The DOI matches its Crossref record; 49 of the 49 references it cites were found in a registry or an index.
Immature integration and segregation of emotion-related brain circuitry in young children
Open accessAbstract
The human brain undergoes protracted development, with dramatic changes in expression and regulation of emotion from childhood to adulthood. The amygdala is a brain structure that plays a pivotal role in emotion-related functions. Investigating developmental characteristics of the amygdala and associated functional circuits in children is important for understanding how emotion processing matures in the developing brain. The basolateral amygdala (BLA) and centromedial amygdala (CMA) are two major amygdalar nuclei that contribute to distinct functions via their unique pattern of interactions with cortical and subcortical regions. Almost nothing is currently known about the maturation of functional circuits associated with these amygdala nuclei in the developing brain. Using intrinsic connectivity analysis of functional magnetic resonance imaging data, we investigated developmental changes in functional connectivity of the BLA and CMA in twenty-four 7- to 9-y-old typically developing children compared with twenty-four 19- to 22-y-old healthy adults. Children showed significantly weaker intrinsic functional connectivity of the amygdala with subcortical, paralimbic, and limbic structures, polymodal association, and ventromedial prefrontal cortex. Importantly, target networks associated with the BLA and CMA exhibited greater overlap and weaker dissociation in children. In line with this finding, children showed greater intraamygdala connectivity between the BLA and CMA. Critically, these developmental differences were reproducibly identified in a second independent cohort of adults and children. Taken together, our findings point toward weak integration and segregation of amygdala circuits in young children. These immature patterns of amygdala connectivity have important implications for understanding typical and atypical development of emotion-related brain circuitry.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Structural and functional connectivity between the amygdala and cortical brain regions undergoes dramatic maturation across adolescence (Qin et al., 2012, Gabard-Durnam et al., 2014).”
From Developmental sex differences in resting state functional connectivity of amygdala sub-regions (2015) · cites this paper as Qin et al., 2012
In the citing paper
“Previous research has shown coupling of mPFC and all amygdala sub-regions with increasing age (Roy et al., 2009, Qin et al., 2012, Gabard-Durnam et al., 2014),”
From Developmental sex differences in resting state functional connectivity of amygdala sub-regions (2015) · cites this paper as Qin et al., 2012
In the citing paper
“which corresponds with adult RSFC patterns of amygdala sub-regions (Roy et al., 2009, Qin et al., 2012, Gabard-Durnam et al., 2014), albeit with varying effects by sex.”
From Developmental sex differences in resting state functional connectivity of amygdala sub-regions (2015) · cites this paper as Qin et al., 2012
In the citing paper
“Previous work has found distinct functional connectivity patterns, as measured with RSFC, across amygdalar nuclei (Roy et al., 2009, Li et al., 2012, Qin et al., 2012, Gabard-Durnam et al., 2014), specifically different patterns of age-dependent positive connectivity between amygdalar nuclei and ventromedial PFC (vmPFC), temporal, and subcortical regions, as well as negative connectivity with pari”
From Developmental sex differences in resting state functional connectivity of amygdala sub-regions (2015) · cites this paper as Qin et al., 2012
In the citing paper
“which is in accordance with a healthy developmental trajectory (Roy et al., 2009, Qin et al., 2012, Gabard-Durnam et al., 2014).”
From Developmental sex differences in resting state functional connectivity of amygdala sub-regions (2015) · cites this paper as Qin et al., 2012
In the citing paper
“As such, RSFC analyses were not conducted with either left or right CMA seed regions, which limits direct comparisons with existing amygdala sub-region RSFC studies (Roy et al., 2009, Li et al., 2012, Qin et al., 2012, Gabard-Durnam et al., 2014).”
