Alcohol Affects Neuronal Substrates of Response Inhibition but Not of Perceptual Processing of Stimuli Signalling a Stop Response

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Nikolaou, Kyriaki ^a,b   Critchley, Hugo ^a,b,c   Duka, Theodora ^a,b  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b BRIGHTON AND SUSSEX MEDICAL SCHOOL   (United Kingdom)

^c SUSSEX PARTNERSHIP NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL;

ANGULAR GYRUS; ARTICLE; BEHAVIOR; CONNECTOME; CONTROLLED STUDY; DRINKING BEHAVIOR; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GLOBUS PALLIDUS; HUMAN; HUMAN EXPERIMENT; INFERIOR PARIETAL LOBULE; LATENT PERIOD; MIDDLE TEMPORAL GYRUS; MOTOR CORTEX; NORMAL HUMAN; OCCIPITAL CORTEX; PARS OPERCULARIS; PERCEPTION; PREFRONTAL CORTEX; REACTION TIME; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; SUPERIOR TEMPORAL GYRUS; SUPRAMARGINAL GYRUS; TASK PERFORMANCE; TEMPORAL CORTEX; THALAMUS; VISUAL ANALOG SCALE; VISUAL STOP SIGNAL TASK;

ADOLESCENT; ADULT; ANALYSIS OF VARIANCE; DOSE-RESPONSE RELATIONSHIP, DRUG; ETHANOL; FEMALE; HUMANS; INHIBITION (PSYCHOLOGY); MALE; MOTOR ACTIVITY; NEURONS; PHOTIC STIMULATION; SIGNAL TRANSDUCTION; VISUAL PERCEPTION; YOUNG ADULT;

EID: 84884566370     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076649     Document Type: Article

References (77)

1. Goldstein RZ, Volkow ND, (2002) Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. Am J Psychiatry 159: 1642-1652. doi:10.1176/appi.ajp.159.10.1642. PubMed: 12359667.
2. Norman AL, Pulido C, Squeglia LM, Spadoni AD, Paulus MP, et al. (2011) Neural activation during inhibition predicts initiation of substance use in adolescence. Drug Alcohol Depend 119: 216-223. doi:10.1016/j.drugalcdep.2011.06.019. PubMed: 21782354.
3. 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. PubMed: 20491732.
4. Steele CM, Southwick L, (1985) Alcohol and social behavior I: The psychology of drunken excess. J Pers Soc Psychol 48: 18-34. doi:10.1037/0022-3514.48.1.18. PubMed: 3981386.
5. Logan GD, Cowan WB, Davis KA, (1984) On the ability to inhibit simple and choice reaction time responses: a model and a method. J Exp Psychol Hum Percept Perform 10: 276-291. doi:10.1037/0096-1523.10.2.276. PubMed: 6232345.
6. 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. doi:10.1111/j.1360-0443.2009.02718.x. PubMed: 19922568.
7. Weafer J, Fillmore MT, (2008) Individual differences in acute alcohol impairment of inhibitory control predict ad libitum alcohol consumption. Psychopharmacology (Berl) 201: 315-324. doi:10.1007/s00213-008-1284-7. PubMed: 18758758.
8. Dougherty DM, Marsh-Richard DM, Hatzis ES, Nouvion SO, Mathias CW, (2008) A test of alcohol dose effects on multiple behavioral measures of impulsivity. Drug Alcohol Depend 96: 111-120. doi:10.1016/j.drugalcdep.2008.02.002. PubMed: 18378098.
9. Guillot CR, Fanning JR, Bullock JS, McCloskey MS, Berman ME, (2010) Effects of alcohol on tests of executive functioning in men and women: a dose response examination. Exp Clin Psychopharmacol 18: 409-417. doi:10.1037/a0021053. PubMed: 20939644.
10. Fillmore MT, Marczinski CA, Bowman AM, (2005) Acute tolerance to alcohol effects on inhibitory and activational mechanisms of behavioral control. J Stud Alcohol 66: 663-672. PubMed: 16331852.
