The DOI matches its Crossref record; 191 of the 191 references it cites were found in a registry or an index.
Development of Anterior Cingulate Functional Connectivity from Late Childhood to Early Adulthood
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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In the citing paper
“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
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“Since development is characterized by an overall increase in long-range functional connections (3-5;25), these studies suggest dysmaturation as a core feature of ASD pathophysiology.”
From Aberrant Striatal Functional Connectivity in Children with Autism (2011) · cites this paper as [5]
In the citing paper
“This resembles TDC functional architecture rather than that of TA (3;5;25), suggesting developmental immaturity in ASD.”
From Aberrant Striatal Functional Connectivity in Children with Autism (2011) · cites this paper as [5]
In the citing paper
“initial R-fMRI studies of adults with ASD demonstrated reduced long-range FC in large-scale networks (3;e.g., 5;50).”
From Aberrant Striatal Functional Connectivity in Children with Autism (2011) · cites this paper as [5]
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“This result, originally predicted by postmortem synaptic data (Huttenlocher 1975; Huttenlocher et al. 1982a), was independently replicated in a sample of 14 healthy children, 12 adolescents and 14 young adults (Kelly et al. 2009).”
BackgroundResultSelf-citationGuo, L., Zhou, F., Zhang, N., Kuang, H., & Feng, Z. L. (2019) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s221010 · Cited by 9
“The different selection of seeds may have a great effect on connectivity patterns.(49) In a word, those studies and our study indicated that the enhanced homotopic connectivity and FC in the MFG in AD subjects are compensatorymechanisms, possibly related to neuroplasticity, to meet the increased requirement of cogniti…”
BackgroundPeters, A. T., Jenkins, L. M., Stange, J. P., Bessette, K. L., Skerrett, K. A., Kling, L. R., Welsh, R. C., Milad, M. R., Phan, K. L., & Langenecker, S. A. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2019.03.007 · Cited by 9
“…seeds pairs were selected based on previous DMN and SN literature: anterior hippocampal formation (antHPF;(Schallmo et al., 2015)), PCC (Alexopoulos et al., 2012; Bluhm et al., 2011), amygdala (McCabe and Mishor, 2011; Pannekoek et al., 2013), and sgACC (Kelly et al., 2008; Margulies et al., 2007).”
MethodMa, Z., Tu, W., & Zhang, N. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.117463 · Cited by 9
“A similar relationship between FC strength and wiring distance was also reported during the development of DMN in human (Fair et al., 2008; Kelly et al., 2009) and animals (Choi et al.”
BackgroundInfluentialWei, X., Li, Q., Chen, J., Shen, B., Wang, W., & Li, W. (2021) · Quantitative Imaging in Medicine and Surgery · doi:10.21037/qims-20-1002 · Cited by 9
“Some studies have indicated that the ACC plays a significant role in behavioral regulation and emotional responses, including reward and punishment (27,28), and that emotional dysregulation is the initiating factor for relapse (29).”
BackgroundOfoghi, Z., Rohr, C. S., Dewey, D., Bray, S., Yeates, K. O., Noel, M. E., & Barlow, K. M. (2021) · Cephalalgia Reports · doi:10.1177/25158163211009477 · Cited by 8
“ACC Seeds 1 Caudal ACC Coordinate-based mask (X ¼ 5, Y ¼ 10, Z ¼ 47) From Kelly et al. (2009); 3.5 mm radius 2 Dorsal ACC Coordinate-based mask (X ¼ 5, Y ¼ 14, Z ¼ 42) 3 Rostral ACC Coordinate-based mask (X ¼ 5, Y ¼ 34, Z ¼ 28) 4 Perigenual ACC Coordinate-based mask (X ¼ 5, Y ¼ 47, Z ¼ 11) 5…”
InfluentialRong, B., Gao, G., Sun, L., Zhou, M., Zhao, H., Huang, J., Wang, H., Xiao, L., & Wang, G. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1159175 · Cited by 9
“In the present study, a total of 10 spherical regions of interest (ROIs) of 5 mm radius were identified for bilateral ACC, and bilateral caudal ACC (±5, −10, 37), dorsal ACC (±5, 10, 33), rostral ACC (±5, 27, 21), perigenual ACC (±5, 47, 11), and subgenual ACC (±5, 34, −4) were created to examine the seed-based, whole…”
MethodKeulers, E. H. H., Birkisdóttir, M. B., Falbo, L., de Bruin, A. B. H., & Stiers, P. L. J. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.12.014 · Cited by 9
“The wide distribution also agrees with reports that teen-age brain maturation takes place particularly in long-range connections, leading to improved whole-brain network integration (Dosenbach et al., 2007; Grayson and Fair, 2017; Kelly et al., 2009; Luna et al., 2015; Stevens, 2016; Vogel et al., 2010).”
