Differential impairments across attentional networks in binge drinking

Lannoy, Séverine; Heeren, Alexandre; Moyaerts, Nathalie; Bruneau, Nicolas; Evrard, Salomé; Billieux, Joël; Maurage, Pierre

doi:10.1007/s00213-017-4538-4

Original Investigation
Published: 31 January 2017

Differential impairments across attentional networks in binge drinking

Séverine Lannoy¹,
Alexandre Heeren²,
Nathalie Moyaerts¹,
Nicolas Bruneau¹,
Salomé Evrard¹,
Joël Billieux¹ &
Pierre Maurage¹

Psychopharmacology volume 234, pages 1059–1068 (2017)Cite this article

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Abstract

Rationale

The cognitive deficits observed in young binge drinkers have been largely documented during the last decade. Yet, these earlier studies have mainly focused on high-level cognitive abilities (particularly memory and executive functions), and uncertainty thus still abounds regarding the integrity of less complex cognitive processes in binge drinking. This is particularly true for attentional abilities, which play a crucial role in behavior regulation and are impaired in other alcohol-related disorders.

Objectives and methods

To specify the attentional deficits associated with binge drinking, two groups of university students (40 binge drinkers and 40 matched controls) performed the Attention Network Task, a theoretically grounded test assessing three independent attentional networks: alerting, orienting, and executive control.

Results

Binge drinkers displayed preserved orienting performance but impaired alerting and executive control. Binge drinking is thus not related to a general attentional impairment but rather to specific impairments of the alerting and executive control networks.

Conclusions

These results underline that, beyond the already explored high-level deficits, binge drinking is also related to impairments for attentional abilities. In view of the role played by attentional impairments in alcohol dependence, the present data also suggest that rehabilitation programs should be developed to improve attentional abilities at the early stages of alcohol-related disorders.

