The Critical Role of V2 Population Receptive Fields in Visual Orientation Crowding

Crowding, the identification difficulty for a target in the presence of nearby flankers, is an essential bottleneck for object recognition and visual awareness [1, 2]. As suggested by multitudes of behavioral studies, crowding occurs because the visual system lacks the necessary resolution (e.g., small receptive field or high resolution of spatial attention) to isolate the target from flankers and therefore integrates them mistakenly [3-12]. However, this idea has rarely been tested with neuroscience methods directly. Here, using the fMRI-based population receptive field (pRF) technique [13, 14], we found that, across individual subjects, the average pRF size of the voxels in V2 responding to the target could predict the magnitude of visual orientation crowding. The smaller the pRF size, the weaker the crowding effect. Furthermore, we manipulated the magnitude of the crowding effect within subjects. The pRF size in V2 was smaller in a weak crowding condition than in a strong crowding condition, and this difference was attention dependent. More importantly, we found that perceptual training could alleviate the orientation crowding and causally shrink the pRF size in V2. Taken together, these findings provide strong and converging evidence for a critical role of V2 pRFs in visual orientation crowding. We speculate that, synergistic with spatial attention, the dynamic and plastic nature of the V2 pRFs serves to prevent interference from the flankers through adjusting their size and consequently reduces visual crowding.

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

[2]  Jelle A. van Dijk,et al.  Cortical idiosyncrasies predict the perception of object size , 2015, Nature Communications.

[3]  F. Fang,et al.  Two-stage perceptual learning to break visual crowding. , 2016, Journal of vision.

[4]  D. Schwarzkopf,et al.  Larger Extrastriate Population Receptive Fields in Autism Spectrum Disorders , 2014, The Journal of Neuroscience.

[5]  Jude F. Mitchell,et al.  Spatial Attention Modulates Center-Surround Interactions in Macaque Visual Area V4 , 2009, Neuron.

[6]  Aaron R. Seitz,et al.  Perceptual learning , 2017, Current Biology.

[7]  S. Dumoulin,et al.  The Relationship between Cortical Magnification Factor and Population Receptive Field Size in Human Visual Cortex: Constancies in Cortical Architecture , 2011, The Journal of Neuroscience.

[8]  T. Womelsdorf,et al.  Dynamic shifts of visual receptive fields in cortical area MT by spatial attention , 2006, Nature Neuroscience.

[9]  E C Wong,et al.  Processing strategies for time‐course data sets in functional mri of the human brain , 1993, Magnetic resonance in medicine.

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

[11]  Susana T. L. Chung,et al.  Ideal observer analysis of crowding and the reduction of crowding through learning. , 2010, Journal of vision.

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

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

[14]  P. Cavanagh,et al.  Attentional resolution , 1997, Trends in Cognitive Sciences.

[15]  Fang Fang,et al.  Position shifts of fMRI-based population receptive fields in human visual cortex induced by Ponzo illusion , 2015, Experimental Brain Research.

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

[17]  Marisa Carrasco,et al.  Attentional enhancement of spatial resolution: linking behavioural and neurophysiological evidence , 2013, Nature Reviews Neuroscience.

[18]  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.

[19]  Dennis M. Levi,et al.  Crowding between first- and second-order letters in amblyopia , 2008, Vision Research.

[20]  U. Polat,et al.  Collinear stimuli regulate visual responses depending on cell's contrast threshold , 1998, Nature.

[21]  Georgios A Keliris,et al.  Population receptive field analysis of the primary visual cortex complements perimetry in patients with homonymous visual field defects , 2014, Proceedings of the National Academy of Sciences.

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

[23]  Rosilari Bellacosa Marotti,et al.  The neural origins of visual crowding as revealed by event-related potentials and oscillatory dynamics , 2016, Cortex.

[24]  Hans Strasburger,et al.  Source confusion is a major cause of crowding. , 2013, Journal of vision.

[25]  Frans W Cornelissen,et al.  Large-scale remapping of visual cortex is absent in adult humans with macular degeneration , 2011, Nature Neuroscience.

[26]  Kendrick N. Kay,et al.  Attention Reduces Spatial Uncertainty in Human Ventral Temporal Cortex , 2015, Current Biology.

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

[28]  Yuka Sasaki,et al.  Perceptual learning: toward a comprehensive theory. , 2015, Annual review of psychology.

[29]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

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

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

[32]  U. Polat,et al.  Lateral interactions between spatial channels: Suppression and facilitation revealed by lateral masking experiments , 1993, Vision Research.

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

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

[35]  Tiangang Zhou,et al.  Perceptual learning modifies the functional specializations of visual cortical areas , 2016, Proceedings of the National Academy of Sciences.

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

[37]  John T. Serences,et al.  Attention modulates spatial priority maps in the human occipital, parietal and frontal cortices , 2013, Nature Neuroscience.

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

[39]  D. Sagi.  Perceptual learning in Vision Research , 2011, Vision Research.

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

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

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

[43]  T. Knapen,et al.  How Visual Cortical Organization Is Altered by Ophthalmologic and Neurologic Disorders. , 2018, Annual review of vision science.

[44]  Jonathan Winawer,et al.  Computational neuroimaging and population receptive fields , 2015, Trends in Cognitive Sciences.

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

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

[47]  E. Louie,et al.  Holistic crowding: selective interference between configural representations of faces in crowded scenes. , 2007, Journal of vision.

[48]  David Whitney,et al.  Multi-level Crowding and the Paradox of Object Recognition in Clutter , 2018, Current Biology.

[49]  Brian A. Wandell,et al.  Population receptive field estimates in human visual cortex , 2008, NeuroImage.