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Sex Effect on Presurgical Language Mapping in Patients With a Brain Tumor.

ABSTRACT: Differences between males and females in brain development and in the organization and hemispheric lateralization of brain functions have been described, including in language. Sex differences in language organization may have important implications for language mapping performed to assess, and minimize neurosurgical risk to, language function. This study examined the effect of sex on the activation and functional connectivity of the brain, measured with presurgical functional magnetic resonance imaging (fMRI) language mapping in patients with a brain tumor. We carried out a retrospective analysis of data from neurosurgical patients treated at our institution who met the criteria of pathological diagnosis (malignant brain tumor), tumor location (left hemisphere), and fMRI paradigms [sentence completion (SC); antonym generation (AG); and resting-state fMRI (rs-fMRI)]. Forty-seven patients (22 females, mean age = 56.0 years) were included in the study. Across the SC and AG tasks, females relative to males showed greater activation in limited areas, including the left inferior frontal gyrus classically associated with language. In contrast, males relative to females showed greater activation in extended areas beyond the classic language network, including the supplementary motor area (SMA) and precentral gyrus. The rs-fMRI functional connectivity of the left SMA in the females was stronger with inferior temporal pole (TP) areas, and in the males with several midline areas. The findings are overall consistent with theories of greater reliance on specialized language areas in females relative to males, and generalized brain areas in males relative to females, for language function. Importantly, the findings suggest that sex could affect fMRI language mapping. Thus, considering sex as a variable in presurgical language mapping merits further investigation.

SUBMITTER: Yao S

PROVIDER: S-EPMC6992642 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Sex Effect on Presurgical Language Mapping in Patients With a Brain Tumor.

Yao Shun S Liebenthal Einat E Juvekar Parikshit P Bunevicius Adomas A Vera Matthew M Rigolo Laura L Golby Alexandra J AJ Tie Yanmei Y

Frontiers in neuroscience 20200124

Differences between males and females in brain development and in the organization and hemispheric lateralization of brain functions have been described, including in language. Sex differences in language organization may have important implications for language mapping performed to assess, and minimize neurosurgical risk to, language function. This study examined the effect of sex on the activation and functional connectivity of the brain, measured with presurgical functional magnetic resonance ...[more]

PMID: 32038154

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Project description:ObjectivesLanguage reorganization may follow tumor invasion of the dominant hemisphere. Tumor location, grade, and genetics influence the communication between eloquent areas and tumor growth dynamics, which are drivers of language plasticity. We evaluated tumor-induced language reorganization studying the relationship of fMRI language laterality to tumor-related variables (grade, genetics, location), and patient-related variables (age, sex, handedness).MethodsThe study was retrospective cross-sectional. We included patients with left-hemispheric tumors (study group) and right-hemispheric tumors (controls). We calculated five fMRI laterality indexes (LI): hemispheric, temporal lobe, frontal lobe, Broca's area (BA), Wernicke's area (WA). We defined LI ≥ 0.2 as left-lateralized (LL) and LI < 0.2 as atypical lateralized (AL). Chi-square test (p < 0.05) was employed to identify the relationship between LI and tumor/patient variables in the study group. For those variables having significant results, confounding factors were evaluated in a multinomial logistic regression model.ResultsWe included 405 patients (235 M, mean age: 51 years old) and 49 controls (36 M, mean age: 51 years old). Contralateral language reorganization was more common in patients than controls. The statistical analysis demonstrated significant association between BA LI and patient sex (p = 0.005); frontal LI, BA LI, and tumor location in BA (p < 0.001); hemispheric LI and fibroblast growth factor receptor (FGFR) mutation (p = 0.019); WA LI and O6-methylguanine-DNA methyltransferase promoter (MGMT) methylation in high-grade gliomas (p = 0.016).ConclusionsTumor genetics, pathology, and location influence language laterality, possibly due to cortical plasticity. Increased fMRI activation in the right hemisphere was seen in patients with tumors in the frontal lobe, BA and WA, FGFR mutation, and MGMT promoter methylation.Key points• Patients harboring left-hemispheric tumors present with contralateral translocation of language function. Influential variables for this phenomenon included frontal tumor location, BA location, WA location, sex, MGMT promoter methylation, and FGFR mutation. • Tumor location, grade, and genetics may influence language plasticity, thereby affecting both communication between eloquent areas and tumor growth dynamics. • In this retrospective cross-sectional study, we evaluated language reorganization in 405 brain tumor patients by studying the relationship of fMRI language laterality to tumor-related variables (grade, genetics, location), and patient-related variables (age, sex, handedness).

