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Human ostensive signals do not enhance gaze following in chimpanzees, but do enhance object-oriented attention

Abstract

The previous studies have shown that human infants and domestic dogs follow the gaze of a human agent only when the agent has addressed them ostensively—e.g., by making eye contact, or calling their name. This evidence is interpreted as showing that they expect ostensive signals to precede referential information. The present study tested chimpanzees, one of the closest relatives to humans, in a series of eye-tracking experiments using an experimental design adapted from these previous studies. In the ostension conditions, a human actor made eye contact, called the participant’s name, and then looked at one of two objects. In the control conditions, a salient cue, which differed in each experiment (a colorful object, the actor’s nodding, or an eating action), attracted participants’ attention to the actor’s face, and then the actor looked at the object. Overall, chimpanzees followed the actor’s gaze to the cued object in both ostension and control conditions, and the ostensive signals did not enhance gaze following more than the control attention-getters. However, the ostensive signals enhanced subsequent attention to both target and distractor objects (but not to the actor’s face) more strongly than the control attention-getters—especially in the chimpanzees who had a close relationship with human caregivers. We interpret this as showing that chimpanzees have a simple form of communicative expectations on the basis of ostensive signals, but unlike human infants and dogs, they do not subsequently use the experimenter’s gaze to infer the intended referent. These results may reflect a limitation of non-domesticated species for interpreting humans’ ostensive signals in inter-species communication.

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References

  1. Behne T, Carpenter M, Tomasello M (2005) One-year-olds comprehend the communicative intentions behind gestures in a hiding game. Dev Sci 8:492–499. https://doi.org/10.1111/j.1467-7687.2005.00440.x

    Article  PubMed  Google Scholar 

  2. Behne T, Liszkowski U, Carpenter M, Tomasello M (2012) Twelve-month-olds’ comprehension and production of pointing. Br J Dev Psychol 30:359–375. https://doi.org/10.1111/j.2044-835X.2011.02043.x

    Article  PubMed  Google Scholar 

  3. Bräuer J, Call J, Tomasello M (2005) All great ape species follow gaze to distant locations and around barriers. J Comp Psychol 119:145–154. https://doi.org/10.1037/0735-7036.119.2.145

    Article  PubMed  Google Scholar 

  4. Bugnyar T, Stöwe M, Heinrich B (2004) Ravens, Corvus corax, follow gaze direction of humans around obstacles. Proc R Soc Lond Ser B Biol Sci 271:1331–1336. https://doi.org/10.1098/rspb.2004.2738

    Article  Google Scholar 

  5. Call J, Tomasello M (1994) Production and comprehension of referential pointing by orangutans (Pongo pygmaeus). J Comp Psychol 108:307. https://doi.org/10.1037//0735-7036.108.4.307

    Article  PubMed  CAS  Google Scholar 

  6. Call J, Tomasello M (1996) The effect of humans on the cognitive development of apes. In: Russon AE, Bard KA, Parker ST (eds) Reaching into thought: the minds of the great apes. Cambridge University Press, New York, pp 371–403

    Google Scholar 

  7. Call J, Tomasello M (2008) Does the chimpanzee have a theory of mind? 30 years later. Trends Cogn Sci 12:187–192. https://doi.org/10.1016/j.tics.2008.02.010

    Article  PubMed  Google Scholar 

  8. Call J, Agnetta B, Tomasello M (2000) Cues that chimpanzees do and do not use to find hidden objects. Anim Cogn 3:23–34. https://doi.org/10.1007/s100710050047

    Article  Google Scholar 

  9. Cooper RP, Aslin RN (1990) Preference for infant directed speech in the first month after birth. Child Dev 61:1584–1595. https://doi.org/10.1111/j.1467-8624.1990.tb02885.x

    Article  PubMed  CAS  Google Scholar 

  10. Csibra G (2010) Recognizing communicative intentions in infancy. Mind Lang 25:141–168. https://doi.org/10.1111/j.1468-0017.2009.01384.x

