High-frequency neural oscillations and visual processing deficits in schizophrenia

Visual information is fundamental to how we understand our environment, make predictions, and interact with others. Recent research has underscored the importance of visuo-perceptual dysfunctions for cognitive deficits and pathophysiological processes in schizophrenia. In the current paper, we review evidence for the relevance of high frequency (beta/gamma) oscillations towards visuo-perceptual dysfunctions in schizophrenia. In the first part of the paper, we examine the relationship between beta/gamma band oscillations and visual processing during normal brain functioning. We then summarize EEG/MEG-studies which demonstrate reduced amplitude and synchrony of high-frequency activity during visual stimulation in schizophrenia. In the final part of the paper, we identify neurobiological correlates as well as offer perspectives for future research to stimulate further inquiry into the role of high-frequency oscillations in visual processing impairments in the disorder.

[1]  Matt W. Jones,et al.  Differential effects of NMDA antagonists on high frequency and gamma EEG oscillations in a neurodevelopmental model of schizophrenia , 2012, Neuropharmacology.

[2]  E. Vogel,et al.  Sensory gain control (amplification) as a mechanism of selective attention: electrophysiological and neuroimaging evidence. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[3]  Amy M. Ni,et al.  Strength of Gamma Rhythm Depends on Normalization , 2013, PLoS biology.

[4]  D. Javitt,et al.  Early-stage visual processing deficits in schizophrenia , 2005, Current opinion in psychiatry.

[5]  I. Nelken,et al.  Transient Induced Gamma-Band Response in EEG as a Manifestation of Miniature Saccades , 2008, Neuron.

[6]  John J. Foxe,et al.  Subcortical visual dysfunction in schizophrenia drives secondary cortical impairments. , 2007, Brain : a journal of neurology.

[7]  Krish D. Singh,et al.  Visual gamma oscillations: The effects of stimulus type, visual field coverage and stimulus motion on MEG and EEG recordings , 2013, NeuroImage.

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

[9]  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.

[10]  K H Nuechterlein,et al.  Backward masking performance in unaffected siblings of schizophrenic patients. Evidence for a vulnerability indicator. , 1997, Archives of general psychiatry.

[11]  Streichenwein Sm,et al.  Am J Psychiatry , 1996 .

[12]  S. Kéri,et al.  Different trait markers for schizophrenia and bipolar disorder: a neurocognitive approach , 2001, Psychological Medicine.

[13]  Pat Levitt,et al.  Molecular Characterization of Schizophrenia Viewed by Microarray Analysis of Gene Expression in Prefrontal Cortex , 2000, Neuron.

[14]  Michael F. Green,et al.  Using event related potentials to explore stages of facial affect recognition deficits in schizophrenia. , 2007, Schizophrenia bulletin.

[15]  P. Schyns,et al.  Entrainment of Perceptually Relevant Brain Oscillations by Non-Invasive Rhythmic Stimulation of the Human Brain , 2011, Front. Psychology.

[16]  J. Pernier,et al.  Oscillatory γ-Band (30–70 Hz) Activity Induced by a Visual Search Task in Humans , 1997, The Journal of Neuroscience.

[17]  J. Pernier,et al.  Gamma‐range Activity Evoked by Coherent Visual Stimuli in Humans , 1995, The European journal of neuroscience.

[18]  Krish D. Singh,et al.  Induced visual illusions and gamma oscillations in human primary visual cortex , 2004, The European journal of neuroscience.

[19]  Stefan Kasicki,et al.  Differential effects produced by ketamine on oscillatory activity recorded in the rat hippocampus, dorsal striatum and nucleus accumbens , 2011, Journal of psychopharmacology.

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

[21]  A. Thiele,et al.  Comparison of spatial integration and surround suppression characteristics in spiking activity and the local field potential in macaque V1 , 2008, The European journal of neuroscience.

[22]  Caspar M. Schwiedrzik,et al.  (Micro)Saccades, corollary activity and cortical oscillations , 2009, Trends in Cognitive Sciences.

[23]  A. Kohn,et al.  No Consistent Relationship between Gamma Power and Peak Frequency in Macaque Primary Visual Cortex , 2013, The Journal of Neuroscience.

[24]  M. Mørup,et al.  Attenuation of beta and gamma oscillations in schizophrenia spectrum patients following hand posture perturbation , 2011, Psychiatry Research.

[25]  R. McCarley,et al.  Early and late stages of visual processing in individuals in prodromal state and first episode schizophrenia: An ERP study , 2013, Schizophrenia Research.

