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Right hemisphere structural adaptation and changing language skills years after left hemisphere stroke

Stroke survivors with acquired language deficits are commonly thought to reach a ‘plateau’ within a year of stroke onset, after which their residual language skills will remain stable. Nevertheless, there have been reports of patients who appear to recover over years. Here, we analysed longitudinal...

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Autores principales: Hope, Thomas M. H., Leff, Alex P., Prejawa, Susan, Bruce, Rachel, Haigh, Zula, Lim, Louise, Ramsden, Sue, Oberhuber, Marion, Ludersdorfer, Philipp, Crinion, Jenny, Seghier, Mohamed L., Price, Cathy J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5445256/
https://www.ncