A mother's past can predict her offspring's future: Previous maternal separation leads to the early emergence of adult-like fear behavior in subsequent male infant rat offspring

Recent evidence has shown that pups exposed to maternal separation exhibit profound changes in their emotional development, for example, early emergence of adult-like fear retention and fear inhibition (Callaghan & Richardson, 2011; Callaghan & Richardson, 2012). Numerous studies have shown that maternal separation is also a significant stressor for the mother. However, no studies have examined how a mother's prior parenting experience affects emotion development of pups in her subsequent litters. In this study female rats were bred and were then separated from their pups (maternal separation, MS) or remained with their pups (standard rearing, SR). After those pups were weaned, females were bred again with all pups from the subsequent litters being standard reared. Hence, these subsequent litter pups had mothers that were either previously separated (MSSUB) or not (SRSUB) from their prior litter. Those pups underwent fear conditioning at postnatal Day 17 and tested for fear retention, or had their fear extinguished and then tested for the renewal effect. The results show that the MSSUB infants respond similarly to infants that had been directly exposed to MS. That is, the MSSUB infants exhibited better retention of fear and more relapse after extinction compared with SRSUB infants. Further experiments demonstrated that MSSUB rats were not more anxious than SRSUB infants. Taken together, these experiments are the first to demonstrate that infant offspring exhibit atypical emotional development of fear conditioning (but not anxiety) as a consequence of their mother's prior exposure to stress