The effects of parental experience on cognition, anxiety-like behaviour, and hippocampal plasticity in a biparental species.

Abstract

Becoming a parent is a transformative event marked by significant changes in behaviour and the brain. In rodents, it is still unclear how parental experience influences behaviours outside of caregiving, such as in spatial cognition and anxiety. Furthermore, studies on the effects of maternal experience have focused on monoparental species, while few studies have investigated the changes associated with fatherhood. To date, a direct comparison on the effects of parental experience on behaviour and the brain in both mothers and fathers of the same species has not been done. The objective of this study was to investigate the effects of parental experience on spatial cognition, anxiety-like behaviour, and hippocampal neuroplasticity-related measures (microglia and perineuronal net expression) in both sexes of the same species, the degu. Degus are biparental rodents allowing us to examine maternal and paternal experiences in addition to maternal experience in single mothers when the male partner is removed (i.e., monoparental maternal experience). Key findings from our study indicated that parental experience differentially affects anxiety-like behaviour and spatial learning and memory in males and females. Biparental females exhibited more anxiogenic behaviour while biparental males showed more anxiolytic behaviour on the elevated plus maze. Furthermore, biparental males exhibited impaired spatial learning, while monoparental females exhibited enhanced spatial learning on the Barnes maze. In the hippocampus, parental experience did not affect the density of microglia and the expression of perineuronal nets in either the dorsal or ventral dentate gyrus. These results demonstrate that parenthood remodels behaviour and affects anxiety and spatial cognition in a differential manner across sexes. However, these alterations in behaviour do not appear to be associated with changes in microglia or perineuronal net expression in the dentate gyrus, suggesting alternative regions and mechanisms are involved.