The Complexity of Dynamics in Small Neural Circuits

Mean-field approximations are a powerful tool for studying large neural networks. However, they do not describe well the behavior of networks composed of a small number of neurons. In this case, major differences between the mean-field approximation and the real behavior of the network can arise. Yet, many interesting problems in neuroscience involve the study of mesoscopic networks composed of a few tens of neurons. Nonetheless, mathematical methods that correctly describe networks of small size are still rare, and this prevents us to make progress in understanding neural dynamics at these intermediate scales. Here we develop a novel systematic analysis of the dynamics of arbitrarily small networks composed of homogeneous populations of excitatory and inhibitory firing-rate neurons. We study the local bifurcations of their neural activity with an approach that is largely analytically tractable, and we numerically determine the global bifurcations. We find that for strong inhibition these networks give rise to very complex dynamics, caused by the formation of multiple branching solutions of the neural dynamics equations that emerge through spontaneous symmetry-breaking. This qualitative change of the neural dynamics is a finite-size effect of the network, that reveals qualitative and previously unexplored differences between mesoscopic cortical circuits and their mean-field approximation. The most important consequence of spontaneous symmetry-breaking is the ability of mesoscopic networks to regulate their degree of functional heterogeneity, which is thought to help reducing the detrimental effect of noise correlations on cortical information processing.

[1]  Jian Xu,et al.  Study of double Hopf bifurcation and chaos for an oscillator with time delayed feedback , 2002 .

[2]  Alain-Sol Sznitman A propagation of chaos result for Burgers' equation , 1986 .

[3]  M. Samuelides,et al.  Random recurrent neural networks dynamics , 2006, math-ph/0612022.

[4]  V. Mountcastle The columnar organization of the neocortex. , 1997, Brain : a journal of neurology.

[5]  Olivier Faugeras,et al.  A Formalism for Evaluating Analytically the Cross-Correlation Structure of a Firing-Rate Network Model , 2015, The Journal of Mathematical Neuroscience (JMN).

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

[7]  Stefano Panzeri,et al.  Modelling and analysis of local field potentials for studying the function of cortical circuits , 2013, Nature Reviews Neuroscience.

[8]  Olivier D. Faugeras,et al.  Noise-Induced Behaviors in Neural Mean Field Dynamics , 2011, SIAM J. Appl. Dyn. Syst..

[9]  A. Sznitman Nonlinear reflecting diffusion process, and the propagation of chaos and fluctuations associated , 1984 .

[10]  H. McKean,et al.  A CLASS OF MARKOV PROCESSES ASSOCIATED WITH NONLINEAR PARABOLIC EQUATIONS , 1966, Proceedings of the National Academy of Sciences of the United States of America.

[11]  C. Koch,et al.  The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes , 2012, Nature Reviews Neuroscience.

[12]  David Terman,et al.  Mathematical foundations of neuroscience , 2010 .

[13]  S. Amari Dynamics of pattern formation in lateral-inhibition type neural fields , 1977, Biological Cybernetics.

[14]  Ben H. Jansen,et al.  A neurophysiologically-based mathematical model of flash visual evoked potentials , 2004, Biological Cybernetics.

[15]  O. Sporns Small-world connectivity, motif composition, and complexity of fractal neuronal connections. , 2006, Bio Systems.

[16]  Willy Govaerts,et al.  MATCONT: A MATLAB package for numerical bifurcation analysis of ODEs , 2003, TOMS.

[17]  D. Buxhoeveden,et al.  The minicolumn hypothesis in neuroscience. , 2002, Brain : a journal of neurology.

[18]  Michael N. Shadlen,et al.  Noise, neural codes and cortical organization , 1994, Current Opinion in Neurobiology.

[19]  Randall D. Beer,et al.  Parameter Space Structure of Continuous-Time Recurrent Neural Networks , 2006, Neural Computation.

[20]  J J Hopfield,et al.  Neurons with graded response have collective computational properties like those of two-state neurons. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Ingber,et al.  Generic mesoscopic neural networks based on statistical mechanics of neocortical interactions. , 1992, Physical review. A, Atomic, molecular, and optical physics.

