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Flexible gaze-following in rhesus monkeys

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Abstract

Humans are characterized by complex social cognitive abilities that emerge early in development. Comparative studies of nonhuman primates can illuminate the evolutionary history of these social capacities. We examined the cognitive skills that rhesus monkeys (Macaca mulatta) use to follow gaze, a foundational skill in human social development. While rhesus monkeys can make inferences about others’ gaze when competing, it is unclear how they think about gaze information in other contexts. In study 1, monkeys (n = 64) observed a demonstrator look upwards either in a barrier condition where a box was overhead, so that monkeys could not see the target of her gaze, or a no barrier condition where nothing blocked her view. In study 2, monkeys (n = 59) could approach to observe the target of the demonstrator’s gaze when the demonstrator looked behind a barrier on the ground or, in the no barrier condition, behind a window frame in the same location. Monkeys were more likely to directly look up in study 1 if they could initially see the location where the demonstrator was looking, but they did not preferentially reorient their bodies to observe the out-of-view location when they could not see that location. In study 2, monkeys did preferentially reorient, but at low rates. This indicates that rhesus monkeys can use social cognitive processes outside of competitive contexts to model what others can or cannot see, but may not be especially motivated to see what others look at in non-competitive contexts, as they reorient infrequently or in an inconsistent fashion. These similarities and differences between gaze-following in monkeys and children can help to illuminate the evolution of human social cognition.

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References

  • Anderson JR, Sallaberry P, Barbier H (1995) Use of experimenter-given cues during object-choice tasks by capuchin monkeys. Anim Behav 49(1):201–208

    Article  Google Scholar 

  • Anderson JR, Montant M, Schmitt D (1996) Rhesus monkeys fail to use gaze direction as an experimenter-given cue in an object-choice task. Behav Proc 37(1):47–55

    Article  CAS  Google Scholar 

  • Baayen RH, Milin P (2010) Analyzing reaction times. Int J Psychol Res 3(2):12–28

    Article  Google Scholar 

  • Baldwin DA, Moses LJ (1994) Early understanding of referential intent and attentional focus: evidence from language and emotion. In: Lewis C, Mitchell P (eds) Children’s early understanding of mind: origins and development. Lawrence Erlbaum Associates Inc, Hillsdale, NJ, pp 133–156

    Google Scholar 

  • Bettle R, Rosati AG (2016) Understanding human gaze. In: Encyclopedia of evolutionary psychological science, pp 1–4

  • Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24(3):127–135

    Article  Google Scholar 

  • Bräuer J, Call J, Tomasello M (2005) All great ape species follow gaze to distant locations and around barriers. J Comp Psychol 119(2):145–154

    Article  PubMed  Google Scholar 

  • Bray J, Krupenye C, Hare B (2014) Ring-tailed lemurs (Lemur catta) exploit information about what others can see but not what they can hear. Anim Cogn 17(3):735–744

    Article  PubMed  Google Scholar 

  • Brent LJ, Heilbronner SR, Horvath JE, Gonzalez-Martinez J, Ruiz-Lambides A, Robinson AG, Platt ML (2013) Genetic origins of social networks in rhesus macaques. Sci Rep 3:1042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brooks R, Meltzoff AN (2005) The development of gaze following and its relation to language. Dev Sci 8(6):535–543

    Article  PubMed  PubMed Central  Google Scholar 

  • Bulloch MJ, Boysen ST, Furlong EE (2008) Visual attention and its relation to knowledge states in chimpanzees, Pan troglodytes. Anim Behav 76(4):1147–1155

    Article  Google Scholar 

  • Burkart JM, Hrdy SB, Van Schaik CP (2009) Cooperative breeding and human cognitive evolution. Evol Anthropol Issues News Rev Issues News Rev 18(5):175–186

    Article  Google Scholar 

  • Butler SC, Caron AJ, Brooks R (2000) Infant understanding of the referential nature of looking. J Cogn Dev 1(4):359–377

    Article  Google Scholar 

  • Butterworth G, Cochran E (1980) Towards a mechanism of joint visual attention in human infancy. Int J Behav Dev 3(3):253–272

    Article  Google Scholar 

  • Butterworth G, Jarrett N (1991) What minds have in common is space: spatial mechanisms serving joint visual attention in infancy. Br J Dev Psychol 9(1):55–72

