Skip to main content
SpringerLink
Log in

Facial perception of conspecifics: chimpanzees (Pan troglodytes) preferentially attend to proper orientation and open eyes

  • Original Paper
  • Published:
Animal Cognition Aims and scope Submit manuscript

Abstract

This paper reports on the use of an eye-tracking technique to examine how chimpanzees look at facial photographs of conspecifics. Six chimpanzees viewed a sequence of pictures presented on a monitor while their eye movements were measured by an eye tracker. The pictures presented conspecific faces with open or closed eyes in an upright or inverted orientation in a frame. The results demonstrated that chimpanzees looked at the eyes, nose, and mouth more frequently than would be expected on the basis of random scanning of faces. More specifically, they looked at the eyes longer than they looked at the nose and mouth when photographs of upright faces with open eyes were presented, suggesting that particular attention to the eyes represents a spontaneous face-scanning strategy shared among monkeys, apes, and humans. In contrast to the results obtained for upright faces with open eyes, the viewing times for the eyes, nose, and mouth of inverted faces with open eyes did not differ from one another. The viewing times for the eyes, nose, and mouth of faces with closed eyes did not differ when faces with closed eyes were presented in either an upright or inverted orientation. These results suggest the possibility that open eyes play an important role in the configural processing of faces and that chimpanzees perceive and process open and closed eyes differently.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adachi I, Chou DP, Hampton RR (2009) Thatcher effect in monkeys demonstrates conservation of face perception across primates. Curr Biol 19:1270–1273

    Article  CAS  PubMed  Google Scholar 

  • Anastasi J, Rhodes MG (2005) An own-age bias in face recognition for children and older adults. Psychon Bull Rev 12:1043–1047

    PubMed  Google Scholar 

  • Bard K, Myowa-Yamokoshi M, Tomonaga M, Tanaka M, Costal A, Matsuzawa T (2005) Group differences in the mutual gaze of chimpanzees (Pan troglodytes). Dev Psychol 41:616–624

    Article  PubMed  Google Scholar 

  • Batki A, Baron-Cohen S, Wheelwright S, Connellan J, Ahluwalia J (2000) Is there an innate gaze module? Evidence from human neonates. Inf Behav Dev 23:223–229

    Article  Google Scholar 

  • Bruce C (1982) Face recognition by monkeys: absence of an inversion effect. Neuropsychologia 20:515–521

    Article  CAS  PubMed  Google Scholar 

  • Collishaw SM, Hole GJ (2000) Featural and configurational processes in the recognition of faces of different familiarity. Perception 29:893–909

    Article  CAS  PubMed  Google Scholar 

  • Dahl CD, Logothetis NK, Hoffman KL (2007) Individuation and holistic processing of faces in rhesus monkeys. Proc R Soc B 274:2069–2076

    Article  PubMed  Google Scholar 

  • Dahl CD, Wallraven C, Bülthoff HH, Logothetis NK (2009) Humans and macaques employ similar face-processing strategies. Curr Biol 19:509–513

    Article  CAS  PubMed  Google Scholar 

  • De Waal FBM (1982) Chimpanzee politics: power and sex among apes. Jonathan Cape, London

    Google Scholar 

  • De Waal FBM (1989) Peacemaking among primates. Harvard University Press, Cambridge

    Google Scholar 

  • Diamond R, Carey S (1986) Why faces are and are not special: an effect of expertise. J Exp Psychol 115:107–117

    CAS  Google Scholar 

  • Dittrich W (1990) Representation of faces in longtailed macaques (Macaca fascicularis). Ethology 85:265–278

    Article  Google Scholar 

  • Emery NJ (2000) The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci Biobehav Rev 24:581–604

    Article  CAS  PubMed  Google Scholar 

  • Farroni T, Csibra G, Simion F, Johnson MH (2002) Eye contact detection in humans from birth. Proc Natl Acad Sci USA 99:9602–9605

