Does Prosopagnosia Take the Eyes Out of Face Representations? Evidence for a Defect in Representing Diagnostic Facial Information following Brain Damage (original) (raw)

Abstract

& One of the most impressive disorders following brain damage to the ventral occipitotemporal cortex is prosopagnosia, or the inability to recognize faces. Although acquired prosopagnosia with preserved general visual and memory functions is rare, several cases have been described in the neuropsychological literature and studied at the functional and neural level over the last decades. Here we tested a braindamaged patient presenting a deficit restricted to the category of faces to clarify the nature of the missing and preserved components of the face processing system when it is selectively damaged. Following learning to identify 10 neutral and happy faces through extensive training, we investigated patient PS's recognition of faces using Bubbles, a response classification technique that sampled facial information across the faces in different bandwidths of spatial frequencies [Bubbles: A technique to reveal the use of information in recognition tasks. Vision Research, 41, 2261Research, 41, -2271Research, 41, , 2001. Although PS gradually used less information (i.e., the number of bubbles) to identify faces over testing, the total information required was much larger than for normal controls and decreased less steeply with practice. Most importantly, the facial information used to identify individual faces differed between PS and controls. Specifically, in marked contrast to controls, PS did not use the optimal eye information to identify familiar faces, but instead the lower part of the face, including the mouth and the external contours, as normal observers typically do when processing unfamiliar faces. Together, the findings reported here suggest that damage to the face processing system is characterized by an inability to use the information that is optimal to judge identity, focusing instead on suboptimal information. & D

Loading...

Loading Preview

Sorry, preview is currently unavailable. You can download the paper by clicking the button above.

References (94)

