Holistic processing of the mouth but not the eyes in developmental prosopagnosia

Cognitive Neuropsychology

Volumn 29, Issue 5-6, 2012, Pages 419-446

  DeGutis, Joseph ^a,b   Cohan, Sarah ^b   Mercado, Rogelio J ^c   Wilmer, Jeremy ^d   Nakayama, Ken ^b  

^a GERIATRIC RESEARCH EDUCATION AND CLINICAL CENTER   (United States)

^b HARVARD UNIVERSITY   (United States)

^c TEMPLE UNIVERSITY   (United States)

^d WELLESLEY COLLEGE   (United States)

Author keywords

Developmental prosopagnosia; Holistic face processing; Part whole task

Indexed keywords

ADULT; ARTICLE; CASE CONTROL STUDY; EYE; FEMALE; HUMAN; MALE; MIDDLE AGED; MOUTH; NEUROPSYCHOLOGICAL TEST; PATHOPHYSIOLOGY; PATTERN RECOGNITION; PERCEPTIVE DISCRIMINATION; PHYSIOLOGY; PROSOPAGNOSIA; RECOGNITION; VISION;

ADULT; CASE-CONTROL STUDIES; DISCRIMINATION (PSYCHOLOGY); EYE; FEMALE; HUMANS; MALE; MIDDLE AGED; MOUTH; NEUROPSYCHOLOGICAL TESTS; PATTERN RECOGNITION, VISUAL; PROSOPAGNOSIA; RECOGNITION (PSYCHOLOGY); VISUAL PERCEPTION; YOUNG ADULT;

MLCS; MLOWN;

EID: 84874448112     PISSN: 02643294     EISSN: 14640627     Source Type: Journal    
DOI: 10.1080/02643294.2012.754745     Document Type: Article

References (89)

