Impulsiveness and insula activation during reward anticipation are associated with genetic variants in GABRA2 in a family sample enriched for alcoholism

Molecular Psychiatry

Volumn 17, Issue 5, 2012, Pages 511-519

  Villafuerte, S ^a,b   Heitzeg, M M ^b,c   Foley, S ^a   Wendy Yau, W Y ^a,c   Majczenko, K ^a,b,c   Zubieta, J K ^a,b   Zucker, R A ^b,c   Burmeister, M ^a,b,d  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

alcohol dependence; fMRI; GABRA2; impulsiveness; insula; SNP

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR ALPHA2;

ADULT; ALCOHOLISM; ALLELE; ANTICIPATION; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; FAMILY HISTORY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; HETEROZYGOTE; HUMAN; IMPULSIVENESS; INSULA; MAJOR CLINICAL STUDY; MALE; PERSONALITY TEST; PRIORITY JOURNAL; PROGENY; REIMBURSEMENT; REWARD; SINGLE NUCLEOTIDE POLYMORPHISM;

ADOLESCENT; ADULT; AGED; ALCOHOLISM; ALLELES; ANTICIPATION, PSYCHOLOGICAL; CEREBRAL CORTEX; FAMILY HEALTH; FEMALE; FUNCTIONAL NEUROIMAGING; GENETIC PREDISPOSITION TO DISEASE; HAPLOTYPES; HUMANS; IMPULSIVE BEHAVIOR; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, GABA-A; REWARD; SEX CHARACTERISTICS;

EID: 84860112368     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2011.33     Document Type: Article

References (57)

