Second language learning induces grey matter volume increase in people with multiple sclerosis
Grey matter volume (GMV) decline is a frequent finding in multiple sclerosis (MS), the most common chronic neurological disease in young adults. Increases of GMV were detected in language related brain regions following second language (L2) learning in healthy adults. Effects of L2 learning in peopl...
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| Vydáno v: | PloS one Ročník 14; číslo 12; s. e0226525 |
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| Hlavní autoři: | , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
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United States
Public Library of Science
23.12.2019
Public Library of Science (PLoS) |
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| ISSN: | 1932-6203, 1932-6203 |
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| Abstract | Grey matter volume (GMV) decline is a frequent finding in multiple sclerosis (MS), the most common chronic neurological disease in young adults. Increases of GMV were detected in language related brain regions following second language (L2) learning in healthy adults. Effects of L2 learning in people with MS (pwMS) have not been investigated so far.
This study prospectively evaluated the potential of an eight-week L2 training on grey matter plasticity measured by 3T-MRI, L2 proficiency and health-related quality of life (HRQoL) in people with relapsing-remitting MS (pwMS, n = 11) and healthy, sex- and age-matched controls (HCs; n = 12).
Categorical voxel-based analysis revealed significantly less GMV bilaterally of the insula extending to the temporal pole in pwMS at baseline. Following L2 training, significant increases of GMV were evident in the right hippocampus, parahippocampus and putamen of pwMS and in the left insula of HCs. L2 training resulted in significant improvements of listening comprehension, speaking fluency and vocabulary knowledge in both pwMS and HCs. GMV increases of right hippocampus and parahippocampus significantly correlated with vocabulary knowledge gain and L2 learning was associated with a significant increase of HRQoL in pwMS.
Our findings demonstrate distinct patterns of GMV increases of language related brain regions in pwMS and HCs and indicate disease-related compensatory cortical and subcortical plasticity to acquire L2 proficiency in pwMS. |
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| AbstractList | Grey matter volume (GMV) decline is a frequent finding in multiple sclerosis (MS), the most common chronic neurological disease in young adults. Increases of GMV were detected in language related brain regions following second language (L2) learning in healthy adults. Effects of L2 learning in people with MS (pwMS) have not been investigated so far. This study prospectively evaluated the potential of an eight-week L2 training on grey matter plasticity measured by 3T-MRI, L2 proficiency and health-related quality of life (HRQoL) in people with relapsing-remitting MS (pwMS, n = 11) and healthy, sex- and age-matched controls (HCs; n = 12). Categorical voxel-based analysis revealed significantly less GMV bilaterally of the insula extending to the temporal pole in pwMS at baseline. Following L2 training, significant increases of GMV were evident in the right hippocampus, parahippocampus and putamen of pwMS and in the left insula of HCs. L2 training resulted in significant improvements of listening comprehension, speaking fluency and vocabulary knowledge in both pwMS and HCs. GMV increases of right hippocampus and parahippocampus significantly correlated with vocabulary knowledge gain and L2 learning was associated with a significant increase of HRQoL in pwMS. Our findings demonstrate distinct patterns of GMV increases of language related brain regions in pwMS and HCs and indicate disease-related compensatory cortical and subcortical plasticity to acquire L2 proficiency in pwMS. Background Grey matter volume (GMV) decline is a frequent finding in multiple sclerosis (MS), the most common chronic neurological disease in young adults. Increases of GMV were detected in language related brain regions following second language (L2) learning in healthy adults. Effects of L2 learning in people with MS (pwMS) have not been investigated so far. Methods This study prospectively evaluated the potential of an eight-week L2 training on grey matter plasticity measured by 3T-MRI, L2 proficiency and