Evoked gamma band response in male adolescent subjects at high risk for alcoholism during a visual oddball task.

This study investigates early evoked gamma band activity in male adolescent subjects at high risk for alcoholism (HR; n=68) and normal controls (LR; n=27) during a visual oddball task. A time-frequency representation method was applied to EEG data in order to obtain stimulus related early evoked (phase-locked) gamma band activity (29-45 Hz) and was analyzed within a 0-150 ms time window range. Significant reduction of the early evoked gamma band response in the frontal and parietal regions during target stimulus processing was observed in HR subjects compared to LR subjects. Additionally, the HR group showed less differentiation between target and non-target stimuli in both frontal and parietal regions compared to the LR group, indicating difficulty in early stimulus processing, probably due to a dysfunctional frontoparietal attentional network. The results indicate that the deficient early evoked gamma band response may precede the development of alcoholism and could be a potential endophenotypic marker of alcoholism risk.

[1]  F. A. Wilson,et al.  EEG activities in the orbitofrontal cortex and dorsolateral prefrontal cortex during the development of morphine dependence, tolerance and withdrawal in rhesus monkeys , 2005, Brain Research.

[2]  K. Sher,et al.  Characteristics of children of alcoholics: putative risk factors, substance use and abuse, and psychopathology. , 1991, Journal of abnormal psychology.

[3]  M. Earleywine,et al.  Personality and EEG β in Older Adults with Alcoholic Relatives , 1995 .

[4]  M. Ding,et al.  Task-related power and coherence changes in neuromagnetic activity during visuomotor coordination , 2002, Experimental Brain Research.

[5]  S. Uchida,et al.  The relationship between the visually evoked P300 event-related potential and gamma band oscillation in the human medial and basal temporal lobes An electrocorticographic study , 2002, Neuroscience Research.

[6]  V. Hesselbrock,et al.  P3 amplitudes in two distinct tasks are decreased in young men with a history of paternal alcoholism. , 1987, Alcohol.

[7]  E. Basar,et al.  Event-related oscillations are 'real brain responses'--wavelet analysis and new strategies. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[8]  Aribert Rothenberger,et al.  Abnormal early stages of task stimulus processing in children with attention-deficit hyperactivity disorder – evidence from event-related gamma oscillations , 2001, Clinical Neurophysiology.

[9]  V. Menon,et al.  Neural basis of protracted developmental changes in visuo-spatial working memory , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[10]  N. Volkow,et al.  Regional brain metabolic response to lorazepam in subjects at risk for alcoholism. , 1995, Alcoholism, clinical and experimental research.

[11]  G. Pfurtscheller,et al.  Human cortical 40 Hz rhythm is closely related to EMG rhythmicity , 1996, Neuroscience Letters.

[12]  R. Benson,et al.  Responses to rare visual target and distractor stimuli using event-related fMRI. , 2000, Journal of neurophysiology.

[13]  F E Bloom,et al.  Meta-analysis of P300 amplitude from males at risk for alcoholism. , 1994, Psychological bulletin.

[14]  A. Kok,et al.  P3 scalp topography to target and novel visual stimuli in children of alcoholics. , 1998, Alcohol.

[15]  H. Begleiter,et al.  Alcoholism and Human Electrophysiology , 2003, Alcohol research & health : the journal of the National Institute on Alcohol Abuse and Alcoholism.

[16]  J. Polich,et al.  Visual P3a in male subjects at high risk for alcoholism , 1999, Biological Psychiatry.

[17]  Aribert Rothenberger,et al.  Developmental event‐related gamma oscillations: effects of auditory attention , 2002, The European journal of neuroscience.

[18]  C S Herrmann,et al.  Magnetoencephalographic responses to illusory figures: early evoked gamma is affected by processing of stimulus features. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[19]  S. Kuperman,et al.  Relationship of child psychopathology to parental alcoholism and antisocial personality disorder. , 1999, Journal of the American Academy of Child and Adolescent Psychiatry.

[20]  John Rohrbaugh,et al.  Resting EEG in offspring of male alcoholics: beta frequencies. , 2004, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[21]  J. Downar,et al.  The Effect of Task Relevance on the Cortical Response to Changes in Visual and Auditory Stimuli: An Event-Related fMRI Study , 2001, NeuroImage.

