Abnormal Entropy Modulation of the EEG Signal in Patients With Schizophrenia During the Auditory Paired-Stimulus Paradigm

The complexity change in brain activity in schizophrenia is an interesting topic clinically. Schizophrenia patients exhibit abnormal task-related modulation of complexity, following entropy of electroencephalogram (EEG) analysis. However, complexity modulation in schizophrenia patients during the sensory gating (SG) task, remains unknown. In this study, the classical auditory paired-stimulus paradigm was introduced to investigate SG, and EEG data were recorded from 55 normal controls and 61 schizophrenia patients. Fuzzy entropy (FuzzyEn) was used to explore the complexity of brain activity under the conditions of baseline (BL) and the auditory paired-stimulus paradigm (S1 and S2). Generally, schizophrenia patients showed significantly higher FuzzyEn values in the frontal and occipital regions of interest (ROIs). Relative to the BL condition, the normalized values of FuzzyEn of normal controls were decreased greatly in condition S1 and showed less variance in condition S2. Schizophrenia patients showed a smaller decrease in the normalized values in condition S1. Moreover, schizophrenia patients showed significant diminution in the suppression ratios of FuzzyEn, attributed to the higher FuzzyEn values in condition S1. These results suggested that entropy modulation during the process of sensory information and SG was obvious in normal controls and significantly deficient in schizophrenia patients. Additionally, the FuzzyEn values measured in the frontal ROI were positively correlated with positive scores of Positive and Negative Syndrome Scale (PANSS), indicating that frontal entropy was a potential indicator in evaluating the clinical symptoms. However, negative associations were found between the FuzzyEn values of occipital ROIs and general and total scores of PANSS, likely reflecting the compensation effect in visual processing. Thus, our findings provided a deeper understanding of the deficits in sensory information processing and SG, which contribute to cognitive deficits and symptoms in patients with schizophrenia.

[1]  Tianyi Yan,et al.  Wide-field retinotopy distinguish subregions of the human MT+ by functional magnetic resonance imaging , 2010, IEEE/ICME International Conference on Complex Medical Engineering.

[2]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[3]  S. Tong,et al.  Abnormal EEG complexity in patients with schizophrenia and depression , 2008, Clinical Neurophysiology.

[4]  R Freedman,et al.  Nicotinic receptor function in schizophrenia. , 1996, Schizophrenia bulletin.

[5]  Zehong Cao,et al.  Inherent Fuzzy Entropy for the Improvement of EEG Complexity Evaluation , 2018, IEEE Transactions on Fuzzy Systems.

[6]  Zhendong Mu,et al.  Driver Fatigue Detection System Using Electroencephalography Signals Based on Combined Entropy Features , 2017 .

[7]  E. Herbener,et al.  Social perception in schizophrenia: Evidence of temporo-occipital and prefrontal dysfunction , 2013, Psychiatry Research: Neuroimaging.

[8]  Koichi Takahashi,et al.  Antipsychotics reverse abnormal EEG complexity in drug-naive schizophrenia: A multiscale entropy analysis , 2010, NeuroImage.

[9]  H. Sauer,et al.  Cortical surface complexity in frontal and temporal areas varies across subgroups of schizophrenia , 2014, Human brain mapping.

[10]  Chin-Teng Lin,et al.  Extraction of SSVEPs-Based Inherent Fuzzy Entropy Using a Wearable Headband EEG in Migraine Patients , 2018, IEEE Transactions on Fuzzy Systems.

[11]  D L Braff,et al.  Sensorimotor gating and schizophrenia. Human and animal model studies. , 1990, Archives of general psychiatry.

[12]  Daniel Senkowski,et al.  Positive and Negative Symptoms in Schizophrenia Relate to Distinct Oscillatory Signatures of Sensory Gating , 2016, Front. Hum. Neurosci..

[13]  K. Cheng,et al.  Analysis of EEG entropy during visual evocation of emotion in schizophrenia , 2017, Annals of General Psychiatry.

[14]  Tadashi Fujita,et al.  Influences of reduced masticatory sensory input from soft-diet feeding upon spatial memory/learning ability in mice. , 2007, Biomedical research.

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

[16]  Michael F. Green,et al.  Gating Deficit Heritability and Correlation With Increased Clinical Severity in Schizophrenia Patients With Positive Family History. , 2016, The American journal of psychiatry.