1. Krystal JH, Staley J, Mason G, Petrakis IL, Kaufman J, Harris RA et al. Gamma-aminobutyric acid type A receptors and alcoholism: intoxication, dependence, vulnerability, and treatment. Arch Gen Psychiatry 2006; 63: 957-968. (Pubitemid 44330454)
2. Grobin AC, Matthews DB, Devaud LL, Morrow AL. The role of GABA(A) receptors in the acute and chronic effects of ethanol. Psychopharmacology (Berlin) 1998; 139: 2-19. (Pubitemid 28416878)
3. Agrawal A, Edenberg HJ, Foroud T, Bierut LJ, Dunne G, Hinrichs AL et al. Association of GABRA2 with drug dependence in the collaborative study of the genetics of alcoholism sample. Behav Genet 2006; 36: 640-650. (Pubitemid 44188079)
4. Bauer LO, Covault J, Harel O, Das S, Gelernter J, Anton R et al. Variation in GABRA2 predicts drinking behavior in project MATCH subjects. Alcohol Clin Exp Res 2007; 31: 1780-1787. (Pubitemid 47609654)
5. Covault J, Gelernter J, Hesselbrock V, Nellissery M, Kranzler HR. Allelic and haplotypic association of GABRA2 with alcohol dependence. Am J Med Genet B 2004; 129: 104-109. (Pubitemid 38989078)
6. Edenberg HJ, Dick DM, Xuei X, Tian H, Almasy L, Bauer LO et al. Variations in GABRA2, encoding the alpha 2 subunit of the GABA(A) receptor, are associated with alcohol dependence and with brain oscillations. Am J Hum Genet 2004; 74: 705-714. (Pubitemid 38420099)
7. Enoch MA, Schwartz L, Albaugh B, Virkkunen M, Goldman D. Dimensional anxiety mediates linkage of GABRA2 haplotypes with alcoholism. Am J Med Genet B 2006; 141: 599-607. (Pubitemid 44434660)
8. Fehr C, Sander T, Tadic A, Lenzen KP, Anghelescu I, Klawe C et al. Confirmation of association of the GABRA2 gene with alcohol dependence by subtype-specific analysis. Psychiatr Genet 2006; 16: 9-17. (Pubitemid 44481214)
9. Lappalainen J, Krupitsky E, Remizov M, Pchelina S, Taraskina A, Zvartau E et al. Association between alcoholism and gammaamino butyric acid alpha2 receptor subtype in a Russian population. Alcohol Clin Exp Res 2005; 29: 493-498. (Pubitemid 40547851)
10. Pierucci-Lagha A, Covault J, Feinn R, Nellissery M, Hernandez-Avila C, Oncken C et al. GABRA2 alleles moderate the subjective effects of alcohol, which are attenuated by finasteride. Neuropsychopharmacology 2005; 30: 1193-1203. (Pubitemid 40720979)
11. Soyka M, Preuss UW, Hesselbrock V, Zill P, Koller G, Bondy B. GABA-A2 receptor subunit gene (GABRA2) polymorphisms and risk for alcohol dependence. J Psychiatr Res 2008; 42: 184-191. (Pubitemid 350278616)
12. Lind PA, Macgregor S, Agrawal A, Montgomery GW, Heath AC, Martin NG et al. The role of GABRA2 in alcohol dependence, smoking, and illicit drug use in an Australian population sample. Alcohol Clin Exp Res 2008; 32: 1721-1731.
13. Rangaswamy M, Porjesz B, Chorlian DB, Wang K, Jones KA, Bauer LO et al. Beta power in the EEG of alcoholics. Biol Psychiatry 2002; 52: 831-842.
14. Rangaswamy M, Porjesz B, Chorlian DB, Wang K, Jones KA, Kuperman S et al. Resting EEG in offspring of male alcoholics: beta frequencies. Int J Psychophysiol 2004; 51: 239-251. (Pubitemid 38220938)
15. Bauer LO. Predicting relapse to alcohol and drug abuse via quantitative electroencephalography. Neuropsychopharmacology 2001; 25: 332-340. (Pubitemid 32777785)
16. Le Roux N, Amar M, Moreau A, Baux G, Fossier P. Impaired GABAergic transmission disrupts normal homeostatic plasticity in rat cortical networks. Eur J Neurosci 2008; 27: 3244-3256. (Pubitemid 351847312)
17. Bonson KR, Grant SJ, Contoreggi CS, Links JM, Metcalfe J, Weyl HL et al. Neural systems and cue-induced cocaine craving. Neuropsychopharmacology 2002; 26: 376-386. (Pubitemid 34159215)
18. Naqvi NH, Bechara A. The hidden island of addiction: the insula. Trends Neurosci 2009; 32: 56-67.
19. Sell LA, Morris JS, Bearn J, Frackowiak RS, Friston KJ, Dolan RJ. Neural responses associated with cue evoked emotional states and heroin in opiate addicts. Drug Alcohol Depend 2000; 60: 207-216. (Pubitemid 30625024)
20. Contreras M, Ceric F, Torrealba F. Inactivation of the interoceptive insula disrupts drug craving and malaise induced by lithium. Science 2007; 318: 655-658. (Pubitemid 350014841)
21. Kilts CD, Schweitzer JB, Quinn CK, Gross RE, Faber TL, Muhammad F et al. Neural activity related to drug craving in cocaine addiction. Arch Gen Psychiatry 2001; 58: 334-341. (Pubitemid 32299529)
22. Brody AL, Mandelkern MA, London ED, Childress AR, Lee GS, Bota RG et al. Brain metabolic changes during cigarette craving. Arch Gen Psychiatry 2002; 59: 1162-1172. (Pubitemid 35424027)
23. Naqvi NH, Rudrauf D, Damasio H, Bechara A. Damage to the insula disrupts addiction to cigarette smoking. Science 2007; 315: 531-534. (Pubitemid 46175760)
24. Simmons A, Strigo I, Matthews SC, Paulus MP, Stein MB. Anticipation of aversive visual stimuli is associated with increased insula activation in anxiety-prone subjects. Biol Psychiatry 2006; 60: 402-409. (Pubitemid 44215851)
25. Stein MB, Simmons AN, Feinstein JS, Paulus MP. Increased amygdala and insula activation during emotion processing in anxiety-prone subjects. Am J Psychiatry 2007; 164: 318-327.
26. Whiteside SP, Lynam DR. The Five Factor Model and impulsivity: using a structural model of personality to understand impulsivity. Person Individ Diff 2001; 30: 669-689. (Pubitemid 33380663)
27. Costa PTJ, McCrae RR. Revised NEO Personality Inventory (NEO-PI-R) and NEO Five-Factor Inventory (NEO-FFI) Professional Manual. Psychological Assessment Resources: Odessa, FL, 1992.