[22]  J. Jonides,et al.  Overlapping mechanisms of attention and spatial working memory , 2001, Trends in Cognitive Sciences.

[23]  S. Berman,et al.  Event-related potentials in alcoholic fathers and their sons. , 1991, Alcohol.

[24]  J. Rohrbaugh,et al.  Amplitude of visual P3 event-related potential as a phenotypic marker for a predisposition to alcoholism: preliminary results from the COGA Project. Collaborative Study on the Genetics of Alcoholism. , 1998, Alcoholism: Clinical and Experimental Research.

[25]  Stephen Theophanis,et al.  Color display of the localized spectrum , 2000 .

[26]  P. Fries,et al.  Is synchronized neuronal gamma activity relevant for selective attention? , 2003, Brain Research Reviews.

[27]  J. Feighner,et al.  Diagnostic criteria for use in psychiatric research. , 1972, Archives of general psychiatry.

[28]  M. Hesselbrock,et al.  A validity study of the SSAGA--a comparison with the SCAN. , 1999, Addiction.

[29]  V. Hesselbrock,et al.  Reduced P300 amplitude in relation to family history of alcoholism and antisocial personality disorder among young men at risk for alcoholism. , 1993, Alcohol and alcoholism (Oxford, Oxfordshire). Supplement.

[30]  Daniel Gembris,et al.  Top-down attentional processing enhances auditory evoked gamma band activity , 2003, Neuroreport.

[31]  H. Begleiter,et al.  S-transform time-frequency analysis of P300 reveals deficits in individuals diagnosed with alcoholism , 2006, Clinical Neurophysiology.

[32]  L. Bierut,et al.  Familial transmission of substance dependence: alcohol, marijuana, cocaine, and habitual smoking: a report from the Collaborative Study on the Genetics of Alcoholism. , 1998, Archives of general psychiatry.

[33]  R. Näätänen,et al.  The transient 40-Hz response, mismatch negativity, and attentional processes in humans , 1997, Progress in Neuro-psychopharmacology and Biological Psychiatry.

[34]  V. Hesselbrock,et al.  Correlates of increased risk for alcoholism in young men , 1986, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[35]  C. Basar-Eroglu,et al.  Gamma response of the brain: a multifunctional oscillation that represents bottom-up with top-down processing. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[36]  C. Ehlers,et al.  Event-related potential responses to alcohol-related stimuli in African-American young adults: relation to family history of alcoholism and drug usage. , 2003, Alcohol and alcoholism.

[37]  Marc A Schuckit,et al.  Linkage and linkage disequilibrium of evoked EEG oscillations with CHRM2 receptor gene polymorphisms: implications for human brain dynamics and cognition. , 2004, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[38]  E. Basar,et al.  A compound P300-40 Hz response of the cat hippocampus. , 1991 .

[39]  Lalu Mansinha,et al.  Localization of the complex spectrum: the S transform , 1996, IEEE Trans. Signal Process..

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

[41]  S. Steinhauer,et al.  Eight-year longitudinal follow-up of P300 and clinical outcome in children from high-risk for alcoholism families , 1995, Biological Psychiatry.

[42]  V E Pollock,et al.  Personality and EEG beta in older adults with alcoholic relatives. , 1995, Alcoholism, clinical and experimental research.

[43]  E Başar,et al.  A new strategy involving multiple cognitive paradigms demonstrates that ERP components are determined by the superposition of oscillatory responses , 2000, Clinical Neurophysiology.

[44]  K. Pope,et al.  Cognitive tasks augment gamma EEG power , 2004, Clinical Neurophysiology.

[45]  E. Basar,et al.  P300-response: possible psychophysiological correlates in delta and theta frequency channels. A review. , 1992, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[46]  R. McCarley,et al.  Abnormal Neural Synchrony in Schizophrenia , 2003, The Journal of Neuroscience.

[47]  M Laruelle,et al.  Alterations of benzodiazepine receptors in type II alcoholic subjects measured with SPECT and [123I]iomazenil. , 1998, The American journal of psychiatry.

[48]  E Başar,et al.  Early gamma response is sensory in origin: a conclusion based on cross-comparison of results from multiple experimental paradigms. , 1998, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[49]  Tatiana Foroud,et al.  Variations in GABRA2, encoding the alpha 2 subunit of the GABA(A) receptor, are associated with alcohol dependence and with brain oscillations. , 2004, American journal of human genetics.

