Specialization within the ventral stream: the case for the visual word form area

Is there specialization for visual word recognition within the visual ventral stream of literate human adults? We review the evidence for a specialized "visual word form area" and critically examine some of the arguments recently placed against this hypothesis. Three distinct forms of specialization must be distinguished: functional specialization, reproducible localization, and regional selectivity. Examination of the literature with this theoretical division in mind indicates that reading activates a precise subpart of the left ventral occipitotemporal sulcus, and that patients with pure alexia consistently exhibit lesions of this region (reproducible localization). Second, this region implements processes adequate for reading in a specific script, such as invariance across upper- and lower-case letters, and its lesion results in the selective loss of reading-specific processes (functional specialization). Third, the issue of regional selectivity, namely, the existence of putative cortical patches dedicated to letter and word recognition, cannot be resolved by positron emission tomography or lesion data, but requires high-resolution neuroimaging techniques. The available evidence from single-subject fMRI and intracranial recordings suggests that some cortical sites respond preferentially to letter strings than to other categories of visual stimuli such as faces or objects, though the preference is often relative rather than absolute. We conclude that learning to read results in the progressive development of an inferotemporal region increasingly responsive to visual words, which is aptly named the visual word form area (VWFA).

[1]  C. J. Price,et al.  Cortical localisation of the visual and auditory word form areas: A reconsideration of the evidence , 2003, Brain and Language.

[2]  R. Desimone,et al.  Clustering of perirhinal neurons with similar properties following visual experience in adult monkeys , 2000, Nature Neuroscience.

[3]  S. Dehaene,et al.  The visual word form area: a prelexical representation of visual words in the fusiform gyrus , 2002, Neuroreport.

[4]  Alfonso Caramazza,et al.  VARIETIES OF PURE ALEXIA: THE CASE OF FAILURE TO ACCESS GRAPHEMIC REPRESENTATIONS. , 1998, Cognitive neuropsychology.

[5]  K Patterson,et al.  Letter-by-letter reading: psychological descriptions of a neurological syndrome. , 1995, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[6]  Michal Lavidor,et al.  Analysis of standard and non-standard visual word format in the two hemispheres , 2001, Neuropsychologia.

[7]  C. Frith,et al.  Inattentional blindness versus inattentional amnesia for fixated but ignored words. , 1999, Science.

[8]  S. Blumstein,et al.  The Role of Segmentation in Phonological Processing: An fMRI Investigation , 2000, Journal of Cognitive Neuroscience.

[9]  M. Albert,et al.  Associative visual agnosia without alexia , 1975, Neurology.

[10]  Pierre A. Hallé,et al.  Where Is the /b/ in “absurde” [apsyrd]? It Is in French Listeners' Minds , 2000 .

[11]  S. Greenblatt,et al.  Alexia without agraphia or hemianopsia. Anatomical analysis of an autopsied case , 2000 .

[12]  Y. Yamane,et al.  Complex objects are represented in macaque inferotemporal cortex by the combination of feature columns , 2001, Nature Neuroscience.

[13]  Tatjana A. Nazir,et al.  Traces of Print Along the Visual Pathway , 2000 .

[14]  K. T. Spoehr,et al.  The role of orthographic and phonotactic rules in perceiving letter patterns. , 1975, Journal of experimental psychology. Human perception and performance.

[15]  Denis G. Pelli,et al.  The remarkable inefficiency of word recognition , 2003, Nature.

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

[17]  Martha J. Farah,et al.  Pure Alexia as a Visual Impairment: A Reconsideration , 1991 .

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

[19]  D. Beversdorf,et al.  Pure alexia: clinical-pathologic evidence for a lateralized visual language association cortex , 2000 .

[20]  N. Logothetis,et al.  Shape representation in the inferior temporal cortex of monkeys , 1995, Current Biology.

[21]  R. Snider Brain Mechanisms , 1965, Neurology.

[22]  M Coltheart,et al.  Basic processes in reading: computation of abstract letter identities. , 1984, Canadian journal of psychology.

[23]  S. Dehaene,et al.  Language-specific tuning of visual cortex? Functional properties of the Visual Word Form Area. , 2002, Brain : a journal of neurology.

[24]  A. Damasio,et al.  The anatomic basis of pure alexia , 1983, Neurology.

[25]  S Lehéricy,et al.  The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients. , 2000, Brain : a journal of neurology.

[26]  A. Gomori,et al.  Visual agnosia without alexia , 1984, Neurology.

[27]  Derek Besner,et al.  On the Role of Outline Shape and Word-Specific Visual Pattern in the Identification of Function Words: None , 1989 .

[28]  D. Bub,et al.  The Neural Substrate for Concrete, Abstract, and Emotional Word Lexica A Positron Emission Tomography Study , 1997, Journal of Cognitive Neuroscience.

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

[30]  R. Salmelin,et al.  Dynamics of visual feature analysis and object-level processing in face versus letter-string perception. , 2002, Brain : a journal of neurology.

[31]  Joel R. Meyer,et al.  Relation between brain activation and lexical performance , 2003, Human brain mapping.

