Emergence of Binocular Disparity Selectivity through Hebbian Learning

Neural selectivity in the early visual cortex strongly reflects the statistics of our environment (Barlow, 2001; Geisler, 2008). Although this has been described extensively in literature through various encoding hypotheses (Barlow and Földiák, 1989; Atick and Redlich, 1992; Olshausen and Field, 1996), an explanation as to how the cortex might develop the computational architecture to support these encoding schemes remains elusive. Here, using the more realistic example of binocular vision as opposed to monocular luminance-field images, we show how a simple Hebbian coincidence-detector is capable of accounting for the emergence of binocular, disparity selective, receptive fields. We propose a model based on spike timing-dependent plasticity, which not only converges to realistic single-cell and population characteristics, but also demonstrates how known biases in natural statistics may influence population encoding and downstream correlates of behavior. Furthermore, we show that the receptive fields we obtain are closer in structure to electrophysiological data reported in macaques than those predicted by normative encoding schemes (Ringach, 2002). We also demonstrate the robustness of our model to the input dataset, noise at various processing stages, and internal parameter variation. Together, our modeling results suggest that Hebbian coincidence detection is an important computational principle and could provide a biologically plausible mechanism for the emergence of selectivity to natural statistics in the early sensory cortex. SIGNIFICANCE STATEMENT Neural selectivity in the early visual cortex is often explained through encoding schemes that postulate that the computational aim of early sensory processing is to use the least possible resources (neurons, energy) to code the most informative features of the stimulus (information efficiency). In this article, using stereo images of natural scenes, we demonstrate how a simple Hebbian rule can lead to the emergence of a disparity-selective neural population that not only shows realistic single-cell and population tunings, but also demonstrates how known biases in natural statistics may influence population encoding and downstream correlates of behavior. Our approach allows us to view early neural selectivity, not as an optimization problem, but as an emergent property driven by biological rules of plasticity.

[1]  W. Singer,et al.  Integrator or coincidence detector? The role of the cortical neuron revisited , 1996, Trends in Neurosciences.

[2]  D. Ringach Spatial structure and symmetry of simple-cell receptive fields in macaque primary visual cortex. , 2002, Journal of neurophysiology.

[3]  Paul B. Manis,et al.  STDP in the Developing Sensory Neocortex , 2010, Front. Syn. Neurosci..

[4]  L. P. O'Keefe,et al.  Neuronal Correlates of Amblyopia in the Visual Cortex of Macaque Monkeys with Experimental Strabismus and Anisometropia , 1998, The Journal of Neuroscience.

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

[6]  J. P. Jones,et al.  An evaluation of the two-dimensional Gabor filter model of simple receptive fields in cat striate cortex. , 1987, Journal of neurophysiology.

[7]  RussLL L. Ds Vnlos,et al.  SPATIAL FREQUENCY SELECTIVITY OF CELLS IN MACAQUE VISUAL CORTEX , 2022 .

[8]  I. Ohzawa,et al.  The binocular organization of simple cells in the cat's visual cortex. , 1986, Journal of neurophysiology.

[9]  Karen R Dobkins,et al.  The face inversion effect in infants is driven by high, and not low, spatial frequencies. , 2014, Journal of vision.

[10]  D. Fitzpatrick,et al.  The development of direction selectivity in ferret visual cortex requires early visual experience , 2006, Nature Neuroscience.

[11]  D. Butts Retinal Waves: Implications for Synaptic Learning Rules during Development , 2002, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[12]  Dale Purves,et al.  Range image statistics can explain the anomalous perception of length , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Y. Chino,et al.  Postnatal Development of Binocular Disparity Sensitivity in Neurons of the Primate Visual Cortex , 1997, The Journal of Neuroscience.

[14]  H. Komatsu,et al.  Image statistics underlying natural texture selectivity of neurons in macaque V4 , 2014, Proceedings of the National Academy of Sciences.

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

[16]  Paul B Hibbard,et al.  Distribution of independent components of binocular natural images. , 2015, Journal of vision.

[17]  G. Stanley Reading and writing the neural code , 2013, Nature Neuroscience.

[18]  Haim Sompolinsky,et al.  Learning Input Correlations through Nonlinear Temporally Asymmetric Hebbian Plasticity , 2003, The Journal of Neuroscience.

[19]  Peter Földiák,et al.  Adaptation and decorrelation in the cortex , 1989 .

[20]  A. Parker,et al.  Range and mechanism of encoding of horizontal disparity in macaque V1. , 2002, Journal of neurophysiology.

