Emergence of Persistent Networks in Long-Term Intracranial EEG Recordings

Over the past two decades, the increased ability to analyze network relationships among neural structures has provided novel insights into brain function. Most network approaches, however, focus on static representations of the brain's physical or statistical connectivity. Few studies have examined how brain functional networks evolve spontaneously over long epochs of continuous time. To address this, we examine functional connectivity networks deduced from continuous long-term electrocorticogram recordings. For a population of six human patients, we identify a persistent pattern of connections that form a frequency-band-dependent network template, and a set of core connections that appear frequently and together. These structures are robust, emerging from brief time intervals (∼100 s) regardless of cognitive state. These results suggest that a metastable, frequency-band-dependent scaffold of brain connectivity exists from which transient activity emerges and recedes.

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

[2]  A. Fingelkurts,et al.  MAKING COMPLEXITY SIMPLER: MULTIVARIABILITY AND METASTABILITY IN THE BRAIN , 2004, The International journal of neuroscience.

[3]  Andrew C. N. Chen,et al.  EEG default mode network in the human brain: Spectral regional field powers , 2008 .

[4]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[5]  Olaf Sporns,et al.  The small world of the cerebral cortex , 2007, Neuroinformatics.

[6]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[7]  M. Greicius Resting-state functional connectivity in neuropsychiatric disorders , 2008, Current opinion in neurology.

[8]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[9]  O Sporns,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009, Proceedings of the National Academy of Sciences.

[10]  M E J Newman Assortative mixing in networks. , 2002, Physical review letters.

[11]  M. Lowe,et al.  Antidepressant Effect on Connectivity of the Mood-Regulating Circuit: An fMRI Study , 2005, Neuropsychopharmacology.

[12]  Stanley Wasserman,et al.  Social Network Analysis: Methods and Applications , 1994, Structural analysis in the social sciences.

[13]  Viktor K. Jirsa,et al.  Noise during Rest Enables the Exploration of the Brain's Dynamic Repertoire , 2008, PLoS Comput. Biol..

[14]  Klaus Lehnertz,et al.  Measuring synchronization in coupled model systems: A comparison of different approaches , 2007 .

[15]  Mark E. J. Newman,et al.  The Structure and Function of Complex Networks , 2003, SIAM Rev..

[16]  M. Lowe,et al.  Functional Connectivity in Single and Multislice Echoplanar Imaging Using Resting-State Fluctuations , 1998, NeuroImage.

[17]  Martijn P. van den Heuvel,et al.  FUNCTIONAL CONNECTIVITY IN SCHIZOPHRENIA , 2010, Schizophrenia Research.

[18]  Stefan Rotter,et al.  How Structure Determines Correlations in Neuronal Networks , 2011, PLoS Comput. Biol..

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

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

[21]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[22]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[23]  V L Towle,et al.  Electrocorticographic coherence patterns. , 1999, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[24]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: II. Decreases in Cerebral Cortex , 1997, Journal of Cognitive Neuroscience.

[25]  Andreas Daffertshofer,et al.  The relationship between structural and functional connectivity: Graph theoretical analysis of an EEG neural mass model , 2010, NeuroImage.

[26]  H. Berendse,et al.  The application of graph theoretical analysis to complex networks in the brain , 2007, Clinical Neurophysiology.

[27]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

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

[29]  D. Long Networks of the Brain , 2011 .

[30]  M. Raichle Two views of brain function , 2010, Trends in Cognitive Sciences.

[31]  A. Fingelkurts,et al.  Persistent operational synchrony within brain default-mode network and self-processing operations in healthy subjects , 2011, Brain and Cognition.

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

[33]  M. Newman,et al.  Finding community structure in networks using the eigenvectors of matrices. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[34]  David G. Norris,et al.  An Investigation of Functional and Anatomical Connectivity Using Magnetic Resonance Imaging , 2002, NeuroImage.

[35]  A. von Stein,et al.  Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[37]  Biyu J. He,et al.  The Temporal Structures and Functional Significance of Scale-free Brain Activity , 2010, Neuron.

[38]  Matthäus Staniek,et al.  Measuring Synchronization in the Epileptic Brain: a Comparison of Different Approaches , 2007, Int. J. Bifurc. Chaos.

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

[40]  N C Andreasen,et al.  Remembering the past: two facets of episodic memory explored with positron emission tomography. , 1995, The American journal of psychiatry.

[41]  T. Sejnowski,et al.  Correlated neuronal activity and the flow of neural information , 2001, Nature Reviews Neuroscience.

[42]  V. Calhoun,et al.  Aberrant "default mode" functional connectivity in schizophrenia. , 2007, The American journal of psychiatry.

