Increased Cortical Activity in Binge Drinkers during Working Memory Task: A Preliminary Assessment through a Functional Magnetic Resonance Imaging Study

Background Cerebral dysfunction is a common feature of both chronic alcohol abusers and binge drinkers. Here, we aimed to study whether, at equated behavioral performance levels, binge drinkers exhibited increased neural activity while performing simple cognitive tasks. Methods Thirty-two participants (16 binge drinkers and 16 matched controls) were scanned using functional magnetic resonance imaging (fMRI) while performing an n-back working memory task. In the control zero-back (N0) condition, subjects were required to press a button with the right hand when the number “2″ was displayed. In the two-back (N2) condition, subjects had to press a button when the displayed number was identical to the number shown two trials before. Results fMRI analyses revealed higher bilateral activity in the pre-supplementary motor area in binge drinkers than matched controls, even though behavioral performances were similar. Moreover, binge drinkers showed specific positive correlations between the number of alcohol doses consumed per occasion and higher activity in the dorsomedial prefrontal cortex, as well as between the number of drinking occasions per week and higher activity in cerebellum, thalamus and insula while performing the N2 memory task. Conclusions Binge alcohol consumption leads to possible compensatory cerebral changes in binge drinkers that facilitate normal behavioral performance. These changes in cerebral responses may be considered as vulnerability factors for developing adult substance use disorders.

[1]  R. Cabeza Hemispheric asymmetry reduction in older adults: the HAROLD model. , 2002, Psychology and aging.

[2]  O. Aasland,et al.  Development of the Alcohol Use Disorders Identification Test (AUDIT): WHO Collaborative Project on Early Detection of Persons with Harmful Alcohol Consumption--II. , 1993, Addiction.

[3]  F. Crews,et al.  Alcoholic neurobiology: changes in dependence and recovery. , 2005, Alcoholism, clinical and experimental research.

[4]  E. Rimm,et al.  Roles of drinking pattern and type of alcohol consumed in coronary heart disease in men. , 2003, The New England journal of medicine.

[5]  Hans-Jochen Heinze,et al.  Preceding attention and the dorsomedial prefrontal cortex: Process specificity versus domain dependence , 2009, Human brain mapping.

[6]  Ting-kai Li,et al.  Is there a future for quantifying drinking in the diagnosis, treatment, and prevention of alcohol use disorders? , 2006, Alcohol and alcoholism.

[7]  Karl J. Friston 22 – Statistics I: Experimental Design and Statistical Parametric Mapping , 2002 .

[8]  R. Friend,et al.  Measurement of social-evaluative anxiety. , 1969, Journal of consulting and clinical psychology.

[9]  Charles D. Spielberger,et al.  State-Trait Anxiety Inventory for Adults , 2012 .

[10]  K. Jennison,et al.  The Short‐Term Effects and Unintended Long‐Term Consequences of Binge Drinking in College: A 10‐Year Follow‐Up Study , 2004, The American journal of drug and alcohol abuse.

[11]  Karl J. Friston Introduction Experimental design and Statistical Parametric Mapping , 2003 .

[12]  P. Philippot,et al.  Latent deleterious effects of binge drinking over a short period of time revealed only by electrophysiological measures. , 2009, Journal of psychiatry & neuroscience : JPN.

[13]  C. Spielberger,et al.  Manual for the State-Trait Anxiety Inventory , 1970 .

[14]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[15]  K. Zilles,et al.  A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis , 2010, Brain Structure and Function.

[16]  S. Tapert,et al.  Adolescent binge drinking linked to abnormal spatial working memory brain activation: differential gender effects. , 2011, Alcoholism, clinical and experimental research.

[17]  A. Damasio,et al.  Deciding Advantageously Before Knowing the Advantageous Strategy , 1997, Science.

[18]  Michael B. Miller,et al.  The principled control of false positives in neuroimaging. , 2009, Social cognitive and affective neuroscience.

[19]  John Polich,et al.  Binge Drinking Effects on EEG in Young Adult Humans , 2010, International journal of environmental research and public health.

