Statistics of visual responses in primate inferotemporal cortex to object stimuli.

We have characterized selectivity and sparseness in anterior inferotemporal cortex, using a large data set. Responses were collected from 674 monkey inferotemporal cells, each stimulated by 806 object photographs. This 806 × 674 matrix was examined in two ways: columnwise, looking at responses of a single neuron to all images (single-neuron selectivity), and rowwise, looking at the responses of all neurons caused by a single image (population sparseness). Selectivity and sparseness were measured as kurtosis of probability distributions. Population sparseness exceeded single-neuron selectivity, with specific values dependent on the size of the data sample. This difference was principally caused by inclusion, within the population, of neurons with a variety of dynamic ranges (standard deviations of responses over all images). Statistics of large responses were examined by quantifying how quickly the upper tail of the probability distribution decreased (tail heaviness). This analysis demonstrated that population responses had heavier tails than single-neuron responses, consistent with the difference between sparseness and selectivity measurements. Population responses with spontaneous activity subtracted had the heaviest tails, following a power law. The very light tails of single-neuron responses indicate that the critical feature for each neuron is simple enough to have a high probability of occurring within a limited stimulus set. Heavy tails of population responses indicate that there are a large number of different critical features to which different neurons are tuned. These results are inconsistent with some structural models of object recognition that posit that objects are decomposed into a small number of standard features.

[1]  C. Gross Single neuron studies of inferior temporal cortex , 2008, Neuropsychologia.

[2]  A. Holden A note on convolution and stable distributions in the nervous system , 1975, Biological cybernetics.

[3]  Peter Földiák,et al.  SPARSE CODING IN THE PRIMATE CORTEX , 2002 .

[4]  Terence D Sanger,et al.  Neural population codes , 2003, Current Opinion in Neurobiology.

[5]  C. Baker,et al.  The neural basis of visual object learning , 2010, Trends in Cognitive Sciences.

[6]  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.

[7]  Yasushi Miyashita,et al.  Forward Processing of Long-Term Associative Memory in Monkey Inferotemporal Cortex , 2003, The Journal of Neuroscience.

[8]  J. L. Nolan Stable Distributions. Models for Heavy Tailed Data , 2001 .

[9]  David J. Field,et al.  Sparse coding with an overcomplete basis set: A strategy employed by V1? , 1997, Vision Research.

[10]  Xin Huang,et al.  Noise correlations in cortical area MT and their potential impact on trial-by-trial variation in the direction and speed of smooth-pursuit eye movements. , 2009, Journal of neurophysiology.

[11]  W. J. Daunicht,et al.  An on-line spike form discriminator for extracellular recordings based on an analog correlation technique , 1986, Journal of Neuroscience Methods.

[12]  T. Poggio,et al.  Object Selectivity of Local Field Potentials and Spikes in the Macaque Inferior Temporal Cortex , 2006, Neuron.

[13]  E. Rolls,et al.  View-invariant representations of familiar objects by neurons in the inferior temporal visual cortex. , 1998, Cerebral cortex.

[14]  H. Tamura,et al.  Visual response properties of cells in the ventral and dorsal parts of the macaque inferotemporal cortex. , 2001, Cerebral cortex.

[15]  Aapo Hyvärinen,et al.  Natural Image Statistics - A Probabilistic Approach to Early Computational Vision , 2009, Computational Imaging and Vision.

[16]  Edmund T. Rolls,et al.  Functions of the Primate Temporal Lobe Cortical Visual Areas in Invariant Visual Object and Face Recognition , 2000, Neuron.

[17]  S L Moody,et al.  A Model That Accounts for Activity in Primate Frontal Cortex during a Delayed Matching-to-Sample Task , 1998, The Journal of Neuroscience.

[18]  Sidney R. Lehky,et al.  Frontiers in Computational Neuroscience Computational Neuroscience , 2022 .

[19]  G. Glover,et al.  Enhancement of Object Representations in Primate Perirhinal Cortex During a Visual Working-Memory Task , 2007 .

[20]  Edmund T. Rolls,et al.  Neuronal selectivity, population sparseness, and ergodicity in the inferior temporal visual cortex , 2007, Biological Cybernetics.

[21]  M. Pickering,et al.  Eye guidance in reading and scene perception , 1998 .

