Maternal buffering beyond glucocorticoids: impact of early life stress on corticolimbic circuits that control infant responses to novelty.
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.
a Department of Psychiatry & Behavioral Sciences , Emory University , Atlanta , GA , USA.|b Yerkes National Primate Research Center , Emory University , Atlanta , GA , USA.|c Institute of Child Development , University of Minnesota , Minneapolis , MN , USA.
Brittany R
BR
Howell
a Department of Psychiatry & Behavioral Sciences , Emory University , Atlanta , GA , USA.|b Yerkes National Primate Research Center , Emory University , Atlanta , GA , USA.
Matthew S
MS
McMurray
a Department of Psychiatry & Behavioral Sciences , Emory University , Atlanta , GA , USA.|b Yerkes National Primate Research Center , Emory University , Atlanta , GA , USA.
Dora B
DB
Guzman
d Biomedical Imaging Technology Center , Emory University and Georgia Institute of Technology , Atlanta , GA , USA.
Govind
G
Nair
e Department of Psychiatry and Computer Science , University of North Carolina , Chapel Hill , NC , USA.
Yundi
Y
Shi
b Yerkes National Primate Research Center , Emory University , Atlanta , GA , USA.|f Department of Psychology , Spelman College , Atlanta , GA , USA.
Kai M
KM
McCormack
d Biomedical Imaging Technology Center , Emory University and Georgia Institute of Technology , Atlanta , GA , USA.
Xiaoping
X
Hu
e Department of Psychiatry and Computer Science , University of North Carolina , Chapel Hill , NC , USA.
Martin A
MA
Styner
a Department of Psychiatry & Behavioral Sciences , Emory University , Atlanta , GA , USA.|b Yerkes National Primate Research Center , Emory University , Atlanta , GA , USA.
Mar M
MM
Sanchez
D000679:Amygdala / Q000000981:diagnostic imaging* / Q000254:growth & development*; D000704:Analysis of Variance; D000818:Animals; D002649:Child Abuse / Q000523:psychology; D038524:Diffusion Magnetic Resonance Imaging; D056324:Diffusion Tensor Imaging; D004195:Disease Models, Animal; D005260:Female; D006801:Humans; D007223:Infant; D008253:Macaca mulatta; D008297:Male; D008425:Maternal Behavior / Q000523:psychology*; D009035:Mothers; D009043:Motor Activity; D017397:Prefrontal Cortex / Q000000981:diagnostic imaging* / Q000254:growth & development*; D011581:Psychological Tests; D011897:Random Allocation; D013315:Stress, Psychological / Q000000981:diagnostic imaging*
Social buffering; infant maltreatment; maternal care; rhesus monkeys; uncinate fasciculus