Cortex
Volume 46, Issue 8 , Pages 949-964 , September 2010

Three cases of developmental prosopagnosia from one family: Detailed neuropsychological and psychophysical investigation of face processing

  • Yunjo Lee

      Affiliations

    • Centre for Vision Research, York University, Toronto, ON, Canada
    • Rotman Research Institute, Baycrest, Toronto, ON, Canada
    • Corresponding Author InformationCorresponding author. Rotman Research Institute, Baycrest Centre, University of Toronto, 3560 Bathurst Street, Toronto, ON M6A 2E1, Canada.
  • ,
  • Bradley Duchaine

      Affiliations

    • Institute of Cognitive Neuroscience, University College London, UK
  • ,
  • Hugh R. Wilson

      Affiliations

    • Centre for Vision Research, York University, Toronto, ON, Canada
  • ,
  • Ken Nakayama

      Affiliations

    • Department of Psychology, Harvard University, Cambridge, MA, USA

Received 11 September 2008 ,Revised 17 April 2009 ,Accepted 23 July 2009.

References 

  1. Andrews TJ, Ewbank MP. Distinct representations for facial identity and changeable aspects of faces in the human temporal lobe. NeuroImage. 2004;23:905–913
  2. Baron-Cohen S, Wheelwright S, Hill J, Raste Y, Plumb I. The ‘Reading the mind in the eyes’ test revised version: A study with normal adults, and adults with Asperger syndrome or high-functioning autism. Journal of Child Psychology and Psychiatry. 2001;42:241–252
  3. Behrmann M, Avidan G. Congenital prosopagnosia: Face-blind from birth. Trends in Cognitive Sciences. 2005;9:180–187
  4. Behrmann M, Avidan G, Marotta J, Kimchi R. Detailed exploration of face-related processing in congenital prosopagnosia: 1. Behavioral findings. Journal of Cognitive Neuroscience. 2005;17:1130–1149
  5. Bentin S, DeGutis JM, D'Esposito M, Robertson LC. Too many trees to see the forest: Performance, event-related potential, and functional magnetic resonance imaging manifestations of integrative congenital prosopagnosia. Journal of Cognitive Neuroscience. 2007;19:132–146
  6. Bentin S, Deouell LY, Soroker N. Selective visual streaming in face recognition: Evidence from developmental prosopagnosia. NeuroReport. 1999;10:823–827
  7. Benton AL, Van Allen MW. Impairment in facial recognition in patients with cerebral disease. Cortex. 1968;4:344–358
  8. Betts LR and Wilson HR. fMRI adaptation in fusiform face area and occipital face area. Perception, 36: 145, 2007 (Supplement, 30th European Conference on Visual Perception).
  9. Brainard DH. The psychophysics toolbox. Spatial Vision. 1997;10:433–436
  10. Bruce V, Young AW. Understanding face recognition. British Journal of Psychology. 1986;77:305–327
  11. Christensen H, Mackinnon AJ, Korten AE, Jorm AF, Henderson AS, Jacomb P, et al. An analysis of diversity in the cognitive performance of elderly community dwellers: Individual differences in change scores as a function of age. Psychology and Aging. 1999;14:365–379
  12. Crawford JR, Howell DC. Comparing an individual's test score against norms derived from small samples. Clinical Neuropsychologist. 1998;12:482–486
  13. Duchaine BC, Dingle K, Butterworth E, Nakayama K. Normal Greeble learning in a severe case of developmental prosopagnosia. Neuron. 2004;43:469–473
  14. Duchaine BC, Parker H, Nakayama K. Normal recognition of emotion in a prosopagnosic. Perception. 2003;32:827–838
  15. Duchaine BC, Nakayama K. Developmental prosopagnosia and the benton facial recognition test. Neurology. 2004;62:1219–1220
  16. Duchaine BC, Nakayama K. Dissociations of face and object recognition in developmental prosopagnosia. Journal of Cognitive Neuroscience. 2005;17:249–261
  17. Duchaine BC, Nakayama K. The Cambridge face memory test: Results for neurologically intact individuals and an investigation of its validity using inverted face stimuli and prosopagnosic participants. Neuropsychologia. 2006;44:576–585
  18. Duchaine BC, Weidenfeld A. An evaluation of two commonly used tests of unfamiliar face recognition. Neuropsychologia. 2003;41:713–720
