A comprehensive data-driven model of cat primary visual cortex

Knowledge integration based on the relationship between structure and function of the neural substrate is one of the main targets of neuroinformatics and data-driven computational modeling. However, the multiplicity of data sources, the diversity of benchmarks, the mixing of observables of different natures, and the necessity of a long-term, systematic approach make such a task challenging. Here we present a first snapshot of a long-term integrative modeling program designed to address this issue: a comprehensive spiking model of cat primary visual cortex satisfying an unprecedented range of anatomical, statistical and functional constraints under a wide range of visual input statistics. In the presence of physiological levels of tonic stochastic bombardment by spontaneous thalamic activity, the modeled cortical reverberations self-generate a sparse asynchronous ongoing activity that quantitatively matches a range of experimentally measured statistics. When integrating feed-forward drive elicited by a high diversity of visual contexts, the simulated network produces a realistic, quantitatively accurate interplay between visually evoked excitatory and inhibitory conductances; contrast-invariant orientation-tuning width; center surround interactions; and stimulus-dependent changes in the precision of the neural code. This integrative model offers numerous insights into how the studied properties interact, contributing to a better understanding of visual cortical dynamics. It provides a basis for future development towards a comprehensive model of low-level perception. Significance statement Computational modeling can integrate fragments of understanding generated by experimental neuroscience. However, most previous models considered only a few features of neural computation at a time, leading to either poorly constrained models with many parameters, or lack of expressiveness in over-simplified models. A solution is to commit to detailed models, but constrain them with a broad range of anatomical and functional data. This requires a long-term systematic approach. Here we present a first snapshot of such an integrative program: a large-scale spiking model of V1, that is constrained by an unprecedented range of anatomical and functional features. Together with the associated modeling infrastructure, this study lays the groundwork for a broad integrative modeling program seeking an in-depth understanding of vision.

[1]  Andrew P. Davison,et al.  Integrated workflows for spiking neuronal network simulations , 2013, Front. Neuroinform..

[2]  G. Buzsáki,et al.  The log-dynamic brain: how skewed distributions affect network operations , 2014, Nature Reviews Neuroscience.

[3]  Ad Aertsen,et al.  Push-Pull Receptive Field Organization and Synaptic Depression: Mechanisms for Reliably Encoding Naturalistic Stimuli in V1 , 2016, Front. Neural Circuits.

[4]  J. P. Jones,et al.  The two-dimensional spatial structure of simple receptive fields in cat striate cortex. , 1987, Journal of neurophysiology.

[5]  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.

[6]  Alex M. Thomson,et al.  Neocortical Layer 6, A Review , 2010, Front. Neuroanat..

[7]  J. Bullier,et al.  Reaching beyond the classical receptive field of V1 neurons: horizontal or feedback axons? , 2003, Journal of Physiology-Paris.

[8]  Elena A Allen,et al.  Dynamic Spatial Processing Originates in Early Visual Pathways , 2006, The Journal of Neuroscience.

[9]  Wulfram Gerstner,et al.  Synaptic Plasticity in Neural Networks Needs Homeostasis with a Fast Rate Detector , 2013, PLoS Comput. Biol..

[10]  J. Movshon,et al.  Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons. , 2002, Journal of neurophysiology.

[11]  Y. Frégnac,et al.  In vitro and in vivo measures of evoked excitatory and inhibitory conductance dynamics in sensory cortices , 2008, Journal of Neuroscience Methods.

[12]  G. Ascoli,et al.  NeuroMorpho.Org: A Central Resource for Neuronal Morphologies , 2007, The Journal of Neuroscience.

[13]  E. Todorov,et al.  A local circuit approach to understanding integration of long-range inputs in primary visual cortex. , 1998, Cerebral cortex.

[14]  L. Palmer,et al.  The retinotopic organization of area 17 (striate cortex) in the cat , 1978, The Journal of comparative neurology.

[15]  Christopher J. Rozell,et al.  Visual Nonclassical Receptive Field Effects Emerge from Sparse Coding in a Dynamical System , 2013, PLoS Comput. Biol..

[16]  F. Rieke,et al.  Mechanisms Regulating Variability of the Single Photon Responses of Mammalian Rod Photoreceptors , 2002, Neuron.

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

[18]  T. Naito,et al.  Surround suppression sharpens orientation tuning in the cat primary visual cortex , 2009, The European journal of neuroscience.

