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Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation
Open accessAbstract
Early adversity, for example poor caregiving, can have profound effects on emotional development. Orphanage rearing, even in the best circumstances, lies outside of the bounds of a species‐typical caregiving environment. The long‐term effects of this early adversity on the neurobiological development associated with socio‐emotional behaviors are not well understood. Seventy‐eight children, who include those who have experienced orphanage care and a comparison group, were assessed. Magnetic resonance imaging (MRI) was used to measure volumes of whole brain and limbic structures (e.g. amygdala, hippocampus). Emotion regulation was assessed with an emotional go‐nogo paradigm, and anxiety and internalizing behaviors were assessed using the Screen for Child Anxiety Related Emotional Disorders, the Child Behavior Checklist, and a structured clinical interview. Late adoption was associated with larger corrected amygdala volumes, poorer emotion regulation, and increased anxiety. Although more than 50% of the children who experienced orphanage rearing met criteria for a psychiatric disorder, with a third having an anxiety disorder, the group differences observed in amygdala volume were not driven by the presence of an anxiety disorder. The findings are consistent with previous reports describing negative effects of prolonged orphanage care on emotional behavior and with animal models that show long‐term changes in the amygdala and emotional behavior following early postnatal stress. These changes in limbic circuitry may underlie residual emotional and social problems experienced by children who have been internationally adopted.
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Maltreated children have higher amygdala volume.
“In the same vein, it has been shown that maltreated children have higher amygdala volume (Lupien et al., 2011;Tottenham et al., 2010).”
From Physiological feelings (2019) · cites this paper as Tottenham et al., 2010
The Results (Morphometry; page not provided) report significantly larger amygdala volumes in children adopted after 15 months of institutional care than in early-adopted and comparison children. They report no significant difference between the institutional-care group as a whole and the comparison group. The claim generalizes this finding to maltreated children broadly and omits the duration-of-care qualification. (LLM, conf=0.88)
Experimental — accuracy not yet measuredAtypical presentations of these same stress-response systems have implications for understanding emotion dysregulation and a range of internalizing and externalizing symptoms.
“and recent data suggest that atypical presentations of these same systems have implications for understanding emotion dysregulation (Miller et al. 2017b, Tottenham et al. 2010) and a range of both internalizing and externalizing symptoms (Burghy et al. 2012, Chen et al. 2015, Nederhof et al. 2015, Slavich & Irwin 2014).”
From Adolescent Suicide as a Failure of Acute Stress-Response Systems. (2019) · cites this paper as Tottenham et al. 2010
Children with histories of severe neglect show marked problems in many other domains, including psychopathology, social competence, emotional reactivity, and academic achievement.
“children with histories of severe neglect show marked problems in many other domains, including psychopathology (34), social competence (35), emotional reactivity (36), and academic achievement (37)”
From Long-term effects of institutional rearing, foster care, and brain activity on memory and executive functioning (2019) · cites this paper as [36]
Induced early life stress is associated with amygdalar hypertrophy in primates, with increased volumes also found in children exposed to neglect and mild maternal disengagement.
“Induced early life stress has been associated with amygdalar hypertrophy in primates (73), with increased volumes also found in children exposed to both neglect (74) and mild maternal disengagement (75).”
From Childhood Trauma, the HPA Axis and Psychiatric Illnesses: A Targeted Literature Synthesis (2022) · cites this paper as [74]
Disorganized attachment during infancy predicts greater amygdala volume.
“Longitudinal studies27 as well as studies of children raised in orphanages28 indicate that disorganized attachment during infancy predicts greater amygdala volume—a hypothesized biomarker of difficulty with emotion regulation28.”
From Psychobiological factors of resilience and depression in late life (2019) · cites this paper as [28]
The hippocampus is highly stress susceptible with sensitive periods in early childhood and puberty, but stress effects on it are less persistent.
“The hippocampus is also highly stress susceptible, with sensitive periods in early childhood and during the pubertal period, but effects of stress are less persistent (15, 24, 47).”
From Disorganized attachment in infancy predicts greater amygdala volume in adulthood (2016) · cites this paper as [24]
Extreme deprivation dramatically alters neural architecture and functioning.
“Extreme deprivation dramatically alters neural architecture and functioning.”
