Omri Weisman

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.

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 Administration to Parent Enhances Infant Physiological and Behavioral Readiness for Social Engagement

BACKGROUND The social milieu provides the context for the organisms survival, endurance, and adaptation. In mammals, social participation originates within the parent-infant bond and is supported by the oxytocin (OT) system, whose functioning is transmitted from parent to child through patterns of parental care. Human studies indicate that OT administration increases affiliative behavior, including trust, empathy, and social reciprocity. Here, we examine whether OT administration to parent can enhance physiological and behavioral processes that support parental social engagement but, moreover, can have parallel effects on the infant. METHODS Utilizing a double-blind, placebo-controlled crossover design, 35 fathers and their 5-month-old infants were observed twice following administration of OT or placebo to father in the face-to-face still-face paradigm. Parent and infant salivary OT were assessed at multiple time points, respiratory sinus arrhythmia (RSA) was measured in the three face-to-face still-face episodes, and social behaviors of the parent and child were micro-coded for indices of social engagement. RESULTS Oxytocin administration increased father salivary OT, RSA during free play, and key parenting behaviors that support parental-infant bonding. Parallel increases were also found in the infants salivary OT, RSA response, and engagement behavior, including social gaze, exploration, and social reciprocity. CONCLUSIONS Results are the first to demonstrate that OT administration to one attachment partner can have parallel effects on the other and underscore the role of OT in the cross-generation transmission of human social participation. Findings have translational implications for conditions associated with early risk for social-emotional growth, including autism and prematurity, without the need to administer drugs to young infants.

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.

Intranasal oxytocin administration is reflected in human saliva

Following the discovery that intranasal administration of neuropeptides can reach the central nervous system, a growing number of studies applied intranasal oxytocin (OT) paradigms to demonstrate the positive effects of OT on social and emotional processes. The three-step paradigm typically included: OT administration, a 45-min waiting period, and approximately 1-h period of active drug effects when experimental manipulations are applied. Yet, this schedule has not been put to systematic validation. Utilizing a double-blind placebo-control within-subject design, ten individuals were administered OT or placebo and salivary OT was measured ten times, at baseline and nine times over four consecutive hours. OT administration induced substantial increases in salivary OT across the entire period. OT rose dramatically 15 min after administration (from 6.9 pg/ml at baseline to 1265.4 pg/ml), reached plateau at 45-120 min (range=131.6 and 105.3 pg/ml), and did not return to baseline by 4h. Results contribute to discussion on brain-periphery coordination of OT and highlight the need for further research on the temporal dynamics and durations of OT administration effects.

Oxytocin administration, salivary testosterone, and father-infant social behavior.

The growing involvement of fathers in childcare is followed by an increased interest in the neurobiology of fatherhood; yet, experimental work on the neuroendocrine basis of paternal care in humans is limited. The steroid Testosterone (T) and the neuropeptide Oxytocin (OT) have each been implicated in complex social behavior including parenting. However, no study to date explored the interaction between these two hormones in the context of fathering. In the current study we first test the relationship between fathers basal salivary T and father and infants social behaviors during parent-child interaction. Second, we examine the effects of intranasal OT administration on fathers T production, and, finally, address the relations between OT-induced change in fathers T with father-infant social behavior. Thirty-five fathers and their infants participated in a double-blind, placebo-controlled, within-subject study. Father-infant interaction was micro-coded for paternal and infant social behavior and synchrony was measured as the coordination between their gaze, affect, and vocalizations. Fathers salivary T levels were measured at baseline and three times after administration. Results indicate that lower baseline T correlated with more optimal father and infants behaviors. OT administration altered T production in fathers, relative to the pattern of T in the placebo condition. Finally, OT-induced change in T levels correlated with parent-child social behaviors, including positive affect, social gaze, touch, and vocal synchrony. Findings support the view that neuroendocrine systems in human males evolved to support committed parenting and are the first to describe the dynamic interactions between OT and T within a bio-behavioral synchrony model.

Sleep-Wake Transitions in Premature Neonates Predict Early Development

OBJECTIVE: To identify patterns of sleep-wake transitions in the neonatal period that might differentiate premature infants who would show better or worse outcomes in multiple developmental domains across the first 5 years of life. METHODS: Participants were 143 low birth weight premature infants (mean birth weight: 1482 g; mean gestational age [GA]: 31.82 weeks). Sleep states were observed at a GA of 37 weeks in 10-second epochs over 4 consecutive evening hours and were analyzed through mathematical clustering. Neurobehavioral maturation was evaluated with the Neonatal Behavior Assessment Scale at discharge, emotional regulation was assessed during infant-mother and infant-father interactions at 3 and 6 months, cognitive development was measured at 6, 12, and 24 months, and verbal IQ, executive functions, and symbolic competence were tested at 5 years. RESULTS: Three types of state-transition patterns were identified, and no differences in birth weight, GA, or medical risk between the 3 groups were found. Infants whose sleep-state transitions were mainly characterized by shifts between quiet sleep and wakefulness exhibited the best development, including greater neonatal neuromaturation, less negative emotionality, better cognitive development, and better verbal, symbolic, and executive competences at 5 years. In comparison, infants who cycled mainly between states of high arousal, such as active sleep and cry, or between short episodes of active and quiet sleep showed poorer outcomes. CONCLUSIONS: Defining sleep organization on the basis of transitions between states proved useful for identifying risk and resilience indicators in neonatal behavior to predict trajectories of neurobehavioral, emotional, and cognitive growth.

