Characterizing Responses of Translation-Invariant Neurons to Natural Stimuli: Maximally Informative Invariant Dimensions

The human visual system is capable of recognizing complex objects even when their appearances change drastically under various viewing conditions. Especially in the higher cortical areas, the sensory neurons reflect such functional capacity in their selectivity for complex visual features and invariance to certain object transformations, such as image translation. Due to the strong nonlinearities necessary to achieve both the selectivity and invariance, characterizing and predicting the response patterns of these neurons represents a formidable computational challenge. A related problem is that such neurons are poorly driven by randomized inputs, such as white noise, and respond strongly only to stimuli with complex high-order correlations, such as natural stimuli. Here we describe a novel two-step optimization technique that can characterize both the shape selectivity and the range and coarseness of position invariance from neural responses to natural stimuli. One step in the optimization is finding the template as the maximally informative dimension given the estimated spatial location where the response could have been triggered within each image. The estimates of the locations that triggered the response are updated in the next step. Under the assumption of a monotonic relationship between the firing rate and stimulus projections on the template at a given position, the most likely location is the one that has the largest projection on the estimate of the template. The algorithm shows quick convergence during optimization, and the estimation results are reliable even in the regime of small signal-to-noise ratios. When we apply the algorithm to responses of complex cells in the primary visual cortex (V1) to natural movies, we find that responses of the majority of cells were significantly better described by translation-invariant models based on one template compared with position-specific models with several relevant features.

[1]  S. Thorpe,et al.  Speed of processing in the human visual system , 1996, Nature.

[2]  R. Desimone,et al.  Stimulus-selective properties of inferior temporal neurons in the macaque , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  D. B. Bender,et al.  Visual properties of neurons in inferotemporal cortex of the Macaque. , 1972, Journal of neurophysiology.

[4]  Guillermo Sapiro,et al.  A subspace reverse-correlation technique for the study of visual neurons , 1997, Vision Research.

[5]  M. Tovée,et al.  Translation invariance in the responses to faces of single neurons in the temporal visual cortical areas of the alert macaque. , 1994, Journal of neurophysiology.

[6]  Michael J. Berry,et al.  The Neural Code of the Retina , 1999, Neuron.

[7]  L. Abbott,et al.  Responses of neurons in primary and inferior temporal visual cortices to natural scenes , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[8]  D. Ruderman,et al.  Independent component analysis of natural image sequences yields spatio-temporal filters similar to simple cells in primary visual cortex , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[9]  N. Logothetis,et al.  Shape representation in the inferior temporal cortex of monkeys , 1995, Current Biology.

[10]  W. Bialek,et al.  Features and dimensions: Motion estimation in fly vision , 2005, q-bio/0505003.

[11]  R. Vogels,et al.  Spatial sensitivity of macaque inferior temporal neurons , 2000, The Journal of comparative neurology.

[12]  Tatyana O Sharpee,et al.  On the importance of static nonlinearity in estimating spatiotemporal neural filters with natural stimuli. , 2008, Journal of neurophysiology.

[13]  Anne Hsu,et al.  Tuning for spectro-temporal modulations as a mechanism for auditory discrimination of natural sounds , 2005, Nature Neuroscience.

[14]  Eero P. Simoncelli,et al.  Natural image statistics and neural representation. , 2001, Annual review of neuroscience.

[15]  D. C. Essen,et al.  Neural responses to polar, hyperbolic, and Cartesian gratings in area V4 of the macaque monkey. , 1996, Journal of neurophysiology.

[16]  Shimon Edelman,et al.  Representation and recognition in vision , 1999 .

[17]  Eero P. Simoncelli,et al.  Natural signal statistics and sensory gain control , 2001, Nature Neuroscience.

[18]  Robert Shapley,et al.  Receptive field structure of neurons in monkey primary visual cortex revealed by stimulation with natural image sequences. , 2002, Journal of vision.

[19]  Keiji Tanaka,et al.  Neuronal selectivities to complex object features in the ventral visual pathway of the macaque cerebral cortex. , 1994, Journal of neurophysiology.

[20]  D. B. Bender,et al.  Visual Receptive Fields of Neurons in Inferotemporal Cortex of the Monkey , 1969, Science.

[21]  Kenneth D. Miller,et al.  Adaptive filtering enhances information transmission in visual cortex , 2006, Nature.