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

[23]  P. Fldik,et al.  The Speed of Sight , 2001, Journal of Cognitive Neuroscience.

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

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

[26]  Rosario N. Mantegna,et al.  Book Review: An Introduction to Econophysics, Correlations, and Complexity in Finance, N. Rosario, H. Mantegna, and H. E. Stanley, Cambridge University Press, Cambridge, 2000. , 2000 .

[27]  Keiji Tanaka,et al.  Object category structure in response patterns of neuronal population in monkey inferior temporal cortex. , 2007, Journal of neurophysiology.

[28]  Ioannis A. Koutrouvelis,et al.  Regression-Type Estimation of the Parameters of Stable Laws , 1980 .

[29]  J. Pickands Statistical Inference Using Extreme Order Statistics , 1975 .

[30]  R. Adler,et al.  A practical guide to heavy tails: statistical techniques and applications , 1998 .

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

[32]  I. Biederman Recognition-by-components: a theory of human image understanding. , 1987, Psychological review.

[33]  David J. Field,et al.  What Is the Goal of Sensory Coding? , 1994, Neural Computation.

[34]  Mohammad Ali Baradaran Ghahfarokhi,et al.  Applications of Stable Distributions in Time Series Analysis, Computer Sciences and Financial Markets , 2009 .

[35]  Keiji Tanaka,et al.  Effects of shape-discrimination training on the selectivity of inferotemporal cells in adult monkeys. , 1998, Journal of neurophysiology.

[36]  Ehud Zohary,et al.  Correlated neuronal discharge rate and its implications for psychophysical performance , 1994, Nature.

[37]  M. Newman Power laws, Pareto distributions and Zipf's law , 2005 .

[38]  Stefano Panzeri,et al.  Firing Rate Distributions and Efficiency of Information Transmission of Inferior Temporal Cortex Neurons to Natural Visual Stimuli , 1999, Neural Computation.

[39]  Sidney R. Lehky,et al.  Frontiers in Computational Neuroscience Computational Neuroscience , 2022 .

[40]  E. Rolls,et al.  The Neurophysiology of Backward Visual Masking: Information Analysis , 1999, Journal of Cognitive Neuroscience.

[41]  S. Edelman Constraining the neural representation of the visual world , 2002, Trends in Cognitive Sciences.

[42]  C. Koch,et al.  Sparse Representation in the Human Medial Temporal Lobe , 2006, The Journal of Neuroscience.

[43]  Keiji Tanaka,et al.  Inferotemporal cortex and object vision. , 1996, Annual review of neuroscience.

[44]  G Kovács,et al.  Cortical correlate of pattern backward masking. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[45]  D. Marr,et al.  Representation and recognition of the spatial organization of three-dimensional shapes , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[46]  S. Thorpe,et al.  The time course of visual processing: Backward masking and natural scene categorisation , 2005, Vision Research.

[47]  Minami Ito,et al.  Columns for visual features of objects in monkey inferotemporal cortex , 1992, Nature.

[48]  R. Quiroga,et al.  Extracting information from neuronal populations : information theory and decoding approaches , 2022 .

[49]  J L Gallant,et al.  Sparse coding and decorrelation in primary visual cortex during natural vision. , 2000, Science.

[50]  Eric P. Smith,et al.  An Introduction to Statistical Modeling of Extreme Values , 2002, Technometrics.

[51]  C. L. Nikias,et al.  Signal processing with alpha-stable distributions and applications , 1995 .

[52]  Andrew Hollingworth,et al.  Eye Movements During Scene Viewing: An Overview , 1998 .

[53]  K. Tanaka,et al.  Divergent Projections from the Anterior Inferotemporal Area TE to the Perirhinal and Entorhinal Cortices in the Macaque Monkey , 1996, The Journal of Neuroscience.

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

[55]  Masaki Tomonaga,et al.  How chimpanzees look at pictures: a comparative eye-tracking study , 2009, Proceedings of the Royal Society B: Biological Sciences.

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

[57]  K. Hoffmann,et al.  Neural Dynamics of Saccadic Suppression , 2009, Journal of Neuroscience.

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

[59]  D. Tolhurst,et al.  Characterizing the sparseness of neural codes , 2001, Network.