health-related quality of life (HRQoL) in people with relapsing-remitting MS (pwMS, n = 11) and healthy, sex- and age-matched controls (HCs; n = 12). Results Categorical voxel-based analysis revealed significantly less GMV bilaterally of the insula extending to the temporal pole in pwMS at baseline. Following L2 training, significant increases of GMV were evident in the right hippocampus, parahippocampus and putamen of pwMS and in the left insula of HCs. L2 training resulted in significant improvements of listening comprehension, speaking fluency and vocabulary knowledge in both pwMS and HCs. GMV increases of right hippocampus and parahippocampus significantly correlated with vocabulary knowledge gain and L2 learning was associated with a significant increase of HRQoL in pwMS. Conclusion Our findings demonstrate distinct patterns of GMV increases of language related brain regions in pwMS and HCs and indicate disease-related compensatory cortical and subcortical plasticity to acquire L2 proficiency in pwMS. BackgroundGrey matter volume (GMV) decline is a frequent finding in multiple sclerosis (MS), the most common chronic neurological disease in young adults. Increases of GMV were detected in language related brain regions following second language (L2) learning in healthy adults. Effects of L2 learning in people with MS (pwMS) have not been investigated so far.MethodsThis study prospectively evaluated the potential of an eight-week L2 training on grey matter plasticity measured by 3T-MRI, L2 proficiency and health-related quality of life (HRQoL) in people with relapsing-remitting MS (pwMS, n = 11) and healthy, sex- and age-matched controls (HCs; n = 12).ResultsCategorical voxel-based analysis revealed significantly less GMV bilaterally of the insula extending to the temporal pole in pwMS at baseline. Following L2 training, significant increases of GMV were evident in the right hippocampus, parahippocampus and putamen of pwMS and in the left insula of HCs. L2 training resulted in significant improvements of listening comprehension, speaking fluency and vocabulary knowledge in both pwMS and HCs. GMV increases of right hippocampus and parahippocampus significantly correlated with vocabulary knowledge gain and L2 learning was associated with a significant increase of HRQoL in pwMS.ConclusionOur findings demonstrate distinct patterns of GMV increases of language related brain regions in pwMS and HCs and indicate disease-related compensatory cortical and subcortical plasticity to acquire L2 proficiency in pwMS. Background Grey matter volume (GMV) decline is a frequent finding in multiple sclerosis (MS), the most common chronic neurological disease in young adults. Increases of GMV were detected in language related brain regions following second language (L2) learning in healthy adults. Effects of L2 learning in people with MS (pwMS) have not been investigated so far. Methods This study prospectively evaluated the potential of an eight-week L2 training on grey matter plasticity measured by 3T-MRI, L2 proficiency and health-related quality of life (HRQoL) in people with relapsing-remitting MS (pwMS, n = 11) and healthy, sex- and age-matched controls (HCs; n = 12). Results Categorical voxel-based analysis revealed significantly less GMV bilaterally of the insula extending to the temporal pole in pwMS at baseline. Following L2 training, significant increases of GMV were evident in the right hippocampus, parahippocampus and putamen of pwMS and in the left insula of HCs. L2 training resulted in significant improvements of listening comprehension, speaking fluency and vocabulary knowledge in both pwMS and HCs. GMV increases of right hippocampus and parahippocampus significantly correlated with vocabulary knowledge gain and L2 learning was associated with a significant increase of HRQoL in pwMS. Conclusion Our findings demonstrate distinct patterns of GMV increases of language related brain regions in pwMS and HCs and indicate disease-related compensatory cortical and subcortical plasticity to acquire L2 proficiency in pwMS. Grey matter volume (GMV) decline is a frequent finding in multiple sclerosis (MS), the most common chronic neurological disease in young adults. Increases of GMV were detected in language related brain regions following second language (L2) learning in healthy adults. Effects of L2 learning in people with MS (pwMS) have not been investigated so far.BACKGROUNDGrey matter volume (GMV) decline is a frequent finding in multiple