Adaptive learning in a compartmental model of visual cortex—how feedback enables stable category learning and refinement

The categorization of real world objects is often reflected in the similarity of their visual appearances. Such categories of objects do not necessarily form disjunct sets of objects, neither semantically nor visually. The relationship between categories can often be described in terms of a hierarchical structure. For instance, tigers and leopards build two separate mammalian categories, both of which are subcategories of the category Felidae. In the last decades, the unsupervised learning of categories of visual input stimuli has been addressed by numerous approaches in machine learning as well as in computational neuroscience. However, the question of what kind of mechanisms might be involved in the process of subcategory learning, or category refinement, remains a topic of active investigation. We propose a recurrent computational network architecture for the unsupervised learning of categorial and subcategorial visual input representations. During learning, the connection strengths of bottom-up weights from input to higher-level category representations are adapted according to the input activity distribution. In a similar manner, top-down weights learn to encode the characteristics of a specific stimulus category. Feedforward and feedback learning in combination realize an associative memory mechanism, enabling the selective top-down propagation of a category's feedback weight distribution. We suggest that the difference between the expected input encoded in the projective field of a category node and the current input pattern controls the amplification of feedforward-driven representations. Large enough differences trigger the recruitment of new representational resources and the establishment of additional (sub-) category representations. We demonstrate the temporal evolution of such learning and show how the proposed combination of an associative memory with a modulatory feedback integration successfully establishes category and subcategory representations.

[1]  A. Borst Seeing smells: imaging olfactory learning in bees , 1999, Nature Neuroscience.

[2]  Stephen Grossberg,et al.  Adaptive Resonance Theory , 2010, Encyclopedia of Machine Learning.

[3]  Henry Kennedy,et al.  The importance of being hierarchical , 2013, Current Opinion in Neurobiology.

[4]  Michael W. Spratling A single functional model of drivers and modulators in cortex , 2013, Journal of Computational Neuroscience.

[5]  Tobias Brosch,et al.  Computing with a Canonical Neural Circuits Model with Pool Normalization and Modulating Feedback , 2014, Neural Computation.

[6]  J. Anthony Movshon,et al.  Linearity and gain control in V1 simple cells , 1999 .

[7]  T. Poggio,et al.  Cognitive neuroscience: Neural mechanisms for the recognition of biological movements , 2003, Nature Reviews Neuroscience.

[8]  Pieter R. Roelfsema,et al.  Attention-Gated Reinforcement Learning of Internal Representations for Classification , 2005, Neural Computation.

[9]  E. Capaldi,et al.  The organization of behavior. , 1992, Journal of applied behavior analysis.

[10]  G. Edelman Neural Darwinism: Selection and reentrant signaling in higher brain function , 1993, Neuron.

[11]  T. Poggio,et al.  Hierarchical models of object recognition in cortex , 1999, Nature Neuroscience.

[12]  Pieter R. Roelfsema,et al.  Different Processing Phases for Features, Figures, and Selective Attention in the Primary Visual Cortex , 2007, Neuron.

[13]  E. Oja Simplified neuron model as a principal component analyzer , 1982, Journal of mathematical biology.

[14]  J.A. Anderson,et al.  Neural Network Models for Pattern Recognition and Associative Memory , 2002 .

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

[16]  D. Heeger,et al.  The Normalization Model of Attention , 2009, Neuron.

[17]  Teuvo Kohonen,et al.  Self-organized formation of topologically correct feature maps , 2004, Biological Cybernetics.

[18]  Gordon Pipa,et al.  SORN: A Self-Organizing Recurrent Neural Network , 2009, Front. Comput. Neurosci..

[19]  S. Grossberg,et al.  ART 2: self-organization of stable category recognition codes for analog input patterns. , 1987, Applied optics.

[20]  Thomas Serre,et al.  A neuromorphic approach to computer vision , 2010, Commun. ACM.

[21]  Lawrence D. Jackel,et al.  Handwritten Digit Recognition with a Back-Propagation Network , 1989, NIPS.

[22]  R. Eckhorn Neural Mechanisms of Visual Feature Binding Investigated with Microelectrodes and Models , 1999 .

[23]  Erkki Oja,et al.  Principal components, minor components, and linear neural networks , 1992, Neural Networks.

[24]  Geoffrey E. Hinton,et al.  Reducing the Dimensionality of Data with Neural Networks , 2006, Science.

[25]  Roman Bek,et al.  Discourse on one way in which a quantum-mechanics language on the classical logical base can be built up , 1978, Kybernetika.

[26]  Stephen Grossberg,et al.  ART 3: Hierarchical search using chemical transmitters in self-organizing pattern recognition architectures , 1990, Neural Networks.

