Ilanit Gordon

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.

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.

Oxytocin enhances brain function in children with autism

Significance This article presents our discovery that intranasal administration of oxytocin enhances activity in the brain for socially meaningful stimuli and attenuates its response to nonsocially meaningful stimuli in children with autism spectrum disorder (ASD) as measured via functional MRI. We also identified a relationship between changes in salivary oxytocin following administration and enhancements in brain function. These discoveries are particularly important given the urgent need for treatments that target the core social dysfunction in ASD. The functional neural attunement we demonstrated might facilitate social learning, thus potentially bringing about long-term change in neural systems and subsequent behavioral improvements. Our results illustrate the power of a translational neuroscience approach to facilitate the development of pharmacological interventions for neurodevelopmental disorders like ASD. Following intranasal administration of oxytocin (OT), we measured, via functional MRI, changes in brain activity during judgments of socially (Eyes) and nonsocially (Vehicles) meaningful pictures in 17 children with high-functioning autism spectrum disorder (ASD). OT increased activity in the striatum, the middle frontal gyrus, the medial prefrontal cortex, the right orbitofrontal cortex, and the left superior temporal sulcus. In the striatum, nucleus accumbens, left posterior superior temporal sulcus, and left premotor cortex, OT increased activity during social judgments and decreased activity during nonsocial judgments. Changes in salivary OT concentrations from baseline to 30 min postadministration were positively associated with increased activity in the right amygdala and orbitofrontal cortex during social vs. nonsocial judgments. OT may thus selectively have an impact on salience and hedonic evaluations of socially meaningful stimuli in children with ASD, and thereby facilitate social attunement. These findings further the development of a neurophysiological systems-level understanding of mechanisms by which OT may enhance social functioning in children with ASD.

Oxytocin and cortisol in romantically unattached young adults: associations with bonding and psychological distress.

Despite extensive research on the involvement of oxytocin (OT) in mammalian bonding, less is known about its role in human social affiliation across the life cycle. Forty-five romantically unattached young adults participated. Plasma oxytocin and salivary cortisol were assessed using enzyme immuno-assay, and self-report measures of bonding, attachment, anxiety, and depression were collected. Oxytocin was associated with bonding to own parents and inversely related to psychological distress, particularly depressive symptoms. Cortisol was related to attachment anxiety. Regression analysis indicated that the adults representations of bonding to parents predicted OT levels above and beyond cortisol, psychological distress, and attachment. Findings are consistent with antistress models of oxytocin and suggest that oxytocin may play a role in bonding-related cognitions across the life span.

The cross-generation transmission of oxytocin in humans

Animal studies demonstrated that the neuropeptide oxytocin (OT), implicated in bond formation across mammalian species, is transmitted from mother to young through mechanisms of early social experiences; however, no research has addressed the cross-generation transmission of OT in humans. Fifty-five parents (36 mothers and 19 fathers) engaged in a 15-min interaction with their infants. Baseline plasma OT was sampled from parents and salivary OT was sampled from parents and infants before and after play and analyzed with ELISA methods. Interactions were micro-coded for parent and childs socio-affective behavior. Parent and infants salivary OT was individually stable across assessments and showed an increase from pre- to post-interaction. Significant correlations emerged between parental and infant OT at both assessments and higher OT levels in parent and child were related to greater affect synchrony and infant social engagement. Parent-infant affect synchrony moderated the relations between parental and infant OT and the associations between OT in parent and child were stronger under conditions of high affect synchrony. Results demonstrate consistency in the neuroendocrine system supporting bond formation in humans and other mammals and underscore the role of early experience in shaping the cross-generation transmission of social affiliation in humans.

Brain mechanisms for processing affective touch.

