Differential Effects of Simulated Cortical Network Lesions on Synchrony and EEG Complexity

Brain function has been proposed to arise as a result of the coordinated activity between distributed brain areas. An important issue in the study of brain activity is the characterization of the synchrony among these areas and the resulting complexity of the system. However, the variety of ways to define and, hence, measure brain synchrony and complexity has sometimes led to inconsistent results. Here, we study the relationship between synchrony and commonly used complexity estimators of electroencephalogram (EEG) activity and we explore how simulated lesions in anatomically based cortical networks would affect key functional measures of activity. We explored this question using different types of neural network lesions while the brain dynamics was modeled with a time-delayed set of 66 Kuramoto oscillators. Each oscillator modeled a region of the cortex (node), and the connectivity and spatial location between different areas informed the creation of a network structure (edges). Each type of lesion consisted on successive lesions of nodes or edges during the simulation of the neural dynamics. For each type of lesion, we measured the synchrony among oscillators and three complexity estimators (Higuchi's Fractal Dimension, Sample Entropy and Lempel-Ziv Complexity) of the simulated EEGs. We found a general negative correlation between EEG complexity metrics and synchrony but Sample Entropy and Lempel-Ziv showed a positive correlation with synchrony when the edges of the network were deleted. This suggests an intricate relationship between synchrony of the system and its estimated complexity. Hence, complexity seems to depend on the multiple states of interaction between the oscillators of the system. Our results can contribute to the interpretation of the functional meaning of EEG complexity.

[1]  G. Edelman,et al.  Consciousness and Complexity , 1998 .

[2]  Antonio José Ibañez-Molina,et al.  Neurocomputational Model of EEG Complexity during Mind Wandering , 2016, Front. Comput. Neurosci..

[3]  John M Beggs,et al.  Critical branching captures activity in living neural networks and maximizes the number of metastable States. , 2005, Physical review letters.

[4]  Yasser Ghanbari,et al.  Joint Analysis of Band-Specific Functional Connectivity and Signal Complexity in Autism , 2015, Journal of autism and developmental disorders.

[5]  J. Kelso,et al.  The Metastable Brain , 2014, Neuron.

[6]  Karl J. Friston,et al.  Characterising the complexity of neuronal interactions , 1995 .

[7]  P. Berg,et al.  A fast method for forward computation of multiple-shell spherical head models. , 1994, Electroencephalography and clinical neurophysiology.

[8]  L Berthouze,et al.  Power-law distribution of phase-locking intervals does not imply critical interaction. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[9]  Norbert Schuff,et al.  White matter damage in frontotemporal dementia and Alzheimer's disease measured by diffusion MRI , 2009, Brain : a journal of neurology.

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

[11]  R. Burwell,et al.  Neuron number in the parahippocampal region is preserved in aged rats with spatial learning deficits. , 2002, Cerebral cortex.

[12]  L M Hively,et al.  Detecting dynamical changes in time series using the permutation entropy. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[13]  Madalena Costa,et al.  Multiscale entropy analysis of biological signals. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[14]  Jaeseung Jeong EEG dynamics in patients with Alzheimer's disease , 2004, Clinical Neurophysiology.

[15]  M. Mattia,et al.  Population dynamics of interacting spiking neurons. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[16]  Murray Shanahan,et al.  Metastability and Inter-Band Frequency Modulation in Networks of Oscillating Spiking Neuron Populations , 2013, PloS one.

[17]  Peter J Hellyer,et al.  The Control of Global Brain Dynamics: Opposing Actions of Frontoparietal Control and Default Mode Networks on Attention , 2014, The Journal of Neuroscience.

[18]  P. Agostino Accardo,et al.  Use of the fractal dimension for the analysis of electroencephalographic time series , 1997, Biological Cybernetics.

[19]  G. Sandini,et al.  Graph theoretical analysis of magnetoencephalographic functional connectivity in Alzheimer's disease. , 2009, Brain : a journal of neurology.

[20]  Karsten Hoechstetter,et al.  BESA Source Coherence: A New Method to Study Cortical Oscillatory Coupling , 2003, Brain Topography.

[21]  J. Fell,et al.  More than synchrony: EEG chaoticity may be necessary for conscious brain functioning. , 2003, Medical hypotheses.

[22]  Habib Benali,et al.  Relating Structure and Function in the Human Brain: Relative Contributions of Anatomy, Stationary Dynamics, and Non-stationarities , 2014, PLoS Comput. Biol..

