Parental oxytocin and early caregiving jointly shape children's oxytocin response and social reciprocity

Abstract

Oxytocin (OT) has an important role in bond formation and social reciprocity, and animal studies indicate that OT functioning is transferred from parent to child through patterns of parental care. Perspectives on attachment suggest that the individual's various attachment bonds are underpinned by the oxytocinergic system. However, prospective human studies that demonstrate the cross-generation transfer of OT as mediated by early caregiving and its impact on children's multiple attachments are lacking. To address these concerns, the current study included 160 mothers and fathers and their firstborn child who participated in a 3-year longitudinal study. At the first and sixth postpartum months, parents' plasma OT was assayed, parent-infant interactions were videotaped and micro-coded, and allelic variations on the OXTR(rs2254298, rs1042778) and CD38rs3796863 genes were measured. At 3 years, parents' and child's salivary OT was assessed and children's social reciprocity observed during interactions with mother, father, and their first best friend. Parents' OT levels were individually stable across the 3-year period, correlated with low-risk OXTR and CD38 alleles, and predicted child OT. Child's social reciprocity with friend was associated with child OT levels, mother's OT-related genes and hormones, and mother-child reciprocity, but not with father's genes, hormones, or behavior. A cross-generation gene-by-environment effect emerged, with low child OT levels predicted by the interaction of maternal high-risk CD38 allele and diminished maternal care in infancy. These results demonstrate individual stability in peripheral OT across several years and describe a cross-generation transfer of OT through caregiving in humans within a prospective longitudinal design. Consistent with other mammals, biobehavioral experiences within the parent-infant bond shape children's affiliative biology and social behavior across multiple attachments. Our findings bear important implications for conditions involving disruptions to maternal-infant bonding and underscore the potential for peer-based interventions.

Figure 1

Correlations between child salivary oxytocin at 3 years with mother's (a) and father's (b) oxytocin across the first 3 years of parenthood.

Figure 2

Child social reciprocity with best friend in relation to mother's and father's cumulative OT risk. The OT risk composite includes risk alleles on the OXTR and CD38 genes and low parental OT. *p<0.05.

Figure 3

Child salivary OT at 3 years stratified by maternal CD38 gene and patterns of maternal care in Infancy. **p<0.02.

Figure 4

An overall model of the findings linking maternal and paternal genes, hormones and parenting behavior with child OT and social reciprocity.