Transition to chaos in random neuronal networks

Firing patterns in the central nervous system often exhibit strong temporal irregularity and heterogeneity in their time averaged response properties. Previous studies suggested that these properties are outcome of an intrinsic chaotic dynamics. Indeed, simplified rate-based large neuronal networks with random synaptic connections are known to exhibit sharp transition from fixed point to chaotic dynamics when the synaptic gain is increased. However, the existence of a similar transition in neuronal circuit models with more realistic architectures and firing dynamics has not been established. In this work we investigate rate based dynamics of neuronal circuits composed of several subpopulations and random connectivity. Nonzero connections are either positive-for excitatory neurons, or negative for inhibitory ones, while single neuron output is strictly positive; in line with known constraints in many biological systems. Using Dynamic Mean Field Theory, we find the phase diagram depicting the regimes of stable fixed point, unstable dynamic and chaotic rate fluctuations. We characterize the properties of systems near the chaotic transition and show that dilute excitatory-inhibitory architectures exhibit the same onset to chaos as a network with Gaussian connectivity. Interestingly, the critical properties near transition depend on the shape of the single- neuron input-output transfer function near firing threshold. Finally, we investigate network models with spiking dynamics. When synaptic time constants are slow relative to the mean inverse firing rates, the network undergoes a sharp transition from fast spiking fluctuations and static firing rates to a state with slow chaotic rate fluctuations. When the synaptic time constants are finite, the transition becomes smooth and obeys scaling properties, similar to crossover phenomena in statistical mechanics

[1]  G. G. Stokes "J." , 1890, The New Yale Book of Quotations.

[2]  H. Sompolinsky,et al.  Relaxational dynamics of the Edwards-Anderson model and the mean-field theory of spin-glasses , 1982 .

[3]  李基炯,et al.  § 14 , 1982, Fichte.

[4]  A. Wolf,et al.  Determining Lyapunov exponents from a time series , 1985 .

[5]  M. Mézard,et al.  Spin Glass Theory and Beyond , 1987 .

[6]  Henry C. Tuckwell,et al.  Introduction to theoretical neurobiology , 1988 .

[7]  Sommers,et al.  Chaos in random neural networks. , 1988, Physical review letters.

[8]  M. V. Rossum,et al.  In Neural Computation , 2022 .

[9]  Physical Review Letters 63 , 1989 .

[10]  최인후,et al.  13 , 1794, Tao te Ching.

[11]  Moshe Abeles,et al.  Corticonics: Neural Circuits of Cerebral Cortex , 1991 .

[12]  W. J. Nowack Methods in Neuronal Modeling , 1991, Neurology.

[13]  D. Heeger Normalization of cell responses in cat striate cortex , 1992, Visual Neuroscience.

[14]  William R. Softky,et al.  The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  K. H. Britten,et al.  Power spectrum analysis of bursting cells in area MT in the behaving monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  Bard Ermentrout,et al.  Reduction of Conductance-Based Models with Slow Synapses to Neural Nets , 1994, Neural Computation.

[17]  Sompolinsky,et al.  Theory of correlations in stochastic neural networks. , 1994, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[18]  D. Signorini,et al.  Neural networks , 1995, The Lancet.

[19]  D. G. Albrecht Visual cortex neurons in monkey and cat: Effect of contrast on the spatial and temporal phase transfer functions , 1995, Visual Neuroscience.

[20]  William R. Softky,et al.  Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons. , 1996, Journal of neurophysiology.

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

[22]  Bard Ermentrout,et al.  Linearization of F-I Curves by Adaptation , 1998, Neural Computation.

[23]  Nicholas J. Priebe,et al.  Contrast-Invariant Orientation Tuning in Cat Visual Cortex: Thalamocortical Input Tuning and Correlation-Based Intracortical Connectivity , 1998, The Journal of Neuroscience.

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

[25]  Nicolas Brunel,et al.  Phase diagrams of sparsely connected networks of excitatory and inhibitory spiking neurons , 2000, Neurocomputing.

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

[27]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[28]  P. Greengard The neurobiology of slow synaptic transmission. , 2001, Science.

[29]  Emery N. Brown,et al.  The Time-Rescaling Theorem and Its Application to Neural Spike Train Data Analysis , 2002, Neural Computation.

[30]  D. Hansel,et al.  How Noise Contributes to Contrast Invariance of Orientation Tuning in Cat Visual Cortex , 2002, The Journal of Neuroscience.

[31]  Henry Markram,et al.  Real-Time Computing Without Stable States: A New Framework for Neural Computation Based on Perturbations , 2002, Neural Computation.

[32]  BMC Neuroscience , 2003 .

[33]  Oren Shriki,et al.  Rate Models for Conductance-Based Cortical Neuronal Networks , 2003, Neural Computation.

[34]  Nils Bertschinger,et al.  Real-Time Computation at the Edge of Chaos in Recurrent Neural Networks , 2004, Neural Computation.

