A coarse-graining framework for spiking neuronal networks: from strongly-coupled conductance-based integrate-and-fire neurons to augmented systems of ODEs

Homogeneously structured, fluctuation-driven networks of spiking neurons can exhibit a wide variety of dynamical behaviors, ranging from homogeneity to synchrony. We extend our partitioned-ensemble average (PEA) formalism proposed in Zhang et al. (Journal of Computational Neuroscience, 37(1), 81–104, 2014a) to systematically coarse grain the heterogeneous dynamics of strongly coupled, conductance-based integrate-and-fire neuronal networks. The population dynamics models derived here successfully capture the so-called multiple-firing events (MFEs), which emerge naturally in fluctuation-driven networks of strongly coupled neurons. Although these MFEs likely play a crucial role in the generation of the neuronal avalanches observed in vitro and in vivo, the mechanisms underlying these MFEs cannot easily be understood using standard population dynamic models. Using our PEA formalism, we systematically generate a sequence of model reductions, going from Master equations, to Fokker-Planck equations, and finally, to an augmented system of ordinary differential equations. Furthermore, we show that these reductions can faithfully describe the heterogeneous dynamic regimes underlying the generation of MFEs in strongly coupled conductance-based integrate-and-fire neuronal networks.

[1]  T. Sejnowski,et al.  Network Oscillations: Emerging Computational Principles , 2006, The Journal of Neuroscience.

[2]  Nicolas Brunel,et al.  Dynamics of the Firing Probability of Noisy Integrate-and-Fire Neurons , 2002, Neural Computation.

[3]  Woodrow L. Shew,et al.  Information Capacity and Transmission Are Maximized in Balanced Cortical Networks with Neuronal Avalanches , 2010, The Journal of Neuroscience.

[4]  Ohira,et al.  Master-equation approach to stochastic neurodynamics. , 1993, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[5]  A. Destexhe,et al.  The high-conductance state of neocortical neurons in vivo , 2003, Nature Reviews Neuroscience.

[6]  Charles J. Wilson,et al.  Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo. , 1997, Journal of neurophysiology.

[7]  Yi Zeng,et al.  Synchrony and Periodicity in Excitable Neural Networks with Multiple Subpopulations , 2014, SIAM J. Appl. Dyn. Syst..

[8]  Lawrence Sirovich,et al.  Dynamics of Neuronal Populations: The Equilibrium Solution , 2000, SIAM J. Appl. Math..

[9]  D. Hansel,et al.  On the Distribution of Firing Rates in Networks of Cortical Neurons , 2011, The Journal of Neuroscience.

[10]  David Ferster,et al.  Membrane Potential Synchrony in Primary Visual Cortex during Sensory Stimulation , 2010, Neuron.

[11]  D. Plenz,et al.  Spontaneous cortical activity in awake monkeys composed of neuronal avalanches , 2009, Proceedings of the National Academy of Sciences.

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

[13]  Theoden I. Netoff,et al.  Synchronization from Second Order Network Connectivity Statistics , 2011, Front. Comput. Neurosci..

[14]  Melanie R. Bernard,et al.  Abbreviated Title: , 2017 .

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

[16]  Porter E. Sargent,et al.  The giant ganglion cells in the spinal cord of ctenolabrus adspersus (Walb.‐Goode) , 1898 .

[17]  L Sirovich,et al.  A population approach to cortical dynamics with an application to orientation tuning , 2000, Network.

[18]  Tim P Vogels,et al.  Signal Propagation and Logic Gating in Networks of Integrate-and-Fire Neurons , 2005, The Journal of Neuroscience.

[19]  Donald B. Percival,et al.  Spectral Analysis for Physical Applications , 1993 .

[20]  Marcus Kaiser,et al.  Temporal Interactions between Cortical Rhythms , 2008, Front. Neurosci..

[21]  Stefan Rotter,et al.  Multiplicatively interacting point processes and applications to neural modeling , 2009, Journal of Computational Neuroscience.

[22]  H. Storch,et al.  Statistical Analysis in Climate Research , 2000 .

[23]  A. Destexhe,et al.  Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. , 1999, Journal of neurophysiology.

[24]  David McLaughlin,et al.  States of High Conductance in a Large-Scale Model of the Visual Cortex , 2002, Journal of Computational Neuroscience.

[25]  David Hansel,et al.  Synchronous Chaos and Broad Band Gamma Rhythm in a Minimal Multi-Layer Model of Primary Visual Cortex , 2011, PLoS Comput. Biol..

[26]  Nicholas G. Hatsopoulos,et al.  Avalanche analysis from multi-electrode ensemble recordings in cat, monkey and human cerebral cortex during wakefulness and sleep , 2012 .

[27]  Moritz Helias,et al.  Instantaneous Non-Linear Processing by Pulse-Coupled Threshold Units , 2010, PLoS Comput. Biol..

[28]  Andreas V. M. Herz,et al.  Earthquake cycles and neural reverberations , 1995 .

[29]  M. Shelley,et al.  An effective kinetic representation of fluctuation-driven neuronal networks with application to simple and complex cells in visual cortex. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[30]  Alain Destexhe,et al.  A Master Equation Formalism for Macroscopic Modeling of Asynchronous Irregular Activity States , 2009, Neural Computation.

[31]  Jiwei Zhang,et al.  Distribution of correlated spiking events in a population-based approach for Integrate-and-Fire networks , 2014, Journal of Computational Neuroscience.

[32]  Aaditya V. Rangan,et al.  Dynamics of spiking neurons: between homogeneity and synchrony , 2012, Journal of Computational Neuroscience.

