, Volume 40, Issue 3, pp 417–438 | Cite as

Inversion effect in perception of human faces in a chimpanzee (Pan troglodytes)

  • Masaki Tomonaga


Three experiments investigated the inversion effect in face perception by a chimpanzee (Pantroglodytes) under the matching-to-sample paradigm. The first two experiments addressed the inversion effect in the perception of human faces. In Experiment 1, the subject received identity matching using 104 photographs of faces and houses presented in four different orientations. The chimpanzee showed better accuracy when the faces were presented upright than when they were inverted. The inversion effect was not found for photographs of houses. In Experiment 2, the subject received rotational matching in which the sample and comparisons differed in orientation. The subject showed a clear inversion effect for faces but not for houses. Experiment 3 explored the hemispheric specialization of the face inversion effect with chimeric (artificially composed) faces. The subject showed no visual-field preference when the chimeric faces were presented as samples under nonreinforced probe testing, while the inversion effect was evident when the discrimination was based on the left part of the chimeric sample. The results suggested that the face-inversion was specific to the left visual field (i.e. right hemispheric processing). In general, these results were consistent with those found in humans in similar testing situations.

Key words

Face perception Inversion effect Matching task Chimpanzee (Pan troglodytesHemispheric specialization 


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  1. Bard, K. A.;Platzman, K. A.;Lester, B. M.;Suomi, S. J. 1992. Orientation to social and nonsocial stimuli in neonatal chimpanzees and humans.Inf. Behav. Develop., 15: 43–56.CrossRefGoogle Scholar
  2. Bauer, H. R.;Philip, M. M. 1983. Facial and vocal individual recognition in the common chimpanzee.Psychol. Record, 33: 161–170.Google Scholar
  3. Baylis, G. C.;Rolls, E. T.;Leonard, C. M. 1985. Selectivity between faces in the responses of a population of neurons in the cortex in the superior temporal sulcus of the monkey.Brain Res. 342: 91–102.PubMedCrossRefGoogle Scholar
  4. Bruce, C. 1982. Face recognition by monkeys: absence of an inversion effect.Neuropsychologia, 20: 515–521.PubMedCrossRefGoogle Scholar
  5. Bruce, C. J.;Desimone, R.;Gross, C. G. 1981. Visual properties of neurons in a polysensory area in superior temporal sulcus of macaque.J. Neurophysiol., 46: 369–384.PubMedGoogle Scholar
  6. Bruce, V. 1983. Recognizing faces.Philosophical Transactions of the Royal Soc. Lond. B, 302: 423–436.Google Scholar
  7. Bruce, V. 1988.Recognising Faces. Erlbaum, Hillsdale, New Jersey.Google Scholar
  8. Bruce, V.;Humphreys, G. W. (eds.). 1994.Object and Face Recognition: Special Issue of Visual Cognition, Vol. 1, Erlbaum, London.Google Scholar
  9. Bruyer, R. (ed.). 1986.The Neuropsychology of Face Perception and Facial Expression, Erlbaum, Hillsdale, New Jersey.Google Scholar
  10. Carey, S.;Diamond, R. 1977. From piecemeal to configurational representation of faces.Science, 195: 312–314.PubMedCrossRefGoogle Scholar
  11. Carey, S.;Diamond, R. 1994. Are faces perceived as configurations more by adults than by children?Visual Cognition, 1: 253–274.Google Scholar
  12. Chevalier-Skolnikoff, S. 1973. Facial expression of emotion in nonhuman primates. In:Darwin and Facial Expression,Ekman,P. (ed.), Academic Press, New York, pp. 11–89.Google Scholar
  13. Dasser, V. 1988. A social concept in Java monkeys.Anim. Behav., 36: 225–230.CrossRefGoogle Scholar
  14. Davies, G.;Ellis, J. (eds.). 1981,Perceiving and Remembering Faces, Academic Press, New York.Google Scholar
  15. Delius, J. D.;Hollard, V. D. 1995. Orientation invariant pattern recognition by pigeons (Columba livia) and humans (Homo sapiens).J. Comp. Psychol., 109: 278–290.PubMedCrossRefGoogle Scholar
