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      Altered Topological Properties of Brain Structural Covariance Networks in Patients With Cervical Spondylotic Myelopathy

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          Abstract

          Background

          Brain structural alterations play an important role in patients with cervical spondylotic myelopathy (CSM). However, while there have been studies on regional brain structural alterations, only few studies have focused on the topological organization of the brain structural covariance network. This work aimed to describe the structural covariance network architecture alterations that are possibly linked to cortex reorganization in patients with CSM.

          Methods

          High-resolution anatomical images of 31 CSM patients and 31 healthy controls (HCs) were included in the study. The images were acquired using a sagittal three-dimensional T1-weighted BRAVO sequence. Firstly, the gray matter volume of 90 brain regions of automated anatomical labeling atlas were computed using a VBM toolbox based on the DARTEL algorithm. Then, the brain structural covariance network was constructed by thresholding the gray matter volume correlation matrices. Subsequently, the network measures and nodal property were calculated based on graph theory. Finally, the differences in the network metrics and nodal property between groups were compared using a non-parametric test.

          Results

          Patients with CSM showed larger global efficiency and smaller local efficiency, clustering coefficient, characteristic path length, and sigma values than HCs. Patients with CSM had greater betweenness in the left superior parietal gyrus (SPG.L) and the left supplementary motor area (SMA.L) than HCs. Besides, patients with CSM had smaller betweenness in right middle occipital gyrus. The brain structural covariance networks of CSM patients exhibited equal resilience to random failure as those of HCs. However, the maximum relative size of giant connected components was approximately 10% larger in HCs than in CSM patients, upon removal of 44 nodes in targeted attack.

          Conclusion

          These observed alternations in global network measures in CSM patients reflect that the brain structural covariance network in CSM exhibits the less optimal small-world model compared to that in HCs. Increased betweenness in SPG.L and SMA.L seems to be related to cortex reorganization to recover multiple sensory functions after spinal cord injury in CSM patients. The network resilience of patients with CSM exhibiting a relative mild vulnerability, compared to HCs, is probably attributable to the balance and interplay between cortex reorganization and ongoing degeneration.

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          Most cited references64

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          An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest.

          In this study, we have assessed the validity and reliability of an automated labeling system that we have developed for subdividing the human cerebral cortex on magnetic resonance images into gyral based regions of interest (ROIs). Using a dataset of 40 MRI scans we manually identified 34 cortical ROIs in each of the individual hemispheres. This information was then encoded in the form of an atlas that was utilized to automatically label ROIs. To examine the validity, as well as the intra- and inter-rater reliability of the automated system, we used both intraclass correlation coefficients (ICC), and a new method known as mean distance maps, to assess the degree of mismatch between the manual and the automated sets of ROIs. When compared with the manual ROIs, the automated ROIs were highly accurate, with an average ICC of 0.835 across all of the ROIs, and a mean distance error of less than 1 mm. Intra- and inter-rater comparisons yielded little to no difference between the sets of ROIs. These findings suggest that the automated method we have developed for subdividing the human cerebral cortex into standard gyral-based neuroanatomical regions is both anatomically valid and reliable. This method may be useful for both morphometric and functional studies of the cerebral cortex as well as for clinical investigations aimed at tracking the evolution of disease-induced changes over time, including clinical trials in which MRI-based measures are used to examine response to treatment.
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            Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain.

            An anatomical parcellation of the spatially normalized single-subject high-resolution T1 volume provided by the Montreal Neurological Institute (MNI) (D. L. Collins et al., 1998, Trans. Med. Imag. 17, 463-468) was performed. The MNI single-subject main sulci were first delineated and further used as landmarks for the 3D definition of 45 anatomical volumes of interest (AVOI) in each hemisphere. This procedure was performed using a dedicated software which allowed a 3D following of the sulci course on the edited brain. Regions of interest were then drawn manually with the same software every 2 mm on the axial slices of the high-resolution MNI single subject. The 90 AVOI were reconstructed and assigned a label. Using this parcellation method, three procedures to perform the automated anatomical labeling of functional studies are proposed: (1) labeling of an extremum defined by a set of coordinates, (2) percentage of voxels belonging to each of the AVOI intersected by a sphere centered by a set of coordinates, and (3) percentage of voxels belonging to each of the AVOI intersected by an activated cluster. An interface with the Statistical Parametric Mapping package (SPM, J. Ashburner and K. J. Friston, 1999, Hum. Brain Mapp. 7, 254-266) is provided as a freeware to researchers of the neuroimaging community. We believe that this tool is an improvement for the macroscopical labeling of activated area compared to labeling assessed using the Talairach atlas brain in which deformations are well known. However, this tool does not alleviate the need for more sophisticated labeling strategies based on anatomical or cytoarchitectonic probabilistic maps.
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              Collective dynamics of 'small-world' networks.

              Networks of coupled dynamical systems have been used to model biological oscillators, Josephson junction arrays, excitable media, neural networks, spatial games, genetic control networks and many other self-organizing systems. Ordinarily, the connection topology is assumed to be either completely regular or completely random. But many biological, technological and social networks lie somewhere between these two extremes. Here we explore simple models of networks that can be tuned through this middle ground: regular networks 'rewired' to introduce increasing amounts of disorder. We find that these systems can be highly clustered, like regular lattices, yet have small characteristic path lengths, like random graphs. We call them 'small-world' networks, by analogy with the small-world phenomenon (popularly known as six degrees of separation. The neural network of the worm Caenorhabditis elegans, the power grid of the western United States, and the collaboration graph of film actors are shown to be small-world networks. Models of dynamical systems with small-world coupling display enhanced signal-propagation speed, computational power, and synchronizability. In particular, infectious diseases spread more easily in small-world networks than in regular lattices.
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                Author and article information

                Contributors
                Journal
                Front Hum Neurosci
                Front Hum Neurosci
                Front. Hum. Neurosci.
                Frontiers in Human Neuroscience
                Frontiers Media S.A.
                1662-5161
                04 September 2020
                2020
                : 14
                : 364
                Affiliations
                Department of Radiology, Renmin Hospital of Wuhan University , Wuhan, China
                Author notes

                Edited by: Feng Liu, Tianjin Medical University General Hospital, China

                Reviewed by: Lei Gao, Zhongnan Hospital of Wuhan University, China; Ning Mao, Peking University People’s Hospital, China; Heng Chen, Guizhou University, China

                *Correspondence: Yunfei Zha, fskyanteam@ 123456126.com

                This article was submitted to Brain Imaging and Stimulation, a section of the journal Frontiers in Human Neuroscience

                Article
                10.3389/fnhum.2020.00364
                7500316
                33100992
                98a129c0-54c3-4539-ab9e-6774a5249d41
                Copyright © 2020 Kuang, Zha, Liu and Chen.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 01 June 2020
                : 10 August 2020
                Page count
                Figures: 5, Tables: 3, Equations: 0, References: 65, Pages: 14, Words: 0
                Categories
                Neuroscience
                Original Research

                Neurosciences
                cervical spondylotic myelopathy,brain structural covariance network,graph theory analysis,small world,topological properties

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