[19]  Jessica A. Cardin,et al.  Stimulus Feature Selectivity in Excitatory and Inhibitory Neurons in Primary Visual Cortex , 2007, The Journal of Neuroscience.

[20]  Nicolas Brunel,et al.  Dynamics of networks of randomly connected excitatory and inhibitory spiking neurons , 2000, Journal of Physiology-Paris.

[21]  Nikola T. Markov,et al.  Anatomy of hierarchy: Feedforward and feedback pathways in macaque visual cortex , 2013, The Journal of comparative neurology.

[22]  G. Edelman,et al.  Neural dynamics in a model of the thalamocortical system. II. The role of neural synchrony tested through perturbations of spike timing. , 1997, Cerebral cortex.

[23]  M. Cynader,et al.  Quantitative distribution of GABA-immunopositive and -immunonegative neurons and synapses in the monkey striate cortex (area 17). , 1992, Cerebral cortex.

[24]  H. Markram,et al.  Differential signaling via the same axon of neocortical pyramidal neurons. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Albert K. Lee,et al.  Whole-Cell Recordings in Freely Moving Rats , 2006, Neuron.

[26]  R. Freeman,et al.  Oscillatory discharge in the visual system: does it have a functional role? , 1992, Journal of neurophysiology.

[27]  James Kozloski,et al.  Self-referential forces are sufficient to explain different dendritic morphologies , 2013, Front. Neuroinform..

[28]  M. Colonnier,et al.  Number of neurons in individual laminae of areas 3B, 4γ, and 6aα of the cat cerebral cortex: A comparison with major visual areas , 1989 .

[29]  Yumiko Yoshimura,et al.  Suppressive effects of receptive field surround on neuronal activity in the cat primary visual cortex , 2002, Neuroscience Research.

[30]  S. Grossberg,et al.  A neural model of how horizontal and interlaminar connections of visual cortex develop into adult circuits that carry out perceptual grouping and learning. , 2010, Cerebral cortex.

[31]  Edward M. Callaway,et al.  Laminar Specificity of Functional Input to Distinct Types of Inhibitory Cortical Neurons , 2009, The Journal of Neuroscience.

[32]  H. Swadlow Fast-spike interneurons and feedforward inhibition in awake sensory neocortex. , 2003, Cerebral cortex.

[33]  Ning Qian,et al.  Comparison among some models of orientation selectivity. , 2006, Journal of neurophysiology.

[34]  Allan R. Jones,et al.  Large-Scale Cellular-Resolution Gene Profiling in Human Neocortex Reveals Species-Specific Molecular Signatures , 2012, Cell.

[35]  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.

[36]  David J. Field,et al.  How Close Are We to Understanding V1? , 2005, Neural Computation.

[37]  Paul Sajda,et al.  Circuitry and the classification of simple and complex cells in V1. , 2006, Journal of neurophysiology.

[38]  Andreas Burkhalter,et al.  Microcircuitry of forward and feedback connections within rat visual cortex , 1996, The Journal of comparative neurology.

[39]  P. Sajda,et al.  Extraclassical receptive field phenomena and short-range connectivity in V1. , 2005, Cerebral cortex.

[40]  Giulio Tononi,et al.  Modeling sleep and wakefulness in the thalamocortical system. , 2005, Journal of neurophysiology.

[41]  Nicholas J. Priebe,et al.  The Emergence of Contrast-Invariant Orientation Tuning in Simple Cells of Cat Visual Cortex , 2007, Neuron.

[42]  Massimo Scanziani,et al.  A collicular visual cortex: Neocortical space for an ancient midbrain visual structure , 2019, Science.

[43]  J. Alonso,et al.  COLUMNAR ORGANIZATION OF SPATIAL PHASE IN VISUAL CORTEX , 2014, Nature Neuroscience.

[44]  Maria V. Sanchez-Vives,et al.  Electrophysiological classes of cat primary visual cortical neurons in vivo as revealed by quantitative analyses. , 2003, Journal of neurophysiology.

[45]  Kevan A. C. Martin,et al.  Fast Recruitment of Recurrent Inhibition in the Cat Visual Cortex , 2012, PloS one.

[46]  S. Nelson,et al.  An emergent model of orientation selectivity in cat visual cortical simple cells , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  V. Bringuier,et al.  Synaptic origin and stimulus dependency of neuronal oscillatory activity in the primary visual cortex of the cat. , 1997, The Journal of physiology.