[27]  Marc Timme,et al.  Analysis of Synaptic Scaling in Combination with Hebbian Plasticity in Several Simple Networks , 2012, Front. Comput. Neurosci..

[28]  A G Barto,et al.  Toward a modern theory of adaptive networks: expectation and prediction. , 1981, Psychological review.

[29]  M. Carandini,et al.  Normalization as a canonical neural computation , 2011, Nature Reviews Neuroscience.

[30]  Arash Yazdanbakhsh,et al.  Seeing surfaces: The brain's vision of the world , 2007 .

[31]  C. Malsburg Self-organization of orientation sensitive cells in the striate cortex , 2004, Kybernetik.

[32]  H. Neumann,et al.  The Role of Attention in Figure-Ground Segregation in Areas V1 and V4 of the Visual Cortex , 2012, Neuron.

[33]  Yoshua. Bengio,et al.  Learning Deep Architectures for AI , 2007, Found. Trends Mach. Learn..

[34]  D. O. Hebb,et al.  The organization of behavior , 1988 .

[35]  T. Sejnowski,et al.  Neural network model of visual cortex for determining surface curvature from images of shaded surfaces , 1990, Proceedings of the Royal Society of London. B. Biological Sciences.

[36]  David G. Lowe,et al.  University of British Columbia. , 1945, Canadian Medical Association journal.

[37]  Michel Vidal-Naquet,et al.  Visual features of intermediate complexity and their use in classification , 2002, Nature Neuroscience.

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

[39]  Karl J. Friston,et al.  Canonical Microcircuits for Predictive Coding , 2012, Neuron.

[40]  Heiko Neumann,et al.  Disambiguating Visual Motion Through Contextual Feedback Modulation , 2004, Neural Computation.

[41]  K. Doya Reinforcement learning: Computational theory and biological mechanisms , 2007 .

[42]  David S. Touretzky,et al.  Advances in neural information processing systems 2 , 1989 .

[43]  Stephen Grossberg,et al.  A massively parallel architecture for a self-organizing neural pattern recognition machine , 1988, Comput. Vis. Graph. Image Process..

[44]  V. Lamme,et al.  The distinct modes of vision offered by feedforward and recurrent processing , 2000, Trends in Neurosciences.

[45]  R. Guillery,et al.  On the actions that one nerve cell can have on another: distinguishing "drivers" from "modulators". , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[46]  M. Elad,et al.  $rm K$-SVD: An Algorithm for Designing Overcomplete Dictionaries for Sparse Representation , 2006, IEEE Transactions on Signal Processing.

[47]  Heiko Neumann,et al.  Recurrent V1–V2 interaction in early visual boundary processing , 1999, Biological Cybernetics.

[48]  J. Bullier,et al.  Visual activity in area V2 during reversible inactivation of area 17 in the macaque monkey. , 1989, Journal of neurophysiology.

[49]  Stephen Grossberg,et al.  Adaptive Resonance Theory: How a brain learns to consciously attend, learn, and recognize a changing world , 2013, Neural Networks.

[50]  P. Roelfsema Cortical algorithms for perceptual grouping. , 2006, Annual review of neuroscience.

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

[52]  C. Fillmore TOWARD A MODERN THEORY OF CASE. , 1966 .

[53]  Lawrence D. Jackel,et al.  Backpropagation Applied to Handwritten Zip Code Recognition , 1989, Neural Computation.

[54]  John K. Tsotsos,et al.  Computational foundations for attentive processes , 2008, Scholarpedia.

[55]  Jeffrey L. Elman,et al.  Finding Structure in Time , 1990, Cogn. Sci..

[56]  Yann LeCun,et al.  Discriminative Recurrent Sparse Auto-Encoders , 2013, ICLR.

[57]  Pieter R. Roelfsema,et al.  Distinct Roles of the Cortical Layers of Area V1 in Figure-Ground Segregation , 2013, Current Biology.

[58]  Yoshua Bengio,et al.  Gradient-based learning applied to document recognition , 1998, Proc. IEEE.

[59]  PoggioTomaso,et al.  Robust Object Recognition with Cortex-Like Mechanisms , 2007 .

[60]  Shimon Ullman,et al.  Combined Top-Down/Bottom-Up Segmentation , 2008, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[61]  C. Koch,et al.  Constraints on cortical and thalamic projections: the no-strong-loops hypothesis , 1998, Nature.

[62]  Y. Dan,et al.  Spike timing-dependent plasticity: a Hebbian learning rule. , 2008, Annual review of neuroscience.

[63]  Tobias Brosch,et al.  Interaction of feedforward and feedback streams in visual cortex in a firing-rate model of columnar computations , 2014, Neural Networks.