[23]  Reza Boostani,et al.  Entropy and complexity measures for EEG signal classification of schizophrenic and control participants , 2009, Artif. Intell. Medicine.

[24]  C. Stam Modern network science of neurological disorders , 2014, Nature Reviews Neuroscience.

[25]  Beom Jun Kim,et al.  Attack vulnerability of complex networks. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[26]  Jorge Iriarte,et al.  Coupling between Beta and High-Frequency Activity in the Human Subthalamic Nucleus May Be a Pathophysiological Mechanism in Parkinson's Disease , 2010, The Journal of Neuroscience.

[27]  O. Kinouchi,et al.  Optimal dynamical range of excitable networks at criticality , 2006, q-bio/0601037.

[28]  Chrysoula Kourtidou-Papadeli,et al.  Monitoring sleepiness with on-board electrophysiological recordings for preventing sleep-deprived traffic accidents , 2007, Clinical Neurophysiology.

[29]  M. P. Griffin,et al.  Sample entropy analysis of neonatal heart rate variability. , 2002, American journal of physiology. Regulatory, integrative and comparative physiology.

[30]  Hae-Jeong Park,et al.  Functional disconnection between the prefrontal and parietal cortices during working memory processing in schizophrenia: a[15(O)]H2O PET study. , 2003, The American journal of psychiatry.

[31]  Nils Bertschinger,et al.  Real-Time Computation at the Edge of Chaos in Recurrent Neural Networks , 2004, Neural Computation.

[32]  H. Adeli,et al.  Improved visibility graph fractality with application for the diagnosis of Autism Spectrum Disorder , 2012 .

[33]  Vasily A. Vakorin,et al.  Spatiotemporal Dependency of Age-Related Changes in Brain Signal Variability , 2013, Cerebral cortex.

[34]  Marcus Kaiser,et al.  Edge vulnerability in neural and metabolic networks , 2004, Biological Cybernetics.

[35]  Antonio José Ibañez-Molina,et al.  Effect of the average delay and mean connectivity of the Kuramoto model on the complexity of the output electroencephalograms , 2015, 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[36]  Hojjat Adeli,et al.  Wavelet-Synchronization Methodology: A New Approach for EEG-Based Diagnosis of ADHD , 2010, Clinical EEG and neuroscience.

[37]  Roberto Hornero,et al.  Nonlinear analysis of electroencephalogram and magnetoencephalogram recordings in patients with Alzheimer's disease , 2009, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

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

[39]  Murray Shanahan,et al.  Metastability and chimera states in modular delay and pulse-coupled oscillator networks. , 2012, Chaos.

[40]  T. Higuchi Approach to an irregular time series on the basis of the fractal theory , 1988 .

[41]  Woodrow L. Shew,et al.  Maximal Variability of Phase Synchrony in Cortical Networks with Neuronal Avalanches , 2012, The Journal of Neuroscience.

[42]  Peter J Hellyer,et al.  Cognitive Flexibility through Metastable Neural Dynamics Is Disrupted by Damage to the Structural Connectome , 2015, The Journal of Neuroscience.

[43]  Albert-László Barabási,et al.  Statistical mechanics of complex networks , 2001, ArXiv.

[44]  Alfred C. Schouten,et al.  Nonlinear Connectivity in the Human Stretch Reflex Assessed by Cross-Frequency Phase Coupling , 2016, Int. J. Neural Syst..

[45]  Murray Shanahan,et al.  Effects of lesions on synchrony and metastability in cortical networks , 2015, NeuroImage.

[46]  Roberto Hornero,et al.  Interpretation of the Lempel-Ziv Complexity Measure in the Context of Biomedical Signal Analysis , 2006, IEEE Transactions on Biomedical Engineering.

[47]  Albert-László Barabási,et al.  Error and attack tolerance of complex networks , 2000, Nature.

[48]  G. Edelman,et al.  Complexity and coherency: integrating information in the brain , 1998, Trends in Cognitive Sciences.

[49]  Gustavo Deco,et al.  Role of local network oscillations in resting-state functional connectivity , 2011, NeuroImage.

[50]  W. Singer,et al.  Abnormal neural oscillations and synchrony in schizophrenia , 2010, Nature Reviews Neuroscience.

[51]  S. Iglesias-Parro,et al.  Fractal characterization of internally and externally generated conscious experiences , 2014, Brain and Cognition.

[52]  Abraham Lempel,et al.  On the Complexity of Finite Sequences , 1976, IEEE Trans. Inf. Theory.

