Bilateral hemispheric processing of words and faces: evidence from word impairments in prosopagnosia and face impairments in pure alexia.

Considerable research has supported the view that faces and words are subserved by independent neural mechanisms located in the ventral visual cortex in opposite hemispheres. On this view, right hemisphere ventral lesions that impair face recognition (prosopagnosia) should leave word recognition unaffected, and left hemisphere ventral lesions that impair word recognition (pure alexia) should leave face recognition unaffected. The current study shows that neither of these predictions was upheld. A series of experiments characterizing speed and accuracy of word and face recognition were conducted in 7 patients (4 pure alexic, 3 prosopagnosic) and matched controls. Prosopagnosic patients revealed mild but reliable word recognition deficits, and pure alexic patients demonstrated mild but reliable face recognition deficits. The apparent comingling of face and word mechanisms is unexpected from a domain-specific perspective, but follows naturally as a consequence of an interactive, learning-based account in which neural processes for both faces and words are the result of an optimization procedure embodying specific computational principles and constraints.

[1]  Isabel Gauthier,et al.  Perceptual Expertise Effects Are Not All or None: Spatially Limited Perceptual Expertise for Faces in a Case of Prosopagnosia , 2006, Journal of Cognitive Neuroscience.

[2]  Stéphane Lehéricy,et al.  The pathophysiology of letter-by-letter reading , 2004, Neuropsychologia.

[3]  M. Tarr,et al.  Activation of the middle fusiform 'face area' increases with expertise in recognizing novel objects , 1999, Nature Neuroscience.

[4]  D. Plaut,et al.  A LITERATURE REVIEW AND NEW DATA SUPPORTING AN INTERACTIVE ACCOUNT OF LETTER-BY-LETTER READING. , 1998, Cognitive neuropsychology.

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

[6]  D. Plaut Graded modality-specific specialisation in semantics: A computational account of optic aphasia , 2002, Cognitive neuropsychology.

[7]  Martha J. Farah,et al.  Associative Visual Agnosia and Alexia Without Prosopagnosia , 1994, Cortex.

[8]  A. Mechelli,et al.  Reading and reading disturbance , 2005, Current Opinion in Neurobiology.

[9]  Mark A. Williams,et al.  Abnormal Configural Face Perception in a Patient with Right Anterior Temporal Lobe Atrophy , 2006, Neurocase.

[10]  M. Behrmann,et al.  Visual complexity in letter-by-letter reading: Pure alexia is not pure , 1998, Neuropsychologia.

[11]  S. Dehaene,et al.  Cultural Recycling of Cortical Maps , 2007, Neuron.

[12]  Marlene Behrmann,et al.  Impairments in part–whole representations of objects in two cases of integrative visual agnosia , 2007, Cognitive neuropsychology.

[13]  J Sergent,et al.  Functional and anatomical decomposition of face processing: evidence from prosopagnosia and PET study of normal subjects. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[14]  Andrew Kirk,et al.  CONTRIBUTIONS TO NEUROPSYCHOLOGICAL ASSESSMENT. 2nd Edition. 1994. By Arthur L. Benton, Abigail B. Sivan, Kerry deS. Hamsher, Nils R. Varney and Otfried Spreen. Published by Oxford University Press. 159 pages. $C34.95 , 1996 .

[15]  S. Dehaene,et al.  Visual word recognition in the left and right hemispheres: anatomical and functional correlates of peripheral alexias. , 2003, Cerebral cortex.

[16]  Martha J. Farah,et al.  Face perception and within-category discrimination in prosopagnosia , 1995, Neuropsychologia.

[17]  K. Grill-Spector,et al.  High-resolution imaging reveals highly selective nonface clusters in the fusiform face area , 2006, Nature Neuroscience.

[18]  M. Tarr,et al.  Can Face Recognition Really be Dissociated from Object Recognition? , 1999, Journal of Cognitive Neuroscience.

[19]  R. Goebel,et al.  Individual faces elicit distinct response patterns in human anterior temporal cortex , 2007, Proceedings of the National Academy of Sciences.

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

[21]  T. Allison,et al.  Human extrastriate visual cortex and the perception of faces, words, numbers, and colors. , 1994, Cerebral cortex.

[22]  J. Ogden Dyslexia in a right-handed patient with a posterior lesion of the right cerebral hemisphere , 1984, Neuropsychologia.

[23]  Marlene Behrmann,et al.  Probing the face-space of individuals with prosopagnosia , 2010, Neuropsychologia.

[24]  J. Sergent,et al.  Functional neuroanatomy of face and object processing. A positron emission tomography study. , 1992, Brain : a journal of neurology.

