The DOI matches its Crossref record; 71 of the 71 references it cites were found in a registry or an index.
Rich-club organization of the newborn human brain
Open accessAbstract
Significance: To investigate the organizational principles of human brain development, we analyzed cerebral structural connectivity in the period leading up to the time of normal birth. We found that a “rich club” of interconnected cortical hubs previously reported in adults is present by 30 wk gestation. From mid to late gestation, connections between core hubs and the rest of the brain increased significantly. To determine the influence of environmental factors on network development, we also compared term-born infants to those born prematurely. Alterations in cortical–subcortical connectivity and short-distance connections outside the core network were associated with prematurity. Rich-club organization in the human brain precedes the emergence of complex neurological function, and alterations during this time may impact negatively on subsequent neurodevelopment.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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
“Rich clubs are also evident in both structural and functional networks in neonates along with both high functional modularity and integration capacity between modules (Ball et al., 2014; Scheinost et al., 2016a; van den Heuvel et al., 2015b).”
From Development of large-scale functional networks from birth to adulthood: A guide to the neuroimaging literature (2017) · cites this paper as Ball et al., 2014
In the citing paper
“These findings suggest that the development of a small-world architecture, as well as the capacity for globally efficient communication and integration, largely occurs during the first year of life and prenatally, a finding that is supported by multimodal structural and functional network analysis in preterm infants (Ball et al., 2014; van den Heuvel et al., 2015b).”
From Development of large-scale functional networks from birth to adulthood: A guide to the neuroimaging literature (2017) · cites this paper as Ball et al., 2014
In the citing paper
“White-matter networks at birth, and even in premature infants at 30 weeks gestational age50, have a rich club property similar to that in adults.”
From Imaging structural and functional brain development in early childhood (2018) · cites this paper as [50]
In the citing paper
“Structural connectivity analyses have demonstrated that well-connected cortical hubs are already evident at 30 weeks' gestation.62”
From Neuroimaging, cardiovascular physiology, and functional outcomes in infants with congenital heart disease (2017) · cites this paper as [62]
In the citing paper
“This is consistent with previous rs-fcMRI studies in adults that used a similar spatial scale of 90 nodes2435 and a diffusion temporal imaging or DTI study in neonates using ~500 nodes36.”
From Functional properties of resting state networks in healthy full-term newborns (2015) · cites this paper as [36]
In the citing paper
“A recent structural study in neonates also identified the hippocampus and insula, as well as association areas such as the paracentral lobules, as hubs, which is consistent with our findings in functional networks36.”
From Functional properties of resting state networks in healthy full-term newborns (2015) · cites this paper as [36]
In the citing paper
“A recent structural study in neonates also identified the hippocampus and insula, as well as association areas such as the paracentral lobules, as hubs, which is consistent with our findings in functional networks36.”
From Functional properties of resting state networks in healthy full-term newborns (2015) · cites this paper as [36]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Complex network measures of brain connectivity: Uses and interpretations
Rubinov, M., & Sporns, O. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2009.10.003 · Cited by 11,522
Distributed hierarchical processing in the primate cerebral cortex
Felleman, D. J., & Van Essen, D. C. (1991) · Cerebral Cortex · doi:10.1093/cercor/1.1.1 · Cited by 7,783
Nonrigid registration using free-form deformations: application to breast mr images
Rueckert, D., Sonoda, L. I., Hayes, C., Hill, D. L. G., Leach, M. O., & Hawkes, D. J. (1999) · IEEE Transactions on Medical Imaging · doi:10.1109/42.796284 · Cited by 5,265
Self-citationSMITH, S., & NICHOLS, T. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2008.03.061 · Cited by 5,250
Preface: Cerebral Cortex Has Come of Age
Goldman, P. S., & RAKIC, P. T. (1991) · Cerebral Cortex · doi:10.1093/cercor/1.1.1-a · Cited by 3,537
Probabilistic diffusion tractography with multiple fibre orientations: What can we gain?
