Skip to main content
SpringerLink
Log in

Moderating effect of working memory capacity on acute alcohol effects on BOLD response during inhibition and error monitoring in male heavy drinkers

  • Original Investigation
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

Rationale

While alcohol intoxication is known to increase disinhibited behavior, the degree to which disinhibition occurs appears to depend on a number of factors including executive functioning ability. However, the neural mechanisms by which individual differences in executive functioning lead to variable degrees of disinhibition remain unclear.

Objectives

The aim of the current study was to examine the neural mechanisms by which individual differences in working memory (WM) capacity moderate alcohol-induced disinhibition.

Methods

Seventeen heavy-drinking males participated in a within-subjects design in which two sessions were completed: an alcohol session (.82 g/kg) and a control session. Participants completed a go/no-go task while undergoing functional magnetic resonance imaging (fMRI) after ingestion of the control or alcohol beverage. WM capacity was measured using an operation span task.

Results

Significant interactions of session and WM capacity emerged in contrasts examining successful response inhibition within superior temporal gyrus and unsuccessful inhibition in regions within the default mode network. In all cases, individuals with low WM capacity demonstrated a relative decrease in blood oxygen level-dependent (BOLD) response during the alcohol compared to control session, whereas the high-WM-capacity group demonstrated relative increases in BOLD response in the alcohol compared to control session.

Conclusions

Low WM capacity appears to be associated with decreased neural response to signals indicating a need for behavioral control, an effect that may lead to increased difficulty with inhibiting responses and increased negative consequences from alcohol intoxication.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Anderson BM, Stevens MC, Meda SA 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

  • Aron A (2007) The neural basis of inhibition in cognitive control. Neuroscientist 13:214–228

    Article  PubMed  Google Scholar 

  • Aron A, Robbins T, Poldrack R (2004) Inhibition and the right inferior frontal cortex. Trends Cogn Sci 8:170–177

    Article  PubMed  Google Scholar 

  • Babor T, Higgins-Biddle JC, Saunders JB, Monteiro MG (2001) AUDIT: The Alcohol Use Disorders Identification Test: guidelines for use in primary care. World Health Organization: Geneva, Switzerland 

  • Bartholow BD, Henry EA, Lust SA et al (2012) Alcohol effects on performance monitoring and adjustment: affect modulation and impairment of evaluative cognitive control. J Abnorm Psychol 121:173–186. doi:10.1037/a0023664

    Article  PubMed Central  PubMed  Google Scholar 

  • Bjork JM, Hommer DW, Grant SJ, Danube C (2004) Impulsivity in abstinent alcohol-dependent patients: relation to control subjects and type 1-/type 2-like traits. Alcohol 34:133–50

    Article  PubMed  Google Scholar 

  • Charlet K, Beck A, Jorde A et al (2013) Increased neural activity during high working memory load predicts low relapse risk in alcohol dependence. Addict Biol. doi:10.1111/adb.12103

    Google Scholar 

  • Chevrier A, Schachar RJ (2010) Error detection in the stop signal task. Neuroimage 53:664–673. doi:10.1016/j.neuroimage.2010.06.056

    Article  PubMed  Google Scholar 

  • Claus ED, Ewing SWF, Filbey FM et al (2011) Identifying neurobiological phenotypes associated with alcohol use disorder severity. Neuropsychopharmacology 36:2086–2096. doi:10.1038/npp.2011.99

    Article  PubMed Central  PubMed  Google Scholar 

  • Claus ED, Feldstein Ewing SW, Filbey FM, Hutchison KE (2013) Behavioral control in alcohol use disorders: relationships with severity. J Stud Alcohol Drugs 74:141–151

    PubMed Central  PubMed  Google Scholar 

  • Curtin JJ, Fairchild BA (2003) Alcohol and cognitive control: implications for regulation of behavior during response conflict. J Abnorm Psychol 112:424–436. doi:10.1037/0021-843X.112.3.424

    Article  PubMed  Google Scholar 

  • Curtin J, Patrick C, Lang A et al (2001) Alcohol affects emotion through cognition. Psychol Sci 12:527–531

    Article  CAS  PubMed  Google Scholar 

  • Deichmann R, Gottfried J, Hutton C, Turner R (2003) Optimized EPI for fMRI studies of the orbitofrontal cortex. Neuroimage 19:430–441

    Article  CAS  PubMed  Google Scholar 

  • Easdon CM, Vogel Sprott M (2000) Alcohol and behavioral control: impaired response inhibition and flexibility in social drinkers. Exp Clin Psychopharmacol 8:387

    Article  CAS  PubMed  Google Scholar 

  • Easdon C, Izenberg A, Armilio ML et al (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

