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      Structural and Functional Rich Club Organization of the Brain in Children and Adults

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          Abstract

          Recent studies using Magnetic Resonance Imaging (MRI) have proposed that the brain’s white matter is organized as a rich club, whereby the most highly connected regions of the brain are also highly connected to each other. Here we use both functional and diffusion-weighted MRI in the human brain to investigate whether the rich club phenomena is present with functional connectivity, and how this organization relates to the structural phenomena. We also examine whether rich club regions serve to integrate information between distinct brain systems, and conclude with a brief investigation of the developmental trajectory of rich-club phenomena. In agreement with prior work, both adults and children showed robust structural rich club organization, comprising regions of the superior medial frontal/dACC, medial parietal/PCC, insula, and inferior temporal cortex. We also show that these regions were highly integrated across the brain’s major networks. Functional brain networks were found to have rich club phenomena in a similar spatial layout, but a high level of segregation between systems. While no significant differences between adults and children were found structurally, adults showed significantly greater functional rich club organization. This difference appeared to be driven by a specific set of connections between superior parietal, insula, and supramarginal cortex. In sum, this work highlights the existence of both a structural and functional rich club in adult and child populations with some functional changes over development. It also offers a potential target in examining atypical network organization in common developmental brain disorders, such as ADHD and Autism.

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          Most cited references29

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          Modularity and community structure in networks

          M. Newman (2006)
          Many networks of interest in the sciences, including a variety of social and biological networks, are found to divide naturally into communities or modules. The problem of detecting and characterizing this community structure has attracted considerable recent attention. One of the most sensitive detection methods is optimization of the quality function known as "modularity" over the possible divisions of a network, but direct application of this method using, for instance, simulated annealing is computationally costly. Here we show that the modularity can be reformulated in terms of the eigenvectors of a new characteristic matrix for the network, which we call the modularity matrix, and that this reformulation leads to a spectral algorithm for community detection that returns results of better quality than competing methods in noticeably shorter running times. We demonstrate the algorithm with applications to several network data sets.
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            Rich-club organization of the human connectome.

            The human brain is a complex network of interlinked regions. Recent studies have demonstrated the existence of a number of highly connected and highly central neocortical hub regions, regions that play a key role in global information integration between different parts of the network. The potential functional importance of these "brain hubs" is underscored by recent studies showing that disturbances of their structural and functional connectivity profile are linked to neuropathology. This study aims to map out both the subcortical and neocortical hubs of the brain and examine their mutual relationship, particularly their structural linkages. Here, we demonstrate that brain hubs form a so-called "rich club," characterized by a tendency for high-degree nodes to be more densely connected among themselves than nodes of a lower degree, providing important information on the higher-level topology of the brain network. Whole-brain structural networks of 21 subjects were reconstructed using diffusion tensor imaging data. Examining the connectivity profile of these networks revealed a group of 12 strongly interconnected bihemispheric hub regions, comprising the precuneus, superior frontal and superior parietal cortex, as well as the subcortical hippocampus, putamen, and thalamus. Importantly, these hub regions were found to be more densely interconnected than would be expected based solely on their degree, together forming a rich club. We discuss the potential functional implications of the rich-club organization of the human connectome, particularly in light of its role in information integration and in conferring robustness to its structural core.
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              A dual-networks architecture of top-down control.

              Complex systems ensure resilience through multiple controllers acting at rapid and slower timescales. The need for efficient information flow through complex systems encourages small-world network structures. On the basis of these principles, a group of regions associated with top-down control was examined. Functional magnetic resonance imaging showed that each region had a specific combination of control signals; resting-state functional connectivity grouped the regions into distinct 'fronto-parietal' and 'cingulo-opercular' components. The fronto-parietal component seems to initiate and adjust control; the cingulo-opercular component provides stable 'set-maintenance' over entire task epochs. Graph analysis showed dense local connections within components and weaker 'long-range' connections between components, suggesting a small-world architecture. The control systems of the brain seem to embody the principles of complex systems, encouraging resilient performance.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                5 February 2014
                : 9
                : 2
                : e88297
                Affiliations
                [1 ]Department of Behavioral Neuroscience, Oregon Health & Science University, Portland, Oregon, United States of America
                [2 ]Center for Neuroscience, University of California – Davis, Davis, California, United States of America
                [3 ]Institute of Psychiatry, Hospital das Clínicas, University of São Paulo Medical School, São Paulo, Brazil
                [4 ]Department of Psychiatry, Oregon Health & Science University, Portland, Oregon, United States of America
                [5 ]Advanced Imaging Research Center, Oregon Health & Science University, Portland, Oregon, United States of America
                Beijing Normal University, China
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: DG DF JN. Performed the experiments: DG SC TGCD CS. Analyzed the data: DG SR. Contributed reagents/materials/analysis tools: DF DG SR SI. Wrote the paper: DF DG.

                Article
                PONE-D-13-32567
                10.1371/journal.pone.0088297
                3915050
                24505468
                2e84dd38-a94c-4b67-b576-319e1f44dfda
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 2 July 2013
                : 6 January 2014
                Page count
                Pages: 13
                Funding
                Funders for grants R00 MH091238 (DF), R01 MH096773 (DF) and R01 MH086654 (JN) are National Institutes of Health and National Institute of Mental Health. Funding also included Oregon Clinical and Translational Research Institute (DF), Medical Research Foundation (DF), R01 MH096773 (DF), and McDonnell Foundation (Petersen/Sporns/DF). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Neuroscience
                Neuroimaging
                fMRI
                Cognitive Neuroscience
                Developmental Neuroscience
                Neural Networks

                Uncategorized
                Uncategorized

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