Association of marijuana use with blunted nucleus accumbens response to reward anticipation

JAMA Psychiatry

Volumn 73, Issue 8, 2016, Pages 838-844

  Martz, Meghan E ^a,b   Trucco, Elisa M ^a,b   Cope, Lora M ^a   Hardee, Jillian E ^a   Jester, Jennifer M ^a   Zucker, Robert A ^a,b   Heitzeg, Mary M ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b FLORIDA INTERNATIONAL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANNABIS;

ADULT; ANTICIPATION; ARTICLE; CANNABIS USE; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; IMAGE ANALYSIS; MAJOR CLINICAL STUDY; MALE; NERVE POTENTIAL; NEUROIMAGING; NUCLEUS ACCUMBENS; REWARD; RISK ASSESSMENT; SMOKING; SUBSTANCE USE; TASK PERFORMANCE; YOUNG ADULT; AROUSAL; CANNABIS ADDICTION; COMPLICATION; DRUG EFFECT; LONGITUDINAL STUDY; MICHIGAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PROSPECTIVE STUDY; RISK;

ANTICIPATION, PSYCHOLOGICAL; AROUSAL; FEMALE; HUMANS; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MALE; MARIJUANA ABUSE; MICHIGAN; NUCLEUS ACCUMBENS; PROSPECTIVE STUDIES; REWARD; RISK; YOUNG ADULT;

EID: 84982861772     PISSN: 2168622X     EISSN: None     Source Type: Journal    
DOI: 10.1001/jamapsychiatry.2016.1161     Document Type: Article

References (54)

