From attachment to independence: stress hormone control of ecologically relevant emergence of infants’ responses to threat

Abstract

Young infant rat pups learn to approach cues associated with pain rather than learning amygdala-dependent fear. This approach response is considered caregiver-seeking and ecologically relevant within the context of attachment. With maturation, increases in the stress hormone corticosterone permit amygdala-dependent fear, which is crucial for survival during independent living. During the developmental transition from attachment to fear learning, maternal presence suppresses corticosterone elevation to block amygdala-dependent fear learning and re-engage the attachment circuitry. Early life trauma disrupts this developmental sequence by triggering a precocious increase of corticosterone, which permits amygdala-dependent threat responses. In this review, we explore the importance of the stress hormone corticosterone in infants’ transition from complete dependence on the caregiver to independence, with consideration for environmental influences on threat response ontogeny and mechanistic importance of social buffering of the stress response.

Early life trauma increases threat response of peri‐weaning rats, reduction of axo‐somatic synapses formed by parvalbumin cells and perineuronal net in the basolateral nucleus of amygdala

“…However, early life trauma, especially when associated with maltreatment by a caregiver, can go beyond adaptation to initiate pathology involving heightened amygdala‐dependent responses to threat, including childhood anxiety and post‐traumatic stress disorder (Fareri & Tottenham, ; Heim & Nemeroff, ; Malter Cohen et al, ; Teicher, Samson, Anderson, & Ohashi, ; Tottenham, ). Rodent and non‐human primate models of early life trauma associated with maternal maltreatment demonstrate a causal role for the amygdala in infant heightened responses to threat (Callaghan, Sullivan, Howell, & Tottenham, ; Drury, Sanchez, & Gonzalez, ; Gunnar, Hostinar, Sanchez, Tottenham, & Sullivan, ; Sanchez, Ladd, & Plotsky, ; Santiago, Aoki, & Sullivan, ). Here, we assess amygdala neural circuitry following an infant maltreatment paradigm previously shown to produce heightened amygdala‐dependent responses to threat—the Scarcity‐Adversity Model (SAM).…”

Local injury and systemic infection in infants alter later nociception and pain affect during early life and adulthood

“…The amygdala can be activated by systemic administration of corticosterone resulting in the expected, and adult-like learned aversions to cues associated with pain ( Moriceau et al., 2004 ). This premature activation of the amygdala then remains abnormally responsive to aversive and social cues in adults [reviewed in ( Santiago et al., 2017 )]. We can speculate that the combination of E-coli and carrageenan might have elevated corticosterone sufficiently to result in premature activation of the amygdala, which is then permanent, and which in turn had long-term consequences for the enhanced aversion to pain in the adults.…”

Effects of Early Life Stress on the Developing Basolateral Amygdala-Prefrontal Cortex Circuit: The Emerging Role of Local Inhibition and Perineuronal Nets

“…Many studies using conditioning paradigms in neonatal rodents have therefore used olfactory cues as the CS ( Jovanovic et al, 2013 ). Elegant studies have shown that during the first 2 weeks of postnatal life in rats, the mother has the ability to modify the emotional valence of stimuli ( Moriceau and Sullivan, 2006 ; Santiago et al, 2017 ; Sullivan, 2017 ) even though pups can learn aversive responses after PND10. Before that time, PND8 rats are able to pair an odor and a foot shock (US), but the conditioned response is approach rather than avoidance to the shock ( Sullivan et al, 2000 ).…”