    Article  Google Scholar 

  • Byrne R, Whiten A (1989) Machiavellian intelligence: social expertise and the evolution of intellect in monkeys, apes, and humans. Oxford Science Publications, Oxford

    Google Scholar 

  • Call J, Hare BA, Tomasello M (1998) Chimpanzee gaze following in an object-choice task. Anim Cogn 1(2):89–99

    Article  CAS  PubMed  Google Scholar 

  • Call J, Agnetta B, Tomasello M (2000) Cues that chimpanzees do and do not use to find hidden objects. Anim Cogn 3(1):23–34

    Article  Google Scholar 

  • Call J, Hare B, Carpenter M, Tomasello M (2004) ‘Unwilling’ versus ‘unable’: chimpanzees’ understanding of human intentional action. Dev Sci 7(4):488–498

    Article  PubMed  Google Scholar 

  • Cheney DL (2011) Extent and limits of cooperation in animals. Proc Natl Acad Sci 108(Supplement 2):10902–10909

    Article  PubMed  Google Scholar 

  • Crockford C, Wittig RM, Mundry R, Zuberbühler K (2012) Wild chimpanzees inform ignorant group members of danger. Curr Biol 22(2):142–146

    Article  CAS  PubMed  Google Scholar 

  • Csibra G, Gergely G (2009) Natural pedagogy. Trends Cogn Sci 13(4):148–153

    Article  PubMed  Google Scholar 

  • Davidson GL, Butler S, Fernández-Juricic E, Thornton A, Clayton NS (2014) Gaze sensitivity: function and mechanisms from sensory and cognitive perspectives. Anim Behav 87:3–15

    Article  Google Scholar 

  • Deaner RO, Platt ML (2003) Reflexive social attention in monkeys and humans. Curr Biol 13(18):1609–1613

    Article  CAS  PubMed  Google Scholar 

  • Drayton LA, Santos LR (2016) A decade of theory of mind research on Cayo Santiago: insights into rhesus macaque social cognition. Am J Primatol 78(1):106–116

    Article  PubMed  Google Scholar 

  • Drayton LA, Santos LR (2017) Do rhesus macaques, Macaca mulatta, understand what others know when gaze following? Anim Behav 134:193–199

    Article  Google Scholar 

  • Emery NJ, Lorincz EN, Perrett DI, Oram MW, Baker CI (1997) Gaze following and joint attention in rhesus monkeys (Macaca mulatta). J Comp Psychol 111(3):286–293

    Article  CAS  PubMed  Google Scholar 

  • Ferrari P, Kohler E, Fogassi L, Gallese V (2000) The ability to follow eye gaze and its emergence during development in macaque monkeys. Proc Natl Acad Sci 97(25):13997–14002

    Article  CAS  PubMed  Google Scholar 

  • Flom R, Lee K, Muir D (2017) Gaze-following: Its development and significance. Psychology Press, London

    Google Scholar 

  • Flombaum JI, Santos LR (2005) Rhesus monkeys attribute perceptions to others. Curr Biol 15(5):447–452

    Article  CAS  PubMed  Google Scholar 

  • Friesen CK, Kingstone A (1998) The eyes have it! Reflexive orienting is triggered by nonpredictive gaze. Psychon Bull Rev 5(3):490–495

    Article  Google Scholar 

  • Goossens BM, Dekleva M, Reader SM, Sterck EH, Bolhuis JJ (2008) Gaze following in monkeys is modulated by observed facial expressions. Anim Behav 75(5):1673–1681

    Article  Google Scholar 

  • Grueneisen S, Duguid S, Saur H, Tomasello M (2017) Children, chimpanzees, and bonobos adjust the visibility of their actions for cooperators and competitors. Sci Rep 7(1):8504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hare B (2001) Can competitive paradigms increase the validity of experiments on primate social cognition? Anim Cogn 4(3):269–280

    Article  CAS  PubMed  Google Scholar 

  • Hare B (2017) Survival of the friendliest: homo sapiens evolved via selection for prosociality. Annu Rev Psychol 68:155–186

    Article  PubMed  Google Scholar 

  • Hare B, Tomasello M (2004) Chimpanzees are more skilful in competitive than in cooperative cognitive tasks. Anim Behav 68(3):571–581

    Article  Google Scholar 

  • Hare B, Tomasello M (2005) Human-like social skills in dogs? Trends Cogn Sci 9(9):439–444

