Aspects of randomness in neural graph structures

In the past two decades, significant advances have been made in understanding the structural and functional properties of biological networks, via graph-theoretic analysis. In general, most graph-theoretic studies are conducted in the presence of serious uncertainties, such as major undersampling of the experimental data. In the specific case of neural systems, however, a few moderately robust experimental reconstructions have been reported, and these have long served as fundamental prototypes for studying connectivity patterns in the nervous system. In this paper, we provide a comparative analysis of these “historical” graphs, both in their directed (original) and symmetrized (a common preprocessing step) forms, and provide a set of measures that can be consistently applied across graphs (directed or undirected, with or without self-loops). We focus on simple structural characterizations of network connectivity and find that in many measures, the networks studied are captured by simple random graph models. In a few key measures, however, we observe a marked departure from the random graph prediction. Our results suggest that the mechanism of graph formation in the networks studied is not well captured by existing abstract graph models in their first- and second-order connectivity.

[1]  Reinhard Diestel,et al.  Graph Theory , 1997 .

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

[3]  Gipsi Lima-Mendez,et al.  The powerful law of the power law and other myths in network biology. , 2009, Molecular bioSystems.

[4]  W. Gerstner,et al.  Non-normal amplification in random balanced neuronal networks. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[5]  Rolf Kötter,et al.  Online retrieval, processing, and visualization of primate connectivity data from the CoCoMac Database , 2007, Neuroinformatics.

[6]  Albert-László Barabási,et al.  Internet: Diameter of the World-Wide Web , 1999, Nature.

[7]  S. N. Dorogovtsev,et al.  Structure of Growing Networks: Exact Solution of the Barabasi--Albert's Model , 2000, cond-mat/0004434.

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

[9]  Julio M. Ottino,et al.  Complex networks , 2004, Encyclopedia of Big Data.

[10]  M. Young The organization of neural systems in the primate cerebral cortex , 1993, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[11]  S. Brenner,et al.  The structure of the nervous system of the nematode Caenorhabditis elegans. , 1986, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[12]  T. S. Evans,et al.  Complex networks , 2004 .

[13]  L. da F. Costa,et al.  Characterization of complex networks: A survey of measurements , 2005, cond-mat/0505185.

[14]  M. A. O'Neil,et al.  The connectional organization of the cortico-thalamic system of the cat. , 1999, Cerebral cortex.

[15]  John Scott What is social network analysis , 2010 .

[16]  U. Alon Biological Networks: The Tinkerer as an Engineer , 2003, Science.

[17]  Kevin E. Bassler,et al.  Efficient and Exact Sampling of Simple Graphs with Given Arbitrary Degree Sequence , 2010, PloS one.

[18]  Alex Roxin,et al.  The Role of Degree Distribution in Shaping the Dynamics in Networks of Sparsely Connected Spiking Neurons , 2011, Front. Comput. Neurosci..

[19]  Marián Boguñá,et al.  Topology of the world trade web. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[20]  S. Shen-Orr,et al.  Network motifs: simple building blocks of complex networks. , 2002, Science.

[21]  Matthieu Gilson,et al.  Emergence of network structure due to spike-timing-dependent plasticity in recurrent neuronal networks IV , 2009, Biological Cybernetics.

[22]  D. Modha,et al.  Network architecture of the long-distance pathways in the macaque brain , 2010, Proceedings of the National Academy of Sciences.

[23]  M. Young,et al.  Advanced database methodology for the Collation of Connectivity data on the Macaque brain (CoCoMac). , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[24]  Shilpa Chakravartula,et al.  Complex Networks: Structure and Dynamics , 2014 .

[25]  P. J. Sjöström,et al.  Functional specificity of local synaptic connections in neocortical networks , 2011, Nature.

[26]  A. Vespignani,et al.  Modeling of Protein Interaction Networks , 2001, Complexus.

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

[28]  K-I Goh,et al.  Fluctuation-driven dynamics of the internet topology. , 2002, Physical review letters.

[29]  S. N. Dorogovtsev,et al.  Structure of growing networks with preferential linking. , 2000, Physical review letters.

[30]  Ulrik Brandes,et al.  Biological Networks , 2013, Handbook of Graph Drawing and Visualization.

[31]  Lav R. Varshney,et al.  Structural Properties of the Caenorhabditis elegans Neuronal Network , 2009, PLoS Comput. Biol..

[32]  Sen Song,et al.  Highly Nonrandom Features of Synaptic Connectivity in Local Cortical Circuits , 2005, PLoS biology.

[33]  Theoden I. Netoff,et al.  Synchronization from Second Order Network Connectivity Statistics , 2011, Front. Comput. Neurosci..

[34]  Olaf Sporns,et al.  Classes of network connectivity and dynamics , 2001, Complex..

[35]  R. Jackson,et al.  The Matthew Effect in Science , 1988, International journal of dermatology.

