Locating the cortical bottleneck for slow reading in peripheral vision.

Yu, Legge, Park, Gage, and Chung (2010) suggested that the neural bottleneck for slow peripheral reading is located in nonretinotopic areas. We investigated the potential rate-limiting neural site for peripheral reading using fMRI, and contrasted peripheral reading with recognition of peripherally presented line drawings of common objects. We measured the BOLD responses to both text (three-letter words/nonwords) and line-drawing objects presented either in foveal or peripheral vision (10° lower right visual field) at three presentation rates (2, 4, and 8/second). The statistically significant interaction effect of visual field × presentation rate on the BOLD response for text but not for line drawings provides evidence for distinctive processing of peripheral text. This pattern of results was obtained in all five regions of interest (ROIs). At the early retinotopic cortical areas, the BOLD signal slightly increased with increasing presentation rate for foveal text, and remained fairly constant for peripheral text. In the Occipital Word-Responsive Area (OWRA), Visual Word Form Area (VWFA), and object sensitive areas (LO and PHA), the BOLD responses to text decreased with increasing presentation rate for peripheral but not foveal presentation. In contrast, there was no rate-dependent reduction in BOLD response for line-drawing objects in all the ROIs for either foveal or peripheral presentation. Only peripherally presented text showed a distinctive rate-dependence pattern. Although it is possible that the differentiation starts to emerge at the early retinotopic cortical representation, the neural bottleneck for slower reading of peripherally presented text may be a special property of peripheral text processing in object category selective cortex.

[1]  Frank Tong,et al.  Temporal limitations in object processing across the human ventral visual pathway. , 2007, Journal of neurophysiology.

[2]  C W Tyler,et al.  Specific deficits of flicker sensitivity in glaucoma and ocular hypertension. , 1981, Investigative ophthalmology & visual science.

[3]  C W Tyler,et al.  Analysis of visual modulation sensitivity. II. Peripheral retina and the role of photoreceptor dimensions. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[4]  J. A. Kraut,et al.  Clinical Low Vision , 1985 .

[5]  R A Schuchard,et al.  Relative locations of macular scotomas near the PRL: effect on low vision reading. , 1999, Journal of rehabilitation research and development.

[6]  S Lehéricy,et al.  The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients. , 2000, Brain : a journal of neurology.

[7]  Talma Hendler,et al.  Center–periphery organization of human object areas , 2001, Nature Neuroscience.

[8]  Liang Wang,et al.  Probabilistic Maps of Visual Topography in Human Cortex. , 2015, Cerebral cortex.

[9]  Simon J. Thorpe,et al.  Ultra-rapid object detection with saccadic eye movements: Visual processing speed revisited , 2006, Vision Research.

[10]  J. Maunsell,et al.  Effects of task difficulty and target likelihood in area V4 of macaque monkeys. , 2006, Journal of neurophysiology.

[11]  M. Tarr,et al.  The Fusiform Face Area is Part of a Network that Processes Faces at the Individual Level , 2000, Journal of Cognitive Neuroscience.

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

[13]  Jane E. Joseph,et al.  fMRI correlates of cortical specialization and generalization for letter processing , 2006, NeuroImage.

[14]  E Peli,et al.  Scrolled and rapid serial visual presentation texts are read at similar rates by the visually impaired. , 1995, Journal of the Optical Society of America. A, Optics, image science, and vision.

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

[16]  Brian A. Wandell,et al.  Position sensitivity in the visual word form area , 2012, Proceedings of the National Academy of Sciences.

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

[18]  Gordon E. Legge,et al.  Development of a training protocol to improve reading performance in peripheral vision , 2010, Vision Research.

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

[20]  D. Heeger,et al.  Two Retinotopic Visual Areas in Human Lateral Occipital Cortex , 2006, The Journal of Neuroscience.

[21]  D. Heeger,et al.  Activity in primary visual cortex predicts performance in a visual detection task , 2000, Nature Neuroscience.

[22]  Gordon E. Legge,et al.  Letter-recognition and reading speed in peripheral vision benefit from perceptual learning , 2004, Vision Research.

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

[24]  Jyrki Rovamo,et al.  Critical flicker frequency as a function of stimulus area and luminance at various eccentricities in human cone vision: A revision of granit-harper and ferry-porter laws , 1988, Vision Research.

[25]  Gordon E Legge,et al.  Does print size matter for reading? A review of findings from vision science and typography. , 2011, Journal of vision.

[26]  S. Markowitz,et al.  Principles of modern low vision rehabilitation. , 2006, Canadian journal of ophthalmology. Journal canadien d'ophtalmologie.

[27]  Stanislas Dehaene,et al.  Specialization within the ventral stream: the case for the visual word form area , 2004, NeuroImage.

[28]  S. Dehaene,et al.  Direct Intracranial, fMRI, and Lesion Evidence for the Causal Role of Left Inferotemporal Cortex in Reading , 2006, Neuron.

[29]  G. Orban,et al.  The Retinotopic Organization of the Human Middle Temporal Area MT/V5 and Its Cortical Neighbors , 2010, The Journal of Neuroscience.

[30]  S. Dehaene,et al.  Language-specific tuning of visual cortex? Functional properties of the Visual Word Form Area. , 2002, Brain : a journal of neurology.

