Reduced auditory evoked gamma band response and cognitive processing deficits in first episode schizophrenia

Abstract Objectives. Gamma-band oscillations (e.g., the early auditory evoked gamma-band response, aeGBR) have been suggested to mediate cognitive and perceptual processes by driving the synchronization of local neuronal populations. Reduced aeGBR is a consistent finding in patients with schizophrenia and high-risk subjects, and has been proposed to represent an endophenotype for the illness. However, it is still unclear whether this reduction represents a deficit in sensory or cognitive processes, or a combination of the two. The present study investigated this question by manipulating the difficulty of an auditory reaction task in patients with first-episode schizophrenia and healthy controls. Methods. A 64-channel EEG was recorded in 23 patients with first-episode schizophrenia and 22 healthy controls during two conditions of an auditory reaction task: an easy condition that merely required low-level vigilance, and a difficult condition that placed significant demands on attention and working memory. Results. In contrast to healthy controls, patients failed to increase aeGBR power and phase-locking in the difficult condition. In patients, aeGBR power and phase-locking indices were associated with working memory deficits. Conclusions. The observed results confirm the applicability of aeGBR disturbances as a stable endophenotype of schizophrenia, and suggest a cognitive, rather than sensory, deficit at their origin.

[1]  S. Kay,et al.  The positive and negative syndrome scale (PANSS) for schizophrenia. , 1987, Schizophrenia bulletin.

[2]  C. Reynolds,et al.  Wechsler memory scale-revised , 1988 .

[3]  S Makeig,et al.  Human auditory evoked gamma-band magnetic fields. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[6]  P. Kalus,et al.  Altered distribution of parvalbumin-immunoreactive local circuit neurons in the anterior cingulate cortex of schizophrenic patients , 1997, Psychiatry Research: Neuroimaging.

[7]  T. Hergueta,et al.  The mini international neuropsychiatric interview , 1998, European Psychiatry.

[8]  D. Sheehan,et al.  The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. , 1998, The Journal of clinical psychiatry.

[9]  Karl J. Friston.  Schizophrenia and the disconnection hypothesis , 1999, Acta psychiatrica Scandinavica. Supplementum.

[10]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[11]  M. Hasselmo,et al.  Gamma frequency-range abnormalities to auditory stimulation in schizophrenia. , 1999, Archives of general psychiatry.

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

[13]  J. Barth,et al.  The Halstead-Reitan Neuropsychological Test Battery. , 2000 .

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

[15]  A. Haig,et al.  An integration of 40 Hz Gamma and phasic arousal: novelty and routinization processing in schizophrenia , 2001, Clinical Neurophysiology.

[16]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[17]  Silke Lux,et al.  Verbaler Lern- und Merkfähigkeitstest , 2001 .

[18]  P. Schlattmann,et al.  Reduced Event-Related Current Density in the Anterior Cingulate Cortex in Schizophrenia , 2001, NeuroImage.

[19]  D. Senkowski,et al.  Effects of task difficulty on evoked gamma activity and ERPs in a visual discrimination task , 2002, Clinical Neurophysiology.

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

[21]  S. Woods,et al.  Chlorpromazine equivalent doses for the newer atypical antipsychotics. , 2003, The Journal of clinical psychiatry.

[22]  I. Gottesman,et al.  The endophenotype concept in psychiatry: etymology and strategic intentions. , 2003, The American journal of psychiatry.

[23]  W. A. Phillips,et al.  Where the rubber meets the road: The importance of implementation , 2003, Behavioral and Brain Sciences.

[24]  Douglas W. Jones,et al.  Prefrontal broadband noise, working memory, and genetic risk for schizophrenia. , 2004, The American journal of psychiatry.

[25]  R. McCarley,et al.  Neural synchrony indexes disordered perception and cognition in schizophrenia. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[26]  D. Senkowski,et al.  Reduced oscillatory gamma-band responses in unmedicated schizophrenic patients indicate impaired frontal network processing , 2004, Clinical Neurophysiology.

[27]  T. Woo,et al.  Density of glutamic acid decarboxylase 67 messenger RNA-containing neurons that express the N-methyl-D-aspartate receptor subunit NR2A in the anterior cingulate cortex in schizophrenia and bipolar disorder. , 2004, Archives of general psychiatry.

[28]  A Malanda,et al.  Gamma band responses to target and non-target auditory stimuli in humans , 2004, Neuroscience Letters.

[29]  L. Elliot Hong,et al.  Evoked gamma band synchronization and the liability for schizophrenia , 2004, Schizophrenia Research.

[30]  E. Gordon,et al.  "Gamma synchrony" in first-episode schizophrenia: a disorder of temporal connectivity? , 2005, The American journal of psychiatry.

[31]  Marcia A. Bockbrader,et al.  Steady state visual evoked potential abnormalities in schizophrenia , 2005, Clinical Neurophysiology.

[32]  S. Faraone,et al.  Identification of the phenotype in psychiatric genetics , 2005, European Archives of Psychiatry and Clinical Neuroscience.

[33]  O. Bertrand,et al.  Attention modulates gamma-band oscillations differently in the human lateral occipital cortex and fusiform gyrus. , 2005, Cerebral cortex.

[34]  Mark van der Gaag,et al.  The five-factor model of the Positive and Negative Syndrome Scale II: A ten-fold cross-validation of a revised model , 2006, Schizophrenia Research.

[35]  Philip D. Harvey,et al.  Negative symptoms and cognitive deficits: what is the nature of their relationship? , 2006, Schizophrenia bulletin.

[36]  N. Swerdlow,et al.  Gamma Band Oscillations Reveal Neural Network Cortical Coherence Dysfunction in Schizophrenia Patients , 2006, Biological Psychiatry.

