Topological organization of functional brain networks in healthy children: differences in relation to age, sex, and intelligence.
paper
Cited
Public
- Authors
- Wu, Kai; Taki, Yasuyuki; Sato, Kazunori; Hashizume, Hiroshi; Sassa, Yuko; Takeuchi, Hikaru; Thyreau, Benjamin; He, Yong; Evans, Alan C; Li, Xiaobo; Kawashima, Ryuta; Fukuda, Hiroshi
- Year
- 2013
- Journal
- PloS one
- PMID
- 23390528
- DOI
- 10.1371/journal.pone.0055347
- PMCID
- PMC3563524
Recent studies have demonstrated developmental changes of functional brain networks derived from functional connectivity using graph theoretical analysis, which has been rapidly translated to studies of brain network organization. However, little is known about sex- and IQ-related differences in the topological organization of functional brain networks during development. In this study, resting-state fMRI (rs-fMRI) was used to map the functional brain networks in 51 healthy children. We then investigated the effects of age, sex, and IQ on economic small-world properties and regional nodal properties of the functional brain networks. At a global level of whole networks, we found significant age-related increases in the small-worldness and local efficiency, significant higher values of the global efficiency in boys compared with girls, and no significant IQ-related difference. Age-related increases in the regional nodal properties were found predominately in the frontal brain regions, whereas the parietal, temporal, and occipital brain regions showed age-related decreases. Significant sex-related differences in the regional nodal properties were found in various brain regions, primarily related to the default mode, language, and vision systems. Positive correlations between IQ and the regional nodal properties were found in several brain regions related to the attention system, whereas negative correlations were found in various brain regions primarily involved in the default mode, emotion, and language systems. Together, our findings of the network topology of the functional brain networks in healthy children and its relationship with age, sex, and IQ bring new insights into the understanding of brain maturation and cognitive development during childhood and adolescence.
Global network properties.(A) The clustering coefficient and (B) the characteristic path length are shown as a function of cost thresholds and compared to the matched random networks. (C) The normalized clustering coefficient, the normalized characteristic path length, and (D) the small-worldness are shown as a function of cost thresholds. Note that the small-world regime of cost threshold adopted in this study was from 0.2 to 0.35. (E) The local efficiency and (F) the global efficiency are shown as a function of cost thresholds and compared to the matched random networks. Error bars indicate standard error in all subjects.
Global hubs in functional brain networks.Global hubs are defined as the brain regions with higher values (>Mean + SD) in any of (A) node degree, (B) node efficiency, and (C) node betweenness. The global hubs are shown in red with node sizes that indicate the values in regional nodal parameters. For a description of the abbreviations, see Table S1.
Effect of age on regional nodal properties.Significant linear positive, linear negative, quadratic positive, and quadratic negative correlations are indicated by red, green, yellow, and blue spheres, respectively. The significances of p<0.05 and p<0.01(uncorrected) are shown by spheres in small and big size, respectively. For a description of the abbreviations, see Table S1.
Effect of sex on regional nodal properties.The significant higher values of regional nodal parameters in female and male groups are shown in red and blue, respectively. The significances of p<0.05 and p<0.01 (uncorrected) are indicated by spheres in small and big size, respectively. For a description of the abbreviations, see Table S1.
Age-by-sex interaction on regional nodal properties.The significant age-by-sex interactions on regional nodal parameters are shown. The correlation between age and regional nodal parameters are shown in female and male groups, respectively. For a description of the abbreviations, see Table S1.
Effect of IQ on regional nodal properties.The significant positive and negative correlation between IQ and regional nodal parameters are shown in red and blue, respectively. The significances of p<0.05 and p<0.01 (uncorrected) are indicated by spheres in small and big size, respectively. For a description of the abbreviations, see Table S1.
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| Name | Type |
|---|---|
| adolescents | cohort |
| adults | cohort |
| age | phenotype |
| Age-related increase local | phenotype |
| Anatomical connectivity local | anatomy |
| angular gyrus | anatomy |
| anterior cingulate cortex | anatomy |
| attention deficit hyperactivity disorder | phenotype |
| Attention system local | anatomy |
| Auditory functions local | phenotype |
| autism | phenotype |
| Automated Anatomical Labeling atlas local | anatomy |
| bilateral inferior parietal cortex | anatomy |
| brain | anatomy |
| brain anatomical networks local | anatomy |
| brain network properties local | phenotype |
| brain networks | anatomy |
| Brain perfusion local | anatomy |
| brain structure | anatomy |
| Calcarine Cortex local | anatomy |
| CAL.R local | anatomy |
| characteristic path length | phenotype |
| children | cohort |
| children and young adults local | cohort |
| children with normal development local | cohort |
| clustering coefficient local | phenotype |
| Clustering coefficient local | phenotype |
| cognition | phenotype |
| control system local | anatomy |
| Control system local | anatomy |
| CUN.L local | anatomy |
| default mode network | anatomy |
| default mode system local | anatomy |
| Default mode system local | anatomy |
| development | phenotype |
| dorsal superior frontal gyrus local | anatomy |
| Dorsal Superior Frontal Gyrus local | anatomy |
| DTI | drug |
| DVARS local | phenotype |
| Emotion | phenotype |
| Emotion system local | anatomy |
| Excluded subjects (9 subjects) local | cohort |
| executive functioning | phenotype |
| Frame-wise displacement local | phenotype |
| frontal cortex | anatomy |
| functional brain network local | anatomy |
| functional connectivity | phenotype |
| functional network measures local | phenotype |
| fusiform gyrus | anatomy |
| girl local | cohort |
| global efficiency local | phenotype |
| Global efficiency local | phenotype |
| global hub local | phenotype |
| gyrus rectus | anatomy |
| head motion | phenotype |
| healthy children local | phenotype |
| Healthy Japanese children local | cohort |
| Healthy pediatric subjects local | cohort |
| heschl gyrus | anatomy |
| HES.L local | anatomy |
| HES.R local | anatomy |
| Higher-order cognitive functions local | phenotype |
| HIP.L local | anatomy |
| hippocampus | anatomy |
| HIP.R local | anatomy |
| human brain | anatomy |
| human brain networks local | anatomy |
| human connectome local | cohort |
| IFGtriang.L local | anatomy |
| Infant brain local | cohort |
| inferior occipital gyrus | anatomy |
| inferior orbital frontal cortex local | anatomy |
| inferior orbitofrontal cortex local | anatomy |
| insula | anatomy |
| intelligence | phenotype |
| IPL | anatomy |
| IQ | phenotype |
| ITG.L local | anatomy |
| language system local | anatomy |
| Language system local | anatomy |
| left cuneus | anatomy |
| left hemispheric network local | anatomy |
| left Heschl's gyrus local | anatomy |
| left hippocampal formation local | anatomy |
| left inferior orbital frontal cortex local | anatomy |
| left inferior parietal lobule | anatomy |
| left inferior temporal gyrus | anatomy |
| left lingual gyrus local | anatomy |
| left medial superior frontal gyrus local | anatomy |
| left middle frontal gyrus | anatomy |
| left olfactory cortex local | anatomy |
| Left REC local | anatomy |
| left rectus gyrus local | anatomy |
| Left SPG local | anatomy |
| left superior temporal gyrus | anatomy |
| Linear age-related decrease local | phenotype |
| linear decrease in node degree local | phenotype |
| linear increase in node degree local | phenotype |
| LING.L local | anatomy |
| lingual gyrus | anatomy |
| local efficiency local | phenotype |
| Local efficiency local | phenotype |
| Locally specialized processing local | phenotype |
| matched random networks local | anatomy |
| MCG.R local | anatomy |
| medial orbitofrontal cortex | anatomy |
| medial prefrontal cortex | anatomy |
| medial superior frontal gyrus | anatomy |
| MFG.L local | anatomy |
| Middle Cingulate Gyrus local | anatomy |
| middle frontal gyrus | anatomy |
| Miyagi child cohort local | cohort |
| negative quadratic trajectory of node degree local | phenotype |
| neurological disorders | phenotype |
| node betweenness local | phenotype |
| Node betweenness local | phenotype |
| Node betweenness in left REC local | phenotype |
| node degree local | phenotype |
