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Sensitive periods of amygdala development: The role of maltreatment in preadolescence
Open accessAbstract
The amygdala is vulnerable to stress-dependent disruptions in neural development. Animal models have shown that stress increases dendritic arborization leading to larger amygdala volumes. Human studies of early stress and amygdala volume, however, remain inconclusive. This study compared amygdala volume in adults with childhood maltreatment to that in healthy controls. Eighteen participants from a longitudinal cohort and 33 cross-sectional controls (17 M/34 F, 25.5±3.1 years) completed a structural magnetic resonance imagining scan and the Maltreatment and Abuse Chronology of Exposure scale. Random forest regression with conditional trees was used to assess relative importance of exposure to adversity at each age on amygdala, thalamic or caudate volume. Severity of exposure to adversity across age accounted for 27% of the variance in right amygdala volume. Peak sensitivity occurred at 10-11 years of age, and importance of exposure at this time was highly significant based on permutation tests (p=0.003). The regression model showed that exposure during this sensitive period resulted in steep dose-response function with maximal response to even modest levels of exposure. Subjects in the highest exposure quartile (MACE-11, range=11-54) had a 9.1% greater right amygdala volume than subjects in the lowest exposure quartile (MACE-11, ≤3.5). No associations emerged between age of exposure and volume of the left amygdala or bilateral caudate or thalamus. Severity of adversity experienced at age 10-11 contributed to larger right but not left amygdala volume in adulthood. Results provide preliminary evidence that the amygdala may have a developmental sensitive period in preadolescence.
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“Interviewed in adulthood, the longitudinal participants reported more severe exposure to maltreatment in childhood than controls and reported lower levels of maternal care on the Parental Bonding Instrument than controls (p = .002).”
From Disorganized attachment in infancy predicts greater amygdala volume in adulthood (2016) · cites this paper as [38]
In the citing paper
“Severity of childhood maltreatment was significantly related to right hemisphere volumes but not to left volumes, with severity of maltreatment at 10–11 years of age the most important predictor of right amygdala volume.”
From Disorganized attachment in infancy predicts greater amygdala volume in adulthood (2016) · cites this paper as [38]
In the citing paper
“Both left and right amygdala volumes were larger among longitudinal participants than controls, with least square mean adjusted amygdala volume 3.8% greater among the longitudinal group.”
From Disorganized attachment in infancy predicts greater amygdala volume in adulthood (2016) · cites this paper as [38]
In the citing paper
“Thus, right amygdala may be differentially responsive to negative or threatening stimuli (107–109), and alterations in structure (38, 109, 110) of the right amygdala in adulthood have been particularly related to exposure to childhood maltreatment.”
From Disorganized attachment in infancy predicts greater amygdala volume in adulthood (2016) · cites this paper as [38]
In the citing paper
“Also notably, compared to cross-sectional controls, the same participants studied here exhibited right amygdala enlargement in relation to the severity of maltreatment in middle childhood, with peak effect from maltreatment between 10 and 11 years of age (38), but show left amygdala enlargement here in relation to quality of early care.”
From Disorganized attachment in infancy predicts greater amygdala volume in adulthood (2016) · cites this paper as [38]
In the citing paper
“Interestingly, we have previously discussed possible evidence for sensitive periods during which childhood maltreatment influences regional brain development, indicating a potential causal mechanism.45,46”
From Ventral striatum dysfunction in children and adolescents with reactive attachment disorder: functional MRI study (2015) · cites this paper as [46]
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BackgroundInfluentialOpposing relationships of childhood threat and deprivation with stria terminalis white matter
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“For example, periods of accelerated brain development, such as in childhood, puberty, or in early adolescence, may leave an individual particularly vulnerable to deleterious effects of early stressful exposures (Andersen & Teicher, 2008; Pechtel et al., 2014).”
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Self-citationParadoxical associations between familial affective responsiveness, stress, and amygdala reactivity.
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“Lebensjahr assoziiert zu sein scheint (31).”
Differences in Executive Functions in Minors Suffering Physical Abuse and Neglect
Manso, J. M. M., García-Baamonde, M. E., Murillo, M. D. L. R., Alonso, M. B., Barona, E. J. G., & Gómez, A. G. (2020) · Journal of Interpersonal Violence · doi:10.1177/0886260520944528 · Cited by 17
“The cognitive and behavioral repercussions for abused minors could be explained by alterations in certain areas of the brain (Davis et al., 2015; Pechtel et al., 2014).”
