Developmental outcomes of early adverse care on amygdala functional connectivity in nonhuman primates

Morin, Elyse L.; Howell, Brittany R.; Feczko, Eric; Earl, Eric; Pincus, Melanie; Reding, Katherine; Kovacs-Balint, Zsofia A.; Meyer, Jerrold S.; Styner, Martin; Fair, Damien; Sanchez, Mar M.

doi:10.1017/s0954579420001133

Cited by 37Child Abuse and TraumaStress Responses and CortisolFunctional Brain Connectivity Studies

Developmental outcomes of early adverse care on amygdala functional connectivity in nonhuman primates

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Morin, Elyse L., Howell, Brittany R., Feczko, Eric, Earl, Eric, Pincus, Melanie, Reding, Katherine, Kovacs-Balint, Zsofia A., Meyer, Jerrold S. +3 more·2020·Development and Psychopathology

DOI 10.1017/s0954579420001133PMC PMC11500993

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Abstract

Despite the strong link between childhood maltreatment and psychopathology, the underlying neurodevelopmental mechanisms are poorly understood and difficult to disentangle from heritable and prenatal factors. This study used a translational macaque model of infant maltreatment in which the adverse experience occurs in the first months of life, during intense maturation of amygdala circuits important for stress and emotional regulation. Thus, we examined the developmental impact of maltreatment on amygdala functional connectivity (FC) longitudinally, from infancy through the juvenile period. Using resting state functional magnetic resonance imaging (MRI) we performed amygdala–prefrontal cortex (PFC) region-of-interest and exploratory whole-brain amygdala FC analyses. The latter showed (a) developmental increases in amygdala FC with many regions, likely supporting increased processing of socioemotional-relevant stimuli with age; and (b) maltreatment effects on amygdala coupling with arousal and stress brain regions (locus coeruleus, laterodorsal tegmental area) that emerged with age. Maltreated juveniles showed weaker FC than controls, which was negatively associated with infant hair cortisol concentrations. Findings from the region-of-interest analysis also showed weaker amygdala FC with PFC regions in maltreated animals than controls since infancy, whereas bilateral amygdala FC was stronger in maltreated animals. These effects on amygdala FC development may underlie the poor behavioral outcomes associated with this adverse experience.

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Stress-induced structural changes in the PFC contribute to the pathophysiology of neuropsychiatric conditions.
“Although stress-induced structural changes in the PFC are equally important in their contribution to the pathophysiology of neuropsychiatric conditions [256–262]”
From Development of prefrontal cortex (2022) · cites this paper as [262]
The Discussion says chronic stress or glucocorticoid exposure affects spine density and dendritic arborization in trauma-vulnerable circuitry, and identifies the PFC as particularly sensitive to cortisol. It does not establish that structural changes in the PFC contribute to the pathophysiology of neuropsychiatric conditions; the study instead examines amygdala functional connectivity after early adverse care. (LLM, conf=0.82)
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“…impact on development of amygdala FC, which may underlie the increased emotional reactivity reported in maltreated animals (Howell et al., 2014; McCormack et al., 2009; McCormack et al., 2006; Morin et al., 2019; Morin et al., 2018); and (b) whether the prolonged exposure to high cortisol…”
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“These findings are consistent with previous reports in human populations with early adverse experiences (VanTieghem & Tottenham, 2018), including adolescents and adults with histories of childhood maltreatment (Thomason et al., 2015) and in humans with PTSD (Fonzo et al., 2010b).”
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Authors: Morin, E. L., Howell, B. R., Feczko, E., Earl, E., Pincus, M., Reding, K., Kovacs-Balint, Z. A., Meyer, J. S., Styner, M., Fair, D., & Sanchez, M. M.
Affiliations: Emory University (US)
Oregon Health & Science University (US)
University of Massachusetts Amherst (US)
University of North Carolina at Chapel Hill (US)
ORCID: Morin, Elyse L.
Howell, Brittany R.
Feczko, Eric
Earl, Eric
Meyer, Jerrold S.
Styner, Martin
Fair, Damien
Venue: Development and Psychopathology
Publisher: Cambridge University Press (CUP)
Published: 2020-12
Volume: 32
Issue: 5
Pages: 1579-1596
ISSN: 0954-5794 (ISSN-L)
1469-2198
DOI: 10.1017/s0954579420001133
PMC: PMC11500993
OpenAlex: W3119797422
Cited by: 37
References: 173
Citations by year: 2026: 3 · 2025: 6 · 2024: 8 · 2023: 6 · 2022: 6 · 2021: 6 · 2020: 1
FWCI: 1.90
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.cambridge.org/core/terms (unspecified, 41 d)
Locations: Development and Psychopathology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
UNC Libraries
Funders: Georgia Clinical and Translational Science Alliance (UL1TR000128)
National Institutes of Health (UL1TR000128, MH901645, MH078105-04S1, MH 078105, MH086203, MH100029, HD079124, MH078105-01S1, P51OD011132)
Yerkes National Primate Research Center, Emory University (P51 OD011132)
National Institute of Mental Health (P50MH078105, R01MH091645, P50MH100029, F31MH086203)
National Institute on Drug Abuse (R01DA038588)
U.S. National Library of Medicine (T15LM007088)
National Center for Advancing Translational Sciences
Eunice Kennedy Shriver National Institute of Child Health and Human Development (U54HD079124, R21HD055255)
Topics: Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
Keywords: child abuse, amygdala functional connectivity, infant maltreatment, macaque model, brain development, locus coeruleus, hair cortisol, stress response, socio-emotional processing
MeSH terms: Adolescent, Amygdala, Animals, Brain, Child, Female, Humans, Magnetic Resonance Imaging, Neural Pathways, Pregnancy, Primates, Prefrontal Cortex

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Developmental outcomes of early adverse care on amygdala functional connectivity in nonhuman primates

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