Social enrichment during postnatal development induces transgenerational effects on emotional and reproductive behavior in mice

James P Curley

doi:10.3389/neuro.08.025.2009

Abstract

Across species there is evidence that the quality of the early social environment can have a profound impact on neurobiology and behavior. In the present study we explore the effect of communal rearing conditions (three dams with three litters per cage) during the postnatal period on offspring (F1) and grand-offspring (F2) anxiety-like and maternal behavior in Balb/c mice. Females rearing pups in communal nests exhibited increased levels of postpartum maternal care and communal rearing was found to abolish sex-differences in weaning weights. In adulthood, communally reared offspring were observed to display reduced anxiety-like behavior when placed in a novel environment. When rearing their own offspring under standard conditions, communally reared females demonstrated higher levels of motivation to retrieve pups, built higher quality nests, and exhibited higher levels of postpartum care compared to standard reared females. When exposed to an intruder male, communally reared females were more subordinate and less aggressive. F2 offspring of communally reared females were observed to engage in reduced anxiety-like behavior, have larger litter sizes and an increased frequency of nursing on PND 1. Analysis of neuropeptide receptor levels suggest that a communal rearing environment may exert sustained effects on behavior through modification of oxytocin and vasopressin (V1a) receptor densities. Though Balb-C mice are often considered “socially-incompetent” and high in anxiety-like behavior, our findings suggest that through enrichment of the postnatal environment, these behavioral and neuroendocrine deficits may be attenuated both within and across generations.

Highlights

In mammals, there is typically an intense period of mother–infant interaction during the postnatal period that is essential for growth and development of offspring
COMMUNAL REARING CONDITIONS ON F0 MATERNAL BEHAVIOR Prior to cross-fostering of pups, those F0 Balb/c females designated to standard vs. communal rearing conditions were found to display equivalent nest qualities and levels of motivation to sniff, retrieve, nestbuild and crouch over pups during the pup retrieval test conducted on PND 0
Standard communal sniff retrieve retrieve retrieve nestbuild crouch stress-sensitive and socially impaired mouse strain. These early rearing effects persist in the absence of continued social enrichment and can be observed amongst F2 female offspring who have never experienced the communal rearing conditions

Summary

Introduction

There is typically an intense period of mother–infant interaction during the postnatal period that is essential for growth and development of offspring. The study of the long-term impact of variation in mother–infant interactions has been conducted using a variety of rodent models but provides converging evidence for maternal influence on offspring gene expression, neurobiology and behavior (Fernandez-Teruel et al, 1997; Lehmann and Feldon, 2000; Meaney, 2001). Within the natural ecology of both mice and rats, it is typical for females to care collectively for pups within a communal nest in which multiple females nurse and interact with offspring (Crowcroft and Rowe, 1963; Mennella et al, 1990; Schultz and Lore, 1993). Significant effects of communal nursing on anxiety-like behavior have been previously demonstrated, with the direction of the effect dependent on the sex, strain and age variation of pups within the nest (Sayler and Salmon, 1971; Branchi et al, 2006b)

Methods

Results

Conclusion