Unique neurobiology during the sensitive period for attachment produces distinctive infant trauma processing

Abstract

Background: Trauma has neurobehavioral effects when experienced at any stage of development, but 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 a critical variable in determining its immediate and enduring consequences. Trauma experienced from an attachment figure, such as occurs in cases of caregiver child maltreatment, is particularly detrimental.

Methods: Using data primarily from 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. We then consider how trauma with and without the caregiver produces long-term changes in emotionality and behavior, and suggest that these experiences initiate distinct pathways to pathology.

Results: 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 toward processing information within the attachment circuitry.

Conclusion: An understanding of developmental differences in trauma processing as well as 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: Trauma; amygdala; attachment; development; infant; maternal care; sensitive period; stress.

Fig. 1

Using a fear conditioning paradigm of odor-shock presentations has enabled us to uncover a developmentally unique learning system in pups that typically supports attachment learning. Data indicate that during the sensitive period for attachment learning (PN≤9), low CORT levels block amygdala plasticity to prevent pups from learning amygdala-dependent fear/threat. Instead, this learning paradigm activates the attachment learning neural circuit involving NE to produce approach responses to the odor (Moriceau et al., 2006). The odor also takes on qualities of the maternal odor to support nipple attachment and enhance prosocial behaviors to the mother. In pups older than PN9, this fear conditioning paradigm accesses the amygdala to support fear/threat learning if the pup is alone. A critical feature of this learning is that shock induces activation of the HPA axis and CORT release, which is necessary for the young amygdala to learn. However, if the mother is present, she socially buffers the pup’s stress response, and pups revert to sensitive period learning and learn an odor preference. This mother-controlled switch between fear and attachment learning is mediated through the mother’s ability to control pups’ CORT (Moriceau, Wilson et al., 2006). A more adult-like fear learning system, which cannot be switched on/off by CORT, develops by PN15. Environmental variables that control pups’ CORT level, such as receiving CORT from a stressed mother via milk, environmental manipulations that increase pups’ CORT (exogenous CORT administration and abusive rearing), or the mother’s ability to socially buffer the pups (compromised in abusive mothers) have the potential to modify the age of these transitions and whether a pup learns fear or attachment (Moriceau & Sullivan, ; Perry & Sullivan, ; Raineki et al., ; Shionoya et al., ; Sullivan & Holman, 2010).

Fig. 2

Timeline of attachment learning and the effects of early life maltreatment on later-life social and emotional behavior in the rat model of trauma associated with attachment. Early infants will learn attachment regardless of the quality of care, whereas slightly older infants (PN10–15) will either learn to fear a traumatic associated stimulus when away from the mother or learn an attachment if acquisition takes place with the mother. Testing later in life shows that only the early life trauma associated with attachment will lead to lifelong amygdala-dependent behavioral deficits, such as poor social behavior (onset prior to weaning) and depressive-like behaviors (onset post-weaning (Raineki et al., ; Sevelinges et al., ; Sullivan et al., 2000)). In pre-weanlings, poor social behavior is defined as decreased nipple attachment and fewer choices toward the maternal odor, indicating disordered attachment. 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. This is in sharp contrast to experience with trauma without attachment, which results in later-life anxiety (Rincón-Cortés & Sullivan, ; Sarro et al., 2014).