Too Many Trees to See the Forest: Performance, Event-related Potential, and Functional Magnetic Resonance Imaging Manifestations of Integrative Congenital Prosopagnosia

Neuropsychological, event-related potential (ERP), and functional magnetic resonance imaging (fMRI) methods were combined to provide a comprehensive description of performance and neurobiological profiles for K.W., a case of congenital prosopagnosia. We demonstrate that K.W.'s visual perception is characterized by almost unprecedented inability to identify faces, a large bias toward local features, and an extreme deficit in global/configural processing that is not confined to faces. This pattern could be appropriately labeled congenital integrative prosopagnosia, and accounts for some, albeit not all, cases of face recognition impairments without identifiable brain lesions. Absence of face selectivity is evident in both biological markers of face processing, fMRI (the fusiform face area [FFA]), and ERPs (N170). Nevertheless, these two neural signatures probably manifest different perceptual mechanisms. Whereas the N170 is triggered by the occurrence of physiognomic stimuli in the visual field, the deficient face-selective fMRI activation in the caudal brain correlates with the severity of global processing deficits. This correlation suggests that the FFA might be associated with global/configural computation, a crucial part of face identification.

[1]  Frederic Dick,et al.  Differential Lateralization for Words and Faces: Category or Psychophysics? , 2008, Journal of Cognitive Neuroscience.

[2]  N. F. Ramsey,et al.  Effects of cross-sex hormones on cerebral activation during language and mental rotation: An fMRI study in transsexuals , 2008, European Neuropsychopharmacology.

[3]  Ken Nakayama,et al.  Developmental prosopagnosia and the Benton Facial Recognition Test , 2004, Neurology.

[4]  Raya Ariel,et al.  Congenital Visual Agnosia and Prosopagnosia in a Child: A Case Report , 1996, Cortex.

[5]  M. Tarr,et al.  The N170 occipito‐temporal component is delayed and enhanced to inverted faces but not to inverted objects: an electrophysiological account of face‐specific processes in the human brain , 2000, Neuroreport.

[6]  Miranka Wirth,et al.  Encoding deficit during face processing within the right fusiform face area in schizophrenia , 2009, Psychiatry Research: Neuroimaging.

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

[8]  Galia Avidan,et al.  Implicit familiarity processing in congenital prosopagnosia. , 2008, Journal of neuropsychology.

[9]  Bruno Debruille,et al.  Brain potentials reveal covert facial recognition in prosopagnosia , 1989, Neuropsychologia.

[10]  I. Gauthier,et al.  How does the brain process upright and inverted faces? , 2002, Behavioral and cognitive neuroscience reviews.

[11]  P. Frank,et al.  Boston Studies in the Philosophy of Science , 1968 .

[12]  Kenneth F. Valyear,et al.  The fusiform face area is not sufficient for face recognition: Evidence from a patient with dense prosopagnosia and no occipital face area , 2006, Neuropsychologia.

[13]  M. Viggiano Event-related potentials in brain-injured patients with neuropsychological disorders: a review. , 1996, Journal of clinical and experimental neuropsychology.

[14]  Irene Daum,et al.  Event-related potentials reflect impaired face recognition in patients with congenital prosopagnosia , 2003, Neuroscience Letters.

[15]  D. Navon Forest before trees: The precedence of global features in visual perception , 1977, Cognitive Psychology.

[16]  Rachel Swainson,et al.  Implicit Processing of Global Information in Balint's Syndrome , 2004, Cortex.

[17]  Margot J. Taylor,et al.  N170 or N1? Spatiotemporal differences between object and face processing using ERPs. , 2004, Cerebral cortex.

[18]  J. Keenan,et al.  Perception of global facial geometry in the inversion effect and prosopagnosia , 2003, Neuropsychologia.

[19]  T. Allison,et al.  Electrophysiological Studies of Face Perception in Humans , 1996, Journal of Cognitive Neuroscience.

[20]  E. D. de Haan,et al.  A familial factor in the development of face recognition deficits. , 1999, Journal of clinical and experimental neuropsychology.

[21]  E. Haan,et al.  Behavioural and Physiological Evidence for Covert Face Recognition in a Prosopagnosic Patient , 1992, Cortex.

[22]  Ken Nakayama,et al.  Normal and abnormal face selectivity of the M170 response in developmental prosopagnosics , 2005, Neuropsychologia.

[23]  Bruno Rossion,et al.  Does physical interstimulus variance account for early electrophysiological face sensitive responses in the human brain? Ten lessons on the N170 , 2008, NeuroImage.

[24]  Galia Avidan,et al.  Detailed Exploration of Face-related Processing in Congenital Prosopagnosia: 1. Behavioral Findings , 2005, Journal of Cognitive Neuroscience.

[25]  M. Riesenhuber,et al.  Face processing in humans is compatible with a simple shape–based model of vision , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[26]  N. Sagiv,et al.  Structural Encoding of Human and Schematic Faces: Holistic and Part-Based Processes , 2001, Journal of Cognitive Neuroscience.

[27]  N. Kanwisher,et al.  Face perception: domain specific, not process specific. , 2004, Neuron.

[28]  Brad Duchaine,et al.  Dissociations of Face and Object Recognition in Developmental Prosopagnosia , 2005, Journal of Cognitive Neuroscience.

[29]  Maria A. Bobes,et al.  Covert Matching of Unfamiliar Faces in a Case of Prosopagnosia: an ERP Study , 2003, Cortex.

[30]  B. Duchaine,et al.  Developmental prosopagnosia with normal configural processing , 2000, Neuroreport.

[31]  L. Deouell,et al.  Cognitive Neuroscience: Selective visual streaming in face recognition: evidence from developmental prosopagnosia , 1999 .

