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  • Review Article
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Facial expression production and perception in non-human primates

Nature Reviews Psychology volume 4, pages 457–469 (2025)Cite this article

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Abstract

Facial expressions are ubiquitous among primates and many clear similarities across species suggest a shared evolutionary history for these behaviours. Investigations of non-human primate facial expressions are therefore vital to enable us to understand the form and function of human facial behaviour. Methodological developments over the past two decades enable fine-grained quantitative comparisons across species and have demonstrated that similar processes underpin facial expressions in non-human and human primates. However, there is a tendency to focus on facial expression as a repertoire of discrete, prototypical expressions that does not always reflect naturalistic behaviour. In this Review, we review the production and perception of non-human primate facial expressions, focusing on methodological approaches and how to address the challenges of studying dynamic facial expressions. Moving forwards, methods that enable the study of dynamic and variable communicative exchange within social interaction might provide a better understanding of how facial expressions function and what (if anything) about facial expression is unique to humans.

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Fig. 1: Examples of bared-teeth facial expressions across primate species.
Fig. 2: Demonstration of the facial action coding system (ChimpFACS152).
Fig. 3: Illustration of methods used in perception experiments.

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References

  1. Rollings, J., Kavanagh, E., Balabanova, A., Keane, O. & Waller, B. M. Facial behaviour and first impressions in computer mediated communication. Comput. Hum. Behav. 161, 108391 (2024).

    Google Scholar 

  2. Kavanagh, E., Kimock, C., Whitehouse, J., Micheletta, J. & Waller, B. M. Revisiting Darwin’s comparisons between human and non-human primate facial signals. Evol. Hum. Sci. 4, e27 (2022).

    PubMed  PubMed Central  Google Scholar 

  3. Darwin, C. The Expression of the Emotions in Man and Animals (John Murray, 1872).

  4. Burrows, A. M. The facial expression musculature in primates and its evolutionary significance. BioEssays 30, 212–225 (2008).

    PubMed  Google Scholar 

  5. Burrows, A. M., Parr, L. A., Durham, E. L., Matthews, L. C. & Smith, T. D. Human faces are slower than chimpanzee faces. PLoS ONE 9, e110523 (2014).

    PubMed  PubMed Central  Google Scholar 

  6. Burrows, A. M., Rogers-Vizena, C. R., Li, L. & Mendelson, B. The mobility of the human face: more than just the musculature. Anat. Rec. 299, 1779–1788 (2016).

    Google Scholar 

  7. Waller, B. M., Julle-Daniere, E. & Micheletta, J. Measuring the evolution of facial ‘expression’ using multi-species FACS. Neurosci. Biobehav. Rev. 113, 1–11 (2020).

    PubMed  Google Scholar 

  8. Mehu, M. & Dunbar, R. I. M. Relationship between smiling and laughter in humans (Homo sapiens): testing the power asymmetry hypothesis. Folia Primatol. 79, 269–280 (2008).

    Google Scholar 

  9. Mehu, M., Grammer, K. & Dunbar, R. I. M. Smiles when sharing. Evol. Hum. Behav. 28, 415–422 (2007).

    Google Scholar 

  10. Samson, A. V. M. & Waller, B. M. Not growling but smiling: new interpretations of the bared‐teeth motif in the pre‐Columbian Caribbean. Curr. Anthropol. 51, 425–433 (2010).

    Google Scholar 

  11. Clark, P. R. et al. Morphological variants of silent bared‐teeth displays have different social interaction outcomes in crested macaques (Macaca nigra). Am. J. Phys. Anthropol. 173, 411–422 (2020). This study used the facial action coding system to show that there are subtle variations within the primate bared-teeth expression, thought to be a homologue of the human smile.

    PubMed  Google Scholar 

  12. Waller, B. M. & Dunbar, R. I. M. Differential behavioural effects of silent bared teeth display and relaxed open mouth display in chimpanzees (Pan troglodytes). Ethology 111, 129–142 (2005).

    Google Scholar 

  13. Van Hooff, J. in Non-Verbal Communication (ed. Hinde, R. A.) 209–241 (Cambridge Univ. Press, 1972). This work compared human smiling and laughing to primate bared-teeth display and play face, setting a framework for the comparative approach to the evolution of human facial expressions.

  14. Preuschoft, S. “Laughter” and “smile” in barbary macaques (Macaca sylvanus). Ethology 91, 220–236 (1992).

    Google Scholar 

  15. Liebal, K., Waller, B. M., Slocombe, K. E. & Burrows, A. M. Primate Communication: A Multimodal Approach (Cambridge Univ. Press, 2014).

  16. Graham, K. E. & Hobaiter, C. Towards a great ape dictionary: inexperienced humans understand common nonhuman ape gestures. PLOS Biol. 21, e3001939 (2023).

    PubMed  PubMed Central  Google Scholar 

  17. Kamiloğlu, R. G., Çalışkan, C., Slocombe, K. E. & Sauter, D. A. Threat vocalisations are acoustically similar between humans (Homo sapiens) and chimpanzees (Pan troglodytes). Bioacoustics 32, 679–692 (2023).

    Google Scholar 

  18. Slocombe, K. E., Waller, B. M. & Liebal, K. The language void: the need for multimodality in primate communication research. Anim. Behav. 81, 919–924 (2011).

