Ethical approval

All procedures were approved by the NICHD Animal Care and Use Committee.

Experiment 1

Rhesus monkey mother–infant dyads (N=10; 4 male infants) were born and raised at the Laboratory of Comparative Ethology’s five-acre field station and the NIH Animal Center in Poolesville, Maryland. We studied dyads in the birth seasons (spring and summer) of 2013 and 2014. This semi free-ranging population of ∼80 monkeys has been well characterized5,36. Mothers and infants were undisturbed for the duration of the study.

Three observers recorded mother–infant interactions, trained to >85% reliability according to the methods detailed by Ferrari et al3,5. We conducted live focal animal observations5,37 between 09:00 and 17:00 hours, one to two times per day, 5 days per week for the first 30 days of the infant’s life; three times per week during days 31–60; and once per week during days 61–90. We coded dyads for 15 min, and sessions were coded from the infant’s perspective. We discarded sessions if the focal animals moved out of sight or if either the mother or infant fell asleep for over 50% of the session5. We recorded the frequencies of mutual gazing, defined as eye-to-eye contact between mother and infant lasting at least 3 s (Supplementary Movie 1), in each 15-min session.

We observed infants from days 30–180 for all occurrences of behaviours using focal animal observations5,37. From days 30–60, infants were coded twice per week for 20 min each session; from day 60 onwards infants were coded weekly for 30 min each session. We recorded behaviours on a MobileDemand xTablet T7200 (Hiawatha, Iowa, USA) using JWatcher software38. For this study, the following behaviours were coded as initiated or received by the infant:

1 Social play: play face, non-aggressive chasing, tagging, swatting, bobbing, biting, pulling, lunging, mouthing or wrestling (rough and tumble) directed towards another animal. 2 Social contact: in physical contact or within arm’s reach of another animal. 3 Social grooming: cleaning/picking/stroking hair.

We calculated the average rates of mutual gazing between mother and infant for the first month of life. We calculated average durations and frequencies of each of the social behaviours for each month between 2–6 months. We used Spearman’s correlations to relate mutual gazing with durations of each of the behaviours at each month of age. In addition, we calculated a composite ‘initiate social’ score for each month (that is, from 2 to 6 months) by averaging the durations of all social behaviour (social play+social contact+grooming) that the infant initiated. We again used Spearman’s correlations to relate mutual gazing with the initiation of social behaviours at each month of age. We ran these latter correlations for interactions between infants and all other social partners, and for interactions between infants and separate classes of social partners (that is, mother, adult female, adult male, juvenile and other infant).

Experiment 2

Infant rhesus macaques (N=48; 27 males) were raised in a nursery from the day of birth following established procedures in our laboratory30,39,40. For unrelated projects, some infants (N=28) were reared in groups of four (peer-reared), while others (N=20) were reared in single cages outfitted with cloth-covered surrogates and given daily 2-h play sessions (surrogate-peer-reared), beginning at ∼40 days of age. Before this time, infants were housed in an incubator for the first 14 days of life, then transferred to a single cage until group formation. The single cages were all contained in the same room so that infants had constant visual and auditory contact with one another.

On the day of birth, we randomly assigned infants to one of the three conditions. In two of these conditions infants received additional daily stimulation: a face-to-face+handling condition (FF, N=16) and a handling-only (HDL, N=15) condition. We compared these stimulated infants with a standard-reared control group (SR, N=17), who received no additional social interactions beyond standard rearing39,40. Each stimulation session was carried out by one of approximately a dozen different caregivers, so that infants did not form an attachment to any one experimenter.

