Alcohol-induced impairment of inhibitory control is linked to attenuated brain responses in right fronto-temporal cortex

Biological Psychiatry

Volumn 76, Issue 9, 2014, Pages 698-707

  Gan, Gabriela ^a   Guevara, Alvaro ^a,b   Marxen, Michael ^a   Neumann, Maike ^a   Jünger, Elisabeth ^a   Kobiella, Andrea ^a   Mennigen, Eva ^a   Pilhatsch, Maximilian ^a   Schwarz, Daniel ^a   Zimmermann, Ulrich S ^a   Smolka, Michael N ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b UNIVERSIDAD DE COSTA RICA   (Costa Rica)

Author keywords

Acute alcohol intoxication; Alcohol consumption; FMRI; Inhibitory control; Response inhibition; Stop signal task

Indexed keywords

ALCOHOL; PLACEBO; ALCOHOL DERIVATIVE; CENTRAL DEPRESSANT AGENT; OXYGEN;

ADULT; ALCOHOL CONSUMPTION; ALCOHOL INTOXICATION; ARTICLE; BEHAVIOR; BRAIN REGION; COGNITION; CONTROLLED STUDY; CROSSOVER PROCEDURE; FEMALE; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; INHIBITION (PSYCHOLOGY); MALE; NEUROIMAGING; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; PROBABILITY; RESPONSE INHIBITION; RESPONSE TIME; SINGLE BLIND PROCEDURE; STOP SIGNAL TASK; TASK PERFORMANCE; TEMPORAL CORTEX; YOUNG ADULT; ADDICTION; ADOLESCENT; BLOOD; CHEMICALLY INDUCED; DECISION MAKING; DRUG EFFECTS; DRUG SELF ADMINISTRATION; FRONTAL LOBE; IMAGE PROCESSING; LEARNING DISORDER; LONGITUDINAL STUDY; METABOLISM; PSYCHOLOGY; RANDOMIZED CONTROLLED TRIAL; SMOKING; TEMPORAL LOBE; TIME; VASCULARIZATION;

ADOLESCENT; ALCOHOLS; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CHOICE BEHAVIOR; CROSS-OVER STUDIES; ETHANOL; FEMALE; FRONTAL LOBE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INHIBITION (PSYCHOLOGY); LEARNING DISORDERS; LONGITUDINAL STUDIES; MALE; OXYGEN; SELF ADMINISTRATION; SINGLE-BLIND METHOD; SMOKING; SUBSTANCE-RELATED DISORDERS; TEMPORAL LOBE; TIME FACTORS; YOUNG ADULT;

EID: 84922640895     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2013.12.017     Document Type: Article

References (61)

