Dimensional reduction of emergent spatiotemporal cortical dynamics via a maximum entropy moment closure

Modern electrophysiological recordings and optical imaging techniques have revealed a diverse spectrum of spatiotemporal neural activities underlying fundamental cognitive processing. Oscillations, traveling waves and other complex population dynamical patterns are often concomitant with sensory processing, information transfer, decision making and memory consolidation. While neural population models such as neural mass, population density and kinetic theoretical models have been used to capture a wide range of the experimentally observed dynamics, a full account of how the multi-scale dynamics emerges from the detailed biophysical properties of individual neurons and the network architecture remains elusive. Here we apply a recently developed coarse-graining framework for reduced-dimensional descriptions of neuronal networks to model visual cortical dynamics. We show that, without introducing any new parameters, how a sequence of models culminating in an augmented system of spatially-coupled ODEs can effectively model a wide range of the observed cortical dynamics, ranging from visual stimulus orientation dynamics to traveling waves induced by visual illusory stimuli. In addition to an efficient simulation method, this framework also offers an analytic approach to studying large-scale network dynamics. As such, the dimensional reduction naturally leads to mesoscopic variables that capture the interplay between neuronal population stochasticity and network architecture that we believe to underlie many emergent cortical phenomena.

[1]  Ha Hong,et al.  Performance-optimized hierarchical models predict neural responses in higher visual cortex , 2014, Proceedings of the National Academy of Sciences.

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

[3]  Andrew T. Sornborger,et al.  Improved dimensionally-reduced visual cortical network using stochastic noise modeling , 2011, Journal of Computational Neuroscience.

[4]  M. de Kamps,et al.  A simple and stable numerical solution for the population density equation. , 2003, Neural computation.

[5]  T. Wiesel,et al.  Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

[8]  Viktor K. Jirsa,et al.  Symmetry Breaking in Space-Time Hierarchies Shapes Brain Dynamics and Behavior , 2017, Neuron.

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

[10]  Andrea Galluzzi,et al.  Dimensional reduction in networks of non-Markovian spiking neurons: Equivalence of synaptic filtering and heterogeneous propagation delays , 2019, PLoS Comput. Biol..

[11]  Gustavo Deco,et al.  Optimal Information Transfer in the Cortex through Synchronization , 2010, PLoS Comput. Biol..

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

[13]  J. Alonso,et al.  Population receptive fields of ON and OFF thalamic inputs to an orientation column in visual cortex , 2011, Nature Neuroscience.

[14]  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.

[15]  R. Shapley,et al.  An egalitarian network model for the emergence of simple and complex cells in visual cortex , 2003, Proceedings of the National Academy of Sciences of the United States of America.

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

[17]  G. Edelman,et al.  Large-scale model of mammalian thalamocortical systems , 2008, Proceedings of the National Academy of Sciences.

[18]  Gregor Schöner,et al.  Temporal Asymmetry in Dark–Bright Processing Initiates Propagating Activity across Primary Visual Cortex , 2016, The Journal of Neuroscience.

[19]  Stephen M Smith,et al.  Fast transient networks in spontaneous human brain activity , 2014, eLife.

[20]  Alan Rubel,et al.  Four ethical priorities for neurotechnologies and AI , 2017, Nature.

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

[22]  D. Fitzpatrick,et al.  Orientation Selectivity and the Arrangement of Horizontal Connections in Tree Shrew Striate Cortex , 1997, The Journal of Neuroscience.

[23]  U. Eysel,et al.  Orientation-specific relationship between populations of excitatory and inhibitory lateral connections in the visual cortex of the cat. , 1997, Cerebral cortex.

[24]  Viktor K. Jirsa,et al.  A Low Dimensional Description of Globally Coupled Heterogeneous Neural Networks of Excitatory and Inhibitory Neurons , 2008, PLoS Comput. Biol..

[25]  G. Blasdel,et al.  Intrinsic connections of macaque striate cortex: afferent and efferent connections of lamina 4C , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  David McLaughlin,et al.  Coarse-Grained Reduction and Analysis of a Network Model of Cortical Response: I. Drifting Grating Stimuli , 2002, Journal of Computational Neuroscience.

[27]  James G. King,et al.  Reconstruction and Simulation of Neocortical Microcircuitry , 2015, Cell.

[28]  Maria V. Sanchez-Vives,et al.  Cellular and network mechanisms of slow oscillatory activity (<1 Hz) and wave propagations in a cortical network model. , 2003, Journal of neurophysiology.

[29]  J. Alonso,et al.  Faster Thalamocortical Processing for Dark than Light Visual Targets , 2011, The Journal of Neuroscience.

[30]  T. Wiesel,et al.  Functional architecture of cortex revealed by optical imaging of intrinsic signals , 1986, Nature.

[31]  Cheng Ly,et al.  A Principled Dimension-Reduction Method for the Population Density Approach to Modeling Networks of Neurons with Synaptic Dynamics , 2013, Neural Computation.