    Google Scholar 

  19. Tomasello, M. Origins of Human Communication (MIT Press, 2010).

  20. Waller, B. M. & Micheletta, J. Facial expression in nonhuman animals. Emot. Rev. 5, 54–59 (2013).

    Google Scholar 

  21. Barrett, L. F., Adolphs, R., Marsella, S., Martinez, A. M. & Pollak, S. D. Emotional expressions reconsidered: challenges to inferring emotion from human facial movements. Psychol. Sci. Public Interest 20, 1–68 (2019). This meta-analysis of human facial expression research showed that there is no strong link between felt emotion and produced or perceived facial expressions.

    PubMed  PubMed Central  Google Scholar 

  22. Fridlund, A. J. Human Facial Expression: an Evolutionary View (Academic Press, 1994).

  23. Hinde, R. A. & Rowell, T. E. Communication by postures and facial expressions in the rhesus monkey (Macaca mulatta). Proc. Zool. Soc. Lond. 138, 1–21 (1962).

    Google Scholar 

  24. Waller, B. M., Whitehouse, J. & Micheletta, J. Rethinking primate facial expression: a predictive framework. Neurosci. Biobehav. Rev. 82, 13–21 (2017).

    PubMed  Google Scholar 

  25. Fridlund, A. J. in The Science of Facial Expression (eds Fernández-Dols, J.-M. & Russell, J. A.) 77–92 (Oxford Univ. Press, 2017).

  26. Crivelli, C. & Fridlund, A. J. Facial displays are tools for social influence. Trends Cogn. Sci. 22, 388–399 (2018).

    PubMed  Google Scholar 

  27. Kavanagh, E., Whitehouse, J. & Waller, B. M. Being facially expressive is socially advantageous. Sci. Rep. 14, 12798 (2024).

    PubMed  PubMed Central  Google Scholar 

  28. Nishida, T., Kano, T., Goodall, J., McGrew, W. C. & Nakamura, M. Ethogram and ethnography of Mahale chimpanzees. Anthropol. Sci. 107, 141–188 (1999).

    Google Scholar 

  29. van Hooff, J. A. R. A. M. in Primate Ethology (ed. Morris, D.) 7–68 (Routledge, 1967).

  30. Chevalier‐Skolnikoff, S. The primate play face: a possible key to the determinants and evolution of play. Rice Institute Pamphlet 60, no. 3. Rice University https://hdl.handle.net/1911/63157 (1974).

  31. Preuschoft, S. Primate faces and facial expressions. Soc. Res. 67, 245–271 (2000).

    Google Scholar 

  32. Ekman, P., Sorenson, E. R. & Friesen, W. V. Pan-cultural elements in facial displays of emotion. Science 164, 86–88 (1969).

    PubMed  Google Scholar 

  33. Kret, M. E., Prochazkova, E., Sterck, E. H. M. & Clay, Z. Emotional expressions in human and non-human great apes. Neurosci. Biobehav. Rev. 115, 378–395 (2020).

    PubMed  Google Scholar 

  34. Nickelson, S. A. & Lockard, J. S. Ethogram of Celebes monkeys (Macaca nigra) in two captive habitats. Primates 19, 437–447 (1978).

    Google Scholar 

  35. Stevenson, M. F. & Poole, T. B. An ethogram of the common marmoset (Calithrix jacchus jacchus): general behavioural repertoire. Anim. Behav. 24, 428–451 (1976).

    PubMed  Google Scholar 

  36. Oswald, M. & Lockard, J. S. Ethogram of the De Brazza’s guenon (Cercopithecus neglectus) in captivity. Appl. Anim. Ethol. 6, 285–296 (1980).

    Google Scholar 

  37. Skinner, S. & Lockard, J. S. An ethogram of the liontail macaque (Macaca silenus) in captivity. Appl. Anim. Ethol. 5, 241–253 (1979).

    Google Scholar 

  38. Kemp, C. & Kaplan, G. Facial expressions in common marmosets (Callithrix jacchus) and their use by conspecifics. Anim. Cogn. 16, 773–788 (2013).

    PubMed  Google Scholar 

  39. Thierry, B., Demaria, C., Preuschoft, S. & Desportes, C. Structural convergence between silent bared-teeth display and relaxed open-mouth display in the Tonkean macaque (Macaca tonkeana). Folia Primatol. 52, 178–184 (1989).

    Google Scholar 

  40. Visalberghi, E., Valenzano, D. R. & Preuschoft, S. Facial displays in Cebus apella. Int. J. Primatol. 27, 1689–1707 (2006).

    Google Scholar 

  41. Kirkevold, B. C., Lockard, J. S. & Heestand, J. E. Development comparisons of grimace and play mouth in infant pigtail macaques (Macaca nemestrina). Am. J. Primatol. 3, 277–283 (1982).

    PubMed  Google Scholar 

  42. Maestripieri, D. Gestural communication in macaques: usage and meaning of nonvocal signals. Evol. Commun. 1, 193–222 (1997).

    Google Scholar 

  43. Maestripieri, D. & Wallen, K. Affiliative and submissive communication in rhesus macaques. Primates 38, 127–138 (1997).

    Google Scholar 

  44. Cordoni, G., Ciantia, A., Guéry, J.-P., Mulot, B. & Norscia, I. Rapid facial mimicry in platyrrhini: play face replication in spider monkeys (Ateles fusciceps, Ateles hybridus, and Ateles paniscus). Am. J. Primatol. 86, e23607 (2024).

