Intact Illusory Contour Formation but Equivalently Impaired Visual Shape Completion in First- and Later-Episode Schizophrenia

Visual shape completion is a fundamental process that constructs contours and shapes on the basis of the geometric relations between spatially separated edge elements. People with schizophrenia are impaired at distinguishing visually completed shapes, but when does the impairment emerge and how does it evolve with illness duration? The question bears on the debate as to whether cognition declines after illness onset. To address the issue, we tested healthy controls (n = 48), first-episode psychosis patients (n = 23), and chronic schizophrenia patients (n = 49) on a classic psychophysical task in which subjects discriminated the relative orientations of four sectored circles that either formed or did not form visually completed shapes (illusory and fragmented conditions, respectively). Visual shape completion was quantified as the extent to which performance in the illusory condition exceeded that of the fragmented. Half of the trials incorporated wire edge elements, which augment contour salience and improve shape completion. Each patient group exhibited large visual shape completion deficits that could not be explained by differences in age, motivation, or orientation tuning. Patients responded normally to changes in illusory contour salience, indicating that they were forming but not adequately employing such contours for discriminating shapes. Shape completion deficits were most apparent for patients with cognitive disorganization, poor premorbid early adolescent functioning, and normal orientation discrimination. Visual shape completion deficits emerge maximally by the first psychotic episode and arise from higher-level disturbances that are related to premorbid functioning and disorganization.

[1]  B. Keane,et al.  Self-Reported Visual Perceptual Abnormalities Are Strongly Associated with Core Clinical Features in Psychotic Disorders , 2018, Front. Psychiatry.

[2]  Brian P. Keane,et al.  Contour interpolation: A case study in Modularity of Mind , 2017, Cognition.

[3]  C. Gilbert,et al.  Interactions between feedback and lateral connections in the primary visual cortex , 2017, Proceedings of the National Academy of Sciences.

[4]  Michael H. Herzog,et al.  About individual differences in vision , 2017, Vision Research.

[5]  S. Kastner,et al.  Visual shape completion deficits arise in first-episode and chronic schizophrenia, but are less severe in bipolar disorder: Evidence for a novel behavioral biomarker , 2016 .

[6]  S. Kastner,et al.  Visual integration dysfunction in schizophrenia arises by the first psychotic episode and worsens with illness duration. , 2016, Journal of abnormal psychology.

[7]  S. Kastner,et al.  Multiple forms of contour grouping deficits in schizophrenia: What is the role of spatial frequency? , 2014, Neuropsychologia.

[8]  R. Rosenheck,et al.  A cross-national factor analytic comparison of three models of PANSS symptoms in schizophrenia , 2014, Psychiatry Research.

[9]  Brian P. Keane,et al.  Late, not early, stages of Kanizsa shape perception are compromised in schizophrenia , 2014, Neuropsychologia.

[10]  R. Kahn,et al.  Schizophrenia is a cognitive illness: time for a change in focus. , 2013, JAMA psychiatry.

[11]  T. Papathomas,et al.  Effects of short-term inpatient treatment on sensitivity to a size contrast illusion in first-episode psychosis and multiple-episode schizophrenia , 2013, Front. Psychol..

[12]  S. Sponheim,et al.  Abnormal Contextual Modulation of Visual Contour Detection in Patients with Schizophrenia , 2013, PloS one.

[13]  Philip J. Kellman,et al.  Reinterpreting Behavioral Receptive Fields: Lightness Induction Alters Visually Completed Shape , 2013, PloS one.

[14]  Gijs Plomp,et al.  Electrophysiological evidence for ventral stream deficits in schizophrenia patients. , 2013, Schizophrenia bulletin.

[15]  J. O. Johannessen,et al.  Is there an optimal factor structure of the Positive and Negative Syndrome Scale in patients with first-episode psychosis? , 2013, Scandinavian journal of psychology.

[16]  John J. Foxe,et al.  Disambiguating the roles of area V1 and the lateral occipital complex (LOC) in contour integration , 2013, NeuroImage.

[17]  Wolf Singer,et al.  Deficits in high- (>60 Hz) gamma-band oscillations during visual processing in schizophrenia , 2013, Front. Hum. Neurosci..

[18]  Victor A. F. Lamme,et al.  Confuse Your Illusion , 2013, Psychological science.

[19]  R. Murray,et al.  The Myth of Schizophrenia as a Progressive Brain Disease , 2012, Schizophrenia bulletin.

[20]  S. Shergill,et al.  Reduced Crowding and Poor Contour Detection in Schizophrenia Are Consistent with Weak Surround Inhibition , 2012, PloS one.

[21]  J. R. Pomerantz,et al.  A century of Gestalt psychology in visual perception: II. Conceptual and theoretical foundations. , 2012, Psychological bulletin.

[22]  J. Ragland,et al.  The spatial range of contour integration deficits in schizophrenia , 2012, Experimental Brain Research.

[23]  Hongjing Lu,et al.  Is interpolation cognitively encapsulated? Measuring the effects of belief on Kanizsa shape discrimination and illusory contour formation , 2012, Cognition.

[24]  Daniel H. Mathalon,et al.  Human Neuroscience Hypothesis and Theory Article Neurobiology of Schizophrenia: Search for the Elusive Correlation with Symptoms , 2022 .

[25]  D. R. Weinberger,et al.  Searching for a consensus five-factor model of the Positive and Negative Syndrome Scale for schizophrenia , 2012, Schizophrenia Research.

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

[27]  Brian P Keane,et al.  Perceptual organization impairment in schizophrenia and associated brain mechanisms: review of research from 2005 to 2010. , 2011, Schizophrenia bulletin.

