Stability of random brain networks with excitatory and inhibitory connections

Stability of randomly connected networks of neural populations with randomly distributed excitatory and inhibitory connections is investigated using a simplified physiologically-based model of brain electrical activity. Connections within a random network are randomly assigned to be excitatory or inhibitory, and the strengths of excitatory and inhibitory connections have two distinct distributions. Stability is shown to depend on the size of the network, the connection probability, and the mean and variance of the network's distribution of connection strengths, thus constraining these quantities. Networks with a nonzero variance for their excitatory and inhibitory strengths are less likely to be stable than networks with zero variance. The effect of changes in overall network activity on an individual population is also investigated. The maximum excitatory and inhibitory inputs into a population are constrained by stability and occur when the magnitudes of the mean excitatory and inhibitory connection strengths are equal and the proportion of connections that are inhibitory has a fixed value less than 0.5. Results consistent with experimentally determined brain networks.

[1]  F. L. D. Silva,et al.  Dynamics of the human alpha rhythm: evidence for non-linearity? , 1999, Clinical Neurophysiology.

[2]  Peter A. Robinson,et al.  Stability and spectra of randomly connected excitatory cortical networks , 2007, Neurocomputing.

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

[4]  Karl J. Friston,et al.  Modulation of excitatory synaptic coupling facilitates synchronization and complex dynamics in a nonlinear model of neuronal dynamics , 2003, Neurocomputing.

[5]  C. L. Chapman,et al.  Toward an integrated continuum model of cerebral dynamics: the cerebral rhythms, synchronous oscillation and cortical stability. , 2001, Bio Systems.

[6]  Peter N. Robinson,et al.  Stability and synchronization of random brain networks with a distribution of connection strengths , 2008, Neurocomputing.

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

[8]  Sitabhra Sinha,et al.  Assortative mixing by degree makes a network more unstable , 2005 .

[9]  M P Young,et al.  Anatomical connectivity defines the organization of clusters of cortical areas in the macaque monkey and the cat. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[10]  O. Sporns,et al.  Organization, development and function of complex brain networks , 2004, Trends in Cognitive Sciences.

[11]  C. Blakemore,et al.  Analysis of connectivity in the cat cerebral cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  P. Goldman-Rakic,et al.  Preface: Cerebral Cortex Has Come of Age , 1991 .

[13]  M. Young,et al.  The architecture of visual cortex and inferential processes in vision. , 2000, Spatial vision.

[14]  P. Robinson,et al.  Dynamics of large-scale brain activity in normal arousal states and epileptic seizures. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[15]  Prof. Dr. Valentino Braitenberg,et al.  Anatomy of the Cortex , 1991, Studies of Brain Function.

[16]  Peter N. Robinson,et al.  STEADY STATES AND GLOBAL DYNAMICS OF ELECTRICAL ACTIVITY IN THE CEREBRAL CORTEX , 1998 .

[17]  Jianfeng Feng,et al.  Synchronization in networks with random interactions: theory and applications. , 2006, Chaos.

[18]  B Jouve,et al.  A mathematical approach to the connectivity between the cortical visual areas of the macaque monkey. , 1998, Cerebral cortex.

[19]  Andre Levchenko,et al.  Dynamic Properties of Network Motifs Contribute to Biological Network Organization , 2005, PLoS biology.

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

[21]  John R. Terry,et al.  A unifying explanation of primary generalized seizures through nonlinear brain modeling and bifurcation analysis. , 2006, Cerebral cortex.

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

[23]  János Komlós,et al.  The eigenvalues of random symmetric matrices , 1981, Comb..

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

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

[26]  Vladimir E. Bondarenko,et al.  A simple neural network model produces chaos similar to the human EEG , 1994 .

[27]  E. Wigner Random Matrices in Physics , 1967 .

[28]  A. Crisanti,et al.  Products of random matrices in statistical physics , 1993 .

[29]  Dmitri B. Chklovskii,et al.  Wiring Optimization in Cortical Circuits , 2002, Neuron.

[30]  C Cherniak,et al.  Component placement optimization in the brain , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  M. Breakspear Nonlinear phase desynchronization in human electroencephalographic data , 2002, Human brain mapping.

[32]  T. Guhr,et al.  RANDOM-MATRIX THEORIES IN QUANTUM PHYSICS : COMMON CONCEPTS , 1997, cond-mat/9707301.

[33]  P. Robinson,et al.  Prediction of electroencephalographic spectra from neurophysiology. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[34]  M P Young,et al.  Hierarchical organization of macaque and cat cortical sensory systems explored with a novel network processor. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[36]  Karl J. Friston,et al.  Modulation of excitatory synaptic coupling facilitates synchronization and complex dynamics in a biophysical model of neuronal dynamics , 2003 .

[37]  Sommers,et al.  Spectrum of large random asymmetric matrices. , 1988, Physical review letters.

[38]  P A Robinson,et al.  Estimation of multiscale neurophysiologic parameters by electroencephalographic means , 2004, Human brain mapping.

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

[40]  Seth Bullock,et al.  Timescale and Stability in Adaptive Behaviour , 2005, ECAL.

[41]  Hod Lipson,et al.  Networks, dynamics, and modularity. , 2004, Physical review letters.

[42]  V. Protopopescu,et al.  Timely detection of dynamical change in scalp EEG signals. , 2000, Chaos.