Explicit and implicit perception of illusory contours in unilateral spatial neglect: behavioural and anatomical correlates of preattentive grouping mechanisms

Studies of hemispatial neglect suggest that some perceptual processes still operate on contralesional stimuli independent from spatial attention or awareness. Here we examined whether preattentive processing in extrastriate areas may group unconnected elements inducing illusory contours despite neglect. While it has been debated whether illusory contours arise from preattentive grouping or higher cognitive processes, neurophysiological studies show that neurones in secondary visual cortex (V2) can code for illusory contours. Twelve patients with right hemisphere damage and left neglect were tested for implicit and explicit detection of illusory contours using, respectively: (1) a bisection task where patients were not explicitly required to attend to lateral elements and judged the midpoint of Kanizsa illusory stimuli, as well as other physically connected or unconnected stimuli of the same length; (2) a matching task where patients had to overtly attend to lateral elements and made same/different judgements on pairs of illusory stimuli with identical or different inducers on the right or left side. In some patients, bisection judgements were consistently similar on Kanizsa stimuli with illusory contours and connected stimuli with real contours but different on unconnected gap figures, regardless of their length, suggesting implicit grouping of inducing elements prior to processing stages where a spatial attentional bias arose. Their lesions centred on the inferior parietal cortex or thalamus. Other patients did not show a systematic bisection pattern and had lesions extending posteriorly in the lateral occipital cortex. However, both groups of patients failed to detect left-side inducers in explicit matching judgements, even though errors often revealed unconscious processing, and they showed similar neglect severity on other standard tests. These findings suggest that grouping by illusory contours can occur preattentively and influence bisection independently from the ability to detect contralateral inducers explicitly, severity of inattention, and other forms of unconscious processing. Implicit grouping may depend on the sparing of lateral occipital areas involved in figure-ground segmentation at early stages of visual processing.

[1]  Clare Porac,et al.  Set and Subjective Contour , 1987 .

[2]  F. Doricchi,et al.  Disappearance of leftward rapid eye movements during sleep in left visual hemi-inattention. , 1991, Neuroreport.

[3]  Terri Gullickson Human Brain Anatomy in Computerized Images. , 1995 .

[4]  Jon Driver,et al.  Object segmentation and visual neglect , 1995, Behavioural Brain Research.

[5]  M. Mozer,et al.  Perceptual and Conceptual Mechanisms in Neglect Dyslexia: Two Contrasting Case Studies , 1990 .

[6]  E. Warrington,et al.  Failure of object recognition due to a breakdown of figure-ground discrimination in a patient with normal acuity , 1991, Neuropsychologia.

[7]  J. Cronly-Dillon,et al.  Visual Agnosias and Other Disturbances of Visual Perception and Cognition , 1991 .

[8]  P. Kellman,et al.  A common mechanism for illusory and occluded object completion. , 1998, Journal of experimental psychology. Human perception and performance.

[9]  J. Driver,et al.  Can Visual Neglect Operate in Object-centred Co-ordinates? An Affirmative Single-case Study , 1991 .

[10]  Jon Driver,et al.  Parallel detection of Kanizsa subjective figures in the human visual system , 1994, Nature.

[11]  Ruth Ann Atchley,et al.  Hemispheric specialization in the detection of subjective objects , 1998, Neuropsychologia.

[12]  Claude Bonnet,et al.  Psychophysical evidence for low-level processing of illusory contours and surfaces in the kanizsa square , 1991, Vision Research.

[13]  V. Ramachandran,et al.  On the perception of illusory contours , 1994, Vision Research.

[14]  J. Marshall,et al.  Line Bisection in Visuo-Spatial Neglect: Disproof of a Conjecture , 1989, Cortex.

[15]  Jordan Grafman,et al.  Handbook of Neuropsychology , 1991 .

[16]  Morris Moscovitch,et al.  Object-Centered Neglect in Patients with Unilateral Neglect: Effects of Left-Right Coordinates of Objects , 1994, Journal of Cognitive Neuroscience.

[17]  Irvin Rock,et al.  A Problem-Solving Approach to Illusory Contours , 1987 .

[18]  J. Marshall,et al.  Blindsight and insight in visuo-spatial neglect , 1988, Nature.

[19]  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.

[20]  Michael J. Hawken,et al.  Macaque VI neurons can signal ‘illusory’ contours , 1993, Nature.

[21]  J. Mattingley,et al.  Preattentive Filling-in of Visual Surfaces in Parietal Extinction , 1997, Science.

[22]  F. Doricchi,et al.  Influence of Figure-Ground Contrast on the Implicit and Explicit Processing of Line Drawings in Patients with Left Unilateral Neglect , 1997 .

