A novel multivariate phase synchrony measure: Application to multichannel newborn EEG analysis

Abstract Phase synchrony assessment across non-stationary multivariate signals is a useful way to characterize the dynamical behavior of their underlying systems. Traditionally, phase synchrony of a multivariate signal has been quantified by first assessing all pair-wise phase relationships between different channels and then, averaging their phase coupling. This approach, however, may not necessarily provide a full picture of multiple phase ratios within non-stationary signals with time-varying statistical properties. Several attempts have been made to generalize pair-wise phase synchrony concept to multivariate signals. In this paper, we introduce a new measure of generalized phase synchrony based on the concept of circular statistics. The performance of the measure is evaluated with simulations using the Kuramoto and Rossler models and compared with that of three existing generalized phase synchrony measures based respectively on 1) the concept of co-integration, 2) S-estimator and 3) hyper-dimensional geometry. The simulation results represent the correct degree of synchronization between channels with negligible mean of squared error, i.e. below 4.2 e − 4 . We then use the proposed measure to assess inter-hemispheric phase synchrony in two abnormal multichannel newborn EEG datasets with manually marked seizure/non-seizure and burst–suppression signatures. The EEG results suggest that the proposed measure is able to detect inter-hemispheric phase synchrony changes with higher accuracy than the other existing measures, i.e. 2% for seizure/non-seizure database and 11% for burst/suppression database than the best performing existing multivariate phase synchrony measure.

[1]  Panos M. Pardalos,et al.  Analysis of Multichannel EEG Recordings Based on Generalized Phase Synchronization and Cointegrated VAR , 2010 .

[2]  Andreas Daffertshofer,et al.  Generative Models of Cortical Oscillations: Neurobiological Implications of the Kuramoto Model , 2010, Front. Hum. Neurosci..

[3]  Michalis E. Zervakis,et al.  Assessment of Linear and Nonlinear Synchronization Measures for Analyzing EEG in a Mild Epileptic Paradigm , 2009, IEEE Transactions on Information Technology in Biomedicine.

[4]  Mahmood Al-khassaweneh,et al.  A Measure of Multivariate Phase Synchrony Using Hyperdimensional Geometry , 2016, IEEE Transactions on Signal Processing.

[5]  Boualem Boashash,et al.  Principles of time-frequency feature extraction for change detection in non-stationary signals: Applications to newborn EEG abnormality detection , 2015, Pattern Recognit..

[6]  Nigel H. Lovell,et al.  Beyond Subjective Self-Rating: EEG Signal Classification of Cognitive Workload , 2015, IEEE Transactions on Autonomous Mental Development.

[7]  M. Rosenblum,et al.  Detecting direction of coupling in interacting oscillators. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[8]  David Nicholls,et al.  Synchrony Dynamics Across Brain Structures in Limbic Epilepsy Vary Between Initiation and Termination Phases of Seizures , 2013, IEEE Transactions on Biomedical Engineering.

[9]  John G. Proakis,et al.  Digital Communications , 1983 .

[10]  Selin Aviyente,et al.  A Tensor Decomposition-Based Approach for Detecting Dynamic Network States From EEG , 2017, IEEE Transactions on Biomedical Engineering.

[11]  J. Wackermann,et al.  Beyond mapping: estimating complexity of multichannel EEG recordings. , 1996, Acta neurobiologiae experimentalis.

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

[13]  Amir H. Omidvarnia,et al.  The dynamics of functional connectivity in neocortical focal epilepsy , 2017, NeuroImage: Clinical.

[14]  Minyou Chen,et al.  Use of phase-locking value in sensorimotor rhythm-based brain–computer interface: zero-phase coupling and effects of spatial filters , 2017, Medical & Biological Engineering & Computing.

[15]  Kaspar Anton Schindler,et al.  Uniform approach to linear and nonlinear interrelation patterns in multivariate time series. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[16]  C. Stam,et al.  Phase lag index: Assessment of functional connectivity from multi channel EEG and MEG with diminished bias from common sources , 2007, Human brain mapping.

[17]  Stefan Haufe,et al.  Consistency of EEG source localization and connectivity estimates , 2016, NeuroImage.

[18]  Martin Hasler,et al.  State Change Detection Using Multivariate Synchronization Measure from Physiological Signals (Special Section on Papers Awarded the Student Paper Award at NCSP'06) , 2006 .

[19]  Andrew Zalesky,et al.  Dynamic coupling between fMRI local connectivity and interictal EEG in focal epilepsy: A wavelet analysis approach , 2017, Human brain mapping.

[20]  Ian Daly,et al.  Brain computer interface control via functional connectivity dynamics , 2012, Pattern Recognit..

[21]  B. Boashash,et al.  Effective implementation of time-frequency matched filter with adapted pre and postprocessing for data-dependent detection of newborn seizures. , 2013, Medical engineering & physics.

[22]  D. Cumin,et al.  Generalising the Kuramoto Model for the study of Neuronal Synchronisation in the Brain , 2007 .

[23]  Boualem Boashash,et al.  Robust multisensor time-frequency signal processing: A tutorial review with illustrations of performance enhancement in selected application areas , 2017, Digit. Signal Process..

[24]  J. Volpe Neurology of the Newborn , 1959, Major problems in clinical pediatrics.

[25]  S. R. Jammalamadaka,et al.  Topics in Circular Statistics , 2001 .

[26]  Jennifer M Walz,et al.  Spatiotemporal mapping of epileptic spikes using simultaneous EEG-functional MRI , 2017, Brain : a journal of neurology.

[27]  C. Stam,et al.  Disturbed functional connectivity in brain tumour patients: Evaluation by graph analysis of synchronization matrices , 2006, Clinical Neurophysiology.