[20]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[21]  Karl J. Friston,et al.  Human Brain Function , 1997 .

[22]  P. Philippot,et al.  Cerebral effects of binge drinking: Respective influences of global alcohol intake and consumption pattern , 2012, Clinical Neurophysiology.

[23]  Ana M. Blanco,et al.  Intermittent ethanol exposure induces inflammatory brain damage and causes long‐term behavioural alterations in adolescent rats , 2007, The European journal of neuroscience.

[24]  F. Cadaveira,et al.  Reduced anterior prefrontal cortex activation in young binge drinkers during a visual working memory task. , 2010, Drug and alcohol dependence.

[25]  E. Sacanella,et al.  Brain impairment in well‐nourished chronic alcoholics is related to ethanol intake , 1997, Annals of neurology.

[26]  M. Orlando,et al.  Patterns and correlates of binge drinking trajectories from early adolescence to young adulthood. , 2003, Health psychology : official journal of the Division of Health Psychology, American Psychological Association.

[27]  D. Jean,et al.  Random-effect analysis. , 2014 .

[28]  G. Patton,et al.  Association of adolescent symptoms of depression and anxiety with alcohol use disorders in young adulthood: findings from the Victorian Adolescent Health Cohort Study , 2011, The Medical journal of Australia.

[29]  I. Franken,et al.  Intentional Modulation of the Late Positive Potential in Response to Smoking Cues by Cognitive Strategies in Smokers , 2011, PloS one.

[30]  B. Grant,et al.  Patterns of DSM-IV alcohol abuse and dependence criteria among adolescents and adults: results from the 2001 National Household Survey on Drug Abuse. , 2005, Alcoholism, clinical and experimental research.

[31]  M. Zvolensky,et al.  Adverse consequences of student drinking: the role of sex, social anxiety, drinking motives. , 2011, Addictive behaviors.

[32]  Latent deleterious effects of binge drinking over a short period of time revealed by electrophysiological measures only. , 2009, NeuroImage.

[33]  G. Patton,et al.  Association of adolescent symptoms of depression and anxiety with daily smoking and nicotine dependence in young adulthood: findings from a 10-year longitudinal study. , 2010, Addiction.

[34]  T. Shallice,et al.  Right prefrontal cortex and episodic memory retrieval: a functional MRI test of the monitoring hypothesis. , 1999, Brain : a journal of neurology.

[35]  Sang Won Seo,et al.  Defining functional SMA and pre-SMA subregions in human MFC using resting state fMRI: Functional connectivity-based parcellation method , 2010, NeuroImage.

[36]  A. Bechara,et al.  Abnormal affective decision making revealed in adolescent binge drinkers using a functional magnetic resonance imaging study. , 2013, Psychology of addictive behaviors : journal of the Society of Psychologists in Addictive Behaviors.

[37]  Lisa T. Eyler,et al.  Neural correlates of verbal learning in adolescent alcohol and marijuana users. , 2011, Addiction.

[38]  I. Hickie,et al.  Pathways to alcohol-induced brain impairment in young people: A review , 2013, Cortex.

[39]  Edward E. Smith,et al.  Verbal Working Memory Load Affects Regional Brain Activation as Measured by PET , 1997, Journal of Cognitive Neuroscience.

[40]  A. Bechara,et al.  A neurocognitive approach to understanding the neurobiology of addiction , 2013, Current Opinion in Neurobiology.

[41]  P. Goldman-Rakic Working memory dysfunction in schizophrenia. , 1994, The Journal of neuropsychiatry and clinical neurosciences.

[42]  M. Enoch,et al.  Genetic and Environmental Influences on the Development of Alcoholism , 2006, Annals of the New York Academy of Sciences.

[43]  C. Spielberger Manual for the State-Trait Anxiety Inventory (STAI) (Form Y , 1983 .

[44]  C. Whitty Cerebral atrophy in young cannabis smokers. , 1971, Lancet.

[45]  G. H. Hall Effects of nicotine and tobacco smoke on the electrical activity of the cerebral cortex and olfactory bulb , 1970, British journal of pharmacology.