[22]  Claudia Clopath,et al.  Local inhibitory plasticity tunes macroscopic brain dynamics and allows the emergence of functional brain networks , 2016, NeuroImage.

[23]  J. Touboul,et al.  Mean-field description and propagation of chaos in networks of Hodgkin-Huxley and FitzHugh-Nagumo neurons , 2012, The Journal of Mathematical Neuroscience.

[24]  Alberto Tesi,et al.  Harmonic balance methods for the analysis of chaotic dynamics in nonlinear systems , 1992, Autom..

[25]  Boris Loginov,et al.  Lyapunov-Schmidt Methods in Nonlinear Analysis and Applications , 2002 .

[26]  Y. Kuznetsov Elements of Applied Bifurcation Theory , 2023, Applied Mathematical Sciences.

[27]  L. Ingber Statistical mechanics of neocortical interactions. Derivation of short-term-memory capacity , 1984 .

[28]  Sofia B. S. D. Castro,et al.  Symmetry-breaking as an origin of species , 2003 .

[29]  T. Sejnowski,et al.  Thalamocortical oscillations in the sleeping and aroused brain. , 1993, Science.

[30]  Toby Elmhirst Sn-Equivariant Symmetry-Breaking bifurcations , 2004, Int. J. Bifurc. Chaos.

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

[32]  Hamid Soltanian-Zadeh,et al.  Integrated MEG/EEG and fMRI model based on neural masses , 2006, IEEE Transactions on Biomedical Engineering.

[33]  J. Cowan,et al.  A mathematical theory of visual hallucination patterns , 1979, Biological Cybernetics.

[34]  Karl J. Friston,et al.  The Dynamic Brain: From Spiking Neurons to Neural Masses and Cortical Fields , 2008, PLoS Comput. Biol..

[35]  Zhang Yi,et al.  Multistability Analysis for Recurrent Neural Networks with Unsaturating Piecewise Linear Transfer Functions , 2003, Neural Computation.

[36]  Germán Mato,et al.  Synchrony in Excitatory Neural Networks , 1995, Neural Computation.

[37]  J. Macke,et al.  Neural population coding: combining insights from microscopic and mass signals , 2015, Trends in Cognitive Sciences.

[38]  R. Williams,et al.  The control of neuron number. , 1988, Annual review of neuroscience.

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

[40]  Olivier Faugeras,et al.  A large deviation principle for networks of rate neurons with correlated synaptic weights , 2013, BMC Neuroscience.

[41]  DeLiang Wang,et al.  Synchronization and desynchronization in a network of locally coupled Wilson-Cowan oscillators , 1996, IEEE Trans. Neural Networks.

[42]  Maurizio Corbetta,et al.  Resting-State Functional Connectivity Emerges from Structurally and Dynamically Shaped Slow Linear Fluctuations , 2013, The Journal of Neuroscience.

[43]  Hiroshi Tanaka Probabilistic treatment of the Boltzmann equation of Maxwellian molecules , 1978 .

[44]  Olaf Sporns,et al.  The Human Connectome: A Structural Description of the Human Brain , 2005, PLoS Comput. Biol..

[45]  P A Robinson,et al.  Simulated Electrocortical Activity at Microscopic, Mesoscopic, and Global Scales , 2003, Neuropsychopharmacology.

[46]  L. Allan The perception of time , 1979 .

[47]  R. Quiroga,et al.  Extracting information from neuronal populations : information theory and decoding approaches , 2022 .

[48]  Henk Nijmeijer,et al.  Synchronization and Graph Topology , 2005, Int. J. Bifurc. Chaos.

[49]  F. Pasemann Complex dynamics and the structure of small neural networks , 2002, Network.

[50]  Nicolas Brunel,et al.  Sensory neural codes using multiplexed temporal scales , 2010, Trends in Neurosciences.

[51]  Eugene M. Izhikevich,et al.  Weakly Connected Quasi-periodic Oscillators, FM Interactions, and Multiplexing in the Brain , 1999, SIAM J. Appl. Math..

[52]  Eugene M. Izhikevich,et al.  Polychronization: Computation with Spikes , 2006, Neural Computation.

