The neural bases of prosopagnosia and pure alexia: Recent insights from functional neuroimaging

Current Opinion in Neurology

Volumn 19, Issue 4, 2006, Pages 386-391

  Kleinschmidt, Andreas ^a,c   Cohen, Laurent ^a,b  

^a SERVICE HOSPITALIER FRÉDÉRIC JOLIOT   (France)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^c INSERM   (France)

Author keywords

Faces; Functional magnetic resonance imaging; Reading; Visual agnosia; Words

Indexed keywords

ALEXIA; BRAIN REGION; COGNITION; EVIDENCE BASED MEDICINE; FACE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; OCCIPITAL CORTEX; PHENOMENOLOGY; PROSOPAGNOSIA; READING; REVIEW; SENSORY NERVE; TEMPORAL CORTEX; VISION; VISUAL STIMULATION; WORD RECOGNITION;

DYSLEXIA; HUMANS; MAGNETIC RESONANCE IMAGING; PROSOPAGNOSIA; READING; RECOGNITION (PSYCHOLOGY);

EID: 33747368487     PISSN: 13507540     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.wco.0000236619.89710.ee     Document Type: Review

References (86)

1. Bodamer J. Die Prosopagnosie [in German]. Archiv für Psychiatrie und Nervenkrankheiten 1947; 179:6-53.
2. Dejerine J. Sur un cas de cecite verbale avec agraphie suivi d'autopsie [in French]. Mem Soc Biol 1891; 3:197-201.
3. Farah MJ. Visual agnosia. Cambridge: MIT Press; 1990.
4. Behrmann M, editor. Handbook of neuropsychology, vol. 4: disorders of visual behavior. 2nd ed. Amsterdam: Elsevier; 2001.
5. Barton JJ. Disorders of face perception and recognition. Neurol Clin 2003; 21:521-548.
6. Puce A, Allison T, Asgari M, et al. Differential sensitivity of human visual cortex to faces, letterstrings, and textures: a functional magnetic resonance imaging study. J Neurosci 1996; 16:5205-5215.
7. Kanwisher N, McDermott J, Chun M. The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 1997; 17:4302-4311.
8. Duchaine BC, Nakayama K. Developmental prosopagnosia: a window to content-specific face processing. Curr Opin Neurobiol 2006; 16:166-173. Excellent up-to-date review of congenital prosopagnosia covering all aspects from clinical phenomenology to neural and genetic bases.
9. Marotta JJ, Genovese CR, Behrmann M. A functional MRI study of face recognition in patients with prosopagnosia. Neuroreport 2001; 12:1581-1587.
10. Hadjikhani N, de Gelder B. Neural basis of prosopagnosia: an fMRI study. Hum Brain Mapp 2002; 16:176-182.
11. Avidan G, Hasson U, Malach R, Behrmann M. Detailed exploration of facerelated processing in congenital prosopagnosia: 2 Functional neuroimaging. J Cogn Neurosci 2005; 17:1150-1167. This detailed fMRI study failed to find differences in FFA responses between five patients with developmental prosopagnosia vs. control subjects across several activation tests.
12. von Kriegstein K, Kleinschmidt A, Giraud AL. Voice recognition and crossmodal responses to familiar speakers' voices in prosopagnosia. Cereb Cortex 2005 Nov 9. [Epub ahead of print]. An fMRI study with the interesting behavioral byproduct of finding voice recognition impairment in developmental prosopagnosia, suggesting that voice processing does not necessarily only compensate for prosopagnosia but can also suffer from it.
13. Rossion B, Caldara R, Seghier M, et al. A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. Brain 2003; 126:2381-2395.
14. Steeves JK, Culham JC, Duchaine BC, et al. The fusiform face area is not sufficient for face recognition: evidence from a patient with dense prosopagnosia and no occipital face area. Neuropsychologia 2006; 44:594-609.
15. Cox D, Meyers E, Sinha P. Contextually evoked object-specific responses in human visual cortex. Science 2004; 304:115-117.
16. Kilgour AR, Kitada R, Servos P, et al. Haptic face identification activates ventral occipital and temporal areas: an fMRI study. Brain Cogn 2005; 59:246-257.
