Effect of relative social rank within a social hierarchy on neural activation in response to familiar or unfamiliar social signals.

Competent social functioning of group-living species relies on the ability of individuals to detect and utilize conspecific social cues to guide behavior. Previous studies have identified numerous brain regions involved in processing these external cues, collectively referred to as the Social Decision-Making Network. However, how the brain encodes social information with respect to an individual's social status has not been thoroughly examined. In mice, cues about an individual's identity, including social status, are conveyed through urinary proteins. In this study, we assessed the neural cFos immunoreactivity in dominant and subordinate male mice exposed to familiar and unfamiliar dominant and subordinate male urine. The posteroventral medial amygdala was the only brain region that responded exclusively to dominant compared to subordinate male urine. In all other brain regions, including the VMH, PMv, and vlPAG, activity is modulated by a combination of odor familiarity and the social status of both the urine donor and the subject receiving the cue. We show that dominant subjects exhibit robust differential activity across different types of cues compared to subordinate subjects, suggesting that individuals perceive social cues differently depending on social experience. These data inform further investigation of neurobiological mechanisms underlying social-status related brain differences and behavior.

Social status in mouse social hierarchies is associated with variation in oxytocin and vasopressin 1a receptor densities.

The neuropeptides oxytocin and vasopressin and their receptors have established roles in the regulation of mammalian social behavior including parental care, sex, affiliation and pair-bonding, but less is known regarding their relationship to social dominance and subordination within social hierarchies. We have previously demonstrated that male mice can form stable linear dominance hierarchies with individuals occupying one of three classes of social status: alpha, subdominant, subordinate. Alpha males exhibit high levels of aggression and rarely receive aggression. Subdominant males exhibit aggression towards subordinate males but also receive aggression from more dominant individuals. Subordinate males rarely exhibit aggression and receive aggression from more dominant males. Here, we examined whether variation in social status was associated with levels of oxytocin (OTR) and vasopressin 1a (V1aR) receptor binding in socially relevant brain regions. We found that socially dominant males had significantly higher OTR binding in the nucleus accumbens core than subordinate animals. Alpha males also had higher OTR binding in the anterior olfactory nucleus, posterior part of the cortical amygdala and rostral lateral septum compared to more subordinate individuals. Conversely, alpha males had lower V1aR binding in the rostral lateral septum and lateral preoptic area compared to subordinates. These observed relationships have two potential explanations. Preexisting individual differences in the patterns of OTR and V1aR binding may underlie behavioral differences that promote or inhibit the acquisition of social status. More likely, the differential social environments experienced by dominant and subordinate animals may shift receptor expression, potentially facilitating the expression of adaptive social behaviors.

Foraging dynamics are associated with social status and context in mouse social hierarchies.

Living in social hierarchies requires individuals to adapt their behavior and physiology. We have previously shown that male mice living in groups of 12 form linear and stable hierarchies with alpha males producing the highest daily level of major urinary proteins and urine. These findings suggest that maintaining alpha status in a social group requires higher food and water intake to generate energetic resources and produce more urine. To investigate whether social status affects eating and drinking behaviors, we measured the frequency of these behaviors in each individual mouse living in a social hierarchy with non-stop video recording for 24 h following the initiation of group housing and after social ranks were stabilized. We show alpha males eat and drink most frequently among all individuals in the hierarchy and had reduced quiescence of foraging both at the start of social housing and after hierarchies were established. Subdominants displayed a similar pattern of behavior following hierarchy formation relative to subordinates. The association strength of foraging behavior was negatively associated with that of agonistic behavior corrected for gregariousness (HWIG), suggesting animals modify foraging behavior to avoid others they engaged with aggressively. Overall, this study provides evidence that animals with different social status adapt their eating and drinking behaviors according to their physiological needs and current social environment.