A reevaluation of achromatic spatio-temporal vision: Nonoriented filters are monocular, they adapt, and can be used for decision making at high flicker speeds

Masking, adaptation, and summation paradigms have been used to investigate the characteristics of early spatio-temporal vision. Each has been taken to provide evidence for (i) oriented and (ii) nonoriented spatial-filtering mechanisms. However, subsequent findings suggest that the evidence for nonoriented mechanisms has been misinterpreted: those experiments might have revealed the characteristics of suppression (eg, gain control), not excitation, or merely the isotropic subunits of the oriented detecting mechanisms. To shed light on this, we used all three paradigms to focus on the ‘high-speed’ corner of spatio-temporal vision (low spatial frequency, high temporal frequency), where cross-oriented achromatic effects are greatest. We used flickering Gabor patches as targets and a 2IFC procedure for monocular, binocular, and dichoptic stimulus presentations. To account for our results, we devised a simple model involving an isotropic monocular filter-stage feeding orientation-tuned binocular filters. Both filter stages are adaptable, and their outputs are available to the decision stage following nonlinear contrast transduction. However, the monocular isotropic filters (i) adapt only to high-speed stimuli—consistent with a magnocellular subcortical substrate—and (ii) benefit decision making only for high-speed stimuli (ie, isotropic monocular outputs are available only for high-speed stimuli). According to this model, the visual processes revealed by masking, adaptation, and summation are related but not identical.

[1]  J. Ross,et al.  Contrast adaptation and contrast masking in human vision , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[2]  Ralph D Freeman,et al.  Spatial frequency-specific contrast adaptation originates in the primary visual cortex. , 2007, Journal of neurophysiology.

[3]  Sarah L. Elliott,et al.  Response normalization and blur adaptation: data and multi-scale model. , 2011, Journal of vision.

[4]  T. Meese Spatially extensive summation of contrast energy is revealed by contrast detection of micro-pattern textures. , 2010, Journal of vision.

[5]  T. Meese,et al.  Spatial and temporal dependencies of cross-orientation suppression in human vision , 2007, Proceedings of the Royal Society B: Biological Sciences.

[6]  C. A. Burbeck,et al.  Contrast gain measurements and the transient/sustained. , 1981, Journal of the Optical Society of America.

[7]  Jose-Manuel Alonso,et al.  Functionally distinct inhibitory neurons at the first stage of visual cortical processing , 2003, Nature Neuroscience.

[8]  G. Blasdel,et al.  Physiological organization of layer 4 in macaque striate cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  Robert J Summers,et al.  Neuronal convergence in early contrast vision: binocular summation is followed by response nonlinearity and area summation. , 2009, Journal of vision.

[10]  David F. Nichols,et al.  Effect of transient versus sustained activation on interocular suppression , 2009, Vision Research.

[11]  A. B. Bonds Role of Inhibition in the Specification of Orientation Selectivity of Cells in the Cat Striate Cortex , 1989, Visual Neuroscience.

[12]  John H. R. Maunsell,et al.  How parallel are the primate visual pathways? , 1993, Annual review of neuroscience.

[13]  Felix Wichmann,et al.  The psychometric function: II. Bootstrap-based confidence intervals and sampling , 2001, Perception & psychophysics.

[14]  Heidi S. Fisher,et al.  Adaptation from invisible flicker. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Kirsten L. Challinor,et al.  A common contrast pooling rule for suppression within and between the eyes , 2008, Visual Neuroscience.

[16]  Tim S. Meese,et al.  Interocular suppression is gated by interocular feature matching , 2005, Vision Research.

[17]  Robert J. Snowden,et al.  Orientation bandwidth: The effect of spatial and temporal frequency , 1992, Vision Research.

[18]  I. Ohzawa,et al.  Binocular cross-orientation suppression in the cat's striate cortex. , 1998, Journal of neurophysiology.

[19]  C. A. Burbeck,et al.  Further evidence for a broadband, isotropic mechanism sensitive to high-velocity stimuli , 1987, Vision Research.

