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      Efficient Network Reconstruction from Dynamical Cascades Identifies Small-World Topology of Neuronal Avalanches

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      1 , 2 , *
      PLoS Computational Biology
      Public Library of Science

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          Abstract

          Cascading activity is commonly found in complex systems with directed interactions such as metabolic networks, neuronal networks, or disease spreading in social networks. Substantial insight into a system's organization can be obtained by reconstructing the underlying functional network architecture from the observed activity cascades. Here we focus on Bayesian approaches and reduce their computational demands by introducing the Iterative Bayesian (IB) and Posterior Weighted Averaging (PWA) methods. We introduce a special case of PWA, cast in nonparametric form, which we call the normalized count (NC) algorithm. NC efficiently reconstructs random and small-world functional network topologies and architectures from subcritical, critical, and supercritical cascading dynamics and yields significant improvements over commonly used correlation methods. With experimental data, NC identified a functional and structural small-world topology and its corresponding traffic in cortical networks with neuronal avalanche dynamics.

          Author Summary

          In many complex systems found across disciplines, such as biological cells and organisms, social networks, economic systems, and the Internet, individual elements interact with each other, thereby forming large networks whose structure is often not known. In these complex networks, local events can easily propagate, resulting in diverse spatio-temporal activity cascades, or avalanches. Examples of such cascading activity are the propagation of diseases in social networks, cascades of chemical reactions inside a cell, the propagation of neuronal activity in the brain, and e-mail forwarding on the Internet. Although the observation of a single cascade provides limited insight into the organization of a complex network, the observation of many cascades allows for the reconstruction of very robust features of network organization, providing valuable insight into network function as well as network failure. The current work develops new algorithms for an efficient reconstruction of relatively large networks in the context of cascading activity. When applied to the brain, these algorithms uncover the structural and functional features of gray matter networks that display activity cascades in the form of neuronal avalanches.

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          Most cited references71

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          Emergence of scaling in random networks

          Systems as diverse as genetic networks or the World Wide Web are best described as networks with complex topology. A common property of many large networks is that the vertex connectivities follow a scale-free power-law distribution. This feature was found to be a consequence of two generic mechanisms: (i) networks expand continuously by the addition of new vertices, and (ii) new vertices attach preferentially to sites that are already well connected. A model based on these two ingredients reproduces the observed stationary scale-free distributions, which indicates that the development of large networks is governed by robust self-organizing phenomena that go beyond the particulars of the individual systems.
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            Identification and Classification of Hubs in Brain Networks

            Brain regions in the mammalian cerebral cortex are linked by a complex network of fiber bundles. These inter-regional networks have previously been analyzed in terms of their node degree, structural motif, path length and clustering coefficient distributions. In this paper we focus on the identification and classification of hub regions, which are thought to play pivotal roles in the coordination of information flow. We identify hubs and characterize their network contributions by examining motif fingerprints and centrality indices for all regions within the cerebral cortices of both the cat and the macaque. Motif fingerprints capture the statistics of local connection patterns, while measures of centrality identify regions that lie on many of the shortest paths between parts of the network. Within both cat and macaque networks, we find that a combination of degree, motif participation, betweenness centrality and closeness centrality allows for reliable identification of hub regions, many of which have previously been functionally classified as polysensory or multimodal. We then classify hubs as either provincial (intra-cluster) hubs or connector (inter-cluster) hubs, and proceed to show that lesioning hubs of each type from the network produces opposite effects on the small-world index. Our study presents an approach to the identification and classification of putative hub regions in brain networks on the basis of multiple network attributes and charts potential links between the structural embedding of such regions and their functional roles.
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              Similar network activity from disparate circuit parameters.

              It is often assumed that cellular and synaptic properties need to be regulated to specific values to allow a neuronal network to function properly. To determine how tightly neuronal properties and synaptic strengths need to be tuned to produce a given network output, we simulated more than 20 million versions of a three-cell model of the pyloric network of the crustacean stomatogastric ganglion using different combinations of synapse strengths and neuron properties. We found that virtually indistinguishable network activity can arise from widely disparate sets of underlying mechanisms, suggesting that there could be considerable animal-to-animal variability in many of the parameters that control network activity, and that many different combinations of synaptic strengths and intrinsic membrane properties can be consistent with appropriate network performance.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Comput Biol
                plos
                ploscomp
                PLoS Computational Biology
                Public Library of Science (San Francisco, USA )
                1553-734X
                1553-7358
                January 2009
                January 2009
                30 January 2009
                : 5
                : 1
                : e1000271
                Affiliations
                [1 ]Mathematical and Statistical Computing Laboratory, Division of Computational Bioscience, Center for Information Technology, National Institutes of Health, Bethesda, Maryland, United States of America
                [2 ]Section on Critical Brain Dynamics, Laboratory of Systems Neuroscience, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland, United States of America
                Indiana University, United States of America
                Author notes

                Conceived and designed the experiments: SP DP. Performed the experiments: SP DP. Analyzed the data: SP DP. Wrote the paper: SP DP.

                Article
                08-PLCB-RA-0592R2
                10.1371/journal.pcbi.1000271
                2615076
                19180180
                e056cc23-fa1f-4904-8752-c30c2a8c504e
                This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
                History
                : 21 July 2008
                : 10 December 2008
                Page count
                Pages: 20
                Categories
                Research Article
                Computational Biology
                Computational Biology/Computational Neuroscience
                Computational Biology/Metabolic Networks
                Computational Biology/Signaling Networks
                Mathematics/Statistics
                Neuroscience
                Neuroscience/Theoretical Neuroscience

                Quantitative & Systems biology
                Quantitative & Systems biology

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