Association of lack of speech arrest during cortical stimulation with interhemispheric reorganization of the functional language network in patients with brain tumors Journal Article


Authors: Pasquini, L.; Tao, A.; Del Ferraro, G.; Jenabi, M.; Peck, K. K.; Napolitano, A.; Fahy, T. A.; Brennan, C.; Moss, N. S.; Tabar, V.; Makse, H.; Holodny, A. I.
Article Title: Association of lack of speech arrest during cortical stimulation with interhemispheric reorganization of the functional language network in patients with brain tumors
Abstract: BACKGROUND. Brain tumors induce language reorganization, which may influence the 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) without SA 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 (i.e., language core) on fMRI using optimal percolation. Language core connectivity in the left and right hemispheres was quantified as fMRI laterality index (LI) and connectivity LI on the basis of fMRI activation maps and connectivity matrices. We compared fMRI LI and connectivity LI between patients with SA and without SA and used multivariable logistic regression (p < .05) to assess associations between DCS and connectivity LI, fMRI LI, tumor location, Broca area and Wernicke area 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 without SA lateralized more to the right hemisphere (p < .001). Between patients with SA and those without, fMRI LI was not significantly different. Patients without SA showed right-greater-than-left connectivity of Broca area and premotor area compared with patients with SA. Regression analysis showed significant association between no SA and right-lateralized connectivity LI (p < .001) and fewer speech deficits before (p < .001) and 1 week after (p = .02) surgery. CONCLUSION. Patients without SA had increased right-hemispheric connections and right translocation of the language core, suggesting language reorganization. Lack of interoperative SA 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. © American Roentgen Ray Society.
Keywords: retrospective studies; nuclear magnetic resonance imaging; brain tumor; glioma; brain neoplasms; magnetic resonance imaging; pathology; diagnostic imaging; retrospective study; physiology; infant, newborn; newborn; fmri; language; brain mapping; speech; wakefulness; procedures; humans; human; reorganization; cortical stimulation
Journal Title: American Journal of Roentgenology
Volume: 221
Issue: 6
ISSN: 0361-803X
Publisher: American Roentgen Ray Society  
Date Published: 2023-12-01
Start Page: 806
End Page: 816
Language: English
DOI: 10.2214/ajr.23.29434
PUBMED: 37377358
PROVIDER: scopus
PMCID: PMC12001089
DOI/URL:
Notes: The MSK Cancer Center Support Grant (P30 CA008748) is acknowledged in the PDF -- Corresponding author is MSK author: Luca Pasquini -- Source: Scopus
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MSK Authors
  1. Viviane S Tabar
    225 Tabar
  2. Cameron Brennan
    226 Brennan
  3. Kyung Peck
    117 Peck
  4. Andrei Holodny
    207 Holodny
  5. Mehrnaz Jenabi
    26 Jenabi
  6. Nelson Moss
    88 Moss
  7. Alice Junling Tao
    3 Tao
  8. Tara Annmarie Fahy
    4 Fahy