Social Competitiveness and Plasticity of Neuroendocrine Function in Old Age: Influence of Neonatal Novelty Exposure and Maternal Care Reliability

Abstract

Early experience is known to have a profound impact on brain and behavioral function later in life. Relatively few studies, however, have examined whether the effects of early experience remain detectable in the aging animal. Here, we examined the effects of neonatal novelty exposure, an early stimulation procedure, on late senescent rats' ability to win in social competition. During the first 3 weeks of life, half of each litter received daily 3-min exposures to a novel environment while the other half stayed in the home cage. At 24 months of age, pairs of rats competed against each other for exclusive access to chocolate rewards. We found that novelty-exposed rats won more rewards than home-staying rats, indicating that early experience exerts a life-long effect on this aspect of social dominance. Furthermore, novelty-exposed but not home-staying rats exhibited habituation of corticosterone release across repeated days of social competition testing, suggesting that early experience permanently enhances plasticity of the stress response system. Finally, we report a surprising finding that across individual rat families, greater effects of neonatal novelty exposure on stress response plasticity were found among families whose dams provided more reliable, instead of a greater total quantity of, maternal care.

Maternal modulation of novelty effects on physical development

“…1B). The familyspecific maternal context is indexed by a measure of maternal stress regulation, the rapid initial rise in the CORT stress response (CORT E ) (34), and by two maternal care measures, the quantity (35) and reliability of maternal care (15,16). Body weights were measured at weaning and adulthood ( Fig.…”

“…To capture this aspect, we examined the reliability of maternal care immediately after the nest disturbance and the brief mother-litter separation entailed by the repeated daily novelty exposure (15,16). Once again, we could not find any evidence that the reliability of postnovelty exposure (PNE) care itself directly affects the weaning and lateadulthood weights of her offspring (Ps > 0.2) (Figs.…”

“…The association between maternal CORT E and post-NNE maternal care reliability was not statistically significant (P > 0.2). reliability and quantity are not only observed in offspring physical development alone, but also in offspring regulation of stress response during social interactions (15) and other forms of learning and plasticity (16).…”

“…First, differences in offspring's HPA and behavioral functions can be created by prenatal (20) and postnatal (6, 7) manipulation of the mother's stress-response system, including directly adding corticosterone (CORT) to her drinking water (6) and injection of CORT into key brain structures (14). Second, within maternal care behavior, the average amount and variability of maternal care are two distinct aspects of maternal care, playing distinct roles (15,16). Such a distinction is also supported by findings from human child development, where it is maternal care sensitivity and consistency (i.e., reliability) but not the average amount of care, that has predictive power for infant development (21,22), particularly when the behavioral outcomes were observed during times of infant distress (23).…”

“…More recently, the maternal modulation hypothesis has been tested for long-range and continuous (as opposed binary) modulation across the offspring's life span. Family-to-family variations in both maternal-care reliability and maternal selfstress regulation have been shown to account for variations in the effects of neonatal novelty exposure on adult offspring behavior and HPA function (15)(16)(17)(18), pointing out an obvious (when thinking human development) (19), yet easily missed possibility (when thinking animal models), that the maternal context itself is multidimensional, including not only her care-giving behaviors (15,16) but also the mother's self-stress regulation (17,18).…”