Radial-tangential anisotropy of crowding in the early visual areas.

Crowding, the inability to recognize an individual object in clutter (Bouma H. Nature 226: 177-178, 1970), is considered a major impediment to object recognition in peripheral vision. Despite its significance, the cortical loci of crowding are not well understood. In particular, the role of the primary visual cortex (V1) remains unclear. Here we utilize a diagnostic feature of crowding to identify the earliest cortical locus of crowding. Controlling for other factors, radially arranged flankers induce more crowding than tangentially arranged ones (Toet A, Levi DM. Vision Res 32: 1349-1357, 1992). We used functional magnetic resonance imaging (fMRI) to measure the change in mean blood oxygenation level-dependent (BOLD) response due to the addition of a middle letter between a pair of radially or tangentially arranged flankers. Consistent with the previous finding that crowding is associated with a reduced BOLD response [Millin R, Arman AC, Chung ST, Tjan BS. Cereb Cortex (July 5, 2013). doi:10.1093/cercor/bht159], we found that the BOLD signal evoked by the middle letter depended on the arrangement of the flankers: less BOLD response was associated with adding the middle letter between radially arranged flankers compared with adding it between tangentially arranged flankers. This anisotropy in BOLD response was present as early as V1 and remained significant in downstream areas. The effect was observed while subjects' attention was diverted away from the testing stimuli. Contrast detection threshold for the middle letter was unaffected by flanker arrangement, ruling out surround suppression of contrast response as a major factor in the observed BOLD anisotropy. Our findings support the view that V1 contributes to crowding.

[1]  S. Klein,et al.  Suppressive and facilitatory spatial interactions in peripheral vision: peripheral crowding is neither size invariant nor simple contrast masking. , 2002, Journal of vision.

[2]  G. B. Wetherill,et al.  SEQUENTIAL ESTIMATION OF POINTS ON A PSYCHOMETRIC FUNCTION. , 1965, The British journal of mathematical and statistical psychology.

[3]  Zoe Kourtzi,et al.  Uncertainty and invariance in the human visual cortex. , 2006, Journal of neurophysiology.

[4]  J A Solomon,et al.  Texture interactions determine perceived contrast , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[5]  H. Wilson,et al.  Lateral interactions in peripherally viewed texture arrays. , 1997, Journal of the Optical Society of America. A, Optics, image science, and vision.

[6]  Tom C. Freeman,et al.  Pursuit eye-movements disambiguate depth order in an ambiguous motion display , 2010 .

[7]  D. Pelli,et al.  Crowding is unlike ordinary masking: distinguishing feature integration from detection. , 2004, Journal of vision.

[8]  B. C. Motter.  Central V4 Receptive Fields Are Scaled by the V1 Cortical Magnification and Correspond to a Constant-Sized Sampling of the V1 Surface , 2009, The Journal of Neuroscience.

[9]  Taiyong Bi,et al.  The effect of crowding on orientation-selective adaptation in human early visual cortex. , 2009, Journal of vision.

[10]  Jeremy Freeman,et al.  Inter-area correlations in the ventral visual pathway reflect feature integration. , 2010, Journal of vision.

[11]  J W Belliveau,et al.  Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. , 1995, Science.

[12]  S. McKee,et al.  The effect of spatial configuration on surround suppression of contrast sensitivity. , 2006, Journal of vision.

[13]  D. Pelli.  Crowding: a cortical constraint on object recognition , 2008, Current Opinion in Neurobiology.

[14]  Matteo Carandini,et al.  Thalamic filtering of retinal spike trains by postsynaptic summation. , 2007, Journal of vision.

[15]  G. Wolford,et al.  Lateral masking vertically and horizontally , 1983 .

[16]  D. Heeger,et al.  Center-surround interactions in foveal and peripheral vision , 2000, Vision Research.

[17]  Craig K. Abbey,et al.  Information distribution for face identificaiton and its relation to human strategies , 2010 .

[18]  Anirvan S. Nandy,et al.  Saccade-confounded image statistics explain visual crowding , 2012, Nature Neuroscience.

[19]  A. Watson,et al.  Quest: A Bayesian adaptive psychometric method , 1983, Perception & psychophysics.

[20]  Yury Petrov,et al.  Asymmetries and idiosyncratic hot spots in crowding , 2011, Vision Research.

[21]  H. Bouma.  Visual interference in the parafoveal recognition of initial and final letters of words. , 1973, Vision research.

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

[23]  S. Klein,et al.  Vernier acuity, crowding and cortical magnification , 1985, Vision Research.

[24]  Jean Bennett,et al.  Lateral Connectivity and Contextual Interactions in Macaque Primary Visual Cortex , 2002, Neuron.

[25]  Michael H. Herzog,et al.  Neural correlates of visual crowding , 2014, NeuroImage.

[26]  Leslie G. Ungerleider,et al.  Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI. , 1998, Science.

[27]  Eero P. Simoncelli,et al.  Metamers of the ventral stream , 2011, Nature Neuroscience.

[28]  S. Dakin,et al.  Context influences contour integration. , 2009, Journal of vision.

[29]  J. Lund,et al.  Compulsory averaging of crowded orientation signals in human vision , 2001, Nature Neuroscience.

