Development of Anterior Cingulate Functional Connectivity from Late Childhood to Early Adulthood

Kelly, A. M. C.; Di Martino, A.; Uddin, L. Q.; Shehzad, Z.; Gee, D. G.; Reiss, P. T.; Margulies, D. S.; Castellanos, F. X.; Milham, M. P.

doi:10.1093/cercor/bhn117

Cited by 572Functional Brain Connectivity StudiesAdvanced Neuroimaging Techniques and ApplicationsNeural and Behavioral Psychology Studies

Development of Anterior Cingulate Functional Connectivity from Late Childhood to Early Adulthood

Kelly, A. M. C., Di Martino, A., Uddin, L. Q., Shehzad, Z., Gee, D. G., Reiss, P. T., Margulies, D. S., Castellanos, F. X. +1 more·2009·Cerebral Cortex

DOI 10.1093/cercor/bhn117

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Abstract

Human cerebral development is remarkably protracted. Although microstructural processes of neuronal maturation remain accessible only to morphometric post-mortem studies, neuroimaging tools permit the examination of macrostructural aspects of brain development. The analysis of resting-state functional connectivity (FC) offers novel possibilities for the investigation of cerebral development. Using seed-based FC methods, we examined the development of 5 functionally distinct cingulate-based intrinsic connectivity networks (ICNs) in children (n = 14, 10.6 +/- 1.5 years), adolescents (n = 12, 15.4 +/- 1.2) and young adults (n=14, 22.4 +/- 1.2). Children demonstrated a more diffuse pattern of correlation with voxels proximal to the seed region of interest (ROI) ("local FC"), whereas adults exhibited more focal patterns of FC, as well as a greater number of significantly correlated voxels at long distances from the seed ROI. Adolescents exhibited intermediate patterns of FC. Consistent with evidence for different maturational time courses, ICNs associated with social and emotional functions exhibited the greatest developmental effects. Our findings demonstrate the utility of FC for the study of developing functional organization. Moreover, given that ICNs are thought to have an anatomical basis in neuronal connectivity, measures of FC may provide a quantitative index of brain maturation in healthy subjects and those with neurodevelopmental disorders.

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Prior to 2012, multiple studies found that functional connectivity between anatomically proximate ROIs gradually decreased, while long-range functional connections, especially anterior-posterior links, gradually increased until adulthood.
“Prior to 2012, multiple studies had found that functional connectivity between anatomically proximate ROIs gradually decreased, whereas long-range functional connections, especially anterior-posterior links, gradually increased until adulthood (Dosenbach et al., 2010; Fair et al., 2009; Kelly et al., 2009; Supekar et al., 2009).”
From Development of large-scale functional networks from birth to adulthood: A guide to the neuroimaging literature (2017) · cites this paper as Kelly et al., 2009
The greatest development in cingulate-based ICNs occurs in those associated with social and emotional functions.
“Also, the greatest development occurred in those ICNs associated with social and emotional functions.”
From Emerging Adulthood, a Pre-adult Life-History Stage (2020) · cites this paper as [35]
The pattern of correlation with voxels proximal to the seed region of interest in cingulate-based ICNs is age-dependent: diffuse in children, less diffuse in adolescents, and becoming focal in young adults.
“They found that the pattern of correlation with voxels proximal to the seed region of interest was age-dependent: the pattern was diffuse in children (mean age 10.6 years), was less diffuse in adolescents (mean age 15.4 years), and showed signs of becoming focal in young adults (mean age 22.4 years).”
From Emerging Adulthood, a Pre-adult Life-History Stage (2020) · cites this paper as [35]
Brain maturation extends beyond adolescence into young adulthood.
“Kelly and colleagues provide additional evidence that brain maturation extends beyond adolescence into young adulthood (35).”
From Emerging Adulthood, a Pre-adult Life-History Stage (2020) · cites this paper as [35]
Diffuse patterns of local FC are gradually replaced by a distributed architecture, dominated by focal long-range connections.
“diffuse patterns of local FC are gradually replaced by a distributed architecture, dominated by focal long-range connections (3-6).”
From Aberrant Striatal Functional Connectivity in Children with Autism (2011) · cites this paper as [5]

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Functional Coactivation Map of the Human Brain
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A comparison of resting-state brain activity in humans and chimpanzees
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FUNCTIONAL CONNECTIVITY IN SCHIZOPHRENIA
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Functional MRI of Global and Local Processing in Children
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Developmental changes in brain metabolism in sedated rhesus macaques and vervet monkeys revealed by positron emission tomography
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“A similar result was observed in monkeys (Jacobs et al. 1995), supporting the idea that the age-related changes in glucose metabolism reflect the periods of synaptic and neurotransmitter excess and”
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Unconscious networking
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Untitled work
Huttenlocher (1997) · doi:10.1002/(sici)1096-9861(19971020)387:2