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References

Abdullaev Y, Posner MI, Nunnally R, Dishion TJ (2010) Functional MRI evidence for inefficient attentional control in adolescent chronic cannabis abuse. Behav Brain Res 215:45–57. doi:10.1016/j.bbr.2010.06.023
Article PubMed Google Scholar
Archie S, Zangeneh Kazemi A, Akhtar-Danesh N (2012) Concurrent binge drinking and depression among Canadian youth: prevalence, patterns, and suicidality. Alcohol 46:165–172. doi:10.1016/j.alcohol.2011.07.001
Article PubMed Google Scholar
Babor T, Higgins-Biddle J, Saunders J, Monteiro M (2001) The alcohol use disorders identification test: guidelines for use in primary care. World Health Organization, Geneva
Google Scholar
Beck AT, Steer RA, Brown GK (1996) Beck depression inventory manual, 2nd edn. Psychological Corporation, San Antonio, TX
Google Scholar
Beck AT, Steer RA, Brown GK (1998) Beck depression inventory manual, 2nd edn. Editions du Centre de Psychologie Appliquee. French adaptation, Paris
Google Scholar
Bø R, Aker M, Billieux J, Landrø NI (2016a) Binge drinkers are fast, able to stop—but they fail to adjust. J Int Neuropsychol Soc 22:38–46. doi:10.1017/S1355617715001204
Article PubMed Google Scholar
Bø R, Billieux J, Landrø NI (2016b) Binge drinking is characterized by decisions favoring positive and discounting negative consequences. Addict Res Theory 24:499–506. doi:10.3109/16066359.2016.1174215
Bruchon-Schweitzer M, Paulhan I (1993) Adaptation francophone de l’inventaire d’anxiété Trait-Etat (Forme Y) de Spielberger. Editions du Centre de Psychologie Appliquée, Paris
Google Scholar
Cohen HL, Wang W, Porjesz B, Begleiter H (1995) Auditory P300 in young alcoholics: regional response characteristics. Alcohol Clin Exp Res 19:469–475
CAS Article PubMed Google Scholar
Cordovil De Sousa Uva M, Luminet O, Cortesi M, Constant E, Derely M, De Timary P (2010) Distinct effects of protracted withdrawal on affect, craving, selective attention and executive functions among alcohol-dependent patients. Alcohol Alcohol 45:241–246. doi:10.1093/alcalc/agq012
Article PubMed Google Scholar
Crego A, Holguín SR, Parada M, Mota N, Corral M, Cadaveira F (2009) Binge drinking affects attentional and visual working memory processing in young university students. Alcohol Clin Exp Res 33:1870–1879. doi:10.1111/j.1530-0277.2009.01025.x
Article PubMed Google Scholar
Czapla M, Simon JJ, Friederich H-C, Herpertz SC, Zimmermann P, Loeber S (2015) Is binge drinking in young adults associated with an alcohol-specific impairment of response inhibition. Eur Addict Res 21:105–113. doi:10.1159/000367939
Article PubMed Google Scholar
Enoch M-A (2006) Genetic and environmental influences on the development of alcoholism: resilience vs. risk. Ann N Y Acad Sci 1094:193–201. doi:10.1196/annals.1376.019
Article PubMed Google Scholar
Evert DL, Oscar-Berman M (2001) Selective attentional processing and the right hemisphere: effects of aging and alcoholism. Neuropsychology 15:452–461. doi:10.1037//0894-4105.15.4.452
CAS Article PubMed Google Scholar
Fan J, Mccandliss B, Sommer T, Raz A, Posner MI (2002) Testing the efficiency and independence of attentional networks. J Cogn Neurosci 14:340–347
Fan J, Mccandliss B, Fossella J, Flombaum J, Posner M (2005) The activation of attentional networks. NeuroImage 26:471–479. doi:10.1016/j.neuroimage.2005.02.004
Article PubMed Google Scholar
Fein G, Andrew C (2011) Event-related potentials during visual target detection in treatment-naïve active alcoholics: P300 and treatment-naïve alcoholics. Alcohol Clin Exp Res 35:1171–1179. doi:10.1111/j.1530-0277.2011.01450.x
Article PubMed PubMed Central Google Scholar
Fernández PJ, Campoy G, García Santos JM, Antequera MM, García-Sevilla J, Castillo A, Antúnez C, Fuentes LJ (2011) Is there a specific pattern of attention deficit in mild cognitive impairment with subcortical vascular features? Evidence from the attention network test. Dement Geriatr Cogn Disord 31:268–275. doi:10.1159/000327165
Article PubMed Google Scholar
Gache P, Michaud P, Landry U, Accietto C, Arfaoui S, Wenger O, Daeppen JB (2005) The alcohol use disorders identification test (AUDIT) as a screening tool for excessive drinking in primary care: reliability and validity of a French version. Alcohol Clin Exp Res 29:2001–2007. doi:10.1097/01.alc.0000187034.58955.64
Article PubMed Google Scholar
Goudriaan AE, Grekin ER, Sher KJ (2007) Decision making and binge drinking: a longitudinal study. Alcohol Clin Exp Res 31:928–938. doi:10.1111/j.1530-0277.2007.00378.x
Article PubMed PubMed Central Google Scholar
Goudriaan AE, Grekin ER, Sher KJ (2011) Decision making and response inhibition as predictors of heavy alcohol use: a prospective study: neurocognitive predictors of heavy alcohol use. Alcohol Clin Exp Res 35:1050–1057. doi:10.1111/j.1530-0277.2011.01437.x
Article PubMed PubMed Central Google Scholar
Hallgren K, McCrady B (2013) Interference in the alcohol Stroop task with college student binge drinkers. J Behav Health 2:112-119. doi:10.5455/jbh.20130224082728
Hartley DE, Elsabagh S, File SE (2004) Binge drinking and sex: effects on mood and cognitive function in healthy young volunteers. Pharmacol Biochem Behav 78:611–619. doi:10.1016/j.pbb.2004.04.027
CAS Article PubMed Google Scholar
Heeren A, McNally RJ (2016) An integrative network approach to social anxiety disorder: the complex dynamic interplay among attentional bias for threat, attentional control, and symptoms. J Anxiety Disord 42:95–104. doi:10.1016/j.janxdis.2016.06.009
