Neural Model of Coding Stimulus Orientation and Adaptation

The coding of line orientation in the visual system has been investigated extensively. During the prolonged viewing of a stimulus, the perceived orientation continuously changes (normalization effect). Also, the orientation of the adapting stimulus and the background stimuli influence the perceived orientation of the subsequently displayed stimulus: tilt after-effect (TAE) or tilt illusion (TI). The neural mechanisms of these effects are not fully understood. The proposed model includes many local analyzers, each consisting of two sets of neurons. The first set has two independent cardinal detectors (CDs), whose responses depend on stimulus orientation. The second set has many orientation detectors (OD) tuned to different orientations of the stimulus. The ODs sum up the responses of the two CDs with respective weightings and output a preferred orientation depending on the ratio of CD responses. It is suggested that during prolonged viewing, the responses of the CDs decrease: the greater the excitation of the detector, the more rapid the decrease in its response. Thereby, the ratio of CD responses changes during the adaptation, causing the normalization effect and the TAE. The CDs of the different local analyzers laterally inhibit each other and cause the TI. We show that the properties of this model are consistent with both psychophysical and neurophysiological findings related to the properties of orientation perception, and we investigate how these mechanisms can affect the orientation's sensitivity.

[1]  D. Foster,et al.  Horizontal—vertical filters in early vision predict anomalous line-orientation identification frequencies , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[2]  D. Samuel Schwarzkopf,et al.  Effective Connectivity within Human Primary Visual Cortex Predicts Interindividual Diversity in Illusory Perception , 2013, The Journal of Neuroscience.

[3]  H. Sompolinsky,et al.  Theory of orientation tuning in visual cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Matteo Carandini,et al.  Cascaded Effects of Spatial Adaptation in the Early Visual System , 2014, Neuron.

[5]  F. Campbell,et al.  The tilt after-effect: a fresh look. , 1971, Vision research.

[6]  M. Sur,et al.  Adaptation-Induced Plasticity of Orientation Tuning in Adult Visual Cortex , 2000, Neuron.

[7]  Haim Sompolinsky,et al.  New perspectives on the mechanisms for orientation , 1997 .

[8]  E. Miller,et al.  Dynamics of neuronal sensitivity in visual cortex and local feature discrimination , 2002, Nature Neuroscience.

[9]  C. Koch,et al.  A detailed model of the primary visual pathway in the cat: comparison of afferent excitatory and intracortical inhibitory connection schemes for orientation selectivity , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  M. Sur,et al.  Dynamic properties of recurrent inhibition in primary visual cortex: contrast and orientation dependence of contextual effects. , 2000, Journal of neurophysiology.

[11]  H. Barlow Summation and inhibition in the frog's retina , 1953, The Journal of physiology.

[12]  J. Kulikowski,et al.  Influences of prolonged viewing of tilted lines on perceived line orientation: the normalization and tilt after-effect. , 2009, Journal of the Optical Society of America. A, Optics, image science, and vision.

[13]  Yang Dan,et al.  Dynamic Modification of Cortical Orientation Tuning Mediated by Recurrent Connections , 2002, Neuron.

[14]  C. Clifford,et al.  A functional angle on some after-effects in cortical vision , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[15]  Bart Krekelberg,et al.  Adaptation without Plasticity. , 2016, Cell reports.

[16]  M. Sur,et al.  Cortical Plasticity: Time For A Change , 2002, Current Biology.

[17]  W. Levick Receptive fields and trigger features of ganglion cells in the visual streak of the rabbit's retina , 1967, The Journal of physiology.

[18]  S. Lehky,et al.  Neural model of stereoacuity and depth interpolation based on a distributed representation of stereo disparity [published erratum appears in J Neurosci 1991 Mar;11(3):following Table of Contents] , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  D. Mitchell,et al.  Does the tilt after-effect occur in the oblique meridian? , 1976, Vision Research.

[20]  D. Foster,et al.  Asymmetries in oriented-line detection indicate two orthogonal filters in early vision , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[21]  J. Gibson,et al.  Journal of Experimental Psychology , 2022 .

[22]  M. Karalius,et al.  A model for the monocular line orientation analyzer , 1983, Biological Cybernetics.

[23]  R. Held Localized normalization of tilted lines. , 1963, The American journal of psychology.

[24]  Peter Wenderoth,et al.  The effects of exposure duration and surrounding frames on direct and indirect tilt aftereffects and illusions , 1989, Perception & psychophysics.

