Functional Brain Networks: Random, “Small World” or Deterministic?

Lately the problem of connectivity in brain networks is being approached frequently by graph theoretical analysis. In several publications based on bivariate estimators of relations between EEG channels authors reported random or “small world” structure of networks. The results of these works often have no relation to other evidence based on imaging, inverse solutions methods, physiological and anatomical data. Herein we try to find reasons for this discrepancy. We point out that EEG signals are very much interdependent, thus bivariate measures applied to them may produce many spurious connections. In fact, they may outnumber the true connections. Giving all connections equal weights, as it is usual in the framework of graph theoretical analysis, further enhances these spurious links. In effect, close to random and disorganized patterns of connections emerge. On the other hand, multivariate connectivity estimators, which are free of the artificial links, show specific, well determined patterns, which are in a very good agreement with other evidence. The modular structure of brain networks may be identified by multivariate estimators based on Granger causality and formalism of assortative mixing. In this way, the strength of coupling may be evaluated quantitatively. During working memory task, by means of multivariate Directed Transfer Function, it was demonstrated that the modules characterized by strong internal bonds exchange the information by weaker connections.

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

[2]  Lutz Jäncke,et al.  The Problem of Thresholding in Small-World Network Analysis , 2013, PloS one.

[3]  M. Kaminski,et al.  Topographic analysis of coherence and propagation of EEG activity during sleep and wakefulness. , 1997, Electroencephalography and clinical neurophysiology.

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

[5]  U Klose,et al.  Coregistration of EEG and fMRI in a simple motor task , 1996, Human brain mapping.

[6]  Katarzyna J. Blinowska,et al.  Multivariate Signal Analysis by Parametric Models , 2006 .

[7]  Artur Marchewka,et al.  A role for the right prefrontal and bilateral parietal cortex in four-term transitive reasoning: an fMRI study with abstract linear syllogism tasks. , 2011, Acta neurobiologiae experimentalis.

[8]  Aneta Brzezicka,et al.  Application of directed transfer function and network formalism for the assessment of functional connectivity in working memory task , 2013, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[9]  Ciprian M Crainiceanu,et al.  Dynamics of event‐related causality in brain electrical activity , 2008, Human brain mapping.

[10]  Katarzyna J. Blinowska,et al.  Review of the methods of determination of directed connectivity from multichannel data , 2011, Medical & Biological Engineering & Computing.

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

[12]  Fuhui Long,et al.  Feature selection based on mutual information criteria of max-dependency, max-relevance, and min-redundancy , 2003, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[13]  Maciej Kaminski,et al.  Transmission of Brain Activity During Cognitive Task , 2010, Brain Topography.

[14]  Arnaud Delorme,et al.  Frontal midline EEG dynamics during working memory , 2005, NeuroImage.

[15]  Sloutsky,et al.  The Neural Correlates of Logical Thinking: An Event-Related fMRI Study , 2005 .

[16]  Vinod Goel,et al.  A role for right ventrolateral prefrontal cortex in reasoning about indeterminate relations , 2009, Neuropsychologia.

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

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

[19]  M E J Newman,et al.  Finding and evaluating community structure in networks. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

[21]  Masahiro Kawasaki,et al.  Oscillatory gamma and theta activity during repeated mental manipulations of a visual image , 2007, Neuroscience Letters.

[22]  P. Nunez,et al.  Electric fields of the brain , 1981 .

[23]  B. Efron Bootstrap Methods: Another Look at the Jackknife , 1979 .

[24]  Manfred G Kitzbichler,et al.  Cognitive Effort Drives Workspace Configuration of Human Brain Functional Networks , 2011, The Journal of Neuroscience.

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

[26]  G Pfurtscheller,et al.  Propagation of EEG Activity in the Beta and Gamma Band during Movement Imagery in Humans , 2005, Methods of Information in Medicine.

[27]  Klaus Lehnertz,et al.  Identifying important nodes in weighted functional brain networks: a comparison of different centrality approaches. , 2012, Chaos.

[28]  Manuel Schabus,et al.  Fronto-parietal EEG coherence in theta and upper alpha reflect central executive functions of working memory. , 2005, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[29]  K. Blinowska,et al.  Propagation of EEG activity during finger movement and its imagination. , 2006, Acta neurobiologiae experimentalis.

[30]  P J Franaszczuk,et al.  Analysis of mesial temporal seizure onset and propagation using the directed transfer function method. , 1994, Electroencephalography and clinical neurophysiology.

[31]  M. Knyazeva,et al.  EEG-Based Functional Brain Networks: Does the Network Size Matter? , 2012, PloS one.

[32]  Vladimir M. Sloutsky,et al.  fMRI Evidence for a Three-Stage Model of Deductive Reasoning , 2006 .

[33]  Jaroslaw Zygierewicz,et al.  Practical Biomedical Signal Analysis Using MATLAB® , 2011 .

[34]  Aneta Brzezicka,et al.  Information Transfer During a Transitive Reasoning Task , 2010, Brain Topography.

[35]  C. Stam,et al.  Altered sleep brain functional connectivity in acutely depressed patients , 2009, Human brain mapping.

[36]  C. Stam,et al.  The organization of physiological brain networks , 2012, Clinical Neurophysiology.

[37]  Francesco Rundo,et al.  Dynamics of the EEG slow-wave synchronization during sleep , 2005, Clinical Neurophysiology.

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

[39]  David Hinkley,et al.  Bootstrap Methods: Another Look at the Jackknife , 2008 .

[40]  M. Kaminski,et al.  Granger causality and information flow in multivariate processes. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[41]  M. Kaminski,et al.  Phase and amplitude analysis in time–frequency space—application to voluntary finger movement , 2001, Journal of Neuroscience Methods.

[42]  Martin Suter,et al.  Small World , 2002 .

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

[44]  Katarzyna J. Blinowska,et al.  Determination of EEG activity propagation: pair-wise versus multichannel estimate , 2004, IEEE Transactions on Biomedical Engineering.

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

[46]  Vladimir M. Sloutsky,et al.  fMRI Evidence for a Three-Stage Model of Deductive Reasoning , 2006, Journal of Cognitive Neuroscience.

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

[48]  C. Stam,et al.  Using graph theoretical analysis of multi channel EEG to evaluate the neural efficiency hypothesis , 2006, Neuroscience Letters.

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

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

[51]  Mahdi Jalili,et al.  Constructing brain functional networks from EEG: partial and unpartial correlations. , 2011, Journal of integrative neuroscience.

[52]  M K Habib,et al.  Dynamics of neuronal firing correlation: modulation of "effective connectivity". , 1989, Journal of neurophysiology.

[53]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.