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

[49]  D. Ferster,et al.  Feedforward Origins of Response Variability Underlying Contrast Invariant Orientation Tuning in Cat Visual Cortex , 2012, Neuron.

[50]  Wulfram Gerstner,et al.  Firing patterns in the adaptive exponential integrate-and-fire model , 2008, Biological Cybernetics.

[51]  George L. Gerstein,et al.  Feature-linked synchronization of thalamic relay cell firing induced by feedback from the visual cortex , 1994, Nature.

[52]  Brian R. Lee,et al.  Visual physiology of the layer 4 cortical circuit in silico , 2018, bioRxiv.

[53]  Jonathan W Peirce,et al.  Two expressions of “surround suppression” in V1 that arise independent of cortical mechanisms of suppression , 2007, Visual Neuroscience.

[54]  D. Ringach Mapping receptive fields in primary visual cortex , 2004, The Journal of physiology.

[55]  Nuno Maçarico da Costa,et al.  How Thalamus Connects to Spiny Stellate Cells in the Cat's Visual Cortex , 2011, The Journal of Neuroscience.

[56]  J. Budd,et al.  Local lateral connectivity of inhibitory clutch cells in layer 4 of cat visual cortex (area 17) , 2001, Experimental Brain Research.

[57]  Yves Frégnac,et al.  Hidden Complexity of Synaptic Receptive Fields in Cat V1 , 2014, The Journal of Neuroscience.

[58]  T. Hromádka,et al.  Sparse Representation of Sounds in the Unanesthetized Auditory Cortex , 2008, PLoS biology.

[59]  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.

[60]  Marc-Oliver Gewaltig,et al.  NEST (NEural Simulation Tool) , 2007, Scholarpedia.

[61]  Trichur Raman Vidyasagar,et al.  Receptive field analysis and orientation selectivity of postsynaptic potentials of simple cells in cat visual cortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[62]  R. Yuste,et al.  Attractor dynamics of network UP states in the neocortex , 2003, Nature.

[63]  Jinde Cao,et al.  Introduction to Computational Neuroscience , 2016 .

[64]  Louis Tao,et al.  Orientation selectivity in visual cortex by fluctuation-controlled criticality , 2006, Proceedings of the National Academy of Sciences.

[65]  Lai-Sang Young,et al.  Orientation Selectivity from Very Sparse LGN Inputs in a Comprehensive Model of Macaque V1 Cortex , 2016, The Journal of Neuroscience.

[66]  Rainer Goebel,et al.  Combined distributed source and single-trial EEG–fMRI modeling: Application to effortful decision making processes , 2009, NeuroImage.

[67]  Nicole C. Rust,et al.  In praise of artifice , 2005, Nature Neuroscience.

[68]  A. Sillito,et al.  Surround suppression in primate V1. , 2001, Journal of neurophysiology.

[69]  Yves Frégnac,et al.  Reading Out the Synaptic Echoes of Low-Level Perception in V1 , 2012, ECCV Workshops.

[70]  Wulfram Gerstner,et al.  Adaptive exponential integrate-and-fire model as an effective description of neuronal activity. , 2005, Journal of neurophysiology.

[71]  A. Yuille,et al.  Opinion TRENDS in Cognitive Sciences Vol.10 No.7 July 2006 Special Issue: Probabilistic models of cognition Vision as Bayesian inference: analysis by synthesis? , 2022 .

[72]  M. Colonnier,et al.  A laminar analysis of the number of round‐asymmetrical and flat‐symmetrical synapses on spines, dendritic trunks, and cell bodies in area 17 of the cat , 1985, The Journal of comparative neurology.

[73]  Risto Miikkulainen,et al.  Computational Maps in the Visual Cortex , 2005 .

[74]  Dario L. Ringach,et al.  Computational Modeling of Orientation Tuning Dynamics in Monkey Primary Visual Cortex , 2000, Journal of Computational Neuroscience.

[75]  Bogdan Dreher,et al.  ‘Simplification’ of responses of complex cells in cat striate cortex: suppressive surrounds and ‘feedback’ inactivation , 2006, The Journal of physiology.

[76]  BsnNr C. Srorn,et al.  CLASSIFYING SIMPLE AND COMPLEX CELLS ON THE BASIS OF RESPONSE MODULATION , 2002 .