Article PubMed Google Scholar
Heeren A, Maurage P, Perrot H, De Volder A, Renier L, Araneda R, Lacroix E, Decat M, Deggouj N, Philippot P (2014) Tinnitus specifically alters the top-down executive control sub-component of attention: evidence from the attention network task. Behav Brain Res 269:147–154. doi:10.1016/j.bbr.2014.04.043
Article PubMed Google Scholar
Heeren A, Billieux J, Philippot P, Maurage P (2015) Looking under the hood of executive function impairments in psychopathology: a commentary on “advancing understanding of executive function impairments and psychopathology: bridging the gap between clinical and cognitive approaches”. Front Psychol 6:1170. doi:10.3389/fpsyg.2015.01170
Article PubMed PubMed Central Google Scholar
Heffernan T, O’Neill T (2012) Time based prospective memory deficits associated with binge drinking: evidence from the Cambridge Prospective Memory Test (CAMPROMPT). Drug Alcohol Depend 123:207–212. doi:10.1016/j.drugalcdep.2011.11.014
Article PubMed Google Scholar
Heffernan T, Clark R, Bartholomew J, Ling J, Stephens S (2010) Does binge drinking in teenagers affect their everyday prospective memory? Drug Alcohol Depend 109:73–78. doi:10.1016/j.drugalcdep.2009.12.013
Henges AL, Marczinski CA (2012) Impulsivity and alcohol consumption in young social drinkers. Addict Behav 37:217–220. doi:10.1016/j.addbeh.2011.09.013
Article PubMed Google Scholar
Hermens DF, Lagopoulos J, Tobias-Webb J, De Regt T, Dore G, Juckes L, Latt N, Hickie IB (2013) Pathways to alcohol-induced brain impairment in young people: a review. Cortex 49:3–17. doi:10.1016/j.cortex.2012.05.021
Article PubMed Google Scholar
Kanny D, Liu Y, Brewer RD, Lu H (2013) Binge drinking—United States 2011. Natl Cent Chronic Dis Prev Health Promot 62:77–80
Google Scholar
Keehn B, Müller R-A, Townsend J (2013) Atypical attentional networks and the emergence of autism. Neurosci Biobehav Rev 37:164–183. doi:10.1016/j.neubiorev.2012.11.014
Article PubMed Google Scholar
Kessler K, Pajak KM, Harkin B, Jones B (2013) A working memory bias for alcohol-related stimuli depends on drinking score. Psychol Addict Behav 27:23–31. doi:10.1037/a0028664
Article PubMed Google Scholar
Kopera M, Wojnar M, Brower K, Glass J, Nowosad I, Gmaj B, Szelenberger W (2012) Cognitive functions in abstinent alcohol-dependent patients. Alcohol 46:665–671. doi:10.1016/j.alcohol.2012.04.005
Article PubMed Google Scholar
Maurage P, Petit G, Campanella S (2013a) Pathways to alcohol-induced brain impairment in young people: a review by Hermens et al., 2013. Cortex 49:1155–1159. doi:10.1016/j.cortex.2012.12.015
Article PubMed Google Scholar
Maurage P, Bestelmeyer PEG, Rouger J, Charest I, Belin P (2013b) Binge drinking influences the cerebral processing of vocal affective bursts in young adults. NeuroImage Clin 3:218–225. doi:10.1016/j.nicl.2013.08.010
Article PubMed PubMed Central Google Scholar
Maurage P, de Timary P, Billieux J, Collignon M, Heeren A (2014) Attentional alterations in alcohol dependence are underpinned by specific executive control deficits. Alcohol Clin Exp Res 38:2105–2112. doi:10.1111/acer.12444
Article PubMed Google Scholar
McKinney A, Coyle K, Penning R, Verster JC (2012) Next day effects of naturalistic alcohol consumption on tasks of attention: alcohol hangover and attention. Hum Psychopharmaco Clin Exp 27:587–594. doi:10.1002/hup.2268
Article Google Scholar
Mota N, Parada M, Crego A, Doallo S, Caamaño-Isorna F, Rodríguez Holguín S, Cadaveira F, Corral M (2013) Binge drinking trajectory and neuropsychological functioning among university students: a longitudinal study. Drug Alcohol Depend 133:108–114. doi:10.1016/j.drugalcdep.2013.05.024
Article PubMed Google Scholar
Nixon SJ, Lawton-Craddock A, Tivis R, Ceballos N (2007) Nicotine’s effects on attentional efficiency in alcoholics. Alcohol Clin Exp Res 31:2083–2091. doi:10.1111/j.1530-0277.2007.00526.x
CAS Article PubMed Google Scholar
Opgen-Rhein C, Neuhaus AH, Urbanek C, Hahn E, Sander T, Dettling M (2008) Executive attention in schizophrenic males and the impact of COMT Val108/158Met genotype on performance on the attention network test. Schizophr Bull 34:1231–1239. doi:10.1093/schbul/sbm155
Article PubMed PubMed Central Google Scholar
Oscar-Berman M, Marinkovic K (2003) Alcoholism and the brain: an overview. Alcohol Res Health 27:125–133
PubMed Google Scholar
Pacheco-Unguetti AP, Acosta A, Marqués E, Lupiáñez J (2011) Alterations of the attentional networks in patients with anxiety disorders. J Anxiety Disord 2:888–895. doi:10.1016/j.janxdis.2011.04.010
Article Google Scholar
Parada M, Corral M, Mota N, Crego A, Rodríguez Holguín S, Cadaveira F (2012) Executive functioning and alcohol binge drinking in university students. Addict Behav 37:167–172. doi:10.1016/j.addbeh.2011.09.015
Article PubMed Google Scholar
Petersen SE, Posner MI (2012) The attention system of the human brain: 20 years after. Annu Rev Neurosci 35:73–89. doi:10.1146/annurev-neuro-062111-150525
CAS Article PubMed PubMed Central Google Scholar
Petit G, Kornreich C, Maurage P, Noël X, Letesson C, Verbanck P, Campanella S (2012) Early attentional modulation by alcohol-related cues in young binge drinkers: an event-related potentials study. Clin Neurophysiol 123:925–936. doi:10.1016/j.clinph.2011.10.042
Article PubMed Google Scholar