| Node degree in left SPG local | phenotype |
| node efficiency local | phenotype |
| Node efficiency local | phenotype |
| Node efficiency in left cuneus local | phenotype |
| Node efficiency in left SPG local | phenotype |
| normalized characteristic path length local | phenotype |
| Normalized characteristic path length local | phenotype |
| normalized clustering coefficient local | phenotype |
| Normalized clustering coefficient local | phenotype |
| Occipital brain region local | anatomy |
| occipital cortex | anatomy |
| OLF.L local | anatomy |
| ORBinf local | anatomy |
| ORBinf.L local | anatomy |
| ORBinf.R local | anatomy |
| ORBmed.R local | anatomy |
| PAL.L local | anatomy |
| pallidum | anatomy |
| paracentral lobule | anatomy |
| Parietal brain region local | anatomy |
| parietal cortex | anatomy |
| PCG.L local | anatomy |
| PCUN.L local | anatomy |
| positive quadratic trajectory of node degree local | phenotype |
| postcentral gyrus | anatomy |
| posterior cingulate cortex | anatomy |
| precuneus | anatomy |
| precuneus/posterior cingulate regions local | anatomy |
| prefrontal lobe local | anatomy |
| Primary motor/somatosensory functions local | phenotype |
| psychiatric disorders | phenotype |
| putamen | anatomy |
| PUT.L local | anatomy |
| Quadratic developmental trajectory local | phenotype |
| REC local | anatomy |
| REC.L local | anatomy |
| resting-state fMRI local | drug |
| right-handed children local | phenotype |
| right hemispheric network local | anatomy |
| right inferior orbital frontal cortex local | anatomy |
| right inferior parietal lobule | anatomy |
| right medial superior frontal gyrus local | anatomy |
| right middle cingulate gyrus local | anatomy |
| right middle frontal gyrus | anatomy |
| right paracentral lobule local | anatomy |
| Right REC local | anatomy |
| rolandic operculum | anatomy |
| rs-fMRI local | drug |
| schizophrenia | phenotype |
| sex | phenotype |
| sex differences | phenotype |
| sexes local | phenotype |
| SFGdor.L local | anatomy |
| SFGmed.R local | anatomy |
| SFMmed.R local | anatomy |
| SMA.L local | anatomy |
| small-worldness local | phenotype |
| Small-worldness local | phenotype |
| Small-world organization local | phenotype |
| Small-world properties | phenotype |
| small-world regime local | phenotype |
| SMA.R local | anatomy |
| SPG.L local | anatomy |
| SPG.R local | anatomy |
| STG.L local | anatomy |
| structural brain networks local | anatomy |
| structural brain networks local | phenotype |
| Structural brain networks local | anatomy |
| structural MRI | drug |
| Study cohort (51 subjects) local | cohort |
| Summary network parameter local | phenotype |
| summary network parameters local | phenotype |
| superior occipital gyrus | anatomy |
| superior orbitofrontal cortex local | anatomy |
| superior parietal gyrus local | anatomy |
| Superior Parietal Gyrus local | anatomy |
| superior temporal gyrus | anatomy |
| superior temporal pole local | anatomy |
| supplementary motor area | anatomy |
| supramarginal gyrus | anatomy |
| Temporal brain region local | anatomy |
| triangular part of inferior frontal gyrus local | anatomy |
| vision system local | anatomy |
| Visual functions local | phenotype |
| Visual-input analysis local | phenotype |
| visual processing | phenotype |
| visuospatial function local | phenotype |
| whole brain | anatomy |
| young adults | cohort |
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In this knowledge base
External
| Title | Authors | Journal | Year | Link |
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| Differential effects of local and general fatigue on brain network efficiency, corticospinal and neuromuscular excitability. | Yu C et al. | — | 2026 | → |
| Sex-specific neurodevelopmental pathways to depressive symptoms. | Chan SY et al. | — | 2026 | → |
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| Fiber length distribution characterizes the brain network maturation during early school-age. | Yu Y et al. | — | 2025 | → |
| Fitbit-measured sleep duration in young adolescents is associated with functional connectivity in attentional, executive control, memory, and sensory networks. | Turan O et al. | — | 2025 | → |
| Human lifespan changes in the brain's functional connectome. | Sun L et al. | — | 2025 | → |
| Regional, but not brain-wide, graph theoretic measures are robustly and reproducibly linked to general cognitive ability. | Molloy MF et al. | — | 2025 | → |