    Article  Google Scholar 

  11. Csibra G, Gergely G (2009) Natural pedagogy. Trends Cogn Sci 13:148–153. https://doi.org/10.1016/j.tics.2009.01.005

    Article  PubMed  Google Scholar 

  12. De Waal FB (1988) The communicative repertoire of captive bonobos (Pan paniscus), compared to that of chimpanzees. Behaviour 106:183–251. https://doi.org/10.1163/156853988X00269

    Article  Google Scholar 

  13. De Waal FBM (1990) Peacemaking among primates. Harvard University Press, Cambridge

    Google Scholar 

  14. Emery NJ (2000) The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci Biobehav Rev 24:581–604. https://doi.org/10.1016/S0149-7634(00)00025-7

    Article  PubMed  CAS  Google Scholar 

  15. Farroni T, Csibra G, Simion F, Johnson MH (2002) Eye contact detection in humans from birth. Proc Nat Acad Sci 99:9602. https://doi.org/10.1073/pnas.152159999

    Article  PubMed  CAS  Google Scholar 

  16. Gergely G, Csibra G (2006) Sylvia’s recipe: the role of imitation and pedagogy in the transmission of cultural knowledge. In: Enfield N, Levenson SC (eds) Roots of human sociality: culture, cognition, and human interaction. Berg, Oxford, pp 229–255

    Google Scholar 

  17. Gergely G, Egyed K, Király I (2007) On pedagogy. Dev Sci 10:139–146. https://doi.org/10.1111/j.1467-7687.2007.00576.x

    Article  PubMed  Google Scholar 

  18. Gomez JC (1996) Ostensive behavior in great apes: the role of eye contact. In: Russon AE, Bard KA, Parker ST (eds) Reaching into thought: the minds of the great apes. Cambridge University Press, New York, pp 131–151

    Google Scholar 

  19. Gredebäck G, Astor K, Fawcett C (2018) Gaze following is not dependent on ostensive cues: a critical test of natural pedagogy. Child dev. https://doi.org/10.1111/cdev.13026 (in press)

    PubMed  Article  Google Scholar 

  20. Hare B, Tomasello M (1999) Domestic dogs (Canis familiaris) use human and conspecific social cues to locate hidden food. J Comp Psychol 113:173. https://doi.org/10.1037//0735-7036.113.2.173

    Article  Google Scholar 

  21. Hare B, Tomasello M (2004) Chimpanzees are more skilful in competitive than in cooperative cognitive tasks. Anim Behav 68:571–581. https://doi.org/10.1016/j.anbehav.2003.11.011

    Article  Google Scholar 

  22. Hare B, Brown M, Williamson C, Tomasello M (2002) The domestication of social cognition in dogs. Science 298:1634–1636. https://doi.org/10.1126/science.1072702

    Article  PubMed  CAS  Google Scholar 

  23. Hattori Y, Kano F, Tomonaga M (2010) Differential sensitivity to conspecific and allospecific cues in chimpanzees and humans: a comparative eye-tracking study. Biology Lett 6:610–613. https://doi.org/10.1098/rsbl.2010.0120

    Article  Google Scholar 

  24. Herrmann E, Tomasello M (2006) Apes’ and children’s understanding of cooperative and competitive motives in a communicative situation. Dev Sci 9:518–529. https://doi.org/10.1111/j.1467-7687.2006.00519.x

    Article  PubMed  Google Scholar 

  25. Heyes C (2016) Born pupils? Natural pedagogy and cultural pedagogy. Perspect Psychol Sci 11:280–295. https://doi.org/10.1177/1745691615621276

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  27. Hoicka E (2016) Parents and toddlers distinguish joke, pretend and literal intentional contexts through communicative and referential cues. J Pragmat 95:137–155. https://doi.org/10.1016/j.pragma.2015.10.010

