The evolution of face processing in primates

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 366, Issue 1571, 2011, Pages 1764-1777

  Parr, Lisa A ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Face recognition; Holistic processing; Primates

Indexed keywords

HOLISTIC APPROACH; PARADIGM SHIFT; PRIMATE; RECOGNITION; SPECIALIZATION;

ANIMAL; COGNITION; DISCRIMINATION LEARNING; EVOLUTION; EYE; FACE; HUMAN; ORIENTATION; PRIMATE; RECOGNITION; REVIEW; SPECIES DIFFERENCE; VISION;

ANIMALS; BIOLOGICAL EVOLUTION; COGNITION; DISCRIMINATION LEARNING; EYE; FACE; HUMANS; ORIENTATION; PRIMATES; RECOGNITION (PSYCHOLOGY); SPECIES SPECIFICITY; VISUAL PERCEPTION;

PAN; PRIMATES;

EID: 79955750931     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2010.0358     Document Type: Review

References (87)

1. Farah,M.J.,Wilson,K.D.,Drain,M. and Tanaka, J.W. 1998 What's special about face perception? Psychol. Rev. 105, 482-498. (doi:10.1037/0033-295X.105.3.482)
2. Maurer, D., Le Grand, R. & Mondloch, C. J. 2002 The many faces of configural processing. Trends Cogn. Sci. 6, 255-260. (doi:10.1016/S1364-6613(20)01903-4)
3. Rossion, B. 2008 Picture-plane inversion leads to qualitative changes of face perception. Acta Psychol. 128, 274-289. (doi:10.1016/j.actpsy.2008.02.003)
4. Haxby, J. V., Hoffman, E. A. & Gobbini, M. I. 2000 The distributed human neural system for face perception. Trends Cogn. Sci. 4, 223-233. (doi:10.1016/S1364-6613(00)01482-0)
5. Kanwisher, N., McDermott, J. & Chun, M. M. 1997 The fusiform face area: a module in human extrastriate cortex specialized for face perception. J. Neurosci. 17, 4302-4311.
6. McCarthy, G., Puce, A., Gore, J. C. & Allison, T. 1997 Face-specific processing in the human fusiform gyrus. J. Cogn. Neurosci. 9, 605-610. (doi:10.1162/jocn.1997. 9.5.605)
7. Tarr, M. J. & Gauthier, I. 2000 FFA: a flexible fusiform area for subordinate-level visual processing automatized by expertise. Nat. Neurosci. 3, 764-769. (doi:10.1038/77666)
8. Rosenfeld, S. A. & Van Hoesen, G. W. 1979 Face recognition in the rhesus monkey. Neuropsychologia 17, 503-509. (doi:10.1016/0028-3932(79)90057-5)
9. Bruce, C. 1982 Face recognition by monkeys: absence of an inversion effect. Neuropsychologia 20, 515-521. (doi:10.1016/0028-3932(82)90025-2)
10. Mendelson, M. J. 1982 Visual and social responses in infant rhesus monkeys. Am. J. Primatol. 3, 333-340. (doi:10.1002/ajp.1350030134)
11. Overman, W. H. & Doty, R. W. 1982 Hemispheric specialization displayed by man but not macaques for analysis of faces. Neuropsychologia 20, 113-128. (doi:10.1016/0028-3932(82)90002-1)
12. Kyes, R. C. & Candland, D. K. 1987 Baboon (Papio hamadryas) visual preferences for regions of the face. J. Comp. Psychol. 101, 345-348. (doi:10.1037/0735-7036.101.4.345)
13. Dittrich, W. 1990 Representation of faces in longtailed macaques (Macaca fascicularis). Ethology 85, 265-278. (doi:10.1111/j.1439-0310.1990.tb00406.x)
14. Keating, C. F. & Keating, E. G. 1993 Monkeys and mug shots: cues used by rhesus monkeys (Macaca mulatta) to recognize a human face. J. Comp. Psychol. 107, 131-139. (doi:10.1037/0735-7036.107.2.131)