[22]  Michael J. Berry,et al.  Selectivity for multiple stimulus features in retinal ganglion cells. , 2006, Journal of neurophysiology.

[23]  Tatyana O Sharpee,et al.  Computational identification of receptive fields. , 2013, Annual review of neuroscience.

[24]  D. Rubin,et al.  Maximum likelihood from incomplete data via the EM - algorithm plus discussions on the paper , 1977 .

[25]  J. Hegdé,et al.  A comparative study of shape representation in macaque visual areas v2 and v4. , 2007, Cerebral cortex.

[26]  O. Andreassen,et al.  Mice Deficient in Cellular Glutathione Peroxidase Show Increased Vulnerability to Malonate, 3-Nitropropionic Acid, and 1-Methyl-4-Phenyl-1,2,5,6-Tetrahydropyridine , 2000, The Journal of Neuroscience.

[27]  Robert Tibshirani,et al.  An Introduction to the Bootstrap , 1994 .

[28]  J. Reynolds,et al.  Trade-off between curvature tuning and position invariance in visual area V4 , 2013, Proceedings of the National Academy of Sciences.

[29]  J. Atick,et al.  STATISTICS OF NATURAL TIME-VARYING IMAGES , 1995 .

[30]  R. Desimone,et al.  Inferior temporal mechanisms for invariant object recognition. , 1994, Cerebral cortex.

[31]  C. Atencio,et al.  Hierarchical computation in the canonical auditory cortical circuit , 2009, Proceedings of the National Academy of Sciences.

[32]  Keiji Tanaka,et al.  Functional architecture in monkey inferotemporal cortex revealed by in vivo optical imaging , 1998, Neuroscience Research.

[33]  William Bialek,et al.  Real-time performance of a movement-sensitive neuron in the blowfly visual system: coding and information transfer in short spike sequences , 1988, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[34]  William Bialek,et al.  Synergy in a Neural Code , 2000, Neural Computation.

[35]  T. Gawne,et al.  Responses of primate visual cortical neurons to stimuli presented by flash, saccade, blink, and external darkening. , 2002, Journal of neurophysiology.

[36]  Kunihiko Fukushima,et al.  Neocognitron: A self-organizing neural network model for a mechanism of pattern recognition unaffected by shift in position , 1980, Biological Cybernetics.

[37]  P Kuyper,et al.  Triggered correlation. , 1968, IEEE transactions on bio-medical engineering.

[38]  Nikos K. Logothetis,et al.  Nonmonotonic noise tuning of BOLD fMRI signal to natural images in the visual cortex of the anesthetized monkey , 2001, Current Biology.

[39]  Joaquín Rapela,et al.  Estimating nonlinear receptive fields from natural images. , 2006, Journal of vision.

[40]  K. Sen,et al.  Spectral-temporal Receptive Fields of Nonlinear Auditory Neurons Obtained Using Natural Sounds , 2022 .

[41]  William H. Press,et al.  The Art of Scientific Computing Second Edition , 1998 .

[42]  Michael J. Berry,et al.  Fine Spatial Information Represented in a Population of Retinal Ganglion Cells , 2011, The Journal of Neuroscience.

[43]  William H. Press,et al.  Book-Review - Numerical Recipes in Pascal - the Art of Scientific Computing , 1989 .

[44]  G. Orban,et al.  Shape interactions in macaque inferior temporal neurons. , 1999, Journal of neurophysiology.

[45]  Sarah M. N. Woolley,et al.  Stimulus-Dependent Auditory Tuning Results in Synchronous Population Coding of Vocalizations in the Songbird Midbrain , 2006, The Journal of Neuroscience.

[46]  T. Sharpee,et al.  Estimating linear–nonlinear models using Rényi divergences , 2009, Network.

[47]  Chia‐Sheng Lin,et al.  Receptive field properties of neurons in the visual cortex of the rat , 1981, Neuroscience Letters.

[48]  Keiji Tanaka,et al.  Optical Imaging of Functional Organization in the Monkey Inferotemporal Cortex , 1996, Science.

[49]  J. Mendel,et al.  ePPR: a new strategy for the characterization of sensory cells from input/output data , 2010, Network.

[50]  G. Orban,et al.  Cue-invariant shape selectivity of macaque inferior temporal neurons. , 1993, Science.

