Abstract
Purpose
An accurate and reliable brain atlas, as the role of navigation, should be effective and vital to differentiate the patients with temporal lobe epilepsy (TLE) from normal controls (NCs). The purpose of this study is to compare the classification performance of identifying TLE patients based on different atlases, which were Desikan-killiany (DK) atlas, Destrieux (DS) atlas and Brainnetome (BN) atlas.
Methods
Twenty-three patients with TLE and thirty NCs were recruited for our study. Seven morphological features of ROIs were calculated firstly. Then individual morphological brain network were constructed. After that, least absolute shrinkage and selection operator (LASSO) algorithm was used in feature selection. Finally, classification with support vector machine (SVM) and leave-one-out cross-validation (LOOCV) were employed for the training and evaluation of the classifiers.
Results
The performance of the experiments using BN atlas was better than DK atlas and DS atlas. LASSO algorithm used for feature selection can improve the classification performance. The SVM analysis using BN atlas revealed best classification with accuracy of 92.45% and 90.57% respectively based on network properties and morphological features.
Conclusion
This study suggested that the choice of atlases is important in the computer-aided classification of TLE.
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References
Engel, J., Jr. (2001). Mesial temporal lobe epilepsy: What have we learned? The Neuroscientist, 7(4), 340–352. https://doi.org/10.1177/107385840100700410
Riley, J. D., Franklin, D. L., Choi, V., et al. (2010). Altered white matter integrity in temporal lobe epilepsy: Association with cognitive and clinical profiles. Epilepsia, 51(4), 536–545. https://doi.org/10.1111/j.1528-1167.2009.02508.x
Oyegbile, T. O., Dow, C., Jones, J., et al. (2004). The nature and course of neuropsychological morbidity in chronic temporal lobe epilepsy. Neurology, 62(10), 1736–1742. https://doi.org/10.1212/01.wnl.0000125186.04867.34
Bell, B., Lin, J. J., Seidenberg, M., & Hermann, B. (2011). The neurobiology of cognitive disorders in temporal lobe epilepsy. Nature Reviews. Neurology, 7(3), 154–164. https://doi.org/10.1038/nrneurol.2011.3
Gleichgerrcht, E., Munsell, B. C., Alhusaini, S., et al. (2021). Artificial intelligence for classification of temporal lobe epilepsy with ROI-level MRI data: A worldwide ENIGMA-Epilepsy study. Neuroimage Clinical, 31, 102765. https://doi.org/10.1016/j.nicl.2021.102765
Eickhoff, S. B., Yeo, B. T. T., & Genon, S. (2018). Imaging-based parcellations of the human brain. Nature Reviews Neuroscience, 19(11), 672–686. https://doi.org/10.1038/s41583-018-0071-7
Desikan, R. S., Ségonne, F., Fischl, B., et al. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage, 31(3), 968–980. https://doi.org/10.1016/j.neuroimage.2006.01.021
Destrieux, C., Fischl, B., Dale, A., & Halgren, E. (2010). Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. NeuroImage, 53(1), 1–15. https://doi.org/10.1016/j.neuroimage.2010.06.010
Fischl, B. (2012). FreeSurfer. NeuroImage, 62(2), 774–781. https://doi.org/10.1016/j.neuroimage.2012.01.021
Chaudhary, S., Kumaran, S. S., Goyal, V., et al. (2021). Cortical thickness and gyrification index measuring cognition in Parkinson’s disease. International Journal of Neuroscience, 131(10), 984–993. https://doi.org/10.1080/00207454.2020.1766459
Jirsaraie, R. J., Sheffield, J. M., & Barch, D. M. (2018). Neural correlates of global and specific cognitive deficits in schizophrenia. Schizophrenia Research, 201, 237–242. https://doi.org/10.1016/j.schres.2018.06.017
Fan, L., Li, H., Zhuo, J., et al. (2016). The human Brainnetome atlas: A new brain atlas based on connectional architecture. Cerebral Cortex, 26(8), 3508–3526. https://doi.org/10.1093/cercor/bhw157
Chen, Y. L., Zhao, X. A., Ng, S. H., et al. (2019). Prediction of the clinical severity of progressive supranuclear palsy by diffusion tensor imaging. Journal of Clinical Medicine, 9(1), 40. https://doi.org/10.3390/jcm9010040
Long, Z., Jing, B., Guo, R., et al. (2018). A Brainnetome atlas based mild cognitive impairment identification using Hurst exponent. Front Aging Neuroscience, 10, 103. https://doi.org/10.3389/fnagi.2018.00103
Shi, W., Fan, L., & Jiang, T. (2021). Developing neuroimaging biomarker for brain diseases with a machine learning framework and the Brainnetome atlas. Neuroscience Bulletin, 37(10), 1523–1525. https://doi.org/10.1007/s12264-021-00722-8
Lai, C., Guo, S., Cheng, L., et al. (2017). Evaluation of feature selection algorithms for classification in temporal lobe epilepsy based on MR images. In Eighth international conference on graphic and image processing. International Society for Optics and Photonics.
