Neocortical layer 4 as a pluripotent function linearizer.

A highly effective kernel-based strategy used in machine learning is to transform the input space into a new "feature" space where nonlinear problems become linear and more readily solvable with efficient linear techniques. We propose that a similar "problem-linearization" strategy is used by the neocortical input layer 4 to reduce the difficulty of learning nonlinear relations between the afferent inputs to a cortical column and its to-be-learned upper layer outputs. The key to this strategy is the presence of broadly tuned feed-forward inhibition in layer 4: it turns local layer 4 domains into functional analogs of radial basis function networks, which are known for their universal function approximation capabilities. With the use of a computational model of layer 4 with feed-forward inhibition and Hebbian afferent connections, self-organized on natural images to closely match structural and functional properties of layer 4 of the cat primary visual cortex, we show that such layer-4-like networks have a strong intrinsic tendency to perform input transforms that automatically linearize a broad repertoire of potential nonlinear functions over the afferent inputs. This capacity for pluripotent function linearization, which is highly robust to variations in network parameters, suggests that layer 4 might contribute importantly to sensory information processing as a pluripotent function linearizer, performing such a transform of afferent inputs to a cortical column that makes it possible for neurons in the upper layers of the column to learn and perform their complex functions using primarily linear operations.

[1]  Kenneth D Miller,et al.  Processing in layer 4 of the neocortical circuit: new insights from visual and somatosensory cortex , 2001, Current Opinion in Neurobiology.

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

[3]  Hillel Adesnik,et al.  Neocortical Disynaptic Inhibition Requires Somatodendritic Integration in Interneurons , 2009, The Journal of Neuroscience.

[4]  M. J. Friedlander,et al.  Plasticity between Neuronal Pairs in Layer 4 of Visual Cortex Varies with Synapse State , 2009, The Journal of Neuroscience.

[5]  Wolfgang Maass,et al.  Motif distribution, dynamical properties, and computational performance of two data-based cortical microcircuit templates , 2009, Journal of Physiology-Paris.

[6]  Bernhard Schölkopf,et al.  Learning with kernels , 2001 .

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

[8]  T. Poggio A theory of how the brain might work. , 1990, Cold Spring Harbor symposia on quantitative biology.

[9]  V. Mountcastle,et al.  An organizing principle for cerebral function : the unit module and the distributed system , 1978 .

[10]  Jose-Manuel Alonso,et al.  Functionally distinct inhibitory neurons at the first stage of visual cortical processing , 2003, Nature Neuroscience.

[11]  S. Sherman,et al.  Glutamatergic inhibition in sensory neocortex. , 2009, Cerebral cortex.

[12]  M. Colonnier,et al.  The number of neurons in the different laminae of the binocular and monocular regions of area 17 in the cat , 1983, The Journal of comparative neurology.

[13]  Nello Cristianini,et al.  Kernel Methods for Pattern Analysis , 2003, ICTAI.

[14]  John R Huguenard,et al.  Barrel Cortex Microcircuits: Thalamocortical Feedforward Inhibition in Spiny Stellate Cells Is Mediated by a Small Number of Fast-Spiking Interneurons , 2006, The Journal of Neuroscience.

[15]  Henry Markram,et al.  Fading memory and kernel properties of generic cortical microcircuit models , 2004, Journal of Physiology-Paris.

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

[17]  Harvey A Swadlow,et al.  Thalamocortical control of feed-forward inhibition in awake somatosensory 'barrel' cortex. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[18]  J. C. Anderson,et al.  Map of the synapses formed with the dendrites of spiny stellate neurons of cat visual cortex , 1994, The Journal of comparative neurology.

[19]  Harvey A Swadlow,et al.  Thalamocortical specificity and the synthesis of sensory cortical receptive fields. , 2005, Journal of neurophysiology.

[20]  Randy M Bruno,et al.  Feedforward Mechanisms of Excitatory and Inhibitory Cortical Receptive Fields , 2002, The Journal of Neuroscience.

[21]  Kenji Okajima,et al.  An Infomax-based learning rule that generates cells similar to visual cortical neurons , 2001, Neural Networks.

[22]  D. Ferster,et al.  Strength and Orientation Tuning of the Thalamic Input to Simple Cells Revealed by Electrically Evoked Cortical Suppression , 1998, Neuron.

[23]  Aapo Hyvärinen,et al.  Simple-Cell-Like Receptive Fields Maximize Temporal Coherence in Natural Video , 2003, Neural Computation.

[24]  J. Lübke,et al.  Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single ‘barrel’ of developing rat somatosensory cortex , 1999, The Journal of physiology.