  1. Barton, J. J. (2003). Disorders of face perception and recognition. Neurologic Clinics, 21, 521-548.
  2. Barton, J. J., Cherkasova, M., & O'Connor, M. (2001). Covert recognition in acquired and developmental prosopagnosia. Neurology, 57, 1161-1168.
  3. Barton, J. J., Cherkasova, M. V., Press, D. Z., Intriligator, J. M., & O'Connor, M. (2004). Perceptual functions in prosopagnosia. Perception, 33, 939-956.
  4. Barton, J. J., Press, D. Z., Keenan, J. P., & O'Connor, M. (2002). Lesions of the fusiform face area impair perception of facial configuration in prosopagnosia. Neurology, 58, 71-78.
  5. Behrmann, M., Avidan, G., Marotta, J. J., & Kimchi, R. (2005). Detailed exploration of face-related processing in congenital prosopagnosia: 1. Behavioral findings. Journal of Cognitive Neuroscience, 17, 1130-1149.
  6. Benton, A., & van Allen, M. (1972). Prosopagnosia and facial discrimination. Journal of the Neurological Sciences, 15, 167-172.
  7. Bodamer, J. (1947). Die prosop-agnosie. Archive fu ¨r Psychiatrie und Nervenkrankheiten, 179, 6-54.
  8. Bouvier, S. E., & Engel, S. A. (2004). Patterns of cortical damage in achromatopsia and prosopagnosia. Journal of Vision, 4, Supplement, 205a.
  9. Brainard, D. H. (1997). The psychophysics toolbox. Spatial Vision, 10, 433-436.
  10. Bruce, V., Burton, A. M., Hanna, E., Healey, P., Mason, O., Coombes, A., Fright, R., & Linney, A. (1993). Sex discrimination: How do we tell the difference between male and female faces? Perception, 22, 131-152.
  11. Bruce, V., Henderson, Z., Greenwood, K., Hancock, P. J. B., Burton, A. M., & Miller, P. (1999). Verification of face identities from images captured on video. Journal of Experimental Psychology: Applied, 5, 339-360.
  12. Bruce, V., & Young, A. (1986). Understanding face recognition. British Journal of Psychology, 77, 305-327.
  13. Bruyer, R., Laterre, C., Seron, X., Feyereisen, P., Strypstein, E., Pierrard, E., & Rectem, D. (1983). A case of prosopagnosia with some preserved covert remembrance of familiar faces. Brain and Cognition, 2, 257-284.
  14. Bukach, C. M., Bub, D. M., Gauthier, I., & Tarr, M. J. (submitted). Perceptual expertise effects are not all or none: Local perceptual expertise for faces in a case of prosopagnosia.
  15. Burton, A. M., Wilson, S., Cowan, M., & Bruce, V. (1999). Face recognition in poor-quality video: Evidence from security surveillance. Psychological Science, 10, 243-248.
  16. Caldara, R., Gauthier, I., Rossion, B., Schuller, A. M., Tarr, M. J., & Mayer, E. (submitted). Prosopagnosia as an inability to develop expertise with visually homogeneous categories: Evidence from a single-case study.
  17. Calder, A. J., Burton, A. M., Miller, P., Young, A. W., & Akamatsu, S. (2001). A principal component analysis of facial expressions. Vision Research, 41, 1179-1208.
  18. Campbell, R., Coleman, M., Walker, J., Benson, P. J., Wallace, S., Michelotti, J., & Baron-Cohen, S. (1999). When does the inner-face advantage in familiar face recognition arise and why? Visual Cognition, 6, 197-216.
  19. Campbell, R., Landis, T., & Regard, M. (1986). Face recognition and lipreading. A neurological dissociation. Brain, 109, 509-521.
  20. Carey, S. (1992). Becoming a face expert. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 335, 95-102; discussion 102-103.
  21. Carey, S., & Diamond, R. (1977). From piecemeal to configurational representation of faces. Science, 195, 312-314.
  22. Carey, S., & Diamond, R. (1994). Are faces perceived as configurations more by adults than by children? In V. Bruce & G. Humphreys (Eds.), Object and face recognition [Special issue]. Visual Cognition, 1, 253-274.
  23. Damasio, A. R. (1985). Disorders of complex visual processing: Agnosias, achromatopsia, Balint's syndrome, and related difficulties in orientation and construction. In M.-M. Mesulam (Ed.), Principles of behavioural neurology (pp. 259-288). Philadelphia: F.A. Davis.
  24. Damasio, A. R., Damasio, H., & Van Hoesen, G. W. (1982). Prosopagnosia: Anatomic basis and behavioral mechanisms. Neurology, 32, 331-341.
  25. Davies, G., Ellis, H., & Shepherd, J. (1977). Cue saliency in faces as assessed by the ''photofit'' technique. Perception, 6, 263-269.
  26. de Haan, E. H., & Hay, D. (1986). The matching of famous and unknown faces, given either the internal or external features: A study on patients with unilateral brain lesions. In H. D. Ellis, F. Jeeves, F. Newcombe, & A. W. Young (Eds.), Aspects of face processing (pp. 302-309). Dordrecht: Martinus Nijhoff.
  27. de Haan, E. H., Young, A., & Newcombe, F. (1987). Faces interfere with name classification in a prosopagnosic patient. Cortex, 23, 309-316.
  28. Diamond, R., & Carey, S. (1986). Why faces are and are not special: An effect of expertise. Journal of Experimental Psychology. General, 115, 107-117.
  29. Dixon, M. J., Bub, D. N., & Arguin, M. (1998). Semantic and visual determinants of face recognition in a prosopagnosic patient. Journal of Cognitive Neuroscience, 10, 362-376.
  30. Donnelly, N., & Davidoff, J. (1999). The mental representations of faces and houses: Issues concerning parts and wholes. Visual Cognition, 6, 319-343.