Rudie, J. D., Colby, J. B., & Salamon, N. (2015). Machine learning classification of mesial temporal sclerosis in epilepsy patients. Epilepsy Research, 117, 63–69. https://doi.org/10.1016/j.eplepsyres.2015.09.005
Alhusaini, S., Doherty, C. P., Palaniyappan, L., et al. (2012). Asymmetric cortical surface area and morphology changes in mesial temporal lobe epilepsy with hippocampal sclerosis. Epilepsia, 53(6), 995–1003. https://doi.org/10.1111/j.1528-1167.2012.03457.x
Ronan, L., Alhusaini, S., Scanlon, C., Doherty, C. P., Delanty, N., & Fitzsimons, M. (2012). Widespread cortical morphologic changes in juvenile myoclonic epilepsy: Evidence from structural MRI. Epilepsia, 53(4), 651–658. https://doi.org/10.1111/j.1528-1167.2012.03413.x
Ristić, A. J., Daković, M., Kerr, M., Kovačević, M., Parojčić, A., & Sokić, D. (2015). Cortical thickness, surface area and folding in patients with psychogenic nonepileptic seizures. Epilepsy Research, 112, 84–91. https://doi.org/10.1016/j.eplepsyres.2015.02.015
Santana, M. T., Jackowski, A. P., Britto Fdos, S., et al. (2014). Gender and hemispheric differences in temporal lobe epilepsy: A VBM study. Seizure, 23(4), 274–279. https://doi.org/10.1016/j.seizure.2013.12.006
Schnack, H. G., van Haren, N. E., Brouwer, R. M., et al. (2015). Changes in thickness and surface area of the human cortex and their relationship with intelligence. Cerebral Cortex, 25(6), 1608–1617. https://doi.org/10.1093/cercor/bht357
Li, W., Yang, C., Shi, F., et al. (2017). Construction of individual morphological brain networks with multiple morphometric features. Frontiers in Neuroanatomy, 11, 34. https://doi.org/10.3389/fnana.2017.00034
Wang, X. H., Jiao, Y., & Li, L. (2018). Diagnostic model for attention-deficit hyperactivity disorder based on interregional morphological connectivity. Neuroscience Letters, 685, 30–34. https://doi.org/10.1016/j.neulet.2018.07.029
Homan, P., Argyelan, M., DeRosse, P., et al. (2019). Structural similarity networks predict clinical outcome in early-phase psychosis. Neuropsychopharmacology, 44(5), 915–922. https://doi.org/10.1038/s41386-019-0322-y
Sepehrband, F., Lynch, K. M., Cabeen, R. P., et al. (2018). Neuroanatomical morphometric characterization of sex differences in youth using statistical learning. NeuroImage, 172, 217–227. https://doi.org/10.1016/j.neuroimage.2018.01.065
Ota, K., Oishi, N., Ito, K., Fukuyama, H., SEAD-J Study Group. (2014). A comparison of three brain atlases for MCI prediction. Journal of Neuroscience Methods, 221, 139–150. https://doi.org/10.1016/j.jneumeth.2013.10.003
Long, Z., Huang, J., Li, B., et al. (2018). A Comparative atlas-based recognition of mild cognitive impairment with voxel-based morphometry. Frontiers in Neuroscience, 12, 916. https://doi.org/10.3389/fnins.2018.00916
Fischl, B., Sereno, M. I., & Dale, A. M. (1999). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. NeuroImage, 9(2), 195–207. https://doi.org/10.1006/nimg.1998.0396
Dale, A. M., Fischl, B., & Sereno, M. I. (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage, 9(2), 179–194. https://doi.org/10.1006/nimg.1998.0395
Fischl, B., Liu, A., & Dale, A. M. (2001). Automated manifold surgery: Constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Transactions on Medical Imaging, 20(1), 70–80. https://doi.org/10.1109/42.906426
Fischl, B., van der Kouwe, A., Destrieux, C., et al. (2004). Automatically parcellating the human cerebral cortex. Cerebral Cortex, 14(1), 11–22. https://doi.org/10.1093/cercor/bhg087
Wang, J., Wang, X., Xia, M., Liao, X., Evans, A., & He, Y. (2015). GRETNA: A graph theoretical network analysis toolbox for imaging connectomics. Frontiers in Human Neuroscience, 9, 386. https://doi.org/10.3389/fnhum.2015.00386
Wang, H., Jin, X., Zhang, Y., & Wang, J. (2016). Single-subject morphological brain networks: Connectivity mapping, topological characterization and test-retest reliability. Brain and Behavior: A Cognitive Neuroscience Perspective, 6(4), e00448. https://doi.org/10.1002/brb3.448