    PubMed  Google Scholar 

  45. Pellis, S. M. & Pellis, V. C. Targets, tactics, and the open mouth face during play fighting in three species of primates. Aggress. Behav. 23, 41–57 (1997).

    Google Scholar 

  46. Waller, B. M. & Cherry, L. Facilitating play through communication: significance of teeth exposure in the gorilla play face. Am. J. Primatol. 74, 157–164 (2012).

    PubMed  Google Scholar 

  47. Palagi, E., Norscia, I. & Spada, G. Relaxed open mouth as a playful signal in wild ring-tailed lemurs. Am. J. Primatol. 76, 1074–1083 (2014).

    PubMed  Google Scholar 

  48. Panksepp, J. & Burgdorf, J. “Laughing” rats and the evolutionary antecedents of human joy? Physiol. Behav. 79, 533–547 (2003).

    PubMed  Google Scholar 

  49. Maglieri, V. et al. Tell-tale signals: faces reveal playful and aggressive mood in wolves. Anim. Behav. 214, 1–9 (2024).

    Google Scholar 

  50. Maglieri, V., Zanoli, A., Mastrandrea, F. & Palagi, E. The relaxed open mouth is a true signal in dogs: demonstrating Tinbergen’s ritualization process. Anim. Behav. 188, 65–74 (2022).

    Google Scholar 

  51. Llamazares-Martín, C., Scopa, C., Guillén-Salazar, F. & Palagi, E. Relaxed open mouth reciprocity favours playful contacts in South American sea lions (Otaria flavescens). Behav. Process. 140, 87–95 (2017).

    Google Scholar 

  52. Davila-Ross, M. & Dezecache, G. The complexity and phylogenetic continuity of laughter and smiles in hominids. Front. Psychol. 12, 648497 (2021).

    PubMed  PubMed Central  Google Scholar 

  53. Pellis, S. M. & Pellis, W. C. On knowing it’s only play: the role of play signals in play fighting. Aggress. Violent Behav. 1, 249–268 (1996).

    Google Scholar 

  54. Bliss-Moreau, E. & Moadab, G. in The Science of Facial Expression (eds. Fernández-Dols, J. M. & Russell, J. A.), 153–171 (Oxford Univ. Press, 2017).

  55. Petersen, R. M., Dubuc, C. & Higham, J. P. in The Facial Displays of Leaders (ed. Senior, C.) 123–143 (Springer International Publishing, 2018).

  56. Waller, B. M., Whitehouse, J. & Micheletta, J. Macaques can predict social outcomes from facial expressions. Anim. Cogn. 19, 1031–1036 (2016).

    PubMed  PubMed Central  Google Scholar 

  57. Thierry, B., Singh, M. & Kaumanns, W. Macaque Societies: A Model for the Study of Social Organization (Cambridge Univ. Press, 2004).

  58. Wiper, S. M. & Semple, S. The function of teeth chattering in male Barbary macaques (Macaca sylvanus). Am. J. Primatol. 69, 1179–1188 (2007).

    PubMed  Google Scholar 

  59. Micheletta, J., Engelhardt, A., Matthews, L., Agil, M. & Waller, B. M. Multicomponent and multimodal lipsmacking in crested macaques (Macaca nigra): lipsmacking behavior in crested macaques. Am. J. Primatol. 75, 763–773 (2013).

    PubMed  Google Scholar 

  60. Albuquerque, N. et al. The shape of lipsmacking: socio-emotional regulation in bearded capuchin monkeys (Sapajus libidinosus). Evol. Hum. Sci. 5, e16 (2023).

    PubMed  PubMed Central  Google Scholar 

  61. Andrew, R. J. Evolution of facial expression. Science 142, 1034–1041 (1963).

    PubMed  Google Scholar 

  62. Parr, L. A. The discrimination of faces and their emotional content by chimpanzees (Pan troglodytes). Ann. NY Acad. Sci. 1000, 56–78 (2003).

    PubMed  Google Scholar 

  63. Liebal, K., Slocombe, K. E. & Waller, B. M. The language void 10 years on: multimodal primate communication research is still uncommon. Ethol. Ecol. Evol. 34, 274–287 (2022).

    Google Scholar 

  64. Genty, E., Clay, Z. & Hobaiter, C. Multi-modal use of a socially directed call in bonobos. PLoS ONE 9, e84738 (2014).

    PubMed  PubMed Central  Google Scholar 

  65. Partan, S. R. Single and multichannel signal composition: facial expressions and vocalizations of rhesus macaques (Macaca mulatta). Behaviour 139, 993–1027 (2002). This comprehensive description of rhesus macaque communication emphasizes the multimodal elements and the importance of multimodal communication for communicative complexity.

    Google Scholar 

  66. Taglialatela, J. P. et al. Multimodal communication in chimpanzees. Am. J. Primatol. 77, 1143–1148 (2015).

    PubMed  PubMed Central  Google Scholar 

  67. Parr, L. A., Cohen, M. & de Waal, F. Influence of social context on the use of blended and graded facial displays in chimpanzees. Int. J. Primatol. 26, 73–103 (2005). This observational study shows the extent to which chimpanzee facial expressions do not always fit discrete categories.

    Google Scholar 

  68. Marler, P. in Growing Points in Ethology (eds Bateson, P. P. G. & Hinde, R. A.) 239–280 (Cambridge Univ. Press, 1976).