BackgroundA Precision Functional Atlas of Network Probabilities and Individual-Specific Network TopographyPreprint
Hermosillo, R. J. M., Moore, L. A., Feczko, E., Dworetsky, A., Pines, A. R., Conan, G., Mooney, M. A., Randolph, A., Adeyemo, B., Earl, E., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.01.12.475422 · Cited by 9
“White circles indicate the location of the subgenual gyrus (subgenal MNI coordinates=±5, 25, -10 (Kelly et al., 2009; Zhou et al., 2016)).”
BackgroundGao, B., Yu, A., Qiao, C., Calhoun, V. D., Stephen, J. M., Wilson, T. W., & Wang, Y. (2024) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2024.3467384 · Cited by 8
“In contrast, young adults demonstrate more integrated FC patterns [48].”
Qiao, L., Luo, X., Zhang, L., Chen, A., Li, H., & Qiu, J. (2020) · Scientific Reports · doi:10.1038/s41598-020-76211-1 · Cited by 7
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“Previously, the pACC not only participated in self-referential and social processing (43) but also is involved in cognitive processing, the same as the dACC (45) and emotion regulation via the sACC (44– 47).”
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“…respectively in the amygdala (Alarcon et al. 2015; Gabard-Durnam et al. 2014), ventral striatum (Fareri et al. 2015), or medial prefrontal cortex (Kelly et al. 2009); or examined multiple networks together (Sole-Padulles et al. 2016; Supekar et al. 2010; Jolles et al. 2011); however, these…”
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“RSFC may be used to measure synchronization between different regional spontaneous neuronal signals and reflect the characteristics of the co-activated cortical networks (16, 17).”
MethodBrain-wide connectivity architecture
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Self-citationElectrophysiology and morphology of human cortical supragranular pyramidal cells in a wide age rangePreprint
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“…influences and experiences and lead to changes in metabolic activities ( Kuzawa et al., 2014 ), changes in functional connectivity patterns ( Kelly et al., 2009 ) and, with the maturation of white matter ( Beck et al., 2021 ; Yeatman et al., 2014 ) changes in the speed of long-distance…”
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“Adolescence is further marked by alterations in functional connectivity between ACC – a hub for emotion and cognitive control (Botvinick, 2007; Egner et al., 2008) – and brain regions involved in social processing and in emotion regulation (Kelly et al., 2009).”
Similarity in functional connectome architecture predicts teenage grit
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“In addition, as the functional architecture of the brain undergoes significant reorganizations during adolescence and early adulthood (Kelly et al., 2009; Power et al., 2010), a whole-brain network-level analysis of movie-watching fMRI data would be well suited for capturing the dynamic trajectory of brain development…”
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“…developing from childhood until adulthood, as indicated by the age-depended linear changes in functional connectivity from the anterior cingulate (Kelly et al., 2009) and differences in orbitofrontal activity between children and adults as well as adolescents and adults (Loh & Rosenkranz, 2022;…”
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“The ACC, whose functionality develops with age (Kelly et al. 2009), is thought to play a central role in conflict monitoring (Alexander and Brown 2019; Ebitz and Platt 2015; Metcalfe and Schwartz 2016).”
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“In this process leading to emotion regulation problems such as bipolar disorder; the interaction of the neuroimmune system with ACC is also remarkable (41).”
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Finding a home: Developmental and neurobiological perspectives on cultural models
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Brain Functional Networks in the Developing Brain Using Resting BOLD
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“An increase in long-distance connections has been reported when comparing school-aged children with adults (Fair et al., 2008; Fair et al., 2009; Kelly et al., 2009).”
BackgroundBrain Development and CNS Plasticity
Fair, D. A., & Schlaggar, B. L. (2009) · Springer eBooks · doi:10.1007/978-1-4419-0134-7_20 · Cited by 3
“Much less work has been done in regards to development, but there are suggestions that spontaneous activity is important for the establishment of early cortical patterns (e.g., ocular dominance columns or ODC) (Sur and Leamey 2001; Katz and Crowley 2002; Luo and O’Leary 2005; Price et al. 2006) and may represent (in a…”
BackgroundThe Default Mode Network and the Problem of Determining Intrinsic Mental Contents
Havlík, M., & Marvan, T. (2015) · Studies in Logic Grammar and Rhetoric · doi:10.1515/slgr-2015-0008 · Cited by 3
Hwang, S., Meffert, H., VanTieghem, M., White, S. F., Sinclair, S., Bookheimer, S. Y., & Blair, J. (2017) · Clinical Psychopharmacology and Neuroscience · doi:10.9758/cpn.2017.15.4.369 · Cited by 3
Special Issues in fMRI Involving Children
Hertz‐Pannier, L., & Noulhiane, M. (2013) · Springer eBooks · doi:10.1007/978-3-642-34342-1_16 · Cited by 3
Spencer, J. P., & Buss, A. T. (2013) · Wiley eBooks · doi:10.1002/9781118732373.ch4 · Cited by 3
The Inter-Subject Correlation of EEG in Response to Naturalistic Stimuli
Cohen, S. S. (2018) · CUNY Academic Works (City University of New York) · Cited by 3
Narrative Review: A Neurobiological Perspective on Resilience in Youth
Khalid, K., Baqir, H., & Stevens, H. E. (2024) · JAACAP Open · doi:10.1016/j.jaacop.2024.05.001 · Cited by 2
“26 There is asymmetric thinning of ACC (right > left) over time in adolescence.”
