Active avoidance under social conditions recruits the anterior cingulate cortex in male and female rats.

Abstract

Actively avoiding potential threats is necessary for survival. Most research has focused on the behavioral and neurobiological processes when individuals avoid potential threats alone, under solitary conditions. Therefore, little is known about how social context affects active avoidance. Using a modified version of the platform-mediated avoidance task, we investigated whether the presence of a social partner attenuates freezing responses and promotes greater avoidance learning compared to avoidance learned under solitary conditions. Rats spent a similar percentage of time avoiding during the conditioned tone under both conditions; however, rats trained under social conditions exhibited greater freezing during the tone and lower pressing for food reward compared to solitary rats. Under solitary conditions, we observed greater avoidance in female compared to male rats, which was not present in rats under social conditions. To gain greater mechanistic insight, we optogenetically inactivated glutamatergic projection neurons in the anterior cingulate cortex (ACC) following avoidance training. Photoinactivation of ACC neurons impaired avoidance expression under social conditions both in the presence and absence of the partner. Under solitary conditions, photoinactivation of ACC delayed avoidance in males but blocked avoidance in females. Our findings suggest that avoidance is mediated by the ACC, regardless of social context, and may be dysfunctional in those suffering from trauma-related disorders. Furthermore, sex differences in prefrontal circuits mediating active avoidance warrant further investigation, given that females experience a higher risk of developing anxiety disorders.