Decreased event-related theta power and phase-synchrony in young binge drinkers during target detection: An anatomically-constrained MEG approach

Background: The prevalence of binge drinking has risen in recent years. It is associated with a range of neurocognitive deficits among adolescents and young emerging adults who are especially vulnerable to alcohol use. Attention is an essential dimension of executive functioning and attentional disturbances may be associated with hazardous drinking. The aim of the study was to examine the oscillatory neural dynamics of attentional control during visual target detection in emerging young adults as a function of binge drinking. Method: In total, 51 first-year university students (18 ± 0.6 years) were assigned to light drinking (n = 26), and binge drinking (n = 25) groups based on their alcohol consumption patterns. A high-density magnetoencephalography signal was combined with structural magnetic resonance imaging in an anatomically constrained magnetoencephalography model to estimate event-related source power in a theta (4–7 Hz) frequency band. Phase-locked co-oscillations were further estimated between the principally activated regions during task performance. Results: Overall, the greatest event-related theta power was elicited by targets in the right inferior frontal cortex and it correlated with performance accuracy and selective attention scores. Binge drinkers exhibited lower theta power and dysregulated oscillatory synchrony to targets in the right inferior frontal cortex, which correlated with higher levels of alcohol consumption. Conclusions: These results confirm that a highly interactive network in the right inferior frontal cortex subserves attentional control, revealing the importance of theta oscillations and neural synchrony for attentional capture and contextual maintenance. Attenuation of theta power and synchronous interactions in binge drinkers may indicate early stages of suboptimal integrative processing in young, highly functioning binge drinkers.

[1]  N. Volkow,et al.  Neurocircuitry of Addiction , 2010, Neuropsychopharmacology.

[2]  H. Hjaltason,et al.  Hemispatial neglect following right hemisphere stroke: clinical course and sensitivity of diagnostic tasks , 2018, Topics in stroke rehabilitation.

[3]  Ksenija Marinkovic,et al.  When the brain changes its mind: Oscillatory dynamics of conflict processing and response switching in a flanker task during alcohol challenge , 2018, PloS one.

[4]  John-Dylan Haynes,et al.  Neural Representations of Hierarchical Rule Sets: The Human Control System Represents Rules Irrespective of the Hierarchical Level to Which They Belong , 2017, The Journal of Neuroscience.

[5]  E. Halgren,et al.  Superficial Slow Rhythms Integrate Cortical Processing in Humans , 2017, Scientific Reports.

[6]  P. Pazo-Álvarez,et al.  Electrophysiological Anomalies in Face–Name Memory Encoding in Young Binge Drinkers , 2017, Front. Psychiatry.

[7]  T. Brumback,et al.  The Burden of Binge and Heavy Drinking on the Brain: Effects on Adolescent and Young Adult Neural Structure and Function , 2017, Front. Psychol..

[8]  R. Hingson,et al.  Drinking Beyond the Binge Threshold: Predictors, Consequences, and Changes in the U.S. , 2017, American journal of preventive medicine.

[9]  Jeonghwa Lee,et al.  Disrupted Control Network Connectivity in Abstinent Patients with Alcohol Dependence , 2017, Psychiatry investigation.

[10]  F. Cadaveira,et al.  Binge drinking affects brain oscillations linked to motor inhibition and execution , 2017, Journal of psychopharmacology.

[11]  P. Maurage,et al.  Differential impairments across attentional networks in binge drinking , 2017, Psychopharmacology.

[12]  Jan R. Wessel,et al.  On the Globality of Motor Suppression: Unexpected Events and Their Influence on Behavior and Cognition , 2017, Neuron.

[13]  J. Cohen-Gilbert,et al.  Neurobiological signatures associated with alcohol and drug use in the human adolescent brain , 2016, Neuroscience & Biobehavioral Reviews.

[14]  Margaret A. Broadwater,et al.  Adolescent Alcohol Exposure Persistently Impacts Adult Neurobiology and Behavior , 2016, Pharmacological Reviews.

[15]  Hongqiang Sun,et al.  Alterations in Brain Structure and Functional Connectivity in Alcohol Dependent Patients and Possible Association with Impulsivity , 2016, PloS one.

[16]  F. Cadaveira,et al.  Functional and structural brain connectivity of young binge drinkers: a follow-up study , 2016, Scientific Reports.

[17]  Megan E. Patrick,et al.  Intoxication and binge and high-intensity drinking among US young adults in their mid-20s , 2016, Substance abuse.

