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

• Published in: The European journal of neuroscience Vol. 62; no. 2; pp. e70190 - n/a
• Main Authors: Sato, Masaaki, Overton, Eric T. N., Fujima, Shuhei, Takumi, Toru
• Format: Journal Article
• Language: English
• Published: France Wiley Subscription Services, Inc 01.07.2025
• Subjects: Animals; Calcium imaging; Conspecifics; Cortex (insular); Discrimination, Psychological - physiology; Familiarity; insular cortex; Insular Cortex - cytology; Insular Cortex - physiology; Male; Mental task performance; Mice; Mice, Inbred C57BL; miniscope; Neuroimaging; Neurons; Neurons - physiology; Recognition, Psychology - physiology; representational drift; Social Behavior; Social Discrimination; Social interactions; Social organization; representational drift; miniscope; insular cortex; calcium imaging; social behavior
• ISSN: 0953-816X; 1460-9568; 1460-9568
• DOI: 10.1111/ejn.70190

ABSTRACT 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. Although neurons in the mouse agranular insular cortex represent ongoing social interactions, the mechanism by which they discriminate between familiar and novel conspecifics remains unknown. Using microendoscopic calcium imaging, we monitored insular neuronal activity during social familiarization and social discrimination tasks. Repeated interactions with the same target gradually activated fewer and largely nonoverlapping cells, whereas adding a novel target elicited an increase in the number of cells responding to the novel target, revealing rapidly reorganizing ensemble activity following changes in the social context.