[77]  J. Budd Extrastriate feedback to primary visual cortex in primates: a quantitative analysis of connectivity , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[78]  S. Sherman,et al.  Receptive-field characteristics of neurons in cat striate cortex: Changes with visual field eccentricity. , 1976, Journal of neurophysiology.

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

[80]  C. Blakemore,et al.  Characteristics of surround inhibition in cat area 17 , 1997, Experimental Brain Research.

[81]  D. Hansel,et al.  How Spike Generation Mechanisms Determine the Neuronal Response to Fluctuating Inputs , 2003, The Journal of Neuroscience.

[82]  A. Thomson,et al.  Interlaminar connections in the neocortex. , 2003, Cerebral cortex.

[83]  Sonja Grün,et al.  The Scientific Case for Brain Simulations , 2019, Neuron.

[84]  Alain Destexhe,et al.  Self-sustained Asynchronous Irregular States and Up–down States in Thalamic, Cortical and Thalamocortical Networks of Nonlinear Integrate-and-fire Neurons , 2022 .

[85]  A. Sillito,et al.  Functional alignment of feedback effects from visual cortex to thalamus , 2006, Nature Neuroscience.

[86]  Idan Segev,et al.  A Biologically Realistic Model of Contrast Invariant Orientation Tuning by Thalamocortical Synaptic Depression , 2007, The Journal of Neuroscience.

[87]  D. Ferster,et al.  Membrane Potential and Conductance Changes Underlying Length Tuning of Cells in Cat Primary Visual Cortex , 2001, The Journal of Neuroscience.

[88]  J. Movshon,et al.  Spatial and temporal contrast sensitivity of neurones in areas 17 and 18 of the cat's visual cortex. , 1978, The Journal of physiology.

[89]  A. Peters,et al.  The Concept of Cat Primary Visual Cortex , 2002 .

[90]  Eike Kiltz,et al.  Tightly-Secure Signatures from Chameleon Hash Functions , 2015, Public Key Cryptography.

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

[92]  L. Abbott,et al.  Synaptic Depression and Cortical Gain Control , 1997, Science.

[93]  Andrew P. Davison,et al.  Arkheia: Data Management and Communication for Open Computational Neuroscience , 2018, Front. Neuroinform..

[94]  O. Creutzfeldt,et al.  An intracellular analysis of visual cortical neurones to moving stimuli: Responses in a co-operative neuronal network , 2004, Experimental Brain Research.

[95]  Brett J. Graham,et al.  Anatomy and function of an excitatory network in the visual cortex , 2016, Nature.

[96]  A. Burkhalter,et al.  Organization of long-range inhibitory connections with rat visual cortex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[97]  D. McCormick,et al.  Turning on and off recurrent balanced cortical activity , 2003, Nature.

[98]  E. P. Gardner,et al.  Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex , 2008, Nature Reviews Neuroscience.

[99]  Judith A Hirsch,et al.  Laminar processing in the visual cortical column , 2006, Current Opinion in Neurobiology.

[100]  C. von der Malsburg,et al.  Establishment of a Scaffold for Orientation Maps in Primary Visual Cortex of Higher Mammals , 2008, The Journal of Neuroscience.

[101]  Alex S. Ferecskó,et al.  Local Potential Connectivity in Cat Primary Visual Cortex , 2008 .

[102]  D. Ferster,et al.  Neural mechanisms of orientation selectivity in the visual cortex. , 2000, Annual review of neuroscience.

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

[104]  Qasim Zaidi,et al.  Neuronal nonlinearity explains greater visual spatial resolution for darks than lights , 2014, Proceedings of the National Academy of Sciences.

[105]  Michael W. Levine,et al.  The distribution of the intervals between neural impulses in the maintained discharges of retinal ganglion cells , 1991, Biological Cybernetics.

[106]  P. Mermelstein,et al.  Opposite Effects of mGluR1a and mGluR5 Activation on Nucleus Accumbens Medium Spiny Neuron Dendritic Spine Density , 2016, PloS one.

[107]  M. Carandini,et al.  Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. , 2000, Journal of neurophysiology.

[108]  K. Martin,et al.  Excitatory synaptic inputs to spiny stellate cells in cat visual cortex , 1996, Nature.

[109]  Yves Frégnac,et al.  Animation of natural scene by virtual eye-movements evokes high precision and low noise in V1 neurons , 2013, Front. Neural Circuits.

[110]  G. Edelman,et al.  Neural dynamics in a model of the thalamocortical system. I. Layers, loops and the emergence of fast synchronous rhythms. , 1997, Cerebral cortex.