[25]  Gustavo Deco,et al.  Decorrelated Hebbian Learning for Clustering and Function Approximation , 1995, Neural Computation.

[26]  D. Tolhurst,et al.  On the variety of spatial frequency selectivities shown by neurons in area 17 of the cat , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[27]  Alexander M Binshtok,et al.  Functionally Distinct NMDA Receptors Mediate Horizontal Connectivity within Layer 4 of Mouse Barrel Cortex , 1998, Neuron.

[28]  Court Hull,et al.  Postsynaptic Mechanisms Govern the Differential Excitation of Cortical Neurons by Thalamic Inputs , 2009, The Journal of Neuroscience.

[29]  Z. Gil,et al.  Adult thalamocortical transmission involves both NMDA and non-NMDA receptors. , 1996, Journal of neurophysiology.

[30]  M. Sur,et al.  Invariant computations in local cortical networks with balanced excitation and inhibition , 2005, Nature Neuroscience.

[31]  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.

[32]  K. Martin,et al.  Map of the synapses onto layer 4 basket cells of the primary visual cortex of the cat , 1997, The Journal of comparative neurology.

[33]  D. Ferster Spatially opponent excitation and inhibition in simple cells of the cat visual cortex , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  B. Sakmann,et al.  The Excitatory Neuronal Network of Rat Layer 4 Barrel Cortex , 2000, The Journal of Neuroscience.

[35]  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.

[36]  John Shawe-Taylor,et al.  Complexity of pattern classes and the Lipschitz property , 2007, Theor. Comput. Sci..

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

[38]  Zhaoping Li,et al.  Toward a Theory of the Striate Cortex , 1994, Neural Computation.

[39]  M. Talagrand,et al.  Probability in Banach Spaces: Isoperimetry and Processes , 1991 .

[40]  David Lowe,et al.  Radial basis function networks , 1998 .

[41]  E. Adelson,et al.  The Plenoptic Function and the Elements of Early Vision , 1991 .

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

[43]  A. Agmon,et al.  Diverse Types of Interneurons Generate Thalamus-Evoked Feedforward Inhibition in the Mouse Barrel Cortex , 2001, The Journal of Neuroscience.

[44]  D J Simons,et al.  Spatial gradients and inhibitory summation in the rat whisker barrel system. , 1996, Journal of neurophysiology.

[45]  Martin Rehn,et al.  A network that uses few active neurones to code visual input predicts the diverse shapes of cortical receptive fields , 2007, Journal of Computational Neuroscience.

[46]  Robert A. Legenstein,et al.  2007 Special Issue: Edge of chaos and prediction of computational performance for neural circuit models , 2007 .

[47]  J. Budd,et al.  Inhibitory basket cell synaptic input to layer IV simple cells in cat striate visual cortex (area 17): A quantitative analysis of connectivity , 2000, Visual Neuroscience.

[48]  L N Cooper,et al.  Statistics of lateral geniculate nucleus (LGN) activity determine the segregation of ON/OFF subfields for simple cells in visual cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[49]  B. Dreher Hypercomplex cells in the cat's striate cortex. , 1972, Investigative ophthalmology.

[50]  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.

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

[52]  Wolfgang Maass,et al.  Cerebral Cortex Advance Access published February 15, 2006 A Statistical Analysis of Information- Processing Properties of Lamina-Specific , 2022 .

[53]  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.

[54]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[55]  Colin Fyfe,et al.  Hebbian Learning and Negative Feedback Networks , 2005, Advanced Information and Knowledge Processing.

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

[57]  A. B. Bonds,et al.  Classifying simple and complex cells on the basis of response modulation , 1991, Vision Research.

[58]  K. Rockland,et al.  Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey , 1979, Brain Research.

[59]  D. Ferster Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[61]  Michael C. Crair,et al.  A critical period for long-term potentiation at thalamocortical synapses , 1995, Nature.

[62]  D J Simons,et al.  Quantitative effects of GABA and bicuculline methiodide on receptive field properties of neurons in real and simulated whisker barrels. , 1996, Journal of neurophysiology.

[63]  T Poggio,et al.  View-based models of 3D object recognition: invariance to imaging transformations. , 1995, Cerebral cortex.

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

[65]  I. Ohzawa,et al.  Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. I. General characteristics and postnatal development. , 1993, Journal of neurophysiology.

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

[67]  Trichur Raman Vidyasagar,et al.  Relationship between orientation tuning and spatial frequency in neurones of cat area 17 , 2004, Experimental Brain Research.

[68]  T. Poggio,et al.  A network that learns to recognize three-dimensional objects , 1990, Nature.