1. Andrews, T. J., Davies-Thompson, J., Kingstone, A., and Young, A. W., 2010. Internal and external features of the face are represented holistically in face-selective regions of visual cortex. The Journal of Neuroscience, 30: 3544–3552. (doi:10.1523/JNEUROSCI.4863-09.2010)
2. Attneave, F., and Olson, R. K., 1967. Discriminability of stimuli varying in physical and retinal orientation. Journal of Experimental Psychology, 74: 149–157. (doi:10.1037/h0024557)
3. Avidan, G., Tanzer, M., and Behrmann, M., 2011. Impaired holistic processing in congenital prosopagnosia. Neuropsychologia, 49: 2541–2552. (doi:10.1016/j.neuropsychologia.2011.05.002)
4. Baron-Cohen, S., Wheelwright, S., Skinner, R., Martin, J., and Clubley, E., 2001. The autism-spectrum quotient (AQ): Evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. Journal of Autism and Developmental Disorders, 31: 5–17. (doi:10.1023/A:1005653411471)
5. Bartlett, J. C., and Searcy, J., 1993. Inversion and configuration of faces. Cognitive Psychology, 25: 281–316. (doi:10.1006/cogp.1993.1007)
6. Barton, J. J., Cherkasova, M. V., Press, D. Z., Intriligator, J. M., and O'Connor, M., 2003. Developmental prosopagnosia: A study of three patients. Brain and Cognition, 51: 12–30. (doi:10.1016/S0278-2626(02)00516-X)
7. Behrmann, M., Avidan, G., Marotta, J. J., and Kimchi, R., 2005. Detailed exploration of face-related processing in congenital prosopagnosia: 1. Behavioral findings. Journal of Cognitive Neuroscience, 17: 1130–1149. (doi:10.1162/0898929054475154)
8. Bukach, C. M., Le Grand, R., Kaiser, M. D., Bub, D. N., and Tanaka, J. W., 2008. Preservation of mouth region processing in two cases of prosopagnosia. Journal of Neuropsychology, 2: 227–244. (doi:10.1348/174866407X231010)
9. Busigny, T., Joubert, S., Felician, O., Ceccaldi, M., and Rossion, B., 2010. Holistic perception of the individual face is specific and necessary: Evidence from an extensive case study of acquired prosopagnosia. Neuropsychologia, 48: 4057–4092. (doi:10.1016/j.neuropsychologia.2010.09.017)
10. Busigny, T., & Rossion, B. (2010). Acquired prosopagnosia abolishes the face inversion effect. Cortex, 46, 965–981.
11. Butler, S., Blais, C., Gosselin, F., Bub, D., and Fiset, D., 2010. Recognizing famous people. Attention, Perception, & Psychophysics, 72: 1444–1449. (doi:10.3758/APP.72.6.1444)
12. Caldara, R., Schyns, P., Mayer, E., Smith, M. L., Gosselin, F., and Rossion, B., 2005. Does prosopagnosia take the eyes out of face representations? Evidence for a defect in representing diagnostic facial information following brain damage. Journal of Cognitive Neuroscience, 17: 1652–1666. (doi:10.1162/089892905774597254)
13. Curby, K. M., and Gauthier, I., 2007. A visual short-term memory advantage for faces. Psychonomic Bulletin & Review, 14: 620–628. (doi:10.3758/BF03196811)
14. Dalton, K. M., Nacewicz, B. M., Johnstone, T., Schaefer, H. S., Gernsbacher, M. A., Goldsmith, H. H., and Davidson, R. J., 2005. Gaze fixation and the neural circuitry of face processing in autism. Nature Neuroscience, 8: 519–526.
15. Davidoff, J., and Donnelly, N., 1990. Object superiority: A comparison of complete and part probes. Acta Psychologica, 73: 225–243. (doi:10.1016/0001-6918(90)90024-A)
16. Davidoff, J., Matthews, B., & Newcombe, F. (1986). Observations on a case of prosopagnosia. In H. Ellis, M. Jeeves, F. Newcombe, & A. Young (Eds.), Aspects of face processing (pp. 279–290). Dordrecht: Martinus Nijhoff.
17. de Gelder, B., and Rouw, R., 2000. Configural face processes in acquired and developmental prosopagnosia: Evidence for two separate face systems?. Neuroreport, 11 (14): 3145–3150. (doi:10.1097/00001756-200009280-00021)