  16. Deruelle, C.;Fagot, J. 1998. Access to the global and local properties of compound stimuli in a visual search task: effects of perceptual grouping in humans and baboons.Psychonomic Bull. Review, 5: 476–481.Google Scholar
  17. Diamond, R.;Carey, S. 1986. Why faces are and are not special: an effect of expertise.J. Exp. Psychol. General, 115: 107–117.CrossRefGoogle Scholar
  18. Dittrich, W. 1990. Representation of faces in longtailed macaques (Macaca fascicularis).Ethology, 85: 265–278.CrossRefGoogle Scholar
  19. 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.PubMedCrossRefGoogle Scholar
  20. 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: 3–12.CrossRefGoogle Scholar
  21. Farah, M. J.;Tanaka, J.;Drain, H. M. 1995. What causes the face inversion effect?J. Exp. Psychol., Human Perception and Performance, 21: 628–634.CrossRefGoogle Scholar
  22. Fujita, K. 1990. Species preference by infant macaques with controlled social experience.Int. J. Primatol., 11: 553–573.CrossRefGoogle Scholar
  23. Fujita, K. 1993. Role of some physical characteristics in species recognition by pigtail monkeys.Primates, 34: 133–140.CrossRefGoogle Scholar
  24. Goldstein, A. G.;Chance, J. E. 1980. Memory for faces and schema theory.J. Psychol., 105: 47–59.Google Scholar
  25. Hamilton, C. R.;Vermeire, B. A. 1983. Discrimination of monkey faces by split-brain monkeys.Behav. Brain Res., 9: 263–275.PubMedCrossRefGoogle Scholar
  26. Hamilton, C. R.;Vermeire, B. A. 1988. Complementary hemispheric specialization in monkeys.Science, 242: 1691–1694.PubMedCrossRefGoogle Scholar
  27. Hamilton, C. R.;Vermeire, B. A. 1991. Functional lateralization in monkeys. In:Cerebral Laterality: Theory and Research,Kitterle,F. L. (ed.) Erlbaum, Hillsdale, New Jersey, pp. 19–34.Google Scholar
  28. Hamm, J.;Matheson, W. R.;Honig, W. K. 1997. Mental rotation in pigeons (Columba livia)?J. Comp. Psychol., 111: 76–81.CrossRefGoogle Scholar
  29. Hasselmo, M. E.;Rolls, E. T.;Baylis, G. C. 1989a. The role of expression and identity in the face-selective responses of neurons in the temporal visual cortex of the monkey.Behav. Brain Res., 32: 203–218.PubMedCrossRefGoogle Scholar
  30. Hasselmo, M. E.;Rolls, E. T.;Baylis, G. C.;Nalwa, V. 1989b. Object-centered encoding by face-selective neurons in the cortex in the superior temporal sulcus of the monkey.Exp. Brain Res., 75: 417–429.PubMedCrossRefGoogle Scholar
  31. Hauser, M. D. 1993. Right hemisphere dominance for the production of facial expression in monkeys.Science, 261: 475–477.PubMedCrossRefGoogle Scholar
  32. Hauser, M. D. 1996.The Evolution of Communication, MIT Press, Cambridge, Massachusetts.Google Scholar
  33. Hayes, K. J.;Nissen, C. H. 1971. Higher mental function of a home-raised chimpanzee. In:Behavior of Nonhuman Primates, Vol. 4,Schreier,A. M.;Stollnitz,F. (eds.), Academic Press, New York, pp. 59–115.Google Scholar
  34. Hellige, J. B. 1993.Hemispheric Asymmetry: What's Right and What's Left? Harvard Univ. Press, Cambridge, Massachusetts.Google Scholar
  35. Hellige, J. B.;Corwin, W. H.;Jonsson, J. E. 1984. Effects of perceptual quality on the processing of human faces presented to the left and right cerebral hemispheres.J. Exp. Psychol., Human Perception and Performance, 10: 90–107.CrossRefGoogle Scholar
  36. Herrnstein, R. J.;Loveland, D. H.;Cable, C. 1976. Natural concept in the pigeon.J. Exp. Psychol., Animal Behavior Processes, 2: 258–302.Google Scholar
  37. Hillger, L. A.;Koenig, O. 1991. Separable mechanisms in face processing: evidence from hemispheric specialization.J. Cognitive Neurosci., 3: 42–58.Google Scholar
  38. Hochberg, J.;Galper, R. E. 1967. Recognition of faces: I. An exploratory study.Psychonomic Sci., 9: 619–620.Google Scholar
  39. Hollard, V. D.;Delius, J. D. 1982. Rotational invariance in visual pattern recognition by pigeons and humans.Science, 218; 804–806.PubMedCrossRefGoogle Scholar
  40. Hopkins, W. D. 1997. Hemispheric specialization for local and global processing of hierarchical visual stimuli in chimpanzees (Pan troglodytes).Neuropsychologia, 35: 343–348.PubMedCrossRefGoogle Scholar
