ESM-AnatTractNet: Advanced deep learning model of true positive eloquent white matter tractography to improve preoperative evaluation of pediatric epilepsy surgery

Accurate preoperative identification of true positive white matter pathways involved in critical eloquent functions such as motor, language, and vision plays a vital role in minimizing the risk of postoperative functional deficits and improving postoperative functional outcomes in pediatric epilepsy surgery. This study proposes a novel deep learning model: "ESM-AnatTractNet" that can accurately classify true positive eloquent white matter pathways across preoperative diffusion weighted imaging tractography data of 85 drug-resistant epilepsy patients (age: 10.70 ± 4.41 years). To enhance geometric and anatomical consistency of true positive tract classification, the ESM-AnatTractNet integrated two features in a point-cloud-based framework, 1) electro-physiologically confirmed spatial coordinates using electrical stimulation mapping (ESM) and 2) anatomically-contexted labels of the end-to-end neural connection using a standard brain atlas. Its overall performance was validated by accurately classifying 14 eloquent functional areas in whole brain, objectively optimizing resection margins to preserve eloquent functions using Kalman filter, and precisely predicting postoperative language outcomes using canonical correlation. Our ESM-AnatTractNet outperformed other baseline models, achieving an accuracy of 97% in correctly classifying eloquent areas within 10mm spatial resolution of clinical subdural grid electroencephalography. The Kalman filter analysis achieved 94% accuracy in predicting no deficits when the ESM-AnatTractNet-defined preservation zones were not resected. Postoperative decrease in language-related white matter connection efficacy defined by the ESM-AnatTractNet analysis was significantly associated with worse postoperative language outcome (R=0.73, p < 0.001). Our findings demonstrate that the ESM-AnatTractNet improves non-invasive localization of true positive eloquent white matter pathways, supporting its potential to enhance current preoperative evaluation of pediatric epilepsy surgery.