[51]  D. Heeger Normalization of cell responses in cat striate cortex , 1992, Visual Neuroscience.

[52]  Maneesh Sahani,et al.  How Linear are Auditory Cortical Responses? , 2002, NIPS.

[53]  C. Connor,et al.  Population coding of shape in area V4 , 2002, Nature Neuroscience.

[54]  R. Wurtz,et al.  Visual responses of inferior temporal neurons in awake rhesus monkey. , 1983, Journal of neurophysiology.

[55]  T. Sharpee Comparison of information and variance maximization strategies for characterizing neural feature selectivity , 2007, Statistics in medicine.

[56]  Feng Qi Han,et al.  Cortical Sensitivity to Visual Features in Natural Scenes , 2005, PLoS biology.

[57]  C. Connor,et al.  Responses to contour features in macaque area V4. , 1999, Journal of neurophysiology.

[58]  R. Shapley,et al.  Fine structure of receptive-field centers of X and Y cells of the cat , 1991, Visual Neuroscience.

[59]  K. Rockland,et al.  Specific and columnar projection from area TEO to TE in the macaque inferotemporal cortex. , 1993, Cerebral cortex.

[60]  J. Touryan,et al.  Spatial Structure of Complex Cell Receptive Fields Measured with Natural Images , 2005, Neuron.

[61]  Eero P. Simoncelli,et al.  Dimensionality reduction in neural models: an information-theoretic generalization of spike-triggered average and covariance analysis. , 2006, Journal of vision.

[62]  D. Ringach,et al.  On the classification of simple and complex cells , 2002, Vision Research.

[63]  C. Atencio,et al.  Cooperative Nonlinearities in Auditory Cortical Neurons , 2008, Neuron.

[64]  S. Ullman High-Level Vision: Object Recognition and Visual Cognition , 1996 .

[65]  Eero P. Simoncelli,et al.  Characterizing Neural Gain Control using Spike-triggered Covariance , 2001, NIPS.

[66]  E. Rolls Functions of the Primate Temporal Lobe Cortical Visual Areas in Invariant Visual Object and Face Recognition , 2000, Neuron.

[67]  J. Hegdé,et al.  Selectivity for Complex Shapes in Primate Visual Area V2 , 2000, The Journal of Neuroscience.

[68]  R. Shapley,et al.  A method of nonlinear analysis in the frequency domain. , 1980, Biophysical journal.

[69]  J. Touryan,et al.  Isolation of Relevant Visual Features from Random Stimuli for Cortical Complex Cells , 2002, The Journal of Neuroscience.

[70]  David J. C. MacKay,et al.  Information-Based Objective Functions for Active Data Selection , 1992, Neural Computation.

[71]  D J Field,et al.  Relations between the statistics of natural images and the response properties of cortical cells. , 1987, Journal of the Optical Society of America. A, Optics and image science.

[72]  William Bialek,et al.  Spikes: Exploring the Neural Code , 1996 .

[73]  William Bialek,et al.  Entropy and Information in Neural Spike Trains , 1996, cond-mat/9603127.

[74]  Tomaso Poggio,et al.  Trade-Off between Object Selectivity and Tolerance in Monkey Inferotemporal Cortex , 2007, The Journal of Neuroscience.

[75]  William Bialek,et al.  Analyzing Neural Responses to Natural Signals: Maximally Informative Dimensions , 2002, Neural Computation.

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

[77]  R. Desimone,et al.  Shape recognition and inferior temporal neurons. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[78]  Shih-Cheng Yen,et al.  Spatial and temporal jitter distort estimated functional properties of visual sensory neurons , 2009, Journal of Computational Neuroscience.

[79]  William H. Press,et al.  Numerical recipes in C. The art of scientific computing , 1987 .

[80]  D G Pelli,et al.  Uncertainty explains many aspects of visual contrast detection and discrimination. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[81]  William Bialek,et al.  The Information Content of Receptive Fields , 2003, Neuron.

[82]  E J Chichilnisky,et al.  Cone inputs to simple and complex cells in V1 of awake macaque. , 2007, Journal of neurophysiology.

[83]  Eero P. Simoncelli,et al.  Spike-triggered neural characterization. , 2006, Journal of vision.

