Selective social buffering of behavioral and endocrine responses and Fos induction in the prelimbic cortex of infants exposed to a novel environment

Abstract

In mammals, the presence of the mother can reduce or "buffer" stress responses of her young in threatening conditions. We compared the effect of the mother, a familiar littermate, and an unfamiliar adult male on three classes of response shown by guinea pig pups in a novel environment: short latency active behaviors, particularly vocalizing; slower developing passive behaviors that appear mediated by inflammatory mechanisms; and hypothalamic-pituitary-adrenal activity. We also examined Fos induction in the prelimbic cortex, a region hypothesized to mediate buffering effects. Only the mother significantly suppressed all classes of behavior. The greatest selectivity was observed for passive behavioral responses. Contrary to expectations, the adult male reduced plasma cortisol levels of pups as effectively as did the mother. The presence of the male also resulted in increased Fos induction in the prelimbic cortex and high levels of social interaction. Maternal buffering was not associated with prelimbic activity. These results confirm the ability of the mother to reduce active behavioral and HPA responses and suggest a specific maternal buffering effect on the later developing passive behavioral responses. The findings also demonstrate an unexpected ability of adult males to reduce HPA responses and raise the possibility that different social partners buffer HPA activity through different underlying processes.

Neurobehavioral assessment of maternal odor in developing rat pups: implications for social buffering

“…This aspect of social support has been described in myriad species, including humans and rodents, and occurs throughout the lifespan (Ditzen & Heinrichs, 2014; Gee et al, 2014; Hennessy, Kaiser, & Sachser, 2009; Hennessy et al, 2015; Hostinar & Gunnar, 2013; Kikusui, Winslow, & Mori, 2006; Moriceau & Sullivan, 2006; Nachmias, Gunnar, Mangelsdorf, Parritz, & Buss, 1996; Sanchez, 2006; Sanchez, McCormack, & Howell, 2015; Shionoya, Moriceau, Bradstock, & Sullivan, 2007; Stanton & Levine, 1990; Takahashi et al, 2013). Social buffering has profound beneficial effects on physiological processes and both short-term and long-term health (Hennessy et al, 2009; Uchino, Cacioppo, & Kiecolt-Glaser, 1996) and also impacts immediate behaviors through reducing the stress response, increasing prosocial behaviors, and decreasing threat/fear (Hennessy et al, 2015; Moriceau & Sullivan, 2006; Shionoya et al, 2007; Upton & Sullivan, 2010). …”

“…Additional work manipulating PVN NE and amygdala corticosterone (CORT) has suggested a causal relationship between stress hormone reduction and infants’ processing of trauma-induced stress during social buffering by the mother (Shionoya et al, 2007). Research also suggests that maternal buffering of children and rodents goes beyond reduction of the HPA axis by activating other brain areas, including the amygdala and medial prefrontal cortex (mPFC) (Gee et al, 2014; Hennessy et al, 2015). …”

Attachment Figure's Regulation of Infant Brain and Behavior

“…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).…”

“…Social buffering is a phenomenon that occurs throughout the animal kingdom and throughout life and describes the ability of a significant attachment figure to reduce the release of stress hormones during painful and traumatic events. Social buffering occurs in humans and occurs across species and across development (Ditzen & Heinrichs, 2014;Ducharme, Stanton, & Ducharme, 1985;Hennessy, 1986;Hennessy, Hornschuh, Kaiser, & Sachser, 2006;Hennessy, Kaiser, & Sachser, 2009;Hennessy et al, 2015;Hostinar et al, 2013;Kikusui, Winslow, & Mori, 2006;McCormack et al, 2006;Raineki et al, 2015;Rosenfeld, Su-checki, & Levine, 1992;Stanton & Levine, 1990;Suchecki, Rosenfeld, & Levine, 1993;Takahashi et al, 2013). Social buffering of the infant by the caregiver wanes as individuals across species mature and become independent (Gee et al, 2014;Hostinar, Johnson, & Gunnar, 2015;McCormack et al, 2006).…”

“…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).…”