The exclusion of social play within an adolescent group interferes with learning and the acquisition of essential social behavior during development and can cause modulations in the social brain areas. However, despite the importance of social play in adolescence, an in-depth explanation of its physiological mechanisms is limited because of the lack of experimental animal models that embody social play exclusion in human society. To determine the mechanism of social play in adolescence, we identified differences in emotional behavior and brain activity in animal models of social play exclusion that mimicked human society. Emotional changes in the social play exclusion and non-exclusion groups were examined by tracking social play-related social interaction behavior, social play-related space preference, social play-related locomotor behavior, and anxiety-like behavior using a behavioral data analysis program. Differences in brain activity among groups were identified using immunohistochemical staining. During the social play exclusion model, the rats preferred the partition zone to the other areas in the test chamber. The exclusion group preferred the partition and the center zone over the non-exclusion group. When comparing before and after the social play exclusion, the exclusion group showed a decrease in mobility and an increase in anxiety-like behavior compared to the non-exclusion group. We found that c-Fos expression in the dentate gyrus (DG) of the exclusion group was lower than that in the non-exclusion group, whereas c-Fos expression in the lateral habenula (LHb) of the exclusion group was higher than that in the non-exclusion group. Taken together, in adolescence, exclusion from social play with peers can increase anxiety-like behavior in the exclusion group and change the neuronal activity of the DG and LHb, suggesting that exclusion from social play is linked to modifications in the DG and LHb, which are regions associated with mood regulation.
