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, which 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 neural circuits underlying these functions.

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

“…Early maltreatment, in both human studies and studies in preclinical animal models, is a strong and established risk factor for negative cognitive, physiologic, immunologic, behavioral, and physical health consequences (Drury, Gonzalez, & Sanchez, 2015; Sanchez et al, 2007). Specific effects include alterations in the functioning of the stress response systems, particularly the hypothalamus–pituitary–adrenal (HPA) axis with changes to both baseline/diurnal and reactive patterns reported across mammalian species (Avishai-Eliner, Yi, Newth, & Baram, 1995; Drury, Gonzalez, et al, 2015; Howell et al, 2013; Ladd, Huot, Thrivikraman, Nemeroff, & Plotsky, 2004; MacMillan et al, 2009; McLaughlin et al, 2015; Sanchez, 2006; Sanchez et al, 2010; Sanchez, McCormack, & Howell, 2015; Stanton, Gutierrez, & Levine, 1988). The patterns and direction of changes in human studies is less consistent than preclinical animal models, perhaps reflective of the complex environmental confounders in human studies.…”

Bio-behavioral synchrony promotes the development of conceptualized emotions

“…Newborns need social assistance in regulating their energy expenditure, temperature and immune function **[3], and accordingly, early life care ensures the newborn’s survival and growth. Importantly, while mothers repeatedly regulate their offspring’s allostasis, they also foster the development of self-regulation *[4, 5]. Offspring brain development depends on the provisioning of adequate maternal care in early life, particularly in neural circuitry involved in allostasis, including the nucleus accumbens (NAcc), amygdala, and hypothalamus-pituitary-adrenal axis (HPA axis) **[4, 6, 7].…”

Attachment Figure's Regulation of Infant Brain and Behavior

“…Extensive research over decades also indicates that social buffering by the parent dramatically decreases stress hormone levels to impact children's behavior (Gunnar & Donzella, 2002;Hostinar, Sullivan, & Gunnar, 2014). Through human, rodent, and nonhuman primate research, we understand the important interaction of the amygdala and social buffering of the stress response to modulate behavior (Hennessy et al, 2009;Hennessy et al, 2015;Hostinar & Gunnar, 2013;Hostinar et al, 2013;Sanchez et al, 2015;Sullivan & Perry, 2015;Tottenham, Shapiro, Telzer, & Humphreys, 2012).…”

“…Subtler "hidden regulation" of the infant occurs during caregiving when the physical stimulation provided by the caretaker regulates the infant's physiological function. For example, hidden regulation occurs as the pattern and intensity of a mother's touch regulates the infant's level of growth hormone, body warmth increases the neurotransmitter norephinephrine (NE), and maternal odor increases behavioral activity and decreases stress hormones (Blaze & Roth, 2013;Feldman, Singer, & Zagoory, 2010;Hofer, 1994Hofer, , 2006Hofer & Sullivan, 2008;Hostinar & Gunnar, 2013;McKenna & McDade, 2005;Porges & Furman, 2011;Sanchez, McCormack, & Howell, 2015;Schanberg, Evoniuk, & Kuhn, 1984;Walker, 2010;Weller & Feldman, 2003). Experimental removal of just one of these sensory stimuli or removal of the mother and replacement of specific sensory stimuli have shown a causal relationship between specific maternal sensory stimulation and the immediate physiological and behavioral response of the rat pup.…”

“…to modulate behavior (Hennessy et al, 2009;Hennessy et al, 2015;Hostinar & Gunnar, 2013;Hostinar et al, 2013;Sanchez et al, 2015;Sullivan & Perry, 2015;Tottenham, Shapiro, Telzer, & Humphreys, 2012).…”