Pfefferbaum A, Desmond JE, Galloway C, Menon V, Glover GH, Sullivan EV (2001) Reorganization of frontal systems used by alcoholics for spatial working memory: an fMRI study. NeuroImage 14:7–20. doi:10.1006/nimg.2001.0785
CAS Article PubMed Google Scholar
Posner MI, Petersen SE (1990) The attention systems of the human brain. Annu Rev Neurosci 13:25–42
CAS Article PubMed Google Scholar
Ramachandran G, Porjesz B, Begleiter H, Litke A (1996) A simple auditory oddball task in young adult males at high risk for alcoholism. Alcohol Clin Exp Res 20:9–15
CAS Article PubMed Google Scholar
Roberts W, Miller MA, Weafer J, Fillmore MT (2014) Heavy drinking and the role of inhibitory control of attention. Exp Clin Psychopharmacol 22:133–140. doi:10.1037/a0035317
Article PubMed PubMed Central Google Scholar
Rupp CI, Kemmler G, Kurz M, Hinterhuber H, Wolfgang Fleischhacker W (2012) Cognitive remediation therapy during treatment for alcohol dependence. J Stud Alcohol Drugs 73:625–634
Article PubMed Google Scholar
Sanhueza C, García-Moreno LM, Expósito J (2011) Weekend alcoholism in youth and neurocognitive aging. Psicothema 23:209–214
PubMed Google Scholar
Scaife JC, Duka T (2009) Behavioural measures of frontal lobe function in a population of young social drinkers with binge drinking pattern. Pharmacol Biochem Behav 93:354–362. doi:10.1016/j.pbb.2009.05.015
CAS Article PubMed Google Scholar
Schulte T, Müller-Oehring EM, Strasburger H, Warzel H, Sabel BA (2001) Acute effects of alcohol on divided and covert attention in men. Psychopharmacology 154:61–69. doi:10.1007/s002130000603
CAS Article PubMed Google Scholar
Schulte T, Müller-Oehring EM, Sullivan EV, Pfefferbaum A (2012) White matter fiber compromise contributes differentially to attention and emotion processing impairment in alcoholism, HIV-infection, and their comorbidity. Neuropsychologia 50:2812–2822. doi:10.1016/j.neuropsychologia.2012.07.042
CAS Article PubMed PubMed Central Google Scholar
Schweinsburg AD, McQueeny T, Nagel BJ, Eyler LT, Tapert SF (2010) A preliminary study of functional magnetic resonance imaging response during verbal encoding among adolescent binge drinkers. Alcohol 44:111–117. doi:10.1016/j.alcohol.2009.09.032
Article PubMed PubMed Central Google Scholar
Schweinsburg AD, Schweinsburg BC, Nagel BJ, Eyler LT, Tapert SF (2011) Neural correlates of verbal learning in adolescent alcohol and marijuana users: fMRI in adolescent users. Addiction 106:564–573. doi:10.1111/j.1360-0443.2010.03197.x
Article PubMed Google Scholar
Serino A, Ciaramelli E, Santantonio AD, Malagù S, Servadei F, Làdavas E (2007) A pilot study for rehabilitation of central executive deficits after traumatic brain injury. Brain Inj 21:11–19. doi:10.1080/02699050601151811
Article PubMed Google Scholar
Spielberger DC, Gorsuch RL, Lushene R, Vagg PR, Jacobs GA (1983) Manual for the state-trait anxiety inventory. Consulting Psychology Press, Palo Alto
Google Scholar
Squeglia LM, Schweinsburg AD, Pulido C, Tapert SF (2011) Adolescent binge drinking linked to abnormal spatial working memory brain activation: differential gender effects: adolescent binge drinking. Alcohol Clin Exp Res 35:1831–1841. doi:10.1111/j.1530-0277.2011.01527.x
Article PubMed PubMed Central Google Scholar
Squeglia LM, Jacobus J, Nguyen-Louie TT, Tapert SF (2014) Inhibition during early adolescence predicts alcohol and marijuana use by late adolescence. Neuropsychology 28:782–790. doi:10.1037/neu0000083
Article PubMed PubMed Central Google Scholar
Squeglia LM, Tapert SF, Sullivan EV, Jacobus J, Meloy MJ, Rohlfing T, Pfefferbaum A (2015) Brain development in heavy-drinking adolescents. Am J Psychiatry 172:531–542
Article PubMed PubMed Central Google Scholar
Sullivan EV, Deshmukh A, Desmond JE, Lim KO, Pfefferbaum A (2000) Cerebellar volume decline in normal aging, alcoholism, and Korsakoff’s syndrome: relation to ataxia. Neuropsychology 14:341–352. doi:10.1037//0894-4105.14.3.341
CAS Article PubMed Google Scholar
Tedstone D, Coyle K (2004) Cognitive impairments in sober alcoholics: performance on selective and divided attention tasks. Drug Alcohol Depend 75:277–286. doi:10.1016/j.drugalcdep.2004.03.005
Article PubMed Google Scholar
Thimm M, Fink GR, Küst J, Karbe H, Sturm W (2006) Impact of alertness training on spatial neglect: a behavioural and fMRI study. Neuropsychologia 44:1230–1246. doi:10.1016/j.neuropsychologia.2005.09.008
CAS Article PubMed Google Scholar
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
Article PubMed Google Scholar
Townshend JM, Kambouropoulos N, Griffin A, Hunt FJ, Milani RM (2014) Binge drinking, reflection impulsivity, and unplanned sexual behavior: impaired decision-making in young social drinkers. Alcohol Clin Exp Res 38:1143–1150. doi:10.1111/acer.12333
Article PubMed Google Scholar
Weafer J, Fillmore MT (2015) Alcohol-related cues potentiate alcohol impairment of behavioral control in drinkers. Psychol Addict Behav 29:290–299. doi:10.1037/adb0000013
Article PubMed Google Scholar
Wester AE, Verster JC, Volkerts ER, Bocker KB, Kenemans JL (2010) Effects of alcohol on attention orienting and dual-task performance during simulated driving: an event-related potential study. J Psychopharmacol 24:1333–1348. doi:10.1177/0269881109348168
CAS Article PubMed Google Scholar
Woicik PA, Moeller SJ, Alia-Klein N, Maloney T, Lukasik TM, Yeliosof O, Wang G-J, Volkow ND, Goldstein RZ (2009) The neuropsychology of cocaine addiction: recent cocaine use masks impairment. Neuropsychopharmacology 34:1112–1122
CAS Article PubMed Google Scholar