BackgroundMudalige, D. M., Guan, D. X., Ballard, C. G., Creese, B., Corbett, A., Pickering, E., Hampshire, A., Roach, P., Smith, E. E., & Ismail, Z. (2025) · Public Health · doi:10.1016/j.puhe.2025.02.008 · Cited by 15
Wang, Z., Cao, X., Zheng, X., Chen, Y., & Zhu, J. (2023) · Psychological Medicine · doi:10.1017/s0033291723001526 · Cited by 14
Infant behavioral reactivity predicts change in amygdala volume 12 years later
Filippi, C. A., Sachs, J. F., Phillips, D. A., Winkler, A. M., Gold, A. L., Leibenluft, E., Pine, D. S., & Fox, N. A. (2020) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2020.100776 · Cited by 14
“Then, around age 10–12 amygdala growth peaks and subsequently stagnates with slower growth from adolescence into adulthood (Payne et al., 2010; Pechtel et al., 2014; Wierenga et al., 2014).”
BackgroundResultOhashi, K., Anderson, C. M., Khan, A., Rohan, M. L., Bolger, E. A., McGreenery, C. E., & Teicher, M. H. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01260-7 · Cited by 16
Self-citationChen, S., Yin, Y., Zhang, Y., Jiang, W., Hou, Z., & Yuan, Y. (2024) · Asian Journal of Psychiatry · doi:10.1016/j.ajp.2024.103946 · Cited by 12
Vannucci, A., Fields, A., Heleniak, C. M., Bloom, P. A., Harmon, C., Nikolaidis, A., Douglas, I. J., Gibson, L., Camacho, N. L., Choy, T., et al. (2025) · Nature Mental Health · doi:10.1038/s44220-024-00355-6 · Cited by 17
“These early childhood windows contrasted those identified in adult samples 27,28 , which found that late childhood and early adolescence were important windows of crEA occurrence for neuroaffective outcomes.”
Dziak, J. J., Coffman, D. L., Reimherr, M. L., Petrovich, J., Li, R., Shiffman, S. S., & Shiyko, M. P. (2019) · Statistics Surveys · doi:10.1214/19-ss126 · Cited by 13
“, child abuse or separation from parents) have the largest harmful effect on a later health outcome [1, 2, 51, 57].”
BackgroundWindle, M. T., Gray, J. C., Lei, M., Barton, A. W., Brody, G. H., Beach, S. R. H., Galván, A., MacKillop, J. M., Clark, U. S., & Sweet, L. H. (2018) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2018.02.007 · Cited by 13
“…sensitive periods of neurodevelopment in which exposures to psychosocial and neurobiological stressors (e.g., substance use, head trauma, child maltreatment) may have a more severe impact on specific brain regions as children mature (Jensen et al., 2015; Luby et al., 2016; Pechtel et al., 2014).”
BackgroundInfluentialStructural covariance networks in children and their associations with maternal behaviors
Richmond, S., Beare, R. J., Johnson, K. A., Allen, N. B., Seal, M. L., & Whittle, S. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.06.043 · Cited by 13
Adverse childhood experiences, low self‐esteem, and salient stimulus response in eating disorders
Lagan, S., Shott, M. E., & Frank, G. (2024) · European Eating Disorders Review · doi:10.1002/erv.3064 · Cited by 12
Duffy, K. A., Sammel, M. D., Johnson, R. L., Morrison, K. E., Bale, T. L., & Epperson, C. N. (2024) · Biological Psychiatry · doi:10.1016/j.biopsych.2024.05.015 · Cited by 13
Bomyea, J. A., Simmons, A. N., Shenton, M. E., Coleman, M. J., Sylvain Bouix, A., Yogesh Rathi, A., Pasternak, O., Coimbra, R. S. M., Shutter, L., George, M. S., et al. (2019) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2019.11.012 · Cited by 13
“First, the neural effects of early stress likely depend on the type and chronicity of stressors, age at which the event(s) occur, and availability of enriching experiences to facilitate neural “catch up” (Andersen et al., 2008; Nelson et al., 2007; Pechtel et al., 2014; Teicher et al., 2006).”