[53]  H. Adeli,et al.  Fractality and a Wavelet-chaos-Methodology for EEG-based Diagnosis of Alzheimer Disease , 2011, Alzheimer disease and associated disorders.

[54]  Silvia Conforto,et al.  Network attack simulations in Alzheimer's disease: The link between network tolerance and neurodegeneration , 2016, 2016 IEEE 13th International Symposium on Biomedical Imaging (ISBI).

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

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

[57]  Martin Randles,et al.  Distributed redundancy and robustness in complex systems , 2011, J. Comput. Syst. Sci..

[58]  Henry Markram,et al.  Real-Time Computing Without Stable States: A New Framework for Neural Computation Based on Perturbations , 2002, Neural Computation.

[59]  W. Singer,et al.  Neuronal Dynamics and Neuropsychiatric Disorders: Toward a Translational Paradigm for Dysfunctional Large-Scale Networks , 2012, Neuron.

[60]  Emilio Salinas,et al.  When Response Variability Increases Neural Network Robustness to Synaptic Noise , 2005, Neural Computation.

[61]  D. Abásolo,et al.  Use of the Higuchi's fractal dimension for the analysis of MEG recordings from Alzheimer's disease patients. , 2009, Medical Engineering and Physics.

[62]  Olaf Sporns,et al.  Modeling the Impact of Lesions in the Human Brain , 2009, PLoS Comput. Biol..

[63]  W. Singer Cortical dynamics revisited , 2013, Trends in Cognitive Sciences.

[64]  A. Faisal,et al.  Noise in the nervous system , 2008, Nature Reviews Neuroscience.

[65]  Jochen Braun,et al.  Attractors and noise: Twin drivers of decisions and multistability , 2010, NeuroImage.

[66]  J. Wackermann,et al.  Dimensional complexity of EEG brain mechanisms in untreated schizophrenia , 1993, Biological Psychiatry.

[67]  G. Tononi An information integration theory of consciousness , 2004, BMC Neuroscience.

[68]  Morten L. Kringelbach,et al.  Exploring the network dynamics underlying brain activity during rest , 2014, Progress in Neurobiology.

[69]  Jianbo Gao,et al.  Multiscale Analysis of Complex Time Series , 2007 .

[70]  Werner Lutzenberger,et al.  Fractal dimension of electroencephalographic time series and underlying brain processes , 1995, Biological Cybernetics.

[71]  N. Thakor,et al.  Detection of non-linearity in the EEG of schizophrenic patients , 2001, Clinical Neurophysiology.

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

[73]  Gudrun Stockmanns,et al.  Electroencephalographic Order Pattern Analysis for the Separation of Consciousness and Unconsciousness: An Analysis of Approximate Entropy, Permutation Entropy, Recurrence Rate, and Phase Coupling of Order Recurrence Plots , 2008, Anesthesiology.

[74]  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.

[75]  Hojjat Adeli,et al.  Fuzzy Synchronization Likelihood with Application to Attention-Deficit/Hyperactivity Disorder , 2011, Clinical EEG and neuroscience.

[76]  Hojjat Adeli,et al.  Fuzzy Synchronization Likelihood-wavelet methodology for diagnosis of autism spectrum disorder , 2012, Journal of Neuroscience Methods.

[77]  H. Adeli,et al.  Visibility graph similarity: A new measure of generalized synchronization in coupled dynamic systems , 2012 .

[78]  Danielle S Bassett,et al.  Brain graphs: graphical models of the human brain connectome. , 2011, Annual review of clinical psychology.

[79]  David B. Grayden,et al.  Probing to Observe Neural Dynamics Investigated with Networked Kuramoto Oscillators , 2017, Int. J. Neural Syst..

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

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

[82]  Thomas K. D. M. Peron,et al.  The Kuramoto model in complex networks , 2015, 1511.07139.

[83]  Ian M. McDonough,et al.  Network complexity as a measure of information processing across resting-state networks: evidence from the Human Connectome Project , 2014, Front. Hum. Neurosci..

[84]  Jari Saramäki,et al.  Two betweenness centrality measures based on Randomized Shortest Paths , 2015, Scientific Reports.

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

[86]  F. Wolf Symmetry, multistability, and long-range interactions in brain development. , 2005, Physical review letters.

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

[88]  Pablo Varona,et al.  Dynamical bridge between brain and mind , 2015, Trends in Cognitive Sciences.

[89]  M. Breakspear Dynamic models of large-scale brain activity , 2017, Nature Neuroscience.

[90]  H. Adeli,et al.  Fractality analysis of frontal brain in major depressive disorder. , 2012, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.