Correlated fluctuations in strongly-coupled binary networks beyond equilibrium

Randomly coupled Ising spins constitute the classical model of collective phenomena in disordered systems, with applications covering ferromagnetism, combinatorial optimization, protein folding, stock market dynamics, and social dynamics. The phase diagram of these systems is obtained in the thermodynamic limit by averaging over the quenched randomness of the couplings. However, many applications require the statistics of activity for a single realization of the possibly asymmetric couplings in finite-sized networks. Examples include reconstruction of couplings from the observed dynamics, learning in the central nervous system by correlation-sensitive synaptic plasticity, and representation of probability distributions for sampling-based inference. The systematic cumulant expansion for kinetic binary (Ising) threshold units with strong, random and asymmetric couplings presented here goes beyond mean-field theory and is applicable outside thermodynamic equilibrium; a system of approximate non-linear equations predicts average activities and pairwise covariances in quantitative agreement with full simulations down to hundreds of units. The linearized theory yields an expansion of the correlation- and response functions in collective eigenmodes, leads to an efficient algorithm solving the inverse problem, and shows that correlations are invariant under scaling of the interaction strengths.

[1]  R. Palmer,et al.  Solution of 'Solvable model of a spin glass' , 1977 .

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

[3]  S. Solla,et al.  Memory networks with asymmetric bonds , 1987 .

[4]  Klas H. Pettersen,et al.  Modeling the Spatial Reach of the LFP , 2011, Neuron.

[5]  John C. Mason,et al.  Mathematics of Neural Networks , 1997, Operations Research/Computer Science Interfaces Series.

[6]  Maxi San Miguel,et al.  Is the Voter Model a model for voters? , 2013, Physical review letters.

[7]  Wulfram Gerstner,et al.  Phenomenological models of synaptic plasticity based on spike timing , 2008, Biological Cybernetics.

[8]  H. Risken Fokker-Planck Equation , 1996 .

[9]  R. Mazo On the theory of brownian motion , 1973 .

[10]  K. Koketsu,et al.  Cholinergic and inhibitory synapses in a pathway from motor‐axon collaterals to motoneurones , 1954, The Journal of physiology.

[11]  H. Sompolinsky,et al.  Transition to chaos in random neuronal networks , 2015, 1508.06486.

[12]  Ehud Zohary,et al.  Correlated neuronal discharge rate and its implications for psychophysical performance , 1994, Nature.

[13]  Marcel Abendroth,et al.  Quantum Field Theory And Critical Phenomena , 2016 .

[14]  Moritz Helias,et al.  Invariance of covariances arises out of noise , 2013 .

[15]  J. Touboul,et al.  Heterogeneous connections induce oscillations in large-scale networks. , 2012, Physical review letters.

[16]  Alessandro Vespignani,et al.  Dynamical Processes on Complex Networks , 2008 .

[17]  S. Fortunato,et al.  Statistical physics of social dynamics , 2007, 0710.3256.

[18]  E. Ising Beitrag zur Theorie des Ferromagnetismus , 1925 .

[19]  J. Cowan,et al.  Field-theoretic approach to fluctuation effects in neural networks. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[20]  Anders Krogh,et al.  Introduction to the theory of neural computation , 1994, The advanced book program.

[21]  Moritz Helias,et al.  Scalability of Asynchronous Networks Is Limited by One-to-One Mapping between Effective Connectivity and Correlations , 2014, PLoS Comput. Biol..

[22]  J. Gleeson Binary-state dynamics on complex networks: pair approximation and beyond , 2012, 1209.2983.

[23]  D. Sornette Physics and financial economics (1776–2014): puzzles, Ising and agent-based models , 2014, Reports on progress in physics. Physical Society.

[24]  H. Nishimori Statistical Physics of Spin Glasses and Information Processing , 2001 .

[25]  Alexander S. Ecker,et al.  Decorrelated Neuronal Firing in Cortical Microcircuits , 2010, Science.

