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Graph Theoretical Analysis of Structural Neuroimaging in Temporal Lobe Epilepsy with and without Psychosis

PURPOSE: Psychosis is one of the most important psychiatric comorbidities in temporal lobe epilepsy (TLE), and its pathophysiology still remains unsolved. We aimed to explore the connectivity differences of structural neuroimaging between TLE with and without psychosis using a graph theoretical anal...

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Autores principales: Sone, Daichi, Matsuda, Hiroshi, Ota, Miho, Maikusa, Norihide, Kimura, Yukio, Sumida, Kaoru, Yokoyama, Kota, Imabayashi, Etsuko, Watanabe, Masako, Watanabe, Yutaka, Okazaki, Mitsutoshi, Sato, Noriko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4934878/
https://www.ncbi.nlm.nih.gov/pubmed/27385130
http://dx.doi.org/10.1371/journal.pone.0158728
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author Sone, Daichi
Matsuda, Hiroshi
Ota, Miho
Maikusa, Norihide
Kimura, Yukio
Sumida, Kaoru
Yokoyama, Kota
Imabayashi, Etsuko
Watanabe, Masako
Watanabe, Yutaka
Okazaki, Mitsutoshi
Sato, Noriko
author_facet Sone, Daichi
Matsuda, Hiroshi
Ota, Miho
Maikusa, Norihide
Kimura, Yukio
Sumida, Kaoru
Yokoyama, Kota
Imabayashi, Etsuko
Watanabe, Masako
Watanabe, Yutaka
Okazaki, Mitsutoshi
Sato, Noriko
author_sort Sone, Daichi
collection PubMed
description PURPOSE: Psychosis is one of the most important psychiatric comorbidities in temporal lobe epilepsy (TLE), and its pathophysiology still remains unsolved. We aimed to explore the connectivity differences of structural neuroimaging between TLE with and without psychosis using a graph theoretical analysis, which is an emerging mathematical method to investigate network connections in the brain as a small-world system. MATERIALS AND METHODS: We recruited 11 TLE patients with unilateral hippocampal sclerosis (HS) presenting psychosis or having a history of psychosis (TLE-P group). As controls, 15 TLE patients with unilateral HS without any history of psychotic episodes were also recruited (TLE-N group). For graph theoretical analysis, the normalized gray matter images of both groups were subjected to Graph Analysis Toolbox (GAT). As secondary analyses, each group was compared to 14 age- and gender-matched healthy subjects. RESULTS: The hub node locations were found predominantly in the ipsilateral hemisphere in the TLE-N group, and mainly on the contralateral side in the TLE-P group. The TLE-P group showed significantly higher characteristic path length, transitivity, lower global efficiency, and resilience to random or targeted attack than those of the TLE-N group. The regional comparison in betweenness centrality revealed significantly decreased connectivity in the contralateral temporal lobe, ipsilateral middle frontal gyrus, and bilateral postcentral gyri in the TLE-P group. The healthy subjects showed well-balanced nodes/edges distributions, similar metrics to TLE-N group except for higher small-worldness/modularity/assortativity, and various differences of regional betweenness/clustering. CONCLUSION: In TLE with psychosis, graph theoretical analysis of structural imaging revealed disrupted connectivity in the contralateral hemisphere. The network metrics suggested that the existence of psychosis can bring vulnerability and decreased efficiency of the whole-brain network. The sharp differences in structural networks between morphologically homogeneous groups are remarkable and may contribute to a better understanding of psychosis in TLE.
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spelling pubmed-49348782016-07-18 Graph Theoretical Analysis of Structural Neuroimaging in Temporal Lobe Epilepsy with and without Psychosis Sone, Daichi Matsuda, Hiroshi Ota, Miho Maikusa, Norihide Kimura, Yukio Sumida, Kaoru Yokoyama, Kota Imabayashi, Etsuko Watanabe, Masako Watanabe, Yutaka Okazaki, Mitsutoshi Sato, Noriko PLoS One Research Article PURPOSE: Psychosis is one of the most important psychiatric comorbidities in temporal lobe epilepsy (TLE), and its pathophysiology still remains unsolved. We aimed to explore the connectivity differences of structural neuroimaging between TLE with and without psychosis using a graph theoretical analysis, which is an emerging mathematical method to investigate network connections in the brain as a small-world system. MATERIALS AND METHODS: We recruited 11 TLE patients with unilateral hippocampal sclerosis (HS) presenting psychosis or having a history of psychosis (TLE-P group). As controls, 15 TLE patients with unilateral HS without any history of psychotic episodes were also recruited (TLE-N group). For graph theoretical analysis, the normalized gray matter images of both groups were subjected to Graph Analysis Toolbox (GAT). As secondary analyses, each group was compared to 14 age- and gender-matched healthy subjects. RESULTS: The hub node locations were found predominantly in the ipsilateral hemisphere in the TLE-N group, and mainly on the contralateral side in the TLE-P group. The TLE-P group showed significantly higher characteristic path length, transitivity, lower global efficiency, and resilience to random or targeted attack than those of the TLE-N group. The regional comparison in betweenness centrality revealed significantly decreased connectivity in the contralateral temporal lobe, ipsilateral middle frontal gyrus, and bilateral postcentral gyri in the TLE-P group. The healthy subjects showed well-balanced nodes/edges distributions, similar metrics to TLE-N group except for higher small-worldness/modularity/assortativity, and various differences of regional betweenness/clustering. CONCLUSION: In TLE with psychosis, graph theoretical analysis of structural imaging revealed disrupted connectivity in the contralateral hemisphere. The network metrics suggested that the existence of psychosis can bring vulnerability and decreased efficiency of the whole-brain network. The sharp differences in structural networks between morphologically homogeneous groups are remarkable and may contribute to a better understanding of psychosis in TLE. Public Library of Science 2016-07-06 /pmc/articles/PMC4934878/ /pubmed/27385130 http://dx.doi.org/10.1371/journal.pone.0158728 Text en © 2016 Sone et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Sone, Daichi
Matsuda, Hiroshi
Ota, Miho
Maikusa, Norihide
Kimura, Yukio
Sumida, Kaoru
Yokoyama, Kota
Imabayashi, Etsuko
Watanabe, Masako
Watanabe, Yutaka
Okazaki, Mitsutoshi
Sato, Noriko
Graph Theoretical Analysis of Structural Neuroimaging in Temporal Lobe Epilepsy with and without Psychosis
title Graph Theoretical Analysis of Structural Neuroimaging in Temporal Lobe Epilepsy with and without Psychosis
title_full Graph Theoretical Analysis of Structural Neuroimaging in Temporal Lobe Epilepsy with and without Psychosis
title_fullStr Graph Theoretical Analysis of Structural Neuroimaging in Temporal Lobe Epilepsy with and without Psychosis
title_full_unstemmed Graph Theoretical Analysis of Structural Neuroimaging in Temporal Lobe Epilepsy with and without Psychosis
title_short Graph Theoretical Analysis of Structural Neuroimaging in Temporal Lobe Epilepsy with and without Psychosis
title_sort graph theoretical analysis of structural neuroimaging in temporal lobe epilepsy with and without psychosis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4934878/
https://www.ncbi.nlm.nih.gov/pubmed/27385130
http://dx.doi.org/10.1371/journal.pone.0158728
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