[25]  Galit Yovel,et al.  The asymmetry of the fusiform face area is a stable individual characteristic that underlies the left-visual-field superiority for faces , 2008, Neuropsychologia.

[26]  N. Kanwisher,et al.  The fusiform face area is selective for faces not animals. , 1999, Neuroreport.

[27]  Stanislas Dehaene,et al.  Specialization within the ventral stream: the case for the visual word form area , 2004, NeuroImage.

[28]  Seth E. Bouvier,et al.  Behavioral deficits and cortical damage loci in cerebral achromatopsia. , 2006, Cerebral cortex.

[29]  Isabel Gauthier,et al.  Behavioral Change and Its Neural Correlates in Visual Agnosia After Expertise Training , 2005, Journal of Cognitive Neuroscience.

[30]  Cheryl L. Grady,et al.  Mapping the functional neuroanatomy of the intact human brain with brain work imaging , 1991, Neuropsychologia.

[31]  D. Plaut,et al.  The neural basis of visual word form processing: a multivariate investigation. , 2013, Cerebral cortex.

[32]  O. Selnes A Compendium of Neuropsychological Tests , 1991, Neurology.

[33]  A. O'Toole,et al.  Stimulus-specific effects in face recognition over changes in viewpoint , 1998, Vision Research.

[34]  H. Kaiser,et al.  [Visual object and space perception battery: normal values for children from 8 to 12]. , 2004, Klinische Monatsblatter fur Augenheilkunde.

[35]  M Behrmann,et al.  The effects of rotation and inversion on face processing in prosopagnosia , 2002, Cognitive neuropsychology.

[36]  James L. McClelland,et al.  A computational model of semantic memory impairment: modality specificity and emergent category specificity. , 1991 .

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

[38]  A. Stringer,et al.  Short forms of the Benton Judgment of Line Orientation Test: development and psychometric properties. , 2000, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[39]  Bruno Rossion,et al.  Hemispheric Asymmetries for Whole-Based and Part-Based Face Processing in the Human Fusiform Gyrus , 2000, Journal of Cognitive Neuroscience.

[40]  Marlene Behrmann,et al.  Notice Warning concerning Copyright Restrictions Cognitive Neuropsychology Pure Alexia and Covert Reading: Evidence from Stroop Tasks Pure Alexia and Covert Reading: Evidence from Stroop Tasks , 2022 .

[41]  Bruno Rossion,et al.  Holistic processing impairment can be restricted to faces in acquired prosopagnosia: evidence from the global/local Navon effect. , 2011, Journal of neuropsychology.

[42]  M. Farah,et al.  Neural Specialization for Letter Recognition , 2002, Journal of Cognitive Neuroscience.

[43]  Joachim Bodamer,et al.  Die Prosop-Agnosie , 2004, Archiv für Psychiatrie und Nervenkrankheiten.

[44]  Mark H. Johnson Interactive Specialization: A domain-general framework for human functional brain development? , 2011, Developmental Cognitive Neuroscience.

[45]  Bruno Rossion,et al.  Acquired prosopagnosia abolishes the face inversion effect , 2010, Cortex.

[46]  T. Allison,et al.  Differential Sensitivity of Human Visual Cortex to Faces, Letterstrings, and Textures: A Functional Magnetic Resonance Imaging Study , 1996, The Journal of Neuroscience.

[47]  E. DeYoe,et al.  Visual Object Agnosia and Pure Word Alexia: Correlation of Functional Magnetic Resonance Imaging and Lesion Localization , 2004, Journal of computer assisted tomography.

[48]  Galia Avidan,et al.  Reduced structural connectivity in ventral visual cortex in congenital prosopagnosia , 2009, Nature Neuroscience.

[49]  M. Behrmann,et al.  Rehabilitation for Pure Alexia: Efficacy of Therapy and Implications for Models of Normal Word Recognition , 1995 .

[50]  Marlene Behrmann,et al.  The joint development of hemispheric lateralization for words and faces. , 2012, Journal of experimental psychology. General.

[51]  Johan Wagemans,et al.  RETRACTED: The visual word form area is organized according to orthography , 2012, NeuroImage.

[52]  C. Marra,et al.  Human Neuroscience , 2022 .

[53]  J. Avery Critical review. , 2006, The Journal of the Arkansas Medical Society.

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

[55]  Sabine Kastner,et al.  The functional neuroanatomy of object agnosia: A case study , 2010 .

[56]  Marlene Behrmann,et al.  Unraveling the distributed neural code of facial identity through spatiotemporal pattern analysis , 2011, Proceedings of the National Academy of Sciences.

[57]  L. Cohen,et al.  The neural bases of prosopagnosia and pure alexia: recent insights from functional neuroimaging , 2006, Current opinion in neurology.

