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Resting-state functional MRI language network connectivity differences in patients with brain tumors: exploration of the cerebellum and contralesional hemisphere
Brain tumors can have far-reaching impacts on functional networks. Language processing is typically lateralized to the left hemisphere, but also involves the right hemisphere and cerebellum. This resting-state functional MRI study investigated the proximal and distal effects of left-hemispheric brai...
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Published in: | Brain imaging and behavior 2022-02, Vol.16 (1), p.252-262 |
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description | Brain tumors can have far-reaching impacts on functional networks. Language processing is typically lateralized to the left hemisphere, but also involves the right hemisphere and cerebellum. This resting-state functional MRI study investigated the proximal and distal effects of left-hemispheric brain tumors on language network connectivity in the ipsilesional and contralesional hemispheres. Separate language resting-state networks were generated from seeding in ipsilesional (left) and contralesional (right) Broca’s Area for 29 patients with left-hemispheric brain tumors and 13 controls. Inclusion criteria for all subjects included language left-dominance based on task-based functional MRI. Functional connectivity was analyzed in each network to the respective Wernicke’s Area and contralateral cerebellum. Patients were assessed for language deficits prior to scanning. Compared to controls, patients exhibited decreased connectivity in the ipsilesional and contralesional hemispheres between the Broca’s Area and Wernicke’s Area homologs (mean connectivity for patients/controls: left 0.51/0.59,
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doi_str_mv | 10.1007/s11682-021-00498-5 |
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p
< 0.002; right 0.52/0.59,
p
< 0.0002). No differences in mean connectivity to the contralateral cerebellum were observed between groups (
p
> 0.09). Crossed cerebro-cerebellar connectivity was correlated in controls (rho = 0.59,
p
< 0.05), patients without language deficits (rho = 0.74,
p
< 0.0002), and patients with high-grade gliomas (rho = 0.78,
p
< 0.0002), but not in patients with language deficits or low-grade gliomas (
p
> 0.l). These findings demonstrate that brain tumors impact the language network in the contralesional hemisphere and cerebellum, which may reflect neurological deficits and lesion-induced cortical reorganization.</description><identifier>ISSN: 1931-7557</identifier><identifier>EISSN: 1931-7565</identifier><identifier>DOI: 10.1007/s11682-021-00498-5</identifier><identifier>PMID: 34333725</identifier><language>eng</language><publisher>New York: Springer US</publisher><subject>Biomedical and Life Sciences ; Biomedicine ; Brain ; Brain cancer ; Brain Mapping ; Brain Neoplasms - diagnostic imaging ; Brain tumors ; Cerebellum ; Cerebellum - diagnostic imaging ; Functional magnetic resonance imaging ; Hemispheres ; Hemispheric laterality ; Homology ; Humans ; Language ; Magnetic Resonance Imaging ; Natural language processing ; Neural networks ; Neurological diseases ; Neuropsychology ; Neuroradiology ; Neurosciences ; Original Research ; Protein seeding ; Psychiatry ; Tumors</subject><ispartof>Brain imaging and behavior, 2022-02, Vol.16 (1), p.252-262</ispartof><rights>The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature 2021</rights><rights>2021. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.</rights><rights>The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature 2021.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c375t-5912cfc5aa323b5339d84c1d9e9da24ba006c5b9397b6c95daadb01f428bf1c33</citedby><cites>FETCH-LOGICAL-c375t-5912cfc5aa323b5339d84c1d9e9da24ba006c5b9397b6c95daadb01f428bf1c33</cites><orcidid>0000-0002-9841-3078</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>315,786,790,27957,27958</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34333725$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Cho, Nicholas S.</creatorcontrib><creatorcontrib>Peck, Kyung K.</creatorcontrib><creatorcontrib>Gene, Madeleine N.</creatorcontrib><creatorcontrib>Jenabi, Mehrnaz</creatorcontrib><creatorcontrib>Holodny, Andrei I.