    Article  PubMed  Google Scholar 

  • Hare B, Call J, Agnetta B, Tomasello M (2000) Chimpanzees know what conspecifics do and do not see. Anim Behav 59(4):771–785

    Article  CAS  PubMed  Google Scholar 

  • Hare B, Call J, Tomasello M (2001) Do chimpanzees know what conspecifics know? Anim Behav 61(1):139–151

    Article  PubMed  Google Scholar 

  • Hare B, Call J, Tomasello M (2006) Chimpanzees deceive a human competitor by hiding. Cognition 101(3):495–514

    Article  PubMed  Google Scholar 

  • Higham JP, Maestripieri D (2010) Revolutionary coalitions in male rhesus macaques. Behaviour 147(13):1889–1908

    Google Scholar 

  • Hood BM, Willen JD, Driver J (1998) Adult’s eyes trigger shifts of visual attention in human infants. Psychol Sci 9(2):131–134

    Article  Google Scholar 

  • Hopkins WD, Taglialatela JP, Leavens DA (2007) Chimpanzees differentially produce novel vocalizations to capture the attention of a human. Anim Behav 73(2):281–286

    Article  PubMed  PubMed Central  Google Scholar 

  • Hostetter AB, Russell JL, Freeman H, Hopkins WD (2007) Now you see me, now you don’t: evidence that chimpanzees understand the role of the eyes in attention. Anim Cogn 10(1):55–62

    Article  PubMed  Google Scholar 

  • Itakura S (1996) An exploratory study of gaze-monitoring in nonhuman primates. Jpn Psychol Res 38(3):174–180

    Article  Google Scholar 

  • Itakura S, Tanaka M (1998) Use of experimenter-given cues during object-choice tasks by chimpanzees (Pan troglodytes), an orangutan (Pongo pygmaeus), and human infants (Homo sapiens). J Comp Psychol 112(2):119–126

    Article  CAS  PubMed  Google Scholar 

  • Joly M, Micheletta J, De Marco A, Langermans JA, Sterck EH, Waller BM (2017) Comparing physical and social cognitive skills in macaque species with different degrees of social tolerance. Proc R Soc B 284(1862):20162738

    Article  PubMed  Google Scholar 

  • Kaminski J, Call J, Tomasello M (2008) Chimpanzees know what others know, but not what they believe. Cognition 109(2):224–234

    Article  PubMed  Google Scholar 

  • 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(6308):110–114

    Article  CAS  PubMed  Google Scholar 

  • Lee K, Eskritt M, Symons LA, Muir D (1998) Children’s use of triadic eye gaze information for “mind reading”. Dev Psychol 34(3):525–539

    Article  CAS  PubMed  Google Scholar 

  • Lindburg DG (1971) The rhesus monkey in North India: an ecological and behavioral study. Primate Behav Dev Field Lab Res 2:1–106

    Google Scholar 

  • Lo S, Andrews S (2015) To transform or not to transform: using generalized linear mixed models to analyse reaction time data. Front Psychol 6:1171

    Article  PubMed  PubMed Central  Google Scholar 

  • Lyons DE, Santos LR (2006) Ecology, domain specificity, and the origins of theory of mind: is competition the catalyst? Philos Compass 1(5):481–492

    Article  Google Scholar 

  • MacLean EL, Hare B (2012) Bonobos and chimpanzees infer the target of another’s attention. Anim Behav 83(2):345–353

    Article  Google Scholar 

  • MacLean EL, Hare B, Nunn CL, Addessi E, Amici F, Anderson RC, Barnard AM (2014) The evolution of self-control. Proc Natl Acad Sci 111(20):E2140–E2148

    Article  CAS  PubMed  Google Scholar 

  • Marticorena DC, Ruiz AM, Mukerji C, Goddu A, Santos LR (2011) Monkeys represent others’ knowledge but not their beliefs. Dev Sci 14(6):1406–1416

    Article  PubMed  PubMed Central  Google Scholar 

  • Martin A, Santos LR (2014) The origins of belief representation: monkeys fail to automatically represent others’ beliefs. Cognition 130(3):300–308

    Article  PubMed  Google Scholar 

  • Martin A, Santos LR (2016) What cognitive representations support primate theory of mind? Trends Cogn Sci 20(5):375–382

