THC reduces the anticipatory nucleus accumbens response to reward in subjects with a nicotine addiction

Translational Psychiatry

Volumn 3, Issue , 2013, Pages

  Jansma, J M ^a   Van Hell, H H ^a   Vanderschuren, L J M J ^a,b   Bossong, M G ^a,c   Jager, G ^a,d   Kahn, R S ^a   Ramsey, N F ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Endocannabinoid system; Functional MRI; Nicotine addiction; Nucleus accumbens; Reward; THC

Indexed keywords

ENDOCANNABINOID; PLACEBO; TETRAHYDROCANNABINOL;

ADULT; ARTICLE; CAUDATE NUCLEUS; CLINICAL ARTICLE; CONTROLLED STUDY; FEEDBACK SYSTEM; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEUS ACCUMBENS; RANDOMIZED CONTROLLED TRIAL; REWARD; TASK PERFORMANCE; TOBACCO DEPENDENCE; ADOLESCENT; CONTROLLED CLINICAL TRIAL; CROSSOVER PROCEDURE; DOUBLE BLIND PROCEDURE; DRUG EFFECT; IMAGE PROCESSING; METHODOLOGY; MOTIVATION; PATHOPHYSIOLOGY; REACTION TIME;

ADOLESCENT; ADULT; CROSS-OVER STUDIES; DOUBLE-BLIND METHOD; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MOTIVATION; NUCLEUS ACCUMBENS; REACTION TIME; REWARD; TETRAHYDROCANNABINOL; TOBACCO USE DISORDER; YOUNG ADULT;

MLCS; MLOWN;

EID: 84875152812     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2013.6     Document Type: Article

References (58)

