fMRI Measures of Perceptual Filling-in in the Human Visual Cortex

Filling-in refers to the tendency of stabilized retinal stimuli to fade and become replaced by their background. This phenomenon is a good example of central brain mechanisms that can selectively add or delete information to/from the retinal input. Importantly, such cortical mechanisms may overlap with those that are used more generally in visual perception. In order to identify cortical areas that contribute to perceptual filling-in, we used functional magnetic resonance imaging to image activity in the visual cortex while subjects experienced filling-in. Nine subjects viewed an achromatic disc with slightly higher luminance than the background and indicated the presence or absence of filling-in by a keypress. The disc was placed in either the upper or lower left quadrant. Similar high-contrast stimuli were used to map out the retinotopic representation of the disc. Unexpectedly, the lower-field high-contrast stimulus produced more parietal cortex activation than the upper-field condition, indicating preferential representation of the lower field by attentional control mechanisms. During perceptual filling-in, we observed significant contralateral reductions in activation in lower-tier retinotopic areas V1 and V2. In contrast, increased activation was consistently observed in visual areas V3A and V4v, higher-level cortex in the intraparietal sulcus, posterior superior temporal sulcus, and the ventral occipital–temporal region, as well as the pulvinar. The filling-in activation pattern was remarkably similar for both the upper- and lower-field conditions. Behaviorally, filling-in was reported to be easier for the lower visual field, and filling-in periods were longer for the lower than the upper quadrant. We suggest this behavioral asymmetry may be partially due to the preferential parietal representation of the lower field. The results lead us to propose that perceptual filling-in recruits high-level control mechanisms to reconcile competing percepts, and alters the normal image-related signals at the first stages of cortical processing. Moreover, the overall pattern of activation during filling-in resembles that seen in other studies of perceptually bistable stimuli, including binocular rivalry, indicating common control mechanisms.

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

[2]  R W Cox,et al.  Real‐time 3D image registration for functional MRI , 1999, Magnetic resonance in medicine.

[3]  D. Purves,et al.  Similarities in normal and binocularly rivalrous viewing. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[4]  A. T. Smith,et al.  Estimating receptive field size from fMRI data in human striate and extrastriate visual cortex. , 2001, Cerebral cortex.

[5]  D. P. Russell,et al.  Increased Synchronization of Neuromagnetic Responses during Conscious Perception , 1999, The Journal of Neuroscience.

[6]  Po-Jang Hsieh,et al.  fMRI reveals that non‐local processing in ventral retinotopic cortex underlies perceptual grouping by temporal synchrony , 2008, Human brain mapping.

[7]  R. Malach,et al.  Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[8]  L. Benevento,et al.  Single neurons with both form/color differential responses and saccade-related responses in the nonretinotopic pulvinar of the behaving macaque monkey , 1995, Visual Neuroscience.

[9]  Terry M. Peters,et al.  3D statistical neuroanatomical models from 305 MRI volumes , 1993, 1993 IEEE Conference Record Nuclear Science Symposium and Medical Imaging Conference.

[10]  G L WALLS,et al.  The filling-in process. , 1954, American journal of optometry and archives of American Academy of Optometry.

[11]  S. Petersen,et al.  Pulvinar nuclei of the behaving rhesus monkey: visual responses and their modulation. , 1985, Journal of neurophysiology.

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

[13]  A. Dale,et al.  Selective averaging of rapidly presented individual trials using fMRI , 1997, Human brain mapping.

[14]  K. Nakayama,et al.  Binocular Rivalry and Visual Awareness in Human Extrastriate Cortex , 1998, Neuron.

[15]  Anders M. Dale,et al.  Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex , 2001, IEEE Transactions on Medical Imaging.

[16]  Leslie G. Ungerleider,et al.  Cue-dependent deficits in grating orientation discrimination after V4 lesions in macaques , 1996, Visual Neuroscience.

[17]  Y. Sakaguchi Visual field anisotropy revealed by perceptual filling-in , 2003, Vision Research.

[18]  G H Glover,et al.  Simple analytic spiral K‐space algorithm , 1999, Magnetic resonance in medicine.

[19]  W. Singer,et al.  Synchronization of oscillatory responses in visual cortex correlates with perception in interocular rivalry. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

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

[21]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[22]  R Gattass,et al.  Filling-in in topographically organized distributed networks. , 1999, Anais da Academia Brasileira de Ciencias.

[23]  R. Desimone,et al.  Attentional control of visual perception: cortical and subcortical mechanisms. , 1990, Cold Spring Harbor symposia on quantitative biology.

[24]  Leslie G. Ungerleider,et al.  Perceptual filling-in: a parametric study , 1998, Vision Research.

[25]  R S Weil,et al.  Neural correlates of perceptual filling-in of an artificial scotoma in humans , 2007, Proceedings of the National Academy of Sciences.

[26]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

[27]  J. Marshall,et al.  Is neglect (only) lateral? A quadrant analysis of line cancellation. , 1989, Journal of clinical and experimental neuropsychology.

[28]  Andreas K. Engel,et al.  Temporal Binding, Binocular Rivalry, and Consciousness , 1999, Consciousness and Cognition.

[29]  R Gattass,et al.  Dynamic surrounds of receptive fields in primate striate cortex: a physiological basis for perceptual completion? , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[30]  Susan K Lemieux,et al.  Retinotopic organization in children measured with fMRI. , 2004, Journal of vision.

[31]  H. Gerrits,et al.  Experiments with retinal stabilized images. Relations between the observations and neural data. , 1966, Vision research.

[32]  Janine Mendola Contextual Shape Processing in Human Visual Cortex: Beginning to Fill-In the Blanks , 2003 .

[33]  F. Tong,et al.  Can attention selectively bias bistable perception? Differences between binocular rivalry and ambiguous figures. , 2004, Journal of vision.

