Primates

, Volume 48, Issue 1, pp 1–12 | Cite as

Visual search for orientation of faces by a chimpanzee (Pan troglodytes): face-specific upright superiority and the role of facial configural properties

Original Article

Abstract

A previous experiment showed that a chimpanzee performed better in searching for a target human face that differed in orientation from distractors when the target had an upright orientation than when targets had inverted or horizontal orientation [Tomonaga (1999a) Primate Res 15:215–229]. This upright superiority effect was also seen when using chimpanzee faces as targets but not when using photographs of a house. The present study sought to extend these results and explore factors affecting the face-specific upright superiority effect. Upright superiority was shown in a visual search for orientation when caricaturized human faces and dog faces were used as stimuli for the chimpanzee but not when shapes of a hand and chairs were presented. Thus, the configural properties of facial features, which cause an inversion effect in face recognition in humans and chimpanzees, were thought to be a source of the upright superiority effect in the visual search process. To examine this possibility, various stimuli manipulations were introduced in subsequent experiments. The results clearly show that the configuration of facial features plays a critical role in the upright superiority effect, and strongly suggest similarity in face processing in humans and chimpanzees.

References

  1. Ballaz C, Boutsen L, Peyrin C, Humphreys GW, Marendaz C (2005) Visual search for object orientation can be modulated by canonical orientation. J Exp Psychol Hum Percept Perform 31:20–39CrossRefPubMedGoogle Scholar
  2. Blough DS (1979) Effects of the number and form of stimuli on visual search in the pigeon. J Exp Psychol Anim Behav Process 5:211–223CrossRefPubMedGoogle Scholar
  3. Bruce C (1982) Face recognition by monkeys: absence of an inversion effect. Neurophsychologia 20:515–521CrossRefGoogle Scholar
  4. Campbell R, Walker J, Baron-Cohen S (1995) The development of differential use of inner and outer face features in familiar face identification. J Exp Child Psychol 59:196–210CrossRefGoogle Scholar
  5. Carey S, Diamond R (1977) From piecemeal to configurational representation of faces. Science 195:312–314CrossRefPubMedGoogle Scholar
  6. Carey S, Diamond R (1994) Are faces perceived as configurations more by adults than by children? Visual Cogn 1:253–274CrossRefGoogle Scholar
  7. Diamond R, Carey S (1986) Why faces are and are not special: an effect of expertise. J Exp Psychol 115:107–117CrossRefGoogle Scholar
  8. Dittrich WH (1990) Representation of faces in longtailed macaques (Macaca fascicularis). Ethology 85:265–278CrossRefGoogle Scholar
  9. Ellis HD, Shepherd JW, Davies GM (1979) Identification of familiar and unfamiliar faces from internal and external features: some implications for theories of face recognition. Perception 8:431–439CrossRefPubMedGoogle Scholar
  10. Fagot J, Tomonaga M (1999) Global-local processing in humans (Homo sapiens) and chimpanzees (Pan troglodytes): use of a visual search task with compound stimuli. J Comp Psychol 113:3–12CrossRefGoogle Scholar
  11. Farah MJ, Tanaka JW, Drain HM (1995) What causes the face inversion effect? J Exp Psychol Hum Percept Perform 21:628–634CrossRefPubMedGoogle Scholar
  12. Gothard KM, Erickson CA, Amaral DG (2004) How do rhesus monkeys (Macaca mulatta) scan faces in a visual paired comparison task? Anim Cogn 7:25–36CrossRefPubMedGoogle Scholar
  13. von Grünau M, Anston C (1995) The detection of gaze direction: a stare-in-the-crowd effect. Perception 24:1297–1313CrossRefGoogle Scholar