[18]  Nevena Padovan,et al.  Alcohol Hits You When It Is Hard: Intoxication, Task Difficulty, and Theta Brain Oscillations , 2016, Alcoholism, clinical and experimental research.

[19]  B. Porjesz,et al.  Delta, theta, and alpha event-related oscillations in alcoholics during Go/NoGo task: Neurocognitive deficits in execution, inhibition, and attention processing , 2016, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[20]  D. Sharp,et al.  Inferior PFC Subregions Have Broad Cognitive Roles , 2015, Trends in Cognitive Sciences.

[21]  A. Pfefferbaum,et al.  The Resting Brain of Alcoholics. , 2015, Cerebral cortex.

[22]  E. Halgren,et al.  Laminar profile of spontaneous and evoked theta: Rhythmic modulation of cortical processing during word integration , 2015, Neuropsychologia.

[23]  Fernando Maestú,et al.  Exploratory Analysis of Power Spectrum and Functional Connectivity During Resting State in Young Binge Drinkers: A MEG Study , 2015, Int. J. Neural Syst..

[24]  I. Gottesman,et al.  Endophenotypes for Alcohol Use Disorder: An Update on the Field , 2015, Current Addiction Reports.

[25]  Vince D Calhoun,et al.  Reduced left executive control network functional connectivity is associated with alcohol use disorders. , 2014, Alcoholism, clinical and experimental research.

[26]  Jeffrey D. Rudie,et al.  Development of the Default Mode and Central Executive Networks across early adolescence: A longitudinal study , 2014, Developmental Cognitive Neuroscience.

[27]  M. Frank,et al.  Frontal theta as a mechanism for cognitive control , 2014, Trends in Cognitive Sciences.

[28]  P. Maurage,et al.  Attentional alterations in alcohol dependence are underpinned by specific executive control deficits. , 2014, Alcoholism, clinical and experimental research.

[29]  Masao Iwase,et al.  Frontal midline theta rhythm and gamma power changes during focused attention on mental calculation: an MEG beamformer analysis , 2014, Front. Hum. Neurosci..

[30]  R. Leech,et al.  A functional network perspective on response inhibition and attentional control , 2014, Nature Communications.

[31]  Beatriz Luna,et al.  Developmental stages and sex differences of white matter and behavioral development through adolescence: A longitudinal diffusion tensor imaging (DTI) study , 2014, NeuroImage.

[32]  T. Robbins,et al.  Inhibition and the right inferior frontal cortex: one decade on , 2014, Trends in Cognitive Sciences.

[33]  Gereon R. Fink,et al.  Dorsal and Ventral Attention Systems , 2014, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[34]  C. Kornreich,et al.  Binge drinking in adolescents: a review of neurophysiological and neuroimaging research. , 2014, Alcohol and alcoholism.

[35]  Martin Luessi,et al.  MNE software for processing MEG and EEG data , 2014, NeuroImage.

[36]  Chantal E. Stern,et al.  Theta rhythm and the encoding and retrieval of space and time , 2014, NeuroImage.

[37]  Simon Hanslmayr,et al.  How brain oscillations form memories — A processing based perspective on oscillatory subsequent memory effects , 2014, NeuroImage.

[38]  R. Hingson,et al.  Trends in extreme binge drinking among US high school seniors. , 2013, JAMA pediatrics.

[39]  Fernando Cadaveira,et al.  Effects of a persistent binge drinking pattern of alcohol consumption in young people: a follow-up study using event-related potentials. , 2013, Alcohol and alcoholism.

[40]  George Fein,et al.  Resting-state synchrony in short-term versus long-term abstinent alcoholics. , 2013, Alcoholism, clinical and experimental research.

[41]  S. Tapert,et al.  Neurotoxic effects of alcohol in adolescence. , 2013, Annual review of clinical psychology.

[42]  M. Criaud,et al.  Have we been asking the right questions when assessing response inhibition in go/no-go tasks with fMRI? A meta-analysis and critical review , 2013, Neuroscience & Biobehavioral Reviews.

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

[44]  Juan Lupiáñez,et al.  Two cognitive and neural systems for endogenous and exogenous spatial attention , 2013, Behavioural Brain Research.

[45]  Linda Chang,et al.  Long-term influence of normal variation in neonatal characteristics on human brain development , 2012, Proceedings of the National Academy of Sciences.

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

[47]  Jason S. Sherfey,et al.  Theta Oscillations Are Sensitive to Both Early and Late Conflict Processing Stages: Effects of Alcohol Intoxication , 2012, PloS one.