[28]  F. Babiloni,et al.  Estimation of Effective and Functional Cortical Connectivity From Neuroelectric and Hemodynamic Recordings , 2009, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[29]  Boualem Boashash,et al.  A time-frequency based approach for generalized phase synchrony assessment in nonstationary multivariate signals , 2013, Digit. Signal Process..

[30]  R Quian Quiroga,et al.  Performance of different synchronization measures in real data: a case study on electroencephalographic signals. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[31]  E. Gysels,et al.  Phase synchronization for the recognition of mental tasks in a brain-computer interface , 2004, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[32]  S. Bressler,et al.  Trial-to-trial variability of cortical evoked responses: implications for the analysis of functional connectivity , 2002, Clinical Neurophysiology.

[33]  Boualem Boashash,et al.  Time-Frequency Signal Analysis and Processing: A Comprehensive Reference , 2015 .

[34]  Boualem Boashash,et al.  Measuring Time-Varying Information Flow in Scalp EEG Signals: Orthogonalized Partial Directed Coherence , 2014, IEEE Transactions on Biomedical Engineering.

[35]  David Rudrauf,et al.  Frequency flows and the time-frequency dynamics of multivariate phase synchronization in brain signals , 2006, NeuroImage.

[36]  Jürgen Kurths,et al.  Detection of n:m Phase Locking from Noisy Data: Application to Magnetoencephalography , 1998 .

[37]  T. Koenig,et al.  Decreased functional connectivity of EEG theta-frequency activity in first-episode, neuroleptic-naı̈ve patients with schizophrenia: preliminary results , 2001, Schizophrenia Research.

[38]  S. Strogatz From Kuramoto to Crawford: exploring the onset of synchronization in populations of coupled oscillators , 2000 .

[39]  John M. O'Toole,et al.  Time-Frequency Processing of Nonstationary Signals: Advanced TFD Design to Aid Diagnosis with Highlights from Medical Applications , 2013, IEEE Signal Processing Magazine.

[40]  S. Johansen Estimation and Hypothesis Testing of Cointegration Vectors in Gaussian Vector Autoregressive Models , 1991 .

[41]  Ali Yener Mutlu,et al.  Multivariate Empirical Mode Decomposition for Quantifying Multivariate Phase Synchronization , 2011, EURASIP J. Adv. Signal Process..

[42]  M. Rosenblum,et al.  Identification of coupling direction: application to cardiorespiratory interaction. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[43]  Mahdi Jalili,et al.  Synchronization of EEG: Bivariate and Multivariate Measures , 2014, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[44]  Nigel H. Lovell,et al.  Estimating cognitive workload using wavelet entropy-based features during an arithmetic task , 2013, Comput. Biol. Medicine.

[45]  Boualem Boashash,et al.  Surrogate data test for nonlinearity of EEG signals: A newborn EEG burst suppression case study , 2017, Digit. Signal Process..

[46]  Junfeng Sun,et al.  Unified framework for detecting phase synchronization in coupled time series. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[47]  Boualem Boashash,et al.  Automatic signal abnormality detection using time-frequency features and machine learning: A newborn EEG seizure case study , 2016, Knowl. Based Syst..

[48]  Boualem Boashash,et al.  An Efficient Algorithm for Instantaneous Frequency Estimation of Nonstationary Multicomponent Signals in Low SNR , 2011, EURASIP J. Adv. Signal Process..

[49]  Yijun Wang,et al.  Phase Synchrony Measurement in Motor Cortex for Classifying Single-trial EEG during Motor Imagery , 2006, 2006 International Conference of the IEEE Engineering in Medicine and Biology Society.

[50]  B. Silverman,et al.  The Stationary Wavelet Transform and some Statistical Applications , 1995 .

[51]  Jennifer M Walz,et al.  Dynamic regional phase synchrony (DRePS) , 2016, Human brain mapping.

[52]  J. Martinerie,et al.  Comparison of Hilbert transform and wavelet methods for the analysis of neuronal synchrony , 2001, Journal of Neuroscience Methods.

[53]  D. P. Mandic,et al.  Measuring phase synchrony using complex extensions of EMD , 2009, 2009 IEEE/SP 15th Workshop on Statistical Signal Processing.

[54]  Robert T. Knight,et al.  Multivariate Phase–Amplitude Cross-Frequency Coupling in Neurophysiological Signals , 2012, IEEE Transactions on Biomedical Engineering.

[55]  Boualem Boashash,et al.  EEG background features that predict outcome in term neonates with hypoxic ischaemic encephalopathy: A structured review , 2016, Clinical Neurophysiology.

[56]  F. Mormann,et al.  Mean phase coherence as a measure for phase synchronization and its application to the EEG of epilepsy patients , 2000 .

[57]  José Luis Pérez Velazquez,et al.  Phase synchronization measurements using electroencephalographic recordings , 2007, Neuroinformatics.

[58]  Richard S. Frackowiak,et al.  Evolution of source EEG synchronization in early Alzheimer's disease , 2013, Neurobiology of Aging.

[59]  Rainer Dahlhaus,et al.  Partial phase synchronization for multivariate synchronizing systems. , 2006, Physical review letters.

[60]  M. Paluš Detecting phase synchronization in noisy systems , 1997 .

[61]  Jin Zhang,et al.  An improved method to calculate phase locking value based on Hilbert–Huang transform and its application , 2013, Neural Computing and Applications.

[62]  Lotfi Senhadji,et al.  Time-frequency characterization of interdependencies in nonstationary signals: application to epileptic EEG , 2005, IEEE Transactions on Biomedical Engineering.

[63]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.