  14. Hamilton CR, Vermeire BA (1983) Discrimination of monkey faces by split-brain monkeys. Behav Brain Res 9:263–275CrossRefPubMedGoogle Scholar
  15. Hamilton CR, Vermeire BA (1988) Complementary hemispheric specialization in monkeys. Science 242:1691–1694CrossRefPubMedGoogle Scholar
  16. Hansen C, Hansen R (1988) Finding the face in the crowd: an anger superiority effect. J Pers Soc Psychol 54:917–924CrossRefPubMedGoogle Scholar
  17. Hershler O, Hochstein S (2005) At first sight: a high-level pop out effect for faces. Vis Res 45:1707–1724CrossRefPubMedGoogle Scholar
  18. Hunnius S, Geuze RH (2004) Developmental changes in visual scanning of dynamic faces and abstract stimuli in infants: a longitudinal study. Infancy 6:231–255CrossRefGoogle Scholar
  19. Jitsumori M, Matsuzawa T (1991) Picture perception in monkeys and pigeons: transfer of rightside-up versus upside-down discrimination of photographic objects across conceptual categories. Primates 32:473–482CrossRefGoogle Scholar
  20. Johnson MH, Morton J (1991) Biology and cognitive development the case of face recognition. Blackwell, CambridgeGoogle Scholar
  21. Kanazawa S (1996) Recognition of facial expressions in a Japanese monkey (Macaca fuscata) and humans (Homo sapiens). Primates 37:25–38CrossRefGoogle Scholar
  22. Keating CF, Keating EG (1993) Monkeys and mug shots: cues used by rhesus monkeys (Macaca mulatta) to recognize a human face. J Comp Psychol 107:131–139CrossRefPubMedGoogle Scholar
  23. Kuwahata H (2004) Comparative–cognitive studies on face recognition in primates. PhD dissertation, Kyoto University, JapanGoogle Scholar
  24. Kuwahata H, Fujita K, Ishikawa S, Myowa-Yamakoshi M, Tomonaga M, Tanaka M, Matsuzawa T (2003) Recognition of facial patterns in infant chimpanzees (in Japanese). In: Tomonaga M, Tanaka M, Matsuzawa (eds) Cognitive and behavioral development in chimpanzees: a comparative approach. Kyoto University Press, Kyoto pp 89–93Google Scholar
  25. Levin DT (1996) Classifying faces by race: the structure of face categories. J Exp Psychol Learn Mem Cogn 22:1364–1382CrossRefGoogle Scholar
  26. Lewis MB, Edmonds AJ (2005) Searching for faces in scrambled scenes. Visual Cogn 12:1309–1336CrossRefGoogle Scholar
  27. Luria AR, Pravdina-Vinarskaya EN, Yarbus AL (1964) Eye movement mechanisms in normal and pathological vision. Sov Psychol Psychiatry 2:28–39Google Scholar
  28. Malinowski P, Hübner R (2001) The effect of familiarity on visual-search performance: evidence for learned basic features. Percept Psychophys 63:458–463CrossRefPubMedGoogle Scholar
  29. Martin-Malivel J, Fagot J (2001) Perception of pictorial human faces by baboons: effects of stimulus orientation on discrimination performance. Anim Learn Behav 29:10–20CrossRefGoogle Scholar
  30. Masuda S (2003) Effect of familiarity on visual search for faces (in Japanese). In: Proceedings of the 67th annual convention of the Japanese Psychological Association. Japanese Psychological Association, Tokyo, p 599Google Scholar
  31. Matsuzawa T (1990) Form perception and visual acuity in a chimpanzee. Folia Primatol 55:24–32CrossRefPubMedGoogle Scholar
  32. Montoute T, Tiberghien G (2001) Unconscious familiarity and local context effects on low-level face processing: a reconstruction hypothesis. Conscious Cogn 10:503–523CrossRefPubMedGoogle Scholar
  33. Myowa-Yamakoshi M, Tomonaga M, Tanaka M, Matsuzawa T (2003) Preference for human direct gaze in infant chimpanzees (Pan troglodytes). Cognition 89:B53–64CrossRefPubMedGoogle Scholar
  34. Myowa-Yamakoshi M, Yamaguchi M, Tomonaga M, Tanaka M, Matsuzawa T (2005) Development of face recognition in infant chimpanzees (Pan troglodytes). Cogn Dev 20:49–63CrossRefGoogle Scholar