[48]  Peter Stiers,et al.  Unravelling the Intrinsic Functional Organization of the Human Lateral Frontal Cortex: A Parcellation Scheme Based on Resting State fMRI , 2012, The Journal of Neuroscience.

[49]  C. Ehlers,et al.  Ethanol reduces the phase locking of neural activity in human and rodent brain , 2012, Brain Research.

[50]  Jonathan D. Cohen,et al.  The Function and Organization of Lateral Prefrontal Cortex: A Test of Competing Hypotheses , 2012, PloS one.

[51]  B. Porjesz,et al.  Event-Related Oscillations in Alcoholism Research: A Review. , 2012, Journal of addiction research & therapy.

[52]  Volker Brass,et al.  Identification of Naturally Processed Hepatitis C Virus-Derived Major Histocompatibility Complex Class I Ligands , 2012, PloS one.

[53]  Elisardo Becoña,et al.  La escala breve de evaluación del Síndrome de Dependencia de la Nicotina (NDSS-S) en fumadores españoles , 2011 .

[54]  Thomas V. Wiecki,et al.  A computational model of inhibitory control in frontal cortex and basal ganglia. , 2011, Psychological review.

[55]  Seth A. Herd,et al.  A Unified Framework for Inhibitory Control Opinion , 2022 .

[56]  C. Lebel,et al.  Longitudinal Development of Human Brain Wiring Continues from Childhood into Adulthood , 2011, The Journal of Neuroscience.

[57]  Diane Swick,et al.  Are the neural correlates of stopping and not going identical? Quantitative meta-analysis of two response inhibition tasks , 2011, NeuroImage.

[58]  A. Wagner,et al.  Annals of the New York Academy of Sciences Cognitive Control and Right Ventrolateral Prefrontal Cortex: Reflexive Reorienting, Motor Inhibition, and Action Updating , 2022 .

[59]  Lawrence M. Ward,et al.  Electrical Neuroimaging of Voluntary Audiospatial Attention: Evidence for a Supramodal Attention Control Network , 2011, The Journal of Neuroscience.

[60]  Ralph Weidner,et al.  Dynamic Coding of Events within the Inferior Frontal Gyrus in a Probabilistic Selective Attention Task , 2011, Journal of Cognitive Neuroscience.

[61]  G. Koob,et al.  Preclinical studies of alcohol binge drinking , 2011, Annals of the New York Academy of Sciences.

[62]  Daniel H. Mathalon,et al.  Frontally mediated inhibitory processing and white matter microstructure: age and alcoholism effects , 2010, Psychopharmacology.

[63]  Jeffrey S. Spence,et al.  Frontal theta and alpha power and coherence changes are modulated by semantic complexity in Go/NoGo tasks. , 2010, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[64]  T. Womelsdorf,et al.  Human Neuroscience , 2022 .

[65]  K. Meador,et al.  Theta oscillations mediate interaction between prefrontal cortex and medial temporal lobe in human memory. , 2010, Cerebral cortex.

[66]  W. Klimesch,et al.  Control mechanisms in working memory: A possible function of EEG theta oscillations , 2010, Neuroscience & Biobehavioral Reviews.

[67]  W. Klimesch,et al.  Oscillatory mechanisms of process binding in memory , 2010, Neuroscience & Biobehavioral Reviews.

[68]  T. Curran,et al.  Functional role of gamma and theta oscillations in episodic memory , 2010, Neuroscience & Biobehavioral Reviews.

[69]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[70]  J. Chikazoe Localizing performance of go/no-go tasks to prefrontal cortical subregions , 2010, Current opinion in psychiatry.

[71]  David Goldman,et al.  Genome-wide association identifies candidate genes that influence the human electroencephalogram , 2010, Proceedings of the National Academy of Sciences.

[72]  John Duncan,et al.  The role of the right inferior frontal gyrus: inhibition and attentional control , 2010, NeuroImage.

[73]  Peter Olausson,et al.  REVIEW: Understanding the construct of impulsivity and its relationship to alcohol use disorders , 2010, Addiction biology.

[74]  M. Corbetta,et al.  Right Hemisphere Dominance during Spatial Selective Attention and Target Detection Occurs Outside the Dorsal Frontoparietal Network , 2010, The Journal of Neuroscience.

[75]  George Fein,et al.  Induced theta oscillations as biomarkers for alcoholism , 2010, Clinical Neurophysiology.

