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      Cliques and cavities in the human connectome

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          Abstract

          Encoding brain regions and their connections as a network of nodes and edges captures many of the possible paths along which information can be transmitted as humans process and perform complex behaviors. Because cognitive processes involve large, distributed networks of brain areas, principled examinations of multi-node routes within larger connection patterns can offer fundamental insights into the complexities of brain function. Here, we investigate both densely connected groups of nodes that could perform local computations as well as larger patterns of interactions that would allow for parallel processing. Finding such structures necessitates that we move from considering exclusively pairwise interactions to capturing higher order relations, concepts naturally expressed in the language of algebraic topology. These tools can be used to study mesoscale network structures that arise from the arrangement of densely connected substructures called cliques in otherwise sparsely connected brain networks. We detect cliques (all-to-all connected sets of brain regions) in the average structural connectomes of 8 healthy adults scanned in triplicate and discover the presence of more large cliques than expected in null networks constructed via wiring minimization, providing architecture through which brain network can perform rapid, local processing. We then locate topological cavities of different dimensions, around which information may flow in either diverging or converging patterns. These cavities exist consistently across subjects, differ from those observed in null model networks, and – importantly – link regions of early and late evolutionary origin in long loops, underscoring their unique role in controlling brain function. These results offer a first demonstration that techniques from algebraic topology offer a novel perspective on structural connectomics, highlighting loop-like paths as crucial features in the human brain’s structural architecture.

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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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            Small-world brain networks.

            Many complex networks have a small-world topology characterized by dense local clustering or cliquishness of connections between neighboring nodes yet a short path length between any (distant) pair of nodes due to the existence of relatively few long-range connections. This is an attractive model for the organization of brain anatomical and functional networks because a small-world topology can support both segregated/specialized and distributed/integrated information processing. Moreover, small-world networks are economical, tending to minimize wiring costs while supporting high dynamical complexity. The authors introduce some of the key mathematical concepts in graph theory required for small-world analysis and review how these methods have been applied to quantification of cortical connectivity matrices derived from anatomical tract-tracing studies in the macaque monkey and the cat. The evolution of small-world networks is discussed in terms of a selection pressure to deliver cost-effective information-processing systems. The authors illustrate how these techniques and concepts are increasingly being applied to the analysis of human brain functional networks derived from electroencephalography/magnetoencephalography and fMRI experiments. Finally, the authors consider the relevance of small-world models for understanding the emergence of complex behaviors and the resilience of brain systems to pathological attack by disease or aberrant development. They conclude that small-world models provide a powerful and versatile approach to understanding the structure and function of human brain systems.
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              The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology.

              The human orbitofrontal cortex is an important brain region for the processing of rewards and punishments, which is a prerequisite for the complex and flexible emotional and social behaviour which contributes to the evolutionary success of humans. Yet much remains to be discovered about the functions of this key brain region, and new evidence from functional neuroimaging and clinical neuropsychology is affording new insights into the different functions of the human orbitofrontal cortex. We review the neuroanatomical and neuropsychological literature on the human orbitofrontal cortex, and propose two distinct trends of neural activity based on a meta-analysis of neuroimaging studies. One is a mediolateral distinction, whereby medial orbitofrontal cortex activity is related to monitoring the reward value of many different reinforcers, whereas lateral orbitofrontal cortex activity is related to the evaluation of punishers which may lead to a change in ongoing behaviour. The second is a posterior-anterior distinction with more complex or abstract reinforcers (such as monetary gain and loss) represented more anteriorly in the orbitofrontal cortex than simpler reinforcers such as taste or pain. Finally, we propose new neuroimaging methods for obtaining further evidence on the localisation of function in the human orbitofrontal cortex.
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                Author and article information

                Contributors
                annsize@seas.upenn.edu
                cgiusti@seas.upenn.edu
                arikahn@seas.upenn.edu
                jvettel@gmail.com
                rbetzel@seas.upenn.edu
                dsb@seas.upenn.edu
                Journal
                J Comput Neurosci
                J Comput Neurosci
                Journal of Computational Neuroscience
                Springer US (New York )
                0929-5313
                1573-6873
                16 November 2017
                16 November 2017
                2018
                : 44
                : 1
                : 115-145
                Affiliations
                [1 ]ISNI 0000 0004 1936 8972, GRID grid.25879.31, Department of Bioengineering, , University of Pennsylvania, ; Philadelphia, PA USA
                [2 ]ISNI 0000 0001 2341 2786, GRID grid.116068.8, Broad Institute, , Harvard University and the Massachusetts Institute of Technology, ; Cambridge, MA USA
                [3 ]ISNI 0000 0001 2151 958X, GRID grid.420282.e, Human Research & Engineering Directorate, , U.S. Army Research Laboratory, ; Aberdeen, MD USA
                [4 ]ISNI 0000 0004 1936 9676, GRID grid.133342.4, Department of Psychological and Brain Sciences, , University of California, ; Santa Barbara, CA USA
                [5 ]ISNI 0000 0004 1936 8972, GRID grid.25879.31, Department of Electrical & Systems Engineering, , University of Pennsylvania, ; Philadelphia, PA USA
                Author notes

                Action Editor: Abraham Zvi Snyder

                Author information
                http://orcid.org/0000-0002-6183-4493
                Article
                672
                10.1007/s10827-017-0672-6
                5769855
                29143250
                8fce7b38-c21e-4419-bad7-cb5a2dd8565b
                © The Author(s) 2017

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

                History
                : 19 May 2017
                : 30 September 2017
                : 27 October 2017
                Funding
                Funded by: FundRef https://doi.org/10.13039/100000086, Directorate for Mathematical and Physical Sciences;
                Award ID: PHY-1554488
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100000088, Directorate for Social, Behavioral and Economic Sciences;
                Award ID: BCS-1441502
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100000870, John D. and Catherine T. MacArthur Foundation;
                Funded by: FundRef https://doi.org/10.13039/100000879, Alfred P. Sloan Foundation;
                Categories
                Article
                Custom metadata
                © Springer Science+Business Media, LLC, part of Springer Nature 2018

                Neurosciences
                applied topology,persistent homology,network neuroscience
                Neurosciences
                applied topology, persistent homology, network neuroscience

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