Object categorization in visual periphery is modulated by delayed foveal noise.

Behavioral studies in humans indicate that peripheral vision can do object recognition to some extent. Moreover, recent studies have shown that some information from brain regions retinotopic to visual periphery is somehow fed back to regions retinotopic to the fovea and disrupting this feedback impairs object recognition in human. However, it is unclear to what extent the information in visual periphery contributes to human object categorization. Here, we designed two series of rapid object categorization tasks to first investigate the performance of human peripheral vision in categorizing natural object images at different eccentricities and abstraction levels (superordinate, basic, and subordinate). Then, using a delayed foveal noise mask, we studied how modulating the foveal representation impacts peripheral object categorization at any of the abstraction levels. We found that peripheral vision can quickly and accurately accomplish superordinate categorization, while its performance in finer categorization levels dramatically drops as the object presents further in the periphery. Also, we found that a 300-ms delayed foveal noise mask can significantly disturb categorization performance in basic and subordinate levels, while it has no effect on the superordinate level. Our results suggest that human peripheral vision can easily process objects at high abstraction levels, and the information is fed back to foveal vision to prime foveal cortex for finer categorizations when a saccade is made toward the target object.

[1]  Olivier R. Joubert,et al.  The Time-Course of Visual Categorizations: You Spot the Animal Faster than the Bird , 2009, PloS one.

[2]  Michèle Fabre-Thorpe,et al.  At 120 msec You Can Spot the Animal but You Don't Yet Know It's a Dog , 2015, Journal of Cognitive Neuroscience.

[3]  Sheng He,et al.  Temporally flexible feedback signal to foveal cortex for peripheral object recognition , 2016, Proceedings of the National Academy of Sciences.

[4]  R. Remington,et al.  Eye Movement Targets Are Released from Visual Crowding , 2013, The Journal of Neuroscience.

[5]  Matin N. Ashtiani,et al.  Object Categorization in Finer Levels Relies More on Higher Spatial Frequencies and Takes Longer , 2017, Front. Psychol..

[6]  Shaul Hochstein,et al.  The wide window of face detection. , 2010, Journal of vision.

[7]  A. Johnston,et al.  Spatiotemporal contrast sensitivity and visual field locus , 1983, Vision Research.

[8]  D. Pelli,et al.  Are faces processed like words? A diagnostic test for recognition by parts. , 2005, Journal of vision.

[9]  Nathalie Guyader,et al.  The Neural Bases of the Semantic Interference of Spatial Frequency-based Information in Scenes , 2015, Journal of Cognitive Neuroscience.

[10]  B. Keppler,et al.  Reviews of Physiology, Biochemistry and Pharmacology , 2003 .

[11]  S. Hochstein,et al.  The reverse hierarchy theory of visual perceptual learning , 2004, Trends in Cognitive Sciences.

[12]  M. Goldberg,et al.  The representation of visual salience in monkey parietal cortex , 1998, Nature.

[13]  H H Bülthoff,et al.  Detection of animals in natural images using far peripheral vision , 2001, The European journal of neuroscience.

[14]  P. Cavanagh,et al.  Visual stability based on remapping of attention pointers , 2010, Trends in Cognitive Sciences.

[15]  J. Henderson Identifying objects across saccades: effects of extrafoveal preview and flanker object context. , 1992, Journal of experimental psychology. Learning, memory, and cognition.

[16]  Garrison W Cottrell,et al.  Central and peripheral vision for scene recognition: A neurocomputational modeling exploration. , 2017, Journal of vision.

[17]  K. Rayner,et al.  Covert visual attention and extrafoveal information use during object identification , 1989, Perception & psychophysics.

[18]  Miguel P. Eckstein,et al.  Foveal analysis and peripheral selection during active visual sampling , 2014, Proceedings of the National Academy of Sciences.

[19]  Isabel Gauthier,et al.  Visual Object Recognition: Do We (Finally) Know More Now Than We Did? , 2016, Annual review of vision science.

[20]  Lester C. Loschky,et al.  The contributions of central versus peripheral vision to scene gist recognition. , 2009, Journal of vision.

[21]  N. Kanwisher,et al.  Feedback of pVisual Object Information to Foveal Retinotopic Cortex , 2008, Nature Neuroscience.

[22]  M. Boucart,et al.  Implicit processing of scene context in macular degeneration. , 2013, Investigative ophthalmology & visual science.

[23]  R. Rosenholtz Capabilities and Limitations of Peripheral Vision. , 2016, Annual review of vision science.