| Digital Media and Developing Brains: Concerns and Opportunities. | Hutton JS et al. | — | 2024 | → |
| Distinct structural brain network properties in children with familial versus non-familial attention-deficit/hyperactivity disorder (ADHD). | Baboli R et al. | — | 2024 | → |
| Functional connectivity development along the sensorimotor-association axis enhances the cortical hierarchy. | Luo AC et al. | — | 2024 | → |
| Local gradient analysis of human brain function using the Vogt-Bailey Index. | Farrugia C et al. | — | 2024 | → |
| Macronutrient intake is associated with intelligence and neural development in adolescents. | Nakamura Y et al. | — | 2024 | → |
| Neural Signature of Rhyming Ability During Story Listening in Preschool-Age Children. | Hutton JS et al. | — | 2024 | → |
| Sex differences in human brain networks in normal and psychiatric populations from the perspective of small-world properties. | Zhou Y et al. | — | 2024 | → |
| Sex-related patterns of functional brain networks in children and adolescents with autism spectrum disorder. | Li C et al. | — | 2024 | → |
| The aging trajectories of brain functional hierarchy and its impact on cognition across the adult lifespan. | Wang X et al. | — | 2024 | → |
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| Brain Networks and Adolescent Alcohol Use. | Yip SW et al. | — | 2023 | → |
| Diffusion tensor imaging reveals sex differences in pain sensitivity of rats. | Cha M et al. | — | 2023 | → |
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| Association between the Use of Folic Acid Supplements during Pregnancy and Children's Cognitive Function at 7-9 Years of Age in the INMA Cohort Study. | Compañ-Gabucio LM et al. | — | 2022 | → |
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| Cognitive stimulation has potential for brain activation in individuals with Rett syndrome. | Migliorelli C et al. | — | 2022 | → |
| Disrupted Resting State Attentional Network Connectivity in Adolescent and Young Adult Cannabis Users following Two-Weeks of Monitored Abstinence. | Harris JC et al. | — | 2022 | → |
| The impact of micronutrient supplementation in alcohol-exposed pregnancies on reaction time responses of preschoolers in Ukraine. | Kable JA et al. | — | 2022 | → |
| White matter and sustained attention in children with attention/deficit-hyperactivity disorder: A longitudinal fixel-based analysis. | Thomson P et al. | — | 2022 | → |
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| Cerebral microinfarcts affect brain structural network topology in cognitively impaired patients. | Zhang L et al. | — | 2021 | → |
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| Intelligence and academic performance: Is it all in your head? | Bottenhorn KL et al. | — | 2021 | — |
| Modifications in the Topological Structure of EEG Functional Connectivity Networks during Listening Tonal and Atonal Concert Music in Musicians and Non-Musicians. | González A et al. | — | 2021 | → |
| The maturation and cognitive relevance of structural brain network organization from early infancy to childhood. | Woodburn M et al. | — | 2021 | → |
| The neurodevelopmental basis of humor appreciation: A fNIRS study of young children. | Mayseless N et al. | — | 2021 | → |
| The Use of Lower or Higher Than Recommended Doses of Folic Acid Supplements during Pregnancy Is Associated with Child Attentional Dysfunction at 4-5 Years of Age in the INMA Project. | Compañ Gabucio LM et al. | — | 2021 | → |
| Within node connectivity changes, not simply edge changes, influence graph theory measures in functional connectivity studies of the brain. | Luo W et al. | — | 2021 | → |
| A Novel Individual Metabolic Brain Network for 18F-FDG PET Imaging. | Huang SY et al. | — | 2020 | → |
| Applications of Resting-State fNIRS in the Developing Brain: A Review From the Connectome Perspective. | Hu Z et al. | — | 2020 | → |
| Associations between Neighborhood SES and Functional Brain Network Development. | Tooley UA et al. | — | 2020 | → |
| Development of Network Topology and Functional Connectivity of the Prefrontal Cortex. | Lopez KC et al. | — | 2020 | → |
| Predicting full-scale and verbal intelligence scores from functional Connectomic data in individuals with autism Spectrum disorder. | Dryburgh E et al. | — | 2020 | → |
| Sex Differences in Functional Connectivity of the Salience, Default Mode, and Central Executive Networks in Youth with ASD. | Lawrence KE et al. | — | 2020 | → |