  31. Ellis, D. M., & Ellis, H. D. (1994). Development of facial transformation processing skills in children. Psychologie Franc ¸aise, 39, 287-300.
  32. Ellis, H. D., & Florence, M. (1990). Bodamer's (1947) paper on prosopagnosia. Cognitive Neuropsychology, 7, 81-105.
  33. Ellis, H. D., Shepherd, J. W., & Davies, G. M. (1979). Identification of familiar and unfamiliar faces from internal and external features: Some implications for theories of face recognition. Perception, 8, 431-439.
  34. Farah, M., Levinson, K. L., & Klein, K. L. (1995). Face perception and within-category discrimination in prosopagnosia. Neuropsychologia, 33, 661-674.
  35. Farah, M. J. (1990). Visual agnosia. Cambridge: MIT Press.
  36. Farah, M. J., McMullen, P. A., & Meyer, M. M. (1991). Can recognition of living things be selectively impaired? Neuropsychologia, 29, 185-193.
  37. Fraser, I. H., Craig, G. L., & Parker, D. M. (1990). Reaction time measures of feature saliency in schematic faces. Perception, 19, 661-673.
  38. Gauthier, I., Behrmann, M., & Tarr, M. J. (1999). Can face recognition really be dissociated from object recognition? Journal of Cognitive Neuroscience, 11, 349-370.
  39. Goldsmith, Z. G., & Liu, G. T. (2001). Facial recognition and prosopagnosia: Past and present concepts. Neuro-Ophthalmology, 25, 177-192.
  40. Gosselin, F., & Schyns, P. G. (2001). Bubbles: A technique to reveal the use of information in recognition tasks. Vision Research, 41, 2261-2271.
  41. Gru ¨sser, O. J., & Landis, T. (1991). Visual agnosias and other disturbances of visual perception and cognition. In Vision and visual dysfunction (Vol. 12). London: Macmillan Press.
  42. Haig, N. D. (1984). The effect of feature displacement on face recognition. Perception, 13, 505-512.
  43. Haig, N. D. (1985). How faces differ-A new comparative technique. Perception, 14, 601-615.
  44. Haig, N. D. (1986). Exploring recognition with interchanged facial features. Perception, 15, 235-247.
  45. Hill, H., Bruce, V., & Akamatsu, S. (1995). Perceiving the sex and race of faces: The role of shape and colour. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 261, 367-373.
  46. Hoffman, E. A., & Haxby, J. V. (2000). Distinct representations of eye gaze and identity in the distributed human neural system for face perception. Nature Neuroscience, 3, 80-84.
  47. Hosie, J. A., Ellis, H. D., & Haig, N. D. (1988). The effect of feature displacement on the perception of well-known faces. Perception, 17, 461-474.
  48. Kemp, R., McManus, C., & Pigott, T. (1990). Sensitivity to the displacement of facial features in negative and inverted images. Perception, 19, 531-543.
  49. Kress, T., & Daum, I. (2003). Developmental prosopagnosia: A review. Behavioral Neurology, 14, 109-121.
  50. Laeng, B., & Caviness, V. S. (2001). Prosopagnosia as a deficit in encoding curved surface. Journal of Cognitive Neuroscience, 13, 556-576.
  51. Landis, T., Regard, M., Bliestle, A., & Kleihues, P. (1988). Prosopagnosia and agnosia for noncanonical views. An autopsied case. Brain, 111, 1287-1297.
  52. Le Grand, R., Mondloch, C. J., Maurer, D., & Brent, H. P. (2001). Neuroperceptionearly visual experience and face processing. Nature, 410, 890.
  53. Le Grand, R., Mondloch, C. J., Maurer, D., & Brent, H. P. (2004). Impairment in holistic face processing following early visual deprivation. Psychological Science, 15, 762-768.
  54. Leder, H., & Bruce, V. (2000). When inverted faces are recognized: The role of configural information in face recognition. Quarterly Journal of Experimental Psychology. A, Human Experimental Psychology, 53, 513-536.
  55. Leder, H., Candrian, G., Huber, O., & Bruce, V. (2001). Configural features in the context of upright and inverted faces. Perception, 30, 73-83.
  56. Levine, D. N., & Calvanio, R. (1989). Prosopagnosia: A defect in visual configural processing. Brain and Cognition, 10, 149-170.
  57. Levine, D. N., Calvanio, R., & Wolf, E. (1980). Disorders of visual behavior following bilateral posterior cerebral lesions. Psychological Research, 41, 217-234.
  58. Macho, S., & Leder, H. (1998). Your eyes only? A test of interactive influence in the processing of facial features. Journal of Experimental Psychology: Human Perception & Performance, 24, 1486-1500.
  59. Malone, D. R., Morris, H. H., Kay, M. C., & Levin, H. S. (1982). Prosopagnosia: A double dissociation between the recognition of familiar and unfamiliar faces. Journal of Neurology, Neurosurgery and Psychiatry, 45, 820-822.
  60. Maurer, D., Grand, R. L., & Mondloch, C. J. (2002). The many faces of configural processing. Trends in Cognitive Sciences, 6, 255-260.
  61. Mayer, E., Fistarol, P., & Valenza, N. (1999). Prise en charge neuropsychologique d'une patiente prosopagnosique.
  62. In P. Azouvi, D. Perrier, & M. Van der Linden (Eds.), La reeducation en neuropsychologie: Etudes de cas. Marseille: Solal.
  63. McKelvie, S. J. (1976). The role of eyes and mouth in the memory of a face. American Journal of Psychology, 89, 311-323.
  64. Mondloch, C. J., Le Grand, R., & Maurer, D. (2002). Configural face processing develops more slowly than featural face processing. Perception, 31, 553-566.