[33]  Jiwei Zhang,et al.  A reduction for spiking integrate-and-fire network dynamics ranging from homogeneity to synchrony , 2014, Journal of Computational Neuroscience.

[34]  Andreas Klaus,et al.  Multi-electrode Array Recordings of Neuronal Avalanches in Organotypic Cultures , 2011, Journal of visualized experiments : JoVE.

[35]  K. Grill-Spector,et al.  The functional architecture of the ventral temporal cortex and its role in categorization , 2014, Nature Reviews Neuroscience.

[36]  B. Knight The Relationship between the Firing Rate of a Single Neuron and the Level of Activity in a Population of Neurons , 1972, The Journal of general physiology.

[37]  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).

[38]  P. Fries Neuronal gamma-band synchronization as a fundamental process in cortical computation. , 2009, Annual review of neuroscience.

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

[40]  Jiwei Zhang,et al.  A coarse-grained framework for spiking neuronal networks: between homogeneity and synchrony , 2014, Journal of Computational Neuroscience.

[41]  L. Paninski,et al.  Information about movement direction obtained from synchronous activity of motor cortical neurons. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[42]  J. Csicsvari,et al.  Ensemble Patterns of Hippocampal CA3-CA1 Neurons during Sharp Wave–Associated Population Events , 2000, Neuron.

[43]  Jiwei Zhang,et al.  Cusps enable line attractors for neural computation. , 2017, Physical review. E.

[44]  Andrew M. Clark,et al.  Stimulus onset quenches neural variability: a widespread cortical phenomenon , 2010, Nature Neuroscience.

[45]  K. Harris,et al.  Laminar Structure of Spontaneous and Sensory-Evoked Population Activity in Auditory Cortex , 2009, Neuron.

[46]  Louis Tao,et al.  KINETIC THEORY FOR NEURONAL NETWORK DYNAMICS , 2006 .

[47]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

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

[49]  David Cai,et al.  Cascade-induced synchrony in stochastically driven neuronal networks. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[50]  J. Touboul Propagation of chaos in neural fields , 2011, 1108.2414.

[51]  David Cai,et al.  Maximum-entropy closures for kinetic theories of neuronal network dynamics. , 2006, Physical review letters.

[52]  S. Bornholdt,et al.  Self-organized critical neural networks. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[53]  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.

[54]  Duane Q. Nykamp,et al.  A Population Density Approach That Facilitates Large-Scale Modeling of Neural Networks: Analysis and an Application to Orientation Tuning , 2004, Journal of Computational Neuroscience.

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

[56]  Bruce W. Knight,et al.  Dynamics of Encoding in a Population of Neurons , 1972, The Journal of general physiology.

[57]  Stefan Rotter,et al.  Correlations and Population Dynamics in Cortical Networks , 2008, Neural Computation.

[58]  V. Torre,et al.  On the Dynamics of the Spontaneous Activity in Neuronal Networks , 2007, PloS one.

[59]  Alain Destexhe,et al.  Modeling mesoscopic cortical dynamics using a mean-field model of conductance-based networks of adaptive exponential integrate-and-fire neurons , 2017, bioRxiv.

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

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

[62]  Gerhard Werner,et al.  Metastability, criticality and phase transitions in brain and its models , 2007, Biosyst..

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

[64]  Tang,et al.  Self-Organized Criticality: An Explanation of 1/f Noise , 2011 .

[65]  Aaditya V Rangan Diagrammatic expansion of pulse-coupled network dynamics. , 2009, Physical review letters.

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

[67]  A. Grinvald,et al.  Spontaneously emerging cortical representations of visual attributes , 2003, Nature.

[68]  Zach D. Haga,et al.  Avalanche Analysis from Multielectrode Ensemble Recordings in Cat, Monkey, and Human Cerebral Cortex during Wakefulness and Sleep , 2012, Front. Physio..

[69]  Aaditya V. Rangan,et al.  Emergent dynamics in a model of visual cortex , 2013, Journal of Computational Neuroscience.

[70]  M. A. Smith,et al.  Stimulus Dependence of Neuronal Correlation in Primary Visual Cortex of the Macaque , 2005, The Journal of Neuroscience.

[71]  R. Traub,et al.  Fast Oscillations in Cortical Circuits , 1999 .

[72]  M. J. Richardson,et al.  Effects of synaptic conductance on the voltage distribution and firing rate of spiking neurons. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[73]  M. Carandini,et al.  Stimulus dependence of two-state fluctuations of membrane potential in cat visual cortex , 2000, Nature Neuroscience.

[74]  Shan Yu,et al.  Higher-Order Interactions Characterized in Cortical Activity , 2011, The Journal of Neuroscience.

[75]  W. Singer,et al.  Neuronal avalanches in spontaneous activity in vivo. , 2010, Journal of neurophysiology.

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

[77]  G. Buzsáki,et al.  Correlated Bursts of Activity in the Neonatal Hippocampus in Vivo , 2002, Science.

[78]  Jonathan D. Touboul,et al.  On the Dynamics of Random Neuronal Networks , 2014, Journal of Statistical Physics.

[79]  K. Linkenkaer-Hansen,et al.  Critical-State Dynamics of Avalanches and Oscillations Jointly Emerge from Balanced Excitation/Inhibition in Neuronal Networks , 2012, The Journal of Neuroscience.

[80]  G. Buzsáki,et al.  Mechanisms of gamma oscillations. , 2012, Annual review of neuroscience.