Behavioral trajectories of aging prairie voles (Microtus ochrogaster): Adapting behavior to social context wanes with advanced age

Abstract

Several studies using mice have examined the effects of aging on cognitive tasks, as well as sensory and motor functions. However, few studies have examined the influence of aging on social behavior. Prairie voles (Microtus ochrogaster) are a socially monogamous and biparental rodent that live in small family groups and are now among the most popular rodent models for studies examining social behavior. Although the social behavioral trajectories of early-life development in prairie voles have been well-studied, how social behavior may change throughout adulthood remains unknown. Here we examined behavior in virgin male and female prairie voles in four different age groups: postnatal day (PND) 60–80, 140–160, 220–240, and 300–320. All animals underwent testing in a novel object task, a dominance test, a resident-intruder test, and several iterations of social approach and social interaction tests with varying types of social stimuli (i.e., novel same-sex conspecific, novel opposite-sex conspecific, familiar same-sex sibling/cagemate, small group of novel same-sex conspecifics). We found that age influenced neophobia and dominance, but not social approach behavior. Further, we found that young adult, but not older adult, prairie voles adapt prosocial and aggressive behavior relative to social context, and that selective aggression occurs in relation to age even in the absence of a pair bond. Our results suggest that prairie voles calibrate social phenotype in a context-dependent manner in young adulthood and stop adjusting behavior to social context in advanced age, demonstrating that social behavior is plastic not only throughout early development, but also well into adulthood. Together, this study provides insight into age-related changes in social behavior in prairie voles and shows that prairie voles may be a viable model for studying the cognitive and physiological benefits of social relationships and social engagement in advanced age.

Aging leads to sex-dependent effects on pair bonding and increased number of oxytocin-producing neurons in monogamous prairie voles

“…However, across all ages at the 4 wks separation timepoint, there was a tendency for females to decrease huddling time with a partner. These phenotypes may reflect an overall change in social behavior, as aging in unpaired voles reduces both prosocial and aggressive behaviors (Powell et al, 2022). However, within the context of a pair bond, these shifts in behavior could promote flexibility to engage with novel animals and potentially form new bonds.…”

“…Yet neither of these studies examined female behavior. Other studies have looked at social behavior outside the context of pair bonds, observing reductions in both prosocial behaviors directed towards a familiar same-sex sibling and aggression towards stranger conspecifics of either sex in non-bonded voles up to ∼9 months (∼mid-adulthood; Powell et al, 2022). Thus, work to date supports the hypothesis that there are sex- and age-dependent changes in social behavior, bonding, and their underlying hormonal bases, but it has not been thoroughly evaluated.…”