  35. Nahm FKD, Perrett A, Amaral DG, Albright TD (1998) How do monkeys look at faces? J Cogn Neurosci 9:611–623CrossRefGoogle Scholar
  36. Nothdurft HC (1993) Faces and facial expressions do not pop out. Perception 22:1287–1298CrossRefPubMedGoogle Scholar
  37. Ochiai T, Matsuzawa T (1998) Planting trees in an outdoor compound of chimpanzees for an enriched environment. In: Hare VJ, Worley E (eds) Proceedings of the third international conference on environmental enrichment. The Shape of Enrichment, San Diego pp 355–364Google Scholar
  38. Öhman A, Lundqvist D, Esteves F (2001) The face in the crowd revisited: a threat advantage with schematic stimuli. J Pers Soc Psychol 80:381–396CrossRefPubMedGoogle Scholar
  39. Overman WH, Doty RW (1982) Hemispheric specialization displayed by man but not macaques for analysis of faces. Neuropsychologia 20:113–128CrossRefPubMedGoogle Scholar
  40. Parr LA, Dove T, Hopkins WD (1998) Why faces may be special: evidence of the inversion effect in chimpanzees. J Cogn Neurosci 10:615–622CrossRefPubMedGoogle Scholar
  41. Parr LA, Winslow IT, Hopkins WD (1999) Is the inversion effect in rhesus monkey face-specific? Anim Cogn 2:123–129CrossRefGoogle Scholar
  42. Perrett DI, Mistlin AJ (1990) Perception of facial characteristics by monkeys. In: Stebbins WC, Berkley MA (eds) Comparative perception vol 2, Wiley, New York, pp 178–215Google Scholar
  43. Phelps MT, Roberts WA (1994) Memory for pictures of upright and inverted primate faces in humans (Homo sapiens), squirrel monkeys (Saimiri sciureus), and pigeons (Columbia livia). J Comp Psychol 108:114–125CrossRefPubMedGoogle Scholar
  44. Purcell DG, Stewart AL (1986) The face-detection effect. Bull Psychon Soc 24:118–120CrossRefGoogle Scholar
  45. Purcell DG, Stewart AL (1988) The face-detection effect: configuration enhances detection. Percept Psychophys 43:355–366CrossRefPubMedGoogle Scholar
  46. Rosenfeld SA, Van Hoesen GW (1979) Face recognition in the rhesus monkey. Neuropsychologia 175:503–509CrossRefGoogle Scholar
  47. Sato N, Nakamura K (1999) Detection of directed gaze in rhesus monkeys (Macaca mulatta). J Comp Psychol 115:115–121CrossRefGoogle Scholar
  48. Senju A, Hasegawa T, Tojo Y (2005) Does perceived direct gaze boost detection in adults and children with and without autism? The stare-in-the-crowd effect revisited. Visual Cogn 12:1474–1496CrossRefGoogle Scholar
  49. Shen J, Reingold EM (2001) Visual search asymmetry: the influence of stimulus familiarity and low-level features. Percept Psychophys 63:464–475CrossRefPubMedGoogle Scholar
  50. Suzuki S, Cavanagh P (1995) Facial organization blocks access to low-level features: an object inferiority effect. J Exp Psychol Hum Percept Perform 21:901–913CrossRefGoogle Scholar
  51. Tanaka JW, Farah MJ (1991) Second-order relational properties and the inversion effect: testing a theory of face perception. Percept Psychophys 50:367–372CrossRefPubMedGoogle Scholar
  52. Tomonaga M (1993a) Use of multiple-alternative matching-to-sample in the study of visual search in a chimpanzee (Pan troglodytes). J Comp Psychol 107:75–83CrossRefPubMedGoogle Scholar
  53. Tomonaga M (1993b) Tests for control by exclusion and negative stimulus relations of arbitrary matching to sample in a “symmetry-emergent” chimpanzee. J Exp Anal Behav 59:215–229CrossRefPubMedPubMedCentralGoogle Scholar
  54. Tomonaga M (1994) How laboratory-raised Japanese monkeys (Macaca fuscata) perceive rotated photographs of monkeys: evidence for an inversion effect in face perception. Primates 35:155–165CrossRefGoogle Scholar
