White matter maturation reshapes structural connectivity in the late developing human brain
Open accessAbstract
From toddler to late teenager, the macroscopic pattern of axonal projections in the human brain remains largely unchanged while undergoing dramatic functional modifications that lead to network refinement. These functional modifications are mediated by increasing myelination and changes in axonal diameter and synaptic density, as well as changes in neurochemical mediators. Here we explore the contribution of white matter maturation to the development of connectivity between ages 2 and 18 y using high b-value diffusion MRI tractography and connectivity analysis. We measured changes in connection efficacy as the inverse of the average diffusivity along a fiber tract. We observed significant refinement in specific metrics of network topology, including a significant increase in node strength and efficiency along with a decrease in clustering. Major structural modules and hubs were in place by 2 y of age, and they continued to strengthen their profile during subsequent development. Recording resting-state functional MRI from a subset of subjects, we confirmed a positive correlation between structural and functional connectivity, and in addition observed that this relationship strengthened with age. Continuously increasing integration and decreasing segregation of structural connectivity with age suggests that network refinement mediated by white matter maturation promotes increased global efficiency. In addition, the strengthening of the correlation between structural and functional connectivity with age suggests that white matter connectivity in combination with other factors, such as differential modulation of axonal diameter and myelin thickness, that are partially captured by inverse average diffusivity, play an increasingly important role in creating brain-wide coherence and synchrony.
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After birth until adulthood, the brain network reshapes to improve integration capacity, with decreased modularity and decreased small-worldness.
“After birth until adulthood, the brain network reshapes to improve integration capacity with the reconfigurations of decreased modularity and decreased small-worldness”
From Quantitative mapping of the brain’s structural connectivity using diffusion MRI tractography: A review (2022) · cites this paper as Hagmann et al., 2010
The Results report increasing network efficiency and a generally decreasing small-world index with age. But the Modularity and Module Composition results say modularity showed no consistent significant age trend, rather than a decrease. The study examined ages 2–18, not the full period from birth to adulthood. (LLM, conf=0.91)
Experimental — accuracy not yet measuredThere is an abundance of research demonstrating a correlation between DWI-tractography connection weights and FC in adults.
“There is an abundance of research demonstrating a correlation between DWI-tractography connection weights and FC in adults (Hagmann et al., 2008; Hagmann et al., 2010; Honey 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 Hagmann et al., 2010
SC-FC correspondence is higher in older adolescents than in young children.
“Hagmann et al. (Hagmann et al., 2010) reported that SC-FC correspondence was higher in older teens versus in young children.”
From Development of large-scale functional networks from birth to adulthood: A guide to the neuroimaging literature (2017) · cites this paper as Hagmann et al., 2010
Network maturation in the first two years after birth generally consists of increased network efficiency and integration, decreased segregation, and some changes in modularity, with most major hubs and modules in place by age two.
“Network maturation in the first 2 years after birth generally consists of increased network efficiency and network integration [G], decreased network segregation [G], and some changes in the modularity48, 51, with most major hubs and modules in place by age 2 years52.”
From Imaging structural and functional brain development in early childhood (2018) · cites this paper as [52]
Graph-theoretic studies using gray matter volume and diffusion MRI tractography have shown age-dependent changes in global topological properties.
“graph-theoretic studies using gray matter volume (Fan et al. 2011) and diffusion MRI tractography (Hagmann et al. 2010) have shown age-dependent changes in the global topological properties”
From Developmental Changes in Organization of Structural Brain Networks (2013) · cites this paper as Hagmann et al. 2010
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- Authors
- Hagmann, P., Sporns, O., Madan, N., Cammoun, L., Pienaar, R., Wedeen, V. J., Meuli, R., Thiran, J.-P., & Grant, P. E.
- Affiliations
- Centre Hospitalier Universitaire Vaudois (CH)
- Indiana University Bloomington (US)
- Tufts Medical Center (US)
- École Polytechnique Fédérale de Lausanne (CH)
- Boston Children's Hospital (US)
- Harvard University (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2010-10-18
- Volume
- 107
- Issue
- 44
- Pages
- 19067-19072
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2973853
- OpenAlex
- W2101328227
- Cited by
- 700
- References
- 61
- Citations by year
- 2026: 27 · 2025: 43 · 2024: 42 · 2023: 30 · 2022: 40 · 2021: 46 · 2020: 42 · 2019: 45 · 2018: 55 · 2017: 65 · 2016: 41 · 2015: 39 · 2014: 57 · 2013: 54 · 2012: 42
- FWCI
- 32.74
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
- IRIS (submittedVersion)
- SERVAL (Université de Lausanne) (submittedVersion)
- Funders
- National Science Foundation
- James S. McDonnell Foundation
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- Université de Lausanne
- National Institutes of Health
- Topics
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Physical Sciences › Physics and Astronomy › Statistical and Nonlinear Physics › Complex Network Analysis Techniques
- Keywords
- white matter maturation, structural connectivity, brain development, myelination, axon diameter, network topology, network hubs, global efficiency, diffusion MRI tractography, resting-state fMRI, human brain
- MeSH terms
- Adolescent, Axons, Cerebral Cortex, Child, Child Development, Child, Preschool, Female, Follow-Up Studies, Humans, Infant, Magnetic Resonance Imaging, Male, Myelin Sheath, Synapses, Adolescent Development
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