From Developmental sex differences in resting state functional connectivity of amygdala sub-regions (2015) · cites this paper as Qin et al., 2012
Citations
Cites
LeDoux, J. E. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.155 · Cited by 8,444
Dissociable intrinsic connectivity networks for salience processing and executive control
Seeley, W. W., Menon, V., Schatzberg, A. F., Keller, J., Glover, G. H., Kenna, H., Reiss, A. L., & Greicius, M. D. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5587-06.2007 · Cited by 7,426
Self-citationSpontaneous fluctuations in brain activity observed with functional magnetic resonance imaging
Fox, M. D., & Raichle, M. E. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2201 · Cited by 6,700
Functional connectivity in the resting brain: a network analysis of the default mode hypothesis
Greicius, M. D., Krasnow, B., Reiss, A. L., & Menon, V. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0135058100 · Cited by 6,358
Self-citationMaldjian, J. A., Laurienti, P. J., Kraft, R., & Burdette, J. H. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00169-1 · Cited by 5,066
A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data
Eickhoff, S. B., Stephan, K. E., Mohlberg, H., Grefkes, C., Fink, G. R., Amunts, K., & Zilles, K. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2004.12.034 · Cited by 4,033
Representational similarity analysis-connecting the branches of systems neuroscience
Kriegeskorte, N. (2008) · Frontiers in Systems Neuroscience · doi:10.3389/neuro.06.004.2008 · Cited by 3,355
Cognitive and affective development in adolescence
Steinberg, L. (2005) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2004.12.005 · Cited by 2,978
The amygdala: vigilance and emotion
Davis, M., & Whalen, P. J. (2001) · Molecular Psychiatry · doi:10.1038/sj.mp.4000812 · Cited by 2,882
Adolphs, R., Tranel, D., Damasio, H., & Damasio, A. (1994) · Nature · doi:10.1038/372669a0 · Cited by 2,360
Prediction of individual brain maturity using fMRI
Dosenbach, N. U. F., Nardos, B., Cohen, A. L., Fair, D. A., Power, J. D., Church, J. A., Nelson, S. M., Wig, G. S., Vogel, A. C., Lessov-Schlaggar, C. N., et al. (2010) · Science · doi:10.1126/science.1194144 · Cited by 2,183
Information-based functional brain mapping
Kriegeskorte, N., Goebel, R., & Bandettini, P. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600244103 · Cited by 2,113
The social brain in adolescence
Blakemore, S.-J. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2353 · Cited by 1,896
The Neural Bases of Emotion Regulation: Reappraisal and Suppression of Negative Emotion
Goldin, P. R., McRae, K., Ramel, W., & Gross, J. J. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.05.031 · Cited by 1,886
Pessoa, L., & Adolphs, R. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2920 · Cited by 1,794
Neurodevelopmental Trajectories of the Human Cerebral Cortex
Shaw, P., Kabani, N. J., Lerch, J. P., Eckstrand, K., Lenroot, R., Gogtay, N., Greenstein, D., Clasen, L., Evans, A., Rapoport, J. L., et al. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.5309-07.2008 · Cited by 1,644
Brain Structures Differ between Musicians and Non-Musicians
Christian Gaser, B., & Gottfried Schlaug, A. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-27-09240.2003 · Cited by 1,626
Mapping brain maturation and cognitive development during adolescence
Paus, T. (2005) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2004.12.008 · Cited by 1,348
LeDoux, J. (2007) · Current Biology · doi:10.1016/j.cub.2007.08.005 · Cited by 1,281
Amunts, K., Kedo, O., Kindler, M., Pieperhoff, P., Mohlberg, H., Shah, N. J., Habel, U., Schneider, F., & Zilles, K. (2005) · Anatomy and Embryology · doi:10.1007/s00429-005-0025-5 · Cited by 1,264
