Converging influence of neonatal novelty experience and maternal self-stress regulation on the plasticity of offspring acoustic startle response latency

Abstract

Behavioral and brain development is influenced by both maternal and non-maternal aspects of the postnatal environment and the precise nature of their interaction is the topic of an ongoing debate. Here, we consider the joint influence of neonatal environmental novelty and maternal self-stress regulation on the development of acoustic startle reflex (ASR), an extensively investigated model system for learning and neural plasticity. We test the hypothesis in the rat that brief repeated neonatal exposures to novelty can affect ASR in late adulthood and that this influence is sensitive to postnatal context of maternal self-stress regulation. We carried out the neonatal and early adulthood novelty exposure (PND 1–21 and PND 54–63 respectively), obtained measures of maternal self-stress regulation after weaning (PND 25–26), and evaluated in the male rats, ASR and ASR plasticity at adulthood (ASR1 and ASR2, one week apart, at 13.5 months of age). During ASR1, offspring, whose mothers had poor self-stress regulation as indexed by a high circulating basal corticosterone (CORT) concentration, showed a novelty-induced decrease of ASR latency. Offspring whose mothers had good self regulation as indexed by a low CORT, showed a novelty-induced increase in ASR latency. From ASR1 to ASR2, offspring whose mothers had poor self-stress regulation, showed a novelty-induced ASR latency habituation (increase in latency) while offspring whose mothers had good self regulation showed no novelty effect. These findings support a novel framework in which maternal and non-maternal postnatal environments exert interacting influences on the neonates, with maternal individual differences in self-stress regulation providing a critical context to enable bidirectional novelty-induced influence across different rat families.