Synchrony and Asynchrony for Neuronal Dynamics Defined on Complex Networks

We describe and analyze a model for a stochastic pulse-coupled neuronal network with many sources of randomness: random external input, potential synaptic failure, and random connectivity topologies. We show that different classes of network topologies give rise to qualitatively different types of synchrony: uniform (Erdős–Rényi) and “small-world” networks give rise to synchronization phenomena similar to that in “all-to-all” networks (in which there is a sharp onset of synchrony as coupling is increased); in contrast, in “scale-free” networks the dependence of synchrony on coupling strength is smoother. Moreover, we show that in the uniform and small-world cases, the fine details of the network are not important in determining the synchronization properties; this depends only on the mean connectivity. In contrast, for scale-free networks, the dynamics are significantly affected by the fine details of the network; in particular, they are significantly affected by the local neighborhoods of the “hubs” in the network.

[1]  Ian Stewart,et al.  Target Patterns and Spirals in Planar Reaction-Diffusion Systems , 2000, J. Nonlinear Sci..

[2]  Charles S Peskin,et al.  Synchrony and Asynchrony in a Fully Stochastic Neural Network , 2008, Bulletin of mathematical biology.

[3]  John M. Beggs,et al.  Neuronal Avalanches Are Diverse and Precise Activity Patterns That Are Stable for Many Hours in Cortical Slice Cultures , 2004, The Journal of Neuroscience.

[4]  S. Strogatz,et al.  The spectrum of the locked state for the Kuramoto model of coupled oscillators , 2005 .

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

[6]  Ian Stewart,et al.  Symmetry and Pattern Formation in Coupled Cell Networks , 1999 .

[7]  Ian Stewart,et al.  Hopf bifurcation with dihedral group symmetry - Coupled nonlinear oscillators , 1986 .

[8]  M. Golubitsky,et al.  Singularities and groups in bifurcation theory , 1985 .

[9]  J. M. Herrmann,et al.  Phase transitions towards criticality in a neural system with adaptive interactions. , 2009, Physical review letters.

[10]  Lawrence Sirovich,et al.  Dynamics of neuronal populations: eigenfunction theory; some solvable cases , 2003, Network.

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

[12]  Charles S. Peskin,et al.  Mathematical aspects of heart physiology , 1975 .

[13]  Y. Kuramoto Collective synchronization of pulse-coupled oscillators and excitable units , 1991 .

[14]  Paul Erdös,et al.  On random graphs, I , 1959 .

[15]  David J. Galas,et al.  A duplication growth model of gene expression networks , 2002, Bioinform..

[16]  Stephen Coombes,et al.  A Dynamical Theory of Spike Train Transitions in Networks of Integrate-and-Fire Oscillators , 2000, SIAM J. Appl. Math..

[17]  Jürgen Kurths,et al.  Synchronization - A Universal Concept in Nonlinear Sciences , 2001, Cambridge Nonlinear Science Series.

[18]  Binghong Wang,et al.  Scaling invariance in spectra of complex networks: a diffusion factorial moment approach. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[19]  M. Golubitsky,et al.  Multiparameter Bifurcation Theory , 1986 .

[20]  Bruce W. Knight,et al.  Dynamics of Encoding in a Population of Neurons , 1972, The Journal of general physiology.

[21]  D. Tranchina,et al.  Population density methods for large-scale modelling of neuronal networks with realistic synaptic kinetics: cutting the dimension down to size. , 2001, Network.

[22]  M. Golubitsky,et al.  Patterns of Oscillation in Coupled Cell Systems , 2002 .

[23]  Svante Janson,et al.  Random graphs , 2000, Wiley-Interscience series in discrete mathematics and optimization.

[24]  M. Golubitsky,et al.  Interior symmetry and local bifurcation in coupled cell networks , 2004 .

[25]  Ian Stewart,et al.  Patterns of Synchrony in Coupled Cell Networks with Multiple Arrows , 2005, SIAM J. Appl. Dyn. Syst..

[26]  M. Golubitsky,et al.  Hopf Bifurcation in the presence of symmetry , 1984 .

[27]  P. Bressloff,et al.  DYNAMICS OF A RING OF PULSE-COUPLED OSCILLATORS : GROUP THEORETIC APPROACH , 1997 .

[28]  Eric Shea-Brown,et al.  Winding Numbers and Average Frequencies in Phase Oscillator Networks , 2006, J. Nonlinear Sci..