15. Tomonaga, M., Itakura, S. & Matsuzawa, T. 1993 Superiority of conspecific faces and reduced inversion effect in face perception by a chimpanzee. Folia Primatol. 61, 110-114. (doi:10.1159/000156737)
16. Phelps, M. T. & Roberts, W. A. 1994 Memory for pictures of upright and inverted primate faces in humans (Homo sapiens), squirrel monkeys (Saimiri sciureus), and pigeons (Columba livia). J. Comp. Psychol. 108, 114-125. (doi:10.1037/0735-7036.108.2.114)
17. Tomonaga, M. 1994 How laboratory-raised Japanese monkeys (Macaca fuscata) perceive rotated photographs of monkeys: evidence for an inversion effect in face perception. Primates 35, 155-165. (doi:10.1007/BF02382051)
18. Wilson, F. A. W. & Goldman-Rakic, P. S. 1994 Viewing preferences of rhesus monkeys related to memory for complex pictures, colours and faces. Behav. Brain Res. 60, 79-89. (doi:10.1016/0166-4328(94)90066-3)
19. Wright, A. A. & Roberts, W. A. 1996 Monkey and human face perception: inversion effects for human faces but not for monkey faces or scenes. J. Cogn. Neurosci. 8, 278-290.(doi:10.1162/jocn.1996.8.3.278)
20. Parr, L. A., Dove, T. & Hopkins, W. D. 1998 Why faces may be special: evidence for the inversion effect inchimpanzees (Pan troglodytes). J. Cogn. Neurosci. 10, 615-622. (doi:10.1162/089892998563013)
21. Parr, L. A. & de Waal, F. B. M. 1999 Visual kin recognition in chimpanzees. Nature 399, 647-648. (doi:10.1038/21345)
22. Vermeire, B. A. & Hamilton, C. R. 1998 Inversion effect for faces in split-brain monkeys. Neuropsychologia 36, 1003-1014. (doi:10.1016/S0028-3932(98)00054-2)
23. Parr, L. A., Winslow, J. T. & Hopkins, W. D. 1999 Is the inversion effect in rhesus monkeys face specific? Anim. Cogn. 2, 123-129. (doi:10.1007/s100710050032)
24. Tomonaga, M. 1999 Inversion effect in perception of human faces in a chimpanzee (Pan troglodytes). Primates 40, 417-438. (doi:10.1007/BF02557579)
25. Parr, L. A., Winslow, J. T., Hopkins, W. D. & de Waal, F. B. M. 2000 Recognizing facial cues: individual recognition in chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta). J. Comp. Psychol. 114, 47-60. (doi:10.1037/0735-7036.114.1.47)
26. Myowa-Yamakoshi, M. & Tomonaga, M. 2001 Developmentof face recognition in an infant gibbon (Hylobatesagilis). Infant Behav. Dev. 24, 215-227. (doi:10.1016/ S0163-6383(01)00076-5)
27. Sato, N. & Nakamura, K. 2001 Detection of directed gaze in rhesus monkeys (Macaca mulatta). J. Comp. Psychol. 115, 115-121. (doi:10.1037/0735-7036.115.2.115)
28. Weiss, D. J., Kralik, J. D. & Hauser, M. D. 2001 Face processing in cotton-top tamarins (Saguinus oedipus). Anim. Cogn. 4, 191-205. (doi:10.1007/s100710000076)
29. Gothard, K. M., Erickson, C. A. & Amaral, D. G. 2004 How do rhesus monkeys (Macaca mulatta) scan faces in a visual paired comparison task? Anim. Cogn. 7, 25-36. (doi:10.1007/s10071-003-0179-6)
30. Kuwahata, H., Adachi, I., Fujita, K., Tomonaga, M. & Matsuzawa, T. 2004 Development of schematic face preferences in macaque monkeys. Behav. Process. 66, 17-21. (doi:10.1016/j.beproc.2003.11.002)
31. Dufour, V., Pascalis, O. & Petit, O. 2006 Face processing limitation to own species in primates: a comparative study in brown capuchins, Tonkean macaques and humans. Behav. Process. 73, 107-113. (doi:10.1016/j.beproc.2006.04.006)
