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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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van Velzen, L. S., Schmaal, L., Jansen, R., Milaneschi, Y., Opmeer, E. M., Elzinga, B. M., van der Wee, N. J. A., Veltman, D. J., & Penninx, B. W. J. H. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsw086 · Cited by 58
“Previous studies have reported conflicting results, including increased (Pechtel et al., 2014), decreased (Edmiston et al., 2011; Hanson et al., 2014) and unaltered amygdala volume (Woon and Hedges, 2008) in maltreated subjects.”
MethodResultFunctional Alterations and Cerebral Variations in Humans Exposed to Early Life Stress
González-Acosta, C. A., Rojas-Cerón, C. A., & Buriticá, E. (2021) · Frontiers in Public Health · doi:10.3389/fpubh.2020.536188 · Cited by 59
Safety learning during development: Implications for development of psychopathology
Grasser, L. R., & Jovanović, T. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113297 · Cited by 57
Kaul, D., Schwab, S. G., Mechawar, N., & Matosin, N. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.01.025 · Cited by 58
Schalinski, I., & Teicher, M. H. (2015) · PLoS ONE · doi:10.1371/journal.pone.0127151 · Cited by 56
“, 3–5 years hippocampus formation, middle childhood for amygdala, and 14–16 years the frontal cortex [23,24,77].”
BackgroundSelf-citationThe Effects of Early Life Stress on the Brain and Behaviour: Insights From Zebrafish Models
Eachus, H., Choi, M., & Ryu, S. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.657591 · Cited by 55
“…CRISPR (Li et al., 2016; Albadri et al., 2017), optogenetics (Arrenberg and Driever, 2013) and live whole-brain imaging in freely behaving animals (Portugues et al., 2014; Orger and De Polavieja, 2017) make the zebrafish a particularly attractive model with which to study molecular mediators of…”
BackgroundKirsch, D. E., Nemeroff, C. B., & Lippard, E. (2020) · Adversity and Resilience Science · doi:10.1007/s42844-020-00005-7 · Cited by 61
Lipina, S. J., & Evers, K. (2017) · Frontiers in Psychology · doi:10.3389/fpsyg.2017.00061 · Cited by 63
“The experience of environmental adversity during puberty, such as maltreatment, could be associated also with changes in the volume of structures that are associated with the HPA axis (e.g., amygdala) during adulthood (Pechtel et al., 2014).”
BackgroundFujisawa, T. X., Shimada, K., Takiguchi, S., Mizushima, S. G., Kosaka, H., Teicher, M. H., & Tomoda, A. (2018) · NeuroImage Clinical · doi:10.1016/j.nicl.2018.07.018 · Cited by 52
“, 2007), as we have used in previous studies (Tomoda et al., 2012; Pechtel et al., 2014; Schalinski and Teicher, 2015; Teicher et al., 2018).”
Self-citationKim‐Spoon, J., Lauharatanahirun, N., Peviani, K. M., Brieant, A. E., Deater-Deckard, K. D., Bickel, W. K., & King‐Casas, B. (2019) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.13015 · Cited by 52
Kim, Y. J., van Rooij, S. J. H., Ely, T. D., Fani, N., Ressler, K. J., Jovanović, T., & Stevens, J. S. (2019) · Depression and Anxiety · doi:10.1002/da.22928 · Cited by 55
Caregiving influences on emotional learning and regulation: applying a sensitive period model
Gee, D. G. (2020) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2020.11.003 · Cited by 50
“For example, exposure to maltreatment between ages 10 and 11 is specifically related to amygdala volume in adulthood, relative to exposure at other ages during development [37], whereas sexual abuse at ages 3–5 and 11–13 is uniquely associated”
BackgroundPratt, M., Goldstein, A., Lévy, J., & Feldman, R. (2016) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2016.10.012 · Cited by 52
Subcortical structural variations associated with low socioeconomic status in adolescents
Jenkins, L. M., Chiang, J. J., Vause, K. J., Hoffer, L. C., Alpert, K. I., Parrish, T. B., Wang, L., & Miller, G. E. (2019) · Human Brain Mapping · doi:10.1002/hbm.24796 · Cited by 48
Mueller, I., & Tronick, E. (2020) · International Journal of Applied Psychoanalytic Studies · doi:10.1002/aps.1668 · Cited by 52
The differential effects of PTSD, MDD, and dissociation on CRP in trauma-exposed women
Powers, A. D., Dixon, H. D., Conneely, K. N., Gluck, R. L., Munoz, A. P., Rochat, C., Mendoza, H., Hartzell, G., Ressler, K. J., Bradley, B., et al. (2019) · Comprehensive Psychiatry · doi:10.1016/j.comppsych.2019.06.007 · Cited by 47
Self-reported neglect, amygdala volume, and symptoms of anxiety in adolescent boys
Roth, M. C., Humphreys, K. L., King, L. S., & Gotlib, I. H. (2018) · Child Abuse & Neglect · doi:10.1016/j.chiabu.2018.03.016 · Cited by 51
“Based on the results of previous studies that examined hemispheric interactions (Mehta et al., 2009; Pechtel et al., 2014) and on recent evidence that stress has lateralized effects on the brain that often implicate the right side (Ocklenburg, Korte, Peterburs, Wolf, & Güntürkün, 2016), we…”
BackgroundResultInfluentialTeicher, M. H., & Khan, A. (2019) · Child Maltreatment · doi:10.1177/1077559519870845 · Cited by 45
Self-citationPosttraumatic Stress and Youth Violence Perpetration: a Population-Based Cross-Sectional Study
Aebi, M., Mohler-Kuo, M., Barra, S., Schnyder, U., Maier, T., & Landolt, M. A. (2017) · European Psychiatry · doi:10.1016/j.eurpsy.2016.08.007 · Cited by 45
“Additionally, social learning mechanisms may explain why boys with PTSD have a higher risk to act violently in social situations: Exposure to PTE leads to the development of symptoms that are found to sensitise the brain to similar situational cues [37].”