[24]  D. Roenker,et al.  Age and visual search: expanding the useful field of view. , 1988, Journal of the Optical Society of America. A, Optics and image science.

[25]  Michelle R. Greene,et al.  Scene categorization at large visual eccentricities , 2013, Vision Research.

[26]  P. Cavanagh,et al.  Predictive remapping of attention across eye movements , 2011, Nature Neuroscience.

[27]  Moshe Bar,et al.  Visual predictions in the orbitofrontal cortex rely on associative content. , 2014, Cerebral cortex.

[28]  R. Rosenholtz,et al.  Context mitigates crowding: Peripheral object recognition in real-world images , 2018, Cognition.

[29]  J R Duhamel,et al.  The updating of the representation of visual space in parietal cortex by intended eye movements. , 1992, Science.

[30]  Anina N. Rich,et al.  Disruption of Foveal Space Impairs Discrimination of Peripheral Objects , 2016, Front. Psychol..

[31]  I. Rentschler,et al.  Peripheral vision and pattern recognition: a review. , 2011, Journal of vision.

[32]  L J Williams,et al.  Tunnel Vision Induced by a Foveal Load Manipulation , 1985, Human factors.

[33]  M. Fabre-Thorpe,et al.  Implicit and explicit object recognition at very large visual eccentricities: No improvement after loss of central vision , 2010 .

[34]  B Fischer,et al.  The preparation of visually guided saccades. , 1987, Reviews of physiology, biochemistry and pharmacology.

[35]  Mitsuo Ikeda,et al.  Influence of foveal load on the functional visual field , 1975 .

[36]  Krista A. Ehinger,et al.  A general account of peripheral encoding also predicts scene perception performance. , 2016, Journal of vision.

[37]  David Whitney,et al.  Facilitating recognition of crowded faces with presaccadic attention , 2014, Front. Hum. Neurosci..

[38]  M. Bar A Cortical Mechanism for Triggering Top-Down Facilitation in Visual Object Recognition , 2003, Journal of Cognitive Neuroscience.

[39]  Julie D. Golomb,et al.  Attentional Facilitation throughout Human Visual Cortex Lingers in Retinotopic Coordinates after Eye Movements , 2010, The Journal of Neuroscience.

[40]  Denis Fize,et al.  Speed of processing in the human visual system , 1996, Nature.

[41]  Christopher D. Chambers,et al.  Is delayed foveal feedback critical for extra-foveal perception? , 2013, Cortex.

[42]  D. Melcher Predictive remapping of visual features precedes saccadic eye movements , 2007, Nature Neuroscience.

[43]  Sébastien M. Crouzet,et al.  Fast saccades toward faces: face detection in just 100 ms. , 2010, Journal of vision.

[44]  Muriel Boucart,et al.  Finding faces, animals, and vehicles in far peripheral vision. , 2016, Journal of vision.

[45]  M. Goldberg,et al.  Neurons in the monkey superior colliculus predict the visual result of impending saccadic eye movements. , 1995, Journal of neurophysiology.

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

[47]  Ryan V. Ringer,et al.  Impairing the useful field of view in natural scenes: Tunnel vision versus general interference. , 2016, Journal of vision.

[48]  Lester C. Loschky,et al.  Scene perception from central to peripheral vision. , 2017, Journal of vision.

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

[50]  Won Mok Shim,et al.  Modulating foveal representation can influence visual discrimination in the periphery. , 2016, Journal of vision.

[51]  Krista A. Ehinger,et al.  Rethinking the Role of Top-Down Attention in Vision: Effects Attributable to a Lossy Representation in Peripheral Vision , 2011, Front. Psychology.

[52]  Julie D. Golomb,et al.  The Native Coordinate System of Spatial Attention Is Retinotopic , 2008, The Journal of Neuroscience.

[53]  Peter J. Bex,et al.  Effects of Peripheral Visual Field Loss on Eye Movements During Visual Search , 2011, Front. Psychology.

[54]  Robert H. Wurtz,et al.  Influence of the thalamus on spatial visual processing in frontal cortex , 2006, Nature.

[55]  Jason B. Mattingley,et al.  Visual Crowding at a Distance during Predictive Remapping , 2013, Current Biology.

[56]  Muriel Boucart,et al.  Face or building superiority in peripheral vision reversed by task requirements , 2009, Advances in cognitive psychology.

[57]  E. Halgren,et al.  Top-down facilitation of visual recognition. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Jyrki Rovamo,et al.  Identification of facial images in peripheral vision , 2001, Vision Research.

[59]  Wayne D. Gray,et al.  Basic objects in natural categories , 1976, Cognitive Psychology.