    Article  Google Scholar 

  28. Kaminski J, Schulz L, Tomasello M (2012) How dogs know when communication is intended for them. Dev Sci 15:222–232. https://doi.org/10.1111/j.1467-7687.2011.01120.x

    Article  PubMed  Google Scholar 

  29. Kano F, Call J (2014a) Cross-species variation of gaze following and conspecific preference among great apes human infants adults. Anim Behav 91:137–150. https://doi.org/10.1016/j.anbehav.2014.03.011

    Article  Google Scholar 

  30. Kano F, Call J (2014b) Great apes generate goal-based action predictions: an eye-tracking study. Psychol Sci 25:1691–1698. https://doi.org/10.1177/0956797614536402

    Article  PubMed  Google Scholar 

  31. Kano F, Tomonaga M (2009) How chimpanzees look at pictures: a comparative eye-tracking study. Proc Roy Soc B 276:1949–1955. https://doi.org/10.1098/rspb.2008.1811

    Article  Google Scholar 

  32. Kano F, Hirata S, Call J, Tomonaga M (2011) The visual strategy specific to humans among hominids: a study using the gap-overlap paradigm. Vis Res 51:2348–2355. https://doi.org/10.1016/j.visres.2011.09.006

    Article  PubMed  Google Scholar 

  33. Kano F, Call J, Tomonaga M (2012) Face and eye scanning in gorillas, orangutans, and humans: unique eye-viewing patterns in humans among hominids. J Comp Psychol 126:388–398. https://doi.org/10.1037/a0029615

    Article  PubMed  Google Scholar 

  34. Kano F, Hirata S, Call J (2015) Social attention in Pan: bonobos exhibit more eye contacts than chimpanzees. PLoS One 10:e0129684. https://doi.org/10.1371/journal.pone.0129684

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Kano F, Krupenye C, Hirata S, Call J (2017) Eye tracking uncovered great apes’ ability to anticipate that other individuals will act according to false beliefs. Commun Integr Biol 10:e1299836. https://doi.org/10.1080/19420889.2017.1299836

    Article  PubMed  PubMed Central  Google Scholar 

  36. Kano F, Shepherd SV, Hirata S, Call J (2018) Primate social attention: species differences and effects of individual experience in humans, great apes, and macaques. PLoS One 13:e0193283. https://doi.org/10.1371/journal.pone.0193283

    Article  PubMed  PubMed Central  Google Scholar 

  37. Krupenye C, Kano F, Hirata S, Call J, Tomasello M (2016) Great apes anticipate that other individuals will act according to false beliefs. Science 354:110–114. https://doi.org/10.1126/science.aaf8110

    Article  PubMed  CAS  Google Scholar 

  38. Liebal K, Call J (2012) The origins of non-human primates’ manual gestures. Philos Trans R Soc Lond B Biol Sci 367:118–128. https://doi.org/10.1098/rstb.2011.0044

    Article  PubMed  PubMed Central  Google Scholar 

  39. Lyn H, Russell JL, Hopkins WD (2010) The impact of environment on the comprehension of declarative communication in apes. Psychol Sci 21:360–365. https://doi.org/10.1177/0956797610362218

    Article  PubMed  Google Scholar 

  40. Miklósi Á, Polgárdi R, Topál J, Csányi V (1998) Use of experimenter-given cues in dogs. Anim Cogn 1:113–121. https://doi.org/10.1007/s100710050016

    Article  PubMed  Google Scholar 

  41. Moore R (2016) Meaning and ostension in great ape gestural communication. Anim Cogn 19:223–231. https://doi.org/10.1007/s10071-015-0905-x

    Article  PubMed  Google Scholar 

  42. Moore R (2017) Gricean communication and cognitive development. Philos Q 67:303–326. https://doi.org/10.1093/pq/pqw049

