The Anatomy of Object Recognition—Visual Form Agnosia Caused by Medial Occipitotemporal Stroke

The influential model on visual information processing by Milner and Goodale (1995) has suggested a dissociation between action- and perception-related processing in a dorsal versus ventral stream projection. It was inspired substantially by the observation of a double dissociation of disturbed visual action versus perception in patients with optic ataxia on the one hand and patients with visual form agnosia (VFA) on the other. Unfortunately, almost all cases with VFA reported so far suffered from inhalational intoxication, the majority with carbon monoxide (CO). Since CO induces a diffuse and widespread pattern of neuronal and white matter damage throughout the whole brain, precise conclusions from these patients with VFA on the selective role of ventral stream structures for shape and orientation perception were difficult. Here, we report patient J.S., who demonstrated VFA after a well circumscribed brain lesion due to stroke etiology. Like the famous patient D.F. with VFA after CO intoxication studied by Milner, Goodale, and coworkers (Goodale et al., 1991, 1994; Milner et al., 1991; Servos et al., 1995; Mon-Williams et al., 2001a,b; Wann et al., 2001; Westwood et al., 2002; McIntosh et al., 2004; Schenk and Milner, 2006), J.S. showed an obvious dissociation between disturbed visual perception of shape and orientation information on the one side and preserved visuomotor abilities based on the same information on the other. In both hemispheres, damage primarily affected the fusiform and the lingual gyri as well as the adjacent posterior cingulate gyrus. We conclude that these medial structures of the ventral occipitotemporal cortex are integral for the normal flow of shape and of contour information into the ventral stream system allowing to recognize objects.

[1]  S. Kastner,et al.  Two hierarchically organized neural systems for object information in human visual cortex , 2008, Nature Neuroscience.

[2]  Cheng-Yu Chen,et al.  Brain injury after acute carbon monoxide poisoning: early and late complications. , 2007, AJR. American journal of roentgenology.

[3]  T. Schenk,et al.  An allocentric rather than perceptual deficit in patient D.F. , 2006, Nature Neuroscience.

[4]  Thomas Schenk,et al.  Concurrent visuomotor behaviour improves form discrimination in a patient with visual form agnosia , 2006, The European journal of neuroscience.

[5]  M. Perenin,et al.  Cortical control of visually guided reaching: evidence from patients with optic ataxia. , 2005, Cerebral cortex.

[6]  Paul H Garthwaite,et al.  Testing for suspected impairments and dissociations in single-case studies in neuropsychology: evaluation of alternatives using monte carlo simulations and revised tests for dissociations. , 2005, Neuropsychology.

[7]  A. Durak,et al.  Magnetic resonance imaging findings in chronic carbon monoxide intoxication , 2005, Acta radiologica.

[8]  Robert D. McIntosh,et al.  Grasping What is Graspable: Evidence from Visual form Agnosia , 2004, Cortex.

[9]  Jason J S Barton,et al.  Perceptual Functions in Prosopagnosia , 2004, Perception.

[10]  Ravi S. Menon,et al.  Behavioral and Neuroimaging Evidence for a Contribution of Color and Texture Information to Scene Classification in a Patient with Visual Form Agnosia , 2004, Journal of Cognitive Neuroscience.

[11]  N. Kanwisher,et al.  The fusiform face area subserves face perception, not generic within-category identification , 2004, Nature Neuroscience.

[12]  M. Goodale,et al.  Ventral occipital lesions impair object recognition but not object-directed grasping: an fMRI study. , 2003, Brain : a journal of neurology.

[13]  K. Chang,et al.  Delayed encephalopathy of acute carbon monoxide intoxication: diffusivity of cerebral white matter lesions. , 2003, AJNR. American journal of neuroradiology.

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

[15]  R. Mohs,et al.  Consortium to establish a registry for Alzheimer's disease (CERAD) clinical and neuropsychological assessment of Alzheimer's disease. , 2002, Psychopharmacology bulletin.

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

[17]  Melvyn A. Goodale,et al.  Grasping two-dimensional images and three-dimensional objects in visual-form agnosia , 2002, Experimental Brain Research.

[18]  N. Kanwisher,et al.  The Human Body , 2001 .

[19]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[20]  Robert D. McIntosh,et al.  The role of size and binocular information in guiding reaching: insights from virtual reality and visual form agnosia III (of III) , 2001, Experimental Brain Research.

[21]  Robert D. McIntosh,et al.  Vertical gaze angle as a distance cue for programming reaching: insights from visual form agnosia II (of III) , 2001, Experimental Brain Research.

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

[23]  H. Hampel,et al.  Zur praktischen Anwendung der CERAD-Testbatterie als neuropsychologisches Demenzscreening , 2001, Der Nervenarzt.

[24]  N. Kanwisher Domain specificity in face perception , 2000, Nature Neuroscience.