  41. Hopkins, W. D.;Fagot, J.;Vauclair, J. 1993. Mirror-image matching and mental rotation problem solving by baboons (Papio papio): unilateral input enhances performance.J. Exp. Psychol., General., 122: 61–72.CrossRefGoogle Scholar
  42. Itakura, S. 1992. Sex discrimination of photographs of human by a chimpanzee.Perceptual Motor Skills, 74: 475–478.CrossRefGoogle Scholar
  43. Jeffreys, D. A. 1989. A face-responsive potential recorded from the human scalp.Exp. Brain Res., 78: 193–202.PubMedCrossRefGoogle Scholar
  44. 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: 473–482.CrossRefGoogle Scholar
  45. Jitsumori, M.;Yoshihara, M. 1997. Categorical discrimination of human facial expression by pigeons: a test of the linear feature model.Quart. J. Exp. Psychol., 50B: 253–268.Google Scholar
  46. Kanazawa, S. 1996. Recognition of facial expressions in a Japanese monkeys (Macaca fuscata) and humans (Homo sapiens).Primates, 37: 25–38.CrossRefGoogle Scholar
  47. Keating, C. F.;Keating, E. G. 1993. Monkeys and mug shots: cues used by rheusus monkeys (Macaca mulatta) to recognize human face.J. Comp. Psychol., 107: 131–139.PubMedCrossRefGoogle Scholar
  48. Köhler, W. 1940.Dynamics in Psychology, Liveright, New York.Google Scholar
  49. Leehey, S. C.;Carey, S.;Diamond, R.;Cahn, A. 1978. Upright and inverted faces: the right hemisphere knows the difference.Cortex, 14: 411–419.PubMedGoogle Scholar
  50. Levy, J.;Heller, W.;Banich, M. T.;Burton, L. A. 1983. Asymmetry of perception in free viewing of chimeric faces.Brain Cogn., 2: 404–419.PubMedCrossRefGoogle Scholar
  51. Ley, R. G.;Bryden, M. P. 1979. Hemispheric differences in recognising faces and emotions.Brain Language, 7: 127–138.CrossRefGoogle Scholar
  52. Matsuzawa, T. 1989. Spontaneous pattern construction in a chimpanzee. In:Understanding Chimpanzees,Heltne,P. G.;Marquardt,L. A. (eds.), Harvard Univ. Press, Cambridge, Massachusetts, pp. 252–265.Google Scholar
  53. Matsuzawa, T. 1990. Form perception and visual acuity in a chimpanzee.Folia Primatol., 55: 24–32.PubMedGoogle Scholar
  54. Morris, R. D.;Hopkins, W. D. 1993. Perception of human chimeric faces by chimpanzees: evidence for a right hemispheric advantage.Brain Cogn., 21: 111–122.PubMedCrossRefGoogle Scholar
  55. Navon, D. 1977. Forest before trees: the precedence effect of global features in visual perception.Cognitive Psychol., 7: 476–484.Google Scholar
  56. Overman, W. A.;Doty, R. W. 1982. Hemispheric specialization displayed by man but not macaques for analysis of faces.Neuropsychologia, 20: 113–128.PubMedCrossRefGoogle Scholar
  57. Parr, L. A.;Dove, T.;Hopkins, W. D. 1998. Why faces may be special: evidence of the inversion effect in chimpanzees.J. Cognitive Neurosci., 10: 615–622.CrossRefGoogle Scholar
  58. Perrett, D. I.;Mistlin, A. J. 1990. Perception of facial characteristics by monkeys. In:Comparative Perception, Vol. 2,Stebbins,W. C.;Berkley,M. A. (eds.), Wiley, New York, pp. 178–215.Google Scholar
  59. Perrett, D. I.;Mistlin, A. J.;Chitty, A. J.;Smith, P. A.;Potter, D. D.;Broennimann, R.;Harries, M. 1988. Specialized face processing and hemispheric asymmetry in man and monkey: evidence from single unit and reaction time studies.Behav. Brain Res., 29: 245–258.PubMedCrossRefGoogle Scholar
  60. Perrett, D. I.;Smith, P. A.;Potter, D. D.;Mistlin, A. J.;Head, A. S.;Milner, A. D.;Jeeves, M. A. 1984. Neurons responsive to faces in the temporal cortex: studies of functional organization, sensitivity to identity and relation to perception.Human Neurobiol., 3: 197–208.Google Scholar
  61. 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.PubMedCrossRefGoogle Scholar
  62. Pineda, J. A.;Nava, C. 1993. Event-related potentials in macaque monkey during passive and attentional processing of faces in a priming paradigm.Behav. Brain Res., 53: 177–187.PubMedCrossRefGoogle Scholar
