Intergenerational Sex-Specific Transmission of Maternal Social Experience

Abstract

The social environment is a major determinant of individual stress response and lifetime health. The present study shows that (1) social enrichment has a significant impact on neuroplasticity and behaviour particularly in females; and (2) social enrichment in females can be transmitted to their unexposed female descendants. Two generations (F0 and F1) of male and female rats raised in standard and social housing conditions were examined for neurohormonal and molecular alterations along with changes in four behavioural modalities. In addition to higher cortical neuronal density and cortical thickness, social experience in mothers reduced hypothalamic-pituitary-adrenal (HPA) axis activity in F0 rats and their F1 non-social housing offspring. Only F0 social mothers and their F1 non-social daughters displayed improved novelty-seeking exploratory behaviour and reduced anxiety-related behaviour whereas their motor and cognitive performance remained unchanged. Also, cortical and mRNA measurements in the F1 generation were affected by social experience intergenerationally via the female lineage (mother-to-daughter). These findings indicate that social experience promotes cortical neuroplasticity, neurohormonal and behavioural outcomes, and these changes can be transmitted to the F1 non-social offspring in a sexually dimorphic manner. Thus, a socially stimulating environment may form new biobehavioural phenotypes not only in exposed individuals, but also in their intergenerationally programmed descendants.

Proximate causes and consequences of intergenerational influences of salient sensory experience

“…It is not uncommon to observe sex‐differences in the effects of intergenerational influences of salient parental environments. Exposing parental rodents to stressors as well as dietary manipulations have been shown to affect one sex and not the other depending not only on the parental perturbation but also the task on which the offspring are tested . Therefore, once again, our data agree with the existing literature that male and female offspring may shoulder the legacy of parental stress differently and attention needs to be paid to the parental environmental experience and the dependent variable being tested in the offspring.…”

Oxytocin-mediated social enrichment promotes longer telomeres and novelty seeking

“…In agreement with our previous findings, female rats that experienced social enrichment across development showed extended exploration of the central areas in the CFT, thus increasing the radius of exploratory activity ( Faraji et al, 2014 ). The latter indicates lowered stress response ( Faraji et al, 2014 ), which agrees with the finding that socially raised female rats display lower HPA axis response and reduced anxiety-related behaviours ( Faraji et al, 2018 ). Accordingly, intensified OT action through social enrichment enhances social bonding and reduces stress responses ( Swain et al, 2014 ).…”

“…Hence, the pathways involved in social experience-induced OT responses may contribute to sex differences in TL in close interaction with the HPA system. Notably, social experiences in our previous findings ( Faraji et al, 2018 ) reduced HPA axis activity in F0 female rats and the F1 non-social housing offspring born to social mothers, which suggests an intergenerational impact of social rearing history through regulation of the HPA response in female rats. Various other genetic mechanisms not investigated here may also determine social behaviours.…”

“…Also, females show facilitated social learning compared to males ( Ervin et al, 2015 ), along with estrogenic control of OT and OT receptor activity ( Anacker and Beery, 2013 ). Accordingly, we have recently shown that prolonged social experiences change brain structure and behaviours in a sexually dimorphic manner in rats ( Faraji et al, 2018 ).…”

Proximate causes and consequences of intergenerational influences of salient sensory experience

“…It is not uncommon to observe sex-differences in the effects of intergenerational influences of salient parental environments. Exposing parental rodents to stressors as well as dietary manipulations have been shown to affect one sex and not the other depending not only on the parental perturbation but also the task on which the offspring are tested [46][47][48][49][50][51][52][53]. Therefore, once again, our data agree with the existing literature that male and female offspring may shoulder the legacy of parental stress differently and attention needs to be paid to the parental environmental experience and the dependent variable being tested in the offspring.…”