[21]  C. Shatz,et al.  A Burst-Based “Hebbian” Learning Rule at Retinogeniculate Synapses Links Retinal Waves to Activity-Dependent Refinement , 2007, PLoS biology.

[22]  Jean-Baptiste Durand,et al.  Neural bases of stereopsis across visual field of the alert macaque monkey. , 2007, Cerebral cortex.

[23]  Arnaud Delorme,et al.  Networks of integrate-and-fire neurons using Rank Order Coding B: Spike timing dependent plasticity and emergence of orientation selectivity , 2001, Neurocomputing.

[24]  Christopher W Tyler,et al.  Recurrent Connectivity Can Account for the Dynamics of Disparity Processing in V1 , 2013, The Journal of Neuroscience.

[25]  Jeffrey S. Perry,et al.  Contour statistics in natural images: Grouping across occlusions , 2009, Visual Neuroscience.

[26]  D. Hubel,et al.  Ordered arrangement of orientation columns in monkeys lacking visual experience , 1974, The Journal of comparative neurology.

[27]  Robert A. Frazor,et al.  Visual cortex neurons of monkeys and cats: temporal dynamics of the contrast response function. , 2002, Journal of neurophysiology.

[28]  J A Movshon,et al.  Effects of early unilateral blur on the macaque's visual system. I. Behavioral observations , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  I. Ohzawa,et al.  Neural mechanisms for processing binocular information I. Simple cells. , 1999, Journal of neurophysiology.

[30]  B. Richmond,et al.  Latency: another potential code for feature binding in striate cortex. , 1996, Journal of neurophysiology.

[31]  Merav Ahissar,et al.  Assessing the applied benefits of perceptual training: Lessons from studies of training working-memory. , 2015, Journal of vision.

[32]  Eero P. Simoncelli,et al.  Cardinal rules: Visual orientation perception reflects knowledge of environmental statistics , 2011, Nature Neuroscience.

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

[34]  Michael S. Lewicki,et al.  Emergence of complex cell properties by learning to generalize in natural scenes , 2009, Nature.

[35]  Timothée Masquelier,et al.  Unsupervised Learning of Visual Features through Spike Timing Dependent Plasticity , 2007, PLoS Comput. Biol..

[36]  D. G. Albrecht,et al.  Spatial frequency selectivity of cells in macaque visual cortex , 1982, Vision Research.

[37]  Keiji Tanaka Organization of geniculate inputs to visual cortical cells in the cat , 1985, Vision Research.

[38]  Shiping Zhu,et al.  Neurons in parafoveal areas V1 and V2 encode vertical and horizontal disparities. , 2002, Journal of neurophysiology.

[39]  Emily A. Cooper,et al.  Perceived Depth in Natural Images Reflects Encoding of Low-Level Luminance Statistics , 2014, The Journal of Neuroscience.

[40]  D. O'Leary,et al.  Molecular gradients and development of retinotopic maps. , 2005, Annual review of neuroscience.

[41]  H. B. Barlow,et al.  Possible Principles Underlying the Transformations of Sensory Messages , 2012 .

[42]  Tim Gollisch,et al.  Rapid Neural Coding in the Retina with Relative Spike Latencies , 2008, Science.

[43]  C. Furmanski,et al.  An oblique effect in human primary visual cortex , 2000, Nature Neuroscience.

[44]  W. Geisler,et al.  Constrained sampling experiments reveal principles of detection in natural scenes , 2017, Proceedings of the National Academy of Sciences.

[45]  Timothée Masquelier,et al.  Learning to recognize objects using waves of spikes and Spike Timing-Dependent Plasticity , 2010, The 2010 International Joint Conference on Neural Networks (IJCNN).

[46]  Joseph J. Atick,et al.  What Does the Retina Know about Natural Scenes? , 1992, Neural Computation.

[47]  P. Dayan,et al.  A correlational model for the development of disparity selectivity in visual cortex that depends on prenatal and postnatal phases. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[48]  D. Ferster,et al.  An intracellular analysis of geniculo‐cortical connectivity in area 17 of the cat. , 1983, The Journal of physiology.

[49]  S. Thorpe,et al.  Dynamics of orientation coding in area V1 of the awake primate , 1993, Visual Neuroscience.

[50]  B. C. Motter,et al.  Responses of neurons in visual cortex (V1 and V2) of the alert macaque to dynamic random-dot stereograms , 1985, Vision Research.

[51]  G C DeAngelis,et al.  The physiology of stereopsis. , 2001, Annual review of neuroscience.