  69. Fedurek, P., Zuberbühler, K. & Dahl, C. D. Sequential information in a great ape utterance. Sci. Rep. 6, 38226 (2016).

    PubMed  PubMed Central  Google Scholar 

  70. Leroux, M. et al. Chimpanzees combine pant hoots with food calls into larger structures. Anim. Behav. 179, 41–50 (2021).

    Google Scholar 

  71. Hobaiter, C. & Byrne, R. W. Serial gesturing by wild chimpanzees: its nature and function for communication. Anim. Cogn. 14, 827–838 (2011).

    PubMed  Google Scholar 

  72. Liebal, K., Call, J. & Tomasello, M. Use of gesture sequences in chimpanzees. Am. J. Primatol. 64, 377–396 (2004).

    PubMed  Google Scholar 

  73. Aychet, J., Blois-Heulin, C. & Lemasson, A. Sequential and network analyses to describe multiple signal use in captive mangabeys. Anim. Behav. 182, 203–226 (2021).

    Google Scholar 

  74. Ekman, P., Friesen, W. V. & Hager, J. C. Facial Action Coding System (Research Nexus, 2002).

  75. Ekman, P & Friesen, W. V. Facial Action Coding System: A Technique for the Measurement of Facial Movement (Consulting Psychologists Press, 1978).

  76. Baltrušaitis, T., Robinson, P. & Morency, L.-P. OpenFace: an open source facial behavior analysis toolkit. In 2016 IEEE Winter Conf. on Applications of Computer Vision (WACV) https://doi.org/10.1109/WACV.2016.7477553 (IEEE, 2016).

  77. Martin, J., Rychlowska, M., Wood, A. & Niedenthal, P. Smiles as multipurpose social signals. Trends Cogn. Sci. 21, 864–877 (2017).

    PubMed  Google Scholar 

  78. Lazow, S. P. & Bergman, T. J. The structural and motivational role of the unique lip-flip movement in the gelada (Theropithecus gelada) facial display repertoire. Am. J. Phys. Anthropol. 172, 280–290 (2020).

    PubMed  Google Scholar 

  79. Partan, S. R. & Marler, P. Communication goes multimodal. Science 283, 1272–1273 (1999).

    PubMed  Google Scholar 

  80. Waller, B. M., Caeiro, C. C. & Davila-Ross, M. Orangutans modify facial displays depending on recipient attention. PeerJ 3, e827 (2015).

    PubMed  PubMed Central  Google Scholar 

  81. Liebal, K., Pika, S. & Tomasello, M. Gestural communication of orangutans (Pongo pygmaeus). Gesture 6, 1–38 (2006).

    Google Scholar 

  82. Scheider, L., Waller, B. M., Oña, L., Burrows, A. M. & Liebal, K. Social use of facial expressions in hylobatids. PLoS ONE 11, e0151733 (2016).

    PubMed  PubMed Central  Google Scholar 

  83. Dobson, S. D. Socioecological correlates of facial mobility in nonhuman anthropoids. Am. J. Phys. Anthropol. 139, 413–420 (2009). This study tested the social complexity hypothesis by showing that facial mobility is positively related to social group size across primate species.

    PubMed  Google Scholar 

  84. Dobson, S. D. Allometry of facial mobility in anthropoid primates: implications for the evolution of facial expression. Am. J. Phys. Anthropol. 138, 70–81 (2009).

    PubMed  Google Scholar 

  85. Kiltie, R. A. Scaling of visual acuity with body size in mammals and birds. Funct. Ecol. 14, 226–234 (2000).

    Google Scholar 

  86. Freeberg, T. M., Dunbar, R. I. M. & Ord, T. J. Social complexity as a proximate and ultimate factor in communicative complexity. Phil. Trans. R. Soc. B 367, 1785–1801 (2012).

    PubMed  PubMed Central  Google Scholar 

  87. Blumstein, D. T. & Armitage, K. B. Does sociality drive the evolution of communicative complexity? A comparative test with ground-dwelling sciurid alarm calls. Am. Nat. 150, 179–200 (1997).

    PubMed  Google Scholar 

  88. Freeberg, T. M. Social complexity can drive vocal complexity: group size influences vocal information in Carolina chickadees. Psychol. Sci. 17, 557–561 (2006).

    PubMed  Google Scholar 

  89. McComb, K. & Semple, S. Coevolution of vocal communication and sociality in primates. Biol. Lett. 1, 381–385 (2005).

    PubMed  PubMed Central  Google Scholar 

  90. Wilkinson, G. S. in Animal Social Complexity: Intelligence, Culture and Individualized Societies (eds De Waal, F. B. M. & Tyack, P. L.) 322–341 (Harvard Univ. Press, 2003).

  91. Birg, J. A. & English, T. Effects of regulating emotional expression on authenticity and likeability in stranger dyads. J. Soc. Pers. Relatsh. 41, 2868–2888 (2024).

    Google Scholar 

  92. Whitehouse, J. et al. Facial expressivity in dominant macaques is linked to group cohesion. Proc. R. Soc. B 291, 20240984 (2024). This paper is an empirical demonstration of the social bonding function of facial expression in rhesus macaques.

    PubMed  PubMed Central  Google Scholar 

  93. Mielke, A. et al. NetFACS: using network science to understand facial communication systems. Behav. Res. Meth. 54, 1912–1927 (2021).

