Association of Lack of Speech Arrest During Cortical Stimulation With Interhemispheric Reorganization of the Functional Language Network in Patients With Brain Tumors.

Overview

abstract

Background: Brain tumors induce language reorganization, which may influence extent of resection in surgical planning. Direct cortical stimulation (DCS) allows definitive language mapping during awake surgery by locating areas of speech arrest (SA) surrounding the tumor. Although functional MRI (fMRI) combined with graph theory analysis can illustrate whole-brain network reorganization, few studies have corroborated these findings with DCS intraoperative mapping and clinical language performance. Objective: We evaluated whether patients with low-grade gliomas (LGGs) with no speech arrest (NSA) during DCS show increased right-hemispheric connections and better speech performance compared with patients with SA. Methods: We retrospectively recruited 44 consecutive patients with left perisylvian LGG, preoperative language task-based fMRI, speech performance evaluation, and awake surgery with DCS. We generated language networks from ROIs corresponding to known language areas (language core) on fMRI using optimal percolation. Language core connectivity in the left and right hemispheres was quantified as fMRI laterality index (fLI) and connectivity laterality index (cLI) on the basis of fMRI activation maps and connectivity matrixes. We compared fLI and cLI between patients with SA and NSA and used multinomial logistic regression (p < .05) to assess associations between DCS and cLI, fLI, tumor location, Broca area (BA) and Wernicke area (WA) involvement, prior treatments, age, handedness, sex, tumor size, and speech deficit before surgery, within 1 week after surgery, and 3-6 months after surgery. Results: Patients with SA showed left-dominant connectivity; patients with NSA lateralized more to the right hemisphere (p < .001). Between patients with SA and those with NSA, fLI was not significantly different. Patients with NSA showed right-greater-than-left connectivity of BA and premotor area compared with SA. Regression analysis showed significant association between NSA and right-lateralized LI (p < .001), fewer presurgical speech deficits (p < .001), and time within 1 week after surgery (p = .02). Conclusion: Patients with NSA had increased right-hemispheric connections and right translocation of the language core, suggesting language reorganization. Intraoperative NSA was associated with fewer speech deficits both before and immediately after surgery. Clinical Impact: These findings support tumor-induced language plasticity as a compensatory mechanism, which may lead to fewer postsurgical deficits and allow extended resection.