Neonatal face-to-face interactions promote later social behaviour in infant rhesus monkeys

Abstract

In primates, including humans, mothers engage in face-to-face interactions with their infants, with frequencies varying both within and across species. However, the impact of this variation in face-to-face interactions on infant social development is unclear. Here we report that infant monkeys (Macaca mulatta) who engaged in more neonatal face-to-face interactions with mothers have increased social interactions at 2 and 5 months. In a controlled experiment, we show that this effect is not due to physical contact alone: monkeys randomly assigned to receive additional neonatal face-to-face interactions (mutual gaze and intermittent lip-smacking) with human caregivers display increased social interest at 2 months, compared with monkeys who received only additional handling. These studies suggest that face-to-face interactions from birth promote young primate social interest and competency.

ARTICLE

Received 26 Jan 2016 | Accepted 13 May 2016 | Published 14 Jun 2016

DOI: 10.1038/ncomms11940 OPEN

Neonatal face-to-face interactions promote later social behaviour in infant rhesus monkeys

Amanda M. Dettmer1,*, Stefano S.K. Kaburu1,2,*, Elizabeth A. Simpson1,3,*, Annika Paukner1, Valentina Sclafani1,4, Kristen L. Byers1, Ashley M. Murphy1, Michelle Miller1,5, Neal Marquez1,6, Grace M. Miller1,7, Stephen J. Suomi1 & Pier F. Ferrari8

In primates, including humans, mothers engage in face-to-face interactions with their infants, with frequencies varying both within and across species. However, the impact of this variation in face-to-face interactions on infant social development is unclear. Here we report that infant monkeys (Macaca mulatta) who engaged in more neonatal face-to-face interactions with mothers have increased social interactions at 2 and 5 months. In a controlled experiment, we show that this effect is not due to physical contact alone: monkeys randomly assigned to receive additional neonatal face-to-face interactions (mutual gaze and intermittent lip-smacking) with human caregivers display increased social interest at 2 months, compared with monkeys who received only additional handling. These studies suggest that face-to-face interactions from birth promote young primate social interest and competency.

1 Laboratory of Comparative Ethology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Poolesville, Maryland 20837, USA. 2 Department of Population Health and Reproduction, University of California, Davis, California 95616, USA. 3 Department of Psychology, University of Miami, Coral Gables, Florida 33146, USA. 4 Winnicott Research Unit, University of Reading, Reading RG 6AL, UK. 5 Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland 21205, USA. 6 Institute for Health Metrics and Evaluation, University of Washington, Seattle, Washington 98121, USA. 7 Clinical and School Psychology, University of Virginia, Charlottesville, Virginia 22904, USA. 8 Department of Neuroscience, University of Parma, 43125 Parma, Italy. * These authors contributed equally to this work. Correspondence and requests for materials should be addressed to A.D. (email: mailto:[email protected]

Web End [email protected] ).

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Highly social species, including human (Homo sapiens) and nonhuman primates (NHPs), evolved a variety of sociocognitive skills and behavioursincluding complex

facial expressions, grooming and playthat facilitate cooperation among group members1. In these societies, characterized by complex and extended social interactions, social competency is critical for survival and reproductive tness2. However, the mechanisms by which individuals acquire social competence early in development are not well understood.

One mechanism proposed to support early social development is face-to-face interactions35. Face-to-face interactions between newborns and caregivers occur across many human cultures6,7, and have also been reported for some NHPs (for example, chimpanzees, Pan troglodytes8; Japanese macaques, Macaca fuscata9; rhesus macaques, Macaca mulatta3), especially during or following physical separation3,5,8,10. In NHPs, face-to-face interactions include mutual gazing (MG), which is often accompanied by facial gestures such as lip-smacking3. Similar to humans11,12, NHPs show considerable variability in face-to-face interactions with newborns3,5,8, and there is evidence that disruption of the motherinfant bond in rhesus monkeys negatively impacts infants social and physiological development13. One possible mechanism for this disruption is the lack of face-to-face interactions between mother and infant. Primates, including humans, are attracted to the eye region of faces from the rst weeks of life14,15, and prefer direct gazes to other visual stimuli1619. In infant rhesus monkeys, increased visual attention to eyes is associated with other social skills such as neonatal imitation15. Face-to-face interactions offer opportunities for the infant to learn key information about the caregiver, about species-specic interactions, and about the foundations of early emotional communication3. However, what remains unclear is the extent to which sustained face-to-face interactions and their variability inuence the expression of social behaviour later in development.