    Article  Google Scholar 

  43. Moore R, Liebal K, Tomasello M (2013) Three-year-olds understand communicative intentions without language, gestures or gaze. Interact Stud 14:62–80. https://doi.org/10.1075/is.14.1.05moo

    Article  Google Scholar 

  44. Moore R, Call J, Tomasello M (2015a) Production and comprehension of gestures between orang-utans (Pongo pygmaeus) in a referential communication game. PloS One 10:e0129726. https://doi.org/10.1371/journal.pone.0129726

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Moore R, Mueller B, Kaminski J, Tomasello M (2015b) Two-year-old children but not domestic dogs understand communicative intentions without language, gestures or gaze. Dev Sci 18:232–242. https://doi.org/10.1111/desc.12206

    Article  PubMed  Google Scholar 

  46. Myowa-Yamakoshi M, Tomonaga M, Tanaka M, Matsuzawa T (2003) Preference for human direct gaze in infant chimpanzees (Pan troglodytes). Cognition 89:113–124. https://doi.org/10.1016/S0010-0277(03)00071-4

    Article  Google Scholar 

  47. Okamoto-Barth S, Call J, Tomasello M (2007) Great apes’ understanding of other individuals’ line of sight. Psychol Sci 18:462–468. https://doi.org/10.1111/j.1467-9280.2007.01922.x

    Article  PubMed  Google Scholar 

  48. 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. https://doi.org/10.1162/089892998563013

    Article  PubMed  CAS  Google Scholar 

  49. Riedel J, Schumann K, Kaminski J, Call J, Tomasello M (2008) The early ontogeny of human–dog communication. Anim Behav 75:1003–1014. https://doi.org/10.1016/j.anbehav.2007.08.010

    Article  Google Scholar 

  50. Scott-Phillips TC (2015a) Meaning in animal and human communication. Anim Cogn 18:801–805. https://doi.org/10.1007/s10071-015-0845-5

    Article  PubMed  Google Scholar 

  51. Scott-Phillips TC (2015b) Nonhuman primate communication, pragmatics, and the origins of language. Curr Anthropol 56:56–80. https://doi.org/10.1086/679674

    Article  Google Scholar 

  52. Senju A, Csibra G (2008) Gaze following in human infants depends on communicative signals. Curr Biol 18:668–671. https://doi.org/10.1016/j.cub.2008.03.059

    Article  PubMed  CAS  Google Scholar 

  53. Senju A, Csibra G (2014) A commentary by Csibra, Senju, et al. on gaze following. http://cognitionandculture.net/blog/icci-blog/for-the-record-a-commentary-by-csibra-senju-et-al-on-gaze-following. Retrieved 1 Jul 2018

  54. Sperber D, Wilson D (1995) Relevance: communication and cognition, 2nd edn. Blackwell, Oxford

    Google Scholar 

  55. Szufnarowska J, Rohlfing KJ, Fawcett C, Gredebäck G (2014) Is ostension any more than attention? Sci Rep 4:5304. https://doi.org/10.1038/srep05304

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Téglás E, Gergely A, Kupán K, Miklósi Á, Topál J (2012) Dogs’ gaze following is tuned to human communicative signals. Curr Biol 22:209–212. https://doi.org/10.1016/j.cub.2011.12.018

    Article  PubMed  CAS  Google Scholar 

  57. Tennie C, Call J, Tomasello M (2009) Ratcheting up the ratchet: on the evolution of cumulative culture. Philos Trans R Soc B Biol Sci 364:2405–2415. https://doi.org/10.1098/rstb.2009.0052

    Article  Google Scholar 

  58. Tomasello M (1999) The cultural origins of human cognition. Harvard University Press, Cambridge

    Google Scholar 

  59. Tomasello M (2006) Why don’t apes point? In: Enfield N, Levinson SC (eds) Roots of human sociality: culture, cognition, and interaction, vol 197. Berg, London, pp 506–524

