Alteration in oxytocin levels induced by early social environment affects maternal behavior and estrogen receptor alpha in mandarin voles (Microtus mandarinus)

•Social deprivation decreased central oxytocin expression in mandarin voles.•Neonatal oxytocin promoted maternal but not paternal behavior in mandarin voles.•Neonatal oxytocin increased ERα expression in female but not male mandarin voles.•Neonatal oxytocin antagonist reduced ERα expression both in females and males. Many studies have shown that the early social environment exerts long-term effects on the brain and also the parental behavior of adults. Oxytocin (OXT) is one of the most important neurotransmitters that regulate social behavior; howerve, whether the early social environment affects parental behavior via OXT remains unclear. Using socially monogamous adult mandarin voles (Microtus mandarinus), the present study found that 1) both paternal deprivation and early social deprivation significantly decreased OXT expression in both the paraventricular hypothalamic nucleus (PVN) and the supraoptic nucleus (SON) of F2 generation offspring; 2) systemic neonatal OXT injection in naïve animals promoted maternal but not paternal behavior in adult F2 offspring; 3) systemic neonatal OXT injection significantly increased ERα expression in both the medial preoptic area (MPOA) and the ventro medial hypothalamic nucleus (VMH) in female but not in male mandarin voles; 4) systemic neonatal administration of an OXT antagonist significantly reduced ERα expression in the bed nucleus of the stria terminalis (BNST), VMH, and the arcuate hypothalamic nucleus (Arc) in females and in all examined brain regions in males. In summary, the obtained data demonstrate that the early social environment could affect OXT level, which in turn leads to long-term effects on ERα expression in relevant brain regions, consequently affecting maternal behavior but not paternal behavior.