[26]  Vincent A Magnotta,et al.  Global white matter abnormalities in schizophrenia: a multisite diffusion tensor imaging study. , 2011, Schizophrenia bulletin.

[27]  Krish D. Singh,et al.  Spatiotemporal frequency tuning of BOLD and gamma band MEG responses compared in primary visual cortex , 2008, NeuroImage.

[28]  E. Whitham,et al.  Scalp electrical recording during paralysis: Quantitative evidence that EEG frequencies above 20Hz are contaminated by EMG , 2007, Clinical Neurophysiology.

[29]  G. González-Burgos,et al.  Perisomatic inhibition and cortical circuit dysfunction in schizophrenia , 2011, Current Opinion in Neurobiology.

[30]  Gregor Thut,et al.  Rhythmic TMS over Parietal Cortex Links Distinct Brain Frequencies to Global versus Local Visual Processing , 2011, Current Biology.

[31]  E. G. Jones,et al.  Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics. , 1995, Archives of general psychiatry.

[32]  W. Singer,et al.  Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex , 1991, Science.

[33]  C. Schroeder,et al.  Predictive Suppression of Cortical Excitability and Its Deficit in Schizophrenia , 2013, The Journal of Neuroscience.

[34]  D. Lewis,et al.  NMDA receptor hypofunction, parvalbumin-positive neurons, and cortical gamma oscillations in schizophrenia. , 2012, Schizophrenia bulletin.

[35]  Klaus P. Ebmeier,et al.  Magnetic resonance imaging studies in bipolar disorder and schizophrenia: meta-analysis. , 2009, The British journal of psychiatry : the journal of mental science.

[36]  Pascal Fries,et al.  A Microsaccadic Rhythm Modulates Gamma-Band Synchronization and Behavior , 2009, The Journal of Neuroscience.

[37]  P. Goldman-Rakic,et al.  The reduced neuropil hypothesis: a circuit based model of schizophrenia , 1999, Biological Psychiatry.

[38]  Randolph Blake,et al.  Weakened Center-Surround Interactions in Visual Motion Processing in Schizophrenia , 2006, The Journal of Neuroscience.

[39]  R. Desimone,et al.  Laminar differences in gamma and alpha coherence in the ventral stream , 2011, Proceedings of the National Academy of Sciences.

[40]  Christoph S. Herrmann,et al.  Anticipation of natural stimuli modulates EEG dynamics: physiology and simulation , 2008, Cognitive Neurodynamics.

[41]  F. Varela,et al.  Perception's shadow: long-distance synchronization of human brain activity , 1999, Nature.

[42]  Jong H. Yoon,et al.  GABA Concentration Is Reduced in Visual Cortex in Schizophrenia and Correlates with Orientation-Specific Surround Suppression , 2010, The Journal of Neuroscience.

[43]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

[44]  W. Singer,et al.  Neural Synchrony in Brain Disorders: Relevance for Cognitive Dysfunctions and Pathophysiology , 2006, Neuron.

[45]  Stefan Debener,et al.  Size matters: effects of stimulus size, duration and eccentricity on the visual gamma-band response , 2004, Clinical Neurophysiology.

[46]  Pejman Sehatpour,et al.  Early visual sensory deficits as endophenotypes for schizophrenia: high-density electrical mapping in clinically unaffected first-degree relatives. , 2006, Archives of general psychiatry.

[47]  A. Kohn,et al.  Gamma and the Coordination of Spiking Activity in Early Visual Cortex , 2013, Neuron.

[48]  W Gaebel,et al.  Neurophysiological correlates of the recognition of facial expressions of emotion as revealed by magnetoencephalography. , 1999, Brain research. Cognitive brain research.

[49]  R. Straub,et al.  Genetic variation in the 6p22.3 gene DTNBP1, the human ortholog of the mouse dysbindin gene, is associated with schizophrenia. , 2002, American journal of human genetics.

[50]  Frances M De Blasio,et al.  Event-related EEG time-frequency analysis and the Orienting Reflex to auditory stimuli. , 2012, Psychophysiology.

[51]  O. Jensen,et al.  Gamma Power Is Phase-Locked to Posterior Alpha Activity , 2008, PloS one.

[52]  Catherine Tallon-Baudry,et al.  The many faces of the gamma band response to complex visual stimuli , 2005, NeuroImage.

[53]  Anina N. Rich,et al.  Spatial attention increases high-frequency gamma synchronisation in human medial visual cortex , 2013, NeuroImage.

