Preference for facial averageness: Evidence for a common mechanism in human and macaque infants

www.nature.com/scientificreports OPEN received: 15 September 2016 accepted: 14 March 2017 Published: 13 April 2017 Preference for facial averageness: Evidence for a common mechanism in human and macaque infants Fabrice Damon1,2, David Méary1,2, Paul C. Quinn3, Kang Lee4, Elizabeth A. Simpson5, Annika Paukner6, Stephen J. Suomi6 & Olivier Pascalis1,2 Human adults and infants show a preference for average faces, which could stem from a general processing mechanism and may be shared among primates. However, little is known about preference for facial averageness in monkeys. We used a comparative developmental approach and eye-tracking methodology to assess visual attention in human and macaque infants to faces naturally varying in their distance from a prototypical face. In Experiment 1, we examined the preference for faces relatively close to or far from the prototype in 12-month-old human infants with human adult female faces. Infants preferred faces closer to the average than faces farther from it. In Experiment 2, we measured the looking time of 3-month-old rhesus macaques (Macaca mulatta) viewing macaque faces varying in their distance from the prototype. Like human infants, macaque infants looked longer to faces closer to the average. In Experiments 3 and 4, both species were presented with unfamiliar categories of faces (i.e., macaque infants tested with adult macaque faces; human infants and adults tested with infant macaque faces) and showed no prototype preferences, suggesting that the prototypicality effect is experience-dependent. Overall, the findings suggest a common processing mechanism across species, leading to averageness preferences in primates. Face processing is of major importance for primates living in large and complex social networks, and plays a crucial role in the formation of inter-individual relationships with multiple group members. Given the importance of face perception for primates, it is reasonable to suggest that such a cognitive skill would be subject to selective pressure through the course of evolution1, and it has been argued that there may be a common primate face recognition system2. Accordingly, several aspects of face processing are shared between humans and nonhuman primates throughout ontogeny and phylogeny3,4. For example, at a behavioral level, the distribution of eye movements in humans and macaques during face scanning appears relatively similar, showing the same systematic modulations with stimulus manipulations such as blurring or inversion5. Moreover, humans fixate more on the eyes than on any other facial feature5,6, which is also consistently reported in adult macaques5,7–10 and infants11–14. At a neural level, examination of the organization of face-selective regions across the temporal lobe in both humans and macaques has revealed a close anatomical correspondence between the human and macaque face-processing systems2,15,16. Moreover, macaque face processing has been shown to be norm-based (i.e., prototype-based) at the cellular level17. Using single-cell recordings, it has been reported that face-responsive neurons of the anterior inferotemporal cortex of adult macaque monkeys show a tuning centered around the average face. These neurons monotonically increased firing for increased levels of caricaturization (i.e., exaggeration of distinguishing features) for a previously learned face. This result suggests that face-processing in macaque monkeys is organized around a prototypical face representation. A similar finding was reported in humans, showing that adaptation to a face biased the perception of subsequently presented faces along an identity trajectory away from the adapting face, and along an axis centered on the prototypical face representation18. Similarities between humans and macaques have also been reported for early developmental processes. Infant macaques present sensitivity for basic face structures (i.e., first-order relations, eyes above the nose, nose above the mouth). They prefer stimuli that respect face-like configuration19–21, and prior work has revealed a similar sensitivity in human neonates22,23. Later, between 3 and 12 months of age, human infants exhibit a perceptual 1 Univ. Grenoble-Alpes, LPNC, France. 2CNRS, LPNC,UMR 5105, France. 3University of Delaware, USA. 4University of Toronto, Canada. 5University of Miami, USA. 6Eunice Kennedy Shriver National Institute of Child Health and Human Development, USA. Correspondence and requests for materials should be addressed to F.D. (email: damon.fabrice@ gmail.com) Scientific Reports | 7:46303 | DOI: 10.1038/srep46303 1 www.nature.com/scientificreports/ tuning for faces in a way that makes processing and recognizing infrequently seen faces (e.g., monkey faces) more difficult24, a phenomenon likely driven by experience25–27. A similar specialization has been shown in Japanese macaques28, whose face viewing preference and discrimination performance was biased towards the species category of faces to which the macaques were first exposed, following a total face deprivation period of up to 6 months28. Despite the aforementioned commonalities, species-specificities in face processing should not be negated4, and a number of issues remain unaddressed. In particular, while humans show a robust preference for facial averageness (i.e., the proximity of a face to the average of a population, in terms of mathematical trait values), it is unknown whether non-human primates are sensitive to such characteristics3. In humans, computer generated composite faces, or prototypes, are appealing to adults29,30, and 6-month-olds look longer at composite faces than at faces rated as unattractive by adults31. Furthermore, typical faces are judged more attractive than distinctive faces32,33, and a meta-analysis has shown that the appeal of averageness is not restricted to face race or sex34, although it might be linked with visual experience35. Two non-mutually exclusive frameworks have been put forward to explain the attraction to average faces in humans. Preferences for attractive faces might have been shaped by sexual selection pressures, as an adaptation for mate choice, because attractiveness and its components may serve as indicators of mate quality, such as health or parasitic resistance36,37, but see ref. 38. Average traits in a face are linked with greater genetic diversity which may result in greater parasitic resistance37, whereas deviation from average could signal chromosomal disorders39, at least for lower scores of face prototypicality (i.e., the “bad genes” hypothesis40). The preference for averageness may reflect a side-effect of sensory processing and may be a by-product of the way brains process information in human adults34,41–43. That is, prototypical stimuli are more fluently processed and human adults show a robust preference for fluently processed stimuli44–46. As would be expected given the preferences, fluently processed stimuli elicit posi (...truncated)