[30]  B. C. Motter,et al.  Modulation of Transient and Sustained Response Components of V4 Neurons by Temporal Crowding in Flashed Stimulus Sequences , 2006, The Journal of Neuroscience.

[31]  Denis G. Pelli,et al.  Substitution and pooling in crowding , 2011, Attention, perception & psychophysics.

[32]  B. C. Motter,et al.  The roles of cortical image separation and size in active visual search performance. , 2007, Journal of vision.

[33]  Ariella V. Popple,et al.  Crowding and surround suppression: not to be confused. , 2007, Journal of vision.

[34]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[35]  P. Cavanagh,et al.  Attentional resolution and the locus of visual awareness , 1996, Nature.

[36]  D. Levi.  Crowding—An essential bottleneck for object recognition: A mini-review , 2008, Vision Research.

[37]  Rachel Millin,et al.  Visual crowding in V1. , 2014, Cerebral cortex.

[38]  C. Gilbert.  Horizontal integration and cortical dynamics , 1992, Neuron.

[39]  D. Pelli,et al.  Crowding is unlike ordinary masking : Distinguishing feature detection and integration , 2001 .

[40]  Susana T. L. Chung.  Cortical Reorganization after Long-Term Adaptation to Retinal Lesions in Humans , 2013, The Journal of Neuroscience.

[41]  Brad C. Motter.  Crowding and object integration within the receptive field of V4 neurons , 2010 .

[42]  Tracey D. Berger,et al.  Crowding and eccentricity determine reading rate. , 2007, Journal of vision.

[43]  David J Heeger,et al.  Response Suppression in V1 Agrees with Psychophysics of Surround Masking , 2003, The Journal of Neuroscience.

[44]  Elaine J. Anderson,et al.  The Neural Correlates of Crowding-Induced Changes in Appearance , 2011, Current Biology.

[45]  R F Hess,et al.  Contour interaction in fovea and periphery. , 2000, Journal of the Optical Society of America. A, Optics, image science, and vision.

[46]  Sheng He,et al.  Reduction of the Crowding Effect in Spatially Adjacent but Cortically Remote Visual Stimuli , 2009, Current Biology.

[47]  Anirvan S. Nandy,et al.  The nature of letter crowding as revealed by first- and second-order classification images. , 2007, Journal of Vision.

[48]  D. Knill,et al.  The role of memory in visually guided reaching. , 2007, Journal of vision.

[49]  L. Maffei,et al.  The unresponsive regions of visual cortical receptive fields , 1976, Vision Research.

[50]  Dennis M. Levi,et al.  Long-range dichoptic interactions in the human visual cortex in the region corresponding to the blind spot , 1994, Vision Research.

[51]  R. Rosenholtz,et al.  A summary-statistic representation in peripheral vision explains visual crowding. , 2009, Journal of vision.

[52]  D. Levi,et al.  The two-dimensional shape of spatial interaction zones in the parafovea , 1992, Vision Research.

[53]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[54]  Dennis M. Levi,et al.  Vernier acuity, crowding and amblyopia , 1985, Vision Research.

[55]  Zhong-Lin Lu,et al.  Generating high gray-level resolution monochrome displays with conventional computer graphics cards and color monitors , 2003, Journal of Neuroscience Methods.

[56]  L. Shah,et al.  Functional magnetic resonance imaging. , 2010, Seminars in roentgenology.

[57]  H. BOUMA,et al.  Interaction Effects in Parafoveal Letter Recognition , 1970, Nature.

[58]  Philippe Lefèvre,et al.  A dynamic representation of target motion drives predictive smooth pursuit during target blanking. , 2008, Journal of vision.

[59]  D. Levi,et al.  The effect of similarity and duration on spatial interaction in peripheral vision. , 1994, Spatial vision.

[60]  Yingchen He,et al.  Attention-Dependent Early Cortical Suppression Contributes to Crowding , 2014, The Journal of Neuroscience.

[61]  D. Levi,et al.  Visual crowding: a fundamental limit on conscious perception and object recognition , 2011, Trends in Cognitive Sciences.

[62]  M. Masson,et al.  Using confidence intervals in within-subject designs , 1994, Psychonomic bulletin & review.

[63]  Fang Fang,et al.  Crowding alters the spatial distribution of attention modulation in human primary visual cortex. , 2008, Journal of vision.

[64]  Bas Rokers,et al.  Strong percepts of motion through depth without strong percepts of position in depth. , 2008, Journal of vision.

[65]  Wim Vanduffel,et al.  The Radial Bias: A Different Slant on Visual Orientation Sensitivity in Human and Nonhuman Primates , 2006, Neuron.

[66]  Jeremy Freeman,et al.  Orientation Decoding Depends on Maps, Not Columns , 2011, The Journal of Neuroscience.

[67]  G. Rhodes,et al.  Sex-specific norms code face identity. , 2011, Journal of vision.

[68]  G. Glover,et al.  Retinotopic organization in human visual cortex and the spatial precision of functional MRI. , 1997, Cerebral cortex.

[69]  Susana T. L. Chung,et al.  Visual Crowding in V 1 , 2014 .

[70]  David Whitney,et al.  Holistic crowding of Mooney faces. , 2009, Journal of vision.

[71]  Jos B. T. M. Roerdink,et al.  A Neurophysiologically Plausible Population Code Model for Feature Integration Explains Visual Crowding , 2010, PLoS Comput. Biol..