Dissociable Effects of Early and Adolescent Adversity on Emotional Contagion

Early-life adversity can alter emotional and social development and increase risk to later stress. We investigated how early adverse experiences (EAE), triggered using the limited bedding and nesting model, and later adverse experiences (LAE) triggered by footshocks affect adult emotional contagion (EC) responses in rats. Adult male and female rats then witnessed a conspecific receiving footshocks. 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. While EAE did altered maternal care, 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 towards lower-frequency 50 kHz vocalizations specifically mediated this effect, suggesting a sex-specific pathway by which early adversity shapes social behavior. 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.