[46]  L L Chao,et al.  Effects of heavy drinking, binge drinking, and family history of alcoholism on regional brain metabolites. , 2004, Alcoholism, clinical and experimental research.

[47]  D. Gitelman,et al.  Neuroanatomic Overlap of Working Memory and Spatial Attention Networks: A Functional MRI Comparison within Subjects , 1999, NeuroImage.

[48]  Fernando Cadaveira,et al.  Increased amplitude of P3 event-related potential in young binge drinkers. , 2012, Alcohol.

[49]  Chengye Ji,et al.  Relationship of binge drinking and other health-compromising behaviors among urban adolescents in China. , 2006, The Journal of adolescent health : official publication of the Society for Adolescent Medicine.

[50]  Anthony D Wagner,et al.  Executive Control during Episodic Retrieval Multiple Prefrontal Processes Subserve Source Memory , 2002, Neuron.

[51]  H. Moselhy,et al.  Frontal lobe changes in alcoholism: a review of the literature. , 2001, Alcohol and alcoholism.

[52]  S. Campanella,et al.  Pathways to alcohol-induced brain impairment in young people: A review by Hermens et al., 2013 , 2013, Cortex.

[53]  W. Velicer,et al.  Binge drinking and health behavior in medical students. , 2007, Addictive behaviors.

[54]  Leslie G. Ungerleider,et al.  Visual Imagery of Famous Faces: Effects of Memory and Attention Revealed by fMRI , 2002, NeuroImage.

[55]  L. Chassin,et al.  Developmental cascades: Linking adolescent substance use, affiliation with substance use promoting peers, and academic achievement to adult substance use disorders , 2010, Development and Psychopathology.

[56]  Michael F. Bunting,et al.  Working memory span tasks: A methodological review and user’s guide , 2005, Psychonomic bulletin & review.

[57]  Gary H. Glover,et al.  Reorganization of Frontal Systems Used by Alcoholics for Spatial Working Memory: An fMRI Study , 2001, NeuroImage.

[58]  Adrian M. Owen,et al.  The role of the lateral frontal cortex in mnemonic processing: the contribution of functional neuroimaging , 2000, Experimental Brain Research.

[59]  Mark D'Esposito,et al.  Region-specific changes in prefrontal function with age: a review of PET and fMRI studies on working and episodic memory. , 2005, Brain : a journal of neurology.

[60]  Kathryn M. McMillan,et al.  N‐back working memory paradigm: A meta‐analysis of normative functional neuroimaging studies , 2005, Human brain mapping.

[61]  A. Owen The Functional Organization of Working Memory Processes Within Human Lateral Frontal Cortex: The Contribution of Functional Neuroimaging , 1997, The European journal of neuroscience.

[62]  R. Coppola,et al.  Physiological characteristics of capacity constraints in working memory as revealed by functional MRI. , 1999, Cerebral cortex.

[63]  Fernando Cadaveira,et al.  Hyperactivation of right inferior frontal cortex in young binge drinkers during response inhibition: a follow-up study. , 2012, Addiction.

[64]  C. Presley,et al.  The introduction of the heavy and frequent drinker: a proposed classification to increase accuracy of alcohol assessments in postsecondary educational settings. , 2006, Journal of studies on alcohol.

[65]  Pierre Maurage,et al.  Early attentional modulation by alcohol-related cues in young binge drinkers: An event-related potentials study , 2012, Clinical Neurophysiology.

[66]  D. Foxcroft,et al.  The effect of alcohol advertising, marketing and portrayal on drinking behaviour in young people: systematic review of prospective cohort studies , 2009, BMC public health.

[67]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[68]  Susan F Tapert,et al.  A preliminary study of functional magnetic resonance imaging response during verbal encoding among adolescent binge drinkers. , 2010, Alcohol.

[69]  G Gmel,et al.  Characteristics of binge drinkers in Europe. , 2004, Social science & medicine.

[70]  A. Pfefferbaum,et al.  Neurocircuitry in alcoholism: a substrate of disruption and repair , 2005, Psychopharmacology.