Neural correlates of visual crowding

In visual crowding, target discrimination strongly deteriorates when flanking elements are added. We have recently shown that crowding cannot be explained by simple low-level interactions and that grouping is a key component instead. We presented a vernier flanked by arrays of vertical lines. When the flankers had the same lengths as the vernier, offset discrimination was strongly impaired. When longer flankers were presented, crowding was weaker. We proposed that crowding is strong when the flankers group with the target (equal length flankers). When the target segregates from the flankers, crowding is weaker (long flankers). To understand the neurophysiological mechanisms of grouping in crowding, here, we adapted the above vernier paradigm to a high-density EEG study. The P1 component reflected basic stimulus characteristics (flanker length) but not crowding. Crowding emerged slowly and manifested as a suppression of the N1 component (after 180ms). Using inverse solutions, we found that the N1 suppression was caused by reduced neural activity in high-level visual areas such as the lateral occipital cortex. Our results suggest that crowding occurs when elements are grouped into wholes, a process reflected by the N1 component.

[1]  G. Mangun,et al.  Luminance and spatial attention effects on early visual processing. , 1995, Brain research. Cognitive brain research.

[2]  I. Rentschler,et al.  Contrast thresholds for identification of numeric characters in direct and eccentric view , 1991, Perception & psychophysics.

[3]  D. Pelli,et al.  The uncrowded window of object recognition , 2008, Nature Neuroscience.

[4]  M C FLOM,et al.  Contour Interaction and Visual Resolution: Contralateral Effects , 1963, Science.

[5]  Stefan Debener,et al.  Size matters: effects of stimulus size, duration and eccentricity on the visual gamma-band response , 2004, Clinical Neurophysiology.

[6]  John J. Foxe,et al.  The Spatiotemporal Dynamics of Illusory Contour Processing: Combined High-Density Electrical Mapping, Source Analysis, and Functional Magnetic Resonance Imaging , 2002, The Journal of Neuroscience.

[7]  M. Bach,et al.  The Freiburg Visual Acuity test--automatic measurement of visual acuity. , 1996, Optometry and vision science : official publication of the American Academy of Optometry.

[8]  Marta Kutas,et al.  Mass univariate analysis of event-related brain potentials/fields II: Simulation studies. , 2011, Psychophysiology.

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

[10]  H. Huynh,et al.  Estimation of the Box Correction for Degrees of Freedom from Sample Data in Randomized Block and Split-Plot Designs , 1976 .

[11]  B. Rockstroh,et al.  Statistical control of artifacts in dense array EEG/MEG studies. , 2000, Psychophysiology.

[12]  Sieu K. Khuu,et al.  Configuration specificity of crowding in peripheral vision , 2011, Vision Research.

[13]  R Shapley,et al.  Illusory contours activate specific regions in human visual cortex: evidence from functional magnetic resonance imaging. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[14]  J. Gibson Adaptation, after-effect, and contrast in the perception of tilted lines. II. Simultaneous contrast and the areal restriction of the after-effect. , 1937 .

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

[16]  A. Dale,et al.  The Representation of Illusory and Real Contours in Human Cortical Visual Areas Revealed by Functional Magnetic Resonance Imaging , 1999, The Journal of Neuroscience.

[17]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[18]  H. Strasburger Unfocused spatial attention underlies the crowding effect in indirect form vision. , 2004, Journal of vision.

[19]  M. Murray,et al.  EEG source imaging , 2004, Clinical Neurophysiology.

[20]  Michael Bach,et al.  Electrophysiological correlates of human texture segregation, an overview , 1998, Documenta Ophthalmologica.

[21]  Gerald Westheimer,et al.  Contrast polarity, chromaticity, and stereoscopic depth modulate contextual interactions in vernier acuity. , 2008, Journal of vision.

[22]  C. Michel,et al.  Noninvasive Localization of Electromagnetic Epileptic Activity. I. Method Descriptions and Simulations , 2004, Brain Topography.

[23]  Éva M. Bankó,et al.  Dissociating the Effect of Noise on Sensory Processing and Overall Decision Difficulty , 2011, The Journal of Neuroscience.

[24]  Michael Bach,et al.  Electrophysiological correlates of texture segregation in the human visual evoked potential , 1992, Vision Research.

[25]  Yaoda Xu,et al.  Distinctive Neural Mechanisms Supporting Visual Object Individuation and Identification , 2009, Journal of Cognitive Neuroscience.

[26]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[27]  Bilge Sayim,et al.  Grouping, pooling, and when bigger is better in visual crowding. , 2012, Journal of vision.