32. Parr, L. A., Heintz, M. & Akamagwuna, U. 2006 Three studies of configural face processing by chimpanzees. Brain Cogn. 62, 30-42. (doi:10.1016/j.bandc.2006.03.006)
33. Parr, L. A. & Heintz, M. 2006 The perception of unfamiliar faces and houses by chimpanzees: influence of rotation angle. Perception 35, 1473-1483. (doi:10.1068/p5455)
34. Dahl, C. D., Logothetis, N. K. & Hoffman, K. L. 2007 Individuation and holistic processing of faces in rhesus monkeys. Proc. R. Soc. B 274, 2069-2076. (doi:10.1098/rspb.2007.0477)
35. Martin-Malivel, J. & Okada, K. 2007 Human and chimpanzee face recognition in chimpanzees (Pan troglodytes): role of exposure and impact on categorical perception. Behav. Neurosci. 121, 1145-1155. (doi:10.1037/0735-7044.121.6.1145)
36. Neiworth, J. J., Hassett, J. M. & Sylvester, C. J. 2007 Face processing in humans and New World monkeys: the influence of experiential and ecological factors. Anim. Cogn. 10, 125-134. (doi:10.1007/s10071-006-0045-4)
37. Tomonaga, M. 2007 Visual search for orientation of faces by a chimpanzee (Pan troglodytes): face-specific upright superiority and the role of facial configural properties. Primates 48, 1-12. (doi:10.1007/s10329-006-0011-4)
38. Parr, L. A. & Heintz, M. 2008 Discrimination of faces and houses by rhesus monkeys: the role of stimulus expertise and rotation angle. Anim. Cogn. 11, 467-474. (doi:10.1007/s10071-008-0137-4)
39. Parr, L. A., Heintz, M. & Pradhan, G. 2008 Rhesus monkeys (Macaca mulatta) lack face expertise. J. Comp. Psychol. 122, 390-402. (doi:10.1037/0735-7036.122.4.390)
40. Parron, C. & Fagot, J. 2008 Baboons (Papio papio) spontaneously process the first-order but not second-order configural properties of faces. Am. J. Primatol. 70, 415-422. (doi:10.1002/ajp.20503)
41. Sugita, Y. 2008 Face perception in monkeys reared with no exposure to faces. Proc. Natl Acad. Sci. USA 105, 394-398. (doi:10.1073/pnas.0706079105)
42. Gothard, K. M., Brooks, K. N. & Peterson, M. A. 2009 Multiple perceptual strategies used by macaque monkeys for face recognition. Anim. Cogn. 12, 155-167. (doi:10. 1007/s10071-008-0179-7)
43. Dahl, C. D., Wallraven, C., Bülthoff, H. H. & Logothetis, N. K. 2009 Humans and macaques employee similar face processing strategies. Curr. Biol. 19, 509-513. (doi:10.1016/j.cub.2009.01.061)
44. Adachi, I., Chou, D. P. & Hampton, R. R. 2009 Thatcher effect in monkeys demonstrates conservation of face perception across primates. Curr. Biol. 19, 1270-1273. (doi:10.1016/j.cub.2009.05.067)
45. Pokorny, J. J. & de Waal, F. B. M. 2009 Face recognition in capuchin monkeys (Cebus paella). J. Comp. Psychol. 123, 151-160. (doi:10.1037/a0014073)
46. Pokorny, J. J. & de Waal, F. B. M. 2009 Monkeys recognize the faces of group mates in photographs. Proc. Natl Acad. Sci. USA 106, 21539-21543. (doi:10.1073/pnas. 0912174106)
47. Taubert, J. & Parr, L. A. 2009 Visual expertise does not predict the composite effect across species: a comparison between spider (Ateles geoffroyi) and rhesus (Macaca mulatta) monkeys. Brain Cogn. 71, 187-195. (doi:10.1016/j.bandc.2009.09.002)
48. Taubert, J. 2010 Evidence of human-like holistic face processing in spider monkeys (Ateles geoffroyi). J. Comp. Psychol. 124, 57-65. (doi:10.1037/a0017704)
