Inhaled oxytocin increases positive social behaviors in newborn macaques

Abstract

Early caregiver-infant interactions are critical for infants' socioemotional and cognitive development. Several hormones and neuromodulators, including oxytocin, affect these interactions. Exogenous oxytocin promotes social behaviors in several species, including human and nonhuman primates. Although exogenous oxytocin increases social function in adults--including expression recognition and affiliation--it is unknown whether oxytocin can increase social interactions in infants. We hypothesized that nebulized oxytocin would increase affiliative social behaviors and such effects would be modulated by infants' social skills, measured earlier in development. We also hypothesized that oxytocin's effects on social behaviors may be due to its anxiolytic effects. We tested these hypotheses in a blind study by nebulizing 7- to 14-d-old macaques (n = 28) with oxytocin or saline. Following oxytocin administration, infants' facial gesturing at a human caregiver increased, and infants' salivary oxytocin was positively correlated with the time spent in close proximity to a caregiver. Infants' imitative skill (measured earlier in development: 1-7 d of age) predicted oxytocin-associated increases in affiliative behaviors--lip smacking, visual attention to a caregiver, and time in close proximity to a caregiver--suggesting that infants with higher propensities for positive social interactions are more sensitive to exogenous oxytocin. Oxytocin also decreased salivary cortisol, but not stress-related behaviors (e.g., scratching), suggesting the possibility of some anxiolytic effects. To our knowledge, this study provides the first evidence that oxytocin increases positive social behaviors in newborns. This information is of critical importance for potential interventions aimed at ameliorating inadequate social behaviors in infants with higher likelihood of developing neurodevelopmental disorder.

Keywords: imitation recognition; individual differences; neonatal imitation.

Fig. 1.

Saliva analysis for oxytocin and cortisol levels, 2 and 4 h after nebulization with either saline control or oxytocin. For salivary oxytocin (light bars; left axis), there was a main effect of condition (Oxytocin > Saline Control) [F_(1,13) = 8.95, P = 0.010, η_p² = 0.408]. For salivary cortisol (dark bars; right axis), there was an effect at 2 h postnebulization (saline control > oxytocin) [t₍₈₎ = 2.97, P = 0.018, d = 0.99], but no effect at 4 h postnebulization [t₍₁₂₎ = 1.28, P = 0.225]. Error bars reflect SEM. *P < 0.05.

Fig. 2.

Infants’ lip smacking (LPS) and tongue protrusion (TP) gesture rates in the imitation recognition task (imitation and still-face periods combined), nebulized with either saline or oxytocin. These data are averaged across time postnebulization (1 and 2 h after nebulization). There was a main effect of condition (oxytocin > saline control) [F_(1,26) = 5.96, P = 0.022, η_p² = 0.186]. Error bars reflect SEM. *P = 0.014, **P = 0.029.

Fig. 3.

Associations between imitative skill and behavioral changes due to oxytocin. Scatter plots reflect the association between the strength of infants’ lip smacking (LPS) imitation in the first week of life (x axis) and the change in behaviors as a consequence of oxytocin administration (y axis: saline control condition subtracted from oxytocin condition; 0 indicates no changes as a consequence of oxytocin) during the imitation recognition task in the second week of life, for (A) the frequency of LPS, (B) time (in seconds) in close proximity to the caregiver, and (C) time (in seconds) looking at the caregiver.

Fig. 4.

Infant during nebulization procedure.