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.

Figure 1. Experimental methods.

A. Timeline. B. Sequential steps in carrying out the within-litter neonatal novelty exposure procedure: (i) Dam is removed from the home cage; (ii) Novel pups are transferred to individual non-home cages and yoked Home pups receive a matching amount of experimenter contact; (iii) After 3 min in the non-home cages, Novel pups are returned to the home cage in which the Home pups remain; (iv) Dam is returned to the home cage. C. Apparatus used to assess rats' ability to compete against a conspecific for exclusive access to chocolate rewards. Note that the runway was sufficiently narrow as to allow only one rat at a time to fully enter.

Figure 2. Permanent effects of neonatal novelty exposure on social competitive success and stress response system function (24 months of age).

AB. When trained individually, Novel and Home rats showed no difference in learning to obtain chocolate rewards nor did they differ in final level of performance (N _Novel = 11, N _Home = 11). C. During paired social competition testing, Novel rats won significantly more rewards than Home rats on Day 1 but not on Day 2 (N = 11 pairs of Novel and Home rats). D. Novel but not Home rats exhibited a significant reduction in wins from Day 1 to Day 2. E. Despite a significant difference between Novel and Home rats in wins on Day 1, there was no parallel difference in post-competition corticosterone (CORT) concentration. Overall, CORT response to social competition significantly decreased across testing days (N = 14 pairs of Novel and Home rats). F. Novel but not Home rats exhibited significant habituation of CORT response across days. In all panels, data are mean±SEM; * indicates p<0.05; ns indicates p>0.05.

Figure 3. Maternal care during brief 10-min windows immediately after repeated novelty exposure predicts the effect of novelty exposure on CORT habituation among aged offspring.

A. Greater average amount of maternal licking and grooming (LG) was associated with greater day-to-day variability in maternal LG (dots and bars indicate average and range, respectively, of LG across days for individual dams; N = 11 litters). B. Greater average amount of maternal LG was associated with negative novelty scores for CORT habituation (marginally significant). D. Smaller day-to-day variability in maternal LG was significantly correlated with positive novelty scores for CORT habituation.