Milking it for all it’s worth: The effects of environmental enrichment on maternal nurturance, lactation quality, and offspring social behavior

Abstract

AbstractWhile alterations in the neonatal environment can have dramatic effects on offspring outcomes, the mechanisms that drive this phenomenon remain unclear. Breastfeeding confers robust benefits to offspring development, including those related to growth, immunity, and neurophysiology. Similarly, improving environmental complexity (i.e., environmental enrichment; EE) contributes developmental advantages to both humans and laboratory animal models. However, the impact of environmental context on maternal care and milk quality has not been thoroughly evaluated, nor are the biological underpinnings of EE on offspring development understood. Here, Sprague-Dawley rats were housed and bred in either EE or standard-housed (SD) conditions. Although EE dams gave birth to a larger number of pups, litters were standardized and cross-fostered across groups on postnatal day (P)1. Maternal milk samples were then collected on P1 (transitional milk phase) and P10 (mature milk phase) for analysis. While EE dams spent less time nursing, postnatal enrichment exposure was associated with heavier offspring bodyweights. Moreover, milk from EE dams had increased triglyceride levels compared to SD dams. Milk from EE mothers also contained a greater microbiome diversity and a significantly higher abundance of bacterial families related to bodyweight and energy metabolism. In addition to changes in lactational quality, we observed sex- and time-dependent effects of EE on offspring social behavior. Specifically, prenatal EE exposure was associated with greater sociability in females, while postnatal EE was associated with greater sociability in male offspring. Together, these results underscore the multidimensional impact of the combined neonatal and maternal environments on offspring development. These data also identify potential deficiencies in the quality of the “gold standard” laboratory housing condition and its impact on the welfare and design of translationally relevant animal models in biomedical research.