Early interactions with mother and peers independently build adult social skills and shape BDNF and oxytocin receptor brain levels

Abstract

The early social environment has a profound impact on developmental trajectories. Although an impoverished early environment can undermine the acquisition of appropriate social skills, the specific role played by the different components of an individual’s early environment in building social competencies has not been fully elucidated. Here we setup an asynchronous communal nesting paradigm in mice to disentangle the influence of maternal care and early peer interactions on adult social behavior and neural systems reportedly involved in the regulation of social interactions. The asynchronous communal nesting consists of three mothers giving birth three days apart, generating three groups of pups -- the Old, the Middle and the Young – all raised in a single nest from birth to weaning. We scored the amount of maternal and peer interactions received by these mice and by a fourth group reared under standard conditions. At adulthood, the four experimental groups have been investigated for social behavior in a social interaction test, i.e. facing an unfamiliar conspecific during five 20-min daily encounters, and for oxytocin receptor and BDNF levels. Results show that only individuals exposed to high levels of both maternal and peer interactions demonstrated elaborate adult agonistic competencies, i.e. the ability to promptly display a social status, and high BDNF levels in the hippocampus, frontal cortex and hypothalamus. By contrast, only individuals exposed to high levels of peer interactions showed enhanced adult affiliative behavior and enhanced oxytocin receptor levels in selected nuclei of the amygdala. Overall these findings indicate that early interactions with mother and peers independently shape specific facets of adult social behavior and neural systems involved in social interaction.

Temporal dynamics of social hierarchy formation and maintenance in male mice

“…Here, we have shown that laboratory mice reliably form linear and stable dominance hierarchies after being put together within 48e96 h. Importantly, each mouse within a hierarchy had a unique and distinct social rank and responded consistently to more and less dominant members of their network with appropriate behaviour indicative of high sociocognitive competence (Branchi et al, 2013;Taborsky & Oliveira, 2012). There also was variability between groups in how unevenly power was distributed within the hierarchy.…”

“…personality variables like risk taking or boldness, or social competence) may be just as important as or more important than aggression in determining social status in mice (David, Auclair, & C ezilly, 2011;Fox, Ladage, Roth, & IIPravosudov, 2009;Hsu, Earley, & Wolf, 2006;Taborsky & Oliveira, 2012). Second, this finding suggests that standard laboratory tests of social dominance using animals tested in pairs in tasks such as the tube-test (van den Berg et al, 2015;Wang et al, 2011), food competition (Benner et al, 2014;de Jong, Korosi, Harris, Perea-Rodriguez, & Saltzman, 2012;Timmer, Cordero, Sevelinges, & Sandi, 2011) or aggression (Bales & Carter, 2003;Branchi et al, 2013) tests, are not necessarily robust indicators of an individual's ability to ascend a social hierarchy when living within a large social group comprising a number of complex social relationships.…”

“…Although these tests reveal behaviour characteristics of individual mice and the relationship between two individuals at a given point in time, they do not provide information about how relationships develop over time or how relationships are adjusted within a large social network. Dominance in pairs of mice is usually assessed with dyadic tubetests (van den Berg, Lamballais, & Kushner, 2015;Curley, 2011;Wang et al, 2011), food, sex or other reward competition tests (Benner, Endo, Endo, Kakeyama, & Tohyama, 2014;Jupp et al, 2015;Nelson, Cunningham, Ruff, & Potts, 2015) and aggression tests (Branchi et al, 2013;Ginsburg & Allee, 1942). Problematically, results in these social contexts do not necessarily relate to overall social dominance within a larger group context where relationships are embedded (Chase, 1982b).…”

Early social exposure in wild chimpanzees: Mothers with sons are more gregarious than mothers with daughters

“…The mother-infant relationship is therefore critical to proper social development; however, research also demonstrates the importance of the larger social milieu (17)(18)(19)(20). For example, a recent study in mice found that early interactions with mothers and peers independently shape adult behavior (21). Likewise, some negative impacts of maternal deprivation are attenuated in macaques that are raised in peer groups (22).…”

Bred to breed?! Implications of continuous mating on the emotional status of mouse offspring

“…While this may be suggested as attractive approach when embedded in neurobiological research it may on the other hand threat studies in which stress is unwanted and could cause artefacts. With regard to a long-range perspective a healthy life relies upon early experiences and adaptations can be made adequately [48,49]. With disadvantaged early conditions like postulated by our CM paradigm there is an increased risk of stress and maladaptation.…”