Abstract
Genes and social experiences interact to create variation in social behavior and vulnerability to develop disorders of the social domain. Socially monogamous prairie voles display remarkable diversity in neuropeptide receptor systems and social behavior. Here, we examine the interaction of early-life adversity and brain oxytocin receptor (OTR) density on adult social attachment in female prairie voles. First, pups were isolated for 3 h per day, or unmanipulated, from postnatal day 1–14. Adult subjects were tested on the partner preference (PP) test to assess social attachment and OTR density in the brain was quantified. Neonatal social isolation impaired female PP formation, without affecting OTR density. Accumbal OTR density was, however, positively correlated with the percent of time spent huddling with the partner in neonatally isolated females. Females with high accumbal OTR binding were resilient to neonatal isolation. These results are consistent with the hypothesis that parental nurturing shapes neural systems underlying social relationships by enhancing striatal OTR signaling. Thus, we next determined whether early touch, mimicking parental licking and grooming, stimulates hypothalamic OT neuron activity. Tactile stimulation induced immediate-early gene activity in OT neurons in neonates. Finally, we investigated whether pharmacologically potentiating OT release using a melanocortin 3/4 agonist, melanotan-II (10 mg kg−1 subcutaneously), would mitigate the social isolation-induced impairments in attachment behavior. Neonatal melanotan-II administration buffered against the effects of early isolation on partner preference formation. Thus, variation in accumbal OTR density and early OT release induced by parental nurturing may moderate susceptibility to early adverse experiences, including neglect.
Highlights
Our results suggest that neonatal oxytocin receptor (OTR) signaling, in response to parental tactile stimulation, may positively influence the development of neural systems involved in adult social attachment
The percent of time spent huddling with the partner after 48 h of cohabitation was significantly positively correlated with OTR binding in the nucleus accumbens (NAcc) (R = 0.779, R2 = 0.607, P = 0.008) in the early-isolated group, but not in the control group (R = 0.006, R2o 0.0001, P = 0.986; Figure 3a)
NAcc OTR binding significantly correlated with partner preference (PP) behavior in neonatally isolated females, and those with high densities of NAcc OTR were resilient to the impact of neonatal social isolation on later PP
Summary
Offspring who have experienced disruptions in parental nurturing often display increased fear responsiveness, hyperactive stress physiology, impaired social competence, and, in humans, an increased vulnerability for mood and anxiety, addiction and personality disorders.[1,2,3,4,5] The quality of early parental care is a salient predictor of adult socioemotional behavior and neurobiology.[6,7,8] Supplemental tactile stimulation to simulate parental nurturing alleviates some deficits resulting from maternal separation in both rats and voles.[9,10] In humans, interventions that apply supplemental touch to preterm infants improve emotional selfregulation and social reciprocity throughout development.[11,12,13]One candidate mechanism by which early tactile stimulation modulates behavior is oxytocin (OT) signaling.[14,15] OT is released centrally and peripherally after touch in adult rats,[16,17,18] and is increased in the saliva of human infants after parental interactions.[19,20] Elevated licking and grooming and peripheral OT injections in rat pups enhance adult maternal behavior.[21,22] Early care shapes OT neural pathways, and rat offspring exhibit an oxytocin receptor (OTR) profile characteristic to that of their rearing mother.[23,24] Together these findings suggest that early OT signaling mediates some of the behavioral changes induced by variation in parental nurturing.
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