49. Dahl, C. D., Logothetis, N. K., Bulthoff, H. H. & Wallraven, C. 2010 The Thatcher illusion in humans and monkeys. Proc. R. Soc. B 277, 2973-2981. (doi:10.1098/rspb.2010.0438)
50. Tomonaga, M. & Imura, T. 2010 Visual search for human gaze direction by a chimpanzee (Pan troglodytes). PLoS ONE 9, e9131. (doi:10.1371/journal.pone.0009131)
51. Diamond, R. & Carey, S. 1986 Why faces are and are not special: an effect of expertise. J. Exp. Psychol. 115, 107-117. (doi:10.1037/0096-3445.115.2.107)
52. Goren, C., Sarty, M. & Wu, P. 1975 Visual following and pattern discrimination of face-like stimuli by newborn infants. Pediatrics 56, 544-549.
53. Valenza, E., Simion, F., Cassia, V. M. & Umilta, C. 1996 Face preference at birth. J. Exp. Psychol. Human 22, 892-903. (doi:10.1037/0096-1523.22.4.892)
54. Bruce, V. & Langton, S. 1994 The use of pigmentation and shading information in recognizing the sex and identities of faces. Perception 23, 803-822. (doi:10.1068/p230803)
55. Mondloch, C. J., Geldart, S., Maurer, D. & Le Grand, R. 2003 Developmental changes in face processing skills. J. Exp. Child Psychol. 86, 67-84. (doi:10.1016/S0022-0965(03)00102-4)
56. Mervis, C. & Rosch, E. 1981 Categorization of natural objects. Annu. Rev. Psychol. 32, 89-115. (doi:10.1146/annurev.ps.32.020181.000513)
57. Rhodes, G. 1988 Looking at faces: first and second-order features as determinants of facial appearance. Perception 17, 43-63. (doi:10.1068/p170043)
58. Richler, J. J., Mack, M. L., Gauthier, I. & Palmeri, T. J. 2009 Holistic processing of faces happens at a glance. Vis. Res. 49, 2856-2861. (doi:10.1016/j.visres.2009.08.025)
59. Tanaka, J. W. & Farah, M. J. 1993 Parts and wholes in face recognition. Q. J. Exp. Psychol. 46A, 225-245.
60. Yin, R. K. 1969 Looking at upside-down faces. J. Exp. Psychol. 81, 141-145. (doi:10.1037/h0027474)
61. Young, A. W., Hellawell, D. & Hay, D. C. 1987 Configurational information in face perception. Perception 16, 747-759. (doi:10.1068/p160747)
62. Robbins, R. & McKone, E. 2007 No face-like processing for objects-of-expertise in three behavioral tasks. Cognition 103, 34-79. (doi:10.1016/j.cognition.2006.02.008)
63. Pascalis, O., de Haan, M. & Nelson, C. A. 2002 Is face processing species-specific during the first year of life? Science 296, 1321-1323. (doi:10.1126/science.1070223)
64. Schwarzer, G., Zauner, N. & Jovanovic, B. 2007 Evidence of a shift from feature to configural face processing in infancy. Dev. Sci. 10, 452-463. (doi:10.1111/j.1467-7687.2007.00599.x)
65. Matsuzawa, T. 2007 Comparative cognitive development. Dev. Sci. 10, 97-103. (doi:10.1111/j.1467-7687.2007.00570.x)
66. de Heering, A., de Liedekerke, C., Deboni, M. & Rossion, B. 2010 The role of experience in childhood in shaping the other-race effect. Dev. Sci. 13, 181-187. (doi:10.1111/j.1467-7687.2009.00876.x)
67. Rhodes, G., Tan, S., Brake, S. & Taylor, K. 1989 Expertise and configural coding in face recognition. Br. J. Psychol. 80, 313-331.
68. Le Grand, R., Mondloch, C. J., Maurer, D. & Brent, H. P. 2001 Early visual experience and face processing. Nature 410, 890. (doi:10.1038/35073749)
69. Valentine, T. 1988 Upside-down faces: a review of the effects of inversion upon face recognition. Br. J. Psychol. 79, 471-491.