28. Dawe S, Gullo MJ, Loxton NJ. Reward drive and rash impulsiveness as dimensions of impulsivity: implications for substance misuse. Addict Behav 2004; 29: 1389-1405. (Pubitemid 39165996)
29. Zucker RA, Fitzgerald HE, Refior SK, Puttler LI, Pallas DM, Ellis DA. The Clinical and Social Ecology of Childhood for Children of Alcoholics: Description and Implications for a Differentiated Social Policy. RoutledgeFalmer: New York, 2000.
30. Knutson B, Westdorp A, Kaiser E, Hommer D. FMRI visualization of brain activity during a monetary incentive delay task. Neuroimage 2000; 12: 20-27. (Pubitemid 30602060)
31. Zucker RA, Ellis DA, Bingham CR, Fitzgerald HE, Sanford KP. Other evidence for at least two alcoholisms, II: life course variation in antisociality and heterogeneity of alcoholic outcome. Devel Psychopathol 1996; 8: 831-848. (Pubitemid 126451047)
32. Zucker RA, Fitzgerald HE, Noll RB. Drinking and Drug History. Michigan State University: East Lansing, MI, 1990.
33. Feighner JP, Robins E, Guze SB, Woodruff Jr RA, Winokur G, Munoz R. Diagnostic criteria for use in psychiatric research. Arch Gen Psychiatry 1972; 26: 57-63.
34. Johnston LD, Bachman JG, O'Malley PM. US Department of Health, Education, and Welfare, National Institute on Drug Abuse DoR: Washington, DC, 1979.
35. Cahalan D, Cisin IH, Crossley HM. American Drinking Practices: A National Study of Drinking Behavior and Attitudes (Monograph No. 6). Publications Division, Rutgers Center of Alcohol Studies: New Brunswick, NJ, 1969.
36. Schuckit MA. Research questionnaire, San Diego, CA: Alcoholism Treatment Program. VA Medical Center, University of California: San Diego, CA, 1978.
37. Room R. Measuring drinking patterns: the experience of the last half century. J Subst Abuse 2000; 12: 23-31. (Pubitemid 38198174)
38. Barrett JC, Fry B, Maller J, Daly MJ. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 2005; 21: 263-265. (Pubitemid 40202029)
39. Chen WM, Abecasis GR. Family-based association tests for genomewide association scans. Am J Hum Genet 2007; 81: 913-926. (Pubitemid 47580246)
40. Glover GH, Law CS. Spiral-in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts. Magn Reson Med 2001; 46: 515-522. (Pubitemid 32831327)
41. Sutton BP, Noll DC, Fessler JA. Fast, iterative image reconstruction for MRI in the presence of field inhomogeneities. IEEE Trans Med Imaging 2003; 22: 178-188.
42. Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 2002; 17: 825-841. (Pubitemid 35317016)
43. Maldjian J, Laurienti P, Burdette J. Precentral gyrus discrepancy in electronic versions of the Talairach atlas. Neuroimage 2004; 21: 450-455. (Pubitemid 38115035)
44. Maldjian J, Laurienti P, Kraft R, Burdette J. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 2003; 19: 1233-1239. (Pubitemid 36918259)
45. 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)
46. Brett M, Anton J-L, Valabregue R, Poline J-B. Region of interest analysis using an SPM toolbox. Proceedings of the Eighth International Conference on Functional Mapping of the Human Brain; June 2-6 2002 Sendai, Japan.
47. Magid V, Maclean MG, Colder CR. Differentiating between sensation seeking and impulsivity through their mediated relations with alcohol use and problems. Addict Behav 2007; 32: 2046-2061. (Pubitemid 47198948)
48. Dick DM, Bierut L, Hinrichs A, Fox L, Bucholz KK, Kramer J et al. The role of GABRA2 in risk for conduct disorder and alcohol and drug dependence across developmental stages. Behav Genet 2006; 36: 577-590. (Pubitemid 43967652)
49. Rubio G, Jimenez M, Rodriguez-Jimenez R, Martinez I, Avila C, Ferre F et al. The role of behavioral impulsivity in the development of alcohol dependence: a 4-year follow-up study. Alcohol Clin Exp Res 2008; 32: 1681-1687.
50. Edenberg HJ, Foroud T. The genetics of alcoholism: identifying specific genes through family studies. Addict Biol 2006; 11: 386-396. (Pubitemid 46696910)
51. Engel SR, Grant KA. Neurosteroids and behavior. Int Rev Neurobiol 2001; 46: 321-348. (Pubitemid 33798726)
52. Gulinello M, Smith SS. Anxiogenic effects of neurosteroid exposure: sex differences and altered GABAA receptor pharmacology in adult rats. J Pharmacol Exp Ther 2003; 305: 541-548. (Pubitemid 36459168)
53. Hartka E, Johnstone B, Leino EV, Motoyoshi M, Temple MT, Fillmore KM. A meta-analysis of depressive symptomatology and alcohol consumption over time. Br J Addict 1991; 86: 1283-1298.
54. Muraven M, Collins RL, Morsheimer ET, Shiffman S, Paty JA. One too many: predicting future alcohol consumption following heavy drinking. Exp Clin Psychopharmacol 2005; 13: 127-136. (Pubitemid 40791821)
55. Poulin C, Hand D, Boudreau B, Santor D. Gender differences in the association between substance use and elevated depressive symptoms in a general adolescent population. Addiction 2005; 100: 525-535. (Pubitemid 40529845)
56. Dick DM, Agrawal A, Schuckit MA, Bierut L, Hinrichs A, Fox L et al. Marital status, alcohol dependence, and GABRA2: evidence for gene-environment correlation and interaction. J Stud Alcohol 2006; 67: 185-194. (Pubitemid 43277286)
57. Dick DM, Latendresse SJ, Lansford JE, Budde JP, Goate A, Dodge KA et al. Role of GABRA2 in trajectories of externalizing behavior across development and evidence of moderation by parental monitoring. Arch Gen Psychiatry 2009; 66: 649-657.