sclerosis (MS), the most common chronic neurological disease in young adults. Increases of GMV were detected in language related brain regions following second language (L2) learning in healthy adults. Effects of L2 learning in people with MS (pwMS) have not been investigated so far.This study prospectively evaluated the potential of an eight-week L2 training on grey matter plasticity measured by 3T-MRI, L2 proficiency and health-related quality of life (HRQoL) in people with relapsing-remitting MS (pwMS, n = 11) and healthy, sex- and age-matched controls (HCs; n = 12).METHODSThis study prospectively evaluated the potential of an eight-week L2 training on grey matter plasticity measured by 3T-MRI, L2 proficiency and health-related quality of life (HRQoL) in people with relapsing-remitting MS (pwMS, n = 11) and healthy, sex- and age-matched controls (HCs; n = 12).Categorical voxel-based analysis revealed significantly less GMV bilaterally of the insula extending to the temporal pole in pwMS at baseline. Following L2 training, significant increases of GMV were evident in the right hippocampus, parahippocampus and putamen of pwMS and in the left insula of HCs. L2 training resulted in significant improvements of listening comprehension, speaking fluency and vocabulary knowledge in both pwMS and HCs. GMV increases of right hippocampus and parahippocampus significantly correlated with vocabulary knowledge gain and L2 learning was associated with a significant increase of HRQoL in pwMS.RESULTSCategorical voxel-based analysis revealed significantly less GMV bilaterally of the insula extending to the temporal pole in pwMS at baseline. Following L2 training, significant increases of GMV were evident in the right hippocampus, parahippocampus and putamen of pwMS and in the left insula of HCs. L2 training resulted in significant improvements of listening comprehension, speaking fluency and vocabulary knowledge in both pwMS and HCs. GMV increases of right hippocampus and parahippocampus significantly correlated with vocabulary knowledge gain and L2 learning was associated with a significant increase of HRQoL in pwMS.Our findings demonstrate distinct patterns of GMV increases of language related brain regions in pwMS and HCs and indicate disease-related compensatory cortical and subcortical plasticity to acquire L2 proficiency in pwMS.CONCLUSIONOur findings demonstrate distinct patterns of GMV increases of language related brain regions in pwMS and HCs and indicate disease-related compensatory cortical and subcortical plasticity to acquire L2 proficiency in pwMS. Grey matter volume (GMV) decline is a frequent finding in multiple sclerosis (MS), the most common chronic neurological disease in young adults. Increases of GMV were detected in language related brain regions following second language (L2) learning in healthy adults. Effects of L2 learning in people with MS (pwMS) have not been investigated so far. This study prospectively evaluated the potential of an eight-week L2 training on grey matter plasticity measured by 3T-MRI, L2 proficiency and health-related quality of life (HRQoL) in people with relapsing-remitting MS (pwMS, n = 11) and healthy, sex- and age-matched controls (HCs; n = 12). Categorical voxel-based analysis revealed significantly less GMV bilaterally of the insula extending to the temporal pole in pwMS at baseline. Following L2 training, significant increases of GMV were evident in the right hippocampus, parahippocampus and putamen of pwMS and in the left insula of HCs. L2 training resulted in significant improvements of listening comprehension, speaking fluency and vocabulary knowledge in both pwMS and HCs. GMV increases of right hippocampus and parahippocampus significantly correlated with vocabulary knowledge gain and L2 learning was associated with a significant increase of HRQoL in pwMS. Our findings demonstrate distinct patterns of GMV increases of language related brain regions in pwMS and HCs and indicate disease-related compensatory cortical and subcortical plasticity to acquire L2 proficiency in pwMS. |
| Audience | Academic |
| Author | Eberharter, Kathrin Spöttl, Carol Amprosi, Matthias Gizewski, Elke R. Steiger, Ruth Tuovinen, Noora Zehentner, Matthias Ehling, Rainer Benke, Thomas Brenneis, Christian Berger, Thomas Bsteh, Gabriel Kremmel, Benjamin Scherfler, Christoph |
