Maternal buffering beyond glucocorticoids: impact of early life stress on corticolimbic circuits that control infant responses to novelty

Abstract

Maternal presence has a potent buffering effect on infant fear and stress responses in primates. We previously reported that maternal presence is not effective in buffering the endocrine stress response in infant rhesus monkeys reared by maltreating mothers. We have also reported that maltreating mothers show low maternal responsiveness and permissiveness/secure-base behavior. Although still not understood, it is possible that this maternal buffering effect is mediated, at least partially, through deactivation of amygdala response circuits when mothers are present. Here we studied rhesus monkey infants that differed in the quality of early maternal care to investigate how this early experience modulated maternal buffering effects on behavioral responses to novelty during the weaning period. We also examined the relationship between these behavioral responses and structural connectivity in one of the underlying regulatory neural circuits: amygdala-prefrontal pathways. Our findings suggest that infant exploration in a novel situation is predicted by maternal responsiveness and structural integrity of amygdala-prefrontal white matter depending on maternal presence (positive relationships when mother is absent). These results provide evidence that maternal buffering of infant behavioral inhibition is dependent on the quality of maternal care and structural connectivity of neural pathways that are sensitive to early life stress.

Connectome-scale functional intrinsic connectivity networks in macaques

“…A total of 10 subjects with longitudinal resting state fMRI (rsfMRI) scans collected during infancy and the juvenile period were used in this study (scans available at four different ages: 3-months: 10 subjects; 6-months: 10 subjects; 12-months: 8 subjects; 18-months: 5 subjects). The subjects represent typically developing, socially-housed rhesus monkeys, studied longitudinally as part of a larger study (Howell et al, 2016; McCormack et al, 2015). They were raised with their mothers and families for the entire duration of the study in large social groups and they span all social hierarchy strata (high, medium and low ranking families).…”

Neurobiology of infant attachment: attachment despite adversity and parental programming of emotionality

“…This model has identified the amygdala as being particularly vulnerable to effects of caregiving quality, as indicated by an increase in depressive-like symptoms and antisocial behaviors in adult offspring who experienced negative caregiving, as well as altered fear-related behaviors, via an amygdala-dependent mechanism [8,40,41] involving decreased amygdala-prefrontal cortex functional connectivity [42]. These infant rodent results mirror altered amygdala-prefrontal cortex connectivity found in orphanage reared human children and nonhuman primates reared with maltreating caregivers [33,43]. …”

Shaping long-term primate development: Telomere length trajectory as an indicator of early maternal maltreatment and predictor of future physiologic regulation

“…Mothers repeat these maltreating behaviors with subsequent offspring with maltreatment running in rhesus families, transmitted across generations through the maternal line both experientially and biologically (Maestripieri, 2005; Maestripieri & Carroll, 1998). In the current study, all infants were cross-fostered and randomly assigned to either competent mothers or mothers with a history of maltreating previous offspring (Howell et al, 2017). Cross-fostering all monkeys permits disentangling the impact of the actual caregiving experience (nurture) from the influence of heritable factors related to the biological mother (nature; Franklin et al, 2010; Huizinga et al, 2006; Maestripieri, 2005; McCormack, Newman, Higley, Maestripieri, & Sanchez, 2009).…”