J.L., Bolla K.I. Abnormal brain activity in prefrontal brain regions in abstinent marijuana users. NeuroImage 2004, 23:914-920.
19. Elphick M.R., Egertova M. The neurobiology and evolution of cannabinoid signalling. Philos. Trans. R. Soc. London 2001, 356:381-408.
20. Friman O., Borga M., Lundberg P., Knutsson H. Adaptive analysis of fMRI data. NeuroImage 2003, 19:837-845.
21. Garavan H., Ross T.J., Stein E.A. Right hemispheric dominance of inhibitory control: an event-related functional MRI study. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:8301-8306.
22. Gruber S.A., Yurgelun-Todd D.A. Neuroimaging of marijuana smokers during inhibitory processing: a pilot investigation. Brain Res. Cogn. Brain Res. 2005, 23:107-118.
23. Harding I.H., Solowij N., Harrison B.J., Takagi M., Lorenzetti V., Lubman D.I., Seal M.L., Pantelis C., Yucel M. Functional connectivity in brain networks underlying cognitive control in chronic cannabis users. Neuropsychopharmacology 2012, 37:1923-1933.
24. Hayasaka S., Nichols T.E. Validating cluster size inference: random field and permutation methods. NeuroImage 2003, 20:2343-2356.
25. Hirose S., Chikazoe J., Watanabe T., Jimura K., Kunimatsu A., Abe O., Ohtomo K., Miyashita Y., Konishi S. Efficiency of Go/No-Go task performance implemented in the left hemisphere. J. Neurosci. 2012, 32:9059-9065.
26. Kay S.R., Opler L.A., Fiszbein A. Significance of positive and negative syndromes in chronic schizophrenia. Br. J. Psychiatry 1986, 149:439-448.
27. Kiehl K.A., Smith A.M., Hare R.D., Liddle P.F. An event-related potential investigation of response inhibition in schizophrenia and psychopathy. Biol. Psychiatry 2000, 48:210-221.
28. Martin-Santos R., Fagundo A.B., Crippa J.A., Atakan Z., Bhattacharyya S., Allen P., Fusar-Poli P., Borgwardt S., Seal M., Busatto G.F., McGuire P. Neuroimaging in cannabis use: a systematic review of the literature. Psychol. Med. 2010, 40:383-398.
29. Mathew R.J., Wilson W.H., Humphreys D.F., Lowe J.V., Wiethe K.E. Regional cerebral blood flow after marijuana smoking. J. Cereb. Blood Flow Metab. 1992, 12:750-758.
30. McDonald J., Schleifer L., Richards J.B., de Wit H. Effects of THC on behavioral measures of impulsivity in humans. Neuropsychopharmacology 2003, 28:1356-1365.
31. McLellan A.T., Luborsky L., Woody G.E., O'Brien C.P. An improved diagnostic evaluation instrument for substance abuse patients. The addiction severity index. J. Nerv. Ment. Dis. 1980, 168:26-33.
32. Menon V., Adleman N.E., White C.D., Glover G.H., Reiss A.L. Error-related brain activation during a Go/NoGo response inhibition task. Hum. Brain Mapp. 2001, 12:131-143.
33. Moore T.H., Zammit S., Lingford-Hughes A., Barnes T.R., Jones P.B., Burke M., Lewis G. Cannabis use and risk of psychotic or affective mental health outcomes: a systematic review. Lancet 2007, 370:319-328.
34. Nelson, H.E., 1982. National Adult Reading Test (NART): Test Manual. NFER-Nelson, Windsor, Berkshire.
35. Norris H. The action of sedatives on brain stem oculomotor systems in man. Neuropharmacology 1971, 10:181-191.
36. Ohlsson A., Lindgren J.E., Wahlen A., Agurell S., Hollister L.E., Gillespie H.K. Plasma delta-9 tetrahydrocannabinol concentrations and clinical effects after oral and intravenous administration and smoking. Clin. Pharmacol. Ther. 1980, 28:409-416.
37. Ramaekers J.G., Kauert G., Theunissen E.L., Toennes S.W., Moeller M.R. Neurocognitive performance during acute THC intoxication in heavy and occasional cannabis users. J. Psychopharmacol. 2009, 23:266-277.
38. Ramaekers J.G., Kauert G., van Ruitenbeek P., Theunissen E.L., Schneider E., Moeller M.R. High-potency marijuana impairs executive function and inhibitory motor control. Neuropsychopharmacology 2006, 31:2296-2303.
39. Roberts G.M., Garavan H. Evidence of increased activation underlying cognitive control in ecstasy and cannabis users. NeuroImage 2010, 52:429-435.
40. Rubia K., Russell T., Overmeyer S., Brammer M.J., Bullmore E.T., Sharma T., Simmons A., Williams S.C., Giampietro V., Andrew C.M., Taylor E. Mapping motor inhibition: conjunctive brain activations across different versions of Go/No-Go and stop tasks. NeuroImage 2001, 13:250-261.
41. Rubia K., Smith A.B., Brammer M.J., Toone B., Taylor E. Abnormal brain activation during inhibition and error detection in medication-naive adolescents with ADHD. Am. J. Psychiatry 2005, 162:1067-1075.
42. Shergill S.S., Brammer M.J., Williams S.C., Murray R.M., McGuire P.K. Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging. Arch. Gen. Psychiatry 2000, 57:1033-1038.
43. Simmonds D.J., Pekar J.J., Mostofsky S.H. Meta-analysis of Go/No-Go tasks demonstrating that fMRI activation associated with response inhibition is task-dependent. Neuropsychologia 2008, 46:224-232.
44. Spielberger C.D. Manual for the State/Trait Anxiety Inventory (form Y): (Self Evaluation Questionnaire) 1983, Consulting Psychologists Press, Palo Alto.
45. Stone J.M., Morrison P.D., Brugger S., Nottage J., Bhattacharyya S., Sumich A., Wilson D., Tunstall N., Feilding A., Brenneisen R., McGuire P., Murray R.M., Ffytche D.H. Communication breakdown: delta-9 tetrahydrocannabinol effects on pre-speech neural coherence. Mol. Psychiatry 2012, 17:568-569.
46. Swick D., Ashley V., Turken U. Are the neural correlates of stopping and not going identical? Quantitative meta-analysis of two response inhibition tasks. NeuroImage 2011, 56:1655-1665.
47. Talairach, J., Tournoux, P., 1988. [Co-planar Stereotaxic Atlas of the Human Brain.]. Thieme Medical New York.
48. Tapert S.F., Schweinsburg A.D., Drummond S.P., Paulus M.P., Brown S.A., Yang T.T., Frank L.R. Functional MRI of inhibitory processing in abstinent adolescent marijuana users. Psychopharmacology (Berl) 2007, 194:173-183.
49. UNODC, 2011. World Drug Report. United Nations Office on Drugs and Crime.
50. Weinstein A., Brickner O., Lerman H., Greemland M., Bloch M., Lester H., Chisin R., Mechoulam R., Bar-Hamburger R., Freedman N., Even-Sapir E. Brain imaging study of the acute effects of Delta9-tetrahydrocannabinol (THC) on attention and motor coordination in regular users of marijuana. Psychopharmacology (Berl) 2008, 196:119-131.