The impact of temporal lobe epilepsy surgery on picture naming and its relationship to network metric change.

Peter Binding, Lawrence; Neal Taylor, Peter; O'Keeffe, Aidan G.; Giampiccolo, Davide; Fleury, Marine; Xiao, Fenglai; Caciagli, Lorenzo; de Tisi, Jane; Winston, Gavin P.; Miserocchi, Anna; McEvoy, Andrew; Duncan, John S.; Vos, Sjoerd B.

Abstract

Background: Anterior temporal lobe resection (ATLR) is a successful treatment for medically-refractory temporal lobe epilepsy (TLE). In the language-dominant hemisphere, 30%- 50% of individuals experience a naming decline which can impact upon daily life. Measures of structural networks are associated with language performance pre-operatively. It is unclear if analysis of network measures may predict post-operative decline. Methods: White matter fibre tractography was performed on preoperative diffusion MRI of 44 left lateralised and left resection individuals with TLE to reconstruct the preoperative structural network. Resection masks, drawn on co-registered pre- and post-operative T1-weighted MRI scans, were used as exclusion regions on pre-operative tractography to estimate the post-operative network. Changes in graph theory metrics, cortical strength, betweenness centrality, and clustering coefficient were generated by comparing the estimated pre- and post-operative networks. These were thresholded based on the presence of the connection in each patient, ranging from 75% to 100% in steps of 5%. The average graph theory metric across thresholds was taken. We incorporated leave-one-out cross-validation with smoothly clipped absolute deviation (SCAD) least absolute shrinkage and selection operator (LASSO) feature selection and a support vector classifier to assess graph theory metrics on picture naming decline. Picture naming was assessed via the Graded Naming Test preoperatively and at 3 and 12 months post-operatively and the outcome was classified using the reliable change index (RCI) to identify clinically significant decline. The best feature combination and model was selected using the area under the curve (AUC). The sensitivity, specificity and F1-score were also reported. Permutation testing was performed to assess the machine learning model and selected regions difference significance. Results: A combination of clinical and graph theory metrics were able to classify outcome of picture naming at 3 months with an AUC of 0.84. At 12 months, change in strength to cortical regions was best able to correctly classify outcome with an AUC of 0.86. Longitudinal analysis revealed that betweenness centrality was the best metric to identify patients who declined at 3 months, who will then continue to experience decline from 3 to 12 months. Both models were significantly higher AUC values than a random classifier. Conclusion: Our results suggest that inferred changes of network integrity were able to correctly classify picture naming decline after ATLR. These measures may be used to prospectively to identify patients who are at risk of picture naming decline after surgery and could potentially be utilised to assist tailoring the resection in order to prevent this decline.

Citation

Peter Binding, L., Neal Taylor, P., O'Keeffe, A. G., Giampiccolo, D., Fleury, M., Xiao, F., Caciagli, L., de Tisi, J., Winston, G. P., Miserocchi, A., McEvoy, A., Duncan, J. S., & Vos, S. B. (2023). The impact of temporal lobe epilepsy surgery on picture naming and its relationship to network metric change. NeuroImage: Clinical, 38, Article 103444. https://doi.org/10.1016/j.nicl.2023.103444

• Journal Article Type: Article
• Acceptance Date: May 22, 2023
• Online Publication Date: May 27, 2023
• Publication Date: 2023
• Deposit Date: Jun 1, 2023
• Publicly Available Date: Jun 1, 2023
• Journal: NeuroImage: Clinical
• Electronic ISSN: 2213-1582
• Publisher: Elsevier
• Peer Reviewed: Peer Reviewed
• Volume: 38
• Article Number: 103444
• DOI: https://doi.org/10.1016/j.nicl.2023.103444
• Keywords: White Matter; Anterior Temporal Lobe Resection; Picture Naming Decline; Graph Theory; Machine Learning
• Public URL: https://nottingham-repository.worktribe.com/output/21371910
• Publisher URL: https://www.sciencedirect.com/science/article/pii/S221315822300133X?via%3Dihub