Xin, W., Yanshuang, R., & Wensheng, Z. (2017). Classification of temporal lobe epilepsy with and without hippocampal sclerosis via two-level feature selection. DEStech Transactions on Computer Science and Engineering. https://doi.org/10.12783/dtcse/cst2017/12546
Tibshirani, R. J. (1996). Regression Shrinkage and selection via the LASSO. Journal of the Royal Statistical Society. Series B: Methodological, 73(1), 273–282. https://doi.org/10.1111/j.2517-6161.1996.tb02080.x
Tibshirani, R. (2011). Regression shrinkage and selection via the lasso: A retrospective. Journal of the Royal Statistical Society: Series B (Statistical Methodology)., 73(3), 267–288. https://doi.org/10.1111/j.1467-9868.2011.00771.x
Cortes, C., & Vapnik, V. (1995). Support-vector networks. Machine Learning, 20(3), 273–297. https://doi.org/10.1023/A:1022627411411
Kamiya, K., Amemiya, S., Suzuki, Y., et al. (2016). Machine learning of DTI structural brain connectomes for lateralization of temporal lobe epilepsy. Magnetic Resonance in Medical Sciences, 15(1), 121–129. https://doi.org/10.2463/mrms.2015-0027
Ting, W., Duo, C., Qiqi, C., et al. (2018). Automatic lateralization of temporal lobe epilepsy based on MEG network features using support vector machines. Complexity, 2018, 1–10. https://doi.org/10.1155/2018/4325096
Wong, T.-T. (2015). Performance evaluation of classification algorithms by k-fold and leave-one-out cross validation. Pattern Recognition, 48(9), 2839–2846. https://doi.org/10.1016/j.patcog.2015.03.009
Li, S., Yuan, X., Pu, F., et al. (2014). Abnormal changes of multidimensional surface features using multivariate pattern classification in amnestic mild cognitive impairment patients. Journal of Neuroscience, 34(32), 10541–10553. https://doi.org/10.1523/JNEUROSCI.4356-13.2014
Bernhardt, B. C., Bonilha, L., & Gross, D. W. (2015). Network analysis for a network disorder: The emerging role of graph theory in the study of epilepsy. Epilepsy & Behavior, 50, 162–170. https://doi.org/10.1016/j.yebeh.2015.06.005
Gleichgerrcht, E., Kocher, M., & Bonilha, L. (2015). Connectomics and graph theory analyses: Novel insights into network abnormalities in epilepsy. Epilepsia, 56(11), 1660–1668. https://doi.org/10.1111/epi.13133
Vaughan, D. N., Rayner, G., Tailby, C., & Jackson, G. D. (2016). MRI-negative temporal lobe epilepsy: A network disorder of neocortical connectivity. Neurology, 87(18), 1934–1942. https://doi.org/10.1212/WNL.0000000000003289
Li, W., Yang, C., Wu, S., et al. (2018). Alterations of graphic properties and related cognitive functioning changes in mild Alzheimer’s disease revealed by individual morphological brain network. Frontiers in Neuroscience, 12, 927. https://doi.org/10.3389/fnins.2018.00927
King, D. J., & Wood, A. G. (2020). Clinically feasible brain morphometric similarity network construction approaches with restricted magnetic resonance imaging acquisitions. Network Neuroscience, 4(1), 274–291. https://doi.org/10.1162/netn_a_00123
Arslan, S., Ktena, S. I., Makropoulos, A., Robinson, E. C., Rueckert, D., & Parisot, S. (2018). Human brain mapping: A systematic comparison of parcellation methods for the human cerebral cortex. NeuroImage, 170, 5–30. https://doi.org/10.1016/j.neuroimage.2017.04.014
Acknowledgements
This study was supported by project Grants from Beijing Nova Program (xx2016120), National Natural Science Foundation of China (81101107, 31640035, 81601126), Natural Science Foundation of Beijing (4162008) and program for Scientific Research Project of Beijing Educational Committee (SQKM201710005013). We are thankful for the support from Intelligent Physiological Measurement and Clinical Translation and Beijing International Base for Scientific and Technological Cooperation.
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Zhang, W., Yang, C., Li, Z. et al. A Comparison of Three Brain Atlases for Temporal Lobe Epilepsy Prediction. J. Med. Biol. Eng. 42, 11–20 (2022). https://doi.org/10.1007/s40846-021-00676-2
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DOI: https://doi.org/10.1007/s40846-021-00676-2