18. DeGutis, J., Chatterjee, G., Mercado, R. J., and Nakayama, N., 2012. Face gender recognition in developmental prosopagnosia: Evidence for holistic processing, Manuscript submitted for publication
19. DeGutis, J., DeNicola, C., Zink, T., McGlinchey, R., and Milberg, W., 2011. Training with own-race faces can improve processing of other-race faces: Evidence from developmental prosopagnosia. Neuropsychologia, 49: 2505–2513. (doi:10.1016/j.neuropsychologia.2011.04.031)
20. DeGutis, J., Wilmer, J., Mercado, R. J., and Cohan, S., 2013. Using regression to measure holistic face processing reveals a strong link with face recognition ability, Cognition, 126, 87–100
21. Diamond, R., and Carey, S., 1986. Why faces are and are not special: An effect of expertise. Journal of Experimental Psychology: General, 115: 107–117. (doi:10.1037/0096-3445.115.2.107)
22. Duchaine, B., Germine, L., and Nakayama, K., 2007. Family resemblance: Ten family members with prosopagnosia and within-class object agnosia. Cognitive Neuropsychology, 24: 419–430. (doi:10.1080/02643290701380491)
23. Duchaine, B., Murray, H., Turner, M., White, S., and Garrido, L., 2009. Normal social cognition in developmental prosopagnosia. Cognitive Neuropsychology, 26: 620–634. (doi:10.1080/02643291003616145)
24. Duchaine, B. C., and Nakayama, K., 2006a. Developmental prosopagnosia: A window to content-specific face processing. Current Opinion in Neurobiology, 16: 166–173. (doi:10.1016/j.conb.2006.03.003)
25. Duchaine, B., and Nakayama, K., 2006b. The Cambridge Face Memory Test: Results for neurologically intact individuals and an investigation of its validity using inverted face stimuli and prosopagnosic participants. Neuropsychologia, 44: 576–585. (doi:10.1016/j.neuropsychologia.2005.07.001)
26. Duchaine, B. C., Yovel, G., Butterworth, E. J., and Nakayama, K., 2006. Prosopagnosia as an impairment to face-specific mechanisms: Elimination of the alternative hypotheses in a developmental case. Cognitive Neuropsychology, 23: 714–747. (doi:10.1080/02643290500441296)
27. Faja, S., Webb, S. J., Merkle, K., Aylward, E., and Dawson, G., 2009. Brief report: Face configuration accuracy and processing speed among adults with high-functioning autism spectrum disorders. Journal of Autism and Developmental Disorders, 39: 532–538. (doi:10.1007/s10803-008-0635-x)
28. Farah, M. J., Wilson, K. D., Drain, H. M., and Tanaka, J. R., 1995. The inverted face inversion effect in prosopagnosia: Evidence for mandatory, face-specific perceptual mechanisms. Vision Research, 35: 2089–2093. (doi:10.1016/0042-6989(94)00273-O)
29. Farah, M. J., Wilson, K. D., Drain, M., and Tanaka, J. N., 1998. What is “special” about face perception?. Psychological Review, 105: 482–498. (doi:10.1037/0033-295X.105.3.482)
30. Garner, W. R., 1974. The processing of information and structure, Potomac, MD: Lawrence Erlbaum Associates.
31. Garrido, L., Duchaine, B., and Nakayama, K., 2008. Face detection in normal and prosopagnosic individuals. Journal of Neuropsychology, 2: 119–140. (doi:10.1348/174866407X246843)
32. Germine, L., Nakayama, K., Duchaine, B., Chabris, C., Chatterjee, G., & Wilmer, J. (2012). Is the web as good as the lab? Comparable performance from web and lab in cognitive/perceptual experiments. Psychonomic Bulletin & Review, 19, 847–857.
33. Hole, G. J., 1994. Configurational factors in the perception of unfamiliar faces. Perception, 23: 65–74. (doi:10.1068/p230065)
34. Hsiao, J. H., and Cottrell, G., 2008. Two fixations suffice in face recognition. Psychological Science, 19: 998–1006. (doi:10.1111/j.1467-9280.2008.02191.x)
35. Ingvalson, E. M., and Wenger, M. J., 2005. A strong test of the dual-mode hypothesis. Perception and Psychophysics, 67: 14–35. (doi:10.3758/BF03195010)