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Toward discovery science of human brain function
Biswal, B. B., Mennes, M., Zuo, X.-N., Gohel, S., Kelly, C., Smith, S. M., Beckmann, C. F., Adelstein, J. S., Buckner, R. L., Colcombe, S., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911855107 · Cited by 2,970 · see citing works
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Neurodegenerative Diseases Target Large-Scale Human Brain Networks
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Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization
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Functional brain networks develop from a local to distributed organization
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Normal development of brain circuits
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A Baseline for the Multivariate Comparison of Resting-State Networks
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Resting-State fMRI: A Review of Methods and Clinical Applications
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The Resting Brain: Unconstrained yet Reliable
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Changes in structural and functional connectivity among resting-state networks across the human lifespan
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Longitudinal Analysis of Neural Network Development in Preterm Infants
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Development of large-scale functional brain networks in children
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The NKI-Rockland Sample: A Model for Accelerating the Pace of Discovery Science in Psychiatry
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The development of human functional brain networks
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Functional connectivity of the human amygdala using resting state fMRI
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Reliable intrinsic connectivity networks: test-retest evaluation using ICA and dual regression approach
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Anterior cingulate cortex: unique role in cognition and emotion
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Sleep, cognition, and behavioral problems in school-age children: a century of research meta-analyzed.
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Functional Brain Correlates of Social and Nonsocial Processes in Autism Spectrum Disorders: An Activation Likelihood Estimation Meta-Analysis
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Development of functional and structural connectivity within the default mode network in young children
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Dynamic reconfiguration of structural and functional connectivity across core neurocognitive brain networks with development
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Evaluation of ICA-AROMA and alternative strategies for motion artifact removal in resting state fMRI
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Aberrant Striatal Functional Connectivity in Children with Autism
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Topological organization of the human brain functional connectome across the lifespan
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Development of large-scale functional networks from birth to adulthood: A guide to the neuroimaging literature
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“…had found that functional connectivity between anatomically proximate ROIs gradually decreased, whereas long-range functional connections, especially anterior-posterior links, gradually increased until adulthood (Dosenbach et al., 2010; Fair et al., 2009; Kelly et al., 2009; Supekar et al., 2009).”
Background
Distinct neural signatures detected for ADHD subtypes after controlling for micro-movements in resting state functional connectivity MRI data
Fair, D. A., Nigg, J. T., Iyer, S., Bathula, D., Mills, K. L., Dosenbach, N. U. F., Schlaggar, B. L., Mennes, M., Gutman, D., Bangaru, S., et al. (2013) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2012.00080 · Cited by 463 · see citing works
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Development of human brain cortical network architecture during infancy
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Shared and distinct intrinsic functional network centrality in autism and attention-deficit/hyperactivity disorder
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Inter-individual differences in resting-state functional connectivity predict task-induced BOLD activity
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Atypical default network connectivity in youth with attention-deficit/hyperactivity disorder
Fair, D. A., Posner, J., Nagel, B. J., Bathula, D., Dias, T. G. C., Mills, K. L., Blythe, M. S., Giwa, A., Schmitt, C. F., & Nigg, J. T. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.07.003 · Cited by 354 · see citing works
Resting-state functional connectivity of subgenual anterior cingulate cortex in depressed adolescents
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Unraveling the Miswired Connectome: A Developmental Perspective
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The contribution of network organization and integration to the development of cognitive control
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Abnormal Medial Prefrontal Cortex Resting-State Connectivity in Bipolar Disorder and Schizophrenia
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Development of the Default Mode and Central Executive Networks across early adolescence: A longitudinal study
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Distortions and disconnections: Disrupted brain connectivity in autism
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Regional Variation in Interhemispheric Coordination of Intrinsic Hemodynamic Fluctuations
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The developmental foundations of human fairness
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Personality Is Reflected in the Brain's Intrinsic Functional Architecture
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Temporal and spatial evolution of brain network topology during the first two years of life
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The implications of brain connectivity in the neuropsychology of autism
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Studying Brain Organization via Spontaneous fMRI Signal
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Functional connectivity: A source of variance in the association between cardiorespiratory fitness and cognition?
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Resting-State Functional Connectivity Indexes Reading Competence in Children and Adults
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Neural correlates of personality: An integrative review
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Brain anatomical networks in early human brain development
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Cross-hemispheric functional connectivity in the human fetal brain
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Emotion-dependent functional connectivity of the default mode network in adolescent depression
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A preliminary study of functional connectivity in comorbid adolescent depression
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Relationship Between Cingulo-Insular Functional Connectivity and Autistic Traits in Neurotypical Adults
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Annual research review: growth connectomics--the organization and reorganization of brain networks during normal and abnormal development
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Assessing the psychedelic "after-glow" in ayahuasca users: Post-acute neurometabolic and functional connectivity changes are associated with enhanced mindfulness capacities
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Emerging Adulthood, a Pre-adult Life-History Stage
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Abnormal resting-state functional connectivity patterns of the putamen in medication-naïve children with attention deficit hyperactivity disorder
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Reduced Functional Integration and Segregation of Distributed Neural Systems Underlying Social and Emotional Information Processing in Autism Spectrum Disorders
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Meta-cognitive processes in executive control development: The case of reactive and proactive control
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Mind wandering perspective on attention-deficit/hyperactivity disorder
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Functional brain connectivity at rest changes after working memory training
Jolles, D. D., van Buchem, M. A., Crone, E. A., & Rombouts, S. A. R. B. (2013) · Human Brain Mapping · doi:10.1002/hbm.21444 · Cited by 183 · see citing works
Developmental changes in brain network hub connectivity in late adolescence
Baker, S. T. E., Lubman, D. I., Yucel, M., Allen, N. B., Whittle, S., Fulcher, B. D., Zalesky, A., & Fornito, A. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.5043-14.2015 · Cited by 168 · see citing works
Age-related increases in long-range connectivity in fetal functional neural connectivity networks in utero
Thomason, M. E., Grove, L. E., Lozon, T. A., Vila, A. M., Ye, Y., Nye, M. J., Manning, J. H., Pappas, A., Hernandez‐Andrade, E. A., Yeo, L., et al. (2014) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2014.09.001 · Cited by 188 · see citing works
A comprehensive study of whole-brain functional connectivity in children and young adults
Jolles, D. D., van Buchem, M. A., Crone, E. A., & Rombouts, S. A. R. B. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq104 · Cited by 181 · see citing works
Regionally specific alterations in functional connectivity of the anterior cingulate cortex in major depressive disorder
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Development of anterior cingulate functional connectivity from late childhood to early adulthood. Cereb Cortex
Kelly, A., Martino, A. D., Uddin, L. Q., Shehzad, Z. E., Gee, D. G., Reiss, P. T., Margulies, S., Castellanos, F. X., & Milham, M. P. (2009)
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Age-related differences in resting-state functional connectivity from childhood to adolescence
Sanders, A. F. P., Harms, M. P., Kandala, S., Marek, S. A., Somerville, L. H., Bookheimer, S. Y., Dapretto, M., Thomas, K. M., Essen, D. C. V., Yacoub, E. S., et al. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad011 · Cited by 67 · see citing works