70. Taubert, J. 2009 Chimpanzee faces are 'special' to humans. Perception 38, 343-356. (doi:10.1068/p6254)
71. McKelvie, S. J. 1976 The role of eyes and mouth in the memory of a face. Am. J. Psychol. 89, 311-323. (doi:10.2307/1421414)
72. Schyns, P. G., Bonnar, L. & Gosselin, F. 2002 Show me the features! Understanding recognition from the use of visual information. Psychol. Sci. 13, 402-409. (doi:10.1111/1467-9280.00472)
73. Hinde, R. A. & Rowell, T. E. 1962 Communication by postures and facial expressions in the rhesus monkey (Macaca mulatta). Proc. Zool. Soc. Lond. 138, 1-21.
74. Van Hooff, J. A. R. A. M. 1967 The facial displays of the Catarrhine monkeys and apes. In Primate ethology (ed. D. Morris), pp. 7-68. Chicago, IL: Aldine.
75. Parr,L.A.,Heintz,M.,Lonsdorf,E. and Wroblewski,E. 2010 Visual kin recognition in nonhuman primates: inbreeding avoidance or male distinctiveness. J. Comp. Psychol. 124, 343-350. (doi:10.1037/a0020545)
76. Bruce, V. 1983 Recognizing faces. Phil. Trans. R. Soc. Lond. B 302, 423-436. (doi:10.1098/rstb.1983.0065)
77. Hancock, P. J. B., Bruce, V. & Burton, A. M. 2000 Recognition of unfamiliar faces. Trends Cogn. Sci. 4, 330-337. (doi:10.1016/S1364-6613(00)01519-9)
78. Megreya, A. M. & Burton, A. M. 2006 Unfamiliar faces are not faces: evidence from a matching task. Mem. Cogn. 34, 865-876. (doi:10.3758/BF03193433)
79. Goffaux, V. & Rossion, B. 2006 Faces are 'spatial': holistic face perception is supported by low-spatial frequencies. J. Exp. Psychol. Human 32, 1023-1039. (doi:10.1037/0096-1523.32.4.1023)
80. de Heering, A., Rossion, B., Turati, C. & Simion, F. 2008 Holistic face processing can be independent of gaze behavior: evidence from the composite face illusion. J. Neuropsychol. 2, 183-195. (doi:10.1348/174866407X 251694)
81. Gibboni, R. R., Zimmerman, P. E. & Gothard, K. M. 2009 Individual differences in scan paths correspond with serotonin transporter genotype and behavioral phenotype in rhesus monkeys (Macaca mulatta). Front. Behav. Neurosci. 3, 50. (doi:10.3389/neuro.08.050.2009)
82. Mondloch, C. J., Le Grand, R. & Maurer, D. 2002 Configural face processing develops more slowly than featural face processing. Perception 31, 553-566. (doi:10.1068/p3339)
83. Parron, C. & Fagot, J. 2007 Baboons (Papio papio) spontaneously process the first-order but not second-order configural properties of faces. Am. J. Primatol. 70, 415-422. (doi:10.1002/ajp.20503)
84. de Waal, F. B. M. & Aureli, F. 1997 Conflict resolution and distress alleviation in monkeys and apes. Ann. N Y Acad. Sci. 807, 317-328. (doi:10.1111/j.1749-6632. 1997.tb51929.x)
85. Fraser, O.N. & Aureli, F. 2008 Reconciliation, consolation and post-conflict behavioral specificity in chimpanzees. Am. J. Primatol. 70, 1114-1123. (doi:10.1002/ajp.20608)
86. Amici, F., Aureli, F. & Call, J. 2008 Fission-fusion dynamics, behavioral flexibility, and inhibitory control in primates. Curr. Biol. 18, 1415-1419. (doi:10.1016/j.cub.2008.08.020)
87. Crookes, K. & McKone, E. 2009 Early maturity of face recognition: no childhood development of holistic processing, novel face encoding, or face space. Cognition 111, 219-247. (doi:10.1016/j.cognition.2009.02.004)