    Article  CAS  PubMed  Google Scholar 

  • Eichele T, Calhoun VD, Debener S (2009) Mining EEG–fMRI using independent component analysis. Int J Psychophysiol 73:53–61. doi:10.1016/j.ijpsycho.2008.12.018

    Article  PubMed Central  PubMed  Google Scholar 

  • Euser AS, Meel CS, Snelleman M, Franken IHA (2011) Acute effects of alcohol on feedback processing and outcome evaluation during risky decision-making: an ERP study. Psychopharmacology 217(1):111–25

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Field M, Wiers RW, Christiansen P et al (2010) Acute alcohol effects on inhibitory control and implicit cognition: implications for loss of control over drinking. Alcohol Clin Exp Res 34:1346–1352. doi:10.1111/j.1530-0277.2010.01218.x

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fillmore MT, Blackburn J (2002) Compensating for alcohol-induced impairment: alcohol expectancies and behavioral disinhibition. J Stud Alcohol 63:237–246

    PubMed  Google Scholar 

  • Fillmore MT, Rush CR (2006) Polydrug abusers display impaired discrimination-reversal learning in a model of behavioural control. J Psychopharmacol 20:24–32. doi:10.1177/0269881105057000

    Article  PubMed  Google Scholar 

  • Fillmore M, Vogel Sprott M, Gavrilescu D (1999) Alcohol effects on intentional behavior: dissociating controlled and automatic influences. Exp Clin Psychopharmacol 7:372–378

    Article  CAS  PubMed  Google Scholar 

  • Fillmore M, Blackburn J, Harrison E (2008) Acute disinhibiting effects of alcohol as a factor in risky driving behavior. Drug Alcohol Depend 95:97–106

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Finn P, Hall J (2004) Cognitive ability and risk for alcoholism: short-term memory capacity and intelligence moderate personality risk for alcohol problems. J Abnorm Psychol 113:569–581

    Article  PubMed  Google Scholar 

  • Finn P, Justus A, Mazas C, Steinmetz J (1999) Working memory, executive processes and the effects of alcohol on Go/No-Go learning: testing a model of behavioral regulation and impulsivity. Psychopharmacology 146:465–472

    Article  CAS  PubMed  Google Scholar 

  • Gan G, Guevara A, Marxen M, et al. (2014) Alcohol-induced impairment of inhibitory controlis linked to attenuated brain responses in rightfronto-temporal cortex. Biol Psychiatry 1–10. doi: 10.1016/j.biopsych.2013.12.017

  • Gehring WJ, Fencsik DE (2001) Functions of the medial frontal cortex in the processing of conflict and errors. J Neurosci 21:9430–9437

    CAS  PubMed  Google Scholar 

  • George WH, Stoner SA (2000) Understanding acute alcohol effects on sexual behavior. Annu Rev Sex Res 11:92–124

    CAS  PubMed  Google Scholar 

  • George WH, Davis KC, Norris J, Heiman JR, Stoner SA, Schacht RL, Hendershot CS, Kajumulo KF (2009) Indirect effects of acute alcohol intoxication on sexual risk-taking: the roles of subjective and physiological sexual arousal. Arch Sex Behav 38(4):498–415

    Article  PubMed Central  PubMed  Google Scholar 

  • Giancola PR (2000) Executive functioning: a conceptual framework for alcohol-related aggression. Exp Clin Psychopharmacol 8:576

    Article  CAS  PubMed  Google Scholar 

  • Giancola PR, Corman MD (2007) Alcohol and aggression: a test of the attention-allocation model. Psychol Sci 18:649–655. doi:10.1111/j.1467-9280.2007.01953.x

    Article  PubMed  Google Scholar 

  • Giancola PR, Zeichner A (1997) The biphasic effects of alcohol on human physical aggression. J Abnorm Psychol 106:598–607

    Article  CAS  PubMed  Google Scholar 

  • Gottlieb J, Snyder LH (2010) Spatial and non-spatial functions of the parietal cortex. Curr Opin Neurobiol 20:731–740. doi:10.1016/j.conb.2010.09.015

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gundersen H, Specht K, Grüner R, Ersland L, Hugdahl K (2008) Separating the effects of alcohol and expectancy on brain activation: an fMRI working memory study. Neuroimage 42:1587–1596

    Article  PubMed  Google Scholar 

  • Hester R, Nestor L, Garavan H (2009) Impaired error awareness and anterior cingulate cortex hypoactivity in chronic cannabis users. Neuropsychopharmacology 34:2450–2458

    Article  PubMed Central  PubMed  Google Scholar 

  • Hirose S, Chikazoe J, Watanabe T et al (2012) Efficiency of go/no-go task performance implemented in the left hemisphere. J Neurosci 32:9059–9065. doi:10.1523/JNEUROSCI.0540-12.2012