Authors: Kelly, A. M. C., Di Martino, A., Uddin, L. Q., Shehzad, Z., Gee, D. G., Reiss, P. T., Margulies, D. S., Castellanos, F. X., & Milham, M. P.
Affiliations: NYU Langone Health (US)
New York University (US)
Humboldt-Universität zu Berlin (DE)
Nathan Kline Institute for Psychiatric Research (US)
ORCID: Uddin, L. Q.
Shehzad, Z.
Gee, D. G.
Reiss, P. T.
Margulies, D. S.
Castellanos, F. X.
Milham, M. P.
Venue: Cerebral Cortex
Publisher: Oxford University Press (OUP)
Published: 2008-07-24
Volume: 19
Issue: 3
Pages: 640-657
ISSN: 1047-3211 (ISSN-L)
1460-2199
DOI: 10.1093/cercor/bhn117
OpenAlex: W2113490642
Cited by: 572
References: 191
Citations by year: 2026: 10 · 2025: 16 · 2024: 17 · 2023: 22 · 2022: 20 · 2021: 34 · 2020: 25 · 2019: 33 · 2018: 37 · 2017: 37 · 2016: 36 · 2015: 37 · 2014: 63 · 2013: 51 · 2012: 43
FWCI: 15.68
Type: journal article
Language: en
Open access: closed
Locations: Cerebral Cortex (publishedVersion)
PubMed (publishedVersion)
Max Planck Digital Library (submittedVersion)
MPG.PuRe (Max Planck Society) (submittedVersion)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords: anterior cingulate cortex, resting-state functional connectivity, resting-state networks, brain maturation, developmental trajectories, children, adolescents, young adults, seed-based functional connectivity
MeSH terms: Adolescent, Age Factors, Child, Female, Gyrus Cinguli, Humans, Functional Laterality, Male, Nerve Net, Young Adult

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Development of Anterior Cingulate Functional Connectivity from Late Childhood to Early Adulthood

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