In the FF condition, a human caregiver attempted to engage the infant in mutual gaze and, on doing so, directed lip-smacking gestures (LPS) at the infant for ∼5 s, followed by a 10-second neutral still-face period (Supplementary Movie 2). This LPS-still period was repeated every 30 s, for a total face-to-face interaction lasting 5 min per session. We chose LPS because it is a common, affiliative behaviour mother rhesus macaques direct to their infants during face-to-face interactions3 and infants imitate LPS in the first week of life40. In the HDL condition, a human caregiver held the infants for the same duration (5 min), but wore a face cover to prevent the infants from seeing the caregiver’s face. For the first 2 weeks of life, we administered both FF and HDL four times per day (at ∼10:00, ∼12:00, ∼14:00 and ∼18:00 hours) during weekdays and twice per day on the weekend (at ∼10:00 and ∼12:00 hours). In the third week of life, we administered FF and HDL three times per day (at ∼10:00, ∼12:00 and ∼14:00 hours) and once per day on weekends (at ∼10:00 hours), while in the fourth week of life we administered FF and HDL twice per day (at ∼10:00 and ∼12:00) during weekdays and once per day on weekends (at ∼10:00 hours). The purpose of this gradual reduction in sessions was to prevent infants from growing accustomed to regular stimulation that would end abruptly, and to mimic naturally-occurring declines in mother–infant face-to-face interactions across development3.

At 40–50 days of age (median=41 days), we tested infants in an eyetracking task to assess preference for social interactions. We recorded infants’ eye movements via corneal reflection using a Tobii T60XL (n=38) or a Tobii TX300 (n=10) eye tracker and a sampling rate ≥60 Hz. We used Tobii Studio software (Tobii Technology, Sweden) to collect and summarize the data.

One experimenter held each infant ca. 65 cm in front of the screen, swaddled in a soft blanket. We calibrated each infant using a five-point calibration to Tobii Studio’s pre-set locations. Infants viewed one 30-s video (Supplementary Movie 3) that depicted a social monkey scene on one side (a macaque mother with her infant being groomed by another adult) and a nonsocial scene on the other side (abstract shapes continuously moving across the screen). Location of the social scene was counterbalanced (left/right) between infants. We repeated the task when infants were 149–246 days (median=161 days); one infant was not re-tested at this older age for non-experimental reasons.

We observed infants in their social groups (that is, during play sessions in the case of peer-reared infants) twice per week, once in the morning and once in the afternoon, using 5-min focal animal sessions37. We recorded the following interactions:

1 Social contact: when the infant was either in physical contact or in close proximity (within arm’s reach) of a peer. 2 Play: play behaviours that included play face, non-aggressive chasing, tagging, swatting, bobbing, biting, pulling, lunging, mouthing and wrestling (rough and tumble). 3 Social grooming: cleaning/picking/stroking hair. 4 Self-scratches: raking one's own hair or skin with fingernails including large movements of arm. 5 Ventral clinging: ventral contact with peers. 6 Surrogate: time spent inside the surrogate.

We collected data on self-scratching, ventral clinging and time spent in the surrogate, as these are considered reliable indicators of anxiety41.

For the eyetracking task, we drew areas of interest for each side of the screen. We extracted total fixation durations using the Tobii filter in Tobii Studio (velocity: 35 pixels per window; distance threshold: 35 pixels). We calculated a preference score for the social video (social /(social+nonsocial)) and compared the amount of time infants looked at the social versus the nonsocial stimuli using a paired sample t-test.

For social interactions, we created a composite social score by taking the average time infants spent in social contact, play and grooming. This social score, as well as mean rates of self-scratching, ventral clinging and time spent in the surrogate were calculated at two different time points: (1) at 2 months (that is, between 36 days, when infants were first introduced to the social group, and 60 days) and (2) at 5 months (that is, 121–150 days). We could not include two infants (one in the FF and one in the SR condition) at 2 months, because they were introduced to the social group when they were older than 2 months. For each time point, we ran one-way ANOVAs that included the behaviour of interest as dependent variable, with condition (FF, HDL and SR), rearing (peer-reared, surrogate-peer-reared) and their interaction as independent variables, and post hoc t-tests to conduct pair-wise comparisons.

Data availability statement

The authors declare that the data supporting the findings of this study are available within the article’s supplementary files (Supplementary Data 1 and 2).