    Article  CAS  PubMed  Google Scholar 

  • Ito TA, Miller N, Pollock VE (1996) Alcohol and aggression: a meta-analysis on the moderating effects of inhibitory cues, triggering events, and self-focused attention. Psychol Bull 120:60

    Article  CAS  PubMed  Google Scholar 

  • Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17:825–841

    Article  PubMed  Google Scholar 

  • Kareken DA, Dzemidzic M, Wetherill L et al (2013) Family history of alcoholism interacts with alcohol to affect brain regions involved in behavioral inhibition. Psychopharmacology 228:335–345. doi:10.1007/s00213-013-3038-4

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kaufman JN, Ross TJ, Stein EA, Garavan H (2003) Cingulate hypoactivity in cocaine users during a GO-NOGO task as revealed by event-related functional magnetic resonance imaging. J Neurosci 23:7839–7843

    CAS  PubMed  Google Scholar 

  • Kokotailo PK, Egan J, Gangnon R et al (2006) Validity of the alcohol use disorders identification test in college students. Alcohol Clin Exp Res 28:914–920. doi:10.1097/01.ALC.0000128239.87611.F5

    Article  Google Scholar 

  • Li C-SR, Yan P, Bergquist KL, Sinha R (2007) Greater activation of the “default” brain regions predicts stop signal errors. Neuroimage 38:640–648. doi:10.1016/j.neuroimage.2007.07.021

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Marczinski C, Fillmore M (2005a) Alcohol increases reliance on cues that signal acts of control. Exp Clin Psychopharmacol 13:15–24. doi:10.1037/1064-1297.13.1.15

    Article  PubMed  Google Scholar 

  • Marczinski C, Fillmore M (2005b) Compensating for alcohol-induced impairment of control: effects on inhibition and activation of behavior. Psychopharmacology 181:337–346

    Article  CAS  PubMed  Google Scholar 

  • Marczinski CA, Combs SW, Fillmore MT (2007) Increased sensitivity to the disinhibiting effects of alcohol in binge drinkers. Psychol Addict Behav 21:346–354. doi:10.1037/0893-164X.21.3.346

    Article  PubMed  Google Scholar 

  • Marinkovic K, Rickenbacher E, Azma S, Artsy E (2011) 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Marinkovic K, Rickenbacher E, Azma S (2012) Effects of alcohol intoxication on response conflict in a flanker task. J Addict Res Ther S3:002. doi:10.4172/2155-6105.S3-002

    Google Scholar 

  • Marinkovic K, Rickenbacher E, Azma S et al (2013) Effects of acute alcohol intoxication on saccadic conflict and error processing. Psychopharmacology 230:487–497. doi:10.1007/s00213-013-3173-y

    Article  CAS  PubMed  Google Scholar 

  • Martin C, Sayette M (1993) Experimental-design in alcohol administration research - limitations and alternatives in the manipulation of dosage-set. J Stud Alcohol 54:750–761

    CAS  PubMed  Google Scholar 

  • Mulvihill L, Skilling T, Vogel Sprott M (1997) Alcohol and the ability to inhibit behavior in men and women. J Stud Alcohol 58:600–605

    CAS  PubMed  Google Scholar 

  • Nelson LD, Patrick CJ, Collins P et al (2011) Alcohol impairs brain reactivity to explicit loss feedback. Psychopharmacology 218:419–428. doi:10.1007/s00213-011-2323-3

    Article  CAS  PubMed  Google Scholar 

  • O’Connor S, Morzorati S, Christian J, Li T (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

    Article  PubMed  Google Scholar 

  • O’Connor S, Ramchandani V, Li T (2000) PBPK modeling as a basis for achieving a steady BrAC of 60 +/- 5 mg% within ten minutes. Alcohol Clin Exp Res 24:426–427

    Article  PubMed  Google Scholar 

  • Poulos CX, Parker JL, Le DA (1998) Increased impulsivity after injected alcohol predicts later alcohol consumption in rats: evidence for “loss-of-control drinking” and marked individual differences. Behav Neurosci 112:1247–1257

    Article  CAS  PubMed  Google Scholar 

  • Raichle M, MacLeod A, Snyder A et al (2001) A default mode of brain function. Proc Natl Acad Sci U S A 98:676–682

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ramchandani V, Bolane J, Li T, O’Connor S (1999) A physiologically-based pharmacokinetic (PBPK) model for alcohol facilitates rapid BrAC clamping. Alcohol Clin Exp Res 23:617–623