  19. Duchaine BC, Yovel G, Butterworth EJ, Nakayama K. Prosopagnosia as an impairment to face-specific mechanisms: Elimination of the alternative hypotheses in a developmental case. Cognitive Neuropsychology. 2006;23:714–747
  20. Duchaine B, Germine L, Nakayama K. Family resemblance: Ten family members with prosopagnosia and within-class object agnosia. Cognitive Neuropsychology. 2007;24:419–430
  21. Duchaine B, Yovel G, Nakayama K. No global processing deficit in the Navon task in 14 developmental prosopagnosics. Social Cognitive and Affective Neuroscience. 2007;2:104–113
  22. 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
  23. Ekman P, Friesen WL. Pictures of Facial Affect. Palo Alto, CA: Consulting Psychologist Press; 1976;
  24. Gallant JL, Connor CE, Rakshit S, Lewis JW, Van Essen DC. Neural responses to polar, hyperbolic, and cartesian gratings in area V4 of the macaque monkey. Journal of Neurophysiology. 1996;76:2718–2739
  25. Gallant JL, Shoup RE, Mazer JA. A human extrastriate area functionally homologous to macaque V4. Neuron. 2000;27:227–235
  26. Garrido L, Duchaine B, Nakayama K. Face detection in normal and prosopagnosic individuals. Journal of Neuropsychology. 2008;2:119–140
  27. Gauthier I, Skudlarski P, Gore JC, Anderson AW. Expertise for cars and birds recruits brain areas involved in face recognition. Nature Neuroscience. 2000;3:191–197
  28. Gold J, Bennett PJ, Sekuler AB. Identification of band-pass filtered letters and faces by human and ideal observers. Vision Research. 1999;39:3537–3560
  29. Grill-Spector K, Malach R. fMR-adaptation: A tool for studying the functional properties of human cortical neurons. Acta Psychologica. 2001;107:293–321
  30. Grueter M, Grueter T, Bell V, Horst J, Wolfgang L, Sperling K, et al. Hereditary prosopagnosia: The first case series. Cortex. 2007;43:734–749
  31. Habak C, Wilkinson F, Wilson HR. Aging disrupts the neural transformations that link facial identity across views. Vision Research. 2008;48:9–15
  32. Haxby JV, Hoffman EA, Gobbini MI. The distributed human neural system for face perception. Trends in Cognitive Sciences. 2000;4:223–233
  33. Haxby JV, Ungerleider LG, Horwitz B, Maisog JM, Rapoport SI. Face encoding and recognition in the human brain. Proceedings of the National Academy of Sciences of the United States of America. 1996;93:922–927
  34. Humphreys K, Avidan G, Behrmann M. A detailed investigation of facial expression processing in congenital prosopagnosia as compared to acquired prosopagnosia. Experimental Brain Research. 2007;176:356–373
  35. Kanwisher N, McDermott J, Chun MM. The fusiform face area: A module in extrastriate cortex specialised for face perception. Journal of Neuroscience. 1997;17:4302–4311
  36. Kennerknecht I, Grüter T, Welling B, Wentzek S, Horst J, Edwards S, et al. First report of prevalence of non-syndromic hereditary prosopagnosia (HPA). American Journal of Medical Genetics Part A. 2006;140A:1617–1622
  37. Kress T, Daum I. Developmental prosopagnosia: A review. Behavioural Neurology. 2003;14:109–121
  38. Laeng B, Caviness VS. Prosopagnosia as a deficit in encoding curved surface. Journal of Cognitive Neuroscience. 2001;13:556–576
  39. Lee Y, Matsumiya K, Wilson HR. Size-invariant but viewpoint-dependent representation of faces. Vision Research. 2006;46:1901–1910
  40. Lee Y, Wilson HR and Rivest J. Matching faces in a prosopagnosic individual [Abstract]. Journal of Vision, 3: 305, 305a, 2003 http://journalofvision.org/3/9/305/, doi: 10.1167/3.9.305.
  41. Le Grand R, Cooper PA, Mondloch CJ, Lewis TL, Sagiv N, de Gelder B, et al. What aspects of face processing are impaired in developmental prosopagnosia?. Brain and Cognition. 2006;61:139–158
  42. Lehky SR. Fine discrimination of faces can be performed rapidly. Journal of Cognitive Neuroscience. 2000;12:848–855
  43. Loffler G, Gordon GE, Wilkinson F, Goren D, Wilson HR. Configural masking of faces: Evidence for high-level interactions in face perception. Vision Research. 2005;45:2287–2297