[54]  G. DeAngelis,et al.  Does Neuronal Synchrony Underlie Visual Feature Grouping? , 2005, Neuron.

[55]  Wolf Singer,et al.  Deficits in high- (>60 Hz) gamma-band oscillations during visual processing in schizophrenia , 2013, Front. Hum. Neurosci..

[56]  W. Singer,et al.  Stimulus-dependent synchronization of neuronal responses in the visual cortex of the awake macaque monkey , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[57]  B. Kocsis,et al.  Comparison of the effects of acute and chronic administration of ketamine on hippocampal oscillations: relevance for the NMDA receptor hypofunction model of schizophrenia , 2011, Brain Structure and Function.

[58]  R S Kahn,et al.  Structural brain abnormalities in patients with schizophrenia and their healthy siblings. , 2000, The American journal of psychiatry.

[59]  S Purcell,et al.  De novo CNV analysis implicates specific abnormalities of postsynaptic signalling complexes in the pathogenesis of schizophrenia , 2011, Molecular Psychiatry.

[60]  A. Sampson,et al.  Gene Expression Deficits in a Subclass of GABA Neurons in the Prefrontal Cortex of Subjects with Schizophrenia , 2003, The Journal of Neuroscience.

[61]  W. Singer,et al.  Gamma oscillations: precise temporal coordination without a metronome , 2013, Trends in Cognitive Sciences.

[62]  John J. Foxe,et al.  Visual sensory processing deficits in schizophrenia: Is there anything to the magnocellular account? , 2012, Schizophrenia Research.

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

[64]  F. Resch,et al.  Evidence for a magnocellular disadvantage in early-onset schizophrenic patients: A source analysis of the N80 visual-evoked component , 2013, Schizophrenia Research.

[65]  Christoph S. Herrmann,et al.  Evoked γ oscillations in human scalp EEG are test–retest reliable , 2007, Clinical Neurophysiology.

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

[67]  Catherine Tallon-Baudry,et al.  The roles of gamma-band oscillatory synchrony in human visual cognition. , 2009, Frontiers in bioscience.

[68]  R. McCarley,et al.  Functional and structural deficits in brain regions subserving face perception in schizophrenia. , 2006, The American journal of psychiatry.

[69]  Bruce I. Turetsky,et al.  Global–Local Visual Processing in Schizophrenia: Evidence for an Early Visual Processing Deficit , 2005, Biological Psychiatry.

[70]  C. Schroeder,et al.  Low-frequency neuronal oscillations as instruments of sensory selection , 2009, Trends in Neurosciences.

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

[72]  P. Benson,et al.  Simple Viewing Tests Can Detect Eye Movement Abnormalities That Distinguish Schizophrenia Cases from Controls with Exceptional Accuracy , 2012, Biological Psychiatry.

[73]  Emil Kraepelin,et al.  Dementia praecox and paraphrenia , 2002 .

[74]  Sonja Grün,et al.  Saccade-Related Modulations of Neuronal Excitability Support Synchrony of Visually Elicited Spikes , 2011, Cerebral cortex.

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

[76]  Martha Elizabeth Shenton,et al.  Predicting inter-hemispheric transfer time from the diffusion properties of the corpus callosum in healthy individuals and schizophrenia patients: A combined ERP and DTI study , 2011, NeuroImage.

[77]  Khalid Hamandi,et al.  The properties of induced gamma oscillations in human visual cortex show individual variability in their dependence on stimulus size , 2013, NeuroImage.

[78]  John J. Foxe,et al.  Early visual processing deficits in schizophrenia: impaired P1 generation revealed by high-density electrical mapping , 2001, Neuroreport.

[79]  M. Kubicki,et al.  Diffusion Tensor Imaging, Structural Connectivity, and Schizophrenia , 2011, Schizophrenia research and treatment.

[80]  M. Siegel,et al.  Dissociating neuronal gamma-band activity from cranial and ocular muscle activity in EEG , 2013, Front. Hum. Neurosci..

[81]  J. Rieger,et al.  Stimulus intensity affects early sensory processing: visual contrast modulates evoked gamma-band activity in human EEG. , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[82]  Jasna Martinovic,et al.  High frequency oscillations as a correlate of visual perception. , 2011, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

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

[85]  T. Womelsdorf,et al.  Attentional Stimulus Selection through Selective Synchronization between Monkey Visual Areas , 2012, Neuron.