[23]  K. D. Hamsher,et al.  Stereopsis and the perception of anomalous contours , 1978, Neuropsychologia.

[24]  Gregory W. Lesher,et al.  Illusory contours: Toward a neurally based perceptual theory , 1995, Psychonomic bulletin & review.

[25]  K. Heilman,et al.  Neglect and Related Disorders , 1984, Seminars in neurology.

[26]  J. Bradshaw,et al.  The Effects of Unilateral Visuospatial Neglect on Perception of Müller-Lyer Illusory Figures , 1995, Perception.

[27]  John C. Marshall,et al.  The Yin and the Yang of visuo-spatial neglect: A case study , 1994, Neuropsychologia.

[28]  S. Grossberg,et al.  Neural dynamics of form perception: boundary completion, illusory figures, and neon color spreading. , 1985, Psychological review.

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

[30]  T Landis,et al.  Illusory contours and spatial neglect , 1998, Neuroreport.

[31]  Kenneth M. Heilman,et al.  The Influence of Center of Mass Effect on the Distribution of Spatial Attention in the Vertical and Horizontal Dimensions , 1997, Brain and Cognition.

[32]  R. Rafal,et al.  Perception of geometric illusions in hemispatial neglect , 1996, Neuropsychologia.

[33]  R. Rafal,et al.  "Both" means more than "two": localizing and counting in patients with visuospatial neglect , 1999, Nature Neuroscience.

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

[35]  E. Bisiach,et al.  Break-Down of Perceptual Awareness in Unilateral Neglect , 1990, Cortex.

[36]  J. Olver,et al.  Analysis of the Syndrome of Unilateral Neglect , 1993, Cortex.

[37]  Stephen Grossberg,et al.  Figure-Ground Separation by Visual Cortex , 1996 .

[38]  I. Rock,et al.  Illusory Contours as the Solution to a Problem , 1979, Perception.

[39]  R. Gregory,et al.  Cognitive Contours , 1972, Nature.

[40]  G. Kanizsa Subjective contours. , 1976, Scientific American.

[41]  J. Horton,et al.  Quadrantic visual field defects. A hallmark of lesions in extrastriate (V2/V3) cortex. , 1991, Brain : a journal of neurology.

[42]  R. Tennant,et al.  Inhibition of leukaemia virus replication by polyadenylic acid. , 1972, Nature: New biology.

[43]  R. von der Heydt,et al.  Illusory contours and cortical neuron responses. , 1984, Science.

[44]  E. Peterhans,et al.  Subjective contours - bridging the gap between psychophysics and physiology , 1991, Trends in Neurosciences.

[45]  S. Zeki,et al.  Brain Activity Related to the Perception of Illusory Contours , 1996, NeuroImage.

[46]  R. Gregory Illusory Contours and Occluding Surfaces , 1987 .

[47]  Chao-Yi Li,et al.  Measurements of geometric illusions, illusory contours and stereo-depth at luminance and colour contrast , 1995, Vision Research.

[48]  L. Gerstman,et al.  In search of closure: Subjective contour illusions, gestalt completion tests, and implications , 1987, Brain and Cognition.

[49]  T. Bonhoeffer,et al.  Current opinion in neurobiology , 1997, Current Opinion in Neurobiology.

[50]  Jon Driver,et al.  Grouping reduces visual extinction: Neuropsychological evidence for weight-linkage in visual selection , 1994 .

[51]  D. Perani,et al.  The anatomy of unilateral neglect after right-hemisphere stroke lesions. A clinical/CT-scan correlation study in man , 1986, Neuropsychologia.

[52]  Jon Driver,et al.  Preserved figure-ground segregation and symmetry perception in visual neglect , 1992, Nature.

[53]  M. Mesulam A cortical network for directed attention and unilateral neglect , 1981, Annals of neurology.

[54]  H. Egeth,et al.  Perception without attention: evidence of grouping under conditions of inattention. , 1997, Journal of Experimental Psychology: Human Perception and Performance.

[55]  Glyn W. Humphreys,et al.  Grouping and Extinction: Evidence for Low-level Modulation of Visual Selection , 1996 .

[56]  M. Metz-Lutz Handbook of neuropsychology, Vol 6 et 7, Rapin I, Segalowitz SJ (Eds.). Elsevier (1992) , 1993 .

[57]  D. Sagi,et al.  Visual extinction and cortical connectivity in human vision. , 1997, Brain research. Cognitive brain research.

[58]  M. Farah,et al.  Unconscious perception of “extinguished” visual stimuli: Reassessing the evidence , 1991, Neuropsychologia.

[59]  L. Spillmann,et al.  Long-range interactions in visual perception , 1996, Trends in Neurosciences.