[64]  S. Grossberg Contour Enhancement , Short Term Memory , and Constancies in Reverberating Neural Networks , 1973 .

[65]  Martin A. Giese,et al.  Learning Representations of Animated Motion Sequences - A Neural Model , 2014, Top. Cogn. Sci..

[66]  Wulfram Gerstner,et al.  A neuronal learning rule for sub-millisecond temporal coding , 1996, Nature.

[67]  A. Kriegstein,et al.  Development and Evolution of the Human Neocortex , 2011, Cell.

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

[69]  David Zipser,et al.  Feature Discovery by Competive Learning , 1986, Cogn. Sci..

[70]  T. Kohonen Self-organized formation of topographically correct feature maps , 1982 .

[71]  K. Doya Reinforcement learning: Computational theory and biological mechanisms , 2007, HFSP journal.

[72]  W. Senn,et al.  Top-down dendritic input increases the gain of layer 5 pyramidal neurons. , 2004, Cerebral cortex.

[73]  Stephen Grossberg,et al.  Competitive Learning: From Interactive Activation to Adaptive Resonance , 1987, Cogn. Sci..

[74]  Geoffrey E. Hinton Learning multiple layers of representation , 2007, Trends in Cognitive Sciences.

[75]  Tomaso A. Poggio,et al.  A Canonical Neural Circuit for Cortical Nonlinear Operations , 2008, Neural Computation.

[76]  G. Johansson Visual perception of biological motion and a model for its analysis , 1973 .

[77]  S. Ullman Object recognition and segmentation by a fragment-based hierarchy , 2007, Trends in Cognitive Sciences.

[78]  S. Grossberg,et al.  How does a brain build a cognitive code? , 1980, Psychological review.

[79]  R. Desimone Visual attention mediated by biased competition in extrastriate visual cortex. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[80]  Pierre Kornprobst,et al.  Neural Mechanisms of Motion Detection, Integration, and Segregation: From Biology to Artificial Image Processing Systems , 2011, EURASIP J. Adv. Signal Process..

[81]  M. Larkum A cellular mechanism for cortical associations: an organizing principle for the cerebral cortex , 2013, Trends in Neurosciences.

[82]  Terrence J. Sejnowski,et al.  Network model of shape-from-shading: neural function arises from both receptive and projective fields , 1988, Nature.

[83]  Stephen Grossberg,et al.  Nonlinear neural networks: Principles, mechanisms, and architectures , 1988, Neural Networks.

[84]  G. Pourtois,et al.  Top-down effects on early visual processing in humans: A predictive coding framework , 2011, Neuroscience & Biobehavioral Reviews.

[85]  Roger C. Tam,et al.  Efficient Training of Convolutional Deep Belief Networks in the Frequency Domain for Application to High-Resolution 2D and 3D Images , 2015, Neural Computation.

[86]  A. Bruckstein,et al.  K-SVD : An Algorithm for Designing of Overcomplete Dictionaries for Sparse Representation , 2005 .

[87]  Reinhard Eckhorn,et al.  Feature Linking via Synchronization among Distributed Assemblies: Simulations of Results from Cat Visual Cortex , 1990, Neural Computation.

[88]  Michael W. Spratling Reconciling Predictive Coding and Biased Competition Models of Cortical Function , 2008, Frontiers Comput. Neurosci..

[89]  G. Bi,et al.  Synaptic modification by correlated activity: Hebb's postulate revisited. , 2001, Annual review of neuroscience.

[90]  S Ullman,et al.  Sequence seeking and counter streams: a computational model for bidirectional information flow in the visual cortex. , 1995, Cerebral cortex.

[91]  Heiko Neumann,et al.  A Model of Motion Transparency Processing with Local Center-Surround Interactions and Feedback , 2011, Neural Computation.

[92]  Peter C. M. Molenaar,et al.  Exact ART: A Complete Implementation of an ART Network , 1997, Neural Networks.

[93]  Matthew W Self,et al.  Different glutamate receptors convey feedforward and recurrent processing in macaque V1 , 2012, Proceedings of the National Academy of Sciences.

[94]  S. Sherman,et al.  A modulatory effect of the feedback from higher visual areas to V1 in the mouse. , 2013, Journal of neurophysiology.

[95]  Peter T. Coleman,et al.  Competitive Learning : “ From Interactive Activation to Adaptive Resonance , 2014 .

[96]  H. Spekreijse,et al.  FigureGround Segregation in a Recurrent Network Architecture , 2002, Journal of Cognitive Neuroscience.

[97]  Yee Whye Teh,et al.  A Fast Learning Algorithm for Deep Belief Nets , 2006, Neural Computation.