Despite the crucial role of touch in social development, there is very little functional magnetic resonance imaging (fMRI) research on brain mechanisms underlying social touch processing. The “skin as a social organ” hypothesis is supported by the discovery of C‐tactile (CT) nerves that are present in hairy skin and project to the insular cortex. CT‐fibers respond specifically well to slow, gentle touch such as that which occurs during close social interactions. Given the social significance of such touch researchers have proposed that the CT‐system represents an evolutionarily conserved mechanism important for normative social development. However, it is currently unknown whether brain regions other than the insula are involved in processing CT‐targeted touch. In the current fMRI study, we sought to characterize the brain regions involved in the perception of CT‐supported affective touch. Twenty‐two healthy adults received manual brush strokes to either the arm or palm. A direct contrast of the blood‐oxygenation‐level‐dependent (BOLD) response to gentle brushing of the arm and palm revealed the involvement of a network of brain regions, in addition to the posterior insula, during CT‐targeted affective touch to the arm. This network included areas known to be involved in social perception and social cognition, including the right posterior superior temporal sulcus and the medial prefrontal cortex (mPFC)/dorso anterior cingulate cortex (dACC). Connectivity analyses with an mPFC/dACC seed revealed coactivation with the left insula and amygdala during arm touch. These findings characterize a network of brain regions beyond the insula involved in coding CT‐targeted affective touch. Hum Brain Mapp, 2013.

Oxytocin and social motivation.

Humans are fundamentally social creatures who are ‘motivated’ to be with others. In this review we examine the role of oxytocin (OT) as it relates to social motivation. OT is synthesized in the brain and throughout the body, including in the heart, thymus, gastrointestinal tract, as well as reproductive organs. The distribution of the OT receptor (OTR) system in both the brain and periphery is even more far-reaching and its expression is subject to changes over the course of development. OTR expression is also sensitive to changes in the external environment and the internal somatic world. The OT system functions as an important element within a complex, developmentally sensitive biobehavioral system. Other elements include sensory inputs, the salience, reward, and threat detection pathways, the hypothalamic-pituitary-gonadal axis, and the hypothalamic-pituitary-adrenal stress response axis. Despite an ever expanding scientific literature, key unresolved questions remain concerning the interplay of the central and peripheral components of this complex biobehavioral system that dynamically engages the brain and the body as humans interact with social partners over the course of development.

Plasma oxytocin distributions in a large cohort of women and men and their gender-specific associations with anxiety

Research has consistently addressed the relations between plasma oxytocin (OT) - a nonapeptide implicated in mammalian social bonding - and psychological distress, but the direction of the association remains unclear. Utilizing the largest sample of plasma OT to date (N=473), the current study had two goals. First, we described the distributions of plasma OT in women and men, and second, we examined whether the relations between OT and two types of anxiety - trait and attachment anxiety - are moderated by gender. Results indicated that OT values (M=375.78 pg/ml, SD=264.03, range=51.40-2752.30) clustered around the mean with a long right tail, indicating trend toward high values. In most participants (N=323), OT was measured again six months after initial assessment and OT levels were highly stable within individuals. After removing outliers 2.5 SD above the mean (≥1098 pg/ml for men and ≥988 pg/ml for women), men showed significantly higher mean OT than women (women: 327.13 pg/ml, SD=164.43; men: 399.91, SD=183.65; t=2.57, p=.01). Gender was found to moderate the relations between OT and anxiety. Trait anxiety was lower among men with higher OT but no such links emerged for women, supporting the hypothesized anxiolytic effects of OT in males only. Furthermore, women with extreme values (≥988 pg/ml) had three times the probability of being classified as highly anxious (STAI-T≥45). Higher OT in women correlated with greater attachment anxiety, but no such relationships were found for men. Results are consistent with models on the differential associations between the neurobiology of attachment and the experience of anxiety in women and men.

Prolactin, Oxytocin, and the development of paternal behavior across the first six months of fatherhood

Animal studies have implicated the neuropeptides Prolactin (PRL) and Oxytocin (OT) in processes of maternal bonding and PRL has similarly been shown to play a role in the neurophysiology of fatherhood. Yet, very little is known on the involvement of PRL and OT in human fathering. Forty-three fathers and their firstborn infant were seen twice: in the second and sixth postpartum months. Paternal plasma PRL and OT were sampled at both time-points and analyzed with ELISA methods. At six months fathers were videotaped interacting with their child in social and exploratory play contexts and interactions were micro-analyzed for father-infant Affect Synchrony and father facilitation of child toy exploration. PRL and OT showed high individual stability across time and were correlated at the second observation. PRL was related to father-infant Coordinated Exploratory Play in the toy context whereas OT was associated with father-infant Affect Synchrony in the social context. Results point to the role of PRL and OT in the development of human fathering and underscore their differential relations with patterns of paternal care.