1. EMCDDA. The state of the drugs problem in Europe 2010.
2. Maldonado R, Valverde O, Berrendero F. Involvement of the endocannabinoid system in drug addiction. Trends Neurosci 2006; 29: 225-232.
3. Castane A, Berrendero F, Maldonado R. The role of the cannabinoid system in nicotine addiction. Pharmacol Biochem Behav 2005; 81: 381-386. (Pubitemid 40807135)
4. Le Foll B, Forget B, Aubin HJ, Goldberg SR. Blocking cannabinoid CB1 receptors for the treatment of nicotine dependence: insights from pre-clinical and clinical studies. Addict Biol 2008; 13: 239-252. (Pubitemid 351692986)
5. Valjent E, Mitchell JM, Besson M-J, Caboche J, Maldonado R. Behavioural and biochemical evidence for interactions between Delta 9-tetrahydrocannabinol and nicotine. Br J Pharmacol 2002; 135: 564-578. (Pubitemid 34151189)
6. Scherma M, Fadda P, Le Foll B, Forget B, Fratta W, Goldberg SR et al. The endocannabinoid system: a new molecular target for the treatment of tobacco addiction. CNS Neurol Disord Drug Targets 2008; 7: 468-481.
7. Lopez-Moreno JA, Echeverry-Alzate V, Buhler KM. The genetic basis of the endocannabinoid system and drug addiction in humans. J Psychopharmacol 2012; 26: 133-143.
8. Cohen C, Perrault G, Voltz C, Steinberg R, Soubrie P. SR141716, a central cannabinoid (CB(1)) receptor antagonist, blocks the motivational and dopamine-releasing effects of nicotine in rats. Behav Pharmacol 2002; 13: 451-463. (Pubitemid 35178842)
9. De Vries TJ, Schoffelmeer AN. Cannabinoid CB1 receptors control conditioned drug seeking. Trends Pharmacol Sci 2005; 26: 420-426. (Pubitemid 41039218)
10. Cippitelli A, Astarita G, Duranti A, Caprioli G, Ubaldi M, Stopponi S et al. Endocannabinoid regulation of acute and protracted nicotine withdrawal: effect of FAAH inhibition. PloS ONE 2011; 6: e28142.
11. Cahill K, Ussher M. Cannabinoid type 1 receptor antagonists (rimonabant) for smoking cessation. Cochrane Database Syst Rev 2007; 17: CD005353.
12. van der Stelt M, Di Marzo V. The endocannabinoid system in the basal ganglia and in the mesolimbic reward system: implications for neurological and psychiatric disorders. Eur J Pharmacol 2003; 480: 133-150. (Pubitemid 37410366)
13. Solinas M, Goldberg SR, Piomelli D. The endocannabinoid system in brain reward processes. Br J Pharmacol 2008; 154: 369-383. (Pubitemid 351670594)
14. Haber SN, Knutson B. The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 2010; 35: 4-26.
15. van Hell HH, Vink M, Ossewaarde L, Jager G, Kahn RS, Ramsey NF. Chronic effects of cannabis use on the human reward system: an fMRI study. Eur Neuropsychopharmacol 2010; 20: 153-163.
16. van Hell HH, Jager G, Bossong MG, Brouwer A, Jansma JM, Zuurman L et al. Involvement of the endocannabinoid system in reward processing in the human brain. Psychopharmacology (Berl) 2012; 219: 981-990.
17. Horder J, Harmer CJ, Cowen PJ, McCabe C. Reduced neural response to reward following 7 days treatment with the cannabinoid CB1 antagonist rimonabant in healthy volunteers. Int J Neuropsychopharmacol 2010; 13: 1103-1113.
18. Curtis VA, Bullmore ET, Brammer MJ, Wright IC, Williams SC, Morris RG et al. Attenuated frontal activation during a verbal fluency task in patients with schizophrenia. Am J Psychiatry 1998; 155: 1056-1063. (Pubitemid 28357731)
19. Williams CM, Kirkham TC. Observational analysis of feeding induced by Delta9-THC and anandamide. Physiol Behav 2002; 76: 241-250. (Pubitemid 34607232)
20. Martin-Soelch C, Leenders KL, Chevalley AF, Missimer J, Kunig G, Magyar S et al. Reward mechanisms in the brain and their role in dependence: evidence from neurophysiological and neuroimaging studies. Brain Res Brain Res Rev 2001; 36: 139-149. (Pubitemid 33020743)
21. Hommer DW, Bjork JM, Gilman JM. Imaging brain response to reward in addictive disorders. Ann N Y Acad Sci 2011; 1216: 50-61.
22. Rose EJ, Ross TJ, Salmeron BJ, Lee M, Shakleya DM, Huestis M et al. Chronic exposure to nicotine is associated with reduced reward-related activity in the striatum but not the midbrain. Biol Psychiatry 2012; 71: 206-213.
23. Bu hler M, Vollsta dt-Klein S, Kobiella A, Budde H, Reed LJ, Braus DF et al. Nicotine dependence is characterized by disordered reward processing in a network driving motivation. Biol Psychiatry 2010; 67: 745-752.
24. Knutson B, Adams CM, Fong GW, Hommer D. Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neurosci 2001; 21: RC159.
25. Everitt BJ, Robbins TW. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 2005; 8: 1481-1489. (Pubitemid 41573659)
26. Kalivas PW, O'Brien C. Drug addiction as a pathology of staged neuroplasticity. Neuropsychopharmacology 2008; 33: 166-180. (Pubitemid 350191316)
27. Koob GF, Volkow ND. Neurocircuitry of addiction. Neuropsychopharmacology 2010; 35: 217-238.
28. Berridge KC, Kringelbach ML. Affective neuroscience of pleasure: reward in humans and animals. Psychopharmacology (Berl) 2008; 199: 457-480.
29. van Hell HH, Bossong MG, Jager G, Kahn RS, Ramsey NF. Methods of the pharmacological imaging of the cannabinoid system (PhICS) study: towards understanding the role of the brain endocannabinoid system in human cognition. Int J Methods Psychiatr Res 2011; 20: 10-27.
30. van Vliet IM, Leroy H, Van Megen HGJM. M.I.N.I. Internationaal Neuropsychiatrisch Interview. Nederlandse Versie 5.0.0 2000.
31. Heatherton TF, Kozlowski LT, Frecker RC, Fagerstrom KO. The Fagerstrom Test for Nicotine Dependence: a revision of the Fagerstrom Tolerance Questionnaire. Br J Addict 1991; 86: 1119-1127.
32. Bond A, Lader M. The use of analogue scales in rating subjective feelings. Br J Med Psychol 1974; 47: 7.