[60]  Keiji Tanaka,et al.  Differences in onset latency of macaque inferotemporal neural responses to primate and non-primate faces. , 2005, Journal of neurophysiology.

[61]  Anthony J. Movshon,et al.  Optimal representation of sensory information by neural populations , 2006, Nature Neuroscience.

[62]  Alexander S. Ecker,et al.  Decorrelated Neuronal Firing in Cortical Microcircuits , 2010, Science.

[63]  P. Goldman-Rakic,et al.  Correlated discharges among putative pyramidal neurons and interneurons in the primate prefrontal cortex. , 2002, Journal of neurophysiology.

[64]  R. Desimone,et al.  Clustering of perirhinal neurons with similar properties following visual experience in adult monkeys , 2000, Nature Neuroscience.

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

[66]  B L McNaughton,et al.  Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. , 1998, Journal of neurophysiology.

[67]  E T Rolls,et al.  Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex. , 1995, Journal of neurophysiology.

[68]  Christian W. Eurich,et al.  Representational Accuracy of Stochastic Neural Populations , 2002, Neural Computation.

[69]  Jeffrey S Bowers,et al.  On the biological plausibility of grandmother cells: implications for neural network theories in psychology and neuroscience. , 2009, Psychological review.

[70]  I. A. Koutrouvelis An iterative procedure for the estimation of the parameters of stable laws , 1981 .

[71]  David L. Sheinberg,et al.  Visual object recognition. , 1996, Annual review of neuroscience.

[72]  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.

[73]  K. Chung,et al.  Limit Distributions for Sums of Independent Random Variables. , 1955 .

[74]  J. Corcoran Modelling Extremal Events for Insurance and Finance , 2002 .

[75]  E. Miller,et al.  Experience-dependent sharpening of visual shape selectivity in inferior temporal cortex. , 2005, Cerebral cortex.

[76]  Sidney R. Lehky Fine Discrimination of Faces can be Performed Rapidly , 2000, Journal of Cognitive Neuroscience.

[77]  D. Perrett,et al.  Rapid serial visual presentation for the determination of neural selectivity in area STSa. , 2004, Progress in brain research.

[78]  P. Levy,et al.  Calcul des Probabilites , 1926, The Mathematical Gazette.

[79]  TJ Gawne,et al.  How independent are the messages carried by adjacent inferior temporal cortical neurons? , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[80]  D. Perrett,et al.  Color sensitivity of cells responsive to complex stimuli in the temporal cortex. , 2003, Journal of neurophysiology.

[81]  F. Mechler,et al.  Independent and Redundant Information in Nearby Cortical Neurons , 2001, Science.

[82]  S. R. Lehky,et al.  Comparison of shape encoding in primate dorsal and ventral visual pathways. , 2007, Journal of neurophysiology.

[83]  V. Zolotarev One-dimensional stable distributions , 1986 .

[84]  N. Kanwisher,et al.  Domain specificity in visual cortex. , 2006, Cerebral cortex.

[85]  D. Amaral,et al.  Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents , 1994, The Journal of comparative neurology.

[86]  M. Tovée,et al.  Processing speed in the cerebral cortex and the neurophysiology of visual masking , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[87]  D. Tolhurst,et al.  The Sparseness of Neuronal Responses in Ferret Primary Visual Cortex , 2009, The Journal of Neuroscience.

[88]  R. Vogels,et al.  Properties of shape tuning of macaque inferior temporal neurons examined using rapid serial visual presentation. , 2007, Journal of neurophysiology.

[89]  Mark A. McComb A Practical Guide to Heavy Tails , 2000, Technometrics.

[90]  C. Klüppelberg,et al.  Modelling Extremal Events , 1997 .

[91]  M. Taqqu,et al.  Stable Non-Gaussian Random Processes : Stochastic Models with Infinite Variance , 1995 .

[92]  R. Desimone,et al.  Selectivity and sparseness in the responses of striate complex cells , 2005, Vision Research.

[93]  B. Mandelbrot The Variation of Certain Speculative Prices , 1963 .

[94]  M. A. Smith,et al.  Spatial and Temporal Scales of Neuronal Correlation in Primary Visual Cortex , 2008, The Journal of Neuroscience.