Neuroimaging Correlates of Functional Outcome Following Pediatric TBI
Dennis, E. L., Keleher, F., & Bartnik‐Olson, B. (2024) · Advances in neurobiology · doi:10.1007/978-3-031-69832-3_3 · Cited by 2
Millevert, C., Vidas-Guscic, N., Adhikari, M. H., Miranda, A., Vanherp, L., Jonckers, E., Joye, P., Audekerke, J. V., Spilbeeck, I. V., Verhoye, M., et al. (2025) · EBioMedicine · doi:10.1016/j.ebiom.2025.105720 · Cited by 3
“53 This suggests that while some maturation of functional networks occurs during this developmental period, major shifts may no longer be evident.”
Self-referential encoding in the developing brain
Sweatman, H., He, Y., Lawrence, R., & Chai, X. J. (2025) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2025.101581 · Cited by 3
“Previous research demonstrates global increases in mPFC function from childhood to early adulthood (Grossmann, 2013; Kelly et al., 2009), especially as children transition into adolescence and social communication and identity become increasingly salient (Blakemore, 2012; Konrad et al., 2013;…”
Syed, M. A., Yang, Z., Rangaprakash, D., Hu, X. P., Dretsch, M. N., Katz, J. S., Denney, T. S., & Deshpande, G. (2019) · Neuroinformatics · doi:10.1007/s12021-019-09422-1 · Cited by 2
The Balance Between n-6 and n-3 and its Relation to Executive Function
Sheppard, K. W., & Cheatham, C. L. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-815238-6.00004-3 · Cited by 2
Opportunities and challenges for current developmental neuroscience
Steinbeis, N., & Margulies, D. S. (2016) · Theory & Psychology · doi:10.1177/0959354316662158 · Cited by 2
“While not the first study to describe various linear and higher-order relationships between network organization and age (e.g., Kelly et al., 2009; Zuo et al., 2010), framing the metric as predictive transferred the status from experimental to clinically relevant.”
BackgroundSelf-citationCalleja, N. G., & Dadah, A. M. (2018) · The Family Journal · doi:10.1177/1066480717752899 · Cited by 2
“…the last decade, we have gained new knowledge of health problems resulting from psychotropic medication use among children and adolescents, ranging from weight gain (Kelly et al., 2009) and fatigue (Cheng-Shannon, McGough, Pataki, & McCracken 2004) to diabetes and seizures (Correll et al., 2006).”
BackgroundGalván, A. (2018) · Cambridge University Press eBooks · doi:10.1017/9781316106143.008 · Cited by 2
Neural correlates of the sound facilitation effect in the modified Simon task in older adults
Manelis, A., Hu, H., Miceli, R., Satz, S., & Schwalbe, M. (2023) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2023.1207707 · Cited by 3
“The anterior cingulate cortex plays a role in conflict monitoring and response selection (Milham and Banich, 2005; Kelly et al., 2009), while the prefrontal cortex plays a role in cognitive control and decision-making (Wong et al.”
BackgroundSimmonds, D. J. (2015) · D-Scholarship@Pitt (University of Pittsburgh) · Cited by 2
The interplay of age and pedagogy in maturation of error-monitoringPreprint
Denervaud, S., Tovar, D. A., Knebel, J., Mullier, E., Alemán‐Gómez, Y., Hagmann, P., & Murray, M. M. (2019) · doi:10.31219/osf.io/7nbqz · Cited by 2
Chavez‐Valdez, R., Northington, F. J., Sharp, A., Burton, V. J., Lammert, D. B., Jantzie, L. L., Robinson, S., Stafstrom, C. E., Ferriero, D. M., Gano, D. L., et al. (2024) · Journal of Child Neurology · doi:10.1177/08830738241259054 · Cited by 2
“25 In summary, the structural and biochemical substrates are likely not suf fi ciently developed during infancy to make a diagnosis of delirium in neonates, even less in preterm infants.”
