Natural variations in maternal behaviour shape trait anxiety and hippocampal neurogenesis in offspring

Abstract

Understanding the early origins of emotional traits and baseline anxiety is crucial for the development of personalized medicine in mood disorders. While previous research primarily focused on extreme conditions like chronic maternal deprivation, in the present study, we investigated how natural variations in maternal care influence anxiety-related behaviour and neurogenesis in C57BL/6J offspring in a longitudinal manner. We observed that mothers engaging in low maternal care (LMC) displayed lower adult neurogenesis in both the olfactory bulb and the dentate gyrus of the hippocampus compared to high maternal care (HMC) mothers. We then observed that LMC-reared pups exhibited increased anxiety-related behaviour at postnatal day (PND) 5, 9, and 22. Furthermore, maternal behaviour induced the development of emotional individuality at early stage. This mood-related phenotype in LMC-reared offspring was associated with decreased neurogenesis after weaning at PND24. In another group of litters, we further examined neurogenesis at an earlier age (PND9) and already found a reduction in the population of adult neural progenitor cells and cell proliferation in the subgranular zone of the dentate gyrus of LMC-reared pups. These results highlight that natural variations in early life experiences such as maternal care, shape long-term brain plasticity and behaviour in offspring. This underscores the relevance of maternal care and adult neurogenesis in shaping personality-like traits related to mood disorders.