[86]  G. Buzsáki,et al.  Mechanisms of gamma oscillations. , 2012, Annual review of neuroscience.

[87]  W. Freeman,et al.  Frequency analysis of olfactory system EEG in cat, rabbit, and rat. , 1980, Electroencephalography and clinical neurophysiology.

[88]  Jessica A. Cardin,et al.  A critical role for NMDA receptors in parvalbumin interneurons for gamma rhythm induction and behavior , 2011, Molecular Psychiatry.

[89]  Y. Kubota,et al.  GABAergic cell subtypes and their synaptic connections in rat frontal cortex. , 1997, Cerebral cortex.

[90]  Daniel C. Javitt,et al.  Impairments in generation of early-stage transient visual evoked potentials to magno- and parvocellular-selective stimuli in schizophrenia , 2005, Clinical Neurophysiology.

[91]  E. John,et al.  Perceptual framing and cortical alpha rhythm , 1981, Neuropsychologia.

[92]  Matthias M. Müller,et al.  Brain electrical tomography (BET) analysis of induced gamma band responses during a simple object recognition task , 2006, NeuroImage.

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

[94]  G. Buzsáki,et al.  Gamma Oscillation by Synaptic Inhibition in a Hippocampal Interneuronal Network Model , 1996, The Journal of Neuroscience.

[95]  John J. Foxe,et al.  Impaired visual object recognition and dorsal/ventral stream interaction in schizophrenia. , 2002, Archives of general psychiatry.

[96]  C. Tallon-Baudry,et al.  Neural Dissociation between Visual Awareness and Spatial Attention , 2008, The Journal of Neuroscience.

[97]  P. Uhlhaas,et al.  Perceptual organization in schizophrenia spectrum disorders: empirical research and theoretical implications. , 2005, Psychological bulletin.

[98]  Mooney Cm,et al.  A new closure test. , 1951 .

[99]  Michael F. Green,et al.  Event-related gamma activity in schizophrenia patients during a visual backward-masking task. , 2005, The American journal of psychiatry.

[100]  S. Dakin,et al.  Visual Perception and Its Impairment in Schizophrenia , 2008, Biological Psychiatry.

[101]  W. Freeman,et al.  Spatial EEG patterns, non-linear dynamics and perception: the neo-sherringtonian view , 1985, Brain Research Reviews.

[102]  D. Lewis,et al.  Cortical inhibitory neurons and schizophrenia , 2005, Nature Reviews Neuroscience.

[103]  Jean Bullier,et al.  The Timing of Information Transfer in the Visual System , 1997 .

[104]  Michael F. Green,et al.  Visual masking as a probe for abnormal gamma range activity in schizophrenia , 2003, Biological Psychiatry.

[105]  Derek K. Jones,et al.  Visual gamma oscillations and evoked responses: Variability, repeatability and structural MRI correlates , 2010, NeuroImage.

[106]  P. Fries,et al.  Robust Gamma Coherence between Macaque V1 and V2 by Dynamic Frequency Matching , 2013, Neuron.

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

[108]  W. Singer,et al.  Alpha Phase Locking Predicts Residual Working Memory Performance in Schizophrenia , 2010, Biological Psychiatry.

[109]  Miles A Whittington,et al.  Cellular mechanisms of neuronal population oscillations in the hippocampus in vitro. , 2004, Annual review of neuroscience.

[110]  Emilio Salinas,et al.  Gain Modulation A Major Computational Principle of the Central Nervous System , 2000, Neuron.

[111]  Michael R. Green,et al.  Gene Expression , 1993, Progress in Gene Expression.

[112]  W. Singer,et al.  Synchronization of Neural Activity across Cortical Areas Correlates with Conscious Perception , 2007, The Journal of Neuroscience.

[113]  D. V. Essen,et al.  Neural mechanisms of form and motion processing in the primate visual system , 1994, Neuron.

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

[115]  J. Ford.  Schizophrenia: the broken P300 and beyond. , 1999, Psychophysiology.

[116]  John J. Foxe,et al.  Filling-in in schizophrenia: a high-density electrical mapping and source-analysis investigation of illusory contour processing. , 2005, Cerebral cortex.

[117]  C. Gray.  The Temporal Correlation Hypothesis of Visual Feature Integration Still Alive and Well , 1999, Neuron.

[118]  R. VanRullen,et al.  The Phase of Ongoing Oscillations Mediates the Causal Relation between Brain Excitation and Visual Perception , 2011, The Journal of Neuroscience.

