The simplest problem in the collective dynamics of neural networks: is synchrony stable?

For spiking neural networks we consider the stability problem of global synchrony, arguably the simplest non-trivial collective dynamics in such networks. We find that even this simplest dynamical problem—local stability of synchrony—is non-trivial to solve and requires novel methods for its solution. In particular, the discrete mode of pulsed communication together with the complicated connectivity of neural interaction networks requires a non-standard approach. The dynamics in the vicinity of the synchronous state is determined by a multitude of linear operators, in contrast to a single stability matrix in conventional linear stability theory. This unusual property qualitatively depends on network topology and may be neglected for globally coupled homogeneous networks. For generic networks, however, the number of operators increases exponentially with the size of the network. We present methods to treat this multi-operator problem exactly. First, based on the Gershgorin and Perron–Frobenius theorems, we derive bounds on the eigenvalues that provide important information about the synchronization process but are not sufficient to establish the asymptotic stability or instability of the synchronous state. We then present a complete analysis of asymptotic stability for topologically strongly connected networks using simple graphtheoretical considerations. For inhibitory interactions between dissipative (leaky) oscillatory neurons the synchronous state is stable, independent of the parameters and the network connectivity. These results indicate that pulse-like interactions play a profound role in network dynamical systems, and in particular in the dynamics of biological synchronization, unless the coupling is homogeneous and all-to-all. The concepts introduced here are expected to also facilitate the exact analysis of

[1]  H. Sompolinsky,et al.  Chaos in Neuronal Networks with Balanced Excitatory and Inhibitory Activity , 1996, Science.

[2]  M. Timme,et al.  Prevalence of unstable attractors in networks of pulse-coupled oscillators. , 2002, Physical review letters.

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

[4]  Marc Timme,et al.  Designing the dynamics of spiking neural networks. , 2006, Physical review letters.

[5]  Antonio Politi,et al.  Desynchronized stable states in diluted neural networks , 2007, Neurocomputing.

[6]  M. Lewin On nonnegative matrices , 1971 .

[7]  Stephen Coombes,et al.  Synchrony in an array of integrate-and-fire neurons with dendritic structure , 1997 .

[8]  Marc Timme,et al.  Breaking synchrony by heterogeneity in complex networks. , 2003, Physical review letters.

[9]  T. Geisel,et al.  Delay-induced multistable synchronization of biological oscillators , 1998 .

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

[11]  Arnold Neumaier,et al.  Introduction to Numerical Analysis , 2001 .

[12]  O. Perron Zur Theorie der Matrices , 1907 .

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

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

[15]  M. Timme,et al.  Designing complex networks , 2006, q-bio/0606041.

[16]  David W. Lewis,et al.  Matrix theory , 1991 .

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

[18]  Wulfram Gerstner,et al.  What Matters in Neuronal Locking? , 1996, Neural Computation.

[19]  Charles M. Gray,et al.  Synchronous oscillations in neuronal systems: Mechanisms and functions , 1994, Journal of Computational Neuroscience.

[20]  R. Rosenfeld Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[21]  Antonio Politi,et al.  Stability of the splay state in pulse-coupled networks. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[22]  Haim Sompolinsky,et al.  Chaotic Balanced State in a Model of Cortical Circuits , 1998, Neural Computation.

[23]  Marc Timme,et al.  Topological speed limits to network synchronization. , 2003, Physical review letters.

[24]  D. Hansel,et al.  Existence and stability of persistent states in large neuronal networks. , 2001, Physical review letters.

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

[26]  M. Timme,et al.  Stable irregular dynamics in complex neural networks. , 2007, Physical review letters.

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

[28]  Antonio Politi,et al.  Desynchronization in diluted neural networks. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[29]  Ernst,et al.  Synchronization induced by temporal delays in pulse-coupled oscillators. , 1995, Physical review letters.

[30]  Vreeswijk,et al.  Partial synchronization in populations of pulse-coupled oscillators. , 1996, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[31]  J. Hopfield,et al.  Earthquake cycles and neural reverberations: Collective oscillations in systems with pulse-coupled threshold elements. , 1995, Physical review letters.

[32]  M. Timme,et al.  Unstable attractors: existence and robustness in networks of oscillators with delayed pulse coupling , 2005, cond-mat/0501384.

[33]  David Golomb,et al.  The Number of Synaptic Inputs and the Synchrony of Large, Sparse Neuronal Networks , 2000, Neural Computation.

[34]  D. Hansel,et al.  Role of delays in shaping spatiotemporal dynamics of neuronal activity in large networks. , 2005, Physical review letters.

[35]  Ad Aertsen,et al.  Stable propagation of synchronous spiking in cortical neural networks , 1999, Nature.

[36]  Arenas,et al.  Synchronization in a lattice model of pulse-coupled oscillators. , 1995, Physical review letters.

[37]  Tianping Chen,et al.  Desynchronization of pulse-coupled oscillators with delayed excitatory coupling , 2007 .

[38]  C. Vanvreeswijk Analysis of the asynchronous state in networks of strongly coupled oscillators , 2000 .

[39]  M. Timme,et al.  Long chaotic transients in complex networks. , 2004, Physical review letters.

[40]  Marc Timme,et al.  Unstable attractors induce perpetual synchronization and desynchronization. , 2002, Chaos.

[41]  R. Eckhorn,et al.  Coherent oscillations: A mechanism of feature linking in the visual cortex? , 1988, Biological Cybernetics.

[42]  Marc Timme,et al.  Speed of synchronization in complex networks of neural oscillators: analytic results based on Random Matrix Theory. , 2005, Chaos.

[43]  Marc Timme,et al.  Coexistence of regular and irregular dynamics in complex networks of pulse-coupled oscillators. , 2002, Physical review letters.

[44]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[45]  Matthias M. Müller,et al.  Human Gamma Band Activity and Perception of a Gestalt , 1999, The Journal of Neuroscience.