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

[33]  G K Morley,et al.  Neurolinguistic analysis of the language abilities of a patient with a "double disconnection syndrome": a case of subangular alexia in the presence of mixed transcortical aphasia. , 1981, Journal of neurology, neurosurgery, and psychiatry.

[34]  J. Fletcher,et al.  Brain mechanisms for reading words and pseudowords: an integrated approach. , 2002, Cerebral cortex.

[35]  M. Tarr,et al.  The Fusiform Face Area is Part of a Network that Processes Faces at the Individual Level , 2000, Journal of Cognitive Neuroscience.

[36]  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.

[37]  S E Petersen,et al.  The processing of single words studied with positron emission tomography. , 1993, Annual review of neuroscience.

[38]  L. Cohen Number processing in pure alexia: The effect of hemispheric asymmetries and task demands , 1995 .

[39]  A. Castro-Caldas,et al.  Right hemifield alexia without hemianopia. , 1984, Archives of neurology.

[40]  Y. Miyashita,et al.  Neural organization for the long-term memory of paired associates , 1991, Nature.

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

[42]  T. Poggio,et al.  Hierarchical models of object recognition in cortex , 1999, Nature Neuroscience.

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

[44]  B. Weekes Differential Effects of Number of Letters on Word and Nonword Naming Latency , 1997 .

[45]  D. LeBihan,et al.  Modulation of Parietal Activation by Semantic Distance in a Number Comparison Task , 2001, NeuroImage.

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

[47]  J. Bowers,et al.  Orthographic, phonological, and articulatory contributions to masked letter and word priming. , 1998, Journal of experimental psychology. Human perception and performance.

[48]  Andrew W. Ellis,et al.  Word Length and Orthographic Neighborhood Size Effects in the Left and Right Cerebral Hemispheres , 2002, Brain and Language.

[49]  J. Ziegler,et al.  Orthography shapes the perception of speech: The consistency effect in auditory word recognition , 1998 .

[50]  T. Allison,et al.  Modulation of human extrastriate visual processing by selective attention to colours and words. , 1998, Brain : a journal of neurology.

[51]  D. Le Bihan,et al.  Visualizing the Neural Bases of a Disconnection Syndrome with Diffusion Tensor Imaging , 2002, Journal of Cognitive Neuroscience.

[52]  Mark S. Seidenberg,et al.  Multiple code activation in word recognition: evidence from rhyme monitoring. , 1981, Journal of experimental psychology. Human learning and memory.

[53]  A. Dale,et al.  Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. , 1998, Science.

[54]  T. Allison,et al.  Word recognition in the human inferior temporal lobe , 1994, Nature.

[55]  P. Skudlarski,et al.  Disruption of posterior brain systems for reading in children with developmental dyslexia , 2002, Biological Psychiatry.

[56]  S. Dehaene,et al.  The priming method: imaging unconscious repetition priming reveals an abstract representation of number in the parietal lobes. , 2001, Cerebral cortex.

[57]  S. Petersen,et al.  Activation of extrastriate and frontal cortical areas by visual words and word-like stimuli. , 1990, Science.

[58]  K. Uutela,et al.  Impaired visual word processing in dyslexia revealed with magnetoencephalography , 1996, Annals of neurology.

[59]  R. Frackowiak,et al.  Demonstrating the implicit processing of visually presented words and pseudowords. , 1996, Cerebral cortex.

[60]  Karl J. Friston,et al.  A multimodal language region in the ventral visual pathway , 1998, Nature.

[61]  James R. Booth,et al.  Functional Anatomy of Intra- and Cross-Modal Lexical Tasks , 2002, NeuroImage.

[62]  C. Price,et al.  The Constraints Functional Neuroimaging Places on Classical Models of Auditory Word Processing , 2001, Journal of Cognitive Neuroscience.

[63]  A. Toga,et al.  Mapping sulcal pattern asymmetry and local cortical surface gray matter distribution in vivo: maturation in perisylvian cortices. , 2002, Cerebral cortex.

[64]  R. Salmelin,et al.  Dynamics of letter string perception in the human occipitotemporal cortex. , 1999, Brain : a journal of neurology.

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

[66]  Elise Temple,et al.  Brain mechanisms in normal and dyslexic readers , 2002, Current Opinion in Neurobiology.

[67]  J. L. Nespoulous,et al.  Optic Aphasia with Pure Alexia: A Mild Form of Visual Associative Agnosia? A Case Study , 1998, Cortex.

[68]  E K Warrington,et al.  Prosopagnosia: A Face-Specific Disorder , 1993, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[69]  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.

[70]  A. Toga,et al.  Three-Dimensional Statistical Analysis of Sulcal Variability in the Human Brain , 1996, The Journal of Neuroscience.

[71]  T. Allison,et al.  Electrophysiological studies of human face perception. III: Effects of top-down processing on face-specific potentials. , 1999, Cerebral cortex.

[72]  E. Darcy Burgund,et al.  Letter-Case-Specific Priming in the Right Cerebral Hemisphere with a Form-Specific Perceptual Identification Task , 1997, Brain and Cognition.