    Google Scholar 

  94. Rincon, A. V. et al. Higher social tolerance is associated with more complex facial behavior in macaques. eLife 12, RP87008 (2023). This paper describes a tool that combines the facial action coding system with social network analysis to quantify complexity of facial expression systems across species.

    PubMed  PubMed Central  Google Scholar 

  95. Kim, Y. & Kret, M. in The Oxford Handbook of Emotional Development (eds Dukes, D. et al.) 129–145 (Oxford Univ. Press, 2022).

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

    Google Scholar 

  97. Kanazawa, S. Recognition of facial expressions in a Japanese monkey (Macaca fuscata) and humans (Homo sapiens). Primates 37, 25–38 (1996).

    Google Scholar 

  98. Parr, L. A., Hopkins, W. D. & de Waal, F. B. M. The perception of facial expressions by chimpanzees, Pan troglodytes. Evol. Commun. 2, 1–23 (1998). This experimental study showed that chimpanzees can identify and discriminate between different static, discrete facial expressions.

    Google Scholar 

  99. Parr, L. A. Perceptual biases for multimodal cues in chimpanzee (Pan troglodytes) affect recognition. Anim. Cogn. 7, 171–178 (2004).

    PubMed  Google Scholar 

  100. Parr, L. A., Waller, B. M. & Heintz, M. Facial expression categorization by chimpanzees using standardized stimuli. Emotion 8, 216–231 (2008).

    PubMed  PubMed Central  Google Scholar 

  101. Parr, L. A. & Heintz, M. Facial expression recognition in rhesus monkeys, Macaca mulatta. Anim. Behav. 77, 1507–1513 (2009).

    PubMed  PubMed Central  Google Scholar 

  102. Micheletta, J. et al. Familiar and unfamiliar face recognition in crested macaques (Macaca nigra). R. Soc. Open Sci. 2, 150109 (2015).

    PubMed  PubMed Central  Google Scholar 

  103. Calcutt, S. E., Rubin, T. L., Pokorny, J. J. & de Waal, F. B. M. Discrimination of emotional facial expressions by tufted capuchin monkeys (Sapajus apella). J. Comp. Psychol. 131, 40–49 (2017).

    PubMed  Google Scholar 

  104. Parr, L. A. & Hecht, E. E. in Oxford Handbook of Face Perception (eds Calder, A. J., Rhodes, G., Johnson, M. H. & Haxby, J. V.) 691–706 (Oxford Univ. Press, 2011).

  105. Öhman, A., Lundqvist, D. & Esteves, F. The face in the crowd revisited: a threat advantage with schematic stimuli. J. Pers. Soc. Psychol. 80, 381–396 (2001).

    PubMed  Google Scholar 

  106. Ohman, A. & Mineka, S. Fears, phobias, and preparedness: toward an evolved module of fear and fear learning. Psychol. Rev. 108, 483–522 (2001).

    PubMed  Google Scholar 

  107. Bachmann, H. P., Japee, S., Merriam, E. P. & Liu, T. T. Emotion and anxiety interact to bias spatial attention. Emotion 24, 1109–1124 (2024).

    PubMed  Google Scholar 

  108. King, H. M., Kurdziel, L. B., Meyer, J. S. & Lacreuse, A. Effects of testosterone on attention and memory for emotional stimuli in male rhesus monkeys. Psychoneuroendocrinology 37, 396–409 (2012).

    PubMed  Google Scholar 

  109. Lacreuse, A., Schatz, K., Strazzullo, S., King, H. M. & Ready, R. Attentional biases and memory for emotional stimuli in men and male rhesus monkeys. Anim. Cogn. 16, 861–871 (2013).

    PubMed  Google Scholar 

  110. Parr, L. A., Modi, M., Siebert, E. & Young, L. J. Intranasal oxytocin selectively attenuates rhesus monkeys’ attention to negative facial expressions. Psychoneuroendocrinology 38, 1748–1756 (2013).

    PubMed  PubMed Central  Google Scholar 

  111. Cassidy, L. C. et al. The dot-probe attention bias task as a method to assess psychological well-being after anesthesia: a study with adult female long-tailed macaques (Macaca fascicularis). Eur. Surg. Res. 64, 37–53 (2023).

    PubMed  Google Scholar 

  112. Wilson, D. A. & Tomonaga, M. Exploring attentional bias towards threatening faces in chimpanzees using the dot probe task. PLoS ONE 13, e0207378 (2018).

    PubMed  PubMed Central  Google Scholar 

  113. Reilly, O. T., Benítez, M. E., Beran, M. J., Barber, S. J. & Brosnan, S. F. No evidence of attentional bias toward threatening conspecific and allospecific faces in capuchin monkeys (Sapajus [Cebus] apella) using a dot-probe task. J. Comp. Psychol. 138, 259–275 (2024).

    PubMed  Google Scholar 

  114. Bethell, E. J., Holmes, A., MacLarnon, A. & Semple, S. Evidence that emotion mediates social attention in rhesus macaques. PLoS ONE 7, e44387 (2012).

    PubMed  PubMed Central  Google Scholar 

  115. Howarth, E. R. I. et al. Developing and validating attention bias tools for assessing trait and state affect in animals: a worked example with Macaca mulatta. Appl. Anim. Behav. Sci. 234, 105198 (2021).