[119]  P. Sullivan,et al.  Schizophrenia as a complex trait: evidence from a meta-analysis of twin studies. , 2003, Archives of general psychiatry.

[120]  Mark Slifstein,et al.  Elevated prefrontal cortex γ-aminobutyric acid and glutamate-glutamine levels in schizophrenia measured in vivo with proton magnetic resonance spectroscopy. , 2012, Archives of general psychiatry.

[121]  B. O’Donnell,et al.  Auditory event-related potential abnormalities in bipolar disorder and schizophrenia. , 2004, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[122]  Deanna Greenstein,et al.  Structural brain MRI abnormalities in healthy siblings of patients with childhood-onset schizophrenia. , 2003, The American journal of psychiatry.

[123]  Catherine Tallon-Baudry,et al.  Visual Grouping and the Focusing of Attention Induce Gamma-band Oscillations at Different Frequencies in Human Magnetoencephalogram Signals , 2006, Journal of Cognitive Neuroscience.

[124]  P. Goldman-Rakic,et al.  Abnormally high neuronal density in the schizophrenic cortex. A morphometric analysis of prefrontal area 9 and occipital area 17. , 1995, Archives of general psychiatry.

[125]  G. Rousselet,et al.  Single-Trial Analyses: Why Bother? , 2011, Front. Psychology.

[126]  Andreas K. Engel,et al.  Oscillatory Synchronization in Large-Scale Cortical Networks Predicts Perception , 2011, Neuron.

[127]  W. Singer,et al.  Synchrony Makes Neurons Fire in Sequence, and Stimulus Properties Determine Who Is Ahead , 2011, The Journal of Neuroscience.

[128]  W. Singer,et al.  Neuroelectromagnetic Correlates of Perceptual Closure Processes , 2010, The Journal of Neuroscience.

[129]  W. Singer,et al.  Neural Synchrony in Cortical Networks: History, Concept and Current Status , 2009, Front. Integr. Neurosci..

[130]  T. Womelsdorf,et al.  The role of neuronal synchronization in selective attention , 2007, Current Opinion in Neurobiology.

[131]  D. Javitt.  When doors of perception close: bottom-up models of disrupted cognition in schizophrenia. , 2009, Annual review of clinical psychology.

[132]  D. Lewis.  GABAergic local circuit neurons and prefrontal cortical dysfunction in schizophrenia , 2000, Brain Research Reviews.

[133]  Michael F. Green,et al.  Visual masking in schizophrenia: overview and theoretical implications. , 2011, Schizophrenia bulletin.

[134]  K. Nuechterlein,et al.  Backward masking in schizophrenia and mania. I. Specifying a mechanism. , 1994, Archives of general psychiatry.

[135]  A. Tzelepi,et al.  Functional properties of sub-bands of oscillatory brain waves to pattern visual stimulation in man , 2000, Clinical Neurophysiology.

[136]  T. Robbins,et al.  Decision making deficits in patients with first-episode and chronic schizophrenia , 2002, Schizophrenia Research.

[137]  P. O’Donnell,et al.  Gamma and Delta Neural Oscillations and Association with Clinical Symptoms under Subanesthetic Ketamine , 2010, Neuropsychopharmacology.

[138]  P. Schyns,et al.  Rhythmic TMS Causes Local Entrainment of Natural Oscillatory Signatures , 2011, Current Biology.

[139]  David A Lewis,et al.  Primary visual cortex volume and total neuron number are reduced in schizophrenia , 2007, The Journal of comparative neurology.

[140]  Paul J. Harrison,et al.  Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence , 2005, Molecular Psychiatry.

[141]  M. A. Smith,et al.  Stimulus Selectivity and Spatial Coherence of Gamma Components of the Local Field Potential , 2011, The Journal of Neuroscience.

[142]  David A. Lewis,et al.  Cortical parvalbumin interneurons and cognitive dysfunction in schizophrenia , 2012, Trends in Neurosciences.

[143]  Gijs Plomp,et al.  Electrophysiological evidence for ventral stream deficits in schizophrenia patients. , 2013, Schizophrenia bulletin.

[144]  M. MacIver,et al.  Anesthetic-induced burst suppression EEG activity requires glutamate-mediated excitatory synaptic transmission. , 2005, Cerebral cortex.

[145]  J. Waddington,et al.  Susceptibility genes for schizophrenia: Characterisation of mutant mouse models at the level of phenotypic behaviour , 2007, Neuroscience & Biobehavioral Reviews.