[26]  Moritz Helias,et al.  Decorrelation of Neural-Network Activity by Inhibitory Feedback , 2012, PLoS Comput. Biol..

[27]  Andrzej Cichocki,et al.  Nonnegative Matrix and Tensor Factorization T , 2007 .

[28]  Brent Doiron,et al.  Self-Organization of Microcircuits in Networks of Spiking Neurons with Plastic Synapses , 2015, PLoS Comput. Biol..

[29]  U. Seifert Stochastic thermodynamics, fluctuation theorems and molecular machines , 2012, Reports on progress in physics. Physical Society.

[30]  G. Bi,et al.  Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type , 1998, The Journal of Neuroscience.

[31]  Cugliandolo,et al.  Analytical solution of the off-equilibrium dynamics of a long-range spin-glass model. , 1993, Physical review letters.

[32]  Carson C. Chow,et al.  Correlations, fluctuations, and stability of a finite-size network of coupled oscillators. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

[34]  A. Fisher,et al.  The Theory of Critical Phenomena: An Introduction to the Renormalization Group , 1992 .

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

[36]  Konrad P Kording,et al.  How advances in neural recording affect data analysis , 2011, Nature Neuroscience.

[37]  Carson C. Chow,et al.  Effective stochastic behavior in dynamical systems with incomplete information. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[38]  R. Kass,et al.  Multiple neural spike train data analysis: state-of-the-art and future challenges , 2004, Nature Neuroscience.

[39]  J J Hopfield,et al.  Neural networks and physical systems with emergent collective computational abilities. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[40]  J. Cowan,et al.  Stochastic neurodynamics and the system size expansion , 1997 .

[41]  Toshiyuki TANAKA Mean-field theory of Boltzmann machine learning , 1998 .

[42]  Peter Dayan,et al.  Computational Differences between Asymmetrical and Symmetrical Networks , 1998, NIPS.

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

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

[45]  Carson C. Chow,et al.  Kinetic theory of coupled oscillators. , 2006, Physical review letters.

[46]  R. Monasson,et al.  High-dimensional inference with the generalized Hopfield model: principal component analysis and corrections. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[47]  G. Buzsáki Large-scale recording of neuronal ensembles , 2004, Nature Neuroscience.

[48]  Adriano Barra,et al.  Extensive parallel processing on scale-free networks. , 2014, Physical review letters.

[49]  Nicolas Brunel,et al.  A Three-Threshold Learning Rule Approaches the Maximal Capacity of Recurrent Neural Networks , 2015, PLoS Comput. Biol..

[50]  Charles M. Newman,et al.  Spin Glasses and Complexity , 2013 .

[51]  Moritz Helias,et al.  The correlation structure of local cortical networks intrinsically results from recurrent dynamics , 2013 .

[52]  S. Amari Homogeneous nets of neuron-like elements , 1975, Biological Cybernetics.

[53]  K. Nakanishi,et al.  Mean-field theory for a spin-glass model of neural networks: TAP free energy and the paramagnetic to spin-glass transition , 1997, cond-mat/9705015.

[54]  Haim Sompolinsky,et al.  Dynamic Theory of the Spin Glass Phase , 1981 .

[55]  Erik Aurell,et al.  Frontiers in Computational Neuroscience , 2022 .

[56]  P. Berkes,et al.  Statistically Optimal Perception and Learning: from Behavior to Neural Representations , 2022 .

[57]  Erik Aurell,et al.  Network inference using asynchronously updated kinetic Ising model. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[58]  S. Shinomoto,et al.  A cognitive and associative memory , 2004, Biological Cybernetics.

[59]  Anthony Unwin,et al.  Reversibility and Stochastic Networks , 1980 .

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

[61]  H. Markram,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997, Science.

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

[63]  James L. McClelland,et al.  Parallel distributed processing: explorations in the microstructure of cognition, vol. 1: foundations , 1986 .