Controlling the familywise error rate in functional neuroimaging: a comparative review
Nichols, T. E., & Hayasaka, S. (2003) · Statistical Methods in Medical Research · doi:10.1191/0962280203sm341ra · Cited by 1,249
Toga, A. W., Thompson, P. M., & Sowell, E. R. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.01.007 · Cited by 872
Development of large-scale functional brain networks in children
Supekar, K., Musen, M., & Menon, V. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000157 · Cited by 807
Self-citationFunctional connectivity of the human amygdala using resting state fMRI
Roy, A. K., Shehzad, Z., Margulies, D. S., Kelly, A. M. C., Uddin, L. Q., Gotimer, K., Biswal, B. B., Castellanos, F. X., & Milham, M. P. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2008.11.030 · Cited by 749
Self-citationWhite matter maturation reshapes structural connectivity in the late developing human brain
Hagmann, P., Sporns, O., Madan, N., Cammoun, L., Pienaar, R., Wedeen, V. J., Meuli, R., Thiran, J.-P., & Grant, P. E. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1009073107 · Cited by 700
Etkin, A., Prater, K. E., Schatzberg, A. F., Menon, V., & Greicius, M. D. (2009) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2009.104 · Cited by 664
Self-citationSpiral‐in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts
Glover, G. H., & Law, C. S. W. (2001) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1222 · Cited by 600
Amygdala Response to Fearful Faces in Anxious and Depressed Children
Thomas, K. M. (2001) · Archives of General Psychiatry · doi:10.1001/archpsyc.58.11.1057 · Cited by 582
Bourgeois, J., & Rakic, P. (1993) · The Journal of Neuroscience · doi:10.1523/jneurosci.13-07-02801.1993 · Cited by 567
Synaptic development of the cerebral cortex: implications for learning, memory and mental illness
(1994) · Progress in Brain Research · doi:10.1016/s0079-6123(08)60543-9 · Cited by 565
Østby, Y., Tamnes, C. K., Fjell, A. M., Westlye, L. T., Due-Tønnessen, P., & Walhovd, K. B. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1242-09.2009 · Cited by 480
Self‐navigated spiral fMRI: Interleaved versus single‐shot
Glover, G. H., & Lai, S. (1998) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910390305 · Cited by 476
Amygdala response to facial expressions in children and adults.
Thomas, K. M., Drevets, W. C., Whalen, P. J., Eccard, C. H., Dahl, R. E., Ryan, N. D., & Casey, B. J. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(00)01066-0 · Cited by 470 · cited 2×
“The weaker connectivity of the amygdala with these regions in children may account for the poorer performance in tasks requiring rapid and accurate recognition and discrimination of different types of emotions (26, 27).”
BackgroundGreater Neural Pattern Similarity Across Repetitions Is Associated with Better Memory
Xue, G., Dong, Q., Chen, C., Lu, Z., Mumford, J. A., & Poldrack, R. A. (2010) · Science · doi:10.1126/science.1193125 · Cited by 383
A developmental examination of amygdala response to facial expressions
Guyer, A. E., Monk, C. S., McClure-Tone, E. B., Nelson, E. E., Roberson-Nay, R., Adler, A. D., Fromm, S. J., Leibenluft, E., Pine, D. S., & Ernst, M. (2008) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2008.20114 · Cited by 357
Uddin, L. Q. (2010) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2010.00021 · Cited by 343
Self-citationBurgund, E. D., Kang, H. C., Kelly, J. E., Buckner, R. L., Snyder, A. Z., Petersen, S. E., & Schlaggar, B. L. (2002) · NeuroImage · doi:10.1006/nimg.2002.1174 · Cited by 329
Amygdala Automaticity in Emotional Processing
DOLAN, R. J., & VUILLEUMIER, P. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07093.x · Cited by 263
Children's understanding of emotion from facial expressions and situations: A review.