[32]  J. Haxby,et al.  The distributed human neural system for face perception , 2000, Trends in Cognitive Sciences.

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

[34]  Lynn C. Robertson,et al.  Functional Plasticity in Ventral Temporal Cortex following Cognitive Rehabilitation of a Congenital Prosopagnosic , 2007, Journal of Cognitive Neuroscience.

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

[36]  A. Young,et al.  Faces Interfere with Name Classification in a Prosopagnosic Patient , 1987, Cortex.

[37]  Rafael Malach,et al.  Face-selective Activation in a Congenital Prosopagnosic Subject , 2003, Journal of Cognitive Neuroscience.

[38]  C. Deruelle,et al.  Attention to low- and high-spatial frequencies in categorizing facial identities, emotions and gender in children with autism , 2008, Brain and Cognition.

[39]  G. Rhodes Looking at Faces: First-Order and Second-Order Features as Determinants of Facial Appearance , 1988, Perception.

[40]  J. Keenan,et al.  Lesions of the fusiform face area impair perception of facial configuration in prosopagnosia , 2002, Neurology.

[41]  L. Deouell,et al.  STRUCTURAL ENCODING AND IDENTIFICATION IN FACE PROCESSING: ERP EVIDENCE FOR SEPARATE MECHANISMS , 2000, Cognitive neuropsychology.

[42]  Jason J S Barton,et al.  The covert priming effect of faces in prosopagnosia , 2004, Neurology.

[43]  B. de Gelder,et al.  Configural face processes in acquired and developmental prosopagnosia: evidence for two separate face systems? , 2000, Neuroreport.

[44]  Mariya V. Cherkasova,et al.  Covert recognition in acquired and developmental prosopagnosia , 2001, Neurology.

[45]  Beatrice de Gelder,et al.  Out of Mind : Varieties of Unconscious Processes , 2001 .

[46]  Galit Yovel,et al.  Specialized Face Perception Mechanisms Extract Both Part and Spacing Information: Evidence from Developmental Prosopagnosia , 2006, Journal of Cognitive Neuroscience.

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

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

[49]  R A McCarthy,et al.  Prosopagnosia and structural encoding of faces: evidence from event-related potentials. , 1999, Neuroreport.

[50]  T Yamamoto,et al.  Selective impairment of facial recognition due to a haematoma restricted to the right fusiform and lateral occipital region , 2001, Journal of neurology, neurosurgery, and psychiatry.

[51]  T. Allison,et al.  Face-Specific Processing in the Human Fusiform Gyrus , 1997, Journal of Cognitive Neuroscience.

[52]  D. Levine,et al.  Prosopagnosia: A defect in visual configural processing , 1989, Brain and Cognition.

[53]  J. Tanaka,et al.  Features and their configuration in face recognition , 1997, Memory & cognition.

[54]  Galia Avidan,et al.  Functional MRI Reveals Compromised Neural Integrity of the Face Processing Network in Congenital Prosopagnosia , 2009, Current Biology.

[55]  Andrea Weidenfeld,et al.  An evaluation of two commonly used tests of unfamiliar face recognition , 2003, Neuropsychologia.

[56]  M. Farah,et al.  What is "special" about face perception? , 1998, Psychological review.

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

[58]  Chris Rorden,et al.  The fate of global information in dorsal simultanagnosia , 2000 .

[59]  M. Behrmann,et al.  Congenital prosopagnosia: face-blind from birth , 2005, Trends in Cognitive Sciences.

[60]  T. Allison,et al.  Electrophysiological studies of human face perception. I: Potentials generated in occipitotemporal cortex by face and non-face stimuli. , 1999, Cerebral cortex.

[61]  R. Malach,et al.  The topography of high-order human object areas , 2002, Trends in Cognitive Sciences.

[62]  Lynn C. Robertson,et al.  Processing the Trees and the Forest during Initial Stages of Face Perception: Electrophysiological Evidence , 2006, Journal of Cognitive Neuroscience.

[63]  Irene Daum,et al.  Developmental Prosopagnosia: A Review , 2003, Behavioural neurology.

[64]  H. R. Bliem,et al.  Direct evidence for a consistent dissociation between structural facial discrimination and facial individuation in prosopagnosia , 1999 .

[65]  K. Nakayama,et al.  The Cambridge Face Memory Test: Results for neurologically intact individuals and an investigation of its validity using inverted face stimuli and prosopagnosic participants , 2006, Neuropsychologia.

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

[67]  D. Navon What does a compound letter tell the psychologist's mind? , 2003, Acta psychologica.

[68]  Jack Honvank,et al.  Conscious and unconscious processing of emotional faces , 2001 .

[69]  Rafael Malach,et al.  Detailed Exploration of Face-related Processing in Congenital Prosopagnosia: 2. Functional Neuroimaging Findings , 2005, Journal of Cognitive Neuroscience.

[70]  Ken Nakayama,et al.  Psychosocial consequences of developmental prosopagnosia: a problem of recognition. , 2008, Journal of psychosomatic research.

[71]  Glyn W. Humphreys,et al.  Visual and Spatial Short-term Memory in Integrative Agnosia , 2003, Cognitive neuropsychology.

[72]  D. Maurer,et al.  The many faces of configural processing , 2002, Trends in Cognitive Sciences.

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

[74]  Nouchine Hadjikhani,et al.  Neural basis of prosopagnosia: An fMRI study , 2002, Human brain mapping.

[75]  Robert D. Jones,et al.  Severe Developmental Prosopagnosia in a Child With Superior Intellect , 2001, Journal of clinical and experimental neuropsychology.