[69]  K. Miller,et al.  Is the development of orientation selectivity instructed by activity? , 1999, Journal of neurobiology.

[70]  J J Jack,et al.  Synaptic interactions between smooth and spiny neurones in layer 4 of cat visual cortex in vitro , 1998, The Journal of physiology.

[71]  A. Keller,et al.  Neonatal whisker clipping alters intracortical, but not thalamocortical projections, in rat barrel cortex , 1999, The Journal of comparative neurology.

[72]  D. H. Hubel,et al.  RECEPTIVE FIELDS, BINOCULAR AND FUNCTIONAL ARCHITECTURE IN THE CAT’S VISUAL CORTEX , 1962 .

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

[74]  J C Anderson,et al.  Synaptic output of physiologically identified spiny stellate neurons in cat visual cortex , 1994, The Journal of comparative neurology.

[75]  I. Ohzawa,et al.  Linear and nonlinear contributions to orientation tuning of simple cells in the cat's striate cortex , 1999, Visual Neuroscience.

[76]  Xiaojin Zhu,et al.  Human Rademacher Complexity , 2009, NIPS.

[77]  Terrence J. Sejnowski,et al.  Unsupervised Learning , 2018, Encyclopedia of GIS.

[78]  M. Sur,et al.  Patterning and Plasticity of the Cerebral Cortex , 2005, Science.

[79]  Jörg Lücke,et al.  Receptive Field Self-Organization in a Model of the Fine Structure in V1 Cortical Columns , 2009, Neural Computation.

[80]  Ralph Linsker,et al.  Deriving Receptive Fields Using an Optimal Encoding Criterion , 1992, NIPS.

[81]  Terrence J. Sejnowski,et al.  The “independent components” of natural scenes are edge filters , 1997, Vision Research.

[82]  T. Sejnowski,et al.  Spatial Transformations in the Parietal Cortex Using Basis Functions , 1997, Journal of Cognitive Neuroscience.

[83]  Yumiko Yoshimura,et al.  Specialized Inhibitory Synaptic Actions Between Nearby Neocortical Pyramidal Neurons , 2007, Science.

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

[85]  D. Ferster,et al.  Orientation selectivity of thalamic input to simple cells of cat visual cortex , 1996, Nature.

[86]  Yun Wang,et al.  Synaptic connections and small circuits involving excitatory and inhibitory neurons in layers 2-5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labelling in vitro. , 2002, Cerebral cortex.

[87]  Tomaso Poggio,et al.  Generalization in vision and motor control , 2004, Nature.

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

[89]  P. Földiák,et al.  Forming sparse representations by local anti-Hebbian learning , 1990, Biological Cybernetics.

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

[91]  R. Reid,et al.  Rules of Connectivity between Geniculate Cells and Simple Cells in Cat Primary Visual Cortex , 2001, The Journal of Neuroscience.

[92]  Jooyoung Park,et al.  Universal Approximation Using Radial-Basis-Function Networks , 1991, Neural Computation.

[93]  B. Connors,et al.  Two networks of electrically coupled inhibitory neurons in neocortex , 1999, Nature.

[94]  B. Sakmann,et al.  Coincidence detection and changes of synaptic efficacy in spiny stellate neurons in rat barrel cortex , 1999, Nature Neuroscience.

[95]  Peter L. Bartlett,et al.  Rademacher and Gaussian Complexities: Risk Bounds and Structural Results , 2003, J. Mach. Learn. Res..

[96]  Tomaso Poggio,et al.  Fast Readout of Object Identity from Macaque Inferior Temporal Cortex , 2005, Science.

[97]  B. Schölkopf,et al.  Does Cognitive Science Need Kernels? , 2009, Trends in Cognitive Sciences.

[98]  Alexander O. Skomorokhov Radial basis function networks in A , 2002 .

[99]  R. Freeman,et al.  Orientation selectivity in the cat's striate cortex is invariant with stimulus contrast , 2004, Experimental Brain Research.

[100]  Tomaso Poggio,et al.  Observations on Cortical Mechanisms for Object Recognition and Learning , 1993 .

[101]  David D. Cox,et al.  Untangling invariant object recognition , 2007, Trends in Cognitive Sciences.

[102]  K. Martin,et al.  Intracortical excitation of spiny neurons in layer 4 of cat striate cortex in vitro. , 1999, Cerebral cortex.

[103]  D J Simons,et al.  Thalamocortical response transformations in simulated whisker barrels , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[104]  C. Blakemore,et al.  An analysis of orientation selectivity in the cat's visual cortex , 1974, Experimental Brain Research.