Psychobiological mechanisms underlying the social buffering of the hypothalamic–pituitary–adrenocortical axis: A review of animal models and human studies across development.

Abstract

Discovering the stress-buffering effects of social relationships has been one of the major findings in psychobiology in the last century. However, an understanding of the underlying neurobiological and psychological mechanisms of this buffering is only beginning to emerge. An important avenue of this research concerns the neurocircuitry that can regulate the activity of the hypothalamic-pituitary-adrenocortical (HPA) axis. The present review is a translational effort aimed at integrating animal models and human studies of the social regulation of the HPA axis from infancy to adulthood, specifically focusing on the process that has been named social buffering. This process has been noted across species and consists of a dampened HPA axis stress response to threat or challenge that occurs with the presence or assistance of a conspecific. We describe aspects of the relevant underlying neurobiology when enough information exists and expose major gaps in our understanding across all domains of the literatures we aimed to integrate. We provide a working conceptual model focused on the role of oxytocinergic systems and prefrontal neural networks as two of the putative biological mediators of this process, and propose that the role of early experiences is critical in shaping later social buffering effects. This synthesis points to both general future directions and specific experiments that need to be conducted to build a more comprehensive model of the HPA social buffering effect across the lifespan that incorporates multiple levels of analysis: neuroendocrine, behavioral, and social.

Mother nurture and the social definition of neurodevelopment

“…A remarkably similar effect occurs in humans where institutional rearing, an obvious instance of parental deprivation, accelerates functional coupling of the amygdala to the prefrontal cortex (18). This effect is likewise mediated by glucocorticoids, which are inhibited by active maternal care in both rodents and humans (16). Accelerated maturation of amygdala-dependent fear behaviors might occur as an adaptation to the absence of effective maternal buffering.…”

“…The relevant literature suggests two alternatives. First, maternal care "buffers" children from stressful conditions, moderating the impact of adversity (16). Second, maternal care is a form of "environmental enrichment" that regulates the expression of neurotrophic factors, such as brain-derived neurotrophic factor, that regulate synaptogenesis (17).…”

“…Rat pups deprived of maternal care show a precocious onset of fear behavior mediated by an accelerated maturation of the amygdala and the capacity to activate stress responses (16). Maternal deprivation activates glucocorticoid release, which triggers amygdala maturation.…”

Allostatic load and biological anthropology

“…By producing life-long dysregulation of stress responses (Lupien et al, 2006;McEwen, 1998bMcEwen, , 2000aMcEwen, , 2000bMcEwen, , 2001McEwen, , 2003McEwen, , 2012 load associates significantly with greater perceived stress (Goldman et al, 2005), hostility (Kubzansky, Kawachi, & Sparrow, 1999;Seeman et al, 2002), poor coping skills (Fernandez et al, 2015), and lack of purpose in life (Zilioli et al, 2015). Conversely, those with more integrated social networks and/or greater perceived social support appear to be protected against damaging after effects of stressors and dysregulation of allostasis (Bovard, 1985;Cohen & Wills, 1985;Goldman et al, 2005; Holt-Lunstad, Smith, & Layton, 2010;Horan & Widom, 2015;Hostinar, Sullivan, & Gunnar, 2014;House, Landis, & Umberson, 1988;Levine, Coe, & Wiener, 1989;McEwen, 2012;Seeman, 1996;Seeman et al, 1994Seeman et al, , 2002Seeman, Glei, et al, 2004;Seeman & McEwen, 1996;Smith & Christakis, 2008;Uchino, 2006;Uchino, Cacioppo, & Kiecolt-Glaser, 1996;Weinstein et al, 2003). Correspondingly, stronger social networks are negatively associated with allostatic load (Glei et al, 2007;Horan & Widom, 2015;Seeman, Glei, et al, 2004;Seeman et al, 2002).…”

DOHaD

“…Le lien entre les conditions ou événements adverses durant l'enfance et la santé ultérieure pourrait être dû en partie aux conséquences à long terme du stress toxique, résultat d'une forte activation, fréquente ou prolongée, des systèmes de réponse au stress de l'organisme en l'absence de la protection d'une relation « tampon » de soutien avec un adulte capable d'atté-nuer l'effet biologique délétère d'un stress chronique potentiel [13]. La stabilité et la nature de la relation entre un enfant et ses caregivers (« aidants » en français) apparaissent comme des éléments fondamentaux dans la modulation et le contrôle des réponses physiologiques au stress, en amortissant les effets des variations de l'environnement de l'enfant [14]. De multiples travaux épidémiologiques montrent ainsi que des relations sécurisées et positives entre jeunes enfants et un ou plusieurs adultes, au cours du développement, impactent positivement l'estime de soi, la compétence sociale actuelle et future, le contrôle émotionnel ou l'état de santé mentale à l'âge adulte.…”