Oxytocin shapes parental motion during father–infant interaction

An infant-oriented parental repertoire contributes to an infants development and well-being. The role of oxytocin (OT) in promoting affiliative bonds and parenting has been established in numerous animal and human studies. Recently, acute administration of OT to a parent was found to enhance the carers, but at the same time also the infants, physiological and behavioural readiness for dyadic social engagement. Yet, the exact cues that are involved in this affiliative transmission process remain unclear. The existing literature suggests that motion and vocalization are key social signals for the offspring that facilitates social participation, and that distance and motion perception are modulated by OT in humans. Here, we employed a computational method on video vignettes of human parent–infant interaction including 32 fathers that were administered OT or a placebo in a crossover experimental design. Results indicate that OT modulates parental proximity to the infant, as well as the fathers head speed and head acceleration but not the fathers vocalization during dyadic interaction. Similarly, the infants OT reactivity is positively correlated with fathers head acceleration. The current findings are the first to report a relationship between the OT system and parental motion characteristics, further suggesting that the cross-generation transmission of parenting in humans might be underlaid by nuanced, infant-oriented, gestures relating to the carers proximity, speed and acceleration within the dyadic context.

The experience of labor, maternal perception of the infant, and the mother’s postpartum mood in a low-risk community cohort

Postpartum negative mood interferes with maternal–infant bonding and carries long-term negative consequences for infant growth. We examined the effects of birth-related risks on mother’s postpartum anxiety and depression. A community cohort of 1,844 low-risk women who delivered a singleton term baby completed measures assessing delivery, emotions during labor, attitudes toward pregnancy and infant, mood regulation, and postpartum anxiety and depression. Under conditions of low risk, 20.5% of parturient women reported high levels of depressive symptoms. Following Cesarean Section Delivery (CSD), 23% reported high depressive symptoms, compared to 19% following Vaginal Delivery (VGD), and 21% after Assisted Vaginal Delivery (AVGD). State anxiety was highest in CSD and lowest in VGD. Mothers undergoing CSD experienced labor as most negative, reported highest somatic symptoms during the last trimester, and were least efficient in regulating negative mood. Postpartum depression was independently associated with higher maternal age, CSD, labor pain, lower negative and higher positive emotions during labor, inefficient mood regulation, somatic symptoms, and more negative and less positive perception of fetus during last trimester. Results demonstrate that elevated depressive symptoms are prevalent in the postpartum even under optimal socioeconomic and health conditions and increase following CSD. Interventions to increase positive infant-related perceptions and emotions may be especially important for promoting bond formation following CSD.

Salivary vasopressin increases following intranasal oxytocin administration.

Extant research has documented the effects of intranasal administration of oxytocin (OT), and to a lesser degree Arginine Vasopressin (AVP) - two structurally-related neuropeptides - on brain and behaviour, yet the effects of exogenous manipulation of one on circulating levels of the other remain unknown. Studies have shown that OT administration impacts the peripheral levels of numerous hormones; however, whether OT administration also increases AVP concentrations has not been explored. Utilizing a double-blind placebo-controlled within-subject design, ten male and female subjects provided ten saliva samples over four consecutive hours: at baseline and nine times following OT administration. Results indicate that salivary AVP increased in the first hour following OT manipulation (OT condition: mean AVP=2.17 pg/ml, SE=28, placebo condition: mean AVP=1.42 pg/ml, SE=.18) but returned to baseline levels at the next assessment (80 min) and remained low for the remaining period. Similar to OT, AVP showed high degree of individual stability and baseline levels of AVP correlated with AVP concentrations at the first and second post-administration hours regardless of drug condition (Pearson r=.85-.93). Validity of salivary AVP ELISA measurement was verified by demonstrating individual stability of salivary AVP over a six-month period (r=.70, p<.000) as well correlation with plasma levels over the same period (r=.32, p=.037) in a sample of 45 young adults who did not participate in the current study. Overall, findings suggest a potential crosstalk between OT and AVP and indicate that baseline levels of the two neuropeptides may shape the degree to which these systems respond to exogenous manipulation.