[29]  Walter Senn,et al.  Similar NonLeaky Integrate-and-Fire Neurons with Instantaneous Couplings Always Synchronize , 2001, SIAM J. Appl. Math..

[30]  M. Golubitsky,et al.  Bifurcations on hemispheres , 1991 .

[31]  Louis Tao,et al.  KINETIC THEORY FOR NEURONAL NETWORK DYNAMICS , 2006 .

[32]  Ian Stewart,et al.  Coupled cells with internal symmetry: I. Wreath products , 1996 .

[33]  Hansel,et al.  Clustering and slow switching in globally coupled phase oscillators. , 1993, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[34]  Deok-Sun Lee Synchronization transition in scale-free networks: clusters of synchrony. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[35]  S. Strogatz,et al.  Synchronization of pulse-coupled biological oscillators , 1990 .

[36]  Sompolinsky,et al.  Pattern of synchrony in inhomogeneous networks of oscillators with pulse interactions. , 1993, Physical review letters.

[37]  Béla Bollobás,et al.  Directed scale-free graphs , 2003, SODA '03.

[38]  J. M. Herrmann,et al.  Finite-size effects of avalanche dynamics. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[39]  A. Winfree The geometry of biological time , 1991 .

[40]  M. Golubitsky,et al.  Nonlinear dynamics of networks: the groupoid formalism , 2006 .

[41]  Adilson E Motter,et al.  Heterogeneity in oscillator networks: are smaller worlds easier to synchronize? , 2003, Physical review letters.

[42]  Mauricio Barahona,et al.  Synchronization in small-world systems. , 2002, Physical review letters.

[43]  Darren J. Wilkinson Stochastic Modelling for Systems Biology , 2006 .

[44]  Jerrold E. Marsden,et al.  Generic bifurcation of Hamiltonian systems with symmetry , 1987 .

[45]  W. T. Gowers,et al.  RANDOM GRAPHS (Wiley Interscience Series in Discrete Mathematics and Optimization) , 2001 .

[46]  Ian Stewart,et al.  Symmetry and stability in Taylor Couette flow , 1986 .

[47]  Alvis Brazma,et al.  Current approaches to gene regulatory network modelling , 2007, BMC Bioinformatics.

[48]  James M. Bower,et al.  Computational modeling of genetic and biochemical networks , 2001 .

[49]  Ian Stewart,et al.  Some Curious Phenomena in Coupled Cell Networks , 2004, J. Nonlinear Sci..

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

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

[52]  Abbott,et al.  Asynchronous states in networks of pulse-coupled oscillators. , 1993, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

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

[54]  Yoshiki Kuramoto,et al.  Chemical Oscillations, Waves, and Turbulence , 1984, Springer Series in Synergetics.

[55]  S. Janson,et al.  Wiley‐Interscience Series in Discrete Mathematics and Optimization , 2011 .

[56]  P. Erdos,et al.  On the evolution of random graphs , 1984 .

[57]  Béla Bollobás,et al.  Random Graphs , 1985 .

[58]  Steven H. Strogatz,et al.  The Spectrum of the Partially Locked State for the Kuramoto Model , 2007, J. Nonlinear Sci..

[59]  Robert D. Leclerc Survival of the sparsest: robust gene networks are parsimonious , 2008, Molecular systems biology.

[60]  Peter Dayan,et al.  Theoretical Neuroscience: Computational and Mathematical Modeling of Neural Systems , 2001 .

[61]  Chris Arney Sync: The Emerging Science of Spontaneous Order , 2007 .

[62]  S. Strogatz,et al.  Solvable model for chimera states of coupled oscillators. , 2008, Physical review letters.

[63]  Cheng Ly,et al.  Population density methods for stochastic neurons with realistic synaptic kinetics: Firing rate dynamics and fast computational methods , 2006, Network.

[64]  M. Golubitsky,et al.  Coupled cells with internal symmetry: II. Direct products , 1996 .

[65]  Marcus Pivato,et al.  Symmetry Groupoids and Patterns of Synchrony in Coupled Cell Networks , 2003, SIAM J. Appl. Dyn. Syst..

[66]  M. Shelley,et al.  An effective kinetic representation of fluctuation-driven neuronal networks with application to simple and complex cells in visual cortex. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[67]  DeLiang Wang,et al.  Synchrony and Desynchrony in Integrate-and-Fire Oscillators , 1998, Neural Computation.