[34]  Ikuya Murakami,et al.  Neural responses in the primary visual cortex of the monkey during perceptual filling-in at the blind spot , 2002, Neuroscience Research.

[35]  Alejandro Lleras,et al.  What You See Is What You Get , 2006, Psychological science.

[36]  A. Nobre The attentive homunculus: Now you see it, now you don't , 2001, Neuroscience & Biobehavioral Reviews.

[37]  R. S. J. Frackowiak,et al.  Human brain activity during spontaneously reversing perception of ambiguous figures , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[38]  Lianggang Lou,et al.  Selective Peripheral Fading: Evidence for Inhibitory Sensory Effect of Attention , 1999, Perception.

[39]  M. Paradiso,et al.  Filling-in Percepts Produced by Luminance Modulation , 1996, Vision Research.

[40]  M. Bar,et al.  Cortical Mechanisms Specific to Explicit Visual Object Recognition , 2001, Neuron.

[41]  R. Turner,et al.  Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[42]  V. Walsh,et al.  Visual field asymmetries in attention and learning. , 2000, Spatial vision.

[43]  D. Heeger,et al.  Neuronal basis of contrast discrimination , 1999, Vision Research.

[44]  A. Chatterjee,et al.  Influence of Reference Frames on Asymmetries in Troxler's Effect , 2002, Perceptual and motor skills.

[45]  Dov Sagi,et al.  Motion-induced blindness in normal observers , 2001, Nature.

[46]  D. B. Bender,et al.  Retinotopic organization of macaque pulvinar. , 1981, Journal of neurophysiology.

[47]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[48]  M. Paradiso,et al.  Neural Correlates of Perceived Brightness in the Retina, Lateral Geniculate Nucleus, and Striate Cortex , 1999, The Journal of Neuroscience.

[49]  Theodor Landis,et al.  Explicit and implicit perception of illusory contours in unilateral spatial neglect: behavioural and anatomical correlates of preattentive grouping mechanisms , 2001, Neuropsychologia.

[50]  H. Komatsu,et al.  Surface representation in the visual system. , 1996, Brain research. Cognitive brain research.

[51]  Ravi S. Menon,et al.  Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[52]  L. Pessoa,et al.  Finding out about filling-in: a guide to perceptual completion for visual science and the philosophy of perception. , 1998, The Behavioral and brain sciences.

[53]  John H. R. Maunsell,et al.  Visual processing in monkey extrastriate cortex. , 1987, Annual review of neuroscience.

[54]  S Grossberg,et al.  3-D vision and figure-ground separation by visual cortex , 2010, Perception & psychophysics.

[55]  Adrian T. Lee,et al.  fMRI of human visual cortex , 1994, Nature.

[56]  R. L. Gregory,et al.  Perceptual filling in of artificially induced scotomas in human vision , 1991, Nature.

[57]  A M Dale,et al.  Measuring the thickness of the human cerebral cortex from magnetic resonance images. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[58]  F. Previc Functional specialization in the lower and upper visual fields in humans: Its ecological origins and neurophysiological implications , 1990, Behavioral and Brain Sciences.

[59]  H. Komatsu,et al.  Neural Responses in the Retinotopic Representation of the Blind Spot in the Macaque V1 to Stimuli for Perceptual Filling-In , 2000, The Journal of Neuroscience.

[60]  G. Rees,et al.  Neural correlates of perceptual rivalry in the human brain. , 1998, Science.

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

[62]  Karl J. Friston,et al.  How the brain learns to see objects and faces in an impoverished context , 1997, Nature.

[63]  G. Rees,et al.  Covariation of activity in visual and prefrontal cortex associated with subjective visual perception. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

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

[65]  M. Posner,et al.  Deficits in human visual spatial attention following thalamic lesions. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[66]  Peter De Weerd,et al.  Responses of cells in monkey visual cortex during perceptual filling-in of an artificial scotoma , 1995, Nature.

[67]  Elisabetta Làdavas,et al.  Automatic and voluntary orienting of attention in patients with visual neglect: Horizontal and vertical dimensions , 1994, Neuropsychologia.

[68]  N. Logothetis,et al.  Multistable phenomena: changing views in perception , 1999, Trends in Cognitive Sciences.

[69]  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.

[70]  D. Heeger,et al.  Neuronal activity in human primary visual cortex correlates with perception during binocular rivalry , 2000, Nature Neuroscience.

[71]  Stephen A. Engel,et al.  Interocular rivalry revealed in the human cortical blind-spot representation , 2001, Nature.

[72]  Ken Nakayama,et al.  Brightness perception and filling-in , 1991, Vision Research.

[73]  B. Chapman,et al.  Turning a Blind Eye to Cortical Receptive Fields , 1996, Neuron.

[74]  S. Petersen,et al.  The pulvinar and visual salience , 1992, Trends in Neurosciences.

[75]  Leslie G. Ungerleider,et al.  Modulation of sensory suppression: implications for receptive field sizes in the human visual cortex. , 2001, Journal of neurophysiology.

[76]  K. Nakayama,et al.  Enhanced Perception of Illusory Contours in the Lower Versus Upper Visual Hemifields , 1996, Science.

[77]  M. Pettet,et al.  Dynamic changes in receptive-field size in cat primary visual cortex. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[78]  R. Rafal,et al.  Deficits in spatial coding and feature binding following damage to spatiotopic maps in the human pulvinar , 2002, Nature Neuroscience.

[79]  I. Ohzawa,et al.  Receptive field structure in the visual cortex: does selective stimulation induce plasticity? , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[80]  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 .

[81]  Sheng He,et al.  Temporal characteristics of binocular rivalry: visual field asymmetries , 2003, Vision Research.