[25]  M. Tarr,et al.  FFA: a flexible fusiform area for subordinate-level visual processing automatized by expertise , 2000, Nature Neuroscience.

[26]  A. Milner Perception and action in visual form agnosia , 2000 .

[27]  I. Gauthier,et al.  Expertise for cars and birds recruits brain areas involved in face recognition , 2000, Nature Neuroscience.

[28]  D. F. Benson,et al.  Visual form agnosia , 2000 .

[29]  R. V. Abadi,et al.  Visual performance in a case of visual agnosia , 2000 .

[30]  D M Reboussin,et al.  A comparison of fast spin-echo, fluid-attenuated inversion-recovery, and diffusion-weighted MR imaging in the first 10 days after cerebral infarction. , 1999, AJNR. American journal of neuroradiology.

[31]  D. C. Howell,et al.  Comparing an Individual's Test Score Against Norms Derived from Small Samples , 1998 .

[32]  H. Chris Dijkerman,et al.  Grasping Spatial Relationships: Failure to Demonstrate Allocentric Visual Coding in a Patient with Visual Form Agnosia , 1998, Consciousness and Cognition.

[33]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[34]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[35]  K. Uemura,et al.  MRI of acute cerebral infarction: a comparison of FLAIR and T2-weighted fast spin-echo imaging , 1997, Neuroradiology.

[36]  Josh H. McDermott,et al.  Functional imaging of human visual recognition. , 1996, Brain research. Cognitive brain research.

[37]  D Atkinson,et al.  Fluid-attenuated inversion recovery (FLAIR) for assessment of cerebral infarction. Initial clinical experience in 50 patients. , 1996, Stroke.

[38]  M A Goodale,et al.  Dissociation between two modes of spatial processing by a visual form agnosic , 1995, Neuroreport.

[39]  T. Allison,et al.  Face-sensitive regions in human extrastriate cortex studied by functional MRI. , 1995, Journal of neurophysiology.

[40]  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.

[41]  H. Bülthoff,et al.  Separate neural pathways for the visual analysis of object shape in perception and prehension , 1994, Current Biology.

[42]  Andrew Blake,et al.  Computational modelling of hand-eye coordination , 1992 .

[43]  G. Ferrigno,et al.  Comparison between the more recent techniques for smoothing and derivative assessment in biomechanics , 1992, Medical and Biological Engineering and Computing.

[44]  F. Drislane,et al.  A historic case of visual agnosia revisited after 40 years. , 1991, Brain : a journal of neurology.

[45]  T. R. Jordan,et al.  Perception and action in 'visual form agnosia'. , 1991, Brain : a journal of neurology.

[46]  L. Jakobson,et al.  A neurological dissociation between perceiving objects and grasping them , 1991, Nature.

[47]  J. Morris,et al.  The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part I. Clinical and neuropsychological assesment of Alzheimer's disease , 1989, Neurology.

[48]  John Campion,et al.  Apperceptive agnosia due to carbon monoxide poisoning. An interpretation based on critical band masking from disseminated lesions , 1985, Behavioural Brain Research.

[49]  D. Benson,et al.  Visual recognition through kinaesthetic mediation , 1982, Psychological Medicine.

[50]  A. Adler DISINTEGRATION AND RESTORATION OF OPTIC RECOGNITION IN VISUAL AGNOSIA: ANALYSIS OF A CASE , 1944 .

[51]  Y. Hsü,et al.  CEREBRAL SUBCORTICAL MYELINOPATHY IN CARBON MONOXIDE POISONING , 1938 .

[52]  P. Downing,et al.  Selectivity for the human body in the fusiform gyrus. , 2005, Journal of neurophysiology.

[53]  James R. Tresilian,et al.  Monocular and binocular distance cues: insights from visual form agnosia I (of III) , 2001, Experimental Brain Research.

[54]  M. Goodale,et al.  The visual brain in action , 1995 .

[55]  M. Arbib,et al.  Opposition Space as a Structuring Concept for the Analysis of Skilled Hand Movements , 1986 .

[56]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

[57]  D. Benson,et al.  Visual form agnosia. A specific defect in visual discrimination. , 1969, Archives of neurology.

[58]  R. Efron,et al.  What is Perception , 1969 .

[59]  D. Benson,et al.  Visual form agnosia: a specific defect in visual recognition. , 1968, Transactions of the American Neurological Association.

[60]  Benson Df,et al.  Visual form agnosia: a specific defect in visual recognition. , 1968 .

[61]  M. Fardeau,et al.  The central nervous system and carbon monoxide poisoning. II. Anatomical study of brain lesions following intoxication with carbon monixide (22 cases). , 1967, Progress in brain research.

[62]  A. Adler Course and outcome of visual agnosia. , 1950, The Journal of nervous and mental disease.