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

被引:25
作者
Sone, Daichi [1 ,2 ]
Matsuda, Hiroshi [3 ]
Ota, Miho [4 ]
Maikusa, Norihide [3 ]
Kimura, Yukio [1 ]
Sumida, Kaoru [1 ]
Yokoyama, Kota [1 ]
Imabayashi, Etsuko [3 ]
Watanabe, Masako [5 ]
Watanabe, Yutaka [5 ]
Okazaki, Mitsutoshi [5 ]
Sato, Noriko [1 ]
机构
[1] Natl Ctr Neurol & Psychiat, Dept Radiol, Tokyo, Japan
[2] Univ Tokyo, Grad Sch Med, Dept Neuropsychiat, Tokyo, Japan
[3] Natl Ctr Neurol & Psychiat, Integrat Brain Imaging Ctr, Tokyo, Japan
[4] Natl Ctr Neurol & Psychiat, Natl Inst Neurosci, Dept Mental Disorder Res, Tokyo, Japan
[5] Natl Ctr Neurol & Psychiat, Dept Psychiat, Tokyo, Japan
基金
日本学术振兴会;
关键词
POSTICTAL PSYCHOSIS; BRAIN NETWORKS; FUNCTIONAL CONNECTIVITY; CORTICAL THICKNESS; SMALL-WORLD; SCHIZOPHRENIA; ORGANIZATION; ABNORMALITIES; MRI;
D O I
10.1371/journal.pone.0158728
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
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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页数:15
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共 36 条
[1]   Imaging structural co-variance between human brain regions [J].
Alexander-Bloch, Aaron ;
Giedd, Jay N. ;
Bullmore, Edward T. .
NATURE REVIEWS NEUROSCIENCE, 2013, 14 (05) :322-336
[2]  
APA, 1994, DSM 4 DIAGN STAT MAN
[3]   A fast diffeomorphic image registration algorithm [J].
Ashburner, John .
NEUROIMAGE, 2007, 38 (01) :95-113
[4]   Hierarchical organization of human cortical networks in health and schizophrenia [J].
Bassett, Danielle S. ;
Bullmore, Edward T. ;
Verchinski, Beth A. ;
Mattay, Venkata S. ;
Weinberger, Daniel R. ;
Meyer-Lindenberg, Andreas .
JOURNAL OF NEUROSCIENCE, 2008, 28 (37) :9239-9248
[5]   Revised terminology and concepts for organization of seizures and epilepsies: Report of the ILAE Commission on Classification and Terminology, 2005-2009 [J].
Berg, Anne T. ;
Berkovic, Samuel F. ;
Brodie, Martin J. ;
Buchhalter, Jeffrey ;
Cross, J. Helen ;
Boas, Walter van Emde ;
Engel, Jerome ;
French, Jacqueline ;
Glauser, Tracy A. ;
Mathern, Gary W. ;
Moshe, Solomon L. ;
Nordli, Douglas ;
Plouin, Perrine ;
Scheffer, Ingrid E. .
EPILEPSIA, 2010, 51 (04) :676-685
[6]   Mapping limbic network organization in temporal lobe epilepsy using morphometric correlations: Insights on the relation between mesiotemporal connectivity and cortical atrophy [J].
Bernhardt, Boris C. ;
Worsley, Keith J. ;
Besson, Pierre ;
Concha, Luis ;
Lerch, Jason P. ;
Evans, Alan C. ;
Bernasconi, Neda .
NEUROIMAGE, 2008, 42 (02) :515-524
[7]   Network analysis for a network disorder: The emerging role of graph theory in the study of epilepsy [J].
Bernhardt, Boris C. ;
Bonilha, Leonardo ;
Gross, Donald W. .
EPILEPSY & BEHAVIOR, 2015, 50 :162-170
[8]   Graph-Theoretical Analysis Reveals Disrupted Small-World Organization of Cortical Thickness Correlation Networks in Temporal Lobe Epilepsy [J].
Bernhardt, Boris C. ;
Chen, Zhang ;
He, Yong ;
Evans, Alan C. ;
Bernasconi, Neda .
CEREBRAL CORTEX, 2011, 21 (09) :2147-2157
[9]   Decreased Basal fMRI Functional Connectivity in Epileptogenic Networks and Contralateral Compensatory Mechanisms [J].
Bettus, Gaelle ;
Guedj, Eric ;
Joyeux, Florian ;
Confort-Gouny, Sylviane ;
Soulier, Elisabeth ;
Laguitton, Virginie ;
Cozzone, Patrick J. ;
Chauvel, Patrick ;
Ranjeva, Jean-Philippe ;
Bartolomei, Fabrice ;
Guye, Maxime .
HUMAN BRAIN MAPPING, 2009, 30 (05) :1580-1591
[10]   Medial temporal lobe epilepsy is associated with neuronal fibre loss and paradoxical increase in structural connectivity of limbic structures [J].
Bonilha, Leonardo ;
Nesland, Travis ;
Martz, Gabriel U. ;
Joseph, Jane E. ;
Spampinato, Maria V. ;
Edwards, Jonathan C. ;
Tabesh, Ali .
JOURNAL OF NEUROLOGY NEUROSURGERY AND PSYCHIATRY, 2012, 83 (09) :903-909