[50]  H. Begleiter,et al.  A simple auditory oddball task in young adult males at high risk for alcoholism. , 1996, Alcoholism, clinical and experimental research.

[51]  H. Begleiter,et al.  Event-related brain potentials in boys at risk for alcoholism. , 1984, Science.

[52]  P. Goldman-Rakic,et al.  Infrequent events transiently activate human prefrontal and parietal cortex as measured by functional MRI. , 1997, Journal of neurophysiology.

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

[54]  H. Begleiter,et al.  Neuroelectric correlates of response production and inhibition in individuals at risk to develop alcoholism , 1997, Biological Psychiatry.

[55]  T. Yoshiura,et al.  Functional MRI study of auditory and visual oddball tasks. , 1999, Neuroreport.

[56]  H Begleiter,et al.  Event-related potentials in individuals at risk for alcoholism. , 1990, Alcohol.

[57]  J. Pernier,et al.  Stimulus Specificity of Phase-Locked and Non-Phase-Locked 40 Hz Visual Responses in Human , 1996, The Journal of Neuroscience.

[58]  John Rohrbaugh,et al.  Delta and Theta Oscillations as Risk Markers in Adolescent Offspring of Alcoholics , 2006 .

[59]  J. Lachaux,et al.  A simple measure of correlation across time, frequency and space between continuous brain signals , 2003, Journal of Neuroscience Methods.

[60]  V. Benegal,et al.  P300 amplitudes vary inversely with continuum of risk in first degree male relatives of alcoholics , 1995, Psychiatric genetics.

[61]  Erol Başar,et al.  The genesis of human event-related responses explained through the theory of oscillatory neural assemblies , 2000, Neuroscience Letters.

[62]  P. Goldman-Rakic,et al.  Coactivation of prefrontal cortex and inferior parietal cortex in working memory tasks revealed by 2DG functional mapping in the rhesus monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[63]  P. Goldman-Rakic,et al.  Functional magnetic resonance imaging of human prefrontal cortex activation during a spatial working memory task. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[64]  M Schürmann,et al.  Delta responses and cognitive processing: single-trial evaluations of human visual P300. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[65]  Odin van der Stelt,et al.  P3 event-related potential, dopamine D2 receptor A1 allele, and sensation-seeking in adult children of alcoholics. , 2001, Alcoholism, clinical and experimental research.

[66]  M. Kenward,et al.  Small sample inference for fixed effects from restricted maximum likelihood. , 1997, Biometrics.

[67]  D. B. Matthews,et al.  The role of GABAA receptors in the acute and chronic effects of ethanol , 1998, Psychopharmacology.

[68]  J. Yordanova,et al.  Brain theta response predicts P300 latency in children , 1996, Neuroreport.

[69]  J. Rohrbaugh,et al.  Visual P300: an interlaboratory consistency study. , 1994, Alcohol.

[70]  H. Crawford,et al.  Enhancement of auditory sensory gating and stimulus-bound gamma band (40 Hz) oscillations in heavy tobacco smokers , 2002, Neuroscience Letters.

[71]  H. Petsche,et al.  Phase-coupling of theta-gamma EEG rhythms during short-term memory processing. , 2002, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[73]  E Başar,et al.  Frontal gamma-band enhancement during multistable visual perception. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[74]  Tatiana Foroud,et al.  Linkage disequilibrium between the beta frequency of the human EEG and a GABAA receptor gene locus , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[75]  Peter C. Chu.  The S-Transform for Obtaining Localized Spectra , 1989 .

[76]  N S Cotton,et al.  The familial incidence of alcoholism: a review. , 1979, Journal of studies on alcohol.

[77]  S. Berman,et al.  P3 in young boys as a predictor of adolescent substance use. , 1993, Alcohol.

[78]  V. Hesselbrock,et al.  Allelic and haplotypic association of GABRA2 with alcohol dependence , 2004, American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics.

[79]  R. Traub,et al.  Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation , 1995, Nature.

[80]  K. Reinikainen,et al.  Selective attention enhances the auditory 40-Hz transient response in humans , 1993, Nature.

[81]  S. Steinhauer,et al.  Assessment of prepubertal and postpubertal boys and girls at risk for developing alcoholism with P300 from a visual discrimination task. , 1993, Journal of studies on alcohol.