  55. Tomonaga M (1995) Visual search by chimpanzees (Pan): assessment of controlling relations. J Exp Anal Behav 63:175–186CrossRefPubMedPubMedCentralGoogle Scholar
  56. Tomonaga M (1997) Precuing the target location in visual searching by a chimpanzee (Pan troglodytes): effects of precue validity. Jpn Psychol Res 39:200–211CrossRefGoogle Scholar
  57. Tomonaga M (1999a) Visual search for orientation of faces by a chimpanzee (Pan troglodytes) (in Japanese with English abstract). Primate Res 15: 215–229 CrossRefGoogle Scholar
  58. Tomonaga M (1999b) Inversion effect in perception of human faces in a chimpanzee (Pan troglodytes). Primates 40:417–438CrossRefGoogle Scholar
  59. Tomonaga M (1999c) Establishing functional classes in a chimpanzee (Pan troglodytes) with a 2-item sequential-responding procedure. J Exp Anal Behav 72:57–79CrossRefGoogle Scholar
  60. Tomonaga M (2001a) Investigating visual perception and cognition in chimpanzees (Pan troglodytes) through visual search and related tasks: from basic to complex processes. In: Matsuzawa T (eds) Primate origin of human cognition and behavior. Springer, Tokyo, pp 55–86Google Scholar
  61. Tomonaga M (2001b) Visual search for biological motion patterns in chimpanzees (Pan troglodytes). Psychologia 44:46–59Google Scholar
  62. Tomonaga M, Matsuzawa T (1992) Perception of complex geometric figures in chimpanzees (Pan troglodytes) and humans (Homo sapiens): analyses of visual similarity on the basis of choice reaction time. J Comp Psychol 106:43–52CrossRefPubMedGoogle Scholar
  63. Tomonaga M, Itakura S, Matsuzawa T (1993) Superiority of conspecific faces and reduced inversion effect in face perception by a chimpanzee. Folia Primatol 61:110–114CrossRefPubMedGoogle Scholar
  64. Tomonaga M, Myowa-Yamakoshi M, Mizuno Y, Yamaguchi MK, Kosugi D, Bard KA, Tanaka M, Matsuzawa T (2004) Development of social cognition in infant chimpanzees (Pan troglodytes): face recognition, smiling, gaze and the lack of triadic interactions. Jpn Psychol Res 46:227–235CrossRefGoogle Scholar
  65. Tong F, Nakayama K (1999) Robust representations for faces: evidence from visual search. J Exp Psychol Hum Percept Perform 25:1016–1035CrossRefPubMedGoogle Scholar
  66. Treisman A, Gelade G (1980) A feature-integration theory of attention. Cogn Psychol 12:97–136CrossRefPubMedGoogle Scholar
  67. Valentine T (1988) Upside-down faces: a review of the effects of inversion upon face recognition. Br J Psychol 79:471–491CrossRefPubMedGoogle Scholar
  68. Wang Q, Cavanagh P, Green M (1994) Familiarity and pop-out in visual search. Percept Psychophys 56:495–500CrossRefPubMedGoogle Scholar
  69. Williams M, Moss SA, Bradshaw JL, Mattingley JB (2005) Look at me, I’m smiling: visual search for threatening and nonthreatening facial expressions. Visual Cogn 12:29–50CrossRefGoogle Scholar
  70. Wolfe JM (2001) Asymmetries in visual search: an introduction. Percept Psychophys 63:381–389CrossRefPubMedGoogle Scholar
  71. Wright AA, Roberts WA (1996) Monkey and human face perception: inversion effects for human but not for monkey faces or scenes. J Cogn Neurosci 8:278–290CrossRefPubMedGoogle Scholar
  72. Yamaguchi MK, Hirukawa T, Kanazawa S (1995) Judgment of gender through facial parts. Perception 24:563–575CrossRefPubMedGoogle Scholar
  73. Yarbus AL (1967) Eye movements and vision. Plenum, New YorkCrossRefGoogle Scholar
  74. Yin RK (1969) Looking at upside-down faces. J Exp Psychol 81:141–145CrossRefGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer-Verlag 2006

Authors and Affiliations

  1. 1.Language and Intelligence Section, Primate Research InstituteKyoto UniversityInuyama, KanrinJapan

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