11. Marczinski CA, Abroms BD, Van Selst M, Fillmore MT, (2005) Alcohol-induced impairment of behavioral control: differential effects on engaging vs. disengaging responses. Psychopharmacology (Berl) 182: 452-459. doi:10.1007/s00213-005-0116-2. PubMed: 16075287.
12. Marczinski CA, Fillmore MT, (2003) Preresponse cues reduce the impairing effects of alcohol on the execution and suppression of responses. Exp Clin Psychopharmacol 11: 110-117. doi:10.1037/1064-1297.11.1.110. PubMed: 12622349.
13. Marczinski CA, Fillmore MT, (2005) Compensating for alcohol-induced impairment of control: effects on inhibition and activation of behavior. Psychopharmacology (Berl) 181: 337-346. doi:10.1007/s00213-005-2269-4. PubMed: 15830219.
14. Fillmore MT, Vogel-Sprott M, (1999) An alcohol model of impaired inhibitory control and its treatment in humans. Exp Clin Psychopharmacol 7: 49-55. doi:10.1037/1064-1297.7.1.49. PubMed: 10036609.
15. 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. PubMed: 9391919.
16. 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. doi:10.1037/0735-7044.114.4.830. PubMed: 10959541.
17. Loeber S, Duka T, (2009) Acute alcohol decreases performance of an instrumental response to avoid aversive consequences in social drinkers. Psychopharmacology (Berl) 205: 577-587. doi:10.1007/s00213-009-1565-9. PubMed: 19468716.
18. Loeber S, Duka T, (2009) Extinction learning of stimulus reward contingencies: The acute effects of alcohol. Drug Alcohol Depend 102: 56-62. doi:10.1016/j.drugalcdep.2009.01.014. PubMed: 19278796.
19. Caswell AJ, Morgan MJ, Duka T, (2013) Acute alcohol effects on subtypes of impulsivity and the role of alcohol-outcome expectancies. Psychopharmacol (Berl), 229: 21-30. PubMed: 23579427.
20. McCarthy DM, Niculete ME, Treloar HR, Morris DH, Bartholow BD, (2012) Acute alcohol effects on impulsivity: associations with drinking and driving behavior. Addiction 107: 2109-2114. doi:10.1111/j.1360-0443.2012.03974.x. PubMed: 22690907.
21. Aron AR, (2007) The neural basis of inhibition in cognitive control. Neuroscientist 13: 214-228. doi:10.1177/1073858407299288. PubMed: 17519365.
22. 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. doi:10.1523/JNEUROSCI.0519-07.2007. PubMed: 17409238.
23. Aron AR, Durston S, Eagle DM, Logan GD, Stinear CM, et al. (2007) Converging evidence for a fronto-basal-ganglia network for inhibitory control of action and cognition. J Neurosci 27: 11860-11864. doi:10.1523/JNEUROSCI.3644-07.2007. PubMed: 17978025.
24. Aron AR, Poldrack RA, (2006) Cortical and subcortical contributions to Stop signal response inhibition: role of the subthalamic nucleus. J Neurosci 26: 2424-2433. doi:10.1523/JNEUROSCI.4682-05.2006. PubMed: 16510720.
25. Chambers CD, Garavan H, Bellgrove MA, (2009) Insights into the neural basis of response inhibition from cognitive and clinical neuroscience. Neurosci Biobehav Rev 33: 631-646. doi:10.1016/j.neubiorev.2008.08.016. PubMed: 18835296.
26. Li CS, Huang C, Constable RT, Sinha R, (2006) Imaging response inhibition in a stop-signal task: neural correlates independent of signal monitoring and post-response processing. J Neurosci 26: 186-192. doi:10.1523/JNEUROSCI.3741-05.2006. PubMed: 16399686.
27. Alexander GE, Crutcher MD, (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13: 266-271. doi:10.1016/0166-2236(90)90107-L. PubMed: 1695401.
28. Alexander GE, Crutcher MD, DeLong MR, (1990) Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. Prog Brain Res 85: 119-146. PubMed: 2094891.
