Developing a Neurobehavioral Animal Model of Infant Attachment to an Abusive Caregiver

Abstract

Background Both abused and well cared for infants show attachment to their caregivers, although the quality of that attachment differs. Moreover, the infant’s attachment to the abusive caregiver is associated with compromised mental health, especially under stress. In an attempt to better understand how abuse by the caregiver can compromise mental health, we explore the neural basis of attachment in both typical and abusive environments using infant rats, which form attachments to the mother through learning her odor. Here, we hypothesize that the neural circuitry for infant attachment differs based on the quality of the attachment, which can be uncovered during stressful situations. Methods We used infant rats to compare infant attachment social behaviors and supporting neurobiology using natural maternal odor, as well as two odor-learning attachment paradigms: odor-stroke (mimics typical attachment) and odor-.5 mA shock conditioning (mimics abusive attachment). Next, to uncover differences in behavior and brain, these pups were injected with systemic corticosterone. Finally, pups were reared with an abusive mother to determine ecological relevance. Results Our results suggest that the natural and learned attachment odors indistinguishably control social behavior in infancy (approach to the odor and interactions with the mother). However, with corticosterone injection, pups with an abusive attachment show disrupted infant social behavior with the mother and engagement of the amygdala. Conclusions This animal model of attachment accommodates both abusive and typical attachment and suggests that pups’ social behavior and underlying neural circuitry may provide clues to understanding attachment in children with various conditions of care.

Enduring good memories of infant trauma: Rescue of adult neurobehavioral deficits via amygdala serotonin and corticosterone interaction

“…2C). Previous work has shown that these effects are odor-specific and limited to paired odor-shock learning (12,20,23,25). Furthermore, a one-way ANOVA revealed that infant trauma (i.e., odor-shock) increased amygdala 5-HT efflux (F (5,14) = 11.03, P < 0.001) at PN12, which was not observed in no-shock controls ( Fig.…”

“…The control group did not receive shock. Subsets of pups were either permitted to grow up (males) or tested during infancy in a Y-maze or a nipple attachment test to assess preference learning (both males and females) (12,25).…”

“…Specifically, we used infant olfactory classical conditioning in which a novel peppermint odor is paired with a mild shock (0.5 mA, 1s) to produce a preferred odor that functions behaviorally as a maternal odor and results in neural activation comparable with that induced by natural maternal odor (20,(23)(24)(25). During the sensitive period, low endogenous levels of corticosterone (CORT) and attenuated shock-induced CORT release prevent the infant amygdala from exhibiting the learning-induced plasticity required for avoidance learning (14,26).…”

Ecologically relevant neurobehavioral assessment of the development of threat learning

“…In other words, threat learning is not observed before PN10, which converges with the emergence of threat responses to natural threats discussed above (Moriceau et al 2004). Specifically, the odor-shock conditioning procedure produces odor preference with behavioral expression similar to learning induced by pairing the odor with milk, suckling, tactile stimulation (to mimic mother grooming), or maternal care in the nest (Brake 1981;Alberts and May 1984;Sullivan and Leon 1986;Weldon et al 1991;Raineki et al 2010b;Roth et al 2013). Learning to prefer an odor paired with an aversive stimulus occurs in spite of a functional pain system as assessed for instance, through shock induced vocalizations and escape-like behaviors (Small 1899;Anderson and Patrick 1934;Stehouwer and Campbell 1978;Fitzgerald and Gibson 1984;Emerich et al 1985;Sullivan et al 2000a;Sevelinges et al 2011).…”

“…This delayed amygdala development might account for the fact that pups younger than PN10 do not learn to fear an odor through odor-shock pairings when moderate shock levels are used (0.5 mA) and malaise is not produced (Haroutunian and Campbell 1979;Sullivan et al , 2000aCamp and Rudy 1988;Roth and Sullivan 2001Moriceau and Sullivan 2004a;Roth et al 2006;Raineki et al 2009Raineki et al , 2010bUpton and Sullivan 2010). Indeed, this conditioning evokes approach responses in a Y-maze and behavioral activation when tested in a small container.…”