  65. O'Donnell, C., & Bruce, V. (2001). Familiarisation with faces selectively enhances sensitivity to changes made to the eyes. Perception, 30, 755-764.
  66. Pelli, D. G. (1997). The VideoToolbox software for visual psychophysics: Transforming numbers into movies. Spatial Vision, 10, 437-442.
  67. Perrett, D. I., Hietanen, J. K., Oram, M. W., & Benson, P. J. (1992). Organization and functions of cells responsive to faces in the temporal cortex. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 335, 23-30.
  68. Perrett, D. I., Rolls, E. T., & Caan, W. (1982). Visual neurones responsive to faces in the monkey temporal cortex. Experimental Brain Research, 47, 329-342.
  69. Quaglino, A. (1867). Emiplegia sinistra con amaurosi- guarigione-perdita totale della percezione dei colori e della memoria della configurazione degli oggetti. Giornale d'Oftalmologia Italiano, 10, 106-112.
  70. Rakover, S. S., & Teucher, B. (1997). Facial inversion effects: Parts and whole relationship. Perception & Psychophysics, 59, 752-761.
  71. Rizzo, M., Corbett, J. J., Thompson, H. S., & Damasio, A. R. (1986). Spatial contrast sensitivity in facial recognition. Neurology, 36, 1254-1256.
  72. Rossion, B., Caldara, R., Seghier, M., Schuller, A. M., Lazeyras, F., & Mayer, E. (2003). A network of occipito-temporal face-sensitive areas besides the right middle fusiform gyrus is necessary for normal face processing. Brain, 126, 2381-2395.
  73. Sadr, J., Jarudi, I., & Sinha, P. (2003). The role of eyebrows in face recognition. Perception, 32, 285-293.
  74. Schiltz, C., Sorger, B., Ahmed, F., Caldara, R., Mayer, E., Goebel, R., & Rossion, B. (submitted). Anomalous response to facial identity in the right middle fusiform gyrus underlies impaired face identification in acquired prosopagnosia.
  75. Schyns, P. G., Bonnar, L., & Gosselin, F. (2002). Show me the features! Understanding recognition from the use of visual information. Psychological Science, 13, 402-409.
  76. Schyns, P. G., & Oliva, A. (1999). Dr. Angry and Mr. Smile: When categorization flexibly modifies the perception of faces in rapid visual presentations. Cognition, 69, 243-265.
  77. Sekuler, A. B., Gaspar, C. M., Gold, J. M., & Bennett, P. J. (2004). Inversion leads to quantitative, not qualitative, changes in face processing. Current Biology, 14, 391-396.
  78. Sergent, J. (1984). Configural processing of faces in the left and the right cerebral hemispheres. Journal of Experimental Psychology Human Perception and Performance, 10, 554-572.
  79. Sergent, J., & Signoret, J. L. (1992). Varieties of functional deficits in prosopagnosia. Cerebral Cortex, 2, 375-388.
  80. Sergent, J., & Villemure, J. G. (1989). Prosopagnosia in a right hemispherectomized patient. Brain, 112, 975-995.
  81. Simoncelli, E. P. (1997). Image and multi-scale pyramid tools [Computer software]. New York: Author.
  82. Smith, M., Cottrell, G. W., Gosselin, F., & Schyns, P. G. (2005). Transmitting and decoding facial expressions. Psychological Science, 16, 184-189.
  83. Sorger, B., Schiltz, C., Caldara, R., Kriegeskorte, N., Mayer, E., Rossion, B., & Goebel, R. (2004). Functional neuroanatomy of the visual system in a prosopagnosic. Neuroimage, 22, S40.
  84. Tanaka, J. W. (2001). The entry point of face recognition: Evidence for face expertise. Journal of Experimental Psychology: General, 130, 534-543.
  85. Tanaka, J. W., & Farah, M. J. (1993). Parts and wholes in face recognition. Quarterly Journal of Experimental Psychology. A, Human Experimental Psychology, 46a, 225-245.
  86. Taylor, M. J., McCarthy, G., Saliba, E., & Degiovanni, E. (1999). ERP evidence of developmental changes in processing of faces. Clinical Neurophysiology, 110, 910-915.
  87. Tranel, D., Damasio, A. R., & Damasio, H. (1988). Intact recognition of facial expression, gender, and age in patients with impaired recognition of face identity. Neurology, 38, 690-696.
  88. Valentine, T. (1991). A unified account of the effects of distinctiveness, inversion, and race in face recognition. Quarterly Journal of Experimental Psychology. A, Human Experimental Psychology, 43a, 161-204.
  89. Vinette, C., Gosselin, F., & Schyns, P. G. (2004). Spatio- temporal dynamics of face recognition in a flash: It's in the eyes. Cognitive Science, 28, 289-301.
  90. Walker Smith, G. J. (1978). The effects of delay and exposure duration in a face recognition task. Perception and Psychophysics, 24, 63-70.
  91. Warrington, E. (1984). Warrington recognition memory test. Los Angeles: Western Psychological Services.
  92. Warrington, E. K. (1996). The Camden memory tests manual. Hove: Psychology Press.
  93. Wigan, A. L. (1844). The duality of the mind: Proved by the structure, functions, and diseases of the brain, and by the phenomena of mental derangement, and shown to be essential to moral responsibility. London: Longman, Brown, Green, and Longmans.
  94. Young, A. W., McWeeny, K. H., Hay, D. C., & Ellis, A. W. (1986). Matching familiar and unfamiliar faces on identity and expression. Psychological Research, 48, 63-68.