29. Boucher L, Palmeri TJ, Logan GD, Schall JD, (2007) Inhibitory control in mind and brain: an interactive race model of countermanding saccades. Psychol Rev 114: 376-397. doi:10.1037/0033-295X.114.2.376. PubMed: 17500631.
30. Nambu A, Tokuno H, Takada M, (2002) Functional significance of the cortico-subthalamo-pallidal 'hyperdirect' pathway. Neurosci Res 43: 111-117. doi:10.1016/S0168-0102(02)00027-5. PubMed: 12067746.
31. Verbruggen F, Logan GD, (2008) Response inhibition in the stop-signal paradigm. Trends Cogn Sci 12: 418-424. doi:10.1016/j.tics.2008.07.005. PubMed: 18799345.
32. 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 error-related processes. Hum Brain Mapp 28: 1163-1177. doi:10.1002/hbm.20347. PubMed: 17538951.
33. Stevens MC, Kiehl KA, Pearlson GD, Calhoun VD, (2007) Functional neural networks underlying response inhibition in adolescents and adults. Behav Brain Res 181: 12-22. doi:10.1016/j.bbr.2007.03.023. PubMed: 17467816.
34. Boehler CN, Appelbaum LG, Krebs RM, Chen LC, Woldorff MG, (2011) The role of stimulus salience and attentional capture across the neural hierarchy in a stop-signal task. PLOS ONE 6: e26386. doi:10.1371/journal.pone.0026386. PubMed: 22022611.
35. 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. doi:10.1016/j.neuroimage.2010.04.276. PubMed: 20452445.
36. Chikazoe J, Jimura K, Asari T, Yamashita K, Morimoto H, et al. (2009) Functional dissociation in right inferior frontal cortex during performance of go/no-go task. Cereb Cortex 19: 146-152. doi:10.1093/cercor/bhn065. PubMed: 18445602.
37. Dodds CM, Morein-Zamir S, Robbins TW, (2011) Dissociating inhibition, attention, and response control in the frontoparietal network using functional magnetic resonance imaging. Cereb Cortex 21: 1155-1165. doi:10.1093/cercor/bhq187. PubMed: 20923963.
38. Hampshire A, Chamberlain SR, Monti MM, Duncan J, Owen AM, (2010) The role of the right inferior frontal gyrus: inhibition and attentional control. Neuroimage 50: 1313-1319. doi:10.1016/j.neuroimage.2009.12.109. PubMed: 20056157.
39. Sharp DJ, Bonnelle V, De Boissezon X, Beckmann CF, James SG, et al. (2010) Distinct frontal systems for response inhibition, attentional capture, and error processing. Proc Natl Acad Sci U S A 107: 6106-6111. doi:10.1073/pnas.1000175107. PubMed: 20220100.
40. Chevrier AD, Noseworthy MD, Schachar R, (2007) Dissociation of response inhibition and performance monitoring in the stop signal task using event-related fMRI. Hum Brain Mapp 28: 1347-1358. doi:10.1002/hbm.20355. PubMed: 17274022.
41. Matthews SC, Simmons AN, Arce E, Paulus MP, (2005) Dissociation of inhibition from error processing using a parametric inhibitory task during functional magnetic resonance imaging. Neuroreport 16: 755-760. doi:10.1097/00001756-200505120-00020. PubMed: 15858420.
42. Anderson BM, Stevens MC, Meda SA, Jordan K, Calhoun VD, et al. (2011) Functional imaging of cognitive control during acute alcohol intoxication. Alcohol Clin Exp Res 35: 156-165. doi:10.1111/j.1530-0277.2010.01332.x. PubMed: 20958334.
43. Schuckit MA, Tapert S, Matthews SC, Paulus MP, Tolentino NJ, et al. (2011) fMRI differences between subjects with low and high responses to alcohol during a stop signal task. Alcohol Clin Exp Res 36: 130-140. PubMed: 22003983.
