Ruth Feldman

Evidence for a Neuroendocrinological Foundation of Human Affiliation Plasma Oxytocin Levels Across Pregnancy and the Postpartum Period Predict Mother-Infant Bonding

Although research on the neurobiological foundation of social affiliation has implicated the neuropeptide oxytocin in processes of maternal bonding in mammals, there is little evidence to support such links in humans. Plasma oxytocin and cortisol of 62 pregnant women were sampled during the first trimester, last trimester, and first postpartum month. Oxytocin was assayed using enzyme immunoassay, and free cortisol was calculated. After the infants were born, their interactions with their mothers were observed, and the mothers were interviewed regarding their infant-related thoughts and behaviors. Oxytocin was stable across time, and oxytocin levels at early pregnancy and the postpartum period were related to a clearly defined set of maternal bonding behaviors, including gaze, vocalizations, positive affect, and affectionate touch; to attachment-related thoughts; and to frequent checking of the infant. Across pregnancy and the postpartum period, oxytocin may play a role in the emergence of behaviors and mental representations typical of bonding in the human mother.

Mother-infant affect synchrony as an antecedent of the emergence of self-control.

This study examined relations between mother-infant affect synchrony and the emergence of childrens self-control. Mother-infant face-to-face play and infant difficult temperament were examined at 3 and 9 months. Maternal and infant affective states at play were coded in 0.25-s frames, and synchrony was computed with cross-correlation functions. Self-control, verbal IQ, and maternal warm discipline were assessed at 2 years. Maternal synchrony with infant affect at 3 months (infant-leads-mother-follows relation) and mutual synchrony at 9 months (cross-dependence between maternal and infant affect) were each related to self-control at 2 years when temperament, IQ, and maternal style were partialed. Infant temperament moderated the relations of synchrony and self-control, and closer associations were found between mutual synchrony and self-control for difficult infants. Shorter lags to maternal synchrony at 3 months were independently related to self-control. The mutual regulation of affect in infancy, as moderated by temperament, is proposed as an important contributor to the emergence of self-regulation.

Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent–infant contact

Animal studies have demonstrated that the neuropeptide oxytocin (OT) plays a critical role in processes of parent-infant bonding through mechanisms of early parental care, particularly maternal grooming and contact. Yet, the involvement of OT in human parenting remains poorly understood, no data are available on the role of OT in the development of human fathering, and the links between patterns of parental care and the OT response have not been explored in humans. One hundred and twelve mothers and fathers engaged in a 15-min play-and-contact interaction with their 4-6-month-old infants and interactions were micro-coded for patterns of parental touch. Results showed that baseline levels of plasma and salivary OT in mothers and fathers were similar, OT levels in plasma and saliva were inter-related, and OT was associated with the parent-specific mode of tactile contact. Human mothers who provided high levels of affectionate contact showed an OT increase following mother-infant interaction but such increase was not observed among mothers displaying low levels of affectionate contact. Among fathers, only those exhibiting high levels of stimulatory contact showed an OT increase. These results demonstrate consistency in the neuroendocrine basis of human parental interactions with those seen in other mammals. The findings underscore the need to provide opportunities for paternal care to trigger the biological basis of fatherhood and suggest that interventions that permit social engagement may be recommended in conditions of diminished maternal-infant contact, such as prematurity or postpartum depression.

Oxytocin and social affiliation in humans.

A conceptual model detailing the process of bio-behavioral synchrony between the online physiological and behavioral responses of attachment partners during social contact is presented as a theoretical and empirical framework for the study of affiliative bonds. Guided by an ethological behavior-based approach, we suggest that micro-level social behaviors in the gaze, vocal, affective, and touch modalities are dynamically integrated with online physiological processes and hormonal response to create dyad-specific affiliations. Studies across multiple attachments throughout life are presented and demonstrate that the extended oxytocin (OT) system provides the neurohormonal substrate for parental, romantic, and filial attachment in humans; that the three prototypes of affiliation are expressed in similar constellations of social behavior; and that OT is stable over time within individuals, is mutually-influencing among partners, and that mechanisms of cross-generation and inter-couple transmission relate to coordinated social behavior. Research showing links between peripheral and genetic markers of OT with concurrent parenting and memories of parental care; between administration of OT to parent and infants physiological readiness for social engagement; and between neuropeptides and the online synchrony of maternal and paternal brain response in social-cognitive and empathy networks support the hypothesis that human attachment develops within the matrix of biological attunement and close behavioral synchrony. The findings have conceptual implications for the study of inter-subjectivity as well as translational implications for the treatment of social disorders originating in early childhood, such as autism spectrum disorders, or those associated with disruptions to early bonding, such as postpartum depression or child abuse and neglect. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.