[111]  K. Miller,et al.  Different Roles for Simple-Cell and Complex-Cell Inhibition in V1 , 2003, The Journal of Neuroscience.

[112]  T. Bonhoeffer,et al.  Relationship Between Lateral Inhibitory Connections and the Topography of the Orientation Map in Cat Visual Cortex , 1994, The European journal of neuroscience.

[113]  David J. Field,et al.  Emergence of simple-cell receptive field properties by learning a sparse code for natural images , 1996, Nature.

[114]  M. Carandini,et al.  The Suppressive Field of Neurons in Lateral Geniculate Nucleus , 2005, The Journal of Neuroscience.

[115]  J. B. Levitt,et al.  Circuits for Local and Global Signal Integration in Primary Visual Cortex , 2002, The Journal of Neuroscience.

[116]  S. Cruikshank,et al.  Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex , 2007, Nature Neuroscience.

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

[118]  Maria V. Sanchez-Vives,et al.  Lack of orientation and direction selectivity in a subgroup of fast-spiking inhibitory interneurons: cellular and synaptic mechanisms and comparison with other electrophysiological cell types. , 2008, Cerebral cortex.

[119]  Felix Scholkmann,et al.  The Physical Mechanism for Retinal Discrete Dark Noise: Thermal Activation or Cellular Ultraweak Photon Emission? , 2016, PloS one.

[120]  Evan S. Schaffer,et al.  Inhibitory Stabilization of the Cortical Network Underlies Visual Surround Suppression , 2009, Neuron.

[121]  Carlos Cepeda,et al.  Dissecting the Contribution of Individual Receptor Subunits to the Enhancement of N-methyl-d-Aspartate Currents by Dopamine D1 Receptor Activation in Striatum , 2011, Front. Syst. Neurosci..

[122]  Marc Timme,et al.  Synaptic Scaling in Combination with Many Generic Plasticity Mechanisms Stabilizes Circuit Connectivity , 2011, Front. Comput. Neurosci..

[123]  Yves Frégnac,et al.  Cortical Correlates of Low-Level Perception: From Neural Circuits to Percepts , 2015, Neuron.

[124]  M. Carandini,et al.  Predictions of a recurrent model of orientation selectivity , 1997, Vision Research.

[125]  Alex S. Ferecskó,et al.  Model‐based analysis of excitatory lateral connections in the visual cortex , 2006, The Journal of comparative neurology.

[126]  Daniel B. Rubin,et al.  The Stabilized Supralinear Network: A Unifying Circuit Motif Underlying Multi-Input Integration in Sensory Cortex , 2015, Neuron.

[127]  R. Reid,et al.  Receptive field structure varies with layer in the primary visual cortex , 2005, Nature Neuroscience.

[128]  Moritz Helmstaedter,et al.  Synaptic Conductance Estimates of the Connection Between Local Inhibitor Interneurons and Pyramidal Neurons in Layer 2/3 of a Cortical Column , 2015, Cerebral cortex.

[129]  A. Sillito,et al.  A re-evaluation of the mechanisms underlying simple cell orientation selectivity , 1980, Brain Research.

[130]  Nicholas J. Priebe,et al.  The contribution of spike threshold to the dichotomy of cortical simple and complex cells , 2004, Nature Neuroscience.

[131]  F. Chavane,et al.  Lateral Spread of Orientation Selectivity in V1 is Controlled by Intracortical Cooperativity , 2011, Front. Syst. Neurosci..

[132]  David S. Greenberg,et al.  Rats maintain an overhead binocular field at the expense of constant fusion , 2013, Nature.

[133]  James A. Bednar,et al.  Development of Maps of Simple and Complex Cells in the Primary Visual Cortex , 2011, Front. Comput. Neurosci..

[134]  Sean L. Hill,et al.  Sleep homeostasis and cortical synchronization: I. Modeling the effects of synaptic strength on sleep slow waves. , 2007, Sleep.

[135]  K. Harris,et al.  Cortical connectivity and sensory coding , 2013, Nature.

[136]  C. Stevens,et al.  An evaluation of causes for unreliability of synaptic transmission. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[137]  A. Cavaggioni,et al.  The dark-discharge of the eye in the unrestrained cat , 2004, Pflügers Archiv.