    Google Scholar 

  116. Pritsch, C., Telkemeyer, S., Mühlenbeck, C. & Liebal, K. Perception of facial expressions reveals selective affect-biased attention in humans and orangutans. Sci. Rep. 7, 7782 (2017).

    PubMed  PubMed Central  Google Scholar 

  117. Zhao, H. et al. Facial expression recognition in golden snub-nosed monkeys. Curr. Zool. 66, 695–697 (2020).

    PubMed  PubMed Central  Google Scholar 

  118. Rayson, H., Massera, A., Belluardo, M., Ben Hamed, S. & Ferrari, P. F. Early social adversity modulates the relation between attention biases and socioemotional behaviour in juvenile macaques. Sci. Rep. 11, 21704 (2021).

    PubMed  PubMed Central  Google Scholar 

  119. Rosati, A. G., Arre, A. M., Platt, M. L. & Santos, L. R. Developmental shifts in social cognition: socio-emotional biases across the lifespan in rhesus monkeys. Behav. Ecol. Sociobiol. 72, 163 (2018).

    Google Scholar 

  120. Parr, L. A. Cognitive and physiological markers of emotional awareness in chimpanzees (Pan troglodytes). Anim. Cogn. 4, 223–229 (2001).

    PubMed  Google Scholar 

  121. Goossens, B. M. A., Dekleva, M., Reader, S. M., Sterck, E. H. M. & Bolhuis, J. J. Gaze following in monkeys is modulated by observed facial expressions. Anim. Behav. 75, 1673–1681 (2008).

    Google Scholar 

  122. Teufel, C., Gutmann, A., Pirow, R. & Fischer, J. Facial expressions modulate the ontogenetic trajectory of gaze-following among monkeys. Dev. Sci. 13, 913–922 (2010). This study is a rare example of an observational study that documented responses to facial expressions (and gaze following) during real-world social interaction.

    PubMed  Google Scholar 

  123. Champ, T. M. et al. Social engagement revealed by gaze following in third-party observers of simulated social conflict. Front. Psychol. 13, 952390 (2022).

    PubMed  PubMed Central  Google Scholar 

  124. Overduin-de Vries, A. M., Bakker, F. A. A., Spruijt, B. M. & Sterck, E. H. M. Male long-tailed macaques (Macaca fascicularis) understand the target of facial threat. Am. J. Primatol. 78, 720–730 (2016).

    PubMed  Google Scholar 

  125. Buttelmann, D., Call, J. & Tomasello, M. Do great apes use emotional expressions to infer desires? Dev. Sci. 12, 688–698 (2009).

    PubMed  Google Scholar 

  126. Morimoto, Y. & Fujita, K. Capuchin monkeys (Cebus apella) use conspecifics’ emotional expressions to evaluate emotional valence of objects. Anim. Cogn. 15, 341–347 (2012). This innovative experimental study showed that capuchin monkeys preferentially selected boxes based on conspecific reactions (including facial expressions), which suggests that they can interpret the meaning of the expressions and use this information to modify their behaviour.

    PubMed  Google Scholar 

  127. Morimoto, Y. & Fujita, K. Capuchin monkeys (Cebus apella) modify their own behaviors according to a conspecific’s emotional expressions. Primates 52, 279–286 (2011).

    PubMed  Google Scholar 

  128. Nieuwburg, E. G. I., Ploeger, A. & Kret, M. E. Emotion recognition in nonhuman primates: how experimental research can contribute to a better understanding of underlying mechanisms. Neurosci. Biobehav. Rev. 123, 24–47 (2021).

    PubMed  Google Scholar 

  129. Hatfield, E., Cacioppo, J. T. & Rapson, R. L. Emotional contagion. Curr. Dir. Psychol. Sci. 2, 96–100 (1993).

    Google Scholar 

  130. Prochazkova, E. & Kret, M. E. Connecting minds and sharing emotions through mimicry: a neurocognitive model of emotional contagion. Neurosci. Biobehav. Rev. 80, 99–114 (2017).

    PubMed  Google Scholar 

  131. Preston, S. D. & de Waal, F. B. M. Empathy: its ultimate and proximate bases. Behav. Brain Sci. 25, 1–20 (2002).

    PubMed  Google Scholar 

  132. Dimberg, U., Thunberg, M. & Elmehed, K. Unconscious facial reactions to emotional facial expressions. Psychol. Sci. 11, 86–89 (2000).

    PubMed  Google Scholar 

  133. Davila Ross, M., Menzler, S. & Zimmermann, E. Rapid facial mimicry in orangutan play. Biol. Lett. 4, 27–30 (2008).

    PubMed  Google Scholar 

  134. Mancini, G., Ferrari, P. F. & Palagi, E. In play we trust. Rapid facial mimicry predicts the duration of playful interactions in geladas. PLoS ONE 8, e66481 (2013).

    PubMed  PubMed Central  Google Scholar 

  135. Rendall, D., Owren, M. J. & Ryan, M. J. What do animal signals mean? Anim. Behav. 78, 233–240 (2009).

    Google Scholar 

  136. Gothard, K. M., Battaglia, F. P., Erickson, C. A., Spitler, K. M. & Amaral, D. G. Neural responses to facial expression and face identity in the monkey amygdala. J. Neurophysiol. 97, 1671–1683 (2007).

