Early life adoption shows rearing environment supersedes transgenerational effects of paternal stress on aggressive temperament in the offspring

Abstract

Prenatal experience and transgenerational influences are increasingly recognized as critical for defining the socio-emotional system, through the development of social competences and of their underlying neural circuitries. Here, we used an established rat model of social stress resulting from male partner aggression induced by peripubertal (P28-42) exposure to unpredictable fearful experiences. Using this model, we aimed to first, characterize adult emotionality in terms of the breadth of the socio-emotional symptoms and second, to determine the relative impact of prenatal vs postnatal influences. For this purpose, male offspring of pairs comprising a control or a peripubertally stressed male were cross-fostered at birth and tested at adulthood on a series of socio-emotional tests. In the offspring of peripubertally stressed males, the expected antisocial phenotype was observed, as manifested by increased aggression towards a female partner and a threatening intruder, accompanied by lower sociability. This negative outcome was yet accompanied by better social memory as well as enhanced active coping, based on more swimming and longer latency to immobility in the forced swim test, and less immobility in the shock probe test. Furthermore, the cross-fostering manipulation revealed that these adult behaviors were largely influenced by the post- but not the prenatal environment, an observation contrasting with both pre- and postnatal effects on attacks during juvenile play behavior. Adult aggression, other active coping behaviors, and social memory were determined by the predominance at this developmental stage of postnatal over prenatal influences. Together, our data highlight the relative persistence of early life influences.