    Article  CAS  PubMed  Google Scholar 

  • Rehm J, Shield KD, Joharchi N, Shuper PA (2011) Alcohol consumption and the intention to engage in unprotected sex: systematic review and meta-analysis of experimental studies. Addiction 107:51–59. doi:10.1111/j.1360-0443.2011.03621.x

    Article  Google Scholar 

  • Ridderinkhof KR, de Vlugt Y, Bramlage A et al (2002) Alcohol consumption impairs detection of performance errors in mediofrontal cortex. Science 298:2209–2211. doi:10.1126/science.1076929

  • Schacht RL, Stoner SA, George WH, Norris J (2010) Idiographically determined versus standard absorption periods in alcohol administration studies. Alcohol Clin Exp Res 34:925–927. doi:10.1111/j.1530-0277.2010.01165.x

    Article  PubMed Central  PubMed  Google Scholar 

  • Schuckit MA, Tapert S, Matthews SC 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. doi:10.1111/j.1530-0277.2011.01590.x

    Article  PubMed Central  PubMed  Google Scholar 

  • Simmonds DJ, Pekar JJ, Mostofsky SH (2008) Meta-analysis of go/no-go tasks demonstrating that fMRI activation associated with response inhibition is task-dependent. Neuropsychologia 46:224–232. doi:10.1016/j.neuropsychologia.2007.07.015

    Article  PubMed Central  PubMed  Google Scholar 

  • Smith SM (2002) Fast robust automated brain extraction. Hum Brain Mapp 17:143–155. doi:10.1002/hbm.10062

    Article  PubMed  Google Scholar 

  • Smith S, Jenkinson M, Woolrich M et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl 1):S208–19

    Article  PubMed  Google Scholar 

  • Sobell L, Sobell M (1992) Timeline follow-back: a technique for assessing self-reported alcohol consumption. In: Litten R, Allen J (eds) Measuring alcohol consumption: psychosocial and biochemical methods. Humana, New York, p 41–72

  • Steele CM, Josephs RA (1990) Alcohol myopia. Its prized and dangerous effects. Am Psychol 45:921–933

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1016/j.neuroimage.2011.02.070

    Article  PubMed  Google Scholar 

  • Taylor SF, Martis B, Fitzgerald KD et al (2006) Medial frontal cortex activity and loss-related responses to errors. J Neurosci 26:4063–4070. doi:10.1523/JNEUROSCI.4709-05.2006

    Article  CAS  PubMed  Google Scholar 

  • Unsworth N, Redick TS, Heitz RP et al (2009) Complex working memory span tasks and higher-order cognition: a latent-variable analysis of the relationship between processing and storage. Memory 17:635–654. doi:10.1080/09658210902998047

    Article  PubMed  Google Scholar 

  • Vogel Sprott M, Easdon C, Fillmore M et al (2001) Alcohol and behavioral control: cognitive and neural mechanisms. Alcohol Clin Exp Res 25:117–121

    Article  CAS  PubMed  Google Scholar 

  • Weafer J, Fillmore MT (2008) Individual differences in acute alcohol impairment of inhibitory control predict ad libitum alcohol consumption. Psychopharmacology 201:315–324. doi:10.1007/s00213-008-1284-7

    Article  CAS  PubMed  Google Scholar 

  • Woolrich M, Behrens T, Beckmann C et al (2004) Multilevel linear modelling for FMRI group analysis using Bayesian inference. Neuroimage 21:1732–1747

    Article  PubMed  Google Scholar 

Download references

Funding

The study was supported, in part, by R21AA020304. NIAAA did not have any input on the design, collection, analysis, or interpretation of the data presented here. The authors maintain full control of all primary data and agree to review by the journal if requested.

Conflict of interest

The authors report no conflicts of interest.

Author information

Authors and Affiliations

  1. Mind Research Network and Lovelace Biomedical and Environmental Research Institute, 1101 Yale Blvd NE, Albuquerque, NM, 87106, USA

    Eric D. Claus

  2. Campbell Family Mental Health Research Institute, Centre for Addiction and Mental Health, Toronto, Ontario, Canada

    Christian S. Hendershot

  3. Department of Psychiatry, University of Toronto, Toronto, Ontario, Canada

    Christian S. Hendershot

Authors
  1. Eric D. Claus
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christian S. Hendershot
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eric D. Claus.

Additional information

Author note

The authors would like to thank Jesse Castillo and Kent Hutchison for assisting with the study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Claus, E.D., Hendershot, C.S. Moderating effect of working memory capacity on acute alcohol effects on BOLD response during inhibition and error monitoring in male heavy drinkers. Psychopharmacology 232, 765–776 (2015). https://doi.org/10.1007/s00213-014-3711-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-014-3711-2

Keywords

Search

Navigation