Early life social complexity shapes adult neural processing in the communal spiny mouse Acomys cahirinus

Rationale Early life social rearing has profound consequences on offspring behavior and resilience. Yet, most studies examining early life development in rodents use species whose young are born immobile and do not produce complex social behavior until later in development. Furthermore, models of rearing under increased social complexity, rather than deprivation, are needed to provide alternative insight into the development of social neural circuitry. Objectives To understand precocial offspring social development, we manipulated early life social complexity in the communal spiny mouse Acomys cahirinus and assessed long-term consequences on offspring social behavior, exploration, and neural responses to novel social stimuli. Methods Spiny mouse pups were raised in the presence or absence of a non-kin breeding group. Upon adulthood, subjects underwent social interaction tests, an open field test, and a novel object test. Subjects were then exposed to a novel conspecific and novel group and neural responses were quantified via immunohistochemical staining in brain regions associated with social behavior. Results Early life social experience did not influence behavior in the test battery, but it did influence social processing. In animals exposed to non-kin during development, adult lateral septal neural responses toward a novel conspecific were weaker and hypothalamic neural responses toward a mixed-sex group were stronger. Conclusions Communal species may exhibit robust behavioral resilience to the early life social environment. But the early life environment can affect how novel social information is processed in the brain during adulthood, with long-term consequences that are likely to shape their behavioral trajectory.