[28]  E. Vogel,et al.  The visual N1 component as an index of a discrimination process. , 2000, Psychophysiology.

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

[30]  C. Herrmann,et al.  Gestalt perception modulates early visual processing , 2001, Neuroreport.

[31]  D. Senkowski,et al.  Effects of task difficulty on evoked gamma activity and ERPs in a visual discrimination task , 2002, Clinical Neurophysiology.

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

[33]  Andreas Bartels,et al.  Parietal Cortex Mediates Conscious Perception of Illusory Gestalt , 2013, The Journal of Neuroscience.

[34]  Clara Casco,et al.  A visual evoked potential correlate of global figure-ground segmentation , 1999, Vision Research.

[35]  M. Berkley,et al.  Evoked potentials elicited by brief vernier offsets: Estimating vernier thresholds and properties of the neural substrate , 1986, Vision Research.

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

[37]  Johan Wagemans,et al.  Context Modulates the ERP Signature of Contour Integration , 2011, PloS one.

[38]  Gerald Westheimer,et al.  Temporal and spatial interference with vernier acuity , 1975, Vision Research.

[39]  Steven C Dakin,et al.  Positional averaging explains crowding with letter-like stimuli , 2009, Proceedings of the National Academy of Sciences.

[40]  N. Kanwisher,et al.  The lateral occipital complex and its role in object recognition , 2001, Vision Research.

[41]  Dov Sagi,et al.  Configuration influence on crowding. , 2007, Journal of vision.

[42]  James T Todd,et al.  The visual identification of relational categories. , 2011, Journal of vision.

[43]  D. Pelli,et al.  The same binding in contour integration and crowding. , 2011, Journal of vision.

[44]  Dennis M. Levi,et al.  Crowding in Peripheral Vision: Why Bigger Is Better , 2009, Current Biology.

[45]  G. Westheimer,et al.  Global stimulus configuration modulates crowding. , 2009, Journal of vision.

[46]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[47]  Johan Wagemans,et al.  Emergence of Perceptual Gestalts in the Human Visual Cortex , 2011, Psychological science.

[48]  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.

[49]  Yury Petrov Locus of spatial attention determines inward - outward anisotropy in crowding , 2007 .

[50]  B. Sayim Global stimulus con fi guration modulates crowding Laboratory of Psychophysics , 2009 .

[51]  Manfred Fahle,et al.  The electrophysiological correlate of contour integration is modulated by task demands , 2006, Brain Research.

[52]  Manuel R. Mercier,et al.  Non-retinotopic feature integration decreases response-locked brain activity as revealed by electrical neuroimaging , 2009, NeuroImage.

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

[54]  P. Cavanagh,et al.  The Spatial Resolution of Visual Attention , 2001, Cognitive Psychology.

[55]  Mark W Pettet,et al.  Temporal dynamics of the human response to symmetry. , 2002, Journal of vision.

[56]  Topi Tanskanen,et al.  From local to global: Cortical dynamics of contour integration. , 2008, Journal of vision.

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

[58]  Gerald Westheimer,et al.  Grouping of contextual elements that affect vernier thresholds. , 2007, Journal of vision.

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

[60]  D. Lehmann,et al.  Reference-free identification of components of checkerboard-evoked multichannel potential fields. , 1980, Electroencephalography and clinical neurophysiology.

[61]  M. Goldberg,et al.  Neuronal Activity in the Lateral Intraparietal Area and Spatial Attention , 2003, Science.

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

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

[64]  Fang Fang,et al.  Perceptual grouping and inverse fMRI activity patterns in human visual cortex. , 2008, Journal of vision.

[65]  Marina Schmid,et al.  An Introduction To The Event Related Potential Technique , 2016 .

[66]  Christoph M. Michel,et al.  Electrical source dynamics in three functional localizer paradigms , 2010, NeuroImage.

[67]  Dennis M. Levi,et al.  Selectivity of the evoked potential for vernier offset , 1985, Vision Research.

[68]  William Prinzmetal,et al.  Configurational effects in visual information processing , 1976 .

[69]  J. Gibson,et al.  ADAPTATION , AFTEREFFECT AND CONTRAST IN THE PERCEPTION OF TILTED LINES , 2004 .

[70]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

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

[72]  J. Mattingley,et al.  Fast and slow parietal pathways mediate spatial attention , 2004, Nature Neuroscience.

[73]  G Wolford,et al.  Lateral masking as a function of spacing , 1983, Perception & psychophysics.

[74]  Hugh R. Wilson,et al.  Responses of spatial mechanisms can explain hyperacuity , 1986, Vision Research.