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Acknowledgements

This research has been supported by the Belgian Fund for Scientific Research, the European Commission for Research on the problematic usage of information and communication technology [Grant ID: FP7-PEOPLE-2013-IEF-627999], and the “Fondation pour la Recherche en Alcoologie (FRA)”. This research also received the support from a postdoctoral fellowship in clinical neuroscience from the “Helaers Foundation” and the “WBI World Excellence Grant: Competitive Cluster in Life Sciences—BIOWIN” (sub/2015/228106243177), both awarded to Alexandre Heeren.

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Laboratory for Experimental Psychopathology, Psychological Science Research Institute, Université Catholique de Louvain, 10 Place du Cardinal Mercier, B-1348, Louvain-la-Neuve, Belgium
Séverine Lannoy, Nathalie Moyaerts, Nicolas Bruneau, Salomé Evrard, Joël Billieux & Pierre Maurage
Department of Psychology, Harvard University, 1230 William James Hall, 33 Kirkland Street, Cambridge, MA, 02138, USA
Alexandre Heeren

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Séverine Lannoy
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Alexandre Heeren
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Nathalie Moyaerts
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Nicolas Bruneau
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Salomé Evrard
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Joël Billieux
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Pierre Maurage
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Correspondence to Pierre Maurage.

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Lannoy, S., Heeren, A., Moyaerts, N. et al. Differential impairments across attentional networks in binge drinking. Psychopharmacology 234, 1059–1068 (2017). https://doi.org/10.1007/s00213-017-4538-4

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Received: 26 August 2016
Accepted: 16 January 2017
Published: 31 January 2017
Issue Date: April 2017
DOI: https://doi.org/10.1007/s00213-017-4538-4

Keywords

Binge drinking
Alcohol dependence
Attentional abilities
Alerting
Orienting
Executive control