| Transcranial photobiomodulation-induced changes in human brain functional connectivity and network metrics mapped by whole-head functional near-infrared spectroscopy <i>in vivo</i>. | Urquhart EL et al. | — | 2020 | → |
| Application of Graph Theory for Identifying Connectivity Patterns in Human Brain Networks: A Systematic Review. | Farahani FV et al. | — | 2019 | → |
| Developmental changes in functional brain networks from birth through adolescence. | Gozdas E et al. | — | 2019 | → |
| First-year development of modules and hubs in infant brain functional networks. | Wen X et al. | — | 2019 | → |
| Functional near-infrared spectroscopy evidence for the development of topological asymmetry between hemispheric brain networks from childhood to adulthood. | Cai L et al. | — | 2019 | → |
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| The development of brain network hubs. | Oldham S et al. | — | 2019 | → |
| What has sex got to do with it? The role of hormones in the transgender brain. | Nguyen HB et al. | — | 2019 | → |
| Age Related Changes in Topological Properties of Brain Functional Network and Structural Connectivity. | Shah C et al. | — | 2018 | → |
| Alterations in Brain Network Topology and Structural-Functional Connectome Coupling Relate to Cognitive Impairment. | Wang J et al. | — | 2018 | → |
| Alterations in Normal Aging Revealed by Cortical Brain Network Constructed Using IBASPM. | Li W et al. | — | 2018 | → |
| A Network Neuroscience Approach to Typical and Atypical Brain Development. | Morgan SE et al. | — | 2018 | → |
| A systematic literature review of sex differences in childhood language and brain development. | Etchell A et al. | — | 2018 | → |
| EEG Resting State Functional Connectivity in Adult Dyslexics Using Phase Lag Index and Graph Analysis. | Fraga González G et al. | — | 2018 | → |
| Key Brain Network Nodes Show Differential Cognitive Relevance and Developmental Trajectories during Childhood and Adolescence. | Kolskår KK et al. | — | 2018 | → |
| PAGANI Toolkit: Parallel graph-theoretical analysis package for brain network big data. | Du H et al. | — | 2018 | → |
| The development of functional network organization in early childhood and early adolescence: A resting-state fNIRS study. | Cai L et al. | — | 2018 | → |
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| Complementarity of sex differences in brain and behavior: From laterality to multimodal neuroimaging. | Gur RC et al. | — | 2017 | → |
| Development of large-scale functional networks from birth to adulthood: A guide to the neuroimaging literature. | Grayson DS et al. | — | 2017 | → |
| Effect of Resting-State fNIRS Scanning Duration on Functional Brain Connectivity and Graph Theory Metrics of Brain Network. | Geng S et al. | — | 2017 | → |
| Functional connectivity abnormalities and associated cognitive deficits in fetal alcohol Spectrum disorders (FASD). | Wozniak JR et al. | — | 2017 | → |
| Genetic correlates of the development of theta event related oscillations in adolescents and young adults. | Chorlian DB et al. | — | 2017 | → |
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| Mechanism of Cerebralcare Granule® for Improving Cognitive Function in Resting-State Brain Functional Networks of Sub-healthy Subjects. | Li J et al. | — | 2017 | → |
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| Functional Connectome before and following Temporal Lobectomy in Mesial Temporal Lobe Epilepsy. | Liao W et al. | — | 2016 | → |
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| Intrinsic connectivity networks from childhood to late adolescence: Effects of age and sex. | Solé-Padullés C et al. | — | 2016 | → |
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| The maturation of mismatch negativity networks in normal adolescence. | Cooray GK et al. | — | 2016 | → |
| Toward Developmental Connectomics of the Human Brain. | Cao M et al. | — | 2016 | → |
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| Connectome-Scale Assessments of Functional Connectivity in Children with Primary Monosymptomatic Nocturnal Enuresis. | Lei D et al. | — | 2015 | → |
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| Sex and the migraine brain. | Borsook D et al. | — | 2014 | → |
| The effects of pediatric epilepsy on a language connectome. | Eddin AS et al. | — | 2014 | → |
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