[84]  I. Ohzawa,et al.  Receptive Field Properties of Neurons in the Early Visual Cortex Revealed by Local Spectral Reverse Correlation , 2006, The Journal of Neuroscience.

[85]  E J Chichilnisky,et al.  A simple white noise analysis of neuronal light responses , 2001, Network.

[86]  I. Ohzawa,et al.  Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. II. Linearity of temporal and spatial summation. , 1993, Journal of neurophysiology.

[87]  Nicole C. Rust,et al.  Selectivity and Tolerance (“Invariance”) Both Increase as Visual Information Propagates from Cortical Area V4 to IT , 2010, The Journal of Neuroscience.

[88]  William Bialek,et al.  Statistics of Natural Images: Scaling in the Woods , 1993, NIPS.

[89]  D. V. van Essen,et al.  Selectivity for polar, hyperbolic, and Cartesian gratings in macaque visual cortex. , 1993, Science.

[90]  Feng Qi Han,et al.  Excitatory and suppressive receptive field subunits in awake monkey primary visual cortex (V1) , 2007, Proceedings of the National Academy of Sciences.

[91]  Ryan J. Rowekamp,et al.  Analyzing multicomponent receptive fields from neural responses to natural stimuli , 2011, Network.

[92]  C. Connor,et al.  Shape representation in area V4: position-specific tuning for boundary conformation. , 2001, Journal of neurophysiology.

[93]  Lawrence C. Sincich,et al.  Preserving Information in Neural Transmission , 2009, The Journal of Neuroscience.

[94]  Leslie G. Ungerleider,et al.  Visual topography of area TEO in the macaque , 1991, The Journal of comparative neurology.

[95]  Anitha Pasupathy,et al.  Transformation of shape information in the ventral pathway , 2007, Current Opinion in Neurobiology.

[96]  Stefano Panzeri,et al.  The Upward Bias in Measures of Information Derived from Limited Data Samples , 1995, Neural Computation.

[97]  Liam Paninski,et al.  Convergence properties of three spike-triggered analysis techniques , 2003, NIPS.

[98]  Christian K. Machens,et al.  Linearity of Cortical Receptive Fields Measured with Natural Sounds , 2004, The Journal of Neuroscience.

[99]  Eero P. Simoncelli,et al.  Spatiotemporal Elements of Macaque V1 Receptive Fields , 2005, Neuron.

[100]  Haim Sompolinsky,et al.  Bayesian model of dynamic image stabilization in the visual system , 2010, Proceedings of the National Academy of Sciences.

[101]  Heekuck Oh,et al.  Neural Networks for Pattern Recognition , 1993, Adv. Comput..

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

[103]  N. C. Singh,et al.  Estimating spatio-temporal receptive fields of auditory and visual neurons from their responses to natural stimuli , 2001 .

[104]  D. Pollen,et al.  Spatial receptive field organization of macaque V4 neurons. , 2002, Cerebral cortex.

[105]  Anirvan S. Nandy,et al.  Classification images with uncertainty. , 2006, Journal of vision.

[106]  J. Maunsell,et al.  Anterior inferotemporal neurons of monkeys engaged in object recognition can be highly sensitive to object retinal position. , 2003, Journal of neurophysiology.

[107]  R. Desimone,et al.  Visual properties of neurons in area V4 of the macaque: sensitivity to stimulus form. , 1987, Journal of neurophysiology.

[108]  T. Sharpee,et al.  Predictable irregularities in retinal receptive fields , 2009, Proceedings of the National Academy of Sciences.

[109]  Michael J. Berry,et al.  Identifying Functional Bases for Multidimensional Neural Computations , 2013, Neural Computation.

[110]  T. Gawne,et al.  Responses of primate visual cortical V4 neurons to simultaneously presented stimuli. , 2002, Journal of neurophysiology.

[111]  Minami Ito,et al.  Size and position invariance of neuronal responses in monkey inferotemporal cortex. , 1995, Journal of neurophysiology.

[112]  T. Poggio,et al.  A model of V4 shape selectivity and invariance. , 2007, Journal of neurophysiology.

[113]  Thane Fremouw,et al.  Sound representation methods for spectro-temporal receptive field estimation , 2006, Journal of Computational Neuroscience.

[114]  Timothy A. Machado,et al.  Functional connectivity in the retina at the resolution of photoreceptors , 2010, Nature.