[76]  D. Nelson,et al.  The intensity of binge alcohol consumption among U.S. adults. , 2010, American journal of preventive medicine.

[77]  C. Kornreich,et al.  Chronic alcoholism: Insights from neurophysiology , 2009, Neurophysiologie Clinique/Clinical Neurophysiology.

[78]  C. Boettiger,et al.  Impulsivity, frontal lobes and risk for addiction , 2009, Pharmacology Biochemistry and Behavior.

[79]  J. Schoffelen,et al.  Source connectivity analysis with MEG and EEG , 2009, Human brain mapping.

[80]  M. Bellgrove,et al.  Insights into the neural basis of response inhibition from cognitive and clinical neuroscience , 2009, Neuroscience & Biobehavioral Reviews.

[81]  John Duncan,et al.  Selective tuning of the right inferior frontal gyrus during target detection , 2009, Cognitive, affective & behavioral neuroscience.

[82]  H. de Wit Impulsivity as a determinant and consequence of drug use: a review of underlying processes , 2009, Addiction biology.

[83]  B. Porjesz,et al.  Uncovering genes for cognitive (dys)function and predisposition for alcoholism spectrum disorders: A review of human brain oscillations as effective endophenotypes , 2008, Brain Research.

[84]  T. Duka,et al.  Cognitive and emotional consequences of binge drinking: role of amygdala and prefrontal cortex , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

[86]  David Badre,et al.  Cognitive control, hierarchy, and the rostro–caudal organization of the frontal lobes , 2008, Trends in Cognitive Sciences.

[87]  J. Gross,et al.  The Neural Bases of Emotion Regulation: Reappraisal and Suppression of Negative Emotion , 2008, Biological Psychiatry.

[88]  S. Petersen,et al.  A dual-networks architecture of top-down control , 2008, Trends in Cognitive Sciences.

[89]  Simon Hanslmayr,et al.  The Electrophysiological Dynamics of Interference during the Stroop Task , 2008, Journal of Cognitive Neuroscience.

[90]  K. Marinković,et al.  Alcohol: Effects on Neurobehavioral Functions and the Brain , 2007, Neuropsychology Review.

[91]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[92]  E. Macaluso,et al.  Dissociation of stimulus relevance and saliency factors during shifts of visuospatial attention. , 2007, Cerebral cortex.

[93]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[94]  M. Sakagami,et al.  Functional role of the ventrolateral prefrontal cortex in decision making , 2007, Current Opinion in Neurobiology.

[95]  M. Brass,et al.  The role of the inferior frontal junction area in cognitive control , 2005, Trends in Cognitive Sciences.

[96]  Jin Fan,et al.  The activation of attentional networks , 2005, NeuroImage.

[97]  H. Begleiter,et al.  The utility of neurophysiological markers in the study of alcoholism , 2005, Clinical Neurophysiology.

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

[99]  B. J. Casey,et al.  Imaging the developing brain: what have we learned about cognitive development? , 2005, Trends in Cognitive Sciences.

[100]  E. Halgren,et al.  Responses of Human Anterior Cingulate Cortex Microdomains to Error Detection, Conflict Monitoring, Stimulus-Response Mapping, Familiarity, and Orienting , 2005, The Journal of Neuroscience.

[101]  Anders M. Dale,et al.  Spectral spatiotemporal imaging of cortical oscillations and interactions in the human brain , 2004, NeuroImage.

[102]  K. Coyle,et al.  Cognitive impairments in sober alcoholics: performance on selective and divided attention tasks. , 2004, Drug and alcohol dependence.

[103]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[104]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[105]  Valerie A. Carr,et al.  Spatiotemporal Dynamics of Modality-Specific and Supramodal Word Processing , 2003, Neuron.

[106]  Patrick M. O'Malley,et al.  Monitoring the Future National Results on Adolescent Drug Use: Overview of Key Findings, 2004. , 2003 .

[107]  Rita Z. Goldstein,et al.  Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. , 2002, The American journal of psychiatry.

[108]  O. Jensen,et al.  Frontal theta activity in humans increases with memory load in a working memory task , 2002, The European journal of neuroscience.

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

[110]  E Halgren,et al.  Arousal-related P3a to novel auditory stimuli is abolished by a moderately low alcohol dose. , 2001, Alcohol and alcoholism.

[111]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[112]  E. Halgren,et al.  Early widespread cortical distribution of coherent fusiform face selective activity , 2000, Human brain mapping.