[68]  Martin Golubitsky,et al.  Pattern Formation in Continuous and Coupled Systems , 1999 .

[69]  N. Alon,et al.  The Probabilistic Method: Alon/Probabilistic , 2008 .

[70]  N. Kopell,et al.  Dynamics of two mutually coupled slow inhibitory neurons , 1998 .

[71]  J. Craggs Applied Mathematical Sciences , 1973 .

[72]  P. Bressloff,et al.  Desynchronization, Mode Locking, and Bursting in Strongly Coupled Integrate-and-Fire Oscillators , 1998 .

[73]  G. Ermentrout,et al.  Synchrony, stability, and firing patterns in pulse-coupled oscillators , 2002 .

[74]  M. Golubitsky,et al.  The Symmetry Perspective , 2002 .

[75]  Béla Bollobás,et al.  Random Graphs: Notation , 2001 .

[76]  M. Golubitsky,et al.  SYNCHRONY VERSUS SYMMETRY IN COUPLED CELLS , 2005 .

[77]  J. M. Herrmann,et al.  Dynamical synapses causing self-organized criticality in neural networks , 2007, 0712.1003.

[78]  Edward R. Dougherty,et al.  Probabilistic Boolean networks: a rule-based uncertainty model for gene regulatory networks , 2002, Bioinform..

[79]  Jurgen Kurths,et al.  Synchronization in complex networks , 2008, 0805.2976.

[80]  A. Pikovsky,et al.  Synchronization: Theory and Application , 2003 .

[81]  Nicolas Brunel,et al.  Fast Global Oscillations in Networks of Integrate-and-Fire Neurons with Low Firing Rates , 1999, Neural Computation.

[82]  P. Bressloff,et al.  Traveling Waves in a Chain of Pulse-Coupled Oscillators , 1998 .

[83]  L F Lago-Fernández,et al.  Fast response and temporal coherent oscillations in small-world networks. , 1999, Physical review letters.

[84]  Ian Stewart,et al.  A modular network for legged locomotion , 1998 .

[85]  Ian Stewart,et al.  Spatiotemporal Symmetries in the Disynaptic Canal-Neck Projection , 2007, SIAM J. Appl. Math..

[86]  B. Bollobás The evolution of random graphs , 1984 .

[87]  Ralf Blossey Computational Biology (Chapman & Hall/Crc Mathematical and Computational Biology Series) , 2006 .

[88]  Noga Alon,et al.  The Probabilistic Method , 2015, Fundamentals of Ramsey Theory.

[89]  W. Gerstner,et al.  Coherence and incoherence in a globally coupled ensemble of pulse-emitting units. , 1993, Physical review letters.

[90]  M. Golubitsky,et al.  Time-periodic spatially periodic planforms in Euclidean equivariant partial differential equations , 1995, Philosophical Transactions of the Royal Society of London. Series A: Physical and Engineering Sciences.

[91]  M. Golubitsky,et al.  Coupled Cells: Wreath Products and Direct Products , 1994 .

[92]  N. Alon,et al.  Wiley‐Interscience Series in Discrete Mathematics and Optimization , 2004 .

[93]  Jiang-Hua Lu,et al.  Progress in Mathematics , 2013 .

[94]  John M. Beggs,et al.  Neuronal Avalanches in Neocortical Circuits , 2003, The Journal of Neuroscience.

[95]  Beom Jun Kim,et al.  Synchronization on small-world networks. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[96]  Bard Ermentrout,et al.  When inhibition not excitation synchronizes neural firing , 1994, Journal of Computational Neuroscience.

[97]  J. Bascompte Networks in ecology , 2007 .

[98]  J. Spencer,et al.  Dynamics of Stochastic Neuronal Networks and the Connections to Random Graph Theory , 2010 .

[99]  Pascal Chossat,et al.  Dynamics, Bifurcation and Symmetry , 1994 .

[100]  V. Latora,et al.  Complex networks: Structure and dynamics , 2006 .

[101]  Lawrence Sirovich,et al.  Dynamics of Neuronal Populations: The Equilibrium Solution , 2000, SIAM J. Appl. Math..

[102]  J. García-Ojalvo,et al.  Effects of noise in excitable systems , 2004 .

[103]  Alan Weinstein,et al.  Geometry, Mechanics, and Dynamics , 2002 .

[104]  Ian Stewart,et al.  SPIRALS IN SCALAR REACTION–DIFFUSION EQUATIONS , 1995 .