[52]  Bruce G Cumming,et al.  Ocular dominance predicts neither strength nor class of disparity selectivity with random-dot stimuli in primate V1. , 2004, Journal of neurophysiology.

[53]  Oren Shriki,et al.  Fast Coding of Orientation in Primary Visual Cortex , 2012, PLoS Comput. Biol..

[54]  Wolfgang Maass,et al.  On the Computational Power of Winner-Take-All , 2000, Neural Computation.

[55]  A. Parker,et al.  Quantitative analysis of the responses of V1 neurons to horizontal disparity in dynamic random-dot stereograms. , 2002, Journal of neurophysiology.

[56]  Johannes Burge,et al.  Accuracy Maximization Analysis for Sensory-Perceptual Tasks: Computational Improvements, Filter Robustness, and Coding Advantages for Scaled Additive Noise , 2017, PLoS Comput. Biol..

[57]  I. Ohzawa,et al.  The binocular organization of complex cells in the cat's visual cortex. , 1986, Journal of neurophysiology.

[58]  W. Geisler Visual perception and the statistical properties of natural scenes. , 2008, Annual review of psychology.

[59]  Wilson S. Geisler,et al.  Optimal speed estimation in natural image movies predicts human performance , 2015, Nature Communications.

[60]  Timothée Masquelier,et al.  Relative spike time coding and STDP-based orientation selectivity in the early visual system in natural continuous and saccadic vision: a computational model , 2011, Journal of Computational Neuroscience.

[61]  Arnaud Delorme,et al.  Spike-based strategies for rapid processing , 2001, Neural Networks.

[62]  Bruce G. Cumming,et al.  A Single Mechanism Can Account for Human Perception of Depth in Mixed Correlation Random Dot Stereograms , 2016, PLoS Comput. Biol..

[63]  Paul R. Martin,et al.  Extraclassical Receptive Field Properties of Parvocellular, Magnocellular, and Koniocellular Cells in the Primate Lateral Geniculate Nucleus , 2002, The Journal of Neuroscience.

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

[65]  Sieu K. Khuu,et al.  Spatial summation across the central visual field: implications for visual field testing. , 2015, Journal of vision.

[66]  G. Bi,et al.  Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type , 1998, The Journal of Neuroscience.

[67]  Romain Brette,et al.  Computing with Neural Synchrony , 2012, PLoS Comput. Biol..

[68]  Timothée Masquelier,et al.  STDP Allows Close-to-Optimal Spatiotemporal Spike Pattern Detection by Single Coincidence Detector Neurons , 2016, Neuroscience.

[69]  R D Freeman,et al.  Development of binocular vision in the kitten's striate cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[70]  Bruce G Cumming,et al.  A simple model accounts for the response of disparity-tuned V1 neurons to anticorrelated images , 2002, Visual Neuroscience.

[71]  Jason M Samonds,et al.  Relative luminance and binocular disparity preferences are correlated in macaque primary visual cortex, matching natural scene statistics , 2012, Proceedings of the National Academy of Sciences.

[72]  H. Barlow The exploitation of regularities in the environment by the brain. , 2001, The Behavioral and brain sciences.

[73]  I. Ohzawa,et al.  Encoding of binocular disparity by complex cells in the cat's visual cortex. , 1996, Journal of neurophysiology.

[74]  W. Geisler,et al.  Optimal disparity estimation in natural stereo images. , 2014, Journal of vision.

[75]  A. Welchman,et al.  “What Not” Detectors Help the Brain See in Depth , 2017, Current Biology.

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

[77]  Roger B. H. Tootell,et al.  Visual field biases for near and far stimuli in disparity selective columns in human visual cortex , 2016, NeuroImage.

[78]  Bevil R. Conway,et al.  Receptive Fields of Disparity-Tuned Simple Cells in Macaque V1 , 2003, Neuron.

[79]  Emily A. Cooper,et al.  Stereopsis is adaptive for the natural environment , 2015, Science Advances.

[80]  Paul B Hibbard,et al.  Stereoscopic correspondence for ambiguous targets is affected by elevation and fixation distance. , 2005, Spatial vision.

[81]  P O Hoyer,et al.  Independent component analysis applied to feature extraction from colour and stereo images , 2000, Network.

[82]  M. Webster,et al.  Adaptation and the color statistics of natural images , 1997, Vision Research.

[83]  Earl L. Smith,et al.  Early Monocular Defocus Disrupts the Normal Development of Receptive-Field Structure in V2 Neurons of Macaque Monkeys , 2014, The Journal of Neuroscience.