    Article  CAS  PubMed  Google Scholar 

  • Gallup GG, Nash RF, Ellison AL (1971) Tonic immobility as a reaction to predation: artificial eyes as a fear stimulus for chickens. Psychon Sci 23:79–80

    Google Scholar 

  • Goffaux V, Hault B, Michel C, Vuong QC, Rossion B (2005) The respective role of low and high spatial frequencies in supporting configural and featural processing of faces. Perception 34:77–86

    Article  PubMed  Google Scholar 

  • Gómez JC (1996) Non-human primate theories of (non-human primate) minds: some issues concerning the origins of mind-reading. In: Carruthers P, Smith PK (eds) Theories of theories of mind. Cambridge University Press, Cambridge, pp 330–343

    Google Scholar 

  • Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Harvard University Press, Cambridge

    Google Scholar 

  • Gothard KM, Erickson CA, Amaral DG (2004) How do rhesus monkeys (Macaca mulatta) scan faces in a visual paired comparison task? Anim Cogn 7(1):25–36

    Article  PubMed  Google Scholar 

  • Gothard KM, Brooks KN, Peterson MA (2009) Multiple perceptual strategies used by macaque monkeys for face recognition. Anim Cogn 12:155–167

    Article  PubMed  Google Scholar 

  • Guo K, Robertson RG, Mahmoodi S, Tadmor Y, Young MP (2003) How do monkeys view faces? A study of eye movements. Exp Brain Res 150:363–374

    PubMed  Google Scholar 

  • Hainline L (1978) Developmental changes in visual scanning of face and nonface patterns by infants. J Exp Child Psychol 25:90–115

    Article  CAS  PubMed  Google Scholar 

  • Hampton RR (1994) Sensitivity to information specifying the line of gaze of humans in sparrows (Passer domesticus). Behaviour 130:41–51

    Article  Google Scholar 

  • Hare B, Call J, Agnetta B, Tomasello M (2000) Chimpanzees know what conspecifics do and do not see. Anim Behav 59:771–785

    Article  PubMed  Google Scholar 

  • Hirata S, Fuwa K (2007) Chimpanzees (Pan troglodytes) learn to act with other individuals in a cooperative task. Primates 48:13–21

    Article  PubMed  Google Scholar 

  • Hirata S, Morimura N, Fuwa K (in press) Intentional communication and comprehension of the partner’s role in experimental cooperative tasks. In: Lonsdorf EV, Ross SR, Matsuzawa T (eds) The mind of the chimpanzees: ecological and experimental perspectives. The University of Chicago Press, Chicago

  • Jones RB (1980) Reactions of male domestic chickens to two-dimensional eye-like shapes. Anim Behav 28:212–218

    Article  Google Scholar 

  • Kaminski J, Call J, Tomasello M (2004) Body orientation and face orientation: two factors controlling apes’ begging behavior from humans. Anim Cogn 7:216–223

    Article  PubMed  Google Scholar 

  • Kano F, Tomonaga M (2009) How chimpanzees look at pictures: a comparative eye-tracking study. Proc R Soc B 276:1949–1955

    Article  PubMed  Google Scholar 

  • Kano F, Tomonaga M (in press) Face scanning in chimpanzees and humans: continuity and discontinuity. Anim Behav in press

  • Keating CF, Keating EG (1982) Visual scan patterns of rhesus monkeys viewing faces. Perception 11:211–219

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi H, Kohshima S (1997) Unique morphology of the human eye. Nature 6635:767–768

    Article  CAS  Google Scholar 

  • Martin-Malivel J, Fagot J (2001) Perception of pictorial human faces by baboons: effects of stimulus orientation on discrimination performance. Anim Learn Behav 29:10–20

    Google Scholar 

  • Maurer D, Le Grand R, Mondloch CJ (2002) The many faces of configural processing. Trends Cogn Sci 6:255–260