</creatorcontrib><title>Resting-state functional MRI language network connectivity differences in patients with brain tumors: exploration of the cerebellum and contralesional hemisphere</title><title>Brain imaging and behavior</title><addtitle>Brain Imaging and Behavior</addtitle><addtitle>Brain Imaging Behav</addtitle><description>Brain tumors can have far-reaching impacts on functional networks. Language processing is typically lateralized to the left hemisphere, but also involves the right hemisphere and cerebellum. This resting-state functional MRI study investigated the proximal and distal effects of left-hemispheric brain tumors on language network connectivity in the ipsilesional and contralesional hemispheres. Separate language resting-state networks were generated from seeding in ipsilesional (left) and contralesional (right) Broca’s Area for 29 patients with left-hemispheric brain tumors and 13 controls. Inclusion criteria for all subjects included language left-dominance based on task-based functional MRI. Functional connectivity was analyzed in each network to the respective Wernicke’s Area and contralateral cerebellum. Patients were assessed for language deficits prior to scanning. Compared to controls, patients exhibited decreased connectivity in the ipsilesional and contralesional hemispheres between the Broca’s Area and Wernicke’s Area homologs (mean connectivity for patients/controls: left 0.51/0.59,
p
< 0.002; right 0.52/0.59,
p
< 0.0002). No differences in mean connectivity to the contralateral cerebellum were observed between groups (
p
> 0.09). Crossed cerebro-cerebellar connectivity was correlated in controls (rho = 0.59,
p
< 0.05), patients without language deficits (rho = 0.74,
p
< 0.0002), and patients with high-grade gliomas (rho = 0.78,
p
< 0.0002), but not in patients with language deficits or low-grade gliomas (
p
> 0.l). These findings demonstrate that brain tumors impact the language network in the contralesional hemisphere and cerebellum, which may reflect neurological deficits and lesion-induced cortical reorganization.</description><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Brain</subject><subject>Brain cancer</subject><subject>Brain Mapping</subject><subject>Brain Neoplasms - diagnostic imaging</subject><subject>Brain tumors</subject><subject>Cerebellum</subject><subject>Cerebellum - diagnostic imaging</subject><subject>Functional magnetic resonance imaging</subject><subject>Hemispheres</subject><subject>Hemispheric laterality</subject><subject>Homology</subject><subject>Humans</subject><subject>Language</subject><subject>Magnetic Resonance Imaging</subject><subject>Natural language processing</subject><subject>Neural networks</subject><subject>Neurological diseases</subject><subject>Neuropsychology</subject><subject>Neuroradiology</subject><subject>Neurosciences</subject><subject>Original Research</subject><subject>Protein seeding</subject><subject>Psychiatry</subject><subject>Tumors</subject><issn>1931-7557</issn><issn>1931-7565</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNp9kc1u1TAUhC0EoqXwAiyQJTbdBPwTJzE7VPFTqQipgrVlO8f3uiR2sB3aPg5vii8pRWLBypb9zZzRGYSeU_KKEtK_zpR2A2sIow0hrRwa8QAdU8lp04tOPLy_i_4IPcn5ihDRDpI-Rke85Zz3TByjn5eQiw-7JhddALs12OJj0BP-dHmOJx12q94BDlCuY_qGbQwBKvHDl1s8eucgQbCQsQ940cVDKBlf-7LHJun6VtY5pvwGw80yxaQP1jg6XPaAbZUamKZ1xjqMB-eS9AR5m76H2edlX5mn6JHTU4Znd-cJ-vr-3Zezj83F5w_nZ28vGst7URohKbPOCq0540ZwLsehtXSUIEfNWqMJ6awwksvedFaKUevREOpaNhhHLecn6HTzXVL8vtatqJrA1oA6QFyzYnWPgndMkIq-_Ae9imuqsSvVsU7QoSV9pdhG2RRzTuDUkvys062iRB0KVFuBqhaofheoRBW9uLNezQzjveRPYxXgG5DrV9hB-jv7P7a_AEj3qpI</recordid><startdate>20220201</startdate><enddate>20220201</enddate><creator>Cho, Nicholas S.</creator><creator>Peck, Kyung K.</creator><creator>Gene, Madeleine N.</creator><creator>Jenabi, Mehrnaz</creator><creator>Holodny, Andrei I.</creator><general>Springer US</general><general>Springer Nature B.V</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7RV</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88G</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB0</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M7P</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-9841-3078</orcidid></search><sort><creationdate>20220201</creationdate><title>Resting-state functional MRI language network connectivity differences in patients with brain tumors: exploration of the cerebellum and contralesional hemisphere</title><author>Cho, Nicholas S. ; Peck, Kyung K. ; Gene, Madeleine N. ; Jenabi, Mehrnaz ; Holodny, Andrei I.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c375t-5912cfc5aa323b5339d84c1d9e9da24ba006c5b9397b6c95daadb01f428bf1c33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Brain</topic><topic>Brain cancer</topic><topic>Brain Mapping</topic><topic>Brain Neoplasms - diagnostic imaging</topic><topic>Brain tumors</topic><topic>Cerebellum</topic><topic>Cerebellum - diagnostic imaging</topic><topic>Functional magnetic resonance imaging</topic><topic>Hemispheres</topic><topic>Hemispheric laterality</topic><topic>Homology</topic><topic>Humans</topic><topic>Language</topic><topic>Magnetic Resonance Imaging</topic><topic>Natural language processing</topic><topic>Neural networks</topic><topic>Neurological diseases</topic><topic>Neuropsychology</topic><topic>Neuroradiology</topic><topic>Neurosciences</topic><topic>Original Research</topic><topic>Protein seeding</topic><topic>Psychiatry</topic><topic>Tumors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Cho, Nicholas S.