17. von Kriegstein K, Kleinschmidt A, Sterzer P, Giraud AL. Interaction of face and voice areas during speaker recognition. J Cogn Neurosci 2005; 17:367-376. The authors observed FFA activation to voices as a function of task and familiarity with the speaker.
18. Wojciulik E, Kanwisher N, Driver J. Covert visual attention modulates face-specific activity in the human fusiform gyrus: fMRI study. J Neurophysiol 1998; 79:1574-1578.
19. Ishai A, Haxby JV, Ungerleider LG. Visual imagery of famous faces: effects of memory and attention revealed by fMRI. Neuroimage 2002; 17:1729-1741.
20. Schiltz C, Sorger B, Caldara R, et al. Impaired face discrimination in acquired prosopagnosia is associated with abnormal response to individual faces in right middle fusiform. Cereb Cortex 2006; 16:574-586. A clever approach to the question of whether lesional prosopagnosia affects identity coding in the FFA even if the structural lesion is outside the FFA and if the FFA stays responsive. The authors find that a lesion at least close to, if not in, the right OFA can cause a dysfunctional FFA response to identity, and as in previous work they emphasize the importance of putatively iterative processes across the OFA and FFA for face identification.
21. Vuilleumier P, Armony J, Driver J, Dolan R. Distinct spatial frequency sensitivities for processing faces and emotional expressions. Nat Neurosci 2003; 6:624-631.
22. Eger E, Schyns PG, Kleinschmidt A. Scale invariant adaptation in fusiform face-responsive regions. Neuroimage 2004; 22:232-242.
23. Andrews TJ, Ewbank MP. Distinct representations for facial identity and changeable aspects of faces in the human temporal lobe. Neuroimage 2004; 23:905-913.
24. Winston JS, Henson RN, Fine-Goulden MR, Dolan RJ. fMRI-adaptation reveals dissociable neural representations of identity and expression in face perception. J Neurophysiol 2004; 92:1830-1839.
25. Pourtois G, Schwartz S, Seghier ML, et al. Portraits or people? Distinct representations of face identity in the human visual cortex. J Cogn Neurosci 2005; 17:1043-1057. Evidence for at least partial rotational viewpoint invariance in FFA activity. Easier generalization from three-quarter views nicely parallels behavioral observations.
26. Rotshtein P, Henson RN, Treves A, et al. Morphing Marilyn into Maggie dissociates physical and identity face representations in the brain. Nat Neurosci 2005; 8:107-113. Well designed fMRI study showing that progressively higher levels of invariant face processing are related to a hierarchical neural architecture.
27. Loffler G, Yourganov G, Wilkinson F, Wilson HR. fMRI evidence for the neural representation of faces. Nat Neurosci 2005; 8:1386-1390. This fMRI study goes beyond response properties and provides support for mechanisms that might underpin face representation and identification. Behavioral and FFA results are compatible with coding in a face space.
28. Hoffman EA, Haxby JV. Distinct representations of eye gaze and identity in the distributed human neural system for face perception. Nat Neurosci 2000; 3:80-84.
29. Henson RN, Goshen-Gottstein Y, Ganel T, et al. Electrophysiological and haemodynamic correlates of face perception, recognition and priming. Cereb Cortex 2003; 13:793-805.
30. Grill-Spector K, Knouf N, Kanwisher N. The fusiform face area subserves face perception, not generic within-category identification. Nat Neurosci 2004; 7:555-562.
31. Pourtois G, Schwartz S, Seghier ML, et al. View-independent coding of face identity in frontal and temporal cortices is modulated by familiarity: an event-related fMRI study. Neuroimage 2005; 24:1214-1224.
