Dissociable Effects of Early and Adolescent Adversity on Emotional Contagion

Background Early-life adversity can alter emotional and social development and increase vulnerability to later life stress. We investigated how early adverse experiences (EAE) and later adverse experiences (LAE) shape adult emotional contagion (EC) responses in female and male rats. Methods EAE was induced using the limited bedding and nesting model during the first postnatal week. LAE was induced via footshocks during adolescence. In adulthood, male and female rats underwent an EC test in which observers witnessed a conspecific receiving footshocks. Results Adolescence-footshock exposed observers showed cingulate cortex-associated increased immobility, proximity, and attention toward distressed conspecifics during adulthood, compared to adult-exposed and sham animals, both in male and female animals. While EAE did alter maternal care, pup stress physiology, and pup weight, we found evidence that it did not alter immobility during EC. However, female demonstrators paired with EAE observers showed increased immobility, linked to a reduced rate and lower frequency of the observers’ 50-kHz vocalizations. Mediation analysis revealed that a shift toward lower-frequency 50-kHz vocalizations specifically mediated this effect, suggesting a sex-specific pathway by which early adversity shapes social behavior. Conclusions Early and adolescent adversity influenced distinct aspects of emotional contagion: EAE mediated an observer-to-demonstrator emotional transfer during EC, while LAE impacted a demonstrator-to-observer transfer, with no evidence of additive effects. Our results highlight developmentally specific and sex-dependent mechanisms by which early and later adversity alter social-affective responses in adulthood.