From Normalization of EEG activity among previously institutionalized children placed into foster care: A 12-year follow-up of the Bucharest Early Intervention Project (2016) · cites this paper as Tottenham et al., 2010
Children deprived of a stable responsive caregiver show high insecure and disorganized attachment and atypical affective development, including heightened emotional reactivity, accelerated amygdala development, poor emotion regulation, and atypical stress reactivity.
“Children deprived of a stable and responsive caregiver exhibit high levels of insecure and disorganized attachment and atypical affective development characterized by heightened emotional reactivity, accelerated functional development of the amygdala, poor emotion regulation, and atypical stress reactivity.(25, 32–37)”
From Neglect as a violation of species-expectant experience: neurodevelopmental consequences (2017) · cites this paper as [33]
Smaller left amygdala and larger right amygdala volumes were reported in a small study of previously institutionalized children, but these patterns have not been replicated in larger studies.
“Smaller left amygdala volume and larger right amygdala volume were reported in a small study of previously-institutionalized children,(128) but these patterns have not been replicated in larger studies.(33, 129)”
From Neglect as a violation of species-expectant experience: neurodevelopmental consequences (2017) · cites this paper as [33]
Stress-induced amygdala morphology and volume changes seem to persist.
“In contrast, stress-induced amygdala morphology and volume changes seem to persist (Vyas et al., 2002, Adamec et al., 2005, Tottenham et al., 2010).”
From The impact of developmental timing for stress and recovery (2015) · cites this paper as Tottenham et al., 2010
In children reared in orphanages abroad and later adopted into stable families, earlier adoption is better.
“In studies of children reared in orphanages abroad and later adopted into stable families, the findings consistently suggest that earlier adoption is better (Rutter, 1998, Gunnar et al., 2000, Tottenham et al., 2010).”
From The impact of developmental timing for stress and recovery (2015) · cites this paper as Tottenham et al., 2010
Human maternal deprivation early in life is associated with atypical frontoamygdala development and function, including greater amygdala volume, amygdala hyperactivity, and less prefrontal activity to emotional stimuli.
“Human studies of maternal deprivation early in life have shown atypical frontoamygdala development and function with greater amygdala volume, amygdala hyperactivity, and less prefrontal activity to emotional stimuli, as well as long-term impairments in anxiety and social behavior (Mehta et al., 2009, Zeanah et al., 2009, Tottenham et al., 2010, Tottenham et al., 2011).”
From The impact of developmental timing for stress and recovery (2015) · cites this paper as Tottenham et al., 2010, Tottenham et al., 2011
Human maternal deprivation early in life is associated with long-term impairments in anxiety and social behavior.
“Human studies of maternal deprivation early in life have shown atypical frontoamygdala development and function with greater amygdala volume, amygdala hyperactivity, and less prefrontal activity to emotional stimuli, as well as long-term impairments in anxiety and social behavior (Mehta et al., 2009, Zeanah et al., 2009, Tottenham et al., 2010, Tottenham et al., 2011).”
From The impact of developmental timing for stress and recovery (2015) · cites this paper as Tottenham et al., 2010, Tottenham et al., 2011
Reduced amygdala volume in youth with CD is counter to the enlarged amygdala volumes found in children with experiences of early deprivation.
“The finding of reduced amygdala volume is counter to the enlarged amygdala volumes found in children with experiences of early deprivation (Tottenham et al, 2010).”
From Deviations from the expectable environment in early childhood and emerging psychopathology (2015) · cites this paper as Tottenham et al, 2010
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“his lack of an early attachment figure, a central feature of early uman experience, has been investigated and reviewed extenively by Tottenham and colleagues (Gee et al., 2013; Tottenham, 012; Tottenham et al., 2010), and as such we do not review these ffects in depth.”
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More than a feeling: A unified view of stress measurement for population science
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“…early life stress to disease development may be mediated by early changes in neural pathways regulating stress, such as amygdala connectivity (e.g., Tottenham et al., 2010), biological pathways such as chronic inflammation in adulthood (Slopen et al., 2010; Surtees et al., 2003; Danese et al.,…”
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The stress acceleration hypothesis: effects of early-life adversity on emotion circuits and behavior
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Self-citationElevated amygdala response to faces following early deprivation
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Self-citationSocial Structure, Adversity, Toxic Stress, and Intergenerational Poverty: An Early Childhood Model
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“2 (11.10) 28 (84.80) x2 = 26.15 .001 t1:8 U N C O R R E C was found in children who had experienced prolonged institutional deprivation (Mehta et al., 2009; Tottenham et al., 2010) or rearing by chronically depressedmothers (Lupien et al., 2011).”