[138]  K. Purpura,et al.  Response variability in retinal ganglion cells of primates. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[139]  B. Olshausen 20 Years of Learning About Vision: Questions Answered, Questions Unanswered, and Questions Not Yet Asked , 2013 .

[140]  M. Carandini,et al.  Summation and division by neurons in primate visual cortex. , 1994, Science.

[141]  Lyle J. Graham,et al.  Orientation and Direction Selectivity of Synaptic Inputs in Visual Cortical Neurons A Diversity of Combinations Produces Spike Tuning , 2003, Neuron.

[142]  H. Sompolinsky,et al.  Theory of orientation tuning in visual cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[143]  J Papaioannou,et al.  Maintained activity of lateral geniculate nucleus neurons as a function of background luminance. , 1972, Experimental neurology.

[144]  R. Shapley,et al.  Contrast's effect on spatial summation by macaque V1 neurons , 1999, Nature Neuroscience.

[145]  B. Dreher,et al.  Contrast dependence of center and surround integration in primary visual cortex of the cat. , 2009, Journal of vision.

[146]  P. J. Sjöström,et al.  Functional specificity of local synaptic connections in neocortical networks , 2011, Nature.

[147]  Louis Tao,et al.  Multiscale modeling of the primary visual cortex , 2009, IEEE Engineering in Medicine and Biology Magazine.

[148]  Nicholas G Hatsopoulos,et al.  High-frequency oscillations in human and monkey neocortex during the wake–sleep cycle , 2016, Proceedings of the National Academy of Sciences.

[149]  K. Miller,et al.  Opponent Inhibition A Developmental Model of Layer 4 of the Neocortical Circuit , 2002, Neuron.

[150]  Daniel K Wójcik,et al.  Effect of cortex inactivation on spontaneous activity of cells in perigeniculate and dorsal lateral geniculate nuclei , 2013, BMC Neuroscience.

[151]  Yves Frégnac,et al.  Big data and the industrialization of neuroscience: A safe roadmap for understanding the brain? , 2017, Science.

[152]  Avi Ziskind,et al.  Neurons in Cat Primary Visual Cortex cluster by degree of tuning but not by absolute spatial phase or temporal response phase , 2013 .

[153]  Nicole C. Rust,et al.  Do We Know What the Early Visual System Does? , 2005, The Journal of Neuroscience.

[154]  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.

[155]  Alex S. Ferecskó,et al.  The fractions of short- and long-range connections in the visual cortex , 2009, Proceedings of the National Academy of Sciences.

[156]  L. Schwabe,et al.  Response facilitation from the "suppressive" receptive field surround of macaque V1 neurons. , 2007, Journal of neurophysiology.

[157]  C. Koch,et al.  Recurrent excitation in neocortical circuits , 1995, Science.

[158]  P. C. Murphy,et al.  Spatial summation in lateral geniculate nucleus and visual cortex , 2000, Experimental Brain Research.

[159]  Henry J. Alitto,et al.  Influence of contrast on orientation and temporal frequency tuning in ferret primary visual cortex. , 2004, Journal of neurophysiology.

[160]  D. McCormick,et al.  Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. , 1985, Journal of neurophysiology.

[161]  R. Reid,et al.  Synaptic Integration in Striate Cortical Simple Cells , 1998, The Journal of Neuroscience.

[162]  Jane W Chan,et al.  The Cat Primary Visual Cortex , 2006 .

[163]  M. Scanziani,et al.  Inhibition of Inhibition in Visual Cortex: The Logic of Connections Between Molecularly Distinct Interneurons , 2013, Nature Neuroscience.

[164]  Yves Frégnac,et al.  Synaptic Correlates of Low-Level Perception in V1 , 2016, The Journal of Neuroscience.

[165]  Arvind Kumar,et al.  The High-Conductance State of Cortical Networks , 2008, Neural Computation.

[166]  A. Destexhe,et al.  Neuronal Noise , 2012, Springer Series in Computational Neuroscience.

[167]  Bernhard A. Kaplan,et al.  SYSTEMS NEUROSCIENCE ORIGINAL RESEARCH ARTICLE , 2011 .

[168]  R. Douglas,et al.  A Quantitative Map of the Circuit of Cat Primary Visual Cortex , 2004, The Journal of Neuroscience.

[169]  V. Bringuier,et al.  Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. , 1999, Science.

[170]  Eric Plutzer,et al.  Evolution and Creationism in America's Classrooms: A National Portrait , 2008, PLoS biology.