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

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.

Paternal social enrichment effects on maternal behavior and offspring growth

“…In BALB/c mice, heightened anxiety-like behavior in adulthood has been attributed to the reduced levels of postpartum maternal care received in infancy (20,21). In the present study we illustrate the combined effect of postnatal communal rearing and postweaning enrichment (ENR males) on ameliorating this phenotype, an effect consistent with previous studies of complex housing and social stimulation (17,18). In contrast to the effects of enrichment, we find that social isolation exerts little effect on anxiety-like behavior in BALB/c mice.…”

“…Variation in behavioral characteristics in rodents is associated with levels of maternal care experienced during postnatal development (18,25,32,33). These phenotypic effects may be achieved through maternal epigenetic programming of offspring gene expression, inducing individual differences that persist into adulthood (29,30,34).…”

“…Social experience across the lifespan has been shown to modulate stress responsivity and anxiety-like behavior across species (17)(18)(19). In BALB/c mice, heightened anxiety-like behavior in adulthood has been attributed to the reduced levels of postpartum maternal care received in infancy (20,21).…”

Early-Life Experience, Epigenetics, and the Developing Brain

“…The experience of brief maternal separation during postnatal development has also been demonstrated to enhance hippocampal-dependent memory (Tang, 2001), although the experience of a novel environment during the separation may be a critical variable in predicting these effects (Tang et al, 2006). In mice, adult females can be induced to increase pup-directed behavior when placed in a communal nest, consisting of multiple caregivers and litters (Curley et al, 2009). Offspring reared in a communal nest are more exploratory in a novel environment, display higher levels of social behavior, and have increased hippocampal neurotrophin levels (Branchi et al, 2006a(Branchi et al, , b, 2013Curley et al, 2009).…”

Hacia una epistemología evolutiva extendida: la retroalimentación entre variación y selección.

“…Entre los más relevantes mencionamos cuatro: 1) la endosimbiosis como mecanismo clave en la evolución de las primeras formas de vida, y 2) el equilibrio puntuado, son argumentos no gradualistas sobre la selección natural que chocan con el paradigma neodarwiniano que niega toda herencia de caracteres adquiridos y se basa en procesos graduales, mientras que los procesos endosimbióticos son bruscos, no graduales (Eldredge y Gould, 1972;Margulis 2003); 3) la herencia de modificaciones epigenéticas que muestra que la variación fenotípica no se da solo por variación en los genes sino también en su mecanismo de expresión. Hay evidencias que muestran que las modificaciones epigenéticas son inducidas muchas veces por el medio ambiente y que además pueden ser heredadas y afectar el desarrollo de la progenie (Cubas, 1999;Hall, 2003;Champagne y Meaney, 2006;Champagne y Meaney, 2007;Galloway y Etterson, 2007;Berger et al, 2009;Bonduriansky, 2009;Curley, 2009); y 4) La importancia de la relación ontogenia-filogenia en el proceso evolutivo.…”