We addressed this question by studying the effects of neonatal MG on the later social behaviour of infant rhesus monkeys, a highly social Old World primate species with strong mother infant bonds and social complexity in adulthood20. We predicted that, if MG is a primary driver of the development of social skills, then monkey infants who receive more MG should be more social later in development. To test this prediction, we rst observed naturally-occurring variation in motherinfant face-to-face interactions (see Supplementary Movie 1) to determine whether the quantity of face-to-face interactions predicts infants later developing social behaviour (Experiment 1). In this study, we focused on face-to-face interactions that occurred during close physical proximity because it was not possible to observe such interactions when monkeys were out of contact (see Methods section). We then carried out a second study in which infants were randomly assigned to receive varying levels of face-to-face interactions (Supplementary Movie 2) and physical contact with human caregivers in a controlled rearing environment (Experiment 2). Thus, through a combination of both naturalistic observations and experimental manipulations we were able to gain a more complete picture of the contributions of neonatal MG to the developing infants social interest and engagement in social behaviours. We report here that infants experiencing more face-to-face interactions in the rst month of life exhibit more social interest at 2 and 5 months, suggesting that face-to-face interactions from birth promote young primate social competency.

ResultsResults from studies of semi free-ranging monkeys. In Experiment 1, we studied MG in semi free-ranging rhesus monkey mothers and infants (N 10) living in a large, 2 ha

enclosure. Researchers recorded the frequency of MG between mothers and infants across the rst three months of life5, and tracked infants social behaviour (that is, social play, close proximity to other monkeys and grooming) for the rst 5 months of life (see Methods section). Infants who engaged in MG more frequently with their mothers in the rst month of life were more sociable later on: they spent more time in social contact with other monkeys at 2 months of age (Spearmans correlation; r(s) 0.68; P 0.031; Fig. 1a), and they initiated more social

interactions at 5 months of age (Spearmans correlation; r(s) 0.78; P 0.007; Fig. 1b). Infants did not preferentially

initiate social behaviours with their mothers; instead they initiated social behaviours with all types of partners: other adults, other infants, juveniles and their mothers.

Results from studies of monkeys in a controlled environment. In Experiment 2, infants were reared in a nursery by human caregivers and had continual contact with peers21. Motherinfant physical contact can promote social behaviours22,23, which may

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Figure 1 | How motherinfant face-to-face interactions inuence infant social behaviour. Results from Experiment 1 examining neonatal motherinfant face-to-face interactions and later infant social behaviour. (a) Correlation between rates of motherinfant mutual gazing in the rst month of life and time the infant spent in social contact at month 2. Rate of gazing total frequency of mutual gaze in rst 30 days/total number of

15-min sessions in rst 30 days. N 10. (b) Correlation between rates of

motherinfant mutual gazing in the rst month of life and time infants spent in social behaviours (for example, groom, play and social contact) they initiated. Rate of gazing total frequency of mutual gaze in rst

30 days/total number of 15-min sessions in rst 30 days. N 10.

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be driving the increased sociality observed in Experiment 1. We, therefore, carried out a second study to determine the extent to which increased physical contact or increased face-to-face interactions inuenced later social behaviour. We randomly assigned infants to receive standard care (N 17), increased

handling by human caregivers without face-to-face contact (caretakers faces were covered; N 15), or both increased

handling and face-to-face interactions (MG and intermittent lip-smacking; N 16), for the rst 4 weeks of life24 (see Methods

section). We then tracked infants social development with two measures across the rst 5 months of life: (1) by assessing infants preference for a social (that is, a macaque mother with her infant being groomed by another adult) versus nonsocial (that is, geometric shape) videos using an eye tracker, and (2) by measuring social behaviour during infants daily interactions with same-aged peers.

Infants who experienced additional face-to-face interactions spent more time at 2 months of age looking at the social stimulus than the nonsocial stimulus (paired sample t-test; t(15) 2.38;

P 0.031, d 0.55, Fig. 2a), whereas infants who experienced

handling-only or standard care exhibited no preference (paired sample t-test; handling-only: t(14) 0.837; P 0.416; standard

care: t(16) 0.446; P 0.661, Fig. 2a). At this age, we also found a

signicant effect of face-to-face interaction on the amount of time infants spent in social interaction with peers (analysis of variance (ANOVA); F(2,40) 4.125; P 0.023, Z2 0.141; Fig. 2b): infants

in the face-to-face condition spent more time interacting with peers (means.d. 157.536.4 s) than infants in the

handling-only (means.d. 125.445.4 s; t(29) 2.133; P 0.042,

d 0.78; post hoc t-tests) or standard care groups

(means.d. 117.1 s; t(31) 2.567, P 0.016; d 0.92; post hoc

t-tests). There was, however, no difference in social behaviour between the handling-only and standard care groups (t(29) 0.48;

P 0.635; post hoc t-tests). Although surrogate peer-reared

infants engaged in social interactions for signicantly longer (153.338.1 s) than peer-reared infants (ANOVA; 117.3 s47.7 s; F(1,40) 7.956, P 0.007, Z2 0.136), there was

no signicant effect of the interaction between treatment group (face-to-face handling, handling-only, standard-reared) and

nursery rearing condition (peer-reared, surrogate peer-reared; ANOVA; F(2,40) 1.138, P 0.331). These ndings indicate that

the effect of the stimulation on infant social behaviour is not driven by any specic rearing condition. Finally, it is possible that the infants in the face-to-face condition were more likely to seek social contact with their peers because they experienced higher levels of anxiety. However, we did not nd any effect of the face-to-face condition on rates of self-scratching (ANOVA; F(2,40) 0.361, P 0.699), time spent in ventral clinging on peers

(ANOVA; F(2,40) 2.170, P 0.127) or time in contact with the

surrogate (ANOVA; F(2,40) 1.080, P 0.349), suggesting that

the effect of face-to-face interaction on social behaviour is not due to the infants seeking reassurance from their peers or to a generalized reduction of anxiety. No group differences were observed on either measure at 5 months of age.

DiscussionOur combined observational and experimental studies demonstrate that, in both a naturalistic and a laboratory setting, early face-to-face interactions between newborn primates and their caregivers signicantly affect infants social behaviour later in development: monkeys engaging in more face-to-face interactions as newborns spend more time in social contact with conspecics, look longer at social stimuli, and initiate more social interactions. These effects do not appear to be due to increased physical contact between the newborn and caregiver, but appear to be driven by face-to-face interactions.

Interestingly, it has been reported that the frequency of motherinfant mutual gaze not involving lip-smacking predicted the amount of lip-smacking that the infants received from their mothers3. Moreover, lip-smacking by adults to infants coincides with mutual gaze3, suggesting that in order for lip-smacking to occur, mutual gaze must be occurring. While these events are difcult to record in the eld, as they require close proximity and detailed video microanalysis, this and other studies suggest they are more common in nonhuman primates than previously thought3,5, and they probably have a signicant impact on infants affective and cognitive development, as also proposed in humans25,26. Further studies are needed to assess which specic component of motherinfant face-to-face interactions play a crucial role in the development of infant macaques social skills.

