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.

Highlights

  • A typical EE has been defined as a rich combination of complex inanimate and social stimulation[1]

  • There was a significant effect of Group linked to reduced CORT levels in social groups (399.59 ± ng/ml vs. 259.28 ± ng/ml) indicating that both male and female F0 animals raised in the social housing condition had lowered HPA axis activity, reduced level of circulating CORT

  • A significant effect of Group was found suggesting that HPA axis activity in F1 animals born to F0 social mothers was significantly impacted by the ancestral experiences

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Summary

Introduction

A typical EE has been defined as a rich combination of complex inanimate and social stimulation[1]. In response to Welch and others[8], Rosenzweig’s team reported[1] that social grouping alone is not sufficient to explain the cerebral effects of EE interventions in rats. We proposed that social experiences are critical influences on offspring phenotype. The present study investigated the sex-specific impact of social enrichment on the parental F0 generation and their F1 offspring. Male and female F0 and F1 rats were raised in two housing conditions, standard and social environments, to reach adulthood. The neuromorphological and behavioural findings revealed that the female F0 brain and behaviour are susceptible to social experience. F0 social mothers transmitted the new phenotype formed by social experiences to only their F1 female offspring. Behavioural programming by social experiences transmitted to the generation arguably depends on a lineage-dependent mechanism

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