Perinatal exposure to polystyrene nanoplastics alters socioemotional behaviors via the microbiota–gut–brain axis in adult offspring mice

Abstract

Polystyrene nanoplastics (PS-NPs), ubiquitous environmental contaminants, have been detected in various tissues of humans and animals, raising significant concerns regarding their potential health hazards. The long-term consequences of PS-NPs exposure during early developmental stages remain inadequately characterized. In this study, we established a murine model to investigate the chronic oral administration of PS-NPs via drinking water during the perinatal period, with a focus on elucidating the impact of PS-NPs ingestion on the social behaviors of adult offspring and the underlying mechanisms, particularly those involving the gut–brain axis. Our findings revealed that perinatal PS-NPs exposure elicited depression-like behaviors, diminished social dominance, and reduced social interactions in adult offspring. Additionally, we observed a decrease in dendritic spine density within hippocampal neurons, along with ultrastructural damage to hippocampal neurons and synapses in the adult offspring. PS-NPs exposure also led to a reduction in the richness and evenness of gut microbiota species composition in both male and female mice, with gut dysbiosis being particularly pronounced in adult males. Furthermore, alterations in metabolite abundance and metabolic pathways were detected in the hippocampus of both male and female adult offspring. Notably, a significant correlation was identified between the relative abundance of intestinal microorganisms and hippocampal metabolites. These results offer new insights into the association between early-life PS-NPs exposure and adult social behaviors, mediated through the microbiota–gut–brain axis.