Development of Gaze Following in Infant Rhesus Macaques (Macaca mulatta)
Gaze following represents a foundational behavior for establishing joint attention and higher-level social cognition (Emery, 2000). Atypical gaze following has been reported in children with Autism Spectrum Disorder and Williams Syndrome (Riby et al., 2013; Lord et al., 2012; Mundy, 2017). To advance our understanding of mechanisms underlying the development of gaze following, rhesus macaques offer an ideal model system: they develop rich and complex social behaviors from infancy onward, similar to humans, and their behavior may help elucidate sensitive periods in the development of gaze following and its neural substrates. Although studies have shown gaze following in older primates living in natural habitats (Maestripieri & Wallen, 1997; Redican, 1975), and a study of semi-free-ranging animals suggests that gaze following emerges by 6-7 months (Rosati et al., 2016), the development of this skill and of its neural underpinning is not well understood.
To study the longitudinal development of gaze following in mother-reared infant rhesus macaques raised in semi-naturalistic groups that allow for typical emergence of rich social behavior.
Twenty-three infant male rhesus macaques were tested every 2 weeks from 2-24 weeks to obtain densely-sampled measures. Gaze following was measured via eye-tracking technology with procedures similar to those used in human infant eye-tracking studies, facilitating interspecies comparisons (Jones & Klin, 2013). Infants viewed semi-naturalistic videos of unfamiliar adult and juvenile male and female macaques. Gaze following comprising of an initial look to the eyes of the onscreen monkey—a moment of “mutual eye contact” when the onscreen monkey was looking directly at the viewer (see Figure 1A)—followed by a gaze shift in the direction in which the onscreen animal subsequently looked (see Figure 1B).
At 1 month, infants looked at the eyes during 22% (±2) of presented mutual gaze cues (mean (±sem)), then engaged in gaze following 57% (±5) of the time. By the 3rd month, infants increased attention to mutual gaze cues, looking at 36% (±2) of presented cues, and engaged in gaze following 57% (±4) of the time. Attention to mutual gaze cues and subsequent gaze following reached a peak at 4 months, looking at 41% (±3) of mutual gaze cues and following gaze 70% (±4) of the time. Thereafter, attention to mutual gaze cues and gaze following decreased to 30% (±7) and 46% (±3) at 5 months.
Steady increase in attention to mutual gaze cues suggests important changes in infants’ awareness of the social saliency of conspecifics’ eyes. At 4 months, the peak in attention to mutual gaze cues and subsequent gaze following suggests significant maturation in social-visual attention and social motivation. The decrease in these skills after 4 months coincides with the beginning of the weaning process (Fooden, 2000), leading to higher reactivity to mutual gaze (a threatening gesture in macaques) and increase in appeasement gestures (i.e. gaze avoidance). In future research, neuroimaging data obtained in the same animals will allow us to connect these shifts with changes in brain development.