[146]  W. Singer,et al.  Impaired Gamma-Band Activity during Perceptual Organization in Adults with Autism Spectrum Disorders: Evidence for Dysfunctional Network Activity in Frontal-Posterior Cortices , 2012, The Journal of Neuroscience.

[147]  S. Tobimatsu,et al.  Studies of human visual pathophysiology with visual evoked potentials , 2006, Clinical Neurophysiology.

[148]  S. Muthukumaraswamy.  High-frequency brain activity and muscle artifacts in MEG/EEG: a review and recommendations , 2013, Front. Hum. Neurosci..

[149]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

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

[151]  E. Basar,et al.  Disturbance in long distance gamma coherence in bipolar disorder , 2010, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[152]  D. Jane,et al.  Pre‐ and post‐synaptic functions of kainate receptors at glutamate and GABA synapses in the rat entorhinal cortex , 2012, Hippocampus.

[153]  A. Sampson,et al.  GABA transporter-1 mRNA in the prefrontal cortex in schizophrenia: decreased expression in a subset of neurons. , 2001, The American journal of psychiatry.

[154]  C. M. Mooney,et al.  A new closure test. , 1951, Canadian journal of psychology.

[155]  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.

[156]  D. Javitt,et al.  Magnocellular and parvocellular contributions to backward masking dysfunction in schizophrenia , 2003, Schizophrenia Research.

[157]  M. Herrmann,et al.  Early-stage face processing dysfunction in patients with schizophrenia. , 2004, The American journal of psychiatry.

[158]  W. Singer,et al.  Synchronization Dynamics in Response to Plaid Stimuli in Monkey V1 , 2009, Cerebral cortex.

[159]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[160]  J. Klosterkötter,et al.  Diagnosing schizophrenia in the initial prodromal phase , 2000, Schizophrenia Research.

[161]  Vladislav Volman,et al.  Downregulation of Parvalbumin at Cortical GABA Synapses Reduces Network Gamma Oscillatory Activity , 2011, The Journal of Neuroscience.

[162]  Jorge V. José,et al.  Synchronization as a mechanism for attentional gain modulation , 2004, Neurocomputing.

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

[164]  E. Adrian,et al.  The electrical activity of the mammalian olfactory bulb. , 1950, Electroencephalography and clinical neurophysiology.

[165]  Edward O. Mann,et al.  Role of GABAergic inhibition in hippocampal network oscillations , 2007, Trends in Neurosciences.

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

[167]  G. Tononi,et al.  Reduced natural oscillatory frequency of frontal thalamocortical circuits in schizophrenia. , 2012, Archives of general psychiatry.

[168]  Catherine Tallon-Baudry,et al.  Unconscious Learning versus Visual Perception: Dissociable Roles for Gamma Oscillations Revealed in MEG , 2009, Journal of Cognitive Neuroscience.

[169]  John H. R. Maunsell,et al.  How parallel are the primate visual pathways? , 1993, Annual review of neuroscience.

[170]  C. Gray,et al.  Dynamics of striate cortical activity in the alert macaque: I. Incidence and stimulus-dependence of gamma-band neuronal oscillations. , 2000, Cerebral cortex.

[171]  S. Hillyard,et al.  Involvement of striate and extrastriate visual cortical areas in spatial attention , 1999, Nature Neuroscience.

[172]  Jordan P. Hamm,et al.  Abnormalities of Neuronal Oscillations and Temporal Integration to Low- and High-Frequency Auditory Stimulation in Schizophrenia , 2011, Biological Psychiatry.

[173]  Markus Butz,et al.  Sustained gamma band synchronization in early visual areas reflects the level of selective attention , 2012, NeuroImage.

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

[175]  B. Turetsky,et al.  Facial emotion recognition in schizophrenia:When and why does it go awry? , 2007, Schizophrenia Research.

[176]  S. Akbarian,et al.  Molecular and cellular mechanisms of altered GAD1/GAD67 expression in schizophrenia and related disorders , 2006, Brain Research Reviews.

[177]  John J. Foxe,et al.  Parvocellular and Magnocellular Contributions to the Initial Generators of the Visual Evoked Potential: High-Density Electrical Mapping of the “C1” Component , 2008, Brain Topography.

[178]  A. Engel,et al.  Neuronal Synchronization along the Dorsal Visual Pathway Reflects the Focus of Spatial Attention , 2008, Neuron.

