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      Controllability of structural brain networks

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          Abstract

          Cognitive function is driven by dynamic interactions between large-scale neural circuits or networks, enabling behaviour. However, fundamental principles constraining these dynamic network processes have remained elusive. Here we use tools from control and network theories to offer a mechanistic explanation for how the brain moves between cognitive states drawn from the network organization of white matter microstructure. Our results suggest that densely connected areas, particularly in the default mode system, facilitate the movement of the brain to many easily reachable states. Weakly connected areas, particularly in cognitive control systems, facilitate the movement of the brain to difficult-to-reach states. Areas located on the boundary between network communities, particularly in attentional control systems, facilitate the integration or segregation of diverse cognitive systems. Our results suggest that structural network differences between cognitive circuits dictate their distinct roles in controlling trajectories of brain network function.

          Abstract

          Cognitive control is fundamental to human intelligence, yet the principles constraining the neural dynamics of cognitive control remain elusive. Here, the authors use network control theory to demonstrate that the structure of brain networks dictates their functional role in controlling dynamics.

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          Most cited references38

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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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            Dynamic reconfiguration of human brain networks during learning.

            Human learning is a complex phenomenon requiring flexibility to adapt existing brain function and precision in selecting new neurophysiological activities to drive desired behavior. These two attributes--flexibility and selection--must operate over multiple temporal scales as performance of a skill changes from being slow and challenging to being fast and automatic. Such selective adaptability is naturally provided by modular structure, which plays a critical role in evolution, development, and optimal network function. Using functional connectivity measurements of brain activity acquired from initial training through mastery of a simple motor skill, we investigate the role of modularity in human learning by identifying dynamic changes of modular organization spanning multiple temporal scales. Our results indicate that flexibility, which we measure by the allegiance of nodes to modules, in one experimental session predicts the relative amount of learning in a future session. We also develop a general statistical framework for the identification of modular architectures in evolving systems, which is broadly applicable to disciplines where network adaptability is crucial to the understanding of system performance.
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              Evidence for hubs in human functional brain networks.

              Hubs integrate and distribute information in powerful ways due to the number and positioning of their contacts in a network. Several resting-state functional connectivity MRI reports have implicated regions of the default mode system as brain hubs; we demonstrate that previous degree-based approaches to hub identification may have identified portions of large brain systems rather than critical nodes of brain networks. We utilize two methods to identify hub-like brain regions: (1) finding network nodes that participate in multiple subnetworks of the brain, and (2) finding spatial locations in which several systems are represented within a small volume. These methods converge on a distributed set of regions that differ from previous reports on hubs. This work identifies regions that support multiple systems, leading to spatially constrained predictions about brain function that may be tested in terms of lesions, evoked responses, and dynamic patterns of activity. Copyright © 2013 Elsevier Inc. All rights reserved.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Pub. Group
                2041-1723
                01 October 2015
                2015
                : 6
                : 8414
                Affiliations
                [1 ]Department of Applied Mathematics and Computational Science, University of Pennsylvania , Philadelphia, Pennsylvania 19104, USA
                [2 ]Department of Bioengineering, University of Pennsylvania , Philadelphia, Pennsylvania 19104, USA
                [3 ]Department of Mechanical Engineering, University of California , Riverside, California 92521, USA
                [4 ]Department of Psychological and Brain Sciences, University of California , Santa Barbara, California 93106, USA
                [5 ]Translational Neuroscience Branch, Army Research Laboratory , Aberdeen Proving Ground, Aberdeen, Maryland 20783, USA
                [6 ]Department of Electrical and Systems Engineering, University of Pennsylvania , Philadelphia, Pennsylvania 19104, USA
                Author notes
                Article
                ncomms9414
                10.1038/ncomms9414
                4600713
                26423222
                ba9fc7c7-8460-4a6e-8e12-c74f2eb9a042
                Copyright © 2015, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 07 April 2015
                : 19 August 2015
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