[82]  Dennis Gabor,et al.  Theory of communication , 1946 .

[83]  J. Nurnberger,et al.  A new, semi-structured psychiatric interview for use in genetic linkage studies: a report on the reliability of the SSAGA. , 1994, Journal of studies on alcohol.

[84]  D. Lieberman.  Children of alcoholics: an update. , 2000, Current opinion in pediatrics.

[85]  J. Rohrbaugh,et al.  Amplitude of visual P3 event-related potential as a phenotypic marker for a predisposition to alcoholism: preliminary results from the COGA Project. Collaborative Study on the Genetics of Alcoholism. , 1998, Alcoholism, clinical and experimental research.

[86]  C. Herrmann,et al.  Gamma responses and ERPs in a visual classification task , 1999, Clinical Neurophysiology.

[87]  P. Goldman-Rakic,et al.  Activation of human prefrontal cortex during spatial and nonspatial working memory tasks measured by functional MRI. , 1996, Cerebral cortex.

[88]  Evian Gordon,et al.  Gamma activity in schizophrenia: evidence of impaired network binding? , 2000, Clinical Neurophysiology.

[89]  E. Basar,et al.  Wavelet analysis of oddball P300. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[90]  P W Woodruff,et al.  Reduced levels of GABA-benzodiazepine receptor in alcohol dependency in the absence of grey matter atrophy , 1998, British Journal of Psychiatry.

[91]  Bernice Porjesz,et al.  Suppression of early evoked gamma band response in male alcoholics during a visual oddball task. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[92]  T M Itil,et al.  Electroencephalograms in children of alcoholic fathers. , 1982, Psychophysiology.

[93]  A. Haig,et al.  Peak gamma latency correlated with reaction time in a conventional oddball paradigm , 1999, Clinical Neurophysiology.

[94]  W. G. Sannita,et al.  Synchronized ∼15.0–35.0Hz oscillatory response to spatially modulated visual patterns in man , 1999, Neuroscience.

[95]  B. Ardekani,et al.  Functional magnetic resonance imaging of brain activity in the visual oddball task. , 2002, Brain research. Cognitive brain research.

[96]  C. Prescott.  The Genetic Epidemiology of Alcoholism: Sex Differences and Future Directions , 2001 .

[97]  P. Finn,et al.  Reduced EEG alpha power in the male and female offspring of alcoholics. , 1999, Alcoholism, clinical and experimental research.

[98]  R. Traub,et al.  A mechanism for generation of long-range synchronous fast oscillations in the cortex , 1996, Nature.

[99]  C. Ehlers,et al.  Effects of age and parental history of alcoholism on EEG findings in mission Indian children and adolescents. , 2001, Alcoholism, clinical and experimental research.

[100]  T. Demiralp,et al.  Human EEG gamma oscillations in neuropsychiatric disorders , 2005, Clinical Neurophysiology.

[101]  E. Basar,et al.  A compound P300-40 Hz response of the cat hippocampus. , 1991, The International journal of neuroscience.

[102]  R Rawlings,et al.  Auditory recovery function and P3 in boys at high risk for alcoholism. , 1987, Alcohol.

[103]  V. Hesselbrock,et al.  EEG, autonomic and subjective correlates of the risk for alcoholism. , 1993, Journal of studies on alcohol.

[104]  J. Desmedt,et al.  Transient phase-locking of 40 Hz electrical oscillations in prefrontal and parietal human cortex reflects the process of conscious somatic perception , 1994, Neuroscience Letters.

[105]  T. Demiralp,et al.  Effects of task variables on the amplitude and phase-locking of auditory gamma band responses in human. , 1997, The International journal of neuroscience.

[106]  S. Karakas,et al.  Early gamma response in human neuroelectric activity is correlated with neuropsychological test scores , 2003, Neuroscience Letters.

[107]  Babak A. Ardekani,et al.  A functional MRI study of visual oddball: evidence for frontoparietal dysfunction in subjects at risk for alcoholism , 2004, NeuroImage.

[108]  L. Marshall,et al.  Event-related gamma band activity during passive and active oddball tasks. , 1996, Neuroreport.

[109]  Laverne W. Stanton,et al.  Applied Regression Analysis: A Research Tool , 1990 .