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

[33]  M. Mattia,et al.  Population dynamics of interacting spiking neurons. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[34]  Cheng Ly,et al.  Critical Analysis of Dimension Reduction by a Moment Closure Method in a Population Density Approach to Neural Network Modeling , 2007, Neural Computation.

[35]  J. B. Demb,et al.  Different Circuits for ON and OFF Retinal Ganglion Cells Cause Different Contrast Sensitivities , 2003, The Journal of Neuroscience.

[36]  D. Fitzpatrick,et al.  Patterns of excitation and inhibition evoked by horizontal connections in visual cortex share a common relationship to orientation columns , 1995, Neuron.

[37]  J. Alonso,et al.  PRINCIPLES UNDERLYING SENSORY MAP TOPOGRAPHY IN PRIMARY VISUAL CORTEX , 2016, Nature.

[38]  Michael P Stryker,et al.  Intrinsic ON Responses of the Retinal OFF Pathway Are Suppressed by the ON Pathway , 2006, The Journal of Neuroscience.

[39]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[40]  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.

[41]  E. Rolls,et al.  Attention, short-term memory, and action selection: A unifying theory , 2005, Progress in Neurobiology.

[42]  Karl J. Friston,et al.  Relating Macroscopic Measures of Brain Activity to Fast, Dynamic Neuronal Interactions , 2000, Neural Computation.

[43]  E. Callaway,et al.  Contributions of individual layer 2–5 spiny neurons to local circuits in macaque primary visual cortex , 1996, Visual Neuroscience.

[44]  Aaditya V. Rangan,et al.  Modeling the spatiotemporal cortical activity associated with the line-motion illusion in primary visual cortex. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[45]  O. Sporns,et al.  Key role of coupling, delay, and noise in resting brain fluctuations , 2009, Proceedings of the National Academy of Sciences.

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

[47]  D. Tranchina,et al.  Population density methods for large-scale modelling of neuronal networks with realistic synaptic kinetics: cutting the dimension down to size. , 2001, Network.

[48]  Stefano Fusi Spike-driven Synaptic Plasticity for Learning Correlated Patterns of Mean Firing Rates , 2003, Reviews in the neurosciences.

[49]  X. Wang,et al.  Synaptic Basis of Cortical Persistent Activity: the Importance of NMDA Receptors to Working Memory , 1999, The Journal of Neuroscience.

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

[51]  Xiao-Jing Wang,et al.  Erratum to: Effects of neuromodulation in a cortical network model of object working memory dominated by recurrent inhibition , 2014, Journal of Computational Neuroscience.

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

[53]  Maurizio Mattia,et al.  Collective Behavior of Networks with Linear (VLSI) Integrate-and-Fire Neurons , 1999, Neural Computation.

[54]  F. Chavane,et al.  Imaging cortical correlates of illusion in early visual cortex , 2004, Nature.

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

[56]  P. Dayan,et al.  Decision theory, reinforcement learning, and the brain , 2008, Cognitive, affective & behavioral neuroscience.

[57]  E. Haskell,et al.  Population density methods for large-scale modelling of neuronal networks with realistic synaptic kinetics: cutting the dimension down to size , 2001 .

[58]  Aaditya V. Rangan,et al.  Architectural and synaptic mechanisms underlying coherent spontaneous activity in V1. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[59]  Aaditya V. Rangan,et al.  Kinetic theory for neuronal networks with fast and slow excitatory conductances driven by the same spike train. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[60]  R. Shapley,et al.  A neuronal network model of macaque primary visual cortex (V1): orientation selectivity and dynamics in the input layer 4Calpha. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[61]  Tobias C. Potjans,et al.  The Cell-Type Specific Cortical Microcircuit: Relating Structure and Activity in a Full-Scale Spiking Network Model , 2012, Cerebral cortex.

[62]  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..

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

[64]  M. Kringelbach,et al.  Metastability and Coherence: Extending the Communication through Coherence Hypothesis Using A Whole-Brain Computational Perspective , 2016, Trends in Neurosciences.

[65]  Wulfram Gerstner,et al.  Population Dynamics of Spiking Neurons: Fast Transients, Asynchronous States, and Locking , 2000, Neural Computation.

[66]  Chun-I Yeh,et al.  On and off domains of geniculate afferents in cat primary visual cortex , 2008, Nature Neuroscience.

[67]  Louis Tao,et al.  A coarse-graining framework for spiking neuronal networks: from strongly-coupled conductance-based integrate-and-fire neurons to augmented systems of ODEs , 2019, Journal of Computational Neuroscience.

[68]  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.

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

[70]  A. Grinvald,et al.  Linking spontaneous activity of single cortical neurons and the underlying functional architecture. , 1999, Science.

[71]  Michael Shelley,et al.  How Simple Cells Are Made in a Nonlinear Network Model of the Visual Cortex , 2001, The Journal of Neuroscience.

[72]  Xiao-Jing Wang,et al.  A Recurrent Network Mechanism of Time Integration in Perceptual Decisions , 2006, The Journal of Neuroscience.

[73]  Misha Tsodyks,et al.  From , 2020, Definitions.

[74]  W. Wildman,et al.  Theoretical Neuroscience , 2014 .