Behrens, T. E. J., Berg, H. J., Jbabdi, S., Rushworth, M. F. S., & Woolrich, M. W. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2006.09.018 · Cited by 3,471
Predicting human resting-state functional connectivity from structural connectivity
Honey, C. J., Sporns, O., Cammoun, L., Gigandet, X., Thiran, J. P., Meuli, R., & Hagmann, P. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811168106 · Cited by 3,307
The economy of brain network organization
Bullmore, E., & Sporns, O. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3214 · Cited by 3,284
Classes of small-world networks
Amaral, L. A. N., Scala, A., Barthélémy, M., & Stanley, H. E. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.200327197 · Cited by 3,051
Specificity and Stability in Topology of Protein Networks
Maslov, S., & Sneppen, K. (2002) · Science · doi:10.1126/science.1065103 · Cited by 3,051
Cited by
Sorted by citations
Items 301–358 of 358
Fields, C. (2017) · Springer eBooks · doi:10.1007/978-3-319-16999-6_2373-1 · Cited by 1
Jang, Y. H., Ham, J., Kasani, P. H., Kim, H., Lee, J. Y., Lee, G. Y., Kim, B.-N., & Lee, H. J. (2024) · Research Square · doi:10.21203/rs.3.rs-3874124/v1 · Cited by 1
Brain age prediction and deviations from normative trajectories in the neonatal connectomePreprint
Sun, H., Mehta, S., Khaitova, M., Cheng, B., Hao, X., Spann, M. N., & Scheinost, D. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.04.23.590811 · Cited by 1
Epihova, G., Epihov, D. Z., Akarca, D., & Astle, D. E. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.05.15.594422 · Cited by 1
How neural network structure alters the brain’s self-organized criticalityPreprint
Sugimoto, Y. A., Yadohisa, H., & Abe, M. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.09.24.614702 · Cited by 1
He, Y. L., & Wang, J. (2014) · International Conference on Natural Computation (ICNC) · doi:10.1109/icnc.2014.6975804
Yates, D. M. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3774
Salvan, P., Arichi, T., Vidaurre, D., Tournier, J., Falconer, S., Chew, A. T. M., Counsell, S. J., & Edwards, A. D. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/282673
Self-citationLangenbach, R. (2017) · Performance Research · doi:10.1080/13528165.2017.1414431
Il caos tra psiche e materia: l'archetipo come attrattore strano
Floro, R. (2018) · STUDI JUNGHIANI · doi:10.3280/jun2017-046002
Early Childhood Brain Development and Schizophrenia: An Imaging Perspective
Gilmore, J. H. (2020) · Springer eBooks · doi:10.1007/978-3-030-35206-6_15
He, Z., Zhang, S., Zhang, S., Zhang⋆, Y., Hu, X., Jiang, X., Guo, L., Liu, T., Du, L., & Zhang, T. (2020) · Lecture notes in computer science · doi:10.1007/978-3-030-59861-7_47
Lifespan changes in brain rhythms and networks
Eggermont, J. J. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-819818-6.00013-3
Algorithmic Problems in Bioinformatics
Szalkai, B. (2018) · Eötvös Loránd Tudományegyetem · doi:10.15476/elte.2018.077
Religionspedagogiska och religionsdidaktiska teorier : En jämförande studie
Sundmark, K. (2012) · KTH Publication Database DiVA (KTH Royal Institute of Technology)
Complexity, Criticality and Computation (C³)
Prokopenko, M. (2017) · MDPI eBooks · doi:10.3390/books978-3-03842-515-1
Network Topology and Psychopathology Following Very Preterm Birth
Vanes, L. D., & Nosarti, C. (2022) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2021.12.011
Fields, C. (2021) · Springer eBooks · doi:10.1007/978-3-319-19650-3_2373
Kirwan, C. B., & Bodily, T. A. (2018) · Springer eBooks · doi:10.1007/978-3-319-57111-9_9074
Bathelt, J., Downes, M., & de Haan, M. D. H. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.22830-7
Kirwan, C. B., & Bodily, T. A. (2017) · Springer eBooks · doi:10.1007/978-3-319-56782-2_9074-1
Kaur, K. K. (2022) · Pharmaceutics and Pharmacology Research · doi:10.31579/2693-7247/084
Quinones, J. F., Hildebrandt, A., Pavan, T., Thiel, C. M., & Heep, A. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4202046
A blueprint of the developing mind
Turk, E. (2022) · Utrecht University Repository (Utrecht University) · doi:10.33540/627
Does there exist rich-club phenomenon within two steps in complex networks?
