Cited by 360Functional Brain Connectivity StudiesAdvanced Neuroimaging Techniques and ApplicationsComplex Network Analysis Techniques

Rich-club organization of the newborn human brain

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Ball, Gareth, Aljabar, Paul, Zebari, Sally, Tusor, Nora, Arichi, Tomoki, Merchant, Nazakat, Robinson, Emma C., Ogundipe, Enitan +3 more·2014·Proceedings of the National Academy of Sciences

Abstract

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 evident in both structural and functional networks in neonates, along with high functional modularity and integration capacity between modules.

    “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).”
  • Development of small-world architecture and capacity for globally efficient communication and integration largely occurs during the first year of life and prenatally.

    “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).”
  • White-matter networks at birth, and even in premature infants at 30 weeks gestational age, have a rich club property similar to that in adults.

    “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.”
  • Structural connectivity analyses have shown that well-connected cortical hubs are already present at 30 weeks' gestation.

    “Structural connectivity analyses have demonstrated that well-connected cortical hubs are already evident at 30 weeks' gestation.62”
  • The right-tailed degree distribution is consistent with previous rs-fcMRI studies in adults using a similar spatial scale of 90 nodes and a DTI study in neonates using ~500 nodes.

    “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.”

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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)
Venue
Proceedings of the National Academy of Sciences
Published
2014-05-05
Volume
111
Issue
20
Pages
7456-7461
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
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 · 2012: 1
FWCI
18.99
Type
journal article
Language
en
Open access
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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