[36]  Eric Shea-Brown,et al.  Motif statistics and spike correlations in neuronal networks , 2012, BMC Neuroscience.

[37]  S N Dorogovtsev,et al.  Effect of the accelerating growth of communications networks on their structure. , 2000, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

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

[40]  Olaf Sporns,et al.  Graph Theory Methods for the Analysis of Neural Connectivity Patterns , 2003 .

[41]  D. V. van Essen,et al.  Corticocortical and thalamocortical information flow in the primate visual system. , 2005, Progress in brain research.

[42]  W. Gerstner,et al.  Connectivity reflects coding: a model of voltage-based STDP with homeostasis , 2010, Nature Neuroscience.

[43]  A. Destexhe,et al.  Structual Vulnerability of the Nematode Worm Neural Graph , 2012, 1208.3383.

[44]  M. Porter,et al.  Critical Truths About Power Laws , 2012, Science.

[45]  Albert-László Barabási,et al.  Scale-free networks , 2008, Scholarpedia.

[46]  Stefan Rotter,et al.  The relevance of network micro-structure for neural dynamics , 2013, Front. Comput. Neurosci..

[47]  K. Goh,et al.  Universal behavior of load distribution in scale-free networks. , 2001, Physical review letters.

[48]  F. Chung,et al.  The average distances in random graphs with given expected degrees , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[49]  D J PRICE,et al.  NETWORKS OF SCIENTIFIC PAPERS. , 1965, Science.

[50]  Albert-László Barabási,et al.  Hierarchical organization in complex networks. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

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

[53]  S. N. Dorogovtsev,et al.  Evolution of networks , 2001, cond-mat/0106144.

[54]  Baktash Babadi,et al.  Pairwise Analysis Can Account for Network Structures Arising from Spike-Timing Dependent Plasticity , 2013, PLoS Comput. Biol..

[55]  S. N. Dorogovtsev,et al.  Giant strongly connected component of directed networks. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[56]  Fan Chung Graham,et al.  A random graph model for massive graphs , 2000, STOC '00.

[57]  Prof. Dr. Dr. Valentino Braitenberg,et al.  Cortex: Statistics and Geometry of Neuronal Connectivity , 1998, Springer Berlin Heidelberg.

[58]  Mark Newman,et al.  Networks: An Introduction , 2010 .

[59]  Stephanie Forrest,et al.  Email networks and the spread of computer viruses. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

[61]  Jacob G Foster,et al.  Edge direction and the structure of networks , 2009, Proceedings of the National Academy of Sciences.

[62]  V. Eguíluz,et al.  Highly clustered scale-free networks. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[63]  Sharon L. Milgram,et al.  The Small World Problem , 1967 .

[64]  Diego Garlaschelli,et al.  Patterns of link reciprocity in directed networks. , 2004, Physical review letters.

[65]  Khadija Iqbal,et al.  An introduction , 1996, Neurobiology of Aging.

[66]  Sarel J Fleishman,et al.  Comment on "Network Motifs: Simple Building Blocks of Complex Networks" and "Superfamilies of Evolved and Designed Networks" , 2004, Science.

[67]  D. V. Essen,et al.  Corticocortical and thalamocortical information flow in the primate visual system. , 2005 .

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

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

[70]  Paul Miller,et al.  Excitatory, Inhibitory, and Structural Plasticity Produce Correlated Connectivity in Random Networks Trained to Solve Paired-Stimulus Tasks , 2011, Front. Comput. Neurosci..

[71]  O. Sporns,et al.  Motifs in Brain Networks , 2004, PLoS biology.

[72]  D. Chklovskii,et al.  Wiring optimization can relate neuronal structure and function. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[73]  Frank Harary,et al.  Graph Theory , 2016 .

[74]  A. Barabasi,et al.  Network biology: understanding the cell's functional organization , 2004, Nature Reviews Genetics.

[75]  D. Bray Molecular Networks: The Top-Down View , 2003, Science.

[76]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[77]  G Tononi,et al.  Theoretical neuroanatomy: relating anatomical and functional connectivity in graphs and cortical connection matrices. , 2000, Cerebral cortex.

[78]  M. A. Muñoz,et al.  Entropic origin of disassortativity in complex networks. , 2010, Physical review letters.

[79]  Marcus Kaiser,et al.  Nonoptimal Component Placement, but Short Processing Paths, due to Long-Distance Projections in Neural Systems , 2006, PLoS Comput. Biol..

[80]  Michele Giugliano,et al.  Emergence of Connectivity Patterns from Long-Term and Short-Term Plasticities , 2012, ICANN.

[81]  M. A. Muñoz,et al.  Scale-free networks from varying vertex intrinsic fitness. , 2002, Physical review letters.

[82]  Tom A. B. Snijders,et al.  Social Network Analysis , 2011, International Encyclopedia of Statistical Science.

[83]  Kevin E. Bassler,et al.  Constructing and sampling directed graphs with given degree sequences , 2011, ArXiv.