    Article  PubMed  Google Scholar 

  • Melis AP, Tomasello M (2013) Chimpanzees’ (Pan troglodytes) strategic helping in a collaborative task. Biol Lett 9(2):20130009

    Article  PubMed  PubMed Central  Google Scholar 

  • Melis AP, Call J, Tomasello M (2006) Chimpanzees (Pan troglodytes) conceal visual and auditory information from others. J Comp Psychol 120(2):154–162

    Article  PubMed  Google Scholar 

  • Micheletta J, Waller BM (2012) Friendship affects gaze following in a tolerant species of macaque, Macaca nigra. Anim Behav 83(2):459–467

    Article  Google Scholar 

  • Moll H, Meltzoff AN (2011) Joint attention as the fundamental basis of understanding perspectives. In: Seemann A (ed) Joint attention: new developments in psychology, philosophy of mind, and social neuroscience. MIT Press, Cambridge, MA, pp 393–413

    Google Scholar 

  • Moll H, Tomasello M (2004) 12-and 18-month-old infants follow gaze to spaces behind barriers. Dev Sci 7(1):F1–F9

    Article  PubMed  Google Scholar 

  • Moll H, Tomasello M (2007) How 14-and 18-month-olds know what others have experienced. Dev Psychol 43(2):309–317

    Article  PubMed  Google Scholar 

  • Morales M, Mundy P, Rojas J (1998) Following the direction of gaze and language development in 6-month-olds. Infant Behav Dev 21(2):373–377

    Article  Google Scholar 

  • Okamoto-Barth S, Call J, Tomasello M (2007) Great apes’ understanding of other individuals’ line of sight. Psychol Sci 18(5):462–468

    Article  PubMed  Google Scholar 

  • Partan SR (2002) Single and multichannel signal composition: facial expressions and vocalizations of rhesus macaques (Macaca mulatta). Behaviour 139(8):993–1027

    Article  Google Scholar 

  • Petit O, Desportes C, Thierry B (1992) Differential probability of “coproduction” in two species of macaque (Macaca tonkeana, M. mulatta). Ethology 90(2):107–120

    Article  Google Scholar 

  • Rawlins RC, Kessler MJ (eds) (1987) The Cayo Santiago macaques: history, behavior and biology. State University of New York Press, Albany

    Google Scholar 

  • R Development Core Team (2017) A language and environment for statistical computing, Vienna, Austria. http://www.R-project.org. Accessed 9 Oct 2017

  • Ricciardelli P, Carcagno S, Vallar G, Bricolo E (2013) Is gaze following purely reflexive or goal-directed instead? Revisiting the automaticity of orienting attention by gaze cues. Exp Brain Res 224(1):93–106

    Article  PubMed  Google Scholar 

  • Rosati AG, Hare B (2009) Looking past the model species: diversity in gaze-following skills across primates. Curr Opin Neurobiol 19(1):45–51

    Article  CAS  PubMed  Google Scholar 

  • Rosati AG, Santos LR (2016) Spontaneous metacognition in rhesus monkeys. Psychol Sci 27(9):1181–1191

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosati AG, Santos LR (2017) Tolerant Barbary macaques maintain juvenile levels of social attention in old age, but despotic rhesus macaques do not. Anim Behav 130:199–207

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosati AG, Wobber V, Hughes K, Santos LR (2014) Comparative developmental psychology: how is human cognitive development unique? Evol Psychol 12(2):448–473

    Article  PubMed  Google Scholar 

  • Rosati AG, Arre AM, Platt ML, Santos LR (2016) Rhesus monkeys show human-like changes in gaze following across the lifespan. Proc R Soc B 283:20160376

    Article  CAS  PubMed  Google Scholar 

  • Ruiz A, Gómez JC, Roeder JJ, Byrne RW (2009) Gaze following and gaze priming in lemurs. Anim Cogn 12(3):427–434

    Article  PubMed  Google Scholar 

  • Sandel AA, MacLean EL, Hare B (2011) Evidence from four lemur species that ringtailed lemur social cognition converges with that of haplorhine primates. Anim Behav 81(5):925–931

    Article  Google Scholar 

  • Santos LR, Nissen AG, Ferrugia JA (2006) Rhesus monkeys, Macaca mulatta, know what others can and cannot hear. Anim Behav 71(5):1175–1181

    Article  Google Scholar 

  • Senju A, Csibra G (2008) Gaze following in human infants depends on communicative signals. Curr Biol 18(9):668–671

