Social buffering of stress responses in nonhuman primates: Maternal regulation of the development of emotional regulatory brain circuits

Abstract

Social buffering, the phenomenon by which the presence of a familiar individual reduces or even eliminates stress- and fear-induced responses, exists in different animal species and has been examined in the context of the mother-infant relationship, in addition to adults. Although it is a well-known effect, the biological mechanisms that underlie it as well as its developmental impact are not well understood. Here, we provide a review of evidence of social and maternal buffering of stress reactivity in nonhuman primates, and some data from our group suggesting that when the mother-infant relationship is disrupted, maternal buffering is impaired. This evidence underscores the critical role that maternal care plays for proper regulation and development of emotional and stress responses of primate infants. Disruptions of the parent-infant bond constitute early adverse experiences associated with increased risk for psychopathology. We will focus on infant maltreatment, a devastating experience not only for humans, but for nonhuman primates as well. Taking advantage of this naturalistic animal model of adverse maternal caregiving, we have shown that competent maternal care is critical for the development of healthy attachment, social behavior, and emotional and stress regulation, as well as of the neural circuits underlying these functions.

Keywords: HPA axis; Nonhuman primates; Social buffering; Stress reactivity.

Figure 1

Impaired ability of the mother’s presence to buffer stress-induced cortisol increases in maltreated infants. Mother-infant pairs were exposed together to a novel stress test when the infant was 2 months old. A baseline (0 min) blood sample was collected from both mother and infant, and another blood sample was collected 30 min following exposure to the novel cage and room (post-test, 30 min). Infants’ plasma cortisol concentrations (µg/dl) are plotted in comparison to the average stress-induced cortisol levels reached when the infants were exposed to a novel stress test alone (without the mother). * Significant difference between the stress-induced increase in cortisol (delta: stress-baseline) of control and maltreated infants (t(18)=−1.936, p=0.034, one-tailed).