Synchronization dynamics and evidence for a repertoire of network states in resting EEG

Intrinsically driven neural activity generated at rest exhibits complex spatiotemporal dynamics characterized by patterns of synchronization across distant brain regions. Mounting evidence suggests that these patterns exhibit fluctuations and nonstationarity at multiple time scales. Resting-state electroencephalographic (EEG) recordings were examined in 12 young adults for changes in synchronization patterns on a fast time scale in the range of tens to hundreds of milliseconds. Results revealed that EEG dynamics continuously underwent rapid transitions between intermittently stable states. Numerous approximate recurrences of states were observed within single recording epochs, across different epochs separated by longer times, and between participants. For broadband (4–30 Hz) data, a majority of states could be grouped into three families, suggesting the existence of a limited repertoire of core states that is continually revisited and shared across participants. Our results document the existence of fast synchronization dynamics iterating amongst a small set of core networks in the resting brain, complementing earlier findings of nonstationary dynamics in electromagnetic recordings and transient EEG microstates.

[1]  Milan Palus,et al.  Small-world topology of functional connectivity in randomly connected dynamical systems , 2012, Chaos.

[2]  M. Breakspear,et al.  Bistability and Non-Gaussian Fluctuations in Spontaneous Cortical Activity , 2009, The Journal of Neuroscience.

[3]  Anthony Randal McIntosh,et al.  Towards a network theory of cognition , 2000, Neural Networks.

[4]  V Latora,et al.  Small-world behavior in time-varying graphs. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[5]  D. Lehmann,et al.  Reference-free identification of components of checkerboard-evoked multichannel potential fields. , 1980, Electroencephalography and clinical neurophysiology.

[6]  Dietrich Lehmann,et al.  Brain Electric Microstates and Cognition: The Atoms of Thought , 1990 .

[7]  Juliane Britz,et al.  EEG microstate sequences in healthy humans at rest reveal scale-free dynamics , 2010, Proceedings of the National Academy of Sciences.

[8]  Michael Vourkas,et al.  Tracking brain dynamics via time-dependent network analysis , 2010, Journal of Neuroscience Methods.

[9]  Stephen M. Smith,et al.  Temporally-independent functional modes of spontaneous brain activity , 2012, Proceedings of the National Academy of Sciences.

[10]  F. Španiel,et al.  Subanesthetic dose of ketamine decreases prefrontal theta cordance in healthy volunteers: implications for antidepressant effect , 2009, Psychological Medicine.

[11]  Tracy Warbrick,et al.  Spontaneous brain activity and EEG microstates. A novel EEG/fMRI analysis approach to explore resting-state networks , 2010, NeuroImage.

[12]  M. Kramer,et al.  Coalescence and Fragmentation of Cortical Networks during Focal Seizures , 2010, The Journal of Neuroscience.

[13]  M E J Newman,et al.  Community structure in social and biological networks , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[14]  A. Opstal Dynamic Patterns: The Self-Organization of Brain and Behavior , 1995 .

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

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

[17]  S. Bressler,et al.  Large-scale brain networks in cognition: emerging methods and principles , 2010, Trends in Cognitive Sciences.

[18]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[19]  J. C. Dunn,et al.  A Fuzzy Relative of the ISODATA Process and Its Use in Detecting Compact Well-Separated Clusters , 1973 .

[20]  Michael Breakspear,et al.  A Novel Method for the Topographic Analysis of Neural Activity Reveals Formation and Dissolution of ‘Dynamic Cell Assemblies’ , 2004, Journal of Computational Neuroscience.

[21]  Benjamin H. Good,et al.  Performance of modularity maximization in practical contexts. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[22]  S. Bressler Large-scale cortical networks and cognition , 1995, Brain Research Reviews.

[23]  J. Kelso,et al.  Cortical coordination dynamics and cognition , 2001, Trends in Cognitive Sciences.

[24]  Karl J. Friston Transients, Metastability, and Neuronal Dynamics , 1997, NeuroImage.

[25]  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.

[26]  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.

[27]  C. Stam,et al.  Small‐world properties of nonlinear brain activity in schizophrenia , 2009, Human brain mapping.

[28]  Jaeseung Jeong,et al.  Quantification of Brain Macrostates Using Dynamical Nonstationarity of Physiological Time Series , 2011, IEEE Transactions on Biomedical Engineering.

[29]  C. J. Stam,et al.  Functional connectivity patterns of human magnetoencephalographic recordings: a ‘small-world’ network? , 2004, Neuroscience Letters.

[30]  E. Bullmore,et al.  Adaptive reconfiguration of fractal small-world human brain functional networks , 2006, Proceedings of the National Academy of Sciences.

