A phase synchrony measure for quantifying dynamic functional integration in the brain

The temporal coordination of neural activity within structural networks of the brain has been posited as a basis for cognition. Changes in the frequency and similarity of oscillating electrical potentials emitted by neuronal populations may reflect the means by which networks of the brain carry out functions critical for adaptive behavior. A computation of the phase relationship between signals recorded from separable brain regions is a method for characterizing the temporal interactions of neuronal populations. Recently, different phase estimation methods for quantifying the time‐varying and frequency‐dependent nature of neural synchronization have been proposed. The most common method for measuring the synchronization of signals through phase computations uses complex wavelet transforms of neural signals to estimate their instantaneous phase difference and locking. In this article, we extend this idea by introducing a new time‐varying phase synchrony measure based on Cohen's class of time–frequency distributions. This index offers improvements over existing synchrony measures by characterizing the similarity of signals from separable brain regions with uniformly high resolution across time and frequency. The proposed measure is applied to both synthesized signals and electroencephalography data to test its effectiveness in estimating phase changes and quantifying neural synchrony in the brain. Hum Brain Mapp, 2010. © 2010 Wiley‐Liss, Inc.

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

[2]  M. Posner,et al.  Localization of a Neural System for Error Detection and Compensation , 1994 .

[3]  David Rudrauf,et al.  Estimating the time-course of coherence between single-trial brain signals: an introduction to wavelet coherence , 2002, Neurophysiologie Clinique/Clinical Neurophysiology.

[4]  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.

[5]  John R. Terry,et al.  NONLINEAR INTERDEPENDENCE IN NEURAL SYSTEMS: MOTIVATION, THEORY, AND RELEVANCE , 2002, The International journal of neuroscience.

[6]  H. Petsche,et al.  Synchronization between prefrontal and posterior association cortex during human working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

[8]  Rodrigo Quian Quiroga,et al.  Nonlinear multivariate analysis of neurophysiological signals , 2005, Progress in Neurobiology.

[9]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

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

[11]  J. Palva,et al.  Phase Synchrony among Neuronal Oscillations in the Human Cortex , 2005, The Journal of Neuroscience.

[12]  J. Fermaglich Electric Fields of the Brain: The Neurophysics of EEG , 1982 .

[13]  Anil K. Seth,et al.  Consciousness and Complexity , 2022 .

[14]  Wolf Singer,et al.  Striving for coherence , 1999 .

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

[16]  D. Tucker,et al.  EEG coherency. I: Statistics, reference electrode, volume conduction, Laplacians, cortical imaging, and interpretation at multiple scales. , 1997, Electroencephalography and clinical neurophysiology.

[17]  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.

[18]  Jechang Jeong,et al.  Kernel design for reduced interference distributions , 1992, IEEE Trans. Signal Process..

[19]  Tomas Sauer,et al.  Conventional and wavelet coherence applied to sensory-evoked electrical brain activity , 2006, IEEE Transactions on Biomedical Engineering.

[20]  Leon Cohen,et al.  Time Frequency Analysis: Theory and Applications , 1994 .

[21]  Hans-Jochen Heinze,et al.  Causal visual interactions as revealed by an information theoretic measure and fMRI , 2006, NeuroImage.

[22]  W. Gehring,et al.  Are all medial frontal negativities created equal ? Toward a richer empirical basis for theories of action monitoring , 2003 .

[23]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[24]  Luiz A. Baccalá,et al.  Partial directed coherence: a new concept in neural structure determination , 2001, Biological Cybernetics.

[25]  S. Rombouts,et al.  Disturbed fluctuations of resting state EEG synchronization in Alzheimer's disease , 2005, Clinical Neurophysiology.

[26]  Karl J. Friston The labile brain. I. Neuronal transients and nonlinear coupling. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[27]  Ranu Jung,et al.  Quantifying Coevolution of Nonstationary Biomedical Signals Using Time-Varying Phase Spectra , 2000, Annals of Biomedical Engineering.

[28]  D. Meyer,et al.  A Neural System for Error Detection and Compensation , 1993 .

[29]  J. Hohnsbein,et al.  Effects of crossmodal divided attention on late ERP components. II. Error processing in choice reaction tasks. , 1991, Electroencephalography and clinical neurophysiology.

[30]  M. Murray,et al.  EEG source imaging , 2004, Clinical Neurophysiology.

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

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

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

[34]  P. Brown Oscillatory nature of human basal ganglia activity: Relationship to the pathophysiology of Parkinson's disease , 2003, Movement disorders : official journal of the Movement Disorder Society.

[35]  M G Coles,et al.  A brain potential manifestation of error-related processing. , 1995, Electroencephalography and clinical neurophysiology. Supplement.

[36]  S. Schiff,et al.  Decreased Neuronal Synchronization during Experimental Seizures , 2002, The Journal of Neuroscience.

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

[38]  J. Martinerie,et al.  Statistical assessment of nonlinear causality: application to epileptic EEG signals , 2003, Journal of Neuroscience Methods.

[39]  M. Breakspear Nonlinear phase desynchronization in human electroencephalographic data , 2002, Human brain mapping.

[40]  Clay B. Holroyd,et al.  Error-related scalp potentials elicited by hand and foot movements: evidence for an output-independent error-processing system in humans , 1998, Neuroscience Letters.

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

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

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

[44]  Clay B. Holroyd,et al.  The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. , 2002, Psychological review.

[45]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[46]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[47]  Minfen Shen,et al.  Analysis of time-varying synchronization of multi-channel EEG signals using wavelet coherence , 2003, International Conference on Neural Networks and Signal Processing, 2003. Proceedings of the 2003.

[48]  August W. Rihaczek,et al.  Signal energy distribution in time and frequency , 1968, IEEE Trans. Inf. Theory.

[49]  F. Varela Resonant cell assemblies: a new approach to cognitive functions and neuronal synchrony. , 1995, Biological research.

[50]  James Theiler,et al.  Testing for nonlinearity in time series: the method of surrogate data , 1992 .

[51]  C. Patrick,et al.  Externalizing Psychopathology and the Error-Related Negativity , 2007, Psychological science.

[52]  Katarzyna J. Blinowska,et al.  A new method of the description of the information flow in the brain structures , 1991, Biological Cybernetics.

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

[54]  C. Granger Investigating causal relations by econometric models and cross-spectral methods , 1969 .

[55]  Mingzhou Ding,et al.  Evaluating causal relations in neural systems: Granger causality, directed transfer function and statistical assessment of significance , 2001, Biological Cybernetics.

[56]  A. Roskies The Binding Problem , 1999, Neuron.

[57]  John J. B. Allen,et al.  Theta EEG dynamics of the error-related negativity , 2007, Clinical Neurophysiology.

[58]  C. Stam,et al.  Nonlinear dynamical analysis of EEG and MEG: Review of an emerging field , 2005, Clinical Neurophysiology.

[59]  Kurths,et al.  Phase synchronization of chaotic oscillators. , 1996, Physical review letters.