[58]  R. Tootell,et al.  An anterior temporal face patch in human cortex, predicted by macaque maps , 2009, Proceedings of the National Academy of Sciences.

[59]  C. Genovese,et al.  A functional MRI study of face recognition in patients with prosopagnosia , 2001, Neuroreport.

[60]  Elinor McKone,et al.  Are Faces Special , 2011 .

[61]  Alexander P. Leff,et al.  Too Little, Too Late: Reduced Visual Span and Speed Characterize Pure Alexia , 2009, Cerebral cortex.

[62]  O. Koenig,et al.  Separable Mechanisms in Face Processing: Evidence from Hemispheric Specialization , 1991, Journal of Cognitive Neuroscience.

[63]  Bryan R. Conroy,et al.  A Common, High-Dimensional Model of the Representational Space in Human Ventral Temporal Cortex , 2011, Neuron.

[64]  Galia Avidan,et al.  A detailed investigation of facial expression processing in congenital prosopagnosia as compared to acquired prosopagnosia , 2006, Experimental Brain Research.

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

[66]  J. Barton Structure and function in acquired prosopagnosia: lessons from a series of 10 patients with brain damage. , 2008, Journal of neuropsychology.

[67]  Russell A. Epstein Cognitive Neuroscience: Scene Layout from Vision and Touch , 2011, Current Biology.

[68]  T. V. Sewards Neural structures and mechanisms involved in scene recognition: A review and interpretation , 2011, Neuropsychologia.

[69]  Rebecca F. Schwarzlose,et al.  Separate Face and Body Selectivity on the Fusiform Gyrus , 2005, The Journal of Neuroscience.

[70]  J. C. Meadows The anatomical basis of prosopagnosia , 1974, Journal of neurology, neurosurgery, and psychiatry.

[71]  Russell A. Epstein,et al.  The Parahippocampal Place Area Recognition, Navigation, or Encoding? , 1999, Neuron.

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

[73]  M. Tagamets,et al.  A Parametric Approach to Orthographic Processing in the Brain: An fMRI Study , 2000, Journal of Cognitive Neuroscience.

[74]  R. Kimchi,et al.  What does visual agnosia tell us about perceptual organization and its relationship to object perception? , 2003, Journal of experimental psychology. Human perception and performance.

[75]  C. Price,et al.  The Interactive Account of ventral occipitotemporal contributions to reading , 2011, Trends in Cognitive Sciences.

[76]  F. Boller,et al.  Trancortical alexia with agraphia folowing a right temporo-occipital hematoma in a right-handed patient , 1994, Neuropsychologia.

[77]  Galia Avidan,et al.  Impaired holistic processing in congenital prosopagnosia , 2011, Neuropsychologia.

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

[79]  Stephen Jose Hanson,et al.  High-resolution imaging of the fusiform face area (FFA) using multivariate non-linear classifiers shows diagnosticity for non-face categories , 2011, NeuroImage.

[80]  J. Grafman,et al.  A Case of Prosopagnosia Following Moderate Closed Head Injury with Left Hemisphere Focal Lesion , 2000, Cortex.

[81]  Leslie G. Ungerleider,et al.  The Representation of Objects in the Human Occipital and Temporal Cortex , 2000, Journal of Cognitive Neuroscience.

[82]  M. Tarr,et al.  DOES VISUAL SUBORDINATE-LEVEL CATEGORISATION ENGAGE THE FUNCTIONALLY DEFINED FUSIFORM FACE AREA? , 2000, Cognitive neuropsychology.

[83]  CJ Price,et al.  Selective activation around the left occipito-temporal sulcus for words relative to pictures: Individual variability or false positives? , 2007 .

[84]  S. Rombouts,et al.  Selective activation around the left occipito‐temporal sulcus for words relative to pictures: Individual variability or false positives? , 2007, Human brain mapping.

[85]  T. Shallice,et al.  Pure Alexia: A Nonspatial Visual Disorder Affecting Letter Activation , 1995 .

[86]  M. Freedman,et al.  Associative (prosop)agnosia without (apparent) perceptual deficits: A case-study , 2007, Neuropsychologia.

[87]  D. Plaut,et al.  Complementary neural representations for faces and words: A computational exploration , 2011, Cognitive neuropsychology.

[88]  M. Sigman,et al.  Opinion TRENDS in Cognitive Sciences Vol.9 No.7 July 2005 The neural code for written words: a proposal , 2022 .

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

[90]  Gaurav Singal,et al.  Lateralization of face processing in the human brain , 2012, Proceedings of the Royal Society B: Biological Sciences.