    PubMed  Google Scholar 

  137. Taubert, J. & Japee, S. Real face value: the processing of naturalistic facial expressions in the macaque inferior temporal cortex. J. Cogn. Neurosci. 36, 2725–2741 (2024).

    PubMed  Google Scholar 

  138. Rutishauser, U., Mamelak, A. N. & Adolphs, R. The primate amygdala in social perception — insights from electrophysiological recordings and stimulation. Trends Neurosci. 38, 295–306 (2015).

    PubMed  PubMed Central  Google Scholar 

  139. Sackett, G. P. Monkeys reared in isolation with pictures as visual input: evidence for an innate releasing mechanism. Science 154, 1468–1473 (1966).

    PubMed  Google Scholar 

  140. Morin, E. L., Howell, B. R., Meyer, J. S. & Sanchez, M. M. Effects of early maternal care on adolescent attention bias to threat in nonhuman primates. Dev. Cogn. Neurosci. 38, 100643 (2019).

    PubMed  PubMed Central  Google Scholar 

  141. O’Callaghan, O., Whitehouse, J., Paukner, A., Witham, C. L. & Waller, B. M. Maternal care predicts facial expression processing in macaques. iScience 28, 112179 (2025).

    PubMed  PubMed Central  Google Scholar 

  142. Fleagle, J. G. & Seiffert, E. R. in Evolutionary Neuroscience 2nd edn (ed. Kaas, J. H.) 483–518 (Elsevier, 2020).

  143. Waller, B. M., Liebal, K., Burrows, A. M. & Slocombe, K. E. How can a multimodal approach to primate communication help us understand the evolution of communication? Evol. Psychol. 11, 147470491301100 (2013).

    Google Scholar 

  144. Fröhlich, M. & van Schaik, C. P. The function of primate multimodal communication. Anim. Cogn. 21, 619–629 (2018).

    PubMed  Google Scholar 

  145. Waller, B. M., Kavanagh, E., Micheletta, J., Clark, P. R. & Whitehouse, J. The face is central to primate multicomponent signals. Int. J. Primatol. 45, 526–542 (2024).

    Google Scholar 

  146. Wieser, M. & Brosch, T. Faces in context: a review and systematization of contextual influences on affective face processing. Front. Psychol. 3, 471 (2012).

    PubMed  PubMed Central  Google Scholar 

  147. Righart, R. & de Gelder, B. Rapid influence of emotional scenes on encoding of facial expressions: an ERP study. Soc. Cogn. Affect. Neurosci. 3, 270–278 (2008).

    PubMed  PubMed Central  Google Scholar 

  148. Barrett, L. F., Mesquita, B. & Gendron, M. Context in emotion perception. Curr. Dir. Psychol. Sci. 20, 286–290 (2011).

    Google Scholar 

  149. Taubert, J. et al. Parallel processing of facial expression and head orientation in the macaque brain. J. Neurosci. 40, 8119–8131 (2020).

    PubMed  PubMed Central  Google Scholar 

  150. Abassi, E. et al. Neural encoding of bodies for primate social perception. J. Neurosci. 44, e1221242024 (2024).

    PubMed  PubMed Central  Google Scholar 

  151. Shepherd, S. V. & Platt, M. L. Noninvasive telemetric gaze tracking in freely moving socially housed prosimian primates. Methods 38, 185–194 (2006).

    PubMed  PubMed Central  Google Scholar 

  152. Vick, S.-J., Waller, B. M., Parr, L. A., Smith Pasqualini, M. C. & Bard, K. A. A cross-species comparison of facial morphology and movement in humans and chimpanzees using the Facial Action Coding System (FACS). J. Nonverbal Behav. 31, 1–20 (2007). This study modified the facial action coding system for use with a non-human primate species.

    PubMed  PubMed Central  Google Scholar 

  153. Hjortsjo, C. H. Man’s Face and Mimic Language (Nordens Boktryckeri, 1970).

  154. Duchenne, G.-B. The Mechanism of Human Facial Expression (Cambridge Univ. Press, 1862).

  155. Efthimiou, T. N., Hernandez, M. P., Elsenaar, A., Mehu, M. & Korb, S. Application of facial neuromuscular electrical stimulation (fNMES) in psychophysiological research: practical recommendations based on a systematic review of the literature. Behav. Res. Meth. 56, 2941–2976 (2024).

    Google Scholar 

  156. Waller, B. M. et al. Intramuscular electrical stimulation of facial muscles in humans and chimpanzees: Duchenne revisited and extended. Emotion 6, 367–382 (2006).

    PubMed  PubMed Central  Google Scholar 

  157. De Bonnecaze, G. et al. Variability in facial-muscle innervation: a comparative study based on electrostimulation and anatomical dissection. Clin. Anat. 32, 169–175 (2019).

    PubMed  Google Scholar 

  158. Parr, L. A., Waller, B. M., Burrows, A. M., Gothard, K. M. & Vick, S. J. MaqFACS: a muscle-based facial movement coding system for the rhesus macaque. Am. J. Phys. Anthropol. 143, 625–630 (2010).

    PubMed  PubMed Central  Google Scholar 

  159. Julle-Danière, É. et al. MaqFACS (Macaque Facial Action Coding System) can be used to document facial movements in Barbary macaques (Macaca sylvanus). PeerJ 3, e1248 (2015).

