Unique infant neurobiology produces distinctive trauma processing

Abstract

Trauma experienced in early life has unique neurobehavioral outcomes related to later life psychiatric sequelae. Recent evidence has further highlighted the context of infant trauma as critical, with trauma experienced within species-atypical aberrations in caregiving quality as particularly detrimental. Using data from primarily rodent models, we review the literature on the interaction between trauma and attachment in early life, which highlights the role of the caregiver's presence in engagement of attachment brain circuitry and suppressing threat processing by the amygdala. Together these data suggest that infant trauma processing and its enduring effects are impacted by both the immaturity of brain areas for processing trauma and the unique functioning of the early-life brain, which is biased towards forming robust attachments regardless of the quality of care. Understanding the critical role of the caregiver in further altering early life brain processing of trauma is important for developing age-relevant treatment and interventions.

Keywords: Amygdala; Attachment; Development; Sensitive period; Stress; Trauma.

Fig. 1

Unique characteristics of the infant brain. A, During a sensitive period, which ends when pups are PN9, infant neurobiology is biased towards attachment learning, regardless of the quality of care, including attaching to abusive caregivers (Roth and Sullivan, 2005). We mimicked attachment learning to an abusive caregiver by using an odor-shock conditioning paradigm, which enabled us to uncover a developmentally unique learning system in pups that typically supports attachment learning. Notably, when aversive stimuli are presented the pup’s attachment learning network is engaged, rather than the adult amygdala-dependent fear learning (Sullivan et al., 2000a). Indeed, following either abusive rearing or odor shock conditioning, pups tested in a Y-maze approach the odor paired with infant adversity. B, This specialized attachment learning system occurs during a sensitive period for attachment learning (PN < 9), with this learning supported by an attachment learning neural circuit involving norepinephrine (NE) from the locus coeruleus (LC) to produce approach responses to the odor (Moriceau et al., 2006). It is noteworthy that this newly learned odor is not simply approached, but the odor also takes on qualities of the maternal odor to support nipple attachment and enhance prosocial behaviors to the mother, even if she is physically abusive. Thus, infants during a sensitive period for attachment will learn attachment regardless of the quality of care, showing a preference for the maternal odor following abuse as well as repeatedly pairing the maternal odor with a tail shock. C, There are short-term benefits from this robust attachment learning network as it ensures pups remain with the abusive caregiver and receive some food and water required for survival. However, there are long-term costs that become salient at weaning, including social behavior deficits, disrupted fear/threat system and a hyperactive amygdala (Sullivan et al., 2000a; Raineki et al., 2010a,b,c; Sevelinges et al., 2011; Raineki et al., 2012a,b). In adolescence and adulthood, rats with a history of abuse will exhibit decreased preference for a social stimulus over a non-social stimulus in Crawley’s three chamber test, depressive-like behavior in the forced swim test and impaired fear conditioning (Rincon-Cortes and Sullivan, 2014; Sarro et al., 2014).