Reorganization of Social Representations in the Insular Cortex During Conspecific Familiarization and Discrimination

The familiarity of socially interacting peers markedly impacts behavior. However, the neuronal representations that distinguish familiar from novel conspecifics within the social brain network are not fully understood. Following our previous findings that neurons in the agranular insular cortex represent ongoing social interactions, we monitored the activity of neurons in the agranular insular cortex using microendoscopic calcium imaging in mice during social recognition memory and linear chamber social discrimination tasks. In the social recognition memory task, repeated interactions with the same target activated largely nonoverlapping cells during each session. The fraction of cells associated with social investigation (hereafter called social cells) decreased as the subject repeatedly interacted with the same target, whereas the substitution of a second novel target and subsequent exchange with the first familiar target recruited more new social cells. In the linear chamber social discrimination task, adding a novel target transiently increased the number of cells responding to both targets, followed by an eventual increase in the number of cells responding to the novel target. These results demonstrate that social cell ensembles in the agranular insular cortex decrease in size while changing their participating neurons during conspecific familiarization. They also rapidly reorganize at the single-cell level to represent interactions with novel peers rather than familiar peers during conspecific discrimination.