Auditory-conditioned fear drives social proximity in mice, requiring oxytocin receptor signaling and amygdala-hippocampus inputs.

Social affiliation is critical for survival, with proximity being a fundamental component. While innate threats reliably increase social cohesion, the role of learned threats in promoting proximity remains underexplored. Understanding the neural mechanisms underlying social responses to learned fear could offer insights into conditions like social anxiety or trauma-related social dysfunction, where social interactions are often altered. This study investigates how learned fear influences social proximity and its underlying neurobiology.

Researchers used same-sex mouse dyads to investigate social proximity responses to an auditory conditioned stimulus (CS). Mice underwent fear conditioning, then their proximity was measured during CS presentation. To probe neural circuitry, DREADD-mediated suppression was used to inactivate specific basolateral amygdala-to-ventral hippocampus inputs. Additionally, the role of oxytocin receptor signaling was assessed via systemic administration of the antagonist L368,899. The primary endpoint was the change in social proximity during CS presentation, with freezing levels also monitored.

Fear-conditioned mice significantly increased proximity to their partners during the auditory CS presentation. This increase in social proximity was observed to be independent of the mice's freezing levels, suggesting a distinct behavioral response.

This CS-evoked proximity critically required familiarity between the mouse partners, indicating that the social bond or prior interaction history is a prerequisite for this fear-induced affiliative behavior. Furthermore, the study demonstrated that intact neural inputs from the basolateral amygdala to the ventral hippocampus were essential for this proximity response, as DREADD-mediated suppression of these inputs abolished the effect. Crucially, the researchers found that oxytocin receptor signaling was indispensable, with systemic administration of the antagonist L368,899 preventing the CS-induced increase in proximity. These findings collectively suggest that learned threats engage shared neural circuitry with innate threats to promote social proximity.