</creatorcontrib><creatorcontrib>Peck, Kyung K.</creatorcontrib><creatorcontrib>Gene, Madeleine N.</creatorcontrib><creatorcontrib>Jenabi, Mehrnaz</creatorcontrib><creatorcontrib>Holodny, Andrei I.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>ProQuest Nursing and Allied Health Journals</collection><collection>Neurosciences Abstracts</collection><collection>ProQuest Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection (Proquest) (PQ_SDU_P3)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Biological Sciences</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Psychology Database (ProQuest)</collection><collection>Biological Science Database</collection><collection>Nursing & Allied Health Premium</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest One Psychology</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><jtitle>Brain imaging and behavior</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Cho, Nicholas S.</au><au>Peck, Kyung K.</au><au>Gene, Madeleine N.</au><au>Jenabi, Mehrnaz</au><au>Holodny, Andrei I.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Resting-state functional MRI language network connectivity differences in patients with brain tumors: exploration of the cerebellum and contralesional hemisphere</atitle><jtitle>Brain imaging and behavior</jtitle><stitle>Brain Imaging and Behavior</stitle><addtitle>Brain Imaging Behav</addtitle><date>2022-02-01</date><risdate>2022</risdate><volume>16</volume><issue>1</issue><spage>252</spage><epage>262</epage><pages>252-262</pages><issn>1931-7557</issn><eissn>1931-7565</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>Brain tumors can have far-reaching impacts on functional networks. Language processing is typically lateralized to the left hemisphere, but also involves the right hemisphere and cerebellum. This resting-state functional MRI study investigated the proximal and distal effects of left-hemispheric brain tumors on language network connectivity in the ipsilesional and contralesional hemispheres. Separate language resting-state networks were generated from seeding in ipsilesional (left) and contralesional (right) Broca’s Area for 29 patients with left-hemispheric brain tumors and 13 controls. Inclusion criteria for all subjects included language left-dominance based on task-based functional MRI. Functional connectivity was analyzed in each network to the respective Wernicke’s Area and contralateral cerebellum. Patients were assessed for language deficits prior to scanning. Compared to controls, patients exhibited decreased connectivity in the ipsilesional and contralesional hemispheres between the Broca’s Area and Wernicke’s Area homologs (mean connectivity for patients/controls: left 0.51/0.59,
p
< 0.002; right 0.52/0.59,
p
< 0.0002). No differences in mean connectivity to the contralateral cerebellum were observed between groups (
p
> 0.09). Crossed cerebro-cerebellar connectivity was correlated in controls (rho = 0.59,
p
< 0.05), patients without language deficits (rho = 0.74,
p
< 0.0002), and patients with high-grade gliomas (rho = 0.78,
p
< 0.0002), but not in patients with language deficits or low-grade gliomas (
p
> 0.l). These findings demonstrate that brain tumors impact the language network in the contralesional hemisphere and cerebellum, which may reflect neurological deficits and lesion-induced cortical reorganization.</abstract><cop>New York</cop><pub>Springer US</pub><pmid>34333725</pmid><doi>10.1007/s11682-021-00498-5</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0002-9841-3078</orcidid></addata></record> |
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subjects | Biomedical and Life Sciences Biomedicine Brain Brain cancer Brain Mapping Brain Neoplasms - diagnostic imaging Brain tumors Cerebellum Cerebellum - diagnostic imaging Functional magnetic resonance imaging Hemispheres Hemispheric laterality Homology Humans Language Magnetic Resonance Imaging Natural language processing Neural networks Neurological diseases Neuropsychology Neuroradiology Neurosciences Original Research Protein seeding Psychiatry Tumors |
title | Resting-state functional MRI language network connectivity differences in patients with brain tumors: exploration of the cerebellum and contralesional hemisphere |
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