[53]  Olivier D. Faugeras,et al.  Neural Mass Activity, Bifurcations, and Epilepsy , 2011, Neural Computation.

[54]  S. Strogatz,et al.  Chimera states for coupled oscillators. , 2004, Physical review letters.

[55]  Bard Ermentrout,et al.  Simulating, analyzing, and animating dynamical systems - a guide to XPPAUT for researchers and students , 2002, Software, environments, tools.

[56]  A V Herz,et al.  Neural codes: firing rates and beyond. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[57]  A. Sznitman Topics in propagation of chaos , 1991 .

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

[59]  Paul C. Bressloff,et al.  Path-Integral Methods for Analyzing the Effects of Fluctuations in Stochastic Hybrid Neural Networks , 2015, The Journal of Mathematical Neuroscience (JMN).

[60]  Hiroshi Tanaka,et al.  Central limit theorem for a simple diffusion model of interacting particles , 1981 .

[61]  Andrew Jenkins,et al.  General Anesthetic Actions on GABAA Receptors , 2010, Current neuropharmacology.

[62]  H. Sompolinsky,et al.  13 Modeling Feature Selectivity in Local Cortical Circuits , 2022 .

[63]  J. Sleigh,et al.  Modelling general anaesthesia as a first-order phase transition in the cortex. , 2004, Progress in biophysics and molecular biology.

[64]  William C. Schieve,et al.  A bifurcation analysis of the four dimensional generalized Hopfield neural network , 1995 .

[65]  Jochen J. Steil,et al.  Input space bifurcation manifolds of recurrent neural networks , 2005, Neurocomputing.

[66]  YU PEI Double Hopf Bifurcations and Chaos of a Nonlinear Vibration System , .

[67]  W J Freeman,et al.  Patterns of variation in waveform of averaged evoked potentials from prepyriform cortex of cats. , 1968, Journal of neurophysiology.

[68]  L. Rüschendorf,et al.  On the Perception of Time , 2009, Gerontology.

[69]  E. Izhikevich,et al.  Weakly connected neural networks , 1997 .

[70]  M. Corbetta,et al.  How Local Excitation–Inhibition Ratio Impacts the Whole Brain Dynamics , 2014, The Journal of Neuroscience.

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

[72]  Ben H. Jansen,et al.  Electroencephalogram and visual evoked potential generation in a mathematical model of coupled cortical columns , 1995, Biological Cybernetics.

[73]  J. D. Cowan,et al.  Large-scale activity in neural nets I: Theory with application to motoneuron pool responses , 2004, Biological Cybernetics.

[74]  François Grimbert Mesoscopic models of cortical structures , 2008 .

[75]  L. M. Ward,et al.  Synchronous neural oscillations and cognitive processes , 2003, Trends in Cognitive Sciences.

[76]  Hiroshi Tanaka,et al.  Some probabilistic problems in the spatially homogeneous Boltzmann equation , 1983 .

[77]  M. Deakin Catastrophe theory. , 1977, Science.

[78]  Marc Benayoun,et al.  Emergent Oscillations in Networks of Stochastic Spiking Neurons , 2011, PloS one.

[79]  R. Romo,et al.  Periodicity and Firing Rate As Candidate Neural Codes for the Frequency of Vibrotactile Stimuli , 2000, The Journal of Neuroscience.

[80]  Leon O. Chua,et al.  The Hopf bifurcation theorem and its applications to nonlinear oscillations in circuits and systems , 1979 .

[81]  H. Markram,et al.  Interneurons of the neocortical inhibitory system , 2004, Nature Reviews Neuroscience.

[82]  Olivier D. Faugeras,et al.  A Constructive Mean-Field Analysis of Multi-Population Neural Networks with Random Synaptic Weights and Stochastic Inputs , 2008, Front. Comput. Neurosci..

[83]  Stephen Coombes,et al.  Mathematical Frameworks for Oscillatory Network Dynamics in Neuroscience , 2015, The Journal of Mathematical Neuroscience.

[84]  Karl Bohlin Sur la solution de l'équation du cinquième degré , 1937 .