[17]  Roberto Hornero,et al.  Complexity and schizophrenia , 2013, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[18]  Dc Washington Diagnostic and Statistical Manual of Mental Disorders, 4th Ed. , 1994 .

[19]  Javier Gomez-Pilar,et al.  Deficit of entropy modulation of the EEG in schizophrenia associated to cognitive performance and symptoms. A replication study , 2017, Schizophrenia Research.

[20]  T Toulopoulou,et al.  Do COMT, BDNF and NRG1 polymorphisms influence P50 sensory gating in psychosis? , 2010, Psychological Medicine.

[21]  Muriel Walshe,et al.  Do COMT, BDNF and NRG-1 polymorphisms influence P50 sensory gating in psychosis? , 2011 .

[22]  N. Huang,et al.  The empirical mode decomposition and the Hilbert spectrum for nonlinear and non-stationary time series analysis , 1998, Proceedings of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[23]  George Zouridakis,et al.  The P50 component of the auditory evoked potential and subtypes of schizophrenia , 1993, Psychiatry Research.

[24]  Mengmeng Zhang,et al.  Age-related oscillatory theta modulation of multisensory integration in frontocentral regions , 2016, Neuroreport.

[25]  Paul J. Harrison,et al.  Schizophrenia and the frontal lobes: post-mortem stereological study of tissue volume. , 2001, The British journal of psychiatry : the journal of mental science.

[26]  Celso Arango,et al.  Neuropsychological correlates of P50 sensory gating in patients with schizophrenia , 2013, Schizophrenia Research.

[27]  Wangxin Yu,et al.  Characterization of Surface EMG Signal Based on Fuzzy Entropy , 2007, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[28]  Yang Li,et al.  An Alpha resting EEG study on nonlinear dynamic analysis for schizophrenia , 2013, 2013 6th International IEEE/EMBS Conference on Neural Engineering (NER).

[29]  B. Turetsky,et al.  Neurophysiological endophenotypes of schizophrenia: the viability of selected candidate measures. , 2006, Schizophrenia bulletin.

[30]  van M.H. Emden,et al.  An analysis of complexity , 1971 .

[31]  Judith M Ford,et al.  Divergent approaches converge on frontal lobe dysfunction in schizophrenia. , 2008, The American journal of psychiatry.

[32]  Alexander Cerquera,et al.  Comparing EEG Nonlinearity in Deficit and Nondeficit Schizophrenia Patients: Preliminary Data , 2017, Clinical EEG and neuroscience.

[33]  Jürgen Gallinat,et al.  Schizophrenia risk polymorphisms in the TCF4 gene interact with smoking in the modulation of auditory sensory gating , 2012, Proceedings of the National Academy of Sciences.

[34]  Roberto Hornero,et al.  Decreased entropy modulation of EEG response to novelty and relevance in schizophrenia during a P300 task , 2015, European Archives of Psychiatry and Clinical Neuroscience.

[35]  Oleg Korzyukov,et al.  Generators of the intracranial P50 response in auditory sensory gating , 2007, NeuroImage.

[36]  J. Richman,et al.  Physiological time-series analysis using approximate entropy and sample entropy. , 2000, American journal of physiology. Heart and circulatory physiology.

[37]  Chun-Hsiang Chuang,et al.  Exploring resting-state EEG complexity before migraine attacks , 2018, Cephalalgia : an international journal of headache.

[38]  Wen-Pin Chang,et al.  Probing the relative contribution of the first and second responses to sensory gating indices: a meta-analysis. , 2011, Psychophysiology.

[39]  Samuel B. Guze,et al.  Diagnostic and Statistical Manual of Mental Disorders, 4th ed. (DSM-IV) , 1995 .

[40]  Petr Bob,et al.  Neural complexity, dissociation and schizophrenia. , 2007, Medical science monitor : international medical journal of experimental and clinical research.

[41]  Patrick W. Corrigan,et al.  Social perception in schizophrenia. , 2001 .

[42]  Stefan Leucht,et al.  What does the PANSS mean? , 2005, Schizophrenia Research.

[43]  Shuo Zhao,et al.  Target object moderation of attentional orienting by gazes or arrows , 2016, Attention, perception & psychophysics.