36. Jacques, C., and Rossion, B., 2009. The initial representation of individual faces in the right occipito-temporal cortex is holistic: Electrophysiological evidence from the composite face illusion. Journal of Vision, 9 (6, Article 8): 1–16. (doi:10.1167/9.6.8)
37. Joseph, R. M., and Tanaka, J., 2003. Holistic and part-based face recognition in children with autism. Journal of Child Psychology and Psychiatry, 44: 529–542. (doi:10.1111/1469-7610.00142)
38. Kohler, W., 1940. Dynamics in psychology, New York, NY: Liveright.
39. Lee, Y., Duchaine, B., Wilson, H. R., and Nakayama, K., 2010. Three cases of developmental prosopagnosia from one family: Detailed neuropsychological and psychophysical investigation of face processing. Cortex, 46: 949–964. (doi:10.1016/j.cortex.2009.07.012)
40. Le Grand, R., Cooper, P. A., Mondloch, C. J., Lewis, T. L., Sagiv, N., de Gelder, B., and Maurer, D., 2006. What aspects of face processing are impaired in developmental prosopagnosia?. Brain and Cognition, 61: 139–158. (doi:10.1016/j.bandc.2005.11.005)
41. Macchi Cassia, V. M., Picozzi, M., Kuefner, D., Bricolo, E., and Turati, C., 2009. Holistic processing for faces and cars in preschool-aged children and adults: Evidence from the composite effect. Developmental Science, 12: 236–248. (doi:10.1111/j.1467-7687.2008.00765.x)
42. Maurer, D., Grand, R. L., and Mondloch, C. J., 2002. The many faces of configural processing. Trends in Cognitive Sciences, 6 (6): 255–260. doi:10.1016/S1364-6613(02)01903-4
43. McKone, E., and Robbins, R., 2007. The evidence rejects the expertise hypothesis: Reply to Gauthier & Bukach. Cognition, 103: 331–336. (doi:10.1016/j.cognition.2006.05.014)
44. McKone, E., and Yovel, G., 2009. Why does picture-plane inversion sometimes dissociate perception of features and spacing in faces, and sometimes not? Toward a new theory of holistic processing. Psychonomic Bulletin & Review, 16: 778–797. (doi:10.3758/PBR.16.5.778)
45. Minnebusch, D. A., Suchan, B., Ramon, M., and Daum, I., 2007. Event-related potentials reflect heterogeneity of developmental prosopagnosia. European Journal of Neuroscience, 25: 2234–2247. (doi:10.1111/j.1460-9568.2007.05451.x)
46. Nunn, J. A., Postma, P., and Pearson, R., 2001. Developmental prosopagnosia: Should it be taken at face value?. Neurocase, 7: 15–27. (doi:10.1093/neucas/7.1.15)
47. Orban de Xivry, J. J., Ramon, M., Lefevre, P., and Rossion, B., 2008. Reduced fixation on the upper area of personally familiar faces following acquired prosopagnosia. Journal of Neuropsychology, 2: 245–268. (doi:10.1348/174866407X260199)
48. Palermo, R., Willis, M. L., Rivolta, D., McKone, E., Wilson, C. E., and Calder, A. J., 2011. Impaired holistic coding of facial expression and facial identity in congenital prosopagnosia. Neuropsychologia, 49: 1226–1235. (doi:10.1016/j.neuropsychologia.2011.02.021)
49. Pitcher, D., Charles, L., Devlin, J. T., Walsh, V., and Duchaine, B., 2009. Triple dissociation of faces, bodies, and objects in extrastriate cortex. Current Biology, 19: 319–324. (doi:10.1016/j.cub.2009.01.007)
50. Ramon, M., Busigny, T., and Rossion, B., 2010. Impaired holistic processing of unfamiliar individual faces in acquired prosopagnosia. Neuropsychologia, 48: 933–944. (doi:10.1016/j.neuropsychologia.2009.11.014)
51. Ramon, M., and Rossion, B., 2010. Impaired processing of relative distances between features and of the eye region in acquired prosopagnosia—Two sides of the same holistic coin?. Cortex, 46: 374–389. (doi:10.1016/j.cortex.2009.06.001)
52. Rhodes, G., Brake, S., and Atkinson, A. P., 1993. What's lost in inverted faces?. Cognition, 47: 25–57. (doi:10.1016/0010-0277(93)90061-Y)
53. Richler, J. J., Cheung, O. S., and Gauthier, I., 2011. Holistic processing predicts face recognition. Psychological Science, 22: 464–471. (doi:10.1177/0956797611401753)