[20]  A. Freeman,et al.  Cross-orientation interactions in human vision. , 2008, Journal of vision.

[21]  Vincent P. Ferrera,et al.  Spatial frequency tuning of transient non-oriented units , 1985, Vision Research.

[22]  I. Ohzawa,et al.  Contrast gain control in the cat's visual system. , 1985, Journal of neurophysiology.

[23]  Amiram Grinvald,et al.  Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns , 1991, Nature.

[24]  D. Hubel,et al.  Projection into the visual field of ocular dominance columns in macaque monkey , 1977, Brain Research.

[25]  Bernice E. Rogowitz,et al.  Human Vision and Electronic Imaging II , 1997 .

[26]  John Ross,et al.  The effects of adaptation and masking on incremental thresholds for contrast , 1993, Vision Research.

[27]  R. Freeman,et al.  Cross-orientation suppression: monoptic and dichoptic mechanisms are different. , 2005, Journal of neurophysiology.

[28]  Robert A. Frazor,et al.  Independence of luminance and contrast in natural scenes and in the early visual system , 2005, Nature Neuroscience.

[29]  F A Wichmann,et al.  Contrast discrimination with sinusoidal gratings of different spatial frequency. , 2002, Journal of the Optical Society of America. A, Optics, image science, and vision.

[30]  T. Meese,et al.  Grating and plaid masks indicate linear summation in a contrast gain pool. , 2004, Journal of vision.

[31]  E. Essock,et al.  Contrast sensitivity for oriented patterns in 1/f noise: contrast response and the horizontal effect. , 2010, Journal of vision.

[32]  T. Meese,et al.  Binocular contrast interactions: Dichoptic masking is not a single process , 2007, Vision Research.

[33]  H. Wilson,et al.  Orientation bandwidths of spatial mechanisms measured by masking. , 1984, Journal of the Optical Society of America. A, Optics and image science.

[34]  Stanley A. Klein,et al.  Seven models of masking , 1997, Electronic Imaging.

[35]  M. Carandini,et al.  The Suppressive Field of Neurons in Lateral Geniculate Nucleus , 2005, The Journal of Neuroscience.

[36]  C. Blakemore,et al.  Interocular suppression in the primary visual cortex: a possible neural basis of binocular rivalry , 1995, Vision Research.

[37]  T. Meese Area summation and masking. , 2004, Journal of vision.

[38]  M. Carandini,et al.  Masking by fast gratings. , 2002, Journal of vision.

[39]  T. Meese,et al.  Psychophysical evidence for two routes to suppression before binocular summation of signals in human vision , 2007, Neuroscience.

[40]  J. M. Foley,et al.  Contrast detection and near-threshold discrimination in human vision , 1981, Vision Research.

[41]  J. P. Thomas,et al.  Neural recoding in human pattern vision: model and mechanisms , 1999, Vision Research.

[42]  H. Wilson,et al.  Spatial frequency tuning of orientation selective units estimated by oblique masking , 1983, Vision Research.

[43]  T. Meese,et al.  Orientation masking and cross-orientation suppression (XOS): implications for estimates of filter bandwidth. , 2010, Journal of vision.

[44]  D. Tolhurst,et al.  The analysis of the drift rate of moving sinusoidal gratings. , 1973, Vision research.

[45]  D. Alais,et al.  Orientation bandwidths are invariant across spatiotemporal frequency after isotropic components are removed. , 2009, Journal of vision.

[46]  Ralph D Freeman,et al.  Contrast sensitivity is enhanced by expansive nonlinear processing in the lateral geniculate nucleus. , 2008, Journal of neurophysiology.

[47]  D. Burr,et al.  Functional implications of cross-orientation inhibition of cortical visual cells. I. Neurophysiological evidence , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[48]  J. M. Foley,et al.  Contrast masking in human vision. , 1980, Journal of the Optical Society of America.

[49]  R. Hess,et al.  Low spatial frequencies are suppressively masked across spatial scale, orientation, field position, and eye of origin. , 2004, Journal of vision.