Gross, A. L., & Ballif, B. (1991) · Developmental Review · doi:10.1016/0273-2297(91)90019-k · Cited by 213
Developing connections for affective regulation: age-related changes in emotional brain connectivity
Perlman, S. B., & Pelphrey, K. A. (2011) · Journal of Experimental Child Psychology · doi:10.1016/j.jecp.2010.08.006 · Cited by 198
Ventral visual cortex in humans: Cytoarchitectonic mapping of two extrastriate areas
Rottschy, C., Eickhoff, S. B., Schleicher, A., Mohlberg, H., Kujovic, M., Zilles, K., & Amunts, K. (2007) · Human Brain Mapping · doi:10.1002/hbm.20348 · Cited by 173
Dougherty, D. D., Rauch, S. L., Deckersbach, T., Marci, C., Loh, R., Shin, L. M., Alpert, N. M., Fischman, A. J., & Fava, M. (2004) · Archives of General Psychiatry · doi:10.1001/archpsyc.61.8.795 · Cited by 161
Talent in the taxi: a model system for exploring expertise
Woollett, K., Spiers, H. J., & Maguire, E. A. (2009) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2008.0288 · Cited by 108
Laterobasal Amygdalar Enlargement in 6- to 7-Year-Old Children With Autism Spectrum Disorder
Kim, J. E., Lyoo, I. K., Estes, A. M., Renshaw, P. F., Shaw, D., Friedman, S. D., Kim, D. J., Yoon, S. J., Hwang, J., & Dager, S. R. (2010) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2010.148 · Cited by 101
Comparison of functional connectivity in default mode and sensorimotor networks at 3 and 7T
Hale, J. R., Brookes, M. J., Hall, E. L., Zumer, J. M., Stevenson, C. M., Francis, S., & Morris, P. G. (2010) · Magnetic Resonance Materials in Physics Biology and Medicine · doi:10.1007/s10334-010-0220-0 · Cited by 51
Challenges and methods in developmental neuroimaging
Crone, E. A., Poldrack, R. A., & Durston, S. (2010) · Human Brain Mapping · doi:10.1002/hbm.21053 · Cited by 22
Functional Connectivity, Neurocognitive Networks, and Brain Dynamics
Menon, V. (2012) · The MIT Press eBooks · doi:10.7551/mitpress/9108.003.0004 · Cited by 10
Self-citationDevelopment of Emotion and Social Reasoning in Adolescence
Crone, E. A., & Güroğlu, B. (2013) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780199988709.013.0008 · Cited by 8
Giedd (1996) · doi:10.1002/(sici)1096-9861(19960304)366:2
Cited by
Sorted by citations
Rudolph, M. D., Graham, A. M., Feczko, E., Miranda-Dominguez, O., Rasmussen, J. M., Nardos, R., Entringer, S., Wadhwa, P. D., Buss, C., & Fair, D. A. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0128-y · Cited by 374
Gabard-Durnam, L. J., Flannery, J., Goff, B., Gee, D. G., Humphreys, K. L., Telzer, E., Hare, T., & Tottenham, N. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.03.038 · Cited by 372
Developmental pathways to functional brain networks: emerging principles
Menon, V. (2013) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2013.09.015 · Cited by 354
Self-citationHippocampal-neocortical functional reorganization underlies children's cognitive development
Qin, S., Cho, S., Chen, T., Rosenberg‐Lee, M., Geary, D. C., & Menon, V. (2014) · Nature Neuroscience · doi:10.1038/nn.3788 · Cited by 283
Self-citationQin, S., Young, C. B., Duan, X., Chen, T., Supekar, K., & Menon, V. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.10.006 · Cited by 249
Self-citation
Metadata
- Authors
- Qin, S., Young, C. B., Supekar, K., Uddin, L. Q., & Menon, V.
- Affiliations
- Stanford Medicine (US)
- Northwestern University (US)
- Stanford University (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2012-04-30
- Volume
- 109
- Issue
- 20
- Pages
- 7941-7946
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3356602
- OpenAlex
- W1965642520
- Cited by
- 130
- References
- 49
- Citations by year
- 2026: 3 · 2025: 9 · 2024: 3 · 2023: 5 · 2022: 10 · 2021: 11 · 2020: 5 · 2019: 9 · 2018: 8 · 2017: 14 · 2016: 15 · 2015: 16 · 2014: 12 · 2013: 9 · 2012: 1
- FWCI
- 6.22
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (446.10.010)
- National Institutes of Health
- National Institute of Mental Health (K01MH092288)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD047520, HD059205, R01HD047520, R01HD059205)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Social Sciences › Psychology › Clinical Psychology › Child and Adolescent Psychosocial and Emotional Development
- Keywords
- amygdala, basolateral amygdala, centromedial amygdala, intrinsic functional connectivity, brain development, emotional processing, children, ventromedial prefrontal cortex, limbic system, integration and segregation, amygdala connectivity
- MeSH terms
- Age Factors, Amygdala, Brain Mapping, Child, Emotions, Humans, Magnetic Resonance Imaging, Models, Neurological, Neural Pathways, Young Adult
About these checks
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review