[31]  K. Müller,et al.  Robustly estimating the flow direction of information in complex physical systems. , 2007, Physical review letters.

[32]  M M Mesulam,et al.  Large‐scale neurocognitive networks and distributed processing for attention, language, and memory , 1990, Annals of neurology.

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

[34]  Mark C. Parsons,et al.  Communicability across evolving networks. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[35]  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.

[36]  D Lehmann,et al.  EEG alpha map series: brain micro-states by space-oriented adaptive segmentation. , 1987, Electroencephalography and clinical neurophysiology.

[37]  Cornelis J. Stam,et al.  Synchronization likelihood with explicit time-frequency priors , 2006, NeuroImage.

[38]  Olaf Sporns,et al.  EEG synchronization to modulated auditory tones in schizophrenia, schizoaffective disorder, and schizotypal personality disorder. , 2003, The American journal of psychiatry.

[39]  James Theiler,et al.  Using surrogate data to detect nonlinearity in time series , 1991 .

[40]  Jean-Loup Guillaume,et al.  Fast unfolding of communities in large networks , 2008, 0803.0476.

[41]  C. Stam,et al.  Synchronization likelihood: an unbiased measure of generalized synchronization in multivariate data sets , 2002 .

[42]  Mark E. J. Newman,et al.  Power-Law Distributions in Empirical Data , 2007, SIAM Rev..

[43]  M. Kramer,et al.  Emergence of Stable Functional Networks in Long-Term Human Electroencephalography , 2012, The Journal of Neuroscience.

[44]  Theiler,et al.  Generating surrogate data for time series with several simultaneously measured variables. , 1994, Physical review letters.

[45]  David A. Leopold,et al.  Dynamic functional connectivity: Promise, issues, and interpretations , 2013, NeuroImage.

[46]  Mert R. Sabuncu,et al.  The influence of head motion on intrinsic functional connectivity MRI , 2012, NeuroImage.

[47]  Cornelis J Stam,et al.  Graph theoretical analysis of complex networks in the brain , 2007, Nonlinear biomedical physics.

[48]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

[49]  Gavan Lintern,et al.  Dynamic patterns: The self-organization of brain and behavior , 1997, Complex.

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

[51]  William P. Hetrick,et al.  Temporal processing dysfunction in schizophrenia , 2008, Brain and Cognition.

[52]  S. P. Lloyd,et al.  Least squares quantization in PCM , 1982, IEEE Trans. Inf. Theory.

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

[54]  Catie Chang,et al.  Time–frequency dynamics of resting-state brain connectivity measured with fMRI , 2010, NeuroImage.

[55]  Yong He,et al.  Graph-based network analysis of resting-state functional MRI. , 2010 .

[56]  C. Stam,et al.  Small-world networks and functional connectivity in Alzheimer's disease. , 2006, Cerebral cortex.

[57]  J. A. Scott Kelso,et al.  Brain coordination dynamics: True and false faces of phase synchrony and metastability , 2009, Progress in Neurobiology.

[58]  M. Corbetta,et al.  Temporal dynamics of spontaneous MEG activity in brain networks , 2010, Proceedings of the National Academy of Sciences.

[59]  A. Provenzale,et al.  Finite correlation dimension for stochastic systems with power-law spectra , 1989 .

[60]  Dorothee P. Auer,et al.  Is sedation-induced BOLD fMRI low-frequency fluctuation increase mediated by increased motion? , 2010, Magnetic Resonance Materials in Physics, Biology and Medicine.

[61]  Danielle S Bassett,et al.  Cognitive fitness of cost-efficient brain functional networks , 2009, Proceedings of the National Academy of Sciences.

[62]  Cornelis J Stam,et al.  Seizure detection in the neonatal EEG with synchronization likelihood , 2003, Clinical Neurophysiology.

[63]  V. Latora,et al.  Persistent patterns of interconnection in time-varying cortical networks estimated from high-resolution EEG recordings in humans during a simple motor act , 2008 .

[64]  Dimitri Van De Ville,et al.  BOLD correlates of EEG topography reveal rapid resting-state network dynamics , 2010, NeuroImage.

[65]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[66]  M Valencia,et al.  Dynamic small-world behavior in functional brain networks unveiled by an event-related networks approach. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[67]  C. Stam,et al.  The influence of ageing on complex brain networks: A graph theoretical analysis , 2009, Human brain mapping.

[68]  C. Stam,et al.  Small-world networks and disturbed functional connectivity in schizophrenia , 2006, Schizophrenia Research.

[69]  F. Takens Detecting strange attractors in turbulence , 1981 .