Backgroundde Jongh, A., Hafkemeijer, L., Hofman, S., Slotema, K., & Hornsveld, H. K. (2024) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2024.1331876 · Cited by 15
Broekhof, R., Nordahl, H. M., Eikenæs, I. U.-M., & Selvik, S. G. (2024) · Journal of Personality Disorders · doi:10.1521/pedi.2024.38.1.19 · Cited by 11
Huguenel, B. M., Leon, S. C., Hindt, L. A., Lutz, N. M., & Osborne, J. L. (2021) · Journal of Traumatic Stress · doi:10.1002/jts.22685 · Cited by 10
Prospective prediction of first lifetime suicide attempts in a multi-site study of substance users
Trout, Z. M., Valencia, E. M. H., Kleiman, E. M., & Liu, R. T. (2016) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2016.09.020 · Cited by 11
“…the specific timing of childhood abuse experiences, with there being growing evidence that this may have a critical role in the development of risk for negative mental health outcomes (McLaughlin et al., 2010) and potential underlying pathophysiology (Lupien et al., 2009; Pechtel et al., 2014).”
BackgroundDisorders in the Executive Performance of Children Suffering Abuse
Manso, J. M. M., Murillo, M. D. L. R., Sánchez, M. E. G.-B., Merino, M. J. G., Lucas-Milán, M. G., & Guerrero‐Molina, M. (2021) · Child Abuse Review · doi:10.1002/car.2681 · Cited by 11
Early sexual or physical abuse in female and male mood disorder patients
Visioli, C., Tondo, L., Miola, A., Pinna, M., Contu, M., & Baldessarini, R. J. (2023) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2023.10.015 · Cited by 10
Türkmen, C., Tan, H., Gerhardt, S., Bougelet, E., Bernardo, M., Machunze, N., Grauduszus, Y., Sicorello, M., Demirakça, T., Kiefer, F., et al. (2024) · Addiction Biology · doi:10.1111/adb.13438 · Cited by 9
“24 While neglect during childhood is associated with an increased amygdala volume, 25,26 abuse in later stages is associated with a decrease in amygdala volume.”
BackgroundSun, J., Jiang, Y., Zilioli, S., Xie, M., Chen, L., & Lin, D. (2022) · Journal of Youth and Adolescence · doi:10.1007/s10964-022-01699-x · Cited by 10
“Moreover, preadolescent children may be particularly vulnerable to stress (e.g., abuse) because this developmental stage marks a critical period for stress-sensitive neurophysiology development (Pechtel et al., 2014; Romeo, 2013).”
BackgroundWillemen, F. E. M., van Zuiden, M., Zantvoord, J. B., de Rooij, S. R., van den Born, B. H., Hak, A. E., Thomaes, K., Segeren, M. W., Elsenburg, L. K., & Lok, A. (2022) · Frontiers in Psychology · doi:10.3389/fpsyg.2022.787029 · Cited by 12
Auswirkungen von Gewalterfahrungen auf die Wahrnehmung und das Handeln betroffener Kinder
Fegert, J. M., & Plener, P. L. (2016) · Springer eBooks · doi:10.1007/978-3-7091-1608-1_3 · Cited by 10
A Developmental Psychopathology Perspective on Foster Care Research
Fisher, P. A., Leve, L. D., Delker, B. C., Roos, L. E., & Cooper, B. (2016) · Wiley eBooks · doi:10.1002/9781119125556.devpsy312 · Cited by 10
New insights into the effects of type and timing of childhood maltreatment on brain morphometry
Grauduszus, Y., Sicorello, M., Demirakça, T., von Schröder, C., Schmahl, C. G., & Ende, G. (2024) · Scientific Reports · doi:10.1038/s41598-024-62051-w · Cited by 15
Sheriff, R. S., Hooff, M. V., Malhi, G. S., Grace, B. S., & McFARLANE, A. C. (2019) · Journal of Traumatic Stress · doi:10.1002/jts.22450 · Cited by 10
Psychometric properties of the Adulthood Trauma Inventory.