[64]  B. Derrida Dynamical phase transition in nonsymmetric spin glasses , 1987 .

[65]  Young,et al.  Inferring statistical complexity. , 1989, Physical review letters.

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

[67]  M. Cohen,et al.  Measuring and interpreting neuronal correlations , 2011, Nature Neuroscience.

[68]  J. Thomson,et al.  Philosophical Magazine , 1945, Nature.

[69]  H. C. LONGUET-HIGGINS,et al.  Non-Holographic Associative Memory , 1969, Nature.

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

[71]  Moritz Helias,et al.  A General and Efficient Method for Incorporating Precise Spike Times in Globally Time-Driven Simulations , 2010, Front. Neuroinform..

[72]  Herbert Jaeger,et al.  The''echo state''approach to analysing and training recurrent neural networks , 2001 .

[73]  鈴木 増雄 Time-Dependent Statistics of the Ising Model , 1965 .

[74]  西森 秀稔 Statistical physics of spin glasses and information processing : an introduction , 2001 .

[75]  Sherrington,et al.  Dynamical replica theory for disordered spin systems. , 1995, Physical review. B, Condensed matter.

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

[77]  J. Gleeson High-accuracy approximation of binary-state dynamics on networks. , 2011, Physical review letters.

[78]  M. Mezard,et al.  Exact mean-field inference in asymmetric kinetic Ising systems , 2011, 1103.3433.

[79]  S. Kirkpatrick,et al.  Solvable Model of a Spin-Glass , 1975 .

[80]  D. Sherrington Stochastic Processes in Physics and Chemistry , 1983 .

[81]  S. Swain Handbook of Stochastic Methods for Physics, Chemistry and the Natural Sciences , 1984 .

[82]  Moritz Helias,et al.  A unified view on weakly correlated recurrent networks , 2013, Front. Comput. Neurosci..

[83]  Christian Heyerdahl-Larsen,et al.  Correlations , 2013 .

[84]  Michael I. Jordan,et al.  Advances in Neural Information Processing Systems 30 , 1995 .

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

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

[87]  W. Maass,et al.  What makes a dynamical system computationally powerful ? , 2022 .

[88]  Michael A. Buice,et al.  Dynamic Finite Size Effects in Spiking Neural Networks , 2013, PLoS Comput. Biol..

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

[90]  W. Ebeling Stochastic Processes in Physics and Chemistry , 1995 .

[91]  Thilo Gross,et al.  Epidemic dynamics on an adaptive network. , 2005, Physical review letters.

[92]  Nicolas Brunel,et al.  Author's Personal Copy Understanding the Relationships between Spike Rate and Delta/gamma Frequency Bands of Lfps and Eegs Using a Local Cortical Network Model , 2022 .

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

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

[95]  S. Sharma,et al.  The Fokker-Planck Equation , 2010 .

[96]  Sonja Grün,et al.  Long-Term Modifications in Motor Cortical Dynamics Induced by Intensive Practice , 2009, The Journal of Neuroscience.

[97]  W. Bialek,et al.  Maximum entropy models for antibody diversity , 2009, Proceedings of the National Academy of Sciences.

[98]  H. Kappen,et al.  Mean field theory for asymmetric neural networks. , 2000, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[99]  Paul C. Bressloff,et al.  Stochastic Neural Field Theory and the System-Size Expansion , 2009, SIAM J. Appl. Math..

[100]  T. Plefka Convergence condition of the TAP equation for the infinite-ranged Ising spin glass model , 1982 .

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

[102]  Michael J. Berry,et al.  Weak pairwise correlations imply strongly correlated network states in a neural population , 2005, Nature.

[103]  Sompolinsky,et al.  Dynamics of spin systems with randomly asymmetric bonds: Langevin dynamics and a spherical model. , 1987, Physical review. A, General physics.

[104]  James P Roach,et al.  Memory recall and spike-frequency adaptation. , 2016, Physical review. E.