Maternal Depression and Anxiety Across the Postpartum Year and Infant Social Engagement, Fear Regulation, and Stress Reactivity

OBJECTIVE To examine the effects of maternal depression on infant social engagement, fear regulation, and cortisol reactivity as compared with maternal anxiety disorders and controls and to assess the role of maternal sensitivity in moderating the relations between maternal depression and infant outcome. METHOD Using an extreme-case design, 971 women reported symptoms of anxiety and depression after childbirth and 215 of those at the high and low ends were reevaluated at 6 months. At 9 months, mothers diagnosed with a major depressive disorder (n = 22) and anxiety disorders (n = 19) and matched controls reporting no symptoms across the postpartum year (n = 59) were visited at home. Infant social engagement was observed during mother-infant interaction, emotion regulation was microcoded from a fear paradigm, and mothers and infants cortisol were sampled at baseline, reactivity, and recovery. RESULTS The infants of depressed mothers scored the poorest on all three outcomes at 9 months-lowest social engagement, less mature regulatory behaviors and more negative emotionality, and highest cortisol reactivity-with anxious dyads scoring less optimally than the controls on maternal sensitivity and infant social engagement. Fear regulation among the children of anxious mothers was similar to that of the controls and their stress reactivity to infants of depressed mothers. Effect of major depressive disorder on social engagement was moderated by maternal sensitivity, whereas two separate effects of maternal disorder and mother sensitivity emerged for stress reactivity. CONCLUSIONS Pathways leading from maternal depression to infant outcome are specific to developmental achievement. Better understanding of such task-specific mechanisms may help devise more specifically targeted interventions.

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

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.

Sensitive parenting is associated with plasma oxytocin and polymorphisms in the OXTR and CD38 genes.

BACKGROUND Research in mammals has demonstrated the involvement of oxytocin (OT) in social bond formation; yet, its role in human bonding remains unclear. Plasma OT has been used as a proxy for central activity and studies indicate its association with human affiliative behaviors. Molecular genetic studies also reveal a role for OT neuropathways in shaping the social brain. However, the links between peripheral OT, genetic markers, and their combined contribution to human parenting are unknown. METHODS Participants included 352 individuals: 272 mothers and fathers and their 4- to 6-month-old-infants and 80 nonparents. Plasma OT was assayed from adults who were genotyped for oxytocin receptor (OXTR) and CD38 risk alleles associated with social dysfunctions. CD38 is an ectoenzyme that mediates the release of brain OT. Parent-infant interactions were microcoded for parental touch and gaze synchrony and participants reported on parental care in childhood. RESULTS OXTR (rs2254298 and rs1042778) and CD38 (rs3796863) risk alleles were each associated with lower plasma OT. Reduced plasma OT and both OXTR and CD38 risk alleles were related to less parental touch. The interaction of high plasma OT and low-risk CD38 alleles predicted longer durations of parent-infant gaze synchrony. Parents reporting greater parental care showed higher plasma OT, low-risk CD38 alleles, and more touch toward their infants. CONCLUSIONS Results indicate that peripheral and genetic markers of the extended OT pathway are interrelated and underpin core behaviors associated with human parenting and social engagement. These findings may have important implications for understanding neuropsychiatric disorders marked by early social dysfunctions.

Parent–Infant Synchrony: Biological Foundations and Developmental Outcomes

Synchrony—a construct used across multiple fields to denote the temporal relationship between events—has been applied to the study of mother–infant interaction and is suggested here as a framework for the study of interpersonal relationships. Defined as the temporal coordination of micro-level social behavior, parent–infant synchrony is charted in its development across infancy from the initial consolidation of biological rhythms during pregnancy to the emergence of symbolic exchange between parent and child. Synchrony is shown to depend on physiological mechanisms supporting bond formation in mammals—particularly physiological oscillators and neuroendocrine systems such as those involving the hormone oxytocin. Developmental outcomes of the synchrony experience are observed in the domains of self-regulation, symbol use, and the capacity for empathy across childhood and adolescence. Specific disruptions to the parameters of synchrony that may be observed in various pathological conditions, such as prematurity or maternal affective disorder, are detailed. A time-based, micro-analytic behavioral approach to the study of human relationship may offer new insights on intersubjectivity across the lifespan.

Oxytocin during pregnancy and early postpartum: Individual patterns and maternal–fetal attachment

Oxytocin (OT), a nanopeptide hormone, plays a role in the emergence of maternal behavior, yet few studies examined OT in humans across pregnancy and the postpartum. We followed healthy women at three points: first trimester of pregnancy, third trimester, and first postpartum month. Plasma OT levels showed high individual stability. A third of the sample showed consistent OT levels, whereas others showed increasing or decreasing trends or peak in late pregnancy. The increase in OT from early to late pregnancy correlated with higher maternal-fetal bonding. These data may help set standards for OT levels and underscore links with maternal-infant attachment.

Testing a family intervention hypothesis: The contribution of mother-infant skin-to-skin contact (kangaroo care) to family interaction, proximity, and touch.

The provision of maternal-infant body contact during a period of maternal separation was examined for its effects on parent-infant and triadic interactions. Participants were 146 three-month-old preterm infants and their parents, half of whom received skin-to-skin contact, or kangaroo care (KC), in the neonatal nursery. Global relational style and micro-patterns of proximity and touch were coded. Following KC, mothers and fathers were more sensitive and less intrusive, infants showed less negative affect, and family style was more cohesive. Among KC families, maternal and paternal affectionate touch of infant and spouse was more frequent, spouses remained in closer proximity, and infant proximity position was conducive to mutual gaze and touch during triadic play. The role of touch as a constituent of the co-regulatory parent-infant and triadic systems and the effects of maternal contact on mothering, co-parenting, and family processes are discussed.