Oxytocin and Social Relationships: From Attachment to Bond Disruption

Abstract

Social relationships throughout life are vital for well-being and physical and mental health. A significant amount of research in animal models as well as in humans suggests that oxytocin (OT) plays an important role in the development of the capacity to form social bonds, the mediation of the positive aspects of early-life nurturing on adult bonding capacity, and the maintenance of social bonding. Here, we focus on the extensive research on a socially monogamous rodent model organism, the prairie vole (Microtus ochrogaster). OT facilitates mating-induced pair bonds in adults through interaction with the mesolimbic dopamine system. Variation in striatal OT receptor density predicts resilience and susceptibility to neonatal social neglect in female prairie voles. Finally, in adults, loss of a partner results in multiple disruptions in OT signaling, including decreased OT release in the striatum, which is caused by an activation of the brain corticotropin releasing factor (CRF) system. The dramatic behavioral consequence of partner loss is increased depressive-like behavior reminiscent of bereavement. Importantly, infusions of OT into the striatum of adults prevents the onset of depressive-like behavior following partner loss, and evoking endogenous OT release using melanocortin agonists during neonatal social isolation rescues impairments in social bonding in adulthood. This work has important translational implications relevant to the disruptions of social bonds in childhood and in adults.

Developmental regulation of olfactory circuit formation in mice

“…Among them, oxytocin appears to be promising, because oxytocin is involved in social memory formation mediated by the MeA (Gur, Tendler, & Wagner, 2014). Furthermore, oxytocin promotes attractive social interactions (Bosch & Young, 2018; Muscatelli, Desarménien, Matarazzo, & Grinevich, 2018) and is highly expressed in the neonatal brain (Sannino, Chini, & Grinevich, 2017).…”

Epigenetic signatures of attachment insecurity and childhood adversity provide evidence for role transition in the pathogenesis of perinatal depression

“…The oxytocin receptor has very well-established roles in interpersonal relationships and mother-infant bonding 69,70 . Oxytocin signaling is of particular importance to the promotion of mother-infant bonding in the early postnatal period, which is the same time period in which attachment insecurity assumes a uniquely strong association with depressive symptoms.…”

Bridging the gap between rodents and humans: The role of non‐human primates in oxytocin research

“…This variation in density has been linked to individual differences in alloparental behavior (Olazábal & Young, 2006a, 2006b), pair-bonding (King et al, 2016; Ross, Cole, et al, 2009; Ross, Freeman, et al, 2009), and resilience to early-life social neglect (Barrett, Arambula, & Young, 2015). Striatal OT receptors also mediate the onset of depressive-like “grieving” behavior in prairie voles following loss of a partner (Bosch et al, 2016), a phenomenon that has been proposed to maintain social bonds (Bosch & Young, 2017; Pohl, Young, & Bosch, 2018). OXTR signaling coordinates brain activity across a social salience network (involving the nucleus accumbens, amygdala, prefrontal cortex, and other brain regions) during mating, facilitating the flow of social information across the network in prairie voles, and nucleus accumbens OXTRs appear to serve as a hub for facilitating coordinated activity across the social salience network (Johnson et al, 2016; Johnson, Walum, Xiao, Riefkohl, & Young, 2017).…”