Sex differences in social synchronization of conditioned fear

Abstract

ABSTRACTCoordinated behaviors are prevalent in the animal kingdom as they promote the survival of social specie. Meanwhile, the distinct social roles of males and females predict sex differences in behavioral coordination. However, because of its complexity, behavioral coordination and the underlying circuits have not been studied extensively in laboratory animals. Recently, we established a mouse model of social synchronization of conditioned fear and identified the ventral hippocampus to the amygdala pathway as the integrator of the affective and social information. We also found that males synchronized freezing bouts more strongly than females. Here, we investigated sex differences further by manipulating the animals’ social cues or emotional states. First, familiarity with social cues increased freezing synchrony in male but not female dyads. Second, the emotional distress from brief immobilization had a sex-dimorphic effect by disrupting freezing synchrony in males and enhancing it in females. Finally, inactivation of the ventral hippocampus abolished fear synchrony in both sexes but elicited negative synchrony in females only. In addition, we evaluated the coordination of snout movement during periods of non-freezing. While males and females did not differ in snout velocities, only females coordinated snout movement, and stress diminished that coordination. These findings reveal that conspecific identity and emotional state are sex-specific modulators of social synchrony, suggesting sex-specific functions within the socio-emotional integrator, which includes the ventral hippocampus and yet unknown circuits.