[43]  O. Sporns,et al.  Key role of coupling, delay, and noise in resting brain fluctuations , 2009, Proceedings of the National Academy of Sciences.

[44]  E. Wolpert A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects. , 1969 .

[45]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[46]  Biyu J. He,et al.  Electrophysiological correlates of the brain's intrinsic large-scale functional architecture , 2008, Proceedings of the National Academy of Sciences.

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

[48]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[49]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[50]  E. Bullmore,et al.  A Resilient, Low-Frequency, Small-World Human Brain Functional Network with Highly Connected Association Cortical Hubs , 2006, The Journal of Neuroscience.

[51]  Biyu J. He,et al.  The fMRI signal, slow cortical potential and consciousness , 2009, Trends in Cognitive Sciences.

[52]  Olaf Sporns,et al.  Network structure of cerebral cortex shapes functional connectivity on multiple time scales , 2007, Proceedings of the National Academy of Sciences.

[53]  Danielle Smith Bassett,et al.  Small-World Brain Networks , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[54]  J. Gabrieli,et al.  Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia , 2009, Proceedings of the National Academy of Sciences.

[55]  Alan C. Evans,et al.  Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. , 2009, Cerebral cortex.

[56]  Lotfi Senhadji,et al.  Quantitative evaluation of linear and nonlinear methods characterizing interdependencies between brain signals. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[57]  Yuji Ikegaya,et al.  Synfire Chains and Cortical Songs: Temporal Modules of Cortical Activity , 2004, Science.

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

[59]  Klaus Lehnertz,et al.  From brain to earth and climate systems: Small-world interaction networks or not? , 2011, Chaos.

[60]  A. Kraskov,et al.  On the predictability of epileptic seizures , 2005, Clinical Neurophysiology.

[61]  Roger Guimerà,et al.  Cartography of complex networks: modules and universal roles , 2005, Journal of statistical mechanics.

[62]  M. Raichle,et al.  Disease and the brain's dark energy , 2010, Nature Reviews Neurology.

[63]  Uri T Eden,et al.  Network inference with confidence from multivariate time series. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[64]  G. Deco,et al.  Emerging concepts for the dynamical organization of resting-state activity in the brain , 2010, Nature Reviews Neuroscience.

[65]  E. Tulving,et al.  Network Analysis of Positron Emission Tomography Regional Cerebral Blood Flow Data: Ensemble Inhibition during Episodic Memory Retrieval , 1996, The Journal of Neuroscience.

[66]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[67]  Jack W. Tsao,et al.  Observed brain dynamics, P.P. Mitra, H. Bokil. Oxford University Press (2008), ISBN-13: 978-0-19-517808-1, 381 pages, $65.00 , 2009 .

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

[69]  Eric D. Kolaczyk,et al.  Statistical Analysis of Network Data: Methods and Models , 2009 .

[70]  M. Weigt,et al.  On the properties of small-world network models , 1999, cond-mat/9903411.

[71]  Yanling Yin,et al.  EEG default mode network in the human brain: Spectral regional field powers , 2008, NeuroImage.

[72]  N. Logothetis What we can do and what we cannot do with fMRI , 2008, Nature.

[73]  Justin L. Vincent,et al.  Disruption of Large-Scale Brain Systems in Advanced Aging , 2007, Neuron.

[74]  A. Schnitzler,et al.  Normal and pathological oscillatory communication in the brain , 2005, Nature Reviews Neuroscience.

[75]  Frederik Barkhof,et al.  Model‐free group analysis shows altered BOLD FMRI networks in dementia , 2009, Human brain mapping.

[76]  Sean M Montgomery,et al.  Entrainment of Neocortical Neurons and Gamma Oscillations by the Hippocampal Theta Rhythm , 2008, Neuron.

[77]  S. Rombouts,et al.  Reduced resting-state brain activity in the "default network" in normal aging. , 2008, Cerebral cortex.

[78]  Jürgen Kurths,et al.  Structural and functional clusters of complex brain networks , 2006 .

[79]  Karl J. Friston Functional and effective connectivity in neuroimaging: A synthesis , 1994 .

[80]  R. F. Galán,et al.  On How Network Architecture Determines the Dominant Patterns of Spontaneous Neural Activity , 2008, PLoS ONE.

[81]  Changsong Zhou,et al.  Hierarchical organization unveiled by functional connectivity in complex brain networks. , 2006, Physical review letters.

[82]  G. Buzsáki,et al.  Gamma Oscillations in the Entorhinal Cortex of the Freely Behaving Rat , 1998, The Journal of Neuroscience.

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