Decreased Amygdala Reactivity to Parent Cues Protects Against Anxiety Following Early Adversity: An Examination Across 3 Years

doi:10.1016/j.bpsc.2019.02.001

Biological Psychiatry: Cognitive Neuroscience and Neuroimaging

Volume 4, Issue 7, July 2019, Pages 664-671

https://doi.org/10.1016/j.bpsc.2019.02.001 Get rights and content

Abstract

Background

The human brain remains highly plastic for a protracted developmental period. Thus, although early caregiving adversities that alter amygdala development can result in enduring emotion regulation difficulties, these trajectories should respond to subsequent enriched caregiving. Exposure to high-quality parenting can regulate (i.e., decrease) children’s amygdala reactivity, a process that, over the long term, is hypothesized to enhance emotion regulation. We tested the hypothesis that even following adversity, the parent–child relationship would be associated with decreases in amygdala reactivity to parent cues, which would in turn predict lower future anxiety.

Methods

Participants were 102 children (6–10 years of age) and adolescents (11–17 years of age), for whom data were collected at one or two time points and who either had experienced institutional care before adoption (n = 45) or had lived always with their biological parents (comparison; n = 57). We examined how amygdala reactivity to visual cues of the parent at time 1 predicted longitudinal change (from time 1 to time 2) in parent-reported child anxiety across 3 years.

Results

At time 1, on average, amygdala reactivity decrements to parent cues were not seen in children who had received institutional care but were seen in children in the comparison group. However, some children who previously experienced institutional care did show decreased amygdala reactivity to parent cues (∼40%), which was associated with greater child-reported feelings of security with their parent. Amygdala decreases at time 1 were followed by steeper anxiety reductions from time 1 to time 2 (i.e., 3 years).

Conclusions

These data provide a neurobiological mechanism by which the parent–child relationship can increase resilience, even in children at significant risk for anxiety symptoms.

Section snippets

Participants

fMRI data were collected from 109 youths. The final sample that provided usable data were 102 participants (mean 10.25 years of age, range 5–16 years of age) (see Supplemental Table S1 and Supplemental Figure 1 for demographics and exclusion criteria). Age was grouped into children versus adolescents because there was no expectation of linear age-related changes in amygdala response to parent cues, and our previous publication showed that typically raised children, but not adolescents, showed

Response in Right Anatomical Amygdala Region of Interest (Parent–Stranger Contrast)

There was a significant caregiving group × age group interaction, F_1,93 = 5.63, p = .020, η²_p = .06 (Figure 2; see Supplemental Figure S2 for the effect broken down into parent and stranger contrasts). Post hoc t tests showed that children in the PI group did not exhibit decreased amygdala reactivity to pictures of the parent, t₂₂ = 0.61, p = .726, and Bayesian analyses (one-sided, one-sample t test) in JASP (44) indicated that the data from the children in the PI group were 6.82 times more

Discussion

We tested three hypotheses generated from the neuroenvironmental loop model (17). First, we tested whether, on average, early caregiver deprivation would reduce the likelihood of children’s right amygdala showing decreased reactivity to parental stimuli. Second, we examined within the PI group whether more secure parent–child relationships (characterized by higher child-reported feelings of security in the attachment relationship) were associated with amygdala reactivity decreases to parent

Acknowledgments and Disclosures

This research was supported by National Institute of Mental Health (Grant No. R01MH091864 [to NT] and Grant No. 1K99MH113821 [to BLC]), the Dana Foundation (to NT), the National Science Foundation (Conference Grant No. BCS-1439258 [to NT and coinvestigators Megan Gunnar, Regina Sullivan, Mar Sanchez, and Camelia Hostinar]), the National Health and Medical Research Council (Early Career Fellowship No. 1091571 [to BLC]), the American Australian Association (to BLC), and the Brain Behavior

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Archival ReportDecreased Amygdala Reactivity to Parent Cues Protects Against Anxiety Following Early Adversity: An Examination Across 3 Years

Abstract

Background

Methods

Results

Conclusions

Section snippets

Participants

Response in Right Anatomical Amygdala Region of Interest (Parent–Stranger Contrast)

Discussion

Acknowledgments and Disclosures

Behav Res Ther

Evol Hum Behav

J Am Acad Child Adolesc Psychiatry

Neuroscience

Horm Behav

Neurobiol Learn Mem

Behav Res Ther

Comput Biomed Res

Curr Opin Behav Sci

Child Abuse Negl

Biol Psychiatry

Risky families: Family social environments and the mental and physical health of offspring

Psychol Bull

Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication I: Associations with first onset of DSM-IV disorders

Arch Gen Psychiatry

Childhood adversities and adult psychiatric disorders in the national comorbidity survey replication II: Associations with persistence of DSM-IV disorders

Arch Gen Psychiatry

Early developmental emergence of mature human amygdala-prefrontal phenotype following maternal deprivation: Evidence of stress-induced acceleration

Proc Natl Acad Sci U S A

Previous institutionalization is followed by broader amygdala–hippocampal–PFC network connectivity during aversive learning in human development

J Neurosci

Maternal-child adrenocortical attunement in early childhood: Continuity and change

Dev Psychobiol

Early relationships as regulators of infant physiology and behavior

Acta Paediatr

Psychobiological mechanisms underlying the social buffering of the hypothalamic–pituitary–adrenocortical axis: A review of animal models and human studies across development

Psychol Bull

Maternal emotional signaling: Its effect on the visual cliff behavior of 1-year-olds

Dev Psychol

Parent support is less effective in buffering cortisol stress reactivity for adolescents compared to children

Dev Sci

Maternal buffering of human amygdala-prefrontal circuitry during childhood but not during adolescence

Psychol Sci

An empirical review of the neural underpinnings of receiving and giving social support: Implications for health

Psychosom Med

Maternal presence serves as a switch between learning fear and attraction in infancy

Nat Neurosci

Early-life stress disrupts attachment learning: The role of amygdala corticosterone, locus ceruleus corticotropin releasing hormone, and olfactory bulb norepinephrine

J Neurosci

The neuro-environmental loop of plasticity: A cross-species analysis of parental effects on emotion circuitry development following typical and adverse caregiving

Neuropsychopharmacology

Archival Report
Decreased Amygdala Reactivity to Parent Cues Protects Against Anxiety Following Early Adversity: An Examination Across 3 Years