Dong, Y. P., & Qi, X. (2022) · International Journal of Modern Physics B · doi:10.1142/s0217979223501254
Zhang, W., Yin, M., Jiang, M., & Dai, Q. (2023) · Computers in Biology and Medicine · doi:10.1016/j.compbiomed.2023.106552
Baldi, S. (2023) · Research Publications (Maastricht University) · doi:10.26481/dis.20230526sb
Resting State Functional Magnetic Resonance Imaging
Ryan, D., Gujar, S. K., & Sair, H. I. (2023) · Springer eBooks · doi:10.1007/978-3-031-10909-6_28
de Haan, M. D. H., Johnson, M. H., & Dumontheil, I. (2023) · Developmental Cognitive Neuroscience · doi:10.1002/9781394260676.refs
(2015) · Developmental Cognitive Neuroscience · doi:10.1002/9781394259083.refs
Development of the Fetal Brain Structural Connectivity Based on In-Utero Diffusion MRI
Chen, R., Xu, X., Zhao, R., Li, M., Sun, C., Wang, G., & Wu, D. (2024) · World Congress on Medical Physics and Biomedical Engineering, September 7 - 12, 2009, Munich, Germany · doi:10.1007/978-3-031-51455-5_25
Role of Structural and Functional Whole-Brain Imaging in the Assessment of Preterm Infants
Rege, O. (2023) · Journal of Student Research · doi:10.47611/jsrhs.v12i4.5789
The Impact of Covid-19 Pandemic on Infants' Functional Brain Network DevelopmentPreprint
van der Velde, B., & Kemner, C. (2024) · SSRN Electronic Journal · doi:10.2139/ssrn.4852836
Perinatal Risk and Later Intellectual and Developmental Disabilities
Manessis, A. G., Rutter, T. M., Cook, K. M., Merrill, L. C., Korom, M., Selvanathan, T., Camacho, M. C., Fetal, I., & Bick, J. (2024) · Contemporary clinical neuroscience · doi:10.1007/978-3-031-66932-3_9
Haemodynamic Responses to Spontaneous Neural Activity on the Electroencephalogram in Preterm Infants
Shiraki, A., Kidokoro, H., Watanabe, H., Taga, G., Yamada, M., Yoshimura, T., Narita, H., Mitsumatsu, T., Kumai, S., Suzui, R., et al. (2024) · Advances in experimental medicine and biology · doi:10.1007/978-3-031-67458-7_16
Wasserman, T. H., & Wasserman, L. D. (2024) · Springer eBooks · doi:10.1007/978-3-031-78732-4_5
Wasserman, T. H., & Wasserman, L. D. (2024) · Springer eBooks · doi:10.1007/978-3-031-78732-4_10
Sun, H., Vernetti, A., Spann, M. N., Chawarska, K., Ment, L. R., & Scheinost, D. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.02.19.638284
Zhang, X., Song, M., Jiang, W., Lu, Y., Chu, C., Li, W., Wang, H., Shi, W., Lan, Y., & Jiang, T. (2025) · Neuroscience Bulletin · doi:10.1007/s12264-025-01393-5
Charting the Normal Development of Structural Brain Connectivity in Utero Using Diffusion MRI
Karimi, D., Li, B., Taymourtash, A., Jaimes, C. E., Grant, P. E., & Warfield, S. K. (2026) · Human Brain Mapping · doi:10.1002/hbm.70609
Quinones, J. F., Gießing, C., Heep, A., & Hildebrandt, A. (2025) · Imaging Neuroscience · doi:10.1162/imag.a.928
Transcriptomic divergence of network hubs in the prenatal human brain
Oldham, S., & Ball, G. (2025) · Communications Biology · doi:10.1038/s42003-025-08962-4 · Cited by 6
Self-citationOrganization of a neuron-resolution central brain network: topology, geometry, and anatomy
Zhang, X.-Y., Yan, G., & Moore, J. M. (2025) · Journal of Complex Networks · doi:10.1093/comnet/cnaf023
The evolution of extended neurodevelopment and increased neuroplasticity in human brains
Drennan, A., Sherwood, C. C., & Gómez‐Robles, A. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-27380-3.00045-2 · Cited by 1
Structural and Functional Coupling in Neonates and its Prediction for Neurocognitive Outcomes
Xu, Y., Zhao, T., Jeon, T., Ouyang, M., Zhu, T., Chalak, L. D., Rollins, N. K., & Huang, H. (2026) · Journal of Pacific Rim Psychology · doi:10.1177/18344909251414889
Intrathalamic morphometry in infants with congenital heart disease and infants born pretermPreprint