All infants, including those who are not exposed to a high rate of lip-smacking from their own mothers, are likely to experience these mutual interactions with other individuals of the social group, which may explain why infants who were not observed to receive face-to-face interactions with their mothers do not show gross social dysfunctions. This seems particularly true after the rst month of life, when such mutual exchanges between macaque mothers and infants dramatically decrease3. Indeed, typically reared infant rhesus macaques become more independent after their rst month of life, when their interest in and proximity to same-age peers and other individuals within the troop steadily increase27. By 6 months of age, infants typically spend the majority of their daytime hours away from their mothers and engaged with peers in social interactions27.

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Figure 2 | Face-to-face interactions, but not extra handling, inuence social development. Results from Experiment 2: (a) Effect of face-to-face handling treatment on average time looking at social (orange) versus

nonsocial/abstract (blue) stimuli during the eyetracking task at 2 months, and (b) effect of face-to-face handling treatment on average time spent in

social contact with peers at two months. Face-to-face handling, N 16;

Handling, N 15; Standard care, N 17. *Po0.05. Error bars reect s.e.m.

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Previous work demonstrated that infant monkeys randomly assigned to receive more face-to-face interactions (mutual gaze and lip-smacking) were more likely to imitate facial gestures at one week of age, compared to infants who did not receive these additional interactions24. The present ndings suggest that these face-to-face interactions may have even longer-lasting effects on infant social behaviour beyond the newborn period. However, the controlled experiment revealed no signicant effects of the face-to-face interaction on social behaviour with peers beyond the second month of life, while the eld experiment showed effects at ve months. This discrepancy is likely due to the fact that in the eld face-to-face interactions between mothers and infants continue well beyond the rst month of life5. In contrast, in the controlled setting, the intervention only lasted for the rst month of life. It is likely that continuing the face-to-face interactions would have resulted in longer-lasting social effects in the nursery group as well.

There was considerable natural variability in the extent to which mothers in the eld interacted with their infants: only about half of the mothers were observed engaging in these face-to-face interactions, consistent with previous reports3,5,8. Those infants whose mothers were not observed to engage in face-to-face interactions with them nonetheless went on to develop normally. That is, there did not seem to be any obvious dysfunction in these mother-raised infants as a function of not having high rates of mutual gaze with their mother as neonates, at least during the rst 5 months of life. Furthermore, because we did not observe such interactions it does not mean they did not occur; interactions may have occurred at times in which they were not observed or may have been subtle or difcult to detect in this context. Nonetheless, these ndings suggest that for some dyads, such motherneonate interactions may be quite rare, and perhaps there may be other causes of variability in these interactions besides human interference (for example, maternal experience and infant sex5).

It is not yet clear what the mechanisms are underlying the differential social behaviour for infants receiving variable early caregiving. One possibility is that variability in face-to-face interactions may modulate the activation of the oxytocin system28, as oxytocin is a neuropeptide that plays a key role in motherinfant bonding and promotes afliative relationships29 and that may inuence downstream social development30. Recent work has shown that endogenous oxytocin in children can be increased through parental contact29 and that exogenous oxytocin increases eye contact in humans with and without autism31. It is, therefore, possible that different levels of oxytocin in infants and/or in caregivers inuence the frequency of face-to-face interactions, or vice versa, which might ultimately promote differential levels of social engagement29. In support of this, aerosolized oxytocin increases afliative behaviour in newborn macaques, especially among infants with stronger social skills, suggesting oxytocin may amplify infants intrinsic social interest30.

Our data suggest that the development of sophisticated social interactions and complex social systems might have been an important factor driving the evolution of motherinfant social gazing. Individuals living in a stable social group need to employ advanced social skills both to coordinate their own behaviours with the behaviours of other group members, and to solve direct and indirect conicts that originate from competition over resources32. The primate species in which mutual gazing has been reported to date, namely macaques (for example, rhesus macaques3; Japanese macaques9), geladas (Thereopithecus gelada33), chimpanzees8 and humans10,11, are all highly social species characterized by multi-male multi-female social systems. Interestingly, in these species, individuals use social tactics to

secure access to resources and increase their reproductive success34,35. We suggest that, in these species, the acquisition of social skills starts in infancy, since being able to learn these skills from caregivers through, for instance, face-to-face interactions promotes social competence, which is critical for survival in adulthood in complex societies32.