[35]  Harald Haas,et al.  Harnessing Nonlinearity: Predicting Chaotic Systems and Saving Energy in Wireless Communication , 2004, Science.

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

[37]  Haim Sompolinsky,et al.  Chaos and synchrony in a model of a hypercolumn in visual cortex , 1996, Journal of Computational Neuroscience.

[38]  Nicolas Brunel,et al.  Dynamics of Sparsely Connected Networks of Excitatory and Inhibitory Spiking Neurons , 2000, Journal of Computational Neuroscience.

[39]  R. Shapley,et al.  Information Tuning of Populations of Neurons in Primary Visual Cortex , 2004, The Journal of Neuroscience.

[40]  Robert A. Legenstein,et al.  2007 Special Issue: Edge of chaos and prediction of computational performance for neural circuit models , 2007 .

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

[42]  Nicholas J. Priebe,et al.  Inhibition, Spike Threshold, and Stimulus Selectivity in Primary Visual Cortex , 2008, Neuron.

[43]  L. F. Abbott,et al.  Generating Coherent Patterns of Activity from Chaotic Neural Networks , 2009, Neuron.

[44]  Herbert Jaeger,et al.  Reservoir computing approaches to recurrent neural network training , 2009, Comput. Sci. Rev..

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

[46]  D. Hansel,et al.  Very long transients, irregular firing, and chaotic dynamics in networks of randomly connected inhibitory integrate-and-fire neurons. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[47]  王丹,et al.  Plos Computational Biology主编关于论文获得发表的10条简单法则的评析 , 2009 .

[48]  Michael A. Buice,et al.  Systematic Fluctuation Expansion for Neural Network Activity Equations , 2009, Neural Computation.

[49]  L. Abbott,et al.  Stimulus-dependent suppression of chaos in recurrent neural networks. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[50]  P. Dayan,et al.  Supporting Online Material Materials and Methods Som Text Figs. S1 to S9 References the Asynchronous State in Cortical Circuits , 2022 .

[51]  Benjamin Schrauwen,et al.  Connectivity, Dynamics, and Memory in Reservoir Computing with Binary and Analog Neurons , 2010, Neural Computation.

[52]  Matthew J. Rosseinsky,et al.  Physical Review B , 2011 .

[53]  Fred Wolf,et al.  Single cell dynamics determine strength of chaos in collective network dynamics , 2011, BMC Neuroscience.

[54]  Nicolas Brunel,et al.  From Spiking Neuron Models to Linear-Nonlinear Models , 2011, PLoS Comput. Biol..

[55]  L. Abbott,et al.  Beyond the edge of chaos: amplification and temporal integration by recurrent networks in the chaotic regime. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[56]  A. Litwin-Kumar,et al.  Slow dynamics and high variability in balanced cortical networks with clustered connections , 2012, Nature Neuroscience.

[57]  G. Wainrib,et al.  Topological and dynamical complexity of random neural networks. , 2012, Physical review letters.

[58]  Jonathan Touboul,et al.  Large Deviations, Dynamics and Phase Transitions in Large Stochastic and Disordered Neural Networks , 2013, Journal of Statistical Physics.

[59]  L. Abbott,et al.  From fixed points to chaos: Three models of delayed discrimination , 2013, Progress in Neurobiology.

[60]  L. F. Abbott,et al.  A Complex-Valued Firing-Rate Model That Approximates the Dynamics of Spiking Networks , 2013, PLoS Comput. Biol..

[61]  W. Newsome,et al.  Context-dependent computation by recurrent dynamics in prefrontal cortex , 2013, Nature.

[62]  Srdjan Ostojic,et al.  Two types of asynchronous activity in networks of excitatory and inhibitory spiking neurons , 2014, Nature Neuroscience.

[63]  Moritz Helias,et al.  The Correlation Structure of Local Neuronal Networks Intrinsically Results from Recurrent Dynamics , 2013, PLoS Comput. Biol..

[64]  Nicolas Brunel,et al.  Single neuron dynamics and computation , 2014, Current Opinion in Neurobiology.

[65]  Kenneth D Miller,et al.  Properties of networks with partially structured and partially random connectivity. , 2013, Physical review. E, Statistical, nonlinear, and soft matter physics.

[66]  David Hansel,et al.  Asynchronous Rate Chaos in Spiking Neuronal Circuits , 2015, bioRxiv.

[67]  Geoffrey Zweig,et al.  Using Recurrent Neural Networks for Slot Filling in Spoken Language Understanding , 2015, IEEE/ACM Transactions on Audio, Speech, and Language Processing.

[68]  Merav Stern,et al.  Transition to chaos in random networks with cell-type-specific connectivity. , 2014, Physical review letters.

[69]  Karin Ackermann,et al.  Progress In Neurobiology , 2016 .

[70]  Sandra Lowe Methods In Neuronal Modeling From Synapses To Networks , 2016 .

[71]  R. K. Simpson Nature Neuroscience , 2022 .

[72]  October I Physical Review Letters , 2022 .