[73]  U. Frith,et al.  Explicit and implicit processing of words and pseudowords by adult developmental dyslexics: A search for Wernicke's Wortschatz? , 1999, Brain : a journal of neurology.

[74]  Keiji Tanaka,et al.  Inferotemporal cortex and object vision. , 1996, Annual review of neuroscience.

[75]  S. Petersen,et al.  Effects of Lexicality, Frequency, and Spelling-to-Sound Consistency on the Functional Anatomy of Reading , 1999, Neuron.

[76]  Rafael Malach,et al.  Large-Scale Mirror-Symmetry Organization of Human Occipito-Temporal Object Areas , 2003, Neuron.

[77]  T. Hendler,et al.  A hierarchical axis of object processing stages in the human visual cortex. , 2001, Cerebral cortex.

[78]  A Yamadori,et al.  Dissociation of letter and picture naming resulting from callosal disconnection , 1998, Neurology.

[79]  Joël Pynte,et al.  Reading as a Perceptual Process , 2000 .

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

[81]  Daniel Holender,et al.  Differential Processing of Phonographic and Logographic Single-Digit Numbers by the Two Hemispheres , 2018, Mathematical Disabilities.

[82]  J. Dejerine,et al.  Contribution a l'etude anatomo-pathologique et clinique des differentes varietes de cecite verbale , 2000 .

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

[84]  J. Binder,et al.  The topography of callosal reading pathways. A case-control analysis. , 1992, Brain : a journal of neurology.

[85]  Joel R. Meyer,et al.  Modality independence of word comprehension , 2002, Human brain mapping.

[86]  J B Poline,et al.  Letter Binding and Invariant Recognition of Masked Words , 2004, Psychological science.

[87]  JAMES W. PAPEZ CEREBRAL MECHANISMS , 1939 .

[88]  Samuel H. Greenblatt Subangular alexia without agraphia or hemianopsia , 2000 .

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

[90]  K R Paap,et al.  Word shape's in poor shape for the race to the lexicon. , 1984, Journal of experimental psychology. Human perception and performance.

[91]  C. Koch,et al.  Category-specific visual responses of single neurons in the human medial temporal lobe , 2000, Nature Neuroscience.

[92]  Antonio R. Damasio,et al.  Pure alexia , 1983, Trends in Neurosciences.

[93]  Marcus Taft,et al.  The influence of orthography on phonological representations in the lexicon , 1985 .

[94]  V. Iragui,et al.  Alexia without agraphia or hemianopia in parietal infarction. , 1991, Journal of neurology, neurosurgery, and psychiatry.

[95]  G. Humphreys,et al.  Disruption to word or letter processing? The origins of case-mixing effects. , 1997, Journal of experimental psychology. Learning, memory, and cognition.

[96]  S. Edelman,et al.  Human Brain Mapping 6:316–328(1998) � A Sequence of Object-Processing Stages Revealed by fMRI in the Human Occipital Lobe , 2022 .

[97]  James L. McClelland,et al.  An interactive activation model of context effects in letter perception: Part 2. The contextual enhancement effect and some tests and extensions of the model. , 1982, Psychological review.

[98]  T. Nazir,et al.  Developing normal reading skills: aspects of the visual processes underlying word recognition. , 2000, Journal of experimental child psychology.

[99]  Richard J. Brown Neuropsychology Mental Structure , 1989 .

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

[101]  P. Pietrini,et al.  Conjoint and extended neural networks for the computation of speech codes: the neural basis of selective impairment in reading words and pseudowords. , 2001, Cerebral cortex.

[102]  M Ingvar,et al.  The illiterate brain. Learning to read and write during childhood influences the functional organization of the adult brain. , 1998, Brain : a journal of neurology.

[103]  T Shallice,et al.  Word-form dyslexia. , 1980, Brain : a journal of neurology.

[104]  Karalyn Patterson,et al.  Letter-by-letter Reading: Psychological Descriptions of a Neurologial Syndrome , 1982 .

[105]  G. M. Reicher Perceptual recognition as a function of meaninfulness of stimulus material. , 1969, Journal of experimental psychology.

[106]  F. Kitterle,et al.  Visual field effects in the discrimination of sine-wave gratings , 1991, Perception & psychophysics.

[107]  Keiji Tanaka,et al.  Optical Imaging of Functional Organization in the Monkey Inferotemporal Cortex , 1996, Science.

[108]  J B Poline,et al.  Cerebral mechanisms of word masking and unconscious repetition priming , 2001, Nature Neuroscience.

[109]  M. Behrmann,et al.  Impact of learning on representation of parts and wholes in monkey inferotemporal cortex , 2002, Nature Neuroscience.

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

[111]  J. Richard Hanley,et al.  Reading speed in pure alexia , 1996, Neuropsychologia.

[112]  Leslie G. Ungerleider,et al.  Object-form topology in the ventral temporal lobe Response to I. Gauthier (2000) , 2000, Trends in Cognitive Sciences.

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

[114]  K. Grill-Spector,et al.  fMR-adaptation: a tool for studying the functional properties of human cortical neurons. , 2001, Acta psychologica.