  63. Premack, D. 1975, Putting a face together.Science, 188: 228–236.PubMedCrossRefGoogle Scholar
  64. Rock, I. 1974. The perception of disoriented figures.Sci. Amer., 230: 78–85.PubMedCrossRefGoogle Scholar
  65. Rosenfeld, S. A.;Van Hoesen, G. W. 1979. Face recognition in the rhesus monkey.Neuropsychologia, 17: 503–509.PubMedCrossRefGoogle Scholar
  66. Sands, S. F.;Lincoln, C. E.;Wright, A. A. 1982. Pictorial similarity judgments and the organization of visual memory in the rhesus monkey.J. Exp. Psychol., General, 111: 369–389.CrossRefGoogle Scholar
  67. Scapinello, K. F.;Yarmey, A. D. 1970. The role of familiarity and orientation in immediate and delayed recognition of pictorial stimuli.Psychonomic Sci., 21: 329–331.Google Scholar
  68. Shepard, R. N.;Metzler, J. 1971. Mental rotation of three-dimensional objects.Science, 171: 701–703.PubMedCrossRefGoogle Scholar
  69. Suberi, M.;McKeever, W. F. 1977. Differential right hemispheric memory storage of emotional and nonemotional faces.Neuropsychologia, 5: 757–768.CrossRefGoogle Scholar
  70. Swartz, K. B. 1983. Species discrimination in infant pigtail macaques with pictorial stimuli.Develop. Psychobiol., 16: 219–231.CrossRefGoogle Scholar
  71. Tomonaga, M. 1993. Tests for control by exclusion and negative stimulus relations of arbitary matching to sample in a “symmetry-emergent” chimpanzee.J. Exp. Anal. Behav., 59: 215–229.PubMedCrossRefGoogle Scholar
  72. 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.CrossRefGoogle Scholar
  73. Tomonaga, M. 1998. Perception of shape from shading in chimpanzees (Pan troglodytes) and humans (Homo sapiens).Anim. Cognition, 1: 25–35.CrossRefGoogle Scholar
  74. 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.PubMedCrossRefGoogle Scholar
  75. Tomonaga, M.;Matsuzawa, T. 1992. Perception of complex geometric figures in chimpanzees (Pan troglodytes) and humans (Homo sapiens): analysis of visual similarity on the basis of choice reaction time.J. Comp. Psychol., 106: 43–52.PubMedCrossRefGoogle Scholar
  76. Tomonaga, M.;Matsuzawa, T.;Fujita, K.;Yamamoto, J. 1991. Emergence of symmetry in a visual conditional discrimination by chimpanzees (Pan troglodytes).Psychol. Rep., 68: 51–60.PubMedCrossRefGoogle Scholar
  77. Tonooka, R.;Matsuzawa, T. 1995. Hand preferences of captive chimpanzees (Pan troglodytes) in simple reaching for food.Int. J. Primatol., 16: 17–35.Google Scholar
  78. Valentine, T. 1988. Upside-down faces: a review of the effects of inversion upon face recognition.British J. Psychol., 79: 471–491.Google Scholar
  79. Valentine, T.;Bruce, V. 1986. The effect of race, inversion and encoding activity upon face recognition.Acta Psychol., 61: 259–273.CrossRefGoogle Scholar
  80. Valentine, T.;Bruce, V. 1988. Mental rotation of faces.Mem. Cogn., 16: 556–566.Google Scholar
  81. van Hooff, J. A. R. A. M. 1967. The facial expressions of catarrhine monkeys and apes. In:Primate Ethology,Morris,D. (ed.), Weidenfield & Nicolson, London, pp. 7–68.Google Scholar
  82. Vauclair, J.;Fagot, J.;Hopkins, W. D. 1993. Rotation of mental images in baboons when the visual input is directed to the left cerebral hemisphere.Psychol. Sci., 4: 99–103.CrossRefGoogle Scholar
  83. Wilde, J.;Vauclair, J.;Fagot, J. 1994. Eye movements in baboons performing a matching-to-sample task presented in a divided-field format.Behav. Brain Res., 63: 61–70.PubMedCrossRefGoogle Scholar
  84. 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. Cognitive Neurosci., 8: 278–290.CrossRefGoogle Scholar
  85. Yin, R. K. 1969. Looking at upside-down faces.J. Exp. Psychol., 81: 141–145.CrossRefGoogle Scholar
  86. Yin, R. K. 1970. Face recognition by brain-injured patients: a dissociable ability?Neuropsychologia, 8: 395–402.PubMedCrossRefGoogle Scholar

Copyright information

© Japan Monkey Centre 1999

Authors and Affiliations

  • Masaki Tomonaga
    • 1
  1. 1.Department of Behavioral and Brain Sciences, Primate Research InstituteKyoto UniversityAichiJapan

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