[25]  P. Lennie,et al.  Rapid adaptation in visual cortex to the structure of images. , 1999, Science.

[26]  R Sekuler,et al.  Letter: Tilt aftereffect following very brief exposures. , 1974, Vision research.

[27]  Risto Miikkulainen,et al.  Tilt Aftereffects in a Self-Organizing Model of the Primary Visual Cortex , 2000, Neural Computation.

[28]  J. Gibson,et al.  Adaptation, after-effect and contrast in the perception of tilted lines. I. Quantitative studies , 1937 .

[29]  Adam Kohn,et al.  The influence of surround suppression on adaptation effects in primary visual cortex. , 2012, Journal of neurophysiology.

[30]  M. Sur,et al.  Foci of orientation plasticity in visual cortex , 2001, Nature.

[31]  F. Campbell,et al.  Orientational selectivity of the human visual system , 1966, The Journal of physiology.

[32]  L. Ganz Mechanism of the figural aftereffects. , 1966, Psychological review.

[33]  H. Seung,et al.  Tilt aftereffect and adaptation-induced changes in orientation tuning in visual cortex. , 2005, Journal of neurophysiology.

[34]  G. Stanley,et al.  Rapid Sensory Adaptation Redux: A Circuit Perspective , 2016, Neuron.

[35]  C. Blakemore,et al.  Lateral Inhibition between Orientation Detectors in the Human Visual System , 1970, Nature.

[36]  Derek H. Arnold,et al.  Evidence for tilt normalization can be explained by anisotropic orientation sensitivity. , 2015, Journal of vision.

[37]  David H. Do,et al.  Dissociable Perceptual Effects of Visual Adaptation , 2009, PloS one.

[38]  A. Sillito The effectiveness of bicuculline as an antagonist of GABA and visually evoked inhibition in the cat's striate cortex. , 1975, The Journal of physiology.

[39]  R. Shapley,et al.  New perspectives on the mechanisms for orientation selectivity , 1997, Current Opinion in Neurobiology.

[40]  Derek H. Arnold,et al.  Face aftereffects involve local repulsion, not renormalization. , 2015, Journal of vision.

[41]  J. J. Kulikowski,et al.  The detection and recognition of two lines , 1981, Vision Research.

[42]  C. Blakemore,et al.  Lateral inhibition between orientation detectors in the cat's visual cortex , 2004, Experimental Brain Research.

[43]  Nicholas J Priebe,et al.  Mechanisms of Orientation Selectivity in the Primary Visual Cortex. , 2016, Annual review of vision science.

[44]  Levin Kuhlmann,et al.  A Computational Study of How Orientation Bias in the Lateral Geniculate Nucleus Can Give Rise to Orientation Selectivity in Primary Visual Cortex , 2011, Front. Syst. Neurosci..

[45]  Valentin Dragoi,et al.  Adaptive coding of visual information in neural populations , 2008, Nature.

[46]  Colin W G Clifford,et al.  The tilt illusion: Phenomenology and functional implications , 2014, Vision Research.

[47]  J. R. Harris,et al.  TWO DIFFERENT AFTER-EFFECTS OF EXPOSURE TO VISUAL TILTS. , 1965, The American journal of psychology.

[48]  C. Koch,et al.  Neuronal connections underlying orientation selectivity in cat visual cortex , 1987, Trends in Neurosciences.

[49]  Mark W. Greenlee,et al.  Saturation of the tilt aftereffect , 1987, Vision Research.

[50]  M. A. Smith,et al.  Neuronal Adaptation: Tired Neurons or Wired Networks? , 2017, Trends in Neurosciences.

[51]  P. Dayan,et al.  Perceptual organization in the tilt illusion. , 2009, Journal of vision.

[52]  I P Howard,et al.  Satiation and the tilt after-effect. , 1965, The American journal of psychology.

[53]  H. Wallach,et al.  Figural aftereffects; an investigation of visual processes. , 1944 .

[54]  S. Molotchnikoff,et al.  Long adaptation reveals mostly attractive shifts of orientation tuning in cat primary visual cortex , 2009, Neuroscience.

[55]  Trichur Raman Vidyasagar,et al.  Geniculate orientation biases as cartesian coordinates for cortical orientation detectors. , 1985 .

[56]  R. Freeman,et al.  Oblique effect: a neural basis in the visual cortex. , 2003, Journal of neurophysiology.

[57]  D. Hubel,et al.  Receptive fields of single neurones in the cat's striate cortex , 1959, The Journal of physiology.