Functional Brain Networks Formed Using Cross-Sample Entropy Are Scale Free

Over the previous decade, there has been an explosion of interest in network science, in general, and its application to the human brain, in particular. Most brain network investigations to date have used linear correlations (LinCorr) between brain areas to construct and then interpret brain networks. In this study, we applied an entropy-based method to establish functional connectivity between brain areas. This method is sensitive to both nonlinear and linear associations. The LinCorr-based and entropy-based techniques were applied to resting-state functional magnetic resonance imaging data from 10 subjects, and the resulting networks were compared. The networks derived from the entropy-based method exhibited power-law degree distributions. Moreover, the entropy-based networks had a higher clustering coefficient and a shorter path length compared with that of the LinCorr-based networks. While the LinCorr-based networks were assortative, with nodes with similar degrees preferentially connected, the entropy-based networks were disassortative, with high-degree hubs directly connected to low-degree nodes. It is likely that the differences in clustering and assortativity are due to "mega-hubs" in the entropy-based networks. These mega-hubs connect to a large majority of the nodes in the network. This is the first work clearly demonstrating differences between functional brain networks using linear and nonlinear techniques. The key finding is that the nonlinear technique produced networks with scale-free degree distributions. There remains debate among the neuroscience community as to whether human brains are scale free. These data support the argument that at least some aspects of the human brain are perhaps scale free.

[1]  Michael Small,et al.  Revising the simple measures of assortativity in complex networks. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

[3]  Albert,et al.  Emergence of scaling in random networks , 1999, Science.

[4]  Xiaoping Xie,et al.  Spatiotemporal nonlinearity in resting-state fMRI of the human brain , 2008, NeuroImage.

[5]  Alan C. Evans,et al.  Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. , 2007, Cerebral cortex.

[6]  Shan Yu,et al.  A Small World of Neuronal Synchrony , 2008, Cerebral cortex.

[7]  Cornelis J. Stam,et al.  Small-world and scale-free organization of voxel-based resting-state functional connectivity in the human brain , 2008, NeuroImage.

[8]  M. Newman,et al.  Mixing patterns in networks. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[9]  Paul J. Laurienti,et al.  The Ubiquity of Small-World Networks , 2011, Brain Connect..

[10]  Shlomo Havlin,et al.  Origins of fractality in the growth of complex networks , 2005, cond-mat/0507216.

[11]  K. Gurney,et al.  Network ‘Small-World-Ness’: A Quantitative Method for Determining Canonical Network Equivalence , 2008, PloS one.

[12]  K. Sneppen,et al.  Detection of topological patterns in complex networks: correlation profile of the internet , 2002, cond-mat/0205379.

[13]  Zhenghui Hu,et al.  Interregional Functional Connectivity via Pattern Synchrony , 2006, 2006 9th International Conference on Control, Automation, Robotics and Vision.

[14]  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.

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

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

[17]  W. Press,et al.  Numerical Recipes in Fortran: The Art of Scientific Computing.@@@Numerical Recipes in C: The Art of Scientific Computing. , 1994 .

[18]  Hong-Bo Xie,et al.  A comparative study of pattern synchronization detection between neural signals using different cross-entropy measures , 2010, Biological Cybernetics.

[19]  Lester Melie-García,et al.  Studying the human brain anatomical network via diffusion-weighted MRI and Graph Theory , 2008, NeuroImage.

[20]  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.

[21]  K. Sneppen,et al.  Specificity and Stability in Topology of Protein Networks , 2002, Science.

[22]  S. Hayasaka,et al.  Aging and the interaction of sensory cortical function and structure , 2009, Human brain mapping.

[23]  Maurizio Corbetta,et al.  Functional connectivity in resting-state fMRI: Is linear correlation sufficient? , 2011, NeuroImage.

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

[25]  G. Cecchi,et al.  Scale-free brain functional networks. , 2003, Physical review letters.

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

[27]  Paul J. Laurienti,et al.  A New Measure of Centrality for Brain Networks , 2010, PloS one.

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

[29]  M. Paluš,et al.  The role of nonlinearity in computing graph-theoretical properties of resting-state functional magnetic resonance imaging brain networks. , 2011, Chaos.

[30]  C. Stam,et al.  Use of non-linear EEG measures to characterize EEG changes during mental activity. , 1996, Electroencephalography and clinical neurophysiology.

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

[32]  Massimo Marchiori,et al.  Error and attacktolerance of complex network s , 2004 .

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

[34]  Tao Zhang,et al.  Cross‐sample entropy statistic as a measure of complexity and regularity of renal sympathetic nerve activity in the rat , 2007, Experimental physiology.

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

[36]  Cornelis J. Stam,et al.  Reliable detection of nonlinearity in experimental time series with strong periodic components , 1998 .

[37]  Paul J. Laurienti,et al.  The Brain as a Complex System: Using Network Science as a Tool for Understanding the Brain , 2011, Brain Connect..

[38]  C. Stam,et al.  Small-world networks and epilepsy: Graph theoretical analysis of intracerebrally recorded mesial temporal lobe seizures , 2007, Clinical Neurophysiology.

[39]  Tao Zhang,et al.  Synchrony analysis between blood pressure and sympathetic nerve signal inhibited by atrial receptor stimulation in Wistar rats , 2002, Experimental physiology.

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

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

[42]  S M Pincus,et al.  Approximate entropy as a measure of system complexity. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[43]  Paul J. Laurienti,et al.  Universal fractal scaling of self-organized networks , 2010 .

[44]  Anthony Randal McIntosh,et al.  Complexity analysis of source activity underlying the neuromagnetic somatosensory steady-state response , 2010, NeuroImage.

[45]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[46]  Stefano Mossa,et al.  Truncation of power law behavior in "scale-free" network models due to information filtering. , 2002, Physical review letters.

[47]  W. Pritchard,et al.  Dimensional analysis of resting human EEG. II: Surrogate-data testing indicates nonlinearity but not low-dimensional chaos. , 1995, Psychophysiology.

[48]  Paul J. Laurienti,et al.  Comparison of characteristics between region-and voxel-based network analyses in resting-state fMRI data , 2010, NeuroImage.

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

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

[51]  Mark W. Woolrich,et al.  Network modelling methods for FMRI , 2011, NeuroImage.

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

[53]  Li-Zhi Liu,et al.  Cross-sample entropy of foreign exchange time series , 2010 .

[54]  H E Stanley,et al.  Classes of small-world networks. , 2000, Proceedings of the National Academy of Sciences of the United States of America.