44. Easdon C, Izenberg A, Armilio ML, Yu H, Alain C, (2005) Alcohol consumption impairs stimulus- and error-related processing during a Go/No-Go Task. Brain Res. Cogn Brain Res 25: 873-883. doi:10.1016/j.cogbrainres.2005.09.009.
45. Kenemans JL, Hebly W, van den Heuvel EH, Grent TJT, (2010) Moderate alcohol disrupts a mechanism for detection of rare events in human visual cortex. J Psychopharmacol 24: 839-845. doi:10.1177/0269881108098868. PubMed: 19028837.
46. Esposito F, Pignataro G, Di Renzo G, Spinali A, Paccone A, et al. (2010) Alcohol increases spontaneous BOLD signal fluctuations in the visual network. Neuroimage 53: 534-543. doi:10.1016/j.neuroimage.2010.06.061. PubMed: 20600963.
47. Mehrabian A, Russell JA, (1978) A questionnaire measure of habitual alcohol use. Psychol Rep 43: 803-806. doi:10.2466/pr0.1978.43.3.803. PubMed: 740823.
48. Weissenborn R, Duka T, (2003) Acute alcohol effects on cognitive function in social drinkers: their relationship to drinking habits. Psychopharmacology (Berl) 165: 306-312. PubMed: 12439627.
49. Rey A, (1964) L'examen clinique en psychologie. Universitaires de France. Paris: France.
50. Patton JH, Stanford MS, Barratt ES, (1995) Factor structure of the Barratt impulsiveness scale. J Clin Psychol 51: 768-774. doi:10.1002/1097-4679(199511)51:6. PubMed: 8778124.
51. Townshend JM, Duka T, (2005) Binge drinking, cognitive performance and mood in a population of young social drinkers. Alcohol Clin Exp Res 29: 317-325. doi:10.1097/01.ALC.0000156453.05028.F5. PubMed: 15770105.
52. Fromme K, Stroot E, Kapla D, (1993) Comprehensive effects of alcohol: development and psychometric assessment of a new expectancy questionnaire. Psychol Assess 5: 7.
53. Duka T, Stephens DN, Russell C, Tasker R, (1998) Discriminative stimulus properties of low doses of ethanol in humans. Psychopharmacology (Berl) 136: 379-389. doi:10.1007/s002130050581. PubMed: 9600584.
54. Verbruggen F, Logan GD, (2009) Models of response inhibition in the stop-signal and stop-change paradigms. Neurosci Biobehav Rev 33: 647-661. doi:10.1016/j.neubiorev.2008.08.014. PubMed: 18822313.
55. Logan GD, (1994) On the ability to inhibit thought and action: A user's guide to the stop signal paradigm. In: Dagenbach D, Carr TH, eds. Inhibitory processes in attention, memory, and language. San Diego: Academic Press. pp. pp. 189-239.
56. Deichmann R, Gottfried JA, Hutton C, Turner R, (2003) Optimized EPI for fMRI studies of the orbitofrontal cortex. Neuroimage 19: 430-441. doi:10.1016/S1053-8119(03)00073-9. PubMed: 12814592.
57. Weiskopf N, Hutton C, Josephs O, Deichmann R, (2006) Optimal EPI parameters for reduction of susceptibility-induced BOLD sensitivity losses: a whole-brain analysis at 3 T and 1.5 T. NeuroImage 33: 493-504. doi:10.1016/j.neuroimage.2006.07.029. PubMed: 16959495.
58. Ashburner J, Friston KJ, (1999) Nonlinear spatial normalization using basis functions. Hum Brain Mapp 7: 254-266. doi:10.1002/(SICI)1097-0193(1999)7:4. PubMed: 10408769.
59. Friston KJ, Fletcher P, Josephs O, Holmes A, Rugg MD, et al. (1998) Event-related fMRI: characterizing differential responses. Neuroimage 7: 30-40. doi:10.1006/nimg.1997.0306. PubMed: 9500830.
60. Henson RN, Hornberger M, Rugg MD, (2005) Further dissociating the processes involved in recognition memory: an FMRI study. J Cogn Neurosci 17: 1058-1073. doi:10.1162/0898929054475208. PubMed: 16102237.