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

[92]  Steven Z. Rapcsak,et al.  Efficient Visual Object and Word Recognition Relies on High Spatial Frequency Coding in the Left Posterior Fusiform Gyrus: Evidence from a Case-Series of Patients with Ventral Occipito-Temporal Cortex Damage , 2012, Cerebral cortex.

[93]  J. Haxby,et al.  Neural systems for recognition of familiar faces , 2007, Neuropsychologia.

[94]  Roel M. Willems,et al.  Cerebral lateralization of face-selective and body-selective visual areas depends on handedness. , 2010, Cerebral cortex.

[95]  H. Coslett,et al.  Reading with the Right-Hemisphere: Evidence from Transcranial Magnetic Stimulation , 1994, Brain and Language.

[96]  T. Nazir,et al.  Reading habits, perceptual learning, and recognition of printed words , 2004, Brain and Language.

[97]  V. Bruce,et al.  The basis of the 3/4 view advantage in face recognition , 1987 .

[98]  James L. McClelland,et al.  No Right to Speak? The Relationship between Object Naming and Semantic Impairment:Neuropsychological Evidence and a Computational Model , 2001, Journal of Cognitive Neuroscience.

[99]  Mary A. Peterson,et al.  Reduction in white matter connectivity, revealed by diffusion tensor imaging, may account for age-related changes in face perception , 2008 .

[100]  M. Montant,et al.  Phonological Activation in Pure Alexia , 2001, Cognitive neuropsychology.

[101]  J. Greene Contributions to Neuropsychological Assessment , 1995 .

[102]  M. Behrmann,et al.  The evolution of pure alexia: A longitudinal study of recovery , 1990, Brain and Language.

[103]  Ferath Kherif,et al.  Automatic Top-Down Processing Explains Common Left Occipito-Temporal Responses to Visual Words and Objects , 2010, Cerebral cortex.

[104]  M. Behrmann,et al.  Number reading in pure alexia—A review , 2011, Neuropsychologia.

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

[106]  Valerie A. Carr,et al.  Spatiotemporal Dynamics of Modality-Specific and Supramodal Word Processing , 2003, Neuron.

[107]  H. Kucera,et al.  Computational analysis of present-day American English , 1967 .

[108]  Martin Kronbichler,et al.  The visual word form area and the frequency with which words are encountered: evidence from a parametric fMRI study , 2004, NeuroImage.

[109]  Thad A Polk,et al.  Functional MRI evidence for an abstract, not perceptual, word-form area. , 2002, Journal of experimental psychology. General.

[110]  C. Gilbert,et al.  Top-Down Reorganization of Activity in the Visual Pathway after Learning a Shape Identification Task , 2005, Neuron.

[111]  A. Ishai,et al.  Distributed neural systems for the generation of visual images , 2000, NeuroImage.

[112]  G. V. Van Hoesen,et al.  Prosopagnosia , 1982, Neurology.

[113]  S. Dehaene,et al.  The unique role of the visual word form area in reading , 2011, Trends in Cognitive Sciences.

[114]  Mark H. Johnson,et al.  Oxford Handbook of Face Perception , 2011 .

[115]  Paul H. Garthwaite,et al.  Statistical Methods for Single-Case Studies in Neuropsychology: Comparing the Slope of a Patient's Regression Line with those of a Control Sample , 2004, Cortex.

[116]  Ralph Adolphs,et al.  The neuropsychology of face perception: beyond simple dissociations and functional selectivity , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[117]  Jason J S Barton,et al.  Disorder of higher visual function. , 2011, Current opinion in neurology.

[118]  Christian Gerlach,et al.  The Visual What For Area: Words and pictures in the left fusiform gyrus , 2007, NeuroImage.

[119]  M. Sereno,et al.  Dissociation of Sensitivity to Spatial Frequency in Word and Face Preferential Areas of the Fusiform Gyrus , 2011, Cerebral cortex.

[120]  N. Kanwisher Functional specificity in the human brain: A window into the functional architecture of the mind , 2010, Proceedings of the National Academy of Sciences.

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

[122]  Joseph T Devlin,et al.  The myth of the visual word form area , 2003, NeuroImage.

[123]  Mariano Sigman,et al.  Hierarchical Coding of Letter Strings in the Ventral Stream: Dissecting the Inner Organization of the Visual Word-Form System , 2007, Neuron.

[124]  Monica Baciu,et al.  A Functional MRI Study of the Ver , 2003 .

[125]  Daniel D. Dilks,et al.  A critical review of the development of face recognition: Experience is less important than previously believed , 2012, Cognitive neuropsychology.

[126]  A. Young,et al.  Understanding face recognition. , 1986, British journal of psychology.

[127]  Jason J S Barton,et al.  What is Meant by Impaired Configural Processing in Acquired Prosopagnosia? , 2009, Perception.