1. Corte CM, Sommers MS (2005): Alcohol and risky behaviors. Annu Rev Nurs Res 23:327-360.
2. Halpern-Felsher BL, Millstein SG, Ellen JM (1996): Relationship of alcohol use and risky sexual behavior: A review and analysis of findings. J Adolesc Health 19:331-336.
3. Gilman JM, Smith AR, Ramchandani VA, Momenan R, Hommer DW (2012): The effect of intravenous alcohol on the neural correlates of risky decision making in healthy social drinkers. Addict Biol 17: 465-478.
4. Giancola PR, Parrott DJ (2008): Further evidence for the validity of the Taylor Aggression Paradigm. Aggress Behav 34:214-229.
5. Hoaken PN, Pihl RO (2000): The effects of alcohol intoxication on aggressive responses in men and women. Alcohol Alcohol 35: 471-477.
6. de Wit H, Crean J, Richards JB (2000): Effects of d-amphetamine and ethanol on a measure of behavioral inhibition in humans. Behav Neurosci 114:830-837.
7. Loeber S, Duka T (2009): Acute alcohol impairs conditioning of a behavioural reward-seeking response and inhibitory control processes -implications for addictive disorders. Addiction 104:2013-2022.
8. Mulvihill LE, Skilling TA, Vogel-Sprott M (1997): Alcohol and the ability to inhibit behavior in men and women. J Stud Alcohol 58: 600-605.
9. Feola TW, de Wit H, Richards JB (2000): Effects of d-amphetamine and alcohol on a measure of behavioral inhibition in rats. Behav Neurosci 114:838-848.
10. Marczinski CA, Abroms BD, Van Selst M, Fillmore MT (2005): Alcoholinduced impairment of behavioral control: Differential effects on engaging vs. disengaging responses. Psychopharmacology (Berl) 182: 452-459.
11. Fillmore MT, Weafer J (2004): Alcohol impairment of behavior in men and women. Addiction 99:1237-1246.
12. Field M, Wiers RW, Christiansen P, Fillmore MT, Verster JC (2010): Acute alcohol effects on inhibitory control and implicit cognition: Implications for loss of control over drinking. Alcohol Clin Exp Res 34: 1346-1352.
13. Weafer J, Fillmore MT (2008): Individual differences in acute alcohol impairment of inhibitory control predict ad libitum alcohol consumption. Psychopharmacology (Berl) 201:315-324.
14. Marczinski CA, Combs SW, Fillmore MT (2007): Increased sensitivity to the disinhibiting effects of alcohol in binge drinkers. Psychol Addict Behav 21:346-354.
15. Anderson BM, Stevens MC, Meda SA, Jordan K, Calhoun VD, Pearlson GD (2011): Functional imaging of cognitive control during acute alcohol intoxication. Alcohol Clin Exp Res 35:156-165.
16. Marinkovic K, Rickenbacher E, Azma S, Artsy E (2012): Acute alcohol intoxication impairs top-down regulation of Stroop incongruity as revealed by blood oxygen level-dependent functional magnetic resonance imaging. Hum Brain Mapp 33:319-333.
17. Schuckit MA, Tapert S, Matthews SC, Paulus MP, Tolentino NJ, Smith TL, et al. (2012): fMRI differences between subjects with low and high responses to alcohol during a stop signal task. Alcohol Clin Exp Res 36: 130-140.
18. Kareken DA, Dzemidzic M, Wetherill L, Eiler W, Oberlin BG, Harezlak J, et al. (2013): Family history of alcoholism interacts with alcohol to affect brain regions involved in behavioral inhibition. Psychopharmacology (Berl) 228:335-345.
19. Swick D, Ashley V, Turken U (2011): Are the neural correlates of stopping and not going identical? Quantitative meta-analysis of two response inhibition tasks. Neuroimage 56:1655-1665.
20. Aron AR, Poldrack RA (2006): Cortical and subcortical contributions to Stop signal response inhibition: Role of the subthalamic nucleus. J Neurosci 26:2424-2433.
21. Aron AR, Behrens TE, Smith S, Frank MJ, Poldrack RA (2007): Triangulating a cognitive control network using diffusion-weighted magnetic resonance imaging (MRI) and functional MRI. J Neurosci 27:3743-3752.
22. Boehler CN, Appelbaum LG, Krebs RM, Hopf JM, Woldorff MG (2010): Pinning down response inhibition in the brain-conjunction analyses of the stop-signal task. Neuroimage 52:1621-1632.
23. Levy BJ, Wagner AD (2011): Cognitive control and right ventrolateral prefrontal cortex: Reflexive reorienting, motor inhibition, and action updating. Ann N Y Acad Sci 1224:40-62.
24. Rubia K, Smith AB, Brammer MJ, Taylor E (2003): Right inferior prefrontal cortex mediates response inhibition while mesial prefrontal cortex is responsible for error detection. Neuroimage 20:351-358.
25. Logan GD, Schachar RJ, Tannock R (1997): Impulsivity and inhibitory control. Psychol Sci 8:60-64.
26. Sharp DJ, Bonnelle V, De B, X, Beckmann CF, James SG, Patel MC, et al. (2010): Distinct frontal systems for response inhibition, attentional capture, and error processing. Proc Natl Acad Sci U S A 107:6106-6111.
27. Duann JR, Ide JS, Luo X, Li CS (2009): Functional connectivity delineates distinct roles of the inferior frontal cortex and presupplementary motor area in stop signal inhibition. J Neurosci 29:10171-10179.
28. Verbruggen F, Aron AR, Stevens MA, Chambers CD (2010): Theta burst stimulation dissociates attention and action updating in human inferior frontal cortex. Proc Natl Acad Sci U S A 107:13966-13971.
29. Whelan R, Conrod PJ, Poline JB, Lourdusamy A, Banaschewski T, Barker GJ, et al. (2012): Adolescent impulsivity phenotypes characterized by distinct brain networks. Nat Neurosci 15:920-153.
30. Rubia K, Smith AB, Brammer MJ, Toone B, Taylor E (2005): Abnormal brain activation during inhibition and error detection in medicationnaive adolescents with ADHD. Am J Psychiatry 162:1067-1075.
31. Rubia K, Smith AB, Taylor E, Brammer M (2007): Linear age-correlated functional development of right inferior fronto-striato-cerebellar networks during response inhibition and anterior cingulate during errorrelated processes. Hum Brain Mapp 28:1163-1177.