[113]  R. Näätänen,et al.  Increased distractibility by task-irrelevant sound changes in abstinent alcoholics. , 2000, Alcoholism, clinical and experimental research.

[114]  E. Halgren,et al.  Dynamic Statistical Parametric Mapping Combining fMRI and MEG for High-Resolution Imaging of Cortical Activity , 2000, Neuron.

[115]  E. Halgren,et al.  LOCALISED FACE PROCESSING BY THE HUMAN PREFRONTAL CORTEX: FACE-SELECTIVE INTRACEREBRAL POTENTIALS AND POST-LESION DEFICITS , 2000, Cognitive neuropsychology.

[116]  A. G. Solé,et al.  Test para la identificación de transtornos por uso de alcohol (AUDIT): Traducción y validación del AUDIT al catalán y castellano , 1999 .

[117]  J. Evenden Varieties of impulsivity , 1999, Psychopharmacology.

[118]  E. Stein,et al.  Right hemispheric dominance of inhibitory control: an event-related functional MRI study. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[119]  P S Goldman-Rakic,et al.  Face-selective neurons during passive viewing and working memory performance of rhesus monkeys: evidence for intrinsic specialization of neuronal coding. , 1999, Cerebral cortex.

[120]  H. Begleiter,et al.  What is inherited in the predisposition toward alcoholism? A proposed model. , 1999, Alcoholism, clinical and experimental research.

[121]  Masamichi Sakagami,et al.  The hierarchical organization of decision making in the primate prefrontal cortex , 1999, Neuroscience Research.

[122]  Joel R. Meyer,et al.  A large-scale distributed network for covert spatial attention: further anatomical delineation based on stringent behavioural and cognitive controls. , 1999, Brain : a journal of neurology.

[123]  O. Bertrand,et al.  Oscillatory gamma activity in humans and its role in object representation , 1999, Trends in Cognitive Sciences.

[124]  Richard S. J. Frackowiak,et al.  Functional localization of the system for visuospatial attention using positron emission tomography. , 1997, Brain : a journal of neurology.

[125]  J. Patton,et al.  Factor structure of the Barratt impulsiveness scale. , 1995, Journal of clinical psychology.

[126]  A. Damasio,et al.  Insensitivity to future consequences following damage to human prefrontal cortex , 1994, Cognition.

[127]  L. Derogatis,et al.  The Brief Symptom Inventory: an introductory report , 1983, Psychological Medicine.

[128]  M. Zuckerman,et al.  Construct validity for the sensation-seeking scale. , 1968, Journal of consulting and clinical psychology.

[129]  Megan E. Patrick,et al.  High‐intensity drinking by underage young adults in the United States , 2017, Addiction.

[130]  B. Porjesz,et al.  Advances in Electrophysiological Research , 2015, Alcohol research : current reviews.

[131]  Bernice Porjesz,et al.  Understanding alcohol use disorders with neuroelectrophysiology. , 2014, Handbook of clinical neurology.

[132]  S. Tapert,et al.  The effect of alcohol use on human adolescent brain structures and systems. , 2014, Handbook of clinical neurology.

[133]  A. Diamond Executive functions. , 2014, Handbook of clinical neurology.

[134]  B. Q. Rosen,et al.  Event-Related Theta Power during Lexical-Semantic Retrieval and Decision Conflict is Modulated by Alcohol Intoxication: Anatomically Constrained MEG , 2012, Front. Psychology.

[135]  E. Becoña,et al.  [The Short Nicotine Dependence Syndrome Scale (NDSS-S) in Spanish smokers]. , 2011, Psicothema.

[136]  J. Schoffelen,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2018 .

[137]  John Polich,et al.  Binge drinking in young adults: Data, definitions, and determinants. , 2009, Psychological bulletin.

[138]  H. Wit Impulsivity as a determinant and consequence of drug use: a review of underlying processes , 2009 .

[139]  K. Miller Executive functions. , 2005, Pediatric annals.

[140]  Bernice Porjesz,et al.  The role of brain oscillations as functional correlates of cognitive systems: a study of frontal inhibitory control in alcoholism. , 2004, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[141]  J. Downar,et al.  A cortical network sensitive to stimulus salience in a neutral behavioral context across multiple sensory modalities. , 2002, Journal of neurophysiology.

[142]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[143]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

[144]  E. M. P. Widmark,et al.  Principles and applications of medicolegal alcohol determination , 1981 .

[145]  E. Koechlin,et al.  The Architecture of Cognitive Control in the Human Prefrontal Cortex , 2003, Science.