Rhesus monkeys show human-like changes in gaze following across the lifespan

Abstract

Gaze following, or co-orienting with others, is a foundational skill for human social behaviour. The emergence of this capacity scaffolds critical humanspecific abilities such as theory of mind and language. Non-human primates also follow others' gaze, but less is known about how the cognitive mechanisms supporting this behaviour develop over the lifespan. Here we experimentally tested gaze following in 481 semi-free-ranging rhesus macaques (Macaca mulatta) ranging from infancy to old age. We found that monkeys began to follow gaze in infancy and this response peaked in the juvenile periodsuggesting that younger monkeys were especially attuned to gaze information, like humans. After sexual maturity, monkeys exhibited human-like sex differences in gaze following, with adult females showing more gaze following than males. Finally, older monkeys showed reduced propensity to follow gaze, just as older humans do. In a second study (n ¼ 80), we confirmed that macaques exhibit similar baseline rates of looking upwards in a control condition, regardless of age. Our findings indicate that-despite important differences in human and non-human primate life-history characteristics and typical social experiences-monkeys undergo robust ontogenetic shifts in gaze following across early development, adulthood and ageing that are strikingly similar to those of humans.

Acute oxytocin improves memory and gaze following in male but not female nursery-reared infant macaques

“…In fact, sex differences in sociality are widespread not only among humans, but throughout mammals, indicating possible evolutionary roots (Christov-Moore et al 2014). Furthermore, a recent study of a large sample of rhesus macaques ( n =481) reported female macaques were more likely to gaze-follow than males (Rosati et al 2016), consistent with our findings. Interestingly, these sex differences were evident across a wide variety of ages, from infancy through adulthood, and grew larger with age, paralleling findings in humans (e.g., Bayliss et al, 2005; Deaner et al 2007).…”

Tolerant Barbary macaques maintain juvenile levels of social attention in old age, but despotic rhesus macaques do not

“…1. Rhesus data were partially reported in previous work (see Study 2 in Rosati et al, 2016). Both populations are semi-free-ranging and highly habituated to humans.…”

“…The demonstrator, experimenter 1 (E1), first attracted the monkey’s attention to her face (by calling ‘monkey’ and/or clapping her hands). When the monkey was looking, E1 said ‘now’ and then looked straight up or down, rotating her entire head with her eyes open for 10 s (following the same procedure in Rosati et al (2016) (see Supplementary Material 1, Fig. S1).…”

“…Consequently, patterns of cognitive development provide a second test of the relationship between social tolerance and social cognition. While some prior work has examined the emergence of gaze following within a single primate species (Rosati, Arre, Platt, & Santos, 2016; Simpson, Miller, Ferrari, Suomi, & Pauker, 2015; Teufel, Gutmann, Pirow, & Fischer, 2010; Tomasello, Hare, & Fogleman, 2001), no study has directly compared life span patterns of social attention across different primates. Moreover, qualitative comparisons of different species’ ontogenetic patterns in different studies are also somewhat contradictory.…”

“…Moreover, qualitative comparisons of different species’ ontogenetic patterns in different studies are also somewhat contradictory. Rhesus macaques show high levels of gaze following in the juvenile period that declines with age (Rosati et al, 2016; Tomasello et al, 2001). Yet pigtail macaques, Macaca nemestrina , which are somewhat more tolerant than rhesus macaques (Thierry, 2007), exhibit relatively delayed development of gaze following and have been hypothesized to need more social experience to acquire this skill (Ferrari, Coude, Gallese, & Fogassi, 2008; Ferrari, Kohler, Fogassi, & Gallese, 2000).…”