1. Center for Behavioral Health Statistics and Quality. Behavioral Health Trends in the United States: Results From the 2014 National Survey on Drug Use and Health: HHS Publication No. SMA 15-4927, NSDUH Series H-50. Rockville, MD: Substance Abuse and Mental Health Services Administration; 2015.
2. Johnston LD, O'Malley PM, Bachman JG, Schulenberg J, Miech RA. Monitoring the Future: National Survey Results on Drug Use, 1975-2014, Volume II: College Students and Adults Ages 19-55. Ann Arbor: Institute for Social Research, The University of Michigan; 2015.
3. Volkow ND, Baler RD, Compton WM, Weiss SRB. Adverse health effects of marijuana use. N Engl J Med. 2014;370(23):2219-2227.
4. D'Souza DC, Perry E, MacDougall L, et al. The psychotomimetic effects of intravenous delta-9-tetrahydrocannabinol in healthy individuals: implications for psychosis. Neuropsychopharmacology. 2004;29(8):1558-1572.
5. Hartman RL, Huestis MA. Cannabis effects on driving skills. Clin Chem. 2013;59(3):478-492.
6. Maggs JL, Staff J, Kloska DD, Patrick ME, O'Malley PM, Schulenberg J. Predicting young adult degree attainment by late adolescent marijuana use. J Adolesc Health. 2015;57(2):205-211.
7. Filbey FM, Aslan S, Calhoun VD, et al. Long-term effects of marijuana use on the brain. Proc Natl Acad Sci U S A. 2014;111(47):16913-16918.
8. Gilman JM, Kuster JK, Lee S, et al. Cannabis use is quantitatively associated with nucleus accumbens and amygdala abnormalities in young adult recreational users. J Neurosci. 2014;34(16):5529-5538.
9. Meier MH, Caspi A, Ambler A, et al. Persistent cannabis users show neuropsychological decline from childhood to midlife. Proc Natl Acad Sci U S A. 2012;109(40):E2657-E2664.
10. Schweinsburg AD, Brown SA, Tapert SF. The influence of marijuana use on neurocognitive functioning in adolescents. Curr Drug Abuse Rev. 2008;1(1):99-111.
11. Chen CY, Storr CL, Anthony JC. Early-onset drug use and risk for drug dependence problems. Addict Behav. 2009;34(3):319-322.
12. Lynskey MT, Heath AC, Bucholz KK, et al. Escalation of drug use in early-onset cannabis users vs co-twin controls. JAMA. 2003;289(4):427-433.
13. Ikemoto S. Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res Rev. 2007;56(1):27-78.
14. Grace AA, Floresco SB, Goto Y, Lodge DJ. Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends Neurosci. 2007;30(5):220-227.
15. Pierce RC, Kumaresan V. The mesolimbic dopamine system: the final common pathway for the reinforcing effect of drugs of abuse? Neurosci Biobehav Rev. 2006;30(2):215-238.
16. Volkow ND, Wang GJ, Telang F, et al. Decreased dopamine brain reactivity in marijuana abusers is associated with negative emotionality and addiction severity. Proc Natl Acad Sci U S A. 2014;111(30):E3149-E3156.
17. Blum K, Braverman ER, Holder JM, et al. Reward deficiency syndrome: a biogenetic model for the diagnosis and treatment of impulsive, addictive, and compulsive behaviors. J Psychoactive Drugs. 2000;32(suppl):i-iv, 1-112.
18. Robinson TE, Berridge KC. Incentive-sensitization and addiction. Addiction. 2001;96(1):103-114.
19. Volkow ND, Morales M. The brain on drugs: from reward to addiction. Cell. 2015;162(4):712-725.
20. Knutson B, Adams CM, Fong GW, Hommer D. Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neurosci. 2001;21(16):RC159.
21. Heitzeg MM, Villafuerte S, Weiland BJ, et al. Effect of GABRA2 genotype on development of incentive-motivation circuitry in a sample enriched for alcoholism risk. Neuropsychopharmacology. 2014;39(13):3077-3086.
22. Yau WY, Zubieta JK, Weiland BJ, Samudra PG, Zucker RA, Heitzeg MM. Nucleus accumbens response to incentive stimuli anticipation in children of alcoholics: relationships with precursive behavioral risk and lifetime alcohol use. J Neurosci. 2012;32(7):2544-2551.
23. Jager G, Block RI, Luijten M, Ramsey NF. Tentative evidence for striatal hyperactivity in adolescent cannabis-using boys: a cross-sectional multicenter fMRI study. J Psychoactive Drugs. 2013;45(2):156-167.
24. Nestor L, Hester R, Garavan H. Increased ventral striatal BOLD activity during non-drug reward anticipation in cannabis users. Neuroimage. 2010;49(1):1133-1143.
25. Enzi B, Lissek S, Edel MA, et al. Alterations of monetary reward and punishment processing in chronic cannabis users: an FMRI study. PLoS One. 2015;10(3):e0119150.
26. Filbey FM, Dunlop J, Myers US. Neural effects of positive and negative incentives during marijuana withdrawal. PLoS One. 2013;8(5):e61470.
27. Karoly HC, Bryan AD, Weiland BJ, Mayer A, Dodd A, Feldstein Ewing SW. Does incentive-elicited nucleus accumbens activation differ by substance of abuse? An examination with adolescents. Dev Cogn Neurosci. 2015;16:5-15.