Gui, S., Liu, Y., Pu, J., Wang, D., Zhong, X., Chen, W., Chen, X., Chen, Y., Chen, X., Wei, T., et al. (2025) · Molecular Neurobiology · doi:10.1007/s12035-025-04766-z · Cited by 1
“The anterior cingulate cortex (ACC), specifically brod-mann area 25 (BA25), plays a crucial role in the limbic system by regulating emotional responses and monitoring outcomes associated with reward or punishment [21].”
Exploring dynamic hubs for face perception in the brain: A graph theoretical measure approach
Gupta, S., & Gandhi, T. K. (2025) · Biomedical Signal Processing and Control · doi:10.1016/j.bspc.2025.107863 · Cited by 1
Karslı, B., Meisinger, V., Hasanaj, G., Kallweit, M. S., Dengl, F., Vural, G., Melcher, J., Korman, M., Klimas, N., Schmölz, S., et al. (2026) · Schizophrenia · doi:10.1038/s41537-026-00730-5 · Cited by 2
Qi, W., Ruan, Y., Tang, Y., Zheng, D., Yuan, Q., Xue, C., & Xiao, C. (2026) · Frontiers in Neuroscience · doi:10.3389/fnins.2026.1748031 · Cited by 1
Introduction: Connecting Brain Development, Disruptive Behavior, and Children
Tolan, P. H., & LEVENTHAL, B. L. (2013) · Springer eBooks · doi:10.1007/978-1-4614-7557-6_1 · Cited by 2
Salavert, J. (2015) · TDX (Tesis Doctorals en Xarxa) · Cited by 1
Functional Connectivity in Autism Spectrum Disorders: Challenges and Perspectives
Müller, R., & Linke, A. C. (2021) · Springer eBooks · doi:10.1007/978-3-030-59797-9_12 · Cited by 1
Linking Mild Childhood Adversity with Conflict and False Feedback Monitoring
Liu, Y., Peng, H., Wu, J., Wang, N., & Duan, H. (2022) · Developmental Neuropsychology · doi:10.1080/87565641.2022.2155163 · Cited by 1
“…systems involved in performance monitoring and cognitive control undergo substantial development from childhood through early adulthood (Gogtay et al., 2004; Kelly et al., 2008), and this maturity process is accompanied by improved cognitive control ability (Griffin, 2017; Luna & Sweeney, 2004).”
Developmental differences in functional organization of multispectral networks
Petro, N. M., Picci, G., Embury, C. M., Ott, L. R., Penhale, S. H., Rempe, M. P., Johnson, H. J., Willett, M. P., Wang, Y., Stephen, J. M., et al. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad193 · Cited by 1
Galván, A. (2018) · Cambridge University Press eBooks · doi:10.1017/9781316106143.006 · Cited by 1
Functional and Structural Longitudinal Change Patterns in Adolescent Brain
Saha, R., Saha, D. K., Fu, Z., Silva, R. F., & Calhoun, V. D. (2023) · Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC) · doi:10.1109/embc40787.2023.10340079 · Cited by 1
Pagliaccio, D. (2015) · Open Scholarship Institutional Repository (Washington University in St. Louis) · doi:10.7936/k7t151t3 · Cited by 1
“have been suggested to represent the accumulated history of co-activation of brain areas (e.g. Dosenbach et al., 2007; Fair et al., 2007; Kelly et al., 2009).”
BackgroundThe Connectivity of Orofacial Systems
Estep, M. E., & Barlow, S. M. (2009) · Perspectives on Speech Science and Orofacial Disorders · doi:10.1044/ssod19.1.28 · Cited by 1
Galván, A. (2018) · Cambridge University Press eBooks · doi:10.1017/9781316106143.002 · Cited by 1
„Default-mode“-Netzwerk des Gehirns. Neurobiologie und klinische Bedeutung
Otti, A., Gündel, H., Wohlschläger, A., Zimmer, C., Sorg, C., & Noll‐Hussong, M. (2012) · Der Nervenarzt · Cited by 1
Advancing Addiction Research through the Integration of Genetics and Neuroimaging
Karoly, H. C., Hagerty, S. L., Weiland, B. J., & Hutchison, K. E. (2015) · Wiley eBooks · doi:10.1002/9781118472415.ch18 · Cited by 1
Age-related changes in spatial and temporal features of resting state fMRIPreprint
Vij, S. G., Nomi, J. S., Dajani, D. R., & Uddin, L. Q. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/109181 · Cited by 1
Self-citation
Metadata
- 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)
- 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
- 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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