[50]  M. Georgeson,et al.  Shading and texture: separate information channels with a common adaptation mechanism? , 2002, Spatial vision.

[51]  J. Kulikowski,et al.  Orientational selectivity of grating and line detectors in human vision. , 1973, Vision research.

[52]  Michael W. Spratling A single functional model accounts for the distinct properties of suppression in cortical area V1 , 2011, Vision Research.

[53]  R. Shiffrin,et al.  Frank J. Restle: In memoriam. , 1981 .

[54]  Kirsten L. Challinor,et al.  Remote facilitation in the Fourier domain , 2007, Vision Research.

[55]  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.

[56]  P. Bex,et al.  Contrast adaptation implies two spatiotemporal channels but three adapting processes. , 2007, Journal of experimental psychology. Human perception and performance.

[57]  T. Meese,et al.  Contrast summation across eyes and space is revealed along the entire dipper function by a "Swiss cheese" stimulus. , 2011, Journal of vision.

[58]  F. Sengpiel,et al.  Intracortical Origins of Interocular Suppression in the Visual Cortex , 2005, The Journal of Neuroscience.

[59]  Viola S. Störmer,et al.  Feature-based interference from unattended visual field during attentional tracking in younger and older adults. , 2011, Journal of vision.

[60]  M. Georgeson,et al.  Perceived contrast of gratings and plaids: Non-linear summation across oriented filters , 1994, Vision Research.

[61]  John M. Foley,et al.  Analysis of the effect of pattern adaptation on pattern pedestal effects: A two-process model , 1997, Vision Research.

[62]  George Sperling,et al.  A gain-control theory of binocular combination. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[65]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[66]  David Fitzpatrick,et al.  A morphological basis for orientation tuning in primary visual cortex , 2004, Nature Neuroscience.

[67]  D. Heeger,et al.  Inter-ocular contrast normalization in human visual cortex. , 2009, Journal of vision.

[68]  R. Shapley,et al.  The effect of contrast on the transfer properties of cat retinal ganglion cells. , 1978, The Journal of physiology.

[69]  C. Tyler,et al.  Signal detection theory in the 2AFC paradigm: attention, channel uncertainty and probability summation , 2000, Vision Research.

[70]  T. Meese,et al.  Cross-orientation masking is speed invariant between ocular pathways but speed dependent within them. , 2009, Journal of vision.

[71]  P. Lennie,et al.  Profound Contrast Adaptation Early in the Visual Pathway , 2004, Neuron.

[72]  C Blakemore,et al.  On the existence of neurones in the human visual system selectively sensitive to the orientation and size of retinal images , 1969, The Journal of physiology.

[73]  P. Lennie,et al.  Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

[74]  B. Dreher,et al.  Relationship between contrast adaptation and orientation tuning in V1 and V2 of cat visual cortex. , 2006, Journal of neurophysiology.

[75]  P. Lennie,et al.  Pattern-selective adaptation in visual cortical neurones , 1979, Nature.

[76]  J. M. Foley,et al.  Human luminance pattern-vision mechanisms: masking experiments require a new model. , 1994, Journal of the Optical Society of America. A, Optics, image science, and vision.

[77]  H R Wilson,et al.  Further evidence for four mechanisms mediating vision at threshold: sensitivities to complex gratings and aperiodic stimuli. , 1979, Journal of the Optical Society of America.

[78]  T. Meese,et al.  The influence of fixation points on contrast detection and discrimination of patches of grating: Masking and facilitation , 2009, Vision Research.

[79]  D. G. Albrecht,et al.  Motion selectivity and the contrast-response function of simple cells in the visual cortex , 1991, Visual Neuroscience.

[80]  F A Wichmann,et al.  Ning for Helpful Comments and Suggestions. This Paper Benefited Con- Siderably from Conscientious Peer Review, and We Thank Our Reviewers the Psychometric Function: I. Fitting, Sampling, and Goodness of Fit , 2001 .

[81]  M. Georgeson,et al.  Binocular contrast vision at and above threshold. , 2006, Journal of vision.