BackgroundResultInfluentialGray matter abnormalities in childhood maltreatment: a voxel-wise meta-analysis
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Early-life stress has persistent effects on amygdala function and development in mice and humans
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Self-citationStress and the adolescent brain
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Self-citationEffects of early life stress on depression, cognitive performance and brain morphology
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“…data suggest that atypical presentations of these same systems have implications for understanding emotion dysregulation (Miller et al. 2017b, Tottenham et al. 2010) and a range of both internalizing and externalizing symptoms (Burghy et al. 2012, Chen et al. 2015, Nederhof et al. 2015,…”
BackgroundDeviations from the expectable environment in early childhood and emerging psychopathology
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“In the same vein, it has been shown that maltreated children have higher amygdala volume (Lupien et al., 2011; Tottenham et al., 2010).”
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FKBP5 and emotional neglect interact to predict individual differences in amygdala reactivity
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Childhood Trauma, the HPA Axis and Psychiatric Illnesses: A Targeted Literature Synthesis
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“Induced early life stress has been associated with amygdalar hypertrophy in primates (73), with increased volumes also found in children exposed to both neglect (74) and mild maternal disengagement (75).”
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The potential of infant fMRI research and the study of early life stress as a promising exemplar
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Insecure attachment during infancy predicts greater amygdala volumes in early adulthood
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Social scaffolding of human amygdala-mPFCcircuit development
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Indiscriminate Amygdala Response to Mothers and Strangers After Early Maternal Deprivation
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Measuring Stress in Young Children Using Hair Cortisol: The State of the Science
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Early secure attachment as a protective factor against later cognitive decline and dementia
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Early deprivation alters structural brain development from middle childhood to adolescence
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Metadata
- Authors
- Tottenham, N., Hare, T. A., Quinn, B. T., McCarry, T. W., Nurse, M., Gilhooly, T., Millner, A., Galvan, A., Davidson, M. C., Eigsti, I., Thomas, K. M., Freed, P. J., Booma, E. S., Gunnar, M. R., Altemus, M., Aronson, J., & Casey, B. J.
- Affiliations
- Cornell University (US)
- California Institute of Technology (US)
- University of Massachusetts Amherst (US)
- University of Connecticut (US)
- University of Minnesota (US)
- Columbia University (US)
- Corresponding author
- Tottenham, Nim
- ORCID
- Venue
- Developmental Science
- Publisher
- Wiley
- Published
- 2009-12-09
- Volume
- 13
- Issue
- 1
- Pages
- 46-61
- ISSN
- 1363-755X (ISSN-L)
- 1467-7687
- PMC
- PMC2817950
- OpenAlex
- W1890675559
- Cited by
- 905
- References
- 87
- Citations by year
- 2026: 21 · 2025: 35 · 2024: 25 · 2023: 48 · 2022: 51 · 2021: 65 · 2020: 125 · 2019: 76 · 2018: 70 · 2017: 62 · 2016: 69 · 2015: 65 · 2014: 64 · 2013: 47 · 2012: 43
- FWCI
- 68.51
- Type
- journal article
- Language
- en
- Open access
- green
- www.zora.uzh.ch
- Licence
- Locations
- Developmental Science (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, other-oa)
- PubMed Central (acceptedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- National Institute of Mental Health (P50MH079513, R01MH073175, R01MH091864)
- Topics
- Social Sciences › Sociology and Political Science › Child Welfare and Adoption
- Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
- Social Sciences › Psychology › Clinical Psychology › Child and Adolescent Psychosocial and Emotional Development
- Keywords
- institutional upbringing, amygdala volume, emotion regulation, childhood adversity, late adoption, anxiety disorders, internalizing problems, limbic system, hippocampus, emotional development, postpartum stress, social-emotional behavior
- MeSH terms
- Adaptation, Psychological, Adolescent, Adoption, Age Factors, Amygdala, Analysis of Variance, Brain Mapping, Child, Child Behavior Disorders, Emotions, Facial Expression, Female, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Neuropsychological Tests, Photic Stimulation, Surveys and Questionnaires, Orphanages, Checklist
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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