33. Bowdle TA, Radant AD, Cowley DS, Kharasch ED, Strassman RJ, Roy-Byrne PP. Psychedelic effects of ketamine in healthy volunteers: relationship to steady-state plasma concentrations. Anesthesiology 1998; 88: 6.
34. Zuurman L, Roy C, Schoemaker RC, Hazekamp A, den Hartigh J, Bender JC et al. Effect of intrapulmonary tetrahydrocannabinol administration in humans. J Psychopharmacol 2008; 22: 707-716.
35. Neggers SF, Hermans EJ, Ramsey NF. Enhanced sensitivity with fast three-dimensional blood-oxygen-level-dependent functional MRI: comparison of SENSE-PRESTO and 2D-EPI at 3T. NMR Biomed 2008; 21: 663-676.
36. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002; 15: 273-289. (Pubitemid 34852226)
37. Merritt LL, Martin BR, Walters C, Lichtman AH, Damaj MI. The endogenous cannabinoid system modulates nicotine reward and dependence. J Pharmacol Exp Ther 2008; 326: 483-492.
38. Fehr C, Yakushev I, Hohmann N, Buchholz HG, Landvogt C, Deckers H et al. Association of low striatal dopamine d2 receptor availability with nicotine dependence similar to that seen with other drugs of abuse. AM J Psychiatry 2008; 165: 507-514. (Pubitemid 351694294)
39. Di Marzo V, Fontana A, Cadas H, Schinelli S, Cimino G, Schwartz JC et al. Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Nature 1994; 372: 686-691.
40. Melis M, Pistis M, Perra S, Muntoni AL, Pillolla G, Gessa GL. Endocannabinoids mediate presynaptic inhibition of glutamatergic transmission in rat ventral tegmental area dopamine neurons through activation of CB1 receptors. J Neurosci 2004; 24: 53-62. (Pubitemid 38181669)
41. Orio L, Crespo I, Lopez-Moreno JA, Reyes-Cabello C, Rodriguez de FonsecaF, Gomez de HerasR. Additive effects of cannabinoid CB1 receptors blockade and cholecystokinin on feeding inhibition. Pharmacol Biochem Behav 2011; 98: 220-226.
42. Castane A, Valjent E, Ledent C, Parmentier M, Maldonado R, Valverde O. Lack of CB1 cannabinoid receptors modifies nicotine behavioural responses, but not nicotine abstinence. Neuropharmacology 2002; 43: 857-867. (Pubitemid 35221396)
43. Scherma M, Panlilio LV, Fadda P, Fattore L, Gamaleddin I, Le Foll B et al. Inhibition of anandamide hydrolysis by cyclohexyl carbamic acid 3'-carbamoyl-3-yl ester (URB597) reverses abuse-related behavioral and neurochemical effects of nicotine in rats. J Pharmacol Exp Ther 2008; 327: 482-490.
44. Fales CL, Barch DM, Rundle MM, Mintun Ma, Snyder AZ, Cohen JD et al. Altered emotional interference processing in affective and cognitive-control brain circuitry in major depression. Biol Psychiatry 2008; 63: 377-384.
45. Forget B, Coen KM, Le Foll B. Inhibition of fatty acid amide hydrolase reduces reinstatement of nicotine seeking but not break point for nicotine self-administration-comparison with CB(1) receptor blockade. Psychopharmacology (Berl) 2009; 205: 613-624.
46. Scherma M, Medalie J, Fratta W, Vadivel SK, Makriyannis A, Piomelli D et al. The endogenous cannabinoid anandamide has effects on motivation and anxiety that are revealed by fatty acid amide hydrolase (FAAH) inhibition. Neuropharmacology 2008; 54: 129-140.
47. Volkow ND, Fowler JS, Wang GJ, Baler R, Telang F. Imaging dopamine's role in drug abuse and addiction. Neuropharmacology 2009; 56(Suppl 1): 3-8.
48. Pava MJ, Woodward JJ. A review of the interactions between alcohol and the endocannabinoid system: implications for alcohol dependence and future directions for research. Alcohol 2012; 46: 185-204.
49. Di Marzo V, Berrendero F, Bisogno T, Gonzalez S, Cavaliere P, Romero J et al. Enhancement of anandamide formation in the limbic forebrain and reduction of endocannabinoid contents in the striatum of delta9-tetrahydrocannabinol- tolerant rats. J Neurochem 2000; 74: 1627-1635. (Pubitemid 30163985)
50. Gonzalez S, Cascio MG, Fernandez-Ruiz J, Fezza F, Di Marzo V, Ramos JA. Changes in endocannabinoid contents in the brain of rats chronically exposed to nicotine, ethanol or cocaine. Brain Res 2002; 954: 73-81. (Pubitemid 35223443)
51. Knutson B, Fong GW, Bennett SM, Adams CM, Hommer D. A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: characterization with rapid event-related fMRI. Neuroimage 2003; 18: 263-272. (Pubitemid 36269138)
52. O'Doherty JP, Deichmann R, Critchley HD, Dolan RJ. Neural responses during anticipation of a primary taste reward. Neuron 2002; 33: 815-826. (Pubitemid 34219251)
53. Martin-Soelch C, Leenders KL, Chevalley aF, Missimer J, Kunig G, Magyar S et al. Reward mechanisms in the brain and their role in dependence: evidence from neurophysiological and neuroimaging studies. Brain Res Rev 2001; 36: 139-149. (Pubitemid 33020743)
54. Beck A, Schlagenhauf F, Wustenberg T, Hein J, Kienast T, Kahnt T et al. Ventral striatal activation during reward anticipation correlates with impulsivity in alcoholics. Biol Psychiatry 2009; 66: 734-742.
55. Wrase J, Schlagenhauf F, Kienast T, Wustenberg T, Bermpohl F, Kahnt T et al. Dysfunction of reward processing correlates with alcohol craving in detoxified alcoholics. Neuroimage 2007; 35: 787-794. (Pubitemid 46402977)
56. Bjork JM, Smith AR, Hommer DW. Striatal sensitivity to reward deliveries and omissions in substance dependent patients. Neuroimage 2008; 42: 1609-1621.
57. Martin-Soelch C, Missimer J, Leenders KL, Schultz W. Neural activity related to the processing of increasing monetary reward in smokers and nonsmokers. Eur J Neurosci 2003; 18: 680-688. (Pubitemid 37041116)
58. Hendricks PS, Ditre JW, Drobes DJ, Brandon TH. The early time course of smoking withdrawal effects. Psychopharmacology (Berl) 2006; 187: 385-396. (Pubitemid 44079930)