32. Eger E, Schweinberger SR, Dolan RJ, Henson RN. Familiarity enhances invariance of face representations in human ventral visual cortex: fMRI evidence. Neuroimage 2005; 26:1128-1139.
33. Hasson U, Levy I, Behrmann M, et al. Eccentricity bias as an organizing principle for human high-order object areas. Neuron 2002; 34:479-490.
34. Cohen L, Dehaene S, Naccache L, 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. Brain 2000; 123:291-307.
35. Cohen L, Lehericy S, Chochon F, et al. Language-specific tuning of visual cortex? Functional properties of the Visual Word Form Area. Brain 2002; 125:1054-1069.
36. Dehaene S, Naccache L, Cohen L, et al. Cerebral mechanisms of word masking and unconscious repetition priming. Nat Neurosci 2001; 4:752-758.
37. Price CJ, Wise RJ, Frackowiak RS. Demonstrating the implicit processing of visually presented words and pseudowords. Cereb Cortex 1996; 6:62-70.
38. Dehaene S, Jobert A, Naccache L, et al. Letter binding and invariant recognition of masked words: behavioral and neuroimaging evidence. Psychol Sci 2004; 15:307-313.
39. Dehaene S, Cohen L, Sigman M, Vinckier F. The neural code for written words: a proposal. Trends Cogn Sci 2005; 9:335-341.
40. Flowers DL, Jones K, Noble K, et al. Attention to single letters activates left extrastriate cortex. Neuroimage 2004; 21:829-839.
41. Pernet C, Celsis P, Demonet JF. Selective response to letter categorization within the left fusiform gyrus. Neuroimage 2005; 28:738-744.
42. Cohen L, Jobert A, Le Bihan D, Dehaene S. Distinct unimodal and multimodal regions for word processing in the left temporal cortex. Neuroimage 2004; 23:1256-1270.
43. Carlesimo GA, Turriziani P, Paulesu E, et al. Brain activity during intra- and cross-modal priming: new empirical data and review of the literature. Neuropsychologia 2004; 42:14-24.
44. Booth JR, Burman DD, Meyer JR, et al. Functional anatomy of intra- and crossmodal lexical tasks. Neuroimage 2002; 16:7-22.
45. Jobard G, Crivello F, Tzourio-Mazoyer N. Evaluation of the dual route theory of reading: a metanalysis of 35 neuroimaging studies. Neuroimage 2003; 20:693-712.
46. Wheatley T, Weisberg J, Beauchamp MS, Martin A. Automatic priming of semantically related words reduces activity in the fusiform gyrus. J Cogn Neurosci 2005; 17:1871-1885. This study reports amongst other findings semantic effects on fMRI responses in the left posterior region of the fusiform gyrus but also the left inferior frontal cortex.
47. Devlin JT, Jamison HL, Matthews PM, Gonnerman LM. Morphology and the internal structure of words. Proc Natl Acad Sci U S A 2004; 101:14984-14988.
48. Dehaene S, Le Clec'HG, Poline JB, et al. The visual word form area: a prelexical representation of visual words in the fusiform gyrus. Neuroreport 2002; 13:321-325.
49. Binder JR, McKiernan KA, Parsons ME, et al. Neural correlates of lexical access during visual word recognition. J Cogn Neurosci 2003; 15:372-393.
50. Molko N, Cohen L, Mangin JF, et al. Visualizing the neural bases of a disconnection syndrome with diffusion tensor imaging. J Cogn Neurosci 2002; 14:629-636.
51. Cohen L, Martinaud O, Lemer C, et al. Visual word recognition in the left and right hemispheres: anatomical and functional correlates of peripheral alexias. Cereb Cortex 2003; 13:1313-1333.
52. Cohen L, Henry C, Dehaene S, et al. The pathophysiology of letter-by-letter reading. Neuropsychologia 2004; 42:1768-1780.