    PubMed  PubMed Central  Google Scholar 

  160. Correia-Caeiro, C., Holmes, K. & Miyabe-Nishiwaki, T. Extending the MaqFACS to measure facial movement in Japanese macaques (Macaca fuscata) reveals a wide repertoire potential. PLoS ONE 16, e0245117 (2021).

    PubMed  PubMed Central  Google Scholar 

  161. Waller, B. M., Lembeck, M., Kuchenbuch, P., Burrows, A. M. & Liebal, K. GibbonFACS: a muscle-based facial movement coding system for hylobatids. Int. J. Primatol. 33, 809–821 (2012).

    Google Scholar 

  162. Caeiro, C. C., Waller, B. M., Zimmermann, E., Burrows, A. M. & Davila-Ross, M. OrangFACS: a muscle-based facial movement coding system for orangutans (Pongo spp.). Int. J. Primatol. 34, 115–129 (2013).

    Google Scholar 

  163. Correia-Caeiro, C., Burrows, A., Wilson, D. A., Abdelrahman, A. & Miyabe-Nishiwaki, T. CalliFACS: the common marmoset facial action coding system. PLoS ONE 17, e0266442 (2022).

    PubMed  PubMed Central  Google Scholar 

  164. Waller, B. M. et al. Paedomorphic facial expressions give dogs a selective advantage. PLoS ONE 8, e82686 (2013).

    PubMed  PubMed Central  Google Scholar 

  165. Wathan, J., Burrows, A. M., Waller, B. M. & McComb, K. EquiFACS: the equine facial action coding system. PLoS ONE 10, e0137818 (2015).

    PubMed  PubMed Central  Google Scholar 

  166. Caeiro, C. C., Burrows, A. M. & Waller, B. M. Development and application of CatFACS: are human cat adopters influenced by cat facial expressions? Appl. Anim. Behav. Sci. 189, 66–78 (2017).

    Google Scholar 

  167. Burrows, A. M., Waller, B. M. & Parr, L. A. Facial musculature in the rhesus macaque (Macaca mulatta): evolutionary and functional contexts with comparisons to chimpanzees and humans. J. Anat. 215, 320–334 (2009).

    PubMed  PubMed Central  Google Scholar 

  168. Burrows, A. M., Waller, B. M. & Micheletta, J. Mimetic muscles in a despotic macaque (Macaca mulatta) differ from those in a closely related tolerant macaque (M. nigra). Anat. Rec. 299, 1317–1324 (2016).

    Google Scholar 

  169. Burrows, A. M., Waller, B. M., Parr, L. A. & Bonar, C. J. Muscles of facial expression in the chimpanzee (Pan troglodytes): descriptive, comparative and phylogenetic contexts. J. Anat. 208, 153–167 (2006).

    PubMed  PubMed Central  Google Scholar 

  170. Burrows, A. M., Diogo, R., Waller, B. M., Bonar, C. J. & Liebal, K. Evolution of the muscles of facial expression in a monogamous ape: evaluating the relative influences of ecological and phylogenetic factors in hylobatids. Anat. Rec. Adv. Integr. Anat. Evol. Biol. 294, 645–663 (2011).

    Google Scholar 

  171. Kaminski, J., Waller, B. M., Diogo, R., Hartstone-Rose, A. & Burrows, A. M. Evolution of facial muscle anatomy in dogs. Proc. Natl Acad. Sci. 116, 14677–14681 (2019).

    PubMed  PubMed Central  Google Scholar 

  172. Waller, B. M., Parr, L. A., Gothard, K. M., Burrows, A. M. & Fuglevand, A. J. Mapping the contribution of single muscles to facial movements in the rhesus macaque. Physiol. Behav. 95, 93–100 (2008).

    PubMed  PubMed Central  Google Scholar 

  173. Bishay, M. et al. AFFDEX 2.0: a real-time facial expression analysis toolkit. In 2023 IEEE 17th Int. Conf. on Automatic Face and Gesture Recognition (FG) (IEEE, 2023).

  174. Stöckli, S., Schulte-Mecklenbeck, M., Borer, S. & Samson, A. C. Facial expression analysis with AFFDEX and FACET: a validation study. Behav. Res. Methods 50, 1446–1460 (2018).

    PubMed  Google Scholar 

  175. Lewinski, P., Den Uyl, T. M. & Butler, C. Automated facial coding: validation of basic emotions and FACS AUs in FaceReader. J. Neurosci. Psychol. Econ. 7, 227–236 (2014).

    Google Scholar 

  176. Morozov, A., Parr, L. A., Gothard, K., Paz, R. & Pryluk, R. Automatic recognition of macaque facial expressions for detection of affective states. eNeuro 8, ENEURO.0117-21.2021 (2021).

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Acknowledgements

The authors thank the FACEDIFF team for helpful discussions. B.W. discloses support for the research of this work from European Research Council (grant number 864694).

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  1. Department of Psychology, Nottingham Trent University, Nottingham, UK

    Bridget M. Waller, Olivia O’Callaghan & Jamie Whitehouse

  2. School of Psychology, Sport and Health Sciences, University of Portsmouth, Portsmouth, UK

    Jérôme Micheletta

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Waller, B.M., O’Callaghan, O., Micheletta, J. et al. Facial expression production and perception in non-human primates. Nat Rev Psychol 4, 457–469 (2025). https://doi.org/10.1038/s44159-025-00462-w

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