32. Chamberlain SR, Hampshire A, Muller U, Rubia K, Del Campo N, Craig K, et al. (2009): Atomoxetine modulates right inferior frontal activation during inhibitory control: A pharmacological functional magnetic resonance imaging study. Biol Psychiatry 65:550-555.
33. Jacobson L, Javitt DC, Lavidor M (2011): Activation of inhibition: Diminishing impulsive behavior by direct current stimulation over the inferior frontal gyrus. J Cogn Neurosci 23:3380-3387.
34. Palmer RH, Young SE, Hopfer CJ, Corley RP, Stallings MC, Crowley TJ, et al. (2009): Developmental epidemiology of drug use and abuse in adolescence and young adulthood: Evidence of generalized risk. Drug Alcohol Depend 102:78-87.
35. Grant JD, Scherrer JF, Lynskey MT, Lyons MJ, Eisen SA, Tsuang MT, et al. (2006): Adolescent alcohol use is a risk factor for adult alcohol and drug dependence: Evidence from a twin design. Psychol Med 36: 109-118.
36. McCambridge J, McAlaney J, Rowe R (2011): Adult consequences of late adolescent alcohol consumption: A systematic review of cohort studies. PLoS Med 8:e1000413.
37. Wiesner M, Weichold K, Silbereisen RK (2007): Trajectories of alcohol use among adolescent boys and girls: Identification, validation, and sociodemographic characteristics. Psychol Addict Behav 21:62-75.
38. Williams BR, Ponesse JS, Schachar RJ, Logan GD, Tannock R (1999): Development of inhibitory control across the life span. Dev Psychol 35: 205-213.
39. Gunther M, Oshio K, Feinberg DA (2005): Single-shot 3D imaging techniques improve arterial spin labeling perfusion measurements. Magn Reson Med 54:491-498.
40. Khalili-Mahani N, van Osch MJ, Baerends E, Soeter RP, de Kam M, Zoethout RW, et al. (2011): Pseudocontinuous arterial spin labeling reveals dissociable effects of morphine and alcohol on regional cerebral blood flow. J Cereb Blood Flow Metab 31:1321-1333.
41. Volkow ND, Mullani N, Gould L, Adler SS, Guynn RW, Overall JE, et al. (1988): Effects of acute alcohol intoxication on cerebral blood flow measured with PET. Psychiatry Res 24:201-209.
42. Wise RG, Tracey I (2006): The role of fMRI in drug discovery. J Magn Reson Imaging 23:862-876.
43. Zimmermann US, Mick I, Laucht M, Vitvitskiy V, Plawecki MH, Mann KF, et al. (2009): Offspring of parents with an alcohol use disorder prefer higher levels of brain alcohol exposure in experiments involvingcomputer-assisted self-infusion of ethanol (CASE). Psychopharmacology (Berl) 202:689-697.
44. O'Connor S, Morzorati S, Christian J, Li TK (1998): Clamping breath alcohol concentration reduces experimental variance: Application to the study of acute tolerance to alcohol and alcohol elimination rate. Alcohol Clin Exp Res 22:202-210.
45. Zimmermann US, Mick I, Vitvitskyi V, Plawecki MH, Mann KF, O'Connor S (2008): Development and pilot validation of computer-assisted selfinfusion of ethanol (CASE): A new method to study alcohol selfadministration in humans. Alcohol Clin Exp Res 32:1321-1328.
46. Ridderinkhof KR, Band GPH, Logan GD (1999): A study of adaptive behavior: Effects of age and irrelevant information on the ability to inhibit one's actions. Acta Psychol 101:315-337.
47. Verbruggen F, Logan GD (2009): Models of response inhibition in the stopsignal and stop-change paradigms. Neurosci Biobehav Rev 33:647-661.
48. Sobell LC, Maisto SA, Sobell MB, Cooper AM (1979): Reliability of alcohol abusers' self-reports of drinking behavior. Behav Res Ther 17:157-160.
49. Corbetta M, Shulman GL (2002): Control of goal-directed and stimulusdriven attention in the brain. Nat Rev Neurosci 3:201-215.
50. Corbetta M, Patel G, Shulman GL (2008): The reorienting system of the human brain: From environment to theory of mind. Neuron 58:306-324.
51. Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, et al. (2007): Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27:2349-2356.
52. Dosenbach NU, Visscher KM, Palmer ED, Miezin FM, Wenger KK, Kang HC, et al. (2006): A core system for the implementation of task sets. Neuron 50:799-812.
53. Hester R, Fassbender C, Garavan H (2004): Individual differences in error processing: A review and reanalysis of three event-related fMRI studies using the GO/NOGO task. Cereb Cortex 14:986-994.
54. Ullsperger M, von Cramon DY (2004): Neuroimaging of performance monitoring: Error detection and beyond. Cortex 40:593-604.
55. Stevens MC, Kiehl KA, Pearlson GD, Calhoun VD (2009): Brain network dynamics during error commission. Hum Brain Mapp 30:24-37.
56. King AC, de Wit H, McNamara PJ, Cao D (2011): Rewarding, stimulant, and sedative alcohol responses and relationship to future binge drinking. Arch Gen Psychiatry 68:389-399.
57. Jantti V, Lang AH, Keskinen E, Lehtinen I, Pakkanen A (1983): Acute effects of intravenously given alcohol on saccadic eye movements and subjective evaluations of intoxication. Psychopharmacology 79: 251-255.
58. Ramchandani VA, O'Connor S, Blekher T, Kareken D, Morzorati S, Nurnberger J Jr., et al. (1999): A preliminary study of acute responses to clamped alcohol concentration and family history of alcoholism. Alcohol Clin Exp Res 23:1320-1330.
59. Leontiev O, Buxton RB (2007): Reproducibility of BOLD, perfusion, and CMRO2 measurements with calibrated-BOLD fMRI. Neuroimage 35: 175-184.
60. Hoge RD, Atkinson J, Gill B, Crelier GR, Marrett S, Pike GB (1999): Investigation of BOLD signal dependence on cerebral blood flow and oxygen consumption: The deoxyhemoglobin dilution model. Magn Reson Med 42:849-863.
61. Pike GB (2012): Quantitative functional MRI: Concepts, issues and future challenges. Neuroimage 62:1234-1240.