61. Penny WD, Holmes AP, Friston KJ, (2003) Random effects analysis. In: Frackowiak RSJ, Friston KJ, Frith C, Dolan R, Price CJ, eds. Human Brain Function. 2nd ed. San Diego, CA: Academic Press.
62. Nichols T, Brett M, Andersson J, Wager T, Poline JB, (2005) Valid conjunction inference with the minimum statistic. Neuroimage 25: 653-660. doi:10.1016/j.neuroimage.2004.12.005. PubMed: 15808966.
63. Green A, Straube B, Weis S, Jansen A, Willmes K, et al. (2009) Neural integration of iconic and unrelated coverbal gestures: a functional MRI study. Hum Brain Mapp 30: 3309-3324. doi:10.1002/hbm.20753. PubMed: 19350562.
64. Katanoda K, Matsuda Y, Sugishita M, (2002) A spatio-temporal regression model for the analysis of functional MRI data. NeuroImage 17: 1415-1428. doi:10.1006/nimg.2002.1209. PubMed: 12414281.
65. Ross RS, Slotnick SD, (2008) The hippocampus is preferentially associated with memory for spatial context. J Cogn Neurosci 20: 432-446. doi:10.1162/jocn.2008.20035. PubMed: 18004952.
66. Slotnick SD, Schacter DL, (2004) A sensory signature that distinguishes true from false memories. Nat Neurosci 7: 664-672. doi:10.1038/nn1252. PubMed: 15156146.
67. Duvernoy HM, (1999) The human brain: surface, blood supply, and three-dimensional anatomy. Wien NY: Springer Verlag.
68. Nikolaou K, Field M, Critchley H, Duka T, (2013) Acute Alcohol Effects on Attentional Bias are Mediated by Subcortical Areas Associated with Arousal and Salience Attribution. Neuropsychopharmacology, 38: 1365-73. PubMed: 23361162.
69. White CN, Mumford JA, Poldrack RA, (2012) Perceptual criteria in the human brain. J Neurosci 32: 16716-16724. doi:10.1523/JNEUROSCI.1744-12.2012. PubMed: 23175825.
70. Aron AR, Robbins TW, Poldrack RA, (2004) Inhibition and the right inferior frontal cortex. Trends Cogn Sci 8: 170-177. doi:10.1016/j.tics.2004.02.010. PubMed: 15050513.
71. Singer T, Critchley HD, Preuschoff K, (2009) A common role of insula in feelings, empathy and uncertainty. Trends Cogn Sci 13: 334-340. doi:10.1016/j.tics.2009.05.001. PubMed: 19643659.
72. Naqvi NH, Bechara A, (2010) The insula and drug addiction: an interoceptive view of pleasure, urges, and decision-making. Brain Struct Funct 214: 435-450. doi:10.1007/s00429-010-0268-7. PubMed: 20512364.
73. 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. doi:10.1002/hbm.21213. PubMed: 21391268.
74. Torta DM, Cauda F, (2011) Different functions in the cingulate cortex, a meta-analytic connectivity modeling study. NeuroImage 56: 2157-2172. doi:10.1016/j.neuroimage.2011.03.066. PubMed: 21459151.
75. Sano M, Wendt PE, Wirsén A, Stenberg G, Risberg J, et al. (1993) Acute effects of alcohol on regional cerebral blood flow in man. J Stud Alcohol 54: 369-376. PubMed: 8487546.
76. Volkow ND, Mullani N, Gould L, Adler SS, Guynn RW, et al. (1988) Effects of acute alcohol intoxication on cerebral blood flow measured with PET. Psychiatry Res 24: 201-209. doi:10.1016/0165-1781(88)90063-7. PubMed: 3261427.
77. Buxton RB, Uludaǧ K, Dubowitz DJ, Liu TT, (2004) Modeling the hemodynamic response to brain activation. NeuroImage 23 (Suppl 1):: S220-S233. doi:10.1016/j.neuroimage.2004.07.013. PubMed: 15501093.