Oxytocin and social motivation

Abstract

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.

Keywords: cortisol; dopamine; dyadic social interactions; epigenetics; estrogen; motivation; oxytocin; parenting; reward; salience; sexual behavior; stress; testosterone; vasopressin.

Fig. 1

Central and peripheral sites of oxytocin (OT) release. Within the brain, OT is released from the paraventricular (PVN) and supraoptic (SON) nuclei of the hypothalamus, and to a lesser extent, the bed nucleus of the stria terminalis, spinal cord and anterior commissural nucleus. Central OT projections are pictured in green. Peripheral sources of OT include OT released into circulation via the posterior pituitary as well as numerous sites outside of the brain, including the heart, thymus, gastrointestinal tract, testis, epididymis, prostate, pregnant intrauterine tissue, ovaries, and adrenal medulla. The breast, pancreas and kidney are peripheral OT targets. NAcc = nucleus accumbens; MPOA = medial preoptic area; BNST = bed nucleus of stria terminalis; VTA = ventral tegmental area; A = amygdala.

Fig. 2

Integrative model. An integrative model of biobehavioral processes involved in the formation and maintenance of caretaker–child bonds and related attachment phenomena. “Responsiveness” includes: (a) a range of perceptual, autonomic, behavioral, emotional and cognitive responses conditioned by the absence, presence, or merely cues of the other; (b) responses conditioned by the caretaker's experience of being cared for as an infant; and (c) responses conditioned by perceived threats and adversity. By entering into a synchronous affective dyadic communication with the infant, the caregiver provides an external support for the infant's developing bioregulatory abilities and thereby conveys lifelong resilience to stress and enhanced coping ability. The experience of the caregiver and child's micro-level matching of affective states and level of arousal during face-to-face dyadic interactions beginning around the second month of life provides the basis for children's self awareness, social development, empathy, and moral internalization. Maternal gaze matching, facial expressions, vocalizations, and regulation of arousal states during face-to-face play provide critical environmental inputs during the sensitive period of maturation of the visual cortex. Furthermore, by synchronizing with infant arousal state, mothers entrain the infant's biological rhythms, providing a “resonance” of internal and external experience, self and other, brain and behavior. Metacognitive representations and mental states correspond to internal working models and are continually being updated and revised. However, one's earliest experiences with caregivers can powerfully shape the landscape of possible and expected interactions with others. For example, stranger anxiety appears when infants experience a mismatch between expected caregiver stimuli and stimuli that the infant encounters when exposed to an unfamiliar person. These metacognitive representations and mental states can be both conscious and unconscious and can directly influence both patterns of responsiveness in the self and others as well as the core neural circuitry and associated peripheral organs that dynamically link (in a context specific fashion) the oxytocin (OT) and arginine vasopressin (AVP) and the dopamine dependent reward pathways along with the hypothalamic-pituitary-adrenal (HPA) and the hypothalamic-pituitary-gonadal (HPG) axes (see text).