Methods

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

Experiment 1. Rhesus monkey motherinfant dyads (N 10; 4 male infants) were

born and raised at the Laboratory of Comparative Ethologys ve-acre eld 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 B80 monkeys has been well characterized5,36. Mothers and infants were undisturbed for the duration of the study.

Three observers recorded motherinfant interactions, trained to 485% 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 rst 30 days of the infants life; three times per week during days 3160; and once per week during days 6190. We coded dyads for 15 min, and sessions were coded from the infants 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, dened 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 30180 for all occurrences of behaviours using focal animal observations5,37. From days 3060, 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 arms 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 rst month of life. We calculated average durations and frequencies of each of the social behaviours for each month between 26 months. We used Spearmans 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 Spearmans 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 outtted with

cloth-covered surrogates and given daily 2-h play sessions (surrogate-peer-reared), beginning at B40 days of age. Before this time, infants were housed in an incubator for the rst 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 B5 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, afliative behaviour mother rhesus macaques direct to their infants during face-to-face interactions3 and infants imitate LPS in the rst week of life40. In the HDL condition, a human caregiver held the infants for the same duration (5 min),

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but wore a face cover to prevent the infants from seeing the caregivers face. For the rst 2 weeks of life, we administered both FF and HDL four times per day(at B10:00, B12:00, B14:00 and B18:00 hours) during weekdays and twice per day on the weekend (at B10:00 and B12:00 hours). In the third week of life, we administered FF and HDL three times per day (at B10:00, B12:00 and B14:00 hours) and once per day on weekends (at B10:00 hours), while in the fourth week of life we administered FF and HDL twice per day (at B10:00 and B12:00) during weekdays and once per day on weekends (at B10:00 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 motherinfant face-to-face interactions across development3.

At 4050 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 reection using a Tobii T60XL (n 38) or a Tobii TX300

(n 10) eye tracker and a sampling rate Z60 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 ve-point calibration to Tobii Studios 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 149246 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 arms 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 ones own hair or skin with ngernails 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 xation durations using the Tobii lter 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 rst introduced to the social group, and 60 days) and (2) at5 months (that is, 121150 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 oneway 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 ndings of this study are available within the articles supplementary les (Supplementary Data 1 and 2).

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Acknowledgements

This work was supported by NICHD Division of Intramural Research and NICHD grant PO1HD064653 (P.F.F.). We are grateful to the animal care and veterinary staff at the NIH Animal Center.

Author contributions

A.M.D. designed Experiment 1. P.F.F., E.A.S., A.P. and V.S. designed Experiment 2. A.M.D., K.L.B. and A.M.M. collected the data for Experiment 1, led by A.M.D. E.A.S,V.S., A.P., K.L.B., A.M.M., M.M., N.M., G.M. and S.S.K.K. carried out the neonatal

interventions in Experiment 2, lead by E.A.S. A.P. and G.M. collected the eyetracking data in Experiment 2. K.L.B., M.M. and N.M. carried out behavioural scoring for Experiment 2. A.M.D. and S.S.K.K. analysed the data and produced the graphs. A.M.D., S.S.K.K., E.A.S., A.P. and P.F.F. drafted the manuscript. S.J.S. and P.F.F. provided resources for the studies. All authors edited and approved the nal version of the manuscript.

Additional information

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Competing nancial interests: The authors declare no competing nancial interests.

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How to cite this article: Dettmer, A. M. et al. Neonatal face-to-face interactions promote later social behaviour in infant rhesus monkeys. Nat. Commun. 7:11940 doi: 10.1038/ncomms11940 (2016).

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