Temporal and spatial evolution of brain network topology during the first two years of life
Open accessAbstract
The mature brain features high wiring efficiency for information transfer. However, the emerging process of such an efficient topology remains elusive. With resting state functional MRI and a large cohort of normal pediatric subjects (n = 147) imaged during a critical time period of brain development, 3 wk- to 2 yr-old, the temporal and spatial evolution of brain network topology is revealed. The brain possesses the small world topology immediately after birth, followed by a remarkable improvement in whole brain wiring efficiency in 1 yr olds and becomes more stable in 2 yr olds. Regional developments of brain wiring efficiency and the evolution of functional hubs suggest differential development trend for primary and higher order cognitive functions during the first two years of life. Simulations of random errors and targeted attacks reveal an age-dependent improvement of resilience. The lower resilience to targeted attack observed in 3 wk old group is likely due to the fact that there are fewer well-established long-distance functional connections at this age whose elimination might have more profound implications in the overall efficiency of information transfer. Overall, our results offer new insights into the temporal and spatial evolution of brain topology during early brain development.
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Neonatal hubs primarily involve early sensorimotor, visual, and limbic regions.
“whereas neonatal hubs primarily involve early sensorimotor, visual, and limbic regions (De Asis-Cruz et al., 2015; Fransson et al., 2011; Gao et al., 2011).”
From Development of large-scale functional networks from birth to adulthood: A guide to the neuroimaging literature (2017) · cites this paper as Gao et al., 2011
These properties marginally increase during the first year and plateau until at least the end of the second year.
“These properties only appear to marginally increase during the first year of life, plateauing thereafter until at least the end of the second year (Gao et al., 2011).”
From Development of large-scale functional networks from birth to adulthood: A guide to the neuroimaging literature (2017) · cites this paper as Gao et al., 2011
During the first two years, hubness of sensorimotor areas gradually decreases and involvement of association cortical areas increases, especially medial frontal and parietal default mode portions.
“The first two years of life reflect a gradual decrease in the hubness of sensorimotor areas and increased involvement of various association cortical areas, especially the medial frontal and parietal portions of the default mode (Gao et al., 2011).”
From Development of large-scale functional networks from birth to adulthood: A guide to the neuroimaging literature (2017) · cites this paper as Gao et al., 2011
Hub configurations are robustly evident after birth.
“Hub configurations are robustly evident after birth (De Asis-Cruz et al., 2015; Fransson et al., 2011; Gao et al., 2011)”
From Development of large-scale functional networks from birth to adulthood: A guide to the neuroimaging literature (2017) · cites this paper as Gao et al., 2011
Long-distance links are preferentially strengthened during the first year and level off thereafter.
“Concomitantly, long-distance links are preferentially strengthened during the first year of life, leveling off thereafter (Gao et al., 2011).”
From Development of large-scale functional networks from birth to adulthood: A guide to the neuroimaging literature (2017) · cites this paper as Gao et al., 2011
Sensory networks exchange information through two-step inter-regional functional connectivity to the default-mode network and lateral frontoparietal, limbic and basal ganglia regions in subsequent steps, mimicking the hierarchy proposed by predictive encoding.
“sensory networks have been demonstrated to exchange information through two-step inter-regional functional connectivity to the default-mode network and lateral frontoparietal, limbic and basal ganglia regions in subsequent steps111, 115, mimicking the hierarchy proposed by the theory of predictive encoding [G]116, 117.”
From Imaging structural and functional brain development in early childhood (2018) · cites this paper as [115]
Step-wise analysis of functional connectivity is a novel technique that could probe the brain's functional hierarchy.
“step-wise analysis [G] of functional connectivity emerges as a novel technique that could probe this hierarchy115.”
From Imaging structural and functional brain development in early childhood (2018) · cites this paper as [115]
The findings are consistent with SWI measured in younger preterm and full-term infants (35-42 weeks gestational age).
“These findings are also consistent with SWI measured in younger preterm and full-term infants (35–42 weeks gestational age)16.”