53. Gaillard R, Naccache L, Pinel P, et al. Direct intracranial, FMRI, and lesion evidence for the causal role of left inferotemporal cortex in reading. Neuron 2006; 50:191-204. A case study combining behavioral, fMRI, and intracranial recording in a patient who developed alexia and letter-by-letter reading subsequent to epilepsy surgery removing tissue close to the presurgically mapped and postoperatively compromised VWFA responses. To date, probably the most compelling evidence for the causal and specific role of the left occipitotemporal cortex in visual word recognition.
54. Barton JJ, Press DZ, Keenan JP, O'Connor M. Lesions of the fusiform face area impair perception of facial configuration in prosopagnosia. Neurology 2002; 58:71-78.
55. Jiang X, Rosen E, Zeffiro T, et al. Evaluation of a shape-based model of human face discrimination using FMRI and behavioral techniques. Neuron 2006; 50:159-172. An interesting study based on a computational object recognition model that can embed face recognition. The authors show fMRI signal changes in FFA that are compatible with the emergence of face perception from object perception.
56. Haxby JV, Gobbini MI, Furey ML, et al. Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science 2001; 293:2425-2430.
57. Hanson SJ, Matsuka T, Haxby JV. Combinatorial codes in ventral temporal lobe for object recognition: Haxby (2001) revisited: is there a ''face'' area? Neuroimage 2004; 23:156-166.
58. O'Toole AJ, Jiang F, Abdi H, Haxby JV. Partially distributed representations of objects and faces in ventral temporal cortex. J Cogn Neurosci 2005; 17:580-590. Very clever analysis showing that brain activity patterns resemble each other the more the visual input does.
59. Leveroni CL, Seidenberg M, Mayer AR, et al. Neural systems underlying the recognition of familiar and newly learned faces. J Neurosci 2000; 20:878-886.
60. Gorno-Tempini ML, Price CJ. Identification of famous faces and buildings: a functional neuroimaging study of semantically unique items. Brain 2001; 124:2087-2097.
61. Shah NJ, Marshall JC, Zafiris O, et al. The neural correlates of person familiarity: a functional magnetic resonance imaging study with clinical implications. Brain 2001; 124:804-815.
62. Kosaka H, Omori M, Iidaka T, et al. Neural substrates participating in acquisition of facial familiarity: an fMRI study. Neuroimage 2003; 20:1734-1742.
63. Turk DJ, Rosenblum AC, Gazzaniga MS, Macrae CN. Seeing John Malkovich: the neural substrates of person categorization. Neuroimage 2005; 24:1147-1153.
64. Mechelli A, Crinion JT, Long S, et al. Dissociating reading processes on the basis of neuronal interactions. J Cogn Neurosci 2005; 17:1753-1765. The authors performed an analysis of functional neural interactions motivated by a dual-route model of reading and show functional correspondence for separable brain systems.
65. Downing PE, Chan AW, Peelen MV, et al. Domain specificity in visual cortex Cereb Cortex 2005 Dec 7. [Epub ahead of print] Extensive mapping survey of category-selective regions in human visual cortex that reproduces selectivity for faces, scenes, and bodies out of a large number of categories tested. A good reminder that at least in terms of overall response preference, domain specificity in the visual cortex is exceptional rather than common.
66. Spiridon M, Fischl B, Kanwisher N. Location and spatial profile of categoryspecific regions in human extrastriate cortex. Hum Brain Mapp 2006; 27:77-89. This fMRI study goes beyond the mere mapping of category-selective brain regions and addresses the spatial tuning function of these response foci. The finding of rather sharp boundaries provides further support for neural specificity for some categorical domains.
