Oxytocin and social affiliation in humans

Department of Psychology and the Gonda Brain Sciences Center, Bar-Ilan University, Ramat-Gan 52900, Israel.
Hormones and Behavior (Impact Factor: 4.63). 01/2012; 61(3):380-91. DOI: 10.1016/j.yhbeh.2012.01.008
Source: PubMed


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 infant's 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.

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    • "In chimpanzees, mothers with sons are more gregarious and spend more time in parties containing males compared to mothers of daughters especially in the first six months of life, probably as a way to influence their sons' social environment in a male-bonded society [Murray et al., 2014]. A wide variety of studies have demonstrated how variations in mother–infant interactions can influence offspring development at a genetic [reviewed in Meaney, 2001], cognitive [Murray et al., 1996; Olson et al., 1986], physiological [Feldman, 2012] and behavioral level [Mitchell & Stevens, 1968]. For example, pups of high licking/grooming-arched-back nursing (LG-ABN) rat mothers show reduced physiological and behavioral reactivity to stressful situations , and are themselves better mothers than low LG-ABN mothers [Meaney, 2001]. "
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    ABSTRACT: Face-to-face interactions between mothers and infants occur in both human and non-human primates, but there is large variability in the occurrence of these behaviors and the reason for this variability remains largely unexplored. Other types of maternal investment have been shown to be dependent on infant sex (e.g. milk production and maternal responsiveness) and maternal experience (e.g. symmetrical communication). Thus, we sought to determine whether variability in face-to-face interactions, that is, mutual gazing (MG), which are hypothesized to be important for later sociocognitive development, could be explained by these variables. We studied 28 semi-free ranging rhesus monkey (Macaca mulatta) mother-infant dyads (6 primiparous; 12 male infants) born and reared at the Laboratory of Comparative Ethology field station at the NIH Animal Center in Poolesville, MD, across the first 90 postnatal days. Infant sex (i.e. male) was a significant predictor of maternal grooming (β ± SE = 0.359 ± 0.164, Z = 2.19, P = 0.029) whereas both parity (i.e. first time mothers) and infant sex (i.e. male) significantly predicted MG (parity: β ± SE = 0.735 ± 0.223, Z = 3.30, P < 0.001; infant sex: β ± SE = 0.436 ± 0.201, Z = 2.17, P ± 0.029). Separation from the mother (outside of arm’s reach) was not influenced by parity or infant sex. Together with existing literature, these findings point toward differential maternal investment for sons versus daughters. Mothers may be investing differentially in sons, behaviorally, to ensure their future social competence and thus later reproductive success. Collectively, our findings add to the literature that is beginning to identify early life experiences that may lead to sex differences in neurological and behavioral development.
    American Journal of Primatology 11/2015; DOI:10.1002/ajp.22503 · 2.44 Impact Factor
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    • "Despite extensive research on the neurobiological mechanisms fundamental to the formation of monogamous ''pair-bonds'' (Young et al., 2011), relatively little is known about the neuroendocrine underpinnings of maintaining that relationship (Resendez and Aragona, 2013). There is considerable evidence that the oxytocin (OXT) system plays a critical role in the facilitation of social bonds (Lim and Young, 2006; Kendrick, 2000) and the expression of prosocial behavior toward a social partner, including affiliation (Feldman, 2012), cooperation (De Dreu, 2012), and trust (Mikolajczak et al., 2010), presumably by acting on OXTrelevant nuclei in the ''social brain'' (Macdonald and Macdonald, 2010). OXT is released endogenously following positive social interactions between existing social partners in humans (Grewen et al., 2005; Tops et al., 2007; Taylor et al., 2010) and nonhuman primates (Snowdon et al., 2010; Crockford et al., 2013). "
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    ABSTRACT: Adult male-female bonds are partly characterized by initiating and maintaining close proximity with a social partner, as well as engaging in high levels of affiliative and sociosexual behavior. Oxytocin (OXT), a neuromodulatory nonapeptide, plays a critical role in the facilitation of social bonding and prosocial behavior toward a social partner (Feldman, 2012). However, less attention has been given to whether augmentation of OXT levels in an individual alters others' perceptions and behavior toward an OXT-treated social partner. We examined social dynamics in well-established male-female pairs of marmoset monkeys (Callithrix jacchus) in which one member of the pair was administered an intranasal OXT agonist, an OXT antagonist (OXTA), or saline. OXT treatment did not alter the expression of affiliative toward an untreated partner. However, OXT did significantly influence the expression of proximity and grooming behavior with a treated partner, as a function of OXT treatment and sex. Female interest in initiating and maintaining proximity with a pair-mate was altered by OXT treatment. Untreated female marmosets departed from their saline-treated partner more frequently than they approached them, as indicated by a low proximity index score. However, when males received an intranasal OXT agonist they had a significantly increased proximity index score relative to saline, indicating that their untreated partner approached them more often than they departed from them). Saline-treated females initiated and received equivalent levels of grooming behavior. However, when female marmosets were treated with an OXT agonist their untreated partner groomed them proportionately more often, for a greater total duration, and for more time per bout, than they initiated grooming behavior. These results suggest that intranasal OXT altered male and female marmosets' stimulus properties in such a way as to increase the amount of grooming behavior that females received from their long-term mate, as well as increase female interest in initiating and maintaining proximity with their long-term mate. Furthermore, these results support the notion that central OXT activity plays an important neuromodulatory role in the maintenance of long-lasting male-female relationships.
    Frontiers in Behavioral Neuroscience 10/2015; 9. DOI:10.3389/fnbeh.2015.00251 · 3.27 Impact Factor
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    • "For example, a series of studies by Ruth Feldman and colleagues have generated the following converging evidence: plasma levels of oxytocin across pregnancy and into the post-partum period are related to a number of maternal bonding behaviors such as infant directed gaze, vocalization, positive affect, and affectionate touch, as well as to attachment related thoughts and frequent checking of the infant (Feldman, Weller, Zagoory-Sharon et al., 2007); high but not low affection mothers, show an increase in plasma and saliva levels of oxytocin after mother-infant interaction, with fathers showing a similar pattern (Feldman, Gordon, Schneiderman et al., 2010); and plasma, saliva, and urine levels of oxytocin in mothers and fathers are associated with their child " s social engagement, the synchrony of their mutual affects, and the occurrence of positive communication sequences between parent and child (Feldman, Gordon, & Zagoory- Sharon., 2011). These studies and others conducted by this group, as well as recent studies by other investigators (Strathearn, Fonagy, Amico et al., 2009; Tost, Kolachana, Hakimi et al., 2010; Bartz, Zaki, Bolger et al., 2011) support the hypothesis that oxytocin plays an important role not only in maternal bonding but in all the major forms of human social affiliation (Feldman, 2012). "
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    DESCRIPTION: This short monograph describes the motivational system that underlies childbearing, as represented by the author's Traits-Desires-Intentions Behavior framework. It then examines how the three motivational components of this framework are related to consciousness, how they are affected by executive functions, and how they are represented and integrated within the brain. Finally, it briefly describes how this motivational system affects the set of behaviors that influence reproductive outcomes.
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