Project description:Repetitive TMS (rTMS) allows for non-invasive and transient disruption of local neuronal functioning. We used machine learning approaches to assess whether brain tumor patients can be accurately classified into aphasic and non-aphasic groups using their rTMS language mapping results as input features. Given that each tumor affects the subject-specific language networks differently, resulting in heterogenous rTMS functional mappings, we propose the use of machine learning strategies to classify potential patterns of rTMS language mapping results. We retrospectively included 90 patients with left perisylvian world health organization (WHO) grade II-IV gliomas that underwent presurgical navigated rTMS language mapping. Within our cohort, 29 of 90 (32.2%) patients suffered from at least mild aphasia as shown in the Aachen Aphasia Test based Berlin Aphasia Score (BAS). After spatial normalization to MNI 152 of all rTMS spots, we calculated the error rate (ER) in each stimulated cortical area (28 regions of interest, ROI) by automated anatomical labeling parcellation (AAL3) and IIT. We used a support vector machine (SVM) to classify significant areas in relation to aphasia. After feeding the ROIs into the SVM model, it revealed that in addition to age (w = 2.98), the ERs of the left supramarginal gyrus (w = 3.64), left inferior parietal gyrus (w = 2.28) and right pars triangularis (w = 1.34) contributed more than other features to the model. The model's sensitivity was 86.2%, the specificity was 82.0%, the overall accuracy was 85.5% and the AUC was 89.3%. Our results demonstrate an increased vulnerability of right inferior pars triangularis to rTMS in aphasic patients due to left perisylvian gliomas. This finding points towards a functional relevant involvement of the right pars triangularis in response to aphasia. The tumor location feature, specified by calculating overlaps with white and grey matter atlases, did not affect the SVM model. The left supramarginal gyrus as a feature improved our SVM model the most. Additionally, our results could point towards a decreasing potential for neuroplasticity with age.

Project description:Task-based functional MRI (tb-fMRI) represents an extremely valuable approach for the identification of language eloquent regions for presurgical mapping in patients with brain tumors. However, its routinely application is limited by patient-related factors, such as cognitive disability and difficulty in coping with long-time acquisitions, and by technical factors, such as lack of equipment availability for stimuli delivery. Resting-state fMRI (rs-fMRI) instead, allows the identification of distinct language networks in a 10-min acquisition without the need of performing active tasks and using specific equipment. Therefore, to test the feasibility of rs-fMRI as a preoperative mapping tool, we reconstructed a lexico-semantic intrinsic connectivity network (ICN) in healthy controls (HC) and in a case series of patients with gliomas and compared the organization of this language network with the one derived from tb-fMRI in the patient's group. We studied three patients with extra-frontal gliomas who underwent functional mapping with auditory verb-generation (AVG) task and rs-fMRI with a seed in the left inferior frontal gyrus (IFG). First, we identified the functional connected areas to the IFG in HC. We qualitatively compared these areas with those that showed functional activation in AVG task derived from Neurosynth meta-analysis. Last, in each patient we performed single-subject analyses both for rs- and tb-fMRI, and we evaluated the spatial overlap between the two approaches. In HC, the IFG-ICN network showed a predominant left fronto-temporal functional connectivity in regions overlapping with the AVG network derived from a meta-analysis. In two patients, rs- and tb-fMRI showed comparable patterns of activation in left fronto-temporal regions, with different levels of contralateral activations. The third patient could not accomplish the AVG task and thus it was not possible to make any comparison with the ICN. However, in this patient, task-free approach disclosed a consistent network of fronto-temporal regions as in HC, and additional parietal regions. Our preliminary findings support the value of rs-fMRI approach for presurgical mapping, particularly for identifying left fronto-temporal core language-related areas in glioma patients. In a preoperative setting, rs-fMRI approach could represent a powerful tool for the identification of eloquent language areas, especially in patients with language or cognitive impairments.

Dataset Information

Sex Effect on Presurgical Language Mapping in Patients With a Brain Tumor.

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Sex Effect on Presurgical Language Mapping in Patients With a Brain Tumor.

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