| AuthorAffiliation | Heinrich-Heine-Universitat Dusseldorf, GERMANY 2 Karl Landsteiner Institut für Interdisziplinäre Forschung am Reha Zentrum Münster, Münster, Austria 1 Department of Neurology, Clinic for Rehabilitation Münster, Münster, Austria 3 Department of Neurology, Medical University of Innsbruck, Innsbruck, Austria 6 Neuroimaging Research Core Facility, Medical University Innsbruck, Innsbruck, Austria 5 Department of Neuroradiology, Medical University of Innsbruck, Innsbruck, Austria 4 Language Testing Research Group Innsbruck, Department for Subject Specific Education, University of Innsbruck, Innsbruck, Austria |
| AuthorAffiliation_xml | – name: 3 Department of Neurology, Medical University of Innsbruck, Innsbruck, Austria – name: Heinrich-Heine-Universitat Dusseldorf, GERMANY – name: 1 Department of Neurology, Clinic for Rehabilitation Münster, Münster, Austria – name: 4 Language Testing Research Group Innsbruck, Department for Subject Specific Education, University of Innsbruck, Innsbruck, Austria – name: 6 Neuroimaging Research Core Facility, Medical University Innsbruck, Innsbruck, Austria – name: 2 Karl Landsteiner Institut für Interdisziplinäre Forschung am Reha Zentrum Münster, Münster, Austria – name: 5 Department of Neuroradiology, Medical University of Innsbruck, Innsbruck, Austria |
| Author_xml | – sequence: 1 givenname: Rainer orcidid: 0000-0002-6291-9659 surname: Ehling fullname: Ehling, Rainer – sequence: 2 givenname: Matthias surname: Amprosi fullname: Amprosi, Matthias – sequence: 3 givenname: Benjamin surname: Kremmel fullname: Kremmel, Benjamin – sequence: 4 givenname: Gabriel surname: Bsteh fullname: Bsteh, Gabriel – sequence: 5 givenname: Kathrin surname: Eberharter fullname: Eberharter, Kathrin – sequence: 6 givenname: Matthias surname: Zehentner fullname: Zehentner, Matthias – sequence: 7 givenname: Ruth surname: Steiger fullname: Steiger, Ruth – sequence: 8 givenname: Noora surname: Tuovinen fullname: Tuovinen, Noora – sequence: 9 givenname: Elke R. surname: Gizewski fullname: Gizewski, Elke R. – sequence: 10 givenname: Thomas surname: Benke fullname: Benke, Thomas – sequence: 11 givenname: Thomas surname: Berger fullname: Berger, Thomas – sequence: 12 givenname: Carol surname: Spöttl fullname: Spöttl, Carol – sequence: 13 givenname: Christian surname: Brenneis fullname: Brenneis, Christian – sequence: 14 givenname: Christoph surname: Scherfler fullname: Scherfler, Christoph |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31869402$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_1007_s00415_024_12395_0 crossref_primary_10_1016_j_neuropsychologia_2020_107593 crossref_primary_10_1016_j_msard_2023_105017 crossref_primary_10_3390_biomedicines10020432 crossref_primary_10_7759_cureus_42103 crossref_primary_10_1002_hbm_70344 crossref_primary_10_1007_s11065_021_09479_3 crossref_primary_10_1016_j_neubiorev_2021_02_029 crossref_primary_10_3390_brainsci12091122 crossref_primary_10_1016_j_neuroscience_2022_03_031 |
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| DOI | 10.1371/journal.pone.0226525 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 ObjectType-Article-2 ObjectType-Feature-1 content type line 23 Competing Interests: The present study was funded by an unrestricted research grant of Merck Austria. None of the authors has an affiliation with Merck Austria. There are no patents, products in development or marketed products to declare. Further, this does not alter our adherence to PLOS ONE policies on sharing data and materials. |
| ORCID | 0000-0002-6291-9659 |
| OpenAccessLink | http://dx.doi.org/10.1371/journal.pone.0226525 |
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| PublicationDate | 2019-12-23 |
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| Snippet | Grey matter volume (GMV) decline is a frequent finding in multiple sclerosis (MS), the most common chronic neurological disease in young adults. Increases of... Background Grey matter volume (GMV) decline is a frequent finding in multiple sclerosis (MS), the most common chronic neurological disease in young adults.... BackgroundGrey matter volume (GMV) decline is a frequent finding in multiple sclerosis (MS), the most common chronic neurological disease in young adults.... Background Grey matter volume (GMV) decline is a frequent finding in multiple sclerosis (MS), the most common chronic neurological disease in young adults.... |
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| Title | Second language learning induces grey matter volume increase in people with multiple sclerosis |
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