[31]  Amir Amedi,et al.  A Ventral Visual Stream Reading Center Independent of Visual Experience , 2012, Current Biology.

[32]  S. Dehaene,et al.  The unique role of the visual word form area in reading , 2011, Trends in Cognitive Sciences.

[33]  Gordon E. Legge,et al.  Psychophysics of reading—II. Low vision , 1985, Vision Research.

[34]  K. Grill-Spector,et al.  The dynamics of object-selective activation correlate with recognition performance in humans , 2000, Nature Neuroscience.

[35]  J. G. Snodgrass,et al.  A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity, and visual complexity. , 1980, Journal of experimental psychology. Human learning and memory.

[36]  J. Joseph,et al.  Shared and dissociated cortical regions for object and letter processing. , 2003, Brain research. Cognitive brain research.

[37]  Sing-Hang Cheung,et al.  Effect of letter spacing on visual span and reading speed. , 2007, Journal of vision.

[38]  G E Legge,et al.  Psychophysics of reading. Clinical predictors of low-vision reading speed. , 1992, Investigative ophthalmology & visual science.

[39]  R F Hess,et al.  Suprathreshold temporal-frequency discrimination in the fovea and the periphery. , 1994, Journal of the Optical Society of America. A, Optics, image science, and vision.

[40]  P. Perona,et al.  Rapid natural scene categorization in the near absence of attention , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Gordon E. Legge,et al.  Psychophysics of reading. XVIII. The effect of print size on reading speed in normal peripheral vision , 1998, Vision Research.

[42]  Mariano Sigman,et al.  Hierarchical Coding of Letter Strings in the Ventral Stream: Dissecting the Inner Organization of the Visual Word-Form System , 2007, Neuron.

[43]  Christopher G. Thomas,et al.  Amplitude response and stimulus presentation frequency response of human primary visual cortex using BOLD EPI at 4 T , 1998, Magnetic resonance in medicine.

[44]  Marisa Carrasco,et al.  Speed of visual processing increases with eccentricity , 2003, Nature Neuroscience.

[45]  Orrin Devinsky,et al.  Sequential then Interactive Processing of Letters and Words in the Left Fusiform Gyrus , 2012, Nature Communications.

[46]  G. Legge,et al.  Comparing reading speed for horizontal and vertical English text. , 2010, Journal of vision.

[47]  K. Rayner Eye movements in reading and information processing: 20 years of research. , 1998, Psychological bulletin.

[48]  T. Nazir,et al.  Letter visibility and word recognition: The optimal viewing position in printed words , 1992, Perception & psychophysics.

[49]  R. Dolan,et al.  Attentional load and sensory competition in human vision: modulation of fMRI responses by load at fixation during task-irrelevant stimulation in the peripheral visual field. , 2005, Cerebral cortex.

[50]  Joseph T Devlin,et al.  The myth of the visual word form area , 2003, NeuroImage.

[51]  B. Wandell,et al.  Visual field maps, population receptive field sizes, and visual field coverage in the human MT+ complex. , 2009, Journal of neurophysiology.

[52]  Mark Jenkinson,et al.  Correspondences between retinotopic areas and myelin maps in human visual cortex , 2014, NeuroImage.

[53]  C. Price,et al.  The Interactive Account of ventral occipitotemporal contributions to reading , 2011, Trends in Cognitive Sciences.

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

[55]  G. Legge,et al.  Is word recognition different in central and peripheral vision? , 2003, Vision Research.

[56]  P T Fox,et al.  Rate dependence of human visual cortical response due to brief stimulation: an event-related fMRI study. , 2001, Magnetic resonance imaging.

[57]  C D Frith,et al.  Modulating irrelevant motion perception by varying attentional load in an unrelated task. , 1997, Science.

[58]  Harvey A Swadlow,et al.  Task difficulty modulates the activity of specific neuronal populations in primary visual cortex , 2008, Nature Neuroscience.

[59]  Hye-Won Lee,et al.  Training improves reading speed in peripheral vision: is it due to attention? , 2010, Journal of vision.

[60]  W Seiple,et al.  Duration Thresholds for Target Detection and Identification in the Peripheral Visual Field , 2001, Optometry and vision science : official publication of the American Academy of Optometry.

[61]  R. Watt,et al.  The utility of image descriptions in the initial stages of vision: a case study of printed text. , 2010, British journal of psychology.

[62]  E. Mehr,et al.  Training and Practice Effects in Performance with Low‐Vision Aids: A Preliminary Study , 1977, American journal of optometry and physiological optics.

[63]  Qiyong Gong,et al.  Robust and Task-Independent Spatial Profile of the Visual Word Form Activation in Fusiform Cortex , 2011, PloS one.

[64]  S. Thorpe,et al.  Word processing speed in peripheral vision measured with a saccadic choice task , 2011, Vision Research.

[65]  Talma Hendler,et al.  Eccentricity Bias as an Organizing Principle for Human High-Order Object Areas , 2002, Neuron.

[66]  H. Spitzer,et al.  Increased attention enhances both behavioral and neuronal performance. , 1988, Science.

[67]  Bruce D. McCandliss,et al.  The visual word form area: expertise for reading in the fusiform gyrus , 2003, Trends in Cognitive Sciences.