54. Richler, J. J., Tanaka, J. W., Brown, D. D., and Gauthier, I., 2008. Why does selective attention to parts fail in face processing?. Journal of Experimental Psychology: Learning, Memory, and Cognition, 34: 1356–1368. (doi:10.1037/a0013080)
55. Riddoch, M. J., and Humphreys, G. W., 1987. A case of integrative visual agnosia. Brain, 110: 1431–1462. (doi:10.1093/brain/110.6.1431)
56. Righart, R., and de Gelder, B., 2007. Impaired face and body perception in developmental prosopagnosia. Proceedings of the National Academy of Sciences, USA, 104: 17234–17238. (doi:10.1073/pnas.0707753104)
57. Rivolta, D., Palermo, R., Schmalzl, L., and Williams, M. A., 2012. Investigating the features of the m170 in congenital prosopagnosia. Frontiers in Human Neuroscience, 6: 45 (doi:10.3389/fnhum.2012.00045)
58. Robbins, R., and McKone, E., 2007. No face-like processing for objects-of-expertise in three behavioural tasks. Cognition, 103: 34–79. (doi:10.1016/j.cognition.2006.02.008)
59. Rossion, B., 2008. Picture-plane inversion leads to qualitative changes of face perception. Acta Psychologica, 128: 274–289. (doi:10.1016/j.actpsy.2008.02.003)
60. Rossion, B., 2009. Distinguishing the cause and consequence of face inversion: The perceptual field hypothesis. Acta Psychologica, 132: 300–312. (doi:10.1016/j.actpsy.2009.08.002)
61. Rossion, B., Gauthier, I., Goffaux, V., Tarr, M. J., and Crommelinck, M., 2002. Expertise training with novel objects leads to left-lateralized facelike electrophysiological responses. Psychological Science, 13: 250–257. (doi:10.1111/1467-9280.00446)
62. Rossion, B., Kaiser, M. D., Bub, D., and Tanaka, J. W., 2009. Is the loss of diagnosticity of the eye region of the face a common aspect of acquired prosopagnosia?. Journal of Neuropsychology, 3: 69–78. (doi:10.1348/174866408X289944)
63. Russell, R., Duchaine, B., and Nakayama, K., 2009. Super-recognizers: People with extraordinary face recognition ability. Psychonomic Bulletin & Review, 16: 252–257. (doi:10.3758/PBR.16.2.252)
64. Schiltz, C., Dricot, L., Goebel, R., and Rossion, B., 2010. Holistic perception of individual faces in the right middle fusiform gyrus as evidenced by the composite face illusion. Journal of Vision, 10 (2, Article 25): 21–16. (doi:10.1167/10.2.25)
65. Schmalzl, L., Palermo, R., and Coltheart, M., 2008. Cognitive heterogeneity in genetically based prosopagnosia: A family study. Journal of Neuropsychology, 2: 99–117. (doi:10.1348/174866407X256554)
66. Schmalzl, L., Palermo, R., Harris, I. M., and Coltheart, M., 2009. Face inversion superiority in a case of prosopagnosia following congenital brain abnormalities: What can it tell us about the specificity and origin of face-processing mechanisms?. Cognitive Neuropsychology, 26: 286–306. (doi:10.1080/02643290903086904)
67. Schyns, P. G., Bonnar, L., and Gosselin, F., 2002. Show me the features! Understanding recognition from the use of visual information. Psychological Science, 13: 402–409. (doi:10.1111/1467-9280.00472)
68. Seitz, K., 2002. Parts and wholes in person recognition: Developmental trends. Journal of Experimental Child Psychology, 82: 367–381. (doi:10.1016/S0022-0965(02)00106-6)
69. Sekuler, A. B., Gaspar, C. M., Gold, J. M., and Bennett, P. J., 2004. Inversion leads to quantitative, not qualitative, changes in face processing. Current Biology, 14: 391–396. (doi:10.1016/j.cub.2004.02.028)
70. Susilo, T., McKone, E., Dennett, H., Darke, H., Palermo, R., Hall, A., and Rhodes, G., 2010. Face recognition impairments despite normal holistic processing and face space coding: Evidence from a case of developmental prosopagnosia. Cognitive Neuropsychology, 27: 636–664. (doi:10.1080/02643294.2011.613372)
