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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.
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“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]
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Citations
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Imaging structural and functional brain development in early childhood
Gilmore, J. H., Knickmeyer, R. C., & Gao, W. (2018) · Nature Reviews Neuroscience · doi:10.1038/nrn.2018.1 · Cited by 1,013
An Integrative Model of the Maturation of Cognitive Control
Luna, B., Marek, S., Larsen, B., Tervo-Clemmens, B., & Chahal, R. (2015) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071714-034054 · Cited by 550
Grayson, D. S., & Fair, D. A. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.01.079 · Cited by 411
“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 (…”
BackgroundResultUnraveling the Miswired Connectome: A Developmental Perspective
Martino, A. D., Fair, D. A., Kelly, C. A. M., Satterthwaite, T. D., Castellanos, F. X., Thomason, M. E., Craddock, R. C., Luna, B., LEVENTHAL, B. L., Zuo, X., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.08.050 · Cited by 357
Developmental connectomics from infancy through early childhood
Cao, M., Huang, H., & He, Y. (2017) · Trends in Neurosciences · doi:10.1016/j.tins.2017.06.003 · Cited by 284
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
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