Wittbrodt, M. T., Vaccarino, V., Shah, A. J., Mayer, E. A., & Bremner, J. D. (2020) · Health Psychology · doi:10.1037/hea0000856 · Cited by 10
Cruciani, G., Boccia, M., Lingiardi, V., Giovanardi, G., Zingaretti, P., & Spitoni, G. F. (2021) · Brain Sciences · doi:10.3390/brainsci11111539 · Cited by 9
“When compared to controls, participants reporting higher exposure to maltreatment and lower levels of maternal care during childhood showed a bilateral enlargement of amygdala volumes; in addition, the severity of maltreatment at 10-11 years of age predicted right amygdala volume in adulthood in longitudinal participa…”
ResultBiological embedding of early trauma: the role of higher prefrontal synaptic strength
Tamman, A. J. F., Jiang, L., Averill, C. L., Mason, G. F., Averill, L. A., & Abdallah, C. G. (2023) · European Journal of Psychotraumatology · doi:10.1080/20008066.2023.2246338 · Cited by 9
Choi, K. R., Bravo, L., Charite, J. L., Cardona, E., Elliott, T., James, K. F., Wisk, L. E., Dunn, E. C., & Saadi, A. (2024) · Academic Pediatrics · doi:10.1016/j.acap.2024.07.006 · Cited by 10
Rethinking traditional behaviour management to better support complex trauma-surviving students
Howard, J. (2016) · International Journal on School Disaffection · doi:10.18546/ijsd.12.2.02 · Cited by 8
“As examples, the brainstem undergoes rapid development in utero prior to birth, there is intensive neural development in the limbic system during the first three to four years of life and again during puberty and the pre-frontal cortex is at its most plastic up until the mid to late 20’s (Pechtel et al., 2014; Porges,…”
BackgroundInfluentialSchalinski, I., Moran, J. K., Elbert, T. R., Reindl, V., & Wienbruch, C. (2017) · Journal of Affective Disorders · doi:10.1016/j.jad.2017.05.009 · Cited by 7
Montoro, I., Moreno-Samaniego, L., Mulet, P., Miró, C., Leunda, A., Llaurador-Coll, M., Muntané, G., Teicher, M. H., Vilella, E., & Gutiérrez‐Zotes, A. (2022) · Journal of Interpersonal Violence · doi:10.1177/08862605221106128 · Cited by 7
“A neuroimaging study conducted with 18 adults showed that the severity of CM in the period of 10–11 years was associated with larger right amygdala volumes in adulthood (Pechtel et al., 2014).”
BackgroundMethodSelf-citationSchiffer, F., Khan, A., Ohashi, K., Garcia, L. C. H., Anderson, C. M., Nickerson, L. D. H., & Teicher, M. H. (2022) · Psychology Research and Behavior Management · doi:10.2147/prbm.s357138 · Cited by 7
“Hence, we used the saved random forest to predict the outcome by adjusting degree of exposure to the predictor of interest from zero to maximum while holding all other predictors constant at as close to their median values as observed in the data to ascertain direction of effect as we have done in previous studies.(63…”
MethodSelf-citation
Metadata
- Authors
- Pechtel, P., Lyons-Ruth, K., Anderson, C. M., & Teicher, M. H.
- Affiliations
- Harvard University (US)
- Corresponding author
- Pechtel, Pia
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2014-08
- Volume
- 97
- Pages
- 236-244
- ISSN
- 1053-8119 (ISSN-L)
- PMC
- PMC4258391
- OpenAlex
- W2079348783
- Cited by
- 342
- References
- 78
- Citations by year
- 2026: 14 · 2025: 21 · 2024: 18 · 2023: 43 · 2022: 31 · 2021: 31 · 2020: 35 · 2019: 26 · 2018: 41 · 2017: 26 · 2016: 31 · 2015: 20 · 2014: 4
- FWCI
- 31.87
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NIH (UL1 RR 025758)
- Frederick Leonhardt Foundation
- Topics
- Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Social Sciences › Psychology › Clinical Psychology › Posttraumatic Stress Disorder Research
- Keywords
- amygdala development, child abuse, sensitive period, late childhood, amygdala volume, adversity exposure, dose-response relationship, thalamus, caudate nucleus, brain structure
- MeSH terms
- Adolescent, Adult, Age Factors, Amygdala, Caudate Nucleus, Child, Child Abuse, Child, Preschool, Cross-Sectional Studies, Female, Hippocampus, Humans, Infant, Longitudinal Studies, Male, Sex Factors, Stress, Psychological, Thalamus, Cohort Studies
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