[85]  Alberto Tesi,et al.  Harmonic balance analysis of period-doubling bifurcations with implications for control of nonlinear dynamics , 1996, Autom..

[86]  B. Cessac Increase in Complexity in Random Neural Networks , 1995 .

[87]  J. Eccles,et al.  Inhibitory Phasing of Neuronal Discharge , 1962, Nature.

[88]  Christof Koch,et al.  Biophysics of Computation: Information Processing in Single Neurons (Computational Neuroscience Series) , 1998 .

[89]  C. Bordenave,et al.  The circular law , 2012 .

[90]  A. Treves Mean-field analysis of neuronal spike dynamics , 1993 .

[91]  Jorge L. Moiola,et al.  Double Hopf Bifurcation Analysis Using Frequency Domain Methods , 2005 .

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

[93]  Dirk Roose,et al.  Numerical bifurcation analysis of delay differential equations using DDE-BIFTOOL , 2002, TOMS.

[94]  J. Cowan,et al.  Excitatory and inhibitory interactions in localized populations of model neurons. , 1972, Biophysical journal.

[95]  Jorge L. Moiola,et al.  On period doubling bifurcations of cycles and the harmonic balance method , 2006 .

[96]  Eva Kaslik,et al.  Bifurcation analysis for a two-dimensional delayed discrete-time Hopfield neural network , 2007 .

[97]  B. Kendall Nonlinear Dynamics and Chaos , 2001 .

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

[99]  Jonathan D. Cohen,et al.  A Model of Interval Timing by Neural Integration , 2011, The Journal of Neuroscience.

[100]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[101]  S. A.,et al.  A Propagation of Chaos Result for Burgers ' Equation , 2022 .

[102]  Merav Stern,et al.  Eigenvalues of block structured asymmetric random matrices , 2014, 1411.2688.

[103]  Jeremy D. Schmahmann,et al.  A Proposal for a Coordinated Effort for the Determination of Brainwide Neuroanatomical Connectivity in Model Organisms at a Mesoscopic Scale , 2009, PLoS Comput. Biol..

[104]  Walter J. Freeman,et al.  Neurodynamics: An Exploration in Mesoscopic Brain Dynamics , 2000, Perspectives in Neural Computing.

[105]  Xiao-Jing Wang Synaptic reverberation underlying mnemonic persistent activity , 2001, Trends in Neurosciences.

[106]  Sun Yi,et al.  Solution of a system of linear delay differential equations using the matrix Lambert function , 2006, 2006 American Control Conference.

[107]  Pei Yu,et al.  Double Hopf Bifurcations and Chaos of a Nonlinear Vibration System , 1999 .

[108]  Nicolas Brunel,et al.  Dynamics of Networks of Excitatory and Inhibitory Neurons in Response to Time-Dependent Inputs , 2011, Front. Comput. Neurosci..

[109]  M. Hp A class of markov processes associated with nonlinear parabolic equations. , 1966 .

[110]  Steven H. Strogatz,et al.  Nonlinear Dynamics and Chaos , 2024 .

[111]  Alexander S. Ecker,et al.  The Effect of Noise Correlations in Populations of Diversely Tuned Neurons , 2011, The Journal of Neuroscience.

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

[113]  Randall D. Beer,et al.  On the Dynamics of Small Continuous-Time Recurrent Neural Networks , 1995, Adapt. Behav..

[114]  Patrick Simen,et al.  Evidence Accumulator or Decision Threshold – Which Cortical Mechanism are We Observing? , 2012, Front. Psychology.

[115]  Steven J. Cox,et al.  Mathematics for Neuroscientists , 2010 .

[116]  Olivier Faugeras,et al.  Asymptotic Description of Neural Networks with Correlated Synaptic Weights , 2013, Entropy.

[117]  Ian Stewart,et al.  Secondary bifurcations in systems with all–to–all coupling , 2003, Proceedings of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[118]  W. Freeman Mesoscopic neurodynamics: From neuron to brain , 2000, Journal of Physiology-Paris.

[119]  W. Freeman Analog simulation of prepyriform cortex in the cat , 1968 .