From Functional properties of resting state networks in healthy full-term newborns (2015) · cites this paper as [16]
Similarities included bilateral insula, right SMA, bilateral rolandic operculum, left fusiform, bilateral olfactory and bilateral inferior frontal orbital cortices.
“Similarities included bilateral insula, right SMA, bilateral rolandic operculum, left fusiform, bilateral olfactory and bilateral inferior frontal orbital cortices.”
From Functional properties of resting state networks in healthy full-term newborns (2015) · cites this paper as [16]
Gao et al. also reported the left insula, right inferior frontal (orbital), and left fusiform among the top nodes (top 20 nodes) in neonates.
“Moreover, Gao et al.16 also reported the left insula, right inferior frontal (orbital), and left fusiform among the top nodes (top 20 nodes) in neonates.”
From Functional properties of resting state networks in healthy full-term newborns (2015) · cites this paper as [16]
We scanned term neonates (GA at birth, range: 37.57-41.86 weeks; GA at scan: 41.50 weeks) whereas previous studies included younger neonates (Gao et al., GA at birth, range: 35-42 weeks; Fransson et al., GA at scan: 39 ± 2 weeks GA).
“We scanned term neonates (GA at birth, range: 37.57–41.86 weeks; GA at scan: 41.50 weeks) whereas previous studies1622 included younger neonates (Gao et al., GA at birth, range: 35–42 weeks; Fransson et al., GA at scan: 39 ± 2 weeks GA).”
From Functional properties of resting state networks in healthy full-term newborns (2015) · cites this paper as [16]
The hubs we identified corresponded better to hubs identified in their 1 year-old cohort.
“Interestingly, the hubs we identified corresponded better to hubs identified in their 1 year-old cohort.”
From Functional properties of resting state networks in healthy full-term newborns (2015) · cites this paper as [16]
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BackgroundInfluentialDynamic Development of Regional Cortical Thickness and Surface Area in Early Childhood
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Self-citationPruett, J. R., Kandala, S., Hoertel, S., Snyder, A. Z., Elison, J. T., Nishino, T., Feczko, E., Dosenbach, N. U. F., Nardos, B., Power, J. D., et al. (2015) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.01.003 · Cited by 57 · see citing works
The emergence of a functionally flexible brain during early infancy
Yin, W., Li, T., Hung, S.-C., Zhang, H., Wang, L., Shen, D., Zhu, H., Mucha, P. J., Cohen, J. R., & Lin, W. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2002645117 · Cited by 56 · see citing works
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Self-citationQuantitative tract-based white matter heritability in twin neonates
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Self-citationDevelopment of visual object recognition
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- Authors
- Gao, W., Gilmore, J. H., Giovanello, K. S., Smith, J. K., Shen, D., Zhu, H., & Lin, W.
- Affiliations
- University of North Carolina at Chapel Hill (US)
- Corresponding author
- Lin, Weili
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-09-23
- Volume
- 6
- Issue
- 9
- Pages
- e25278
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3179501
- OpenAlex
- W2026622593
- Cited by
- 272
- References
- 55
- Citations by year
- 2026: 12 · 2025: 15 · 2024: 18 · 2023: 11 · 2022: 21 · 2021: 17 · 2020: 47 · 2019: 18 · 2018: 29 · 2017: 17 · 2016: 14 · 2015: 18 · 2014: 15 · 2013: 16 · 2012: 3
- FWCI
- 5.68
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- UNC Libraries
- Funders
- National Institutes of Health (MH064065)
- National Institute of Mental Health (MH064065, P50MH064065, R01MH070890)
- National Institute of Neurological Disorders and Stroke (NS055754, R01NS055754)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD053000, HD053000)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Physical Sciences › Physics and Astronomy › Statistical and Nonlinear Physics › Complex Network Analysis Techniques
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Keywords
- brain network topology, infant brain development, small-world networks, functional hubs, network resilience, targeted attacks, random error, resting-state functional connectivity, information transmission, early childhood
- MeSH terms
- Brain, Brain Mapping, Female, Humans, Infant, Infant, Newborn, Magnetic Resonance Imaging, Male
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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.
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