[44]  Ann Summerfelt,et al.  Review of clinical correlates of P50 sensory gating abnormalities in patients with schizophrenia. , 2005, Schizophrenia bulletin.

[45]  Fatma Latifoglu,et al.  Analysis of the Complexity Measures in the EEG of Schizophrenia Patients , 2016, Int. J. Neural Syst..

[46]  U. Rajendra Acharya,et al.  Application of Entropy Measures on Intrinsic Mode Functions for the Automated Identification of Focal Electroencephalogram Signals , 2015, Entropy.

[47]  S ShenbagaDevi,et al.  EEG signal complexity analysis for schizophrenia during rest and mental activity , 2017 .

[48]  Brian F. O'Donnell,et al.  Contributions of subtype and spectral frequency analyses to the study of P50 ERP amplitude and suppression in schizophrenia , 2005, Schizophrenia Research.

[49]  Xiang Yang Zhang,et al.  P50 suppression deficits and psychopathology in Han Chinese patients with schizophrenia , 2017, Neuroscience Letters.

[50]  Giulio Tononi,et al.  Topographic deficits in alpha-range resting EEG activity and steady state visual evoked responses in schizophrenia , 2015, Schizophrenia Research.

[51]  Matthijs Vink,et al.  Symptom attribution and frontal cortical thickness in first‐episode schizophrenia , 2018, Early intervention in psychiatry.

[52]  Amity E. Green,et al.  The relevance of attention in schizophrenia P50 paired stimulus studies , 2016, Clinical Neurophysiology.

[53]  Robert Freedman,et al.  Varied effects of atypical neuroleptics on P50 auditory gating in schizophrenia patients. , 2004, The American journal of psychiatry.

[54]  Richard A Armstrong,et al.  When to use the Bonferroni correction , 2014, Ophthalmic & physiological optics : the journal of the British College of Ophthalmic Opticians.

[55]  Celso Arango,et al.  P50 gating in deficit and nondeficit schizophrenia , 2010, Schizophrenia Research.

[56]  Daniel Senkowski,et al.  Corrigendum: Positive and Negative Symptoms in Schizophrenia Relate to Distinct Oscillatory Signatures of Sensory Gating , 2016, Front. Hum. Neurosci..

[57]  F. Fan,et al.  Smoking, MATRICS consensus cognitive battery and P50 sensory gating in a Han Chinese population. , 2014, Drug and alcohol dependence.

[58]  D L Braff,et al.  Normal P50 suppression in schizophrenia patients treated with atypical antipsychotic medications. , 2000, The American journal of psychiatry.

[59]  J. Lieberman,et al.  Cerebral volume asymmetries in schizophrenia and mood disorders: a quantitative magnetic resonance imaging study. , 1999, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[60]  E. Walker,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[61]  Farookh Khadeer Hussain,et al.  Effects of repetitive SSVEPs on EEG complexity using multiscale inherent fuzzy entropy , 2018, Neurocomputing.

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

[63]  Peter F. Liddle,et al.  Attention orienting dysfunction during salient novel stimulus processing in schizophrenia , 2005, Schizophrenia Research.

[64]  Jiang Wang,et al.  Characterization of complexity in the electroencephalograph activity of Alzheimer's disease based on fuzzy entropy. , 2015, Chaos.

[65]  S. A. Hosseini,et al.  Emotion recognition method using entropy analysis of EEG signals , 2011 .

[66]  Moses O. Sokunbi,et al.  Nonlinear Complexity Analysis of Brain fMRI Signals in Schizophrenia , 2014, PloS one.

[67]  Brett A Clementz,et al.  Response to the first stimulus determines reduced auditory evoked response suppression in schizophrenia: single trials analysis using MEG , 2001, Clinical Neurophysiology.

[68]  Roberto Hornero,et al.  Lempel–Ziv complexity in schizophrenia: A MEG study , 2011, Clinical Neurophysiology.

[69]  Joel E. W. Koh,et al.  A Novel Depression Diagnosis Index Using Nonlinear Features in EEG Signals , 2015, European Neurology.

[70]  Junjie Chen,et al.  The detection of epileptic seizure signals based on fuzzy entropy , 2015, Journal of Neuroscience Methods.

[71]  G. Thaker,et al.  Neurophysiological endophenotypes across bipolar and schizophrenia psychosis. , 2007, Schizophrenia bulletin.