Sex differences in social synchronization of conditioned fear.

Abstract

Socially coordinated threat responses support the survival of social groups, and the distinct social roles of males and females predict sex differences in such coordination. However, this study area remains unexplored in mice, the most commonly used laboratory species. Here, we examined two behaviors: a recently reported fear synchrony, where paired mice synchronize auditory-conditioned freezing more strongly in males, and a newly identified CS-induced affiliation, where mice increase proximity upon a conditioned stimulus. These behaviors necessitate the integration of social cues with emotional CS. To understand how sex influences that process, we manipulated social cues through partner familiarity and emotional states via prior stress. Unfamiliarity moderately reduced synchrony in male dyads but not in females. Whereas stress disrupted male synchrony and contrarily enhanced female synchrony. Unfamiliarity eliminated CS-induced affiliation in both sexes, while stress caused males to distance each other but had no effects in females. Interestingly, heterosexual dyads showed resilience in both coordinated behaviors unaffected by stress or unfamiliarity. These findings reveal sex-specific adaptations in socio-emotional integration when orchestrating socially coordinated behaviors and suggest that the sex-recognition circuits confer stress- and unfamiliarity-resilience, in particular, in heterosexual dyads.