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

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 mini...

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Main Authors: Shun Yao, Einat Liebenthal, Parikshit Juvekar, Adomas Bunevicius, Matthew Vera, Laura Rigolo, Alexandra J. Golby, Yanmei Tie
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-01-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnins.2020.00004/full
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spelling doaj-812f917ac4114fd0b84559735587e08a2020-11-25T01:54:26ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2020-01-011410.3389/fnins.2020.00004481139Sex Effect on Presurgical Language Mapping in Patients With a Brain TumorShun Yao0Shun Yao1Shun Yao2Einat Liebenthal3Einat Liebenthal4Parikshit Juvekar5Adomas Bunevicius6Matthew Vera7Laura Rigolo8Alexandra J. Golby9Alexandra J. Golby10Yanmei Tie11Department of Neurosurgery, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, United StatesCenter for Pituitary Tumor Surgery, Department of Neurosurgery, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, ChinaWuhan School of Clinical Medicine, Southern Medical University, Wuhan, ChinaDepartment of Psychiatry, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, United StatesInstitute for Technology in Psychiatry, McLean Hospital, Harvard Medical School, Belmont, MA, United StatesDepartment of Neurosurgery, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, United StatesDepartment of Neurosurgery, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, United StatesDepartment of Neurosurgery, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, United StatesDepartment of Neurosurgery, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, United StatesDepartment of Neurosurgery, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, United StatesDepartment of Radiology, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, United StatesDepartment of Neurosurgery, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, United StatesDifferences 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.https://www.frontiersin.org/article/10.3389/fnins.2020.00004/fullsex effectpresurgical language mappingbrain tumorfunctional MRI (fMRI)functional connectivitysupplementary motor area (SMA)
collection DOAJ
language English
format Article
sources DOAJ
author Shun Yao
Shun Yao
Shun Yao
Einat Liebenthal
Einat Liebenthal
Parikshit Juvekar
Adomas Bunevicius
Matthew Vera
Laura Rigolo
Alexandra J. Golby
Alexandra J. Golby
Yanmei Tie
spellingShingle Shun Yao
Shun Yao
Shun Yao
Einat Liebenthal
Einat Liebenthal
Parikshit Juvekar
Adomas Bunevicius
Matthew Vera
Laura Rigolo
Alexandra J. Golby
Alexandra J. Golby
Yanmei Tie
Sex Effect on Presurgical Language Mapping in Patients With a Brain Tumor
Frontiers in Neuroscience
sex effect
presurgical language mapping
brain tumor
functional MRI (fMRI)
functional connectivity
supplementary motor area (SMA)
author_facet Shun Yao
Shun Yao
Shun Yao
Einat Liebenthal
Einat Liebenthal
Parikshit Juvekar
Adomas Bunevicius
Matthew Vera
Laura Rigolo
Alexandra J. Golby
Alexandra J. Golby
Yanmei Tie
author_sort Shun Yao
title Sex Effect on Presurgical Language Mapping in Patients With a Brain Tumor
title_short Sex Effect on Presurgical Language Mapping in Patients With a Brain Tumor
title_full Sex Effect on Presurgical Language Mapping in Patients With a Brain Tumor
title_fullStr Sex Effect on Presurgical Language Mapping in Patients With a Brain Tumor
title_full_unstemmed Sex Effect on Presurgical Language Mapping in Patients With a Brain Tumor
title_sort sex effect on presurgical language mapping in patients with a brain tumor
publisher Frontiers Media S.A.
series Frontiers in Neuroscience
issn 1662-453X
publishDate 2020-01-01
description 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.
topic sex effect
presurgical language mapping
brain tumor
functional MRI (fMRI)
functional connectivity
supplementary motor area (SMA)
url https://www.frontiersin.org/article/10.3389/fnins.2020.00004/full
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