    Google Scholar 

  60. Tomasello M, Hare B, Lehmann H, Call J (2007) Reliance on head versus eyes in the gaze following of great apes and human infants: the cooperative eye hypothesis. J Hum Evol 52:314–320. https://doi.org/10.1016/j.jhevol.2006.10.001

    Article  PubMed  Google Scholar 

  61. Tomonaga M (1999) Inversion effect in perception of human faces in a chimpanzee (Pan troglodytes). Primates 40:417–438. https://doi.org/10.1007/BF02557579

    Article  Google Scholar 

  62. Topál J, Gergely G, Erdőhegyi Á, Csibra G, Miklósi Á (2009) Differential sensitivity to human communication in dogs wolves human infants. Science 325:1269–1272. https://doi.org/10.1126/science.1176960

    Article  PubMed  CAS  Google Scholar 

  63. Topál J, Kis A, Oláh K (2014) Dogs’ sensitivity to human ostensive cues: a unique adaptation. In: Kaminski J, Marshall-Pescini S (eds) The social dog: behavior and cognition. Elsevier, New York, pp 319–346

  64. Ueno A et al (2010) Brain activity in an awake chimpanzee in response to the sound of her own name. Biol Lett 6:311–313. https://doi.org/10.1098/rsbl.2009.0864

    Article  PubMed  Google Scholar 

  65. Virányi Z, Gácsi M, Kubinyi E, Topál J, Belényi B, Ujfalussy D, Miklósi Á (2008) Comprehension of human pointing gestures in young human-reared wolves (Canis lupus) and dogs (Canis familiaris). Anim Cogn 11:373. https://doi.org/10.1007/s10071-007-0127-y

    Article  PubMed  Google Scholar 

  66. Vorms M (2012) A-not-B errors: testing the limits of natural pedagogy theory. Rev Philos Psychol 3:525–545. https://doi.org/10.1007/s13164-012-0113-4

    Article  Google Scholar 

  67. Whiten A, McGuigan N, Marshall-Pescini S, Hopper LM (2009) Emulation, imitation, over-imitation and the scope of culture for child and chimpanzee. Philos Trans R Soc Lond B Biol Sci 364:2417–2428. https://doi.org/10.1016/j.anbehav.2007.08.010

    Article  PubMed  PubMed Central  Google Scholar 

  68. Yamagiwa J (1992) Functioinal analysis of social staring behavior in an all-male group of mountain gorillas. Primates 33:523–544. https://doi.org/10.1007/BF02381153

    Article  Google Scholar 

  69. Yamamoto S, Humle T, Tanaka M (2012) Chimpanzees’ flexible targeted helping based on an understanding of conspecifics’ goals. Proc Natl Acad Sci 109:3588–3592. https://doi.org/10.1073/pnas.1108517109

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank Naruki Morimura, Yutaro Sato, Ruiting Song and the staff at Kumamoto Sanctuary, Primate Research Institute, Kyoto University Institute for Advanced Study, and Wolfgang Kohler Primate Research Center for their assistance in conducting the series of experiments. We also thank two anonymous reviewers for their helpful comments. Financial support came from Ministry of Education, Culture, Sports, Science and Technology [K-CONNEX to FK], Japan Society for Promotion of Science KAKENHI 26885040, 16K21108, and 18H05072 to FK, 26245069, 16H06301, 16H06283, and 18H05524 to SH, 15H05709, 16H06238, and JSPS-CCSN to MT, and JSPS-LGP-U04 and Great Ape Information Network to SH and MT, and the European Research Council [SOMICS 609819 to JC].

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Correspondence to Fumihiro Kano.

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Kano, F., Moore, R., Krupenye, C. et al. Human ostensive signals do not enhance gaze following in chimpanzees, but do enhance object-oriented attention. Anim Cogn 21, 715–728 (2018). https://doi.org/10.1007/s10071-018-1205-z

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Keywords

  • Domestication
  • Gaze following
  • Great ape
  • Ostensive signals
  • Referential communication