[179]  P. Uhlhaas,et al.  Perceptual anomalies in schizophrenia: integrating phenomenology and cognitive neuroscience. , 2006, Schizophrenia bulletin.

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

[181]  Gareth R. Barnes,et al.  Stimuli of varying spatial scale induce gamma activity with distinct temporal characteristics in human visual cortex , 2007, NeuroImage.

[182]  C. Tallon-Baudry,et al.  How Ongoing Fluctuations in Human Visual Cortex Predict Perceptual Awareness: Baseline Shift versus Decision Bias , 2009, The Journal of Neuroscience.

[183]  Randolph Blake,et al.  Visual Context Processing in Schizophrenia , 2013, Clinical psychological science : a journal of the Association for Psychological Science.

[184]  G. Buzsáki,et al.  Cellular bases of hippocampal EEG in the behaving rat , 1983, Brain Research Reviews.

[185]  E. Bramon,et al.  Meta-analysis of the P300 and P50 waveforms in schizophrenia , 2004, Schizophrenia Research.

[186]  J. Kaas,et al.  Extrastriate Cortex in Primates , 1997, Cerebral Cortex.

[187]  R. Gur,et al.  Dysbindin-1 mutant mice implicate reduced fast-phasic inhibition as a final common disease mechanism in schizophrenia , 2011, Proceedings of the National Academy of Sciences.

[188]  David A Lewis,et al.  Conserved regional patterns of GABA-related transcript expression in the neocortex of subjects with schizophrenia. , 2008, The American journal of psychiatry.

[189]  W. Singer,et al.  Gamma Responses Correlate with Temporal Expectation in Monkey Primary Visual Cortex , 2011, The Journal of Neuroscience.

[190]  K. Sauvé.  Gamma-Band Synchronous Oscillations: Recent Evidence Regarding Their Functional Significance , 1999, Consciousness and Cognition.

[191]  J. Maunsell,et al.  Differences in Gamma Frequencies across Visual Cortex Restrict Their Possible Use in Computation , 2010, Neuron.

[192]  W. Singer,et al.  Dysfunctional Long-Range Coordination of Neural Activity during Gestalt Perception in Schizophrenia , 2006, The Journal of Neuroscience.

[193]  Y. Chen,et al.  Abnormal visual motion processing in schizophrenia: a review of research progress. , 2011, Schizophrenia bulletin.

[194]  W G Sannita,et al.  Scalp-recorded oscillatory potentials evoked by transient pattern-reversal visual stimulation in man. , 1995, Electroencephalography and clinical neurophysiology.

[195]  A. Revonsuo,et al.  The neural generation of a unified illusion in human vision , 1997, Neuroreport.

[196]  Jessica A. Cardin,et al.  Driving fast-spiking cells induces gamma rhythm and controls sensory responses , 2009, Nature.

[197]  W. Freeman.  The physiology of perception. , 1991, Scientific American.

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

[199]  W Gaebel,et al.  Disturbed facial affect recognition in patients with schizophrenia associated with hypoactivity in distributed brain regions: a magnetoencephalographic study. , 2001, The American journal of psychiatry.

[200]  A. Thiele,et al.  Neuronal synchrony does not correlate with motion coherence in cortical area MT , 2003, Nature.

[201]  W. Singer,et al.  Cortical Oscillatory Activity Is Critical for Working Memory as Revealed by Deficits in Early-Onset Schizophrenia , 2009, The Journal of Neuroscience.

[202]  Michael N. Shadlen,et al.  Synchrony Unbound A Critical Evaluation of the Temporal Binding Hypothesis , 1999, Neuron.

[203]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[204]  G. Barnes,et al.  Induced Gamma activity in primary visual cortex is related to luminance and not color contrast: An MEG study. , 2008, Journal of vision.

[205]  C. Herrmann.  Human EEG responses to 1–100 Hz flicker: resonance phenomena in visual cortex and their potential correlation to cognitive phenomena , 2001, Experimental Brain Research.

[206]  E. Bleuler.  [Dementia praecox or the group of schizophrenias]. , 1968, Vertex.

[207]  Matthias M. Müller,et al.  Human Gamma Band Activity and Perception of a Gestalt , 1999, The Journal of Neuroscience.

[208]  Lakshminarayan V. Chinta,et al.  Disrupted cortical conductivity in schizophrenia: TMS-EEG study. , 2014, Cerebral cortex.

[209]  Cameron S Carter,et al.  Gamma Oscillatory Power is Impaired During Cognitive Control Independent of Medication Status in First-Episode Schizophrenia , 2010, Neuropsychopharmacology.