[28]  Tyrone D. Cannon,et al.  Thought disorder and communication deviance as predictors of outcome in youth at clinical high risk for psychosis. , 2011, Journal of the American Academy of Child and Adolescent Psychiatry.

[29]  Marley W. Watkins,et al.  Investigation of the factor structure of the Wechsler Adult Intelligence Scale--Fourth Edition (WAIS-IV): exploratory and higher order factor analyses. , 2010, Psychological assessment.

[30]  John J. Foxe,et al.  Impaired visual object processing across an occipital-frontal-hippocampal brain network in schizophrenia: an integrated neuroimaging study. , 2010, Archives of general psychiatry.

[31]  L. Kiorpes,et al.  Global visual processing in macaques studied using Kanizsa illusory shapes , 2010, Visual Neuroscience.

[32]  N. Andreasen,et al.  Antipsychotic Dose Equivalents and Dose-Years: A Standardized Method for Comparing Exposure to Different Drugs , 2010, Biological Psychiatry.

[33]  Szabolcs Kéri,et al.  Attentional modulation of perceptual organisation in schizophrenia , 2009, Cognitive neuropsychiatry.

[34]  B. Tjan,et al.  Better discrimination for illusory than for occluded perceptual completions. , 2008, Journal of vision.

[35]  Marianne Maertens,et al.  Local determinants of contour interpolation , 2008 .

[36]  R. McCarley,et al.  Orbitofrontal volume deficit in schizophrenia and thought disorder. , 2007, Brain : a journal of neurology.

[37]  Philip J. Kellman,et al.  Classification images reveal spatiotemporal contour interpolation , 2007, Vision Research.

[38]  M. Seghier,et al.  Functional Neuroimaging Findings on the Human Perception of Illusory Contours , 2022 .

[39]  John J. Foxe,et al.  Boundary Completion Is Automatic and Dissociable from Shape Discrimination , 2006, The Journal of Neuroscience.

[40]  S. Kéri,et al.  Spatial frequency processing in schizophrenia: trait or state marker? , 2006, Journal of abnormal psychology.

[41]  John J. Foxe,et al.  Filling-in in schizophrenia: a high-density electrical mapping and source-analysis investigation of illusory contour processing. , 2005, Cerebral cortex.

[42]  W. Spaulding,et al.  Poor premorbid social functioning and theory of mind deficit in schizophrenia: evidence of reduced context processing? , 2005, Journal of psychiatric research.

[43]  D. Javitt,et al.  Early-stage visual processing and cortical amplification deficits in schizophrenia. , 2005, Archives of general psychiatry.

[44]  Nava Rubin,et al.  Rapid detection of salient regions: evidence from apparent motion. , 2004, Journal of vision.

[45]  W. A. Phillips,et al.  Evidence for impaired visual context processing in schizotypy with thought disorder , 2004, Schizophrenia Research.

[46]  Szabolcs Kéri,et al.  Reduced facilitation effect of collinear flankers on contrastdetection reveals impaired lateral connectivity in the visual cortex of schizophrenia patients , 2004, Neuroscience Letters.

[47]  A. Nieder,et al.  Seeing more than meets the eye: processing of illusory contours in animals , 2002, Journal of Comparative Physiology A.

[48]  J. Addington,et al.  Assessment of premorbid function in first-episode schizophrenia: modifications to the Premorbid Adjustment Scale. , 2002, Journal of psychiatry & neuroscience : JPN.

[49]  S. Klein,et al.  Measuring, estimating, and understanding the psychometric function: A commentary , 2001, Perception & psychophysics.

[50]  T. S. Lee,et al.  Dynamics of subjective contour formation in the early visual cortex. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[51]  G. A. Miller,et al.  Misunderstanding analysis of covariance. , 2001, Journal of abnormal psychology.

[52]  B. Turetsky,et al.  Reduced dorsal and orbital prefrontal gray matter volumes in schizophrenia. , 2000, Archives of general psychiatry.

[53]  R. Kahn,et al.  School performance as a premorbid marker for schizophrenia: A twin study , 2000, Schizophrenia Research.

[54]  C. Tyler,et al.  Bayesian adaptive estimation of psychometric slope and threshold , 1999, Vision Research.

[55]  R. Shapley,et al.  Spatial and Temporal Properties of Illusory Contours and Amodal Boundary Completion , 1996, Vision Research.

[56]  P. Kellman,et al.  A theory of visual interpolation in object perception , 1991, Cognitive Psychology.

[57]  A. Farmer,et al.  Heterogeneity in schizophrenia: A cluster-analytic approach , 1983, Psychiatry Research.

[58]  A. Caspi,et al.  Neuropsychological decline in schizophrenia from the premorbid to the postonset period: evidence from a population-representative longitudinal study. , 2014, The American journal of psychiatry.

[59]  A. Roe,et al.  Influence of parallel and orthogonal real lines on illusory contour perception. , 2010, Journal of neurophysiology.

[60]  P. Czobor,et al.  The multidimensional scale of independent functioning: a new instrument for measuring functional disability in psychiatric populations. , 2003, Schizophrenia bulletin.

[61]  D. Sheehan,et al.  The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. , 1998, The Journal of clinical psychiatry.

[62]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[63]  S. Kay,et al.  The positive and negative syndrome scale (PANSS) for schizophrenia. , 1987, Schizophrenia bulletin.

[64]  R. Wyatt,et al.  Measurement of premorbid adjustment in chronic schizophrenia. , 1982, Schizophrenia bulletin.