[37]  C. Carter,et al.  Impairments in frontal cortical γ synchrony and cognitive control in schizophrenia , 2006, Proceedings of the National Academy of Sciences.

[38]  C. Carter,et al.  Impairments in frontal cortical gamma synchrony and cognitive control in schizophrenia. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[39]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[40]  P. Jonas,et al.  Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks , 2007, Nature Reviews Neuroscience.

[41]  Ingo Fründ,et al.  Stimulus intensity affects early sensory processing: sound intensity modulates auditory evoked gamma-band activity in human EEG. , 2007, International Journal of Psychophysiology.

[42]  W. Singer,et al.  The gamma cycle , 2007, Trends in Neurosciences.

[43]  Gregor Leicht,et al.  Auditory cortex and anterior cingulate cortex sources of the early evoked gamma-band response: Relationship to task difficulty and mental effort , 2007, Neuropsychologia.

[44]  Tony W Wilson,et al.  Cortical gamma generators suggest abnormal auditory circuitry in early-onset psychosis. , 2008, Cerebral cortex.

[45]  Robert W. McCarley,et al.  γ-Band Auditory Steady-State Responses Are Impaired in First Episode Psychosis , 2008, Biological Psychiatry.

[46]  L Elliot Hong,et al.  Sensory gating endophenotype based on its neural oscillatory pattern and heritability estimate. , 2008, Archives of general psychiatry.

[47]  Donald C. Rojas,et al.  Cortical source estimates of gamma band amplitude and phase are different in schizophrenia , 2008, NeuroImage.

[48]  Robert W. McCarley,et al.  Sensory-Evoked Gamma Oscillations in Chronic Schizophrenia , 2008, Biological Psychiatry.

[49]  John O. Willis,et al.  Wechsler Adult Intelligence Scale–Third Edition , 2008 .

[50]  Peter J. Siekmeier,et al.  Modeling GABA alterations in schizophrenia: a link between impaired inhibition and altered gamma and beta range auditory entrainment. , 2008, Journal of neurophysiology.

[51]  Christian Seifert,et al.  Single-trial coupling of EEG and fMRI reveals the involvement of early anterior cingulate cortex activation in effortful decision making , 2008, NeuroImage.

[52]  D. Mathalon,et al.  Event-related EEG time-frequency analysis: an overview of measures and an analysis of early gamma band phase locking in schizophrenia. , 2008, Schizophrenia bulletin.

[53]  R. McCarley,et al.  γ-Band Auditory Steady-State Responses Are Impaired in First Episode Psychosis , 2008, Biological Psychiatry.

[54]  K. Spencer.  The Functional Consequences of Cortical Circuit Abnormalities on Gamma Oscillations in Schizophrenia: Insights from Computational Modeling , 2009, Front. Hum. Neurosci..

[55]  K. Deisseroth,et al.  Parvalbumin neurons and gamma rhythms enhance cortical circuit performance , 2009, Nature.

[56]  Maximilian Reiser,et al.  Single-trial coupling of the gamma-band response and the corresponding BOLD signal , 2010, NeuroImage.

[57]  S. Kapur,et al.  The heterogeneity of antipsychotic response in the treatment of schizophrenia , 2010, Schizophrenia Research.

[58]  Valerie Kirsch,et al.  Reduced Early Auditory Evoked Gamma-Band Response in Patients with Schizophrenia , 2010, Biological Psychiatry.

[59]  W. Singer,et al.  Abnormal neural oscillations and synchrony in schizophrenia , 2010, Nature Reviews Neuroscience.

[60]  Ingo Fründ,et al.  Human gamma-band activity: A review on cognitive and behavioral correlates and network models , 2010, Neuroscience & Biobehavioral Reviews.

[61]  D. Wedding.  Halstead‐Reitan Neuropsychological Test Battery , 2010 .

[62]  S. Kapur,et al.  Trajectories of response to treatment with atypical antipsychotic medication in patients with schizophrenia pooled from 6 double-blind, randomized clinical trials , 2011, Schizophrenia Research.

[63]  D. Rujescu,et al.  Alterations of the early auditory evoked gamma-band response in first-degree relatives of patients with schizophrenia: hints to a new intermediate phenotype. , 2011, Journal of psychiatric research.

[64]  Abnormalities in task‐related neural network formation in schizophrenia , 2011, Acta psychiatrica Scandinavica.

[65]  E. Bramon,et al.  The early auditory gamma-band response is heritable and a putative endophenotype of schizophrenia. , 2011, Schizophrenia bulletin.

[66]  D. Levy,et al.  Sensory gating event-related potentials and oscillations in schizophrenia patients and their unaffected relatives. , 2011, Schizophrenia bulletin.

[67]  J. Edgar,et al.  Gamma synchrony: Towards a translational biomarker for the treatment-resistant symptoms of schizophrenia , 2012, Neuropharmacology.

[68]  Kevin M. Spencer,et al.  Baseline gamma power during auditory steady-state stimulation in schizophrenia , 2012, Front. Hum. Neurosci..

[69]  Jordan P. Hamm,et al.  Augmented gamma band auditory steady-state responses: Support for NMDA hypofunction in schizophrenia , 2012, Schizophrenia Research.

[70]  J. Ford,et al.  Converging evidence for gamma synchrony deficits in schizophrenia. , 2013, Supplements to Clinical neurophysiology.

[71]  Wolf Singer,et al.  High-frequency oscillations and the neurobiology of schizophrenia , 2013, Dialogues in clinical neuroscience.

[72]  J. Ford,et al.  Early auditory gamma-band responses in patients at clinical high risk for schizophrenia. , 2013, Supplements to Clinical neurophysiology.

[73]  R. McCarley,et al.  Early auditory gamma band response abnormalities in first hospitalized schizophrenia. , 2013, Supplements to Clinical neurophysiology.