67. Tsao DY, Freiwald WA, Tootell R, et al. A cortical region consisting entirely of face-selective cells. Science 2006; 311:670-674. Undoubtedly a study that will rise to landmark standing. Of general interest in that it piloted fMRI-guided electrophysiological studies in nonhuman primates. This approach yielded an unprecedented and stunning degree of face selectivity in at least one of the several face-sensitive patches mapped by fMRI.
68. Gauthier I, Skudlarski P, Gore JC, Anderson AW. Expertise for cars and birds recruits brain areas involved in face recognition. Nat Neurosci 2000; 3:191-197.
69. Rhodes G, Byatt G, Michie PT, Puce A. Is the fusiform face area specialized for faces, individuation, or expert individuation? J Cogn Neurosci 2004; 16:189-203.
70. Xu Y. Revisiting the role of the fusiform face area in visual expertise. Cereb Cortex 2005; 15:1234-1242.
71. Gilaie-Dotan S, Malach R. Sub-exemplar shape tuning in human face-related areas. Cereb Cortex 2006 Mar 8. [Epub ahead of print].
72. Gauthier I, Tarr MJ, Anderson AW, et al. Activation of the middle fusiform 'face area' increases with expertise in recognizing novel objects. Nat Neurosci 1999; 2:568-573.
73. Caldara R, Seghier ML, Rossion B, et al. The fusiform face area is tuned for curvilinear patterns with more high-contrasted elements in the upper part. Neuroimage 2006 Feb 3. [Epub ahead of print]. Simple and direct contribution to a longstanding ardent question: what does it take to make neural face-sensitive mechanisms respond without showing faces?
74. Duchaine B, Dingle K, Butterworth E, Nakayama K. Normal greeble learning in a severe case of developmental prosopagnosia. Neuron 2004; 43:469-473.
75. Gauthier I, Behrmann M, Tarr MJ. Are Greebles like faces? Using the neuropsychological exception to test the rule. Neuropsychologia 2004; 42:1961-1970.
76. Aylward EH, Park JE, Field KM, et al. Brain activation during face perception: evidence of a developmental change. J Cogn Neurosci 2005; 17:308-319.
77. Gathers AD, Bhatt R, Corbly CR, et al. Developmental shifts in cortical loci for face and object recognition. Neuroreport 2004; 15:1549-1553.
78. Changizi MA, Zhang Q, Ye H, Shimojo S. The structures of letters and symbols throughout human history are selected to match those found in objects in natural scenes. Am Nat 2006; 167:E117-E139. Configurational similarity of cultural symbols as letters with real world stimuli may reflect that symbol configuration was informed by a preexisting perceptual proficiency that the brain has developed in response to natural visual input.
79. Changizi MA, Shimojo S. Character complexity and redundancy in writing systems over human history. Proc Biol Sci 2005; 272:267-275. This analysis across a wide variety of writing systems reveals universal commonalities that may reflect visual or motor selection criteria that have shaped these symbol sets.
80. Cohen L, Dehaene S. Specialization within the ventral stream: the case for the visual word form area. Neuroimage 2004; 22:466-476.
81. Price CJ, Friston KJ, Degeneracy. cognitive anatomy. Trends Cogn Sci 2002; 6:416-421.
82. Winston JS, Vuilleumier P, Dolan RJ. Effects of low-spatial frequency components of fearful faces on fusiform cortex activity. Curr Biol 2003; 13:1824-1829.
83. Yovel G, Kanwisher N. Face perception: domain specific, not process specific. Neuron 2004; 44:889-898.
84. Ganel T, Valyear KF, Goshen-Gottstein Y, Goodale MA. The involvement of the "fusiform face area" in processing facial expression. Neuropsychologia 2005; 43:1645-1654.
85. Duchaine B, Parker H, Nakayama K. Normal emotion recognition in a prosopagnosic. Perception 2003; 32:827-838.
86. Young MP, Hilgetag CC, Scannell JW. On imputing function to structure from the behavioural effects of brain lesions. Phil Trans R Soc Lond B Biol Sci 2000; 355:147-161.