  44. Loffler G, Yourganov G, Wilkinson F, Wilson HR. fMRI evidence for the neural representation of faces. Nature Neuroscience. 2005;8:1386–1390
  45. Macmillan NA, Creelman CD. Detection Theory: A User's Guide. Psychology Press; 2004;
  46. Marotta JJ, McKeeff TJ, Behrmann M. The effects of rotation and inversion on face processing in prosopagnosia. Cognitive Neuropsychology. 2002;19:31–47
  47. McConachie HR. Developmental prosopagnosia. a single case report. Cortex. 1976;12:76–82
  48. Näsänen R. Spatial frequency bandwidth used in the recognition of facial images. Vision Research. 1999;39:3824–3833
  49. Navon D. Forest before trees: The precedence of global features in visual perception. Cognitive Psychology. 1977;9:353–383
  50. Nunn JA, Postma P, Pearson R. Developmental prosopagnosia: Should it be taken at face value?. Neurocase. 2001;7:15–27
  51. Pelli DG. The VideoToolbox software for visual psychophysics: Transforming numbers into movies. Spatial Vision. 1997;10:437–442
  52. Pourtois G, Schwartz S, Seghier ML, Lazeyras F, Vuilleumier P. Portraits or people? Distinct representations of face identity in the human visual cortex. Journal of Cognitive Neuroscience. 2005;17:1043–1057
  53. Pourtois G, Schwartz S, Seghier ML, Lazeyras F, Vuilleumier P. 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
  54. Quick RF. A vector-magnitude model of contrast detection. Kybernetik. 1974;16:1299–1302
  55. Quiroga RQ, Reddy L, Kreiman G, Koch C, Fried I. Invariant visual representation by single neurons in the human brain. Nature. 2005;435:1102–1107
  56. Riesenhuber M, Poggio T. Hierarchical models of object recognition in cortex. Nature Neuroscience. 1999;2:1019–1025
  57. Schmalzl L, Palermo R, Coltheart M. Cognitive heterogeneity in genetically based prosopagnosia: A family study. Journal of Neuropsychology. 2008;2:99–117
  58. Schwarzer G, Huber S, Grüter M, Grüter T, Groß C, Hipfel M, et al. Gaze behaviour in hereditary prosopagnosia. Psychological Research. 2007;71:583–590
  59. Thomas C, Avidan G, Humphreys K, Jung K, Gao F, Behrmann M. Reduced structural connectivity in ventral visual cortex in congenital prosopagnosia. Nature Neuroscience. 2009;12:29–31
  60. Wallis G, Bülthoff H. Effects of temporal association on recognition memory. Proceedings of the National Academy of Sciences of the United States of America. 2001;98:4800–4804
  61. Weibull WA. A statistical distribution function of wide applicability. Journal of Applied Mechanics. 1951;18:292–297
  62. Wilkinson F, James TW, Wilson HR, Gati JS, Menon RS, Goodale MA. An fMRI study of the selective activation of human extrastriate form vision areas by radial and concentric gratings. Current Biology. 2000;10:1455–1458
  63. Wilkinson F, Wilson HR, Habak C. Detection and recognition of radial frequency patterns. Vision Research. 1998;38:3555–3568
  64. Wilson HR, Diaconescu A. Learning alters local face space geometry. Vision Research. 2006;46:4143–4151
  65. Wilson HR, Loffler G, Wilkinson F. Synthetic faces, face cubes, and the geometry of face space. Vision Research. 2002;42:2909–2923
  66. Wilson HR, Wilkinson F. Symmetry perception: A novel approach for biological shapes. Vision Research. 2002;42:589–597
  67. Wilson HR, Wilkinson F, Asaad W. Concentric orientation summation in human form vision. Vision Research. 1997;37:2325–2330
  68. Wilson HR, Wilkinson F, Lin L-M, Castillo M. Perception of head orientation. Vision Research. 2000;40:459–472
  69. Yotsumoto Y, Kahana MJ, Wilson HR, Sekuler R. Recognition memory for realistic synthetic faces. Memory and Cognition. 2007;35:1233–1244
  70. Yovel G, Duchaine B. Specialized face perception mechanisms extract both part and spacing information: Evidence from developmental prosopagnosia. Journal of Cognitive Neuroscience. 2006;18:580–593

PII: S0010-9452(09)00224-X

doi: 10.1016/j.cortex.2009.07.012

Cortex
Volume 46, Issue 8 , Pages 949-964 , September 2010