71. Tanaka, J. W., and Farah, M. J., 1993. Parts and wholes in face recognition. Quarterly Journal of Experimental Psychology A, 46: 225–245.
72. Tanaka, J. W., Kiefer, M., and Bukach, C. M., 2004. A holistic account of the own-race effect in face recognition: Evidence from a cross-cultural study. Cognition, 93: B1–B9. (doi:10.1016/j.cognition.2003.09.011)
73. Todorov, A., Loehr, V., and Oosterhof, N. N., 2010. The obligatory nature of holistic processing of faces in social judgments. Perception, 39: 514–532. (doi:10.1068/p6501)
74. Tree, J. J., and Wilkie, J., 2010. Face and object imagery in congenital prosopagnosia: A case series. Cortex, 46: 1189–1198. (doi:10.1016/j.cortex.2010.03.005)
75. Valentine, T., 1988. Upside-down faces: A review of the effect of inversion upon face recognition. British Journal of Psychology, 79: 471–491. (doi:10.1111/j.2044-8295.1988.tb02747.x)
76. Van Belle, G., De Graef, P., Verfaillie, K., Rossion, B., and Lefevre, P., 2010. Face inversion impairs holistic perception: Evidence from gaze-contingent stimulation. Journal of Vision, 10: 10 (doi:10.1167/10.5.10)
77. Van den Stock, J., van de Riet, W. A., Righart, R., and de Gelder, B., 2008. Neural correlates of perceiving emotional faces and bodies in developmental prosopagnosia: An event-related fMRI-study. PLoS ONE, 3: e3195 (doi:10.1371/journal.pone.0003195)
78. Vinette, C., Gosselin, F., and Schyns, P. G., 2004. Spatio-temporal dynamics of face recognition in a flash: It's in the eyes. Cognitive Science, 28: 289–301.
79. Wang, R., Li, J., Fang, H., Tian, M., and Liu, J., 2012. Individual differences in holistic processing predict face recognition ability. Psychological Science, 23: 169–177. (doi:10.1177/0956797611420575)
80. Weigelt, S., Koldewyn, K., and Kanwisher, N., 2012. Face identity recognition in autism spectrum disorders: A review of behavioral studies. Neuroscience and Biobehavioral Reviews, 36: 1060–1084. (doi:10.1016/j.neubiorev.2011.12.008)
81. Wilmer, J. B., Germine, L., Chabris, C. F., Chatterjee, G., Williams, M., Loken, E., and Duchaine, B., 2010. Human face recognition ability is specific and highly heritable. Proceedings of the National Academy of Sciences of the USA, 107: 5238–5241. (doi:10.1073/pnas.0913053107)
82. Wong, A. C., Palmeri, T. J., and Gauthier, I., 2009. Conditions for facelike expertise with objects: Becoming a Ziggerin expert—But which type?. Psychological Science, 20: 1108–1117. (doi:10.1111/j.1467-9280.2009.02430.x)
83. Xu, Y., Liu, J., and Kanwisher, N., 2005. The M170 is selective for faces, not for expertise. Neuropsychologia, 43: 588–597. (doi:10.1016/j.neuropsychologia.2004.07.016)
84. Yin, R. K., 1969. Looking at upside-down faces. Journal of Experimental Psychology, 81: 141–145. (doi:10.1037/h0027474)
85. Young, A. W., Hellawell, D., and Hay, D. C., 1987. Configurational information in face perception. Perception, 16: 747–759. (doi:10.1068/p160747)
86. Yovel, G., 2009. The shape of facial features and the spacing among them generate similar inversion effects: A reply to Rossion (2008). Acta Psychologica, 132: 293–299. (doi:10.1016/j.actpsy.2009.07.009)
87. Yovel, G., and Duchaine, B., 2006. Specialized face perception mechanisms extract both part and spacing information: Evidence from developmental prosopagnosia. Journal of Cognitive Neuroscience, 18: 580–593. (doi:10.1162/jocn.2006.18.4.580)
88. Yovel, G., Paller, K. A., and Levy, J., 2005. A whole face is more than the sum of its halves: Interactive processing in face perception. Visual Cognition, 12: 337–352. (doi:10.1080/13506280444000210)
89. Yovel, G., Pelc, T., and Lubetzky, I., 2010. It's all in your head: Why is the body inversion effect abolished for headless bodies?. Journal of Experimental Psychology: Human Perception and Performance, 36: 759–767. (doi:10.1037/a0017451)