Clayden, B., Gal-Er, B., van der Meijden, M. E. M., Cromb, D., Wilson, S., Pushparajah, K., Simpson, J. M., Kelly, C. J., Chew, A. T. M., Hajnal, J. V., et al. (2026) · medRxiv · doi:10.64898/2026.03.16.26348485
Self-citationResting-state EEG functional connectivity analysis in benign childhood epilepsy and neonate
Adebimpe, A. (2016) · theses.fr (ABES) · doi:10.70675/24b394a3zd618z4e1ezbf52z364f1629a084
Leprince, E. (2021) · theses.fr (ABES) · doi:10.70675/ea9385dbz28a4z4b9ez8a79zabae124a5f5b
Ma, J. X., Chen, T. X., Wang, H., Luo, C., Yin, Y.-H., Xie, L., Hui, R., Liu, Y., He, R., Yu, X., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.05.11.723545
Neonatal Brain Network Integration Trajectories Predict Neurodevelopment in Congenital Heart DiseasePreprint
Harasymiw, L., Kuang, A. W., Xu, D., Scheffler, A., George, E., Peyvandi, S., & McQuillen, P. S. (2026) · medRxiv · doi:10.64898/2026.06.06.26355074
Brain structural and functional connectivity converge prenatally but diverge after birth
Zhao, R., Li, M., ZHANG, Y., Chen, R., Ning, C., Zhao, Z., Yan, Z., Wang, M., & Wu, D. W. (2026) · PLoS Biology · doi:10.1371/journal.pbio.3003927
An Approximation Algorithm for the Rich-Club Coefficient via Sample Complexity
Fukuyama, E. Y., Zatesko, L. M., & da Silva, M. V. G. (2026) · doi:10.5753/etc.2026.22277
A systematic review of structural brain differences in school-aged children born preterm
Coward, E., Mckinnon, K., Richardson, H., & Fletcher-Watson, S. (2026) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2026.101818
Attenni, M., Vinci, G. V., & Scattoni, M. L. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.09.24.754103
Yi, T., Wei, W., Cai, Q., & Jin, K. (2026) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2026.112340
Neonatal brain network integration trajectories predict neurodevelopment in congenital heart disease
Harasymiw, L. A., Kuang, A. W., Xu, D., Scheffler, A., George, E., Peyvandi, S., & McQuillen, P. S. (2026) · Pediatric Research · doi:10.1038/s41390-026-05546-8
Metadata
- Authors
- Ball, G., Aljabar, P., Zebari, S., Tusor, N., Arichi, T., Merchant, N., Robinson, E. C., Ogundipe, E., Rueckert, D., Edwards, A. D., & Counsell, S. J.
- Affiliations
- St Thomas' Hospital (GB)
- University of Oxford (GB)
- Chelsea and Westminster Hospital (GB)
- Imperial College London (GB)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2014-05-05
- Volume
- 111
- Issue
- 20
- Pages
- 7456-7461
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC4034228
- OpenAlex
- W1989523430
- Cited by
- 360
- References
- 71
- Citations by year
- 2026: 16 · 2025: 17 · 2024: 34 · 2023: 28 · 2022: 29 · 2021: 33 · 2020: 27 · 2019: 29 · 2018: 43 · 2017: 37 · 2016: 30 · 2015: 27 · 2014: 9
- FWCI
- 18.99
- 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)
- Research Portal (King's College London) (submittedVersion, other-oa)
- Funders
- Action Medical Research
- National Institute for Health and Care Research (RP-PG-0707-10154, CL-2012-17-006, ACF-2006-21-028)
- Medical Research Council (MR/K006355/1, MR/J014311/1)
- Engineering and Physical Sciences Research Council (EP/I000445/1)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Physical Sciences › Physics and Astronomy › Statistical and Nonlinear Physics › Complex Network Analysis Techniques
- Keywords
- rich club, brain development, cortical hubs, gestational age, preterm infants, cortical-subcortical connectivity, corticocortical connections, brain network architecture, preterm birth
- MeSH terms
- Brain, Brain Mapping, Cognition, Female, Humans, Infant, Newborn, Infant, Premature, Male, Nerve Net, Neural Pathways, Time Factors, Diffusion Magnetic Resonance Imaging, Premature Birth, Term Birth, Connectome
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