BackgroundAssociation of youth age at exposure to household dysfunction with outcomes in early adulthood.
Andersen, S. H. (2021) · JAMA Network Open · doi:10.1001/jamanetworkopen.2020.32769 · Cited by 45
Zhu, J., Anderson, C. M., Ohashi, K., Khan, A., & Teicher, M. H. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02002-5 · Cited by 47
“We used the saved random forest to delineate this relationship, as we have done in prior studies [12, 13, 16], by varying degree of exposure to the signi fi cant risk factors while holding all other variables constant at their modal value to produce a predicted dose-dependent outcome.”
InfluentialSelf-citationHolschneider, D. P., Guo, Y., Mayer, E. A., & Wang, Z. (2015) · Neurobiology of Stress · doi:10.1016/j.ynstr.2015.12.003 · Cited by 44
“…also reported ELS-associated structural alterations in a number of these structures, namely the hippocampus (Frodl and O'Keane, 2013), amygdala (Pechtel et al., 2014; Whittle et al., 2013) and hypothalamus (Kuhlmann et al., 2013), cingulate and insula (Baker et al., 2013; Teicher et al.,…”
BackgroundResultInfluentialBenasi, G., Fava, G. A., & Rafanelli, C. (2020) · Psychotherapy and Psychosomatics · doi:10.1159/000506110 · Cited by 50
Butler, K., Klaus, K., Edwards, L., & Pennington, K. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.07.013 · Cited by 43
“2016) and this is in line with other research suggesting that there may be a stress-sensitive period in amygdala development which peaks at 10 to 11 years of age (Pechtel et al. 2014) and that pre-pubertal children may be more sensitive than adolescents to negative feedback mechanisms that control cortisol output (De…”
Childhood adversity and vagal regulation: A systematic review and meta-analysis
Wesarg, C., van den Akker, A. L., Oei, N. Y. L., Wiers, R. W. H. J., Staaks, J. P. C., Thayer, J. F., Williams, D. P., & Hoeve, M. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104920 · Cited by 54
“…periods across studies, broadly speaking, the amygdala appears particularly sensitive to adversity during early childhood, whereas the prefrontal cortex is likely rather sensitive during adolescence (Andersen and Teicher, 2008; Gard et al., 2020; Humphreys et al., 2019; Pechtel et al., 2014).”
BackgroundWhite, J. D., Arefin, T. M., Pugliese, A., Lee, C. H., Gassen, J., Zhang, J., & Kaffman, A. (2020) · eLife · doi:10.7554/elife.58301 · Cited by 43
“…volumes in the frontal cortex (Carrion et al., 2001; De Bellis et al., 2002; Heim et al., 2013), reduced corpus callosum volume (Teicher and Samson, 2016), increased anterior cingulate (Zuo et al., 2019), and increased AMY volume (Pechtel et al., 2014; Mehta et al., 2009; Tottenham et al., 2010).”
BackgroundO’Shea, B. Q., Demakakos, P., Cadar, D., & Kobayashi, L. C. (2021) · American Journal of Epidemiology · doi:10.1093/aje/kwab019 · Cited by 44
“These factors contribute to variation in the impact of early-life adversity on brain development (57, 58).”
BackgroundAndre, Q. R., McMorris, C. A., Kar, P., Ritter, C., Gibbard, W. B., Tortorelli, C., & Lebel, C. A. (2020) · Human Brain Mapping · doi:10.1002/hbm.25130 · Cited by 41
The body keeps the score: The neurobiological profile of traumatized adolescents
Laricchiuta, D., Panuccio, A., Picerni, E., Biondo, D., Genovesi, B., & Petrosini, L. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105033 · Cited by 51
Norton, A. R., & Abbott, M. J. (2017) · Behaviour Change · doi:10.1017/bec.2017.7 · Cited by 39
Childhood emotional neglect and oxytocin receptor variants: Association with limbic brain volumes
Womersley, J. S., Hemmings, S. M. J., Ziegler, C., Gutridge, A., Ahmed-Leitao, F., Rosenstein, D., Domschke, K., & Seedat, S. (2019) · The World Journal of Biological Psychiatry · doi:10.1080/15622975.2019.1584331 · Cited by 42
The Role of the Thalamus in Post-Traumatic Stress Disorder
Yoshii, T. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22041730 · Cited by 40
“Volume reduction (not significant) [26–28] Volume loss in the right thalamus was detected in PTSD malingerers [29] Negative correlation between volume of right thalamus and re-experiencing [30] Volume loss in the bilateral thalamus in pain meta-analysis [16] Negative correlation between right thalamic volume and child…”
BackgroundTottenham, N. (2020) · Development and Psychopathology · doi:10.1017/s0954579420001169 · Cited by 46
Lecei, A., & van Winkel, R. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.11.010 · Cited by 45
Superficial white matter microstructure affects processing speed in cerebral small vessel disease
Wang, S., Zhang, F., Huang, P., Hong, H., Jiaerken, Y., Yu, X., Zhang, R., Zeng, Q., Zhang, Y., Kikinis, R., et al. (2022) · Human Brain Mapping · doi:10.1002/hbm.26004 · Cited by 34
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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