    Article  PubMed  Google Scholar 

  • Mondloch CJ, Le Grand R, Maurer D (2002) Configural face processing develops more slowly than featural processing. Perception 31:553–566

    Article  PubMed  Google Scholar 

  • Myowa-Yamakoshi M, Tomonaga M, Tanaka M, Matsuzawa T (2003) Preference for human direct gaze in infant chimpanzees (Pan troglodytes). Cognition 89:B53–B64

    Google Scholar 

  • Nahm FKD, Perret A, Amaral DG, Albright TD (1997) How do monkeys look at faces? J Cogn Neurosci 9:611–623

    Article  Google Scholar 

  • Parr LA, Dove T, Hopkins WD (1998) Why faces may be special: evidence of the inversion effect in chimpanzees. J Cogn Neurosci 10:615–622

    Article  CAS  PubMed  Google Scholar 

  • Parr LA, Winslow JT, Hopkins WD (1999) Is the inversion effect in rhesus monkeys face-specific? Anim Cogn 2:123–129

    Article  Google Scholar 

  • Povinelli DJ, Bering JM, Giambrone S (2000) Toward a science of other minds: escaping the argument by analogy. Cogn Sci 24:509–541

    Article  Google Scholar 

  • Redican WK (1975) Facial expressions in nonhuman primates. In: Rosenblum LA (ed) Primate behavior, vol 4. Academic Press, New York, pp 103–194

    Google Scholar 

  • Scaife M (1976a) The response to eye-like shapes by birds I: The effect of context, a predator and a strange bird. Anim Behav 24:195–199

    Article  Google Scholar 

  • Scaife M (1976b) The response to eye-like shapes by birds II: the importance of staring, pairedness and shape. Anim Behav 24:200–206

    Article  Google Scholar 

  • Senju A, Csibra G (2008) Gaze following in human infants depends on communicative signals. Curr Biol 18:668–671

    Article  CAS  PubMed  Google Scholar 

  • Tomasello M, Call J, Hare B (2003) Chimpanzees understand psychological states—the question is which ones and to what extent. Trends Cogn Sci 7:153–156

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Valentine T (1988) Upside-down faces: a review of the effects of inversion on face recognition. Br J Psychol 79:471–491

    PubMed  Google Scholar 

  • Weiss DJ, Kralik JD, Hauser MD (2001) Face processing in cotton-top tamarins (Saguinus oedipus). Anim Cogn 4:191–205

    Article  Google Scholar 

  • Yin RK (1969) Looking at upside down faces. J Exp Psychol 81:141–145

    Article  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the Ministry of Education, Culture, Sports, Science, and Technology of Japan (#20220004 and #20680015). We thank Kazuo Fujita, Shoji Itakura, and Masako Myowa-Yamakoshi for their support in conducting the experiment, Robert W. Shumaker for helpful comments on the manuscript, and the staff of the Great Ape Research Institute, Hayashibara Biochemical Laboratories, Inc. for support in conducting the experiment and for caring for the chimpanzees. All chimpanzees were cared for according to the Guide for the Care and Use of Laboratory Animals of Hayashibara Biochemical Laboratories, Inc. and the guidelines established by the Primate Society of Japan. The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Hayashibara Biochemical Laboratories, Inc., Great Ape Research Institute, 952-2 Nu, Tamano, Okayama, 706-0316, Japan

    Satoshi Hirata, Koki Fuwa, Keiko Sugama, Kiyo Kusunoki & Shin Fujita

Authors
  1. Satoshi Hirata
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Koki Fuwa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Keiko Sugama
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kiyo Kusunoki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shin Fujita
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Satoshi Hirata.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hirata, S., Fuwa, K., Sugama, K. et al. Facial perception of conspecifics: chimpanzees (Pan troglodytes) preferentially attend to proper orientation and open eyes. Anim Cogn 13, 679–688 (2010). https://doi.org/10.1007/s10071-010-0316-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-010-0316-y

Keywords

Search

Navigation