[210]  A. Fisahn,et al.  Neuregulin-1 modulates hippocampal gamma oscillations: implications for schizophrenia. , 2009, Cerebral cortex.

[211]  D. Spinelli,et al.  Spatiotemporal analysis of the cortical sources of the steady‐state visual evoked potential , 2007, Human brain mapping.

[212]  P. Fries,et al.  Magnetoencephalography in Twins Reveals a Strong Genetic Determination of the Peak Frequency of Visually Induced Gamma-Band Synchronization , 2012, The Journal of Neuroscience.

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

[214]  U. Frith,et al.  Vagaries of Visual Perception in Autism , 2005, Neuron.

[215]  Krish D. Singh,et al.  Orientation Discrimination Performance Is Predicted by GABA Concentration and Gamma Oscillation Frequency in Human Primary Visual Cortex , 2009, The Journal of Neuroscience.

[216]  Danko Nikolić,et al.  Frequencies of gamma/beta oscillations are stably tuned to stimulus properties , 2010, Neuroreport.

[217]  P. Meehl.  Factors and Taxa, Traits and Types, Differences of Degree and Differences in Kind , 1992 .

[218]  K. D. Singh,et al.  Spectral properties of induced and evoked gamma oscillations in human early visual cortex to moving and stationary stimuli. , 2009, Journal of neurophysiology.

[219]  Daniel C. Javitt,et al.  Magnocellular contributions to impaired motion processing in schizophrenia , 2006, Schizophrenia Research.

[220]  Sarah A. J. Reading,et al.  Neurobiology of Schizophrenia , 2006, Neuron.

[221]  R. Traub,et al.  Region-specific changes in gamma and beta2 rhythms in NMDA receptor dysfunction models of schizophrenia. , 2008, Schizophrenia bulletin.

[222]  E. J. Place,et al.  Perceptual organization in schizophrenia. , 1980, Journal of abnormal psychology.

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

[224]  S. Silverstein,et al.  Stimulus configuration and context effects in perceptual organization in schizophrenia. , 1996, Journal of abnormal psychology.

[225]  Andreas K. Engel,et al.  The saccadic spike artifact in MEG , 2012, NeuroImage.

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

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

[228]  Randolph Blake,et al.  Callosal Connections of Primary Visual Cortex Predict the Spatial Spreading of Binocular Rivalry Across the Visual Hemifields , 2011, Front. Hum. Neurosci..

[229]  A. Antal,et al.  Transcranial alternating current stimulation (tACS) , 2013, Front. Hum. Neurosci..

[230]  C. Schroeder,et al.  A spatiotemporal profile of visual system activation revealed by current source density analysis in the awake macaque. , 1998, Cerebral cortex.

[231]  Miles A. Whittington,et al.  Human Neuroscience , 2022 .

[232]  Luc H. Arnal,et al.  Cortical oscillations and sensory predictions , 2012, Trends in Cognitive Sciences.

[233]  K H Nuechterlein,et al.  Backward masking in unmedicated schizophrenic patients in psychotic remission: possible reflection of aberrant cortical oscillation. , 1999, The American journal of psychiatry.

[234]  A. Engel,et al.  Cognitive functions of gamma-band activity: memory match and utilization , 2004, Trends in Cognitive Sciences.

[235]  W. Singer,et al.  Neuronal Dynamics and Neuropsychiatric Disorders: Toward a Translational Paradigm for Dysfunctional Large-Scale Networks , 2012, Neuron.

[236]  Martin Vreugdenhil,et al.  NMDA Receptor Hypofunction Phase Couples Independent γ-Oscillations in the Rat Visual Cortex , 2011, Neuropsychopharmacology.

[237]  W. A. Phillips,et al.  Perceptual grouping in disorganized schizophrenia , 2006, Psychiatry Research.

[238]  S. Hillyard,et al.  Cortical sources of the early components of the visual evoked potential , 2002, Human brain mapping.

[239]  Jorge V. José,et al.  Inhibitory synchrony as a mechanism for attentional gain modulation , 2004, Journal of Physiology-Paris.

[240]  Daniel C Javitt,et al.  Early sensory contributions to contextual encoding deficits in schizophrenia. , 2011, Archives of general psychiatry.

[241]  K. Nakazawa,et al.  Postnatal NMDA receptor ablation in corticolimbic interneurons confers schizophrenia-like phenotypes , 2010, Nature Neuroscience.