28. Bjork JM, Smith AR, Hommer DW. Striatal sensitivity to reward deliveries and omissions in substance dependent patients. Neuroimage. 2008;42(4):1609-1621.
29. Forbes EE, Brown SM, Kimak M, Ferrell RE, Manuck SB, Hariri AR. Genetic variation in components of dopamine neurotransmission impacts ventral striatal reactivity associated with impulsivity. Mol Psychiatry. 2009;14(1):60-70.
30. Hahn T, Dresler T, Ehlis AC, et al. Neural response to reward anticipation is modulated by Gray's impulsivity. Neuroimage. 2009;46(4):1148-1153.
31. Zucker RA, Fitzgerald HE, Refior SK, Puttler LI, Pallas DM, Ellis DA. The clinical and social ecology of childhood for children of alcoholics: description of a study and implications for a differentiated social policy. In: Fitzgerald HE, Lester BM, Zucker RA, eds. Children of Addiction: Research, Health and Policy Issues. New York, NY: Routledge Falmer; 2000:109-141.
32. Robins L, Cottler LB, Bucholz KK, Compton WM, North CS, Rourke K. Diagnostic Interview Schedule for the DSM-IV. St. Louis, MO: Washington University School of Medicine; 2000.
33. Zucker RA, Ellis DE, Fitzgerald HE, Bingham CR, Sanford KP. Other evidence for at least two alcoholisms, II: life course variation in antisociality and heterogeneity of alcoholic outcome. Dev Psychopathol. 1996;8(4):831-848.
34. Zucker RA, Fitzgerald HE, Noll RB. Drinking and Drug History. Revised ed, version 4. East Lansing: Michigan State University Department of Psychology; 1990.
35. Glover GH, Law CS. Spiral-in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts. Magn Reson Med. 2001;46(3):515-522.
36. Kriegeskorte N, Simmons WK, Bellgowan PSF, Baker CI. Circular analysis in systems neuroscience: the dangers of double dipping. Nat Neurosci. 2009;12(5):535-540.
37. Brett M, Anton JL, Valabregue R, Poline JB. Region of interest analysis using an SPM toolbox [abstract]. In: Eighth International Conference on Functional Mapping of the Human Brain; Sendai, Japan; June 2-6, 2002.
38. Muthén BO, Muthén LK. Mplus (Version 7.2). Los Angeles, CA: Muthén & Muthén; 2014.
39. Zucker RA. Genes, brain, behavior, and context: the developmental matrix of addictive behavior. In: Stoltenberg SF, ed. Genes and the Motivation to Use Substances. Vol 61: Nebraska Symposium on Motivation. New York: Springer New York; 2014:51-69.
40. Kandel DB, Chen K. Types of marijuana users by longitudinal course. J Stud Alcohol. 2000;61(3):367-378.
41. Jackson KM, Sher KJ, Schulenberg JE. Conjoint developmental trajectories of young adult substance use. Alcohol Clin Exp Res. 2008;32(5):723-737.
42. Neal DJ, Fromme K. Event-level covariation of alcohol intoxication and behavioral risks during the first year of college. J Consult Clin Psychol. 2007;75(2):294-306.
43. Jansma JM, van Hell HH, Vanderschuren LJMJ, et al. THC reduces the anticipatory nucleus accumbens response to reward in subjects with a nicotine addiction. Transl Psychiatry. 2013;3(2):e234.
44. 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(3):153-163.
45. Hu L, Bentler PM. Cutoff criteria for fit indexes in covariance structure analysis: conventional criteria vs new alternatives. Struct Equ Modeling. 1999;6(1):1-55.
46. Blum K, Cull JG, Braverman ER, Comings DE. Reward deficiency syndrome. Am Sci. 1996;84(2):132-145.
47. Robinson TE, Berridge KC. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev. 1993;18(3):247-291.
48. Martin M, Ledent C, Parmentier M, Maldonado R, Valverde O. Involvement of CB1 cannabinoid receptors in emotional behaviour. Psychopharmacology (Berl). 2002;159(4):379-387.
49. Bambico FR, Nguyen NT, Katz N, Gobbi G. Chronic exposure to cannabinoids during adolescence but not during adulthood impairs emotional behaviour and monoaminergic neurotransmission. Neurobiol Dis. 2010;37(3):641-655.
50. 9 -tetrahydrocannabinol during adolescence provokes sex-dependent changes in the emotional profile in adult rats: behavioral and biochemical correlates. Neuropsychopharmacology. 2008;33(11):2760-2771.
51. Heitzeg MM, Cope LM, Martz ME, Hardee JE, Zucker RA. Brain activation to negative stimuli mediates a relationship between adolescent marijuana use and later emotional functioning. Dev Cogn Neurosci. 2015;16:71-83.
52. Wrase J, Schlagenhauf F, Kienast T, et al. Dysfunction of reward processing correlates with alcohol craving in detoxified alcoholics. Neuroimage. 2007;35(2):787-794.
53. Beck A, Schlagenhauf F, Wüstenberg T, et al. Ventral striatal activation during reward anticipation correlates with impulsivity in alcoholics. Biol Psychiatry. 2009;66(8):734-742.
54. National Institute on Alcohol Abuse and Alcoholism. NIAAA council approves definition of binge drinking. NIAAA News. 2004(3):3.