    Article  CAS  PubMed  Google Scholar 

  • Shepherd SV (2010) Following gaze: gaze-following behavior as a window into social cognition. Front Integr Neurosci 4:5

    PubMed  PubMed Central  Google Scholar 

  • Shepherd SV, Deaner RO, Platt ML (2006) Social status gates social attention in monkeys. Curr Biol 16(4):R119–R120

    Article  CAS  PubMed  Google Scholar 

  • Teufel C, Alexis DM, Clayton NS, Davis G (2010) Mental-state attribution drives rapid, reflexive gaze following. Attent Percept Psychophys 72(3):695–705

    Article  Google Scholar 

  • Thierry B (2002) Covariation of conflict management patterns across macaque species. In: Aureli F, de Waal FBM (eds) Natural conflict resolution. University of California Press, Berkeley, pp 106–128

    Google Scholar 

  • Tomasello M (1995) Joint attention as social cognition. In: Moore C, Dunham PJ (eds) Joint attention: its origins and role in development. Lawrence Erlbaum Associates Inc, Hillsdale, NJ, pp 103–130

    Google Scholar 

  • Tomasello M (2014) A natural history of human thinking. Harvard University Press, Cambridge

    Book  Google Scholar 

  • Tomasello M, Carpenter M (2007) Shared intentionality. Dev Sci 10(1):121–125

    Article  PubMed  Google Scholar 

  • Tomasello M, Hare B, Agnetta B (1999) Chimpanzees, Pan troglodytes, follow gaze direction geometrically. Anim Behav 58(4):769–777

    Article  CAS  PubMed  Google Scholar 

  • Tomasello M, Hare B, Fogleman T (2001) The ontogeny of gaze following in chimpanzees, Pan troglodytes, and rhesus macaques, Macaca mulatta. Anim Behav 61(2):335–343

    Article  Google Scholar 

  • Vick S-J, Anderson JR (2000) Learning and limits of use of eye gaze by capuchin monkeys (Cebus apella) in an object-choice task. J Comp Psychol 114(2):200–207

    Article  CAS  PubMed  Google Scholar 

  • Widdig A, Nürnberg P, Krawczak M, Streich WJ, Bercovitch F (2002) Affiliation and aggression among adult female rhesus macaques: a genetic analysis of paternal cohorts. Behaviour 139(2):371–391

    Article  Google Scholar 

  • Widdig A, Streich WJ, Nürnberg P, Croucher PJ, Bercovitch FB, Krawczak M (2006) Paternal kin bias in the agonistic interventions of adult female rhesus macaques (Macaca mulatta). Behav Ecol Sociobiol 61(2):205–214

    Article  Google Scholar 

  • Yamamoto S, Humle T, Tanaka M (2012) Chimpanzees’ flexible targeted helping based on an understanding of conspecifics’ goals. Proc Natl Acad Sci 109(9):3588–3592

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank Megan Cole, Francesca De Petrillo, Hayoung Chang, Megan Mulhinch, and Yijia Zheng for assistance with data collection and coding; Thore Bergman for helpful comments on an earlier version of the manuscript; and CSCAR at the University of Michigan for statistical advice. The authors are grateful to the Cayo Santiago Field Station and staff including Angelina Ruiz Lambides, Nahiri Rivera Barreto, Giselle Caraballo Cruz, and Bianca Giura for their research support.

Funding

This work was supported by a National Center for Research Resources CM-5-P40RR003640-13 award to the Caribbean Primate Research Center and the University of Puerto Rico, and an Office of Research Infrastructure Programs (ORIP) of the National Institutes of Health (NIH) through Grant Number 5P40OD012217 to the Caribbean Primate Research Center and the University of Puerto Rico. This research was supported in part by a Human Evolutionary Biology Early Training and Research Support Grant from Harvard University to RB. AR was supported by a Sloan Foundation fellowship.

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Correspondence to Rosemary Bettle.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All non-invasive behavioral tests were approved by the Institutional Animal Care and Use Committee (IACUC) for the University of Puerto Rico Medical Sciences Campus (protocol #A140116), and adhered to site guidelines for animal research.

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Bettle, R., Rosati, A.G. Flexible gaze-following in rhesus monkeys. Anim Cogn 22, 673–686 (2019). https://doi.org/10.1007/s10071-019-01263-4

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