Abnormal behavioral and neurotrophic development in the younger sibling receiving less maternal care in a communal nursing paradigm in rats

Abstract

Maternal behavior in rodents has been proposed to vary as a function of the external environment and, in turn, adjust offspring's stress and fear responses. Early handling (brief periods of maternal separation during the first two weeks of life) studies and analyses of spontaneously high-caring rat mothers converge to indicate that increased levels of maternal care may reduce offspring emotionality in adulthood. However, the hypothesis that environment-dependent reduction in maternal care correlates with increased offspring vulnerability to pathology has been scarcely investigated. To test this hypothesis we studied maternal care and offspring development in young, adolescent and young-adult Sprague-Dawley rats reared in a communal nursing situation, characterized by two dams delivering their offspring four days apart and communally caring for them until weaning. We show that dams of the first-born litter show increased aggression towards the pregnant female and that offspring belonging to the second-born litter receive less maternal care compared to older cage-mates. Additionally, second-born rats show increased anxiety-related behavior in a plus-maze test in adolescence and adulthood and abnormal developmental trajectories in terms of social interaction and BDNF levels in the amygdala and hippocampus compared to both the first-born litter and to animal facility reared controls. This is the first indication that adverse environments, not requiring experimenter handling, may reduce maternal care and in turn increase offspring's emotionality and modify social behavior and BDNF developmental trajectories.