Perinatal and juvenile social environments interact to shape cognitive behaviour and neural phenotype in prairie voles

Social environments experienced at different developmental stages profoundly shape adult behavioural and neural phenotypes, and may have important interactive effects. We asked if social experience before and after weaning influenced adult social cognition in male prairie voles. Animals were raised either with or without fathers and then either housed singly or in sibling pairs. Males that were socially deprived before (fatherless) and after (singly housed) weaning did not demonstrate social recognition or dissociate spatial from social information. We also examined oxytocin and vasopressin receptors (OTR and V1aR) in areas of the forebrain associated with social behaviour and memory. Pre- and post-wean experience differentially altered receptor expression in several structures. Of note, OTR in the lateral septum—an area in which oxytocin inhibits social recognition—was greatest in animals that did not clearly demonstrate social recognition. The combination of absentee fathers on V1aR in the retrosplenial cortex and single housing on OTR in the septohippocampal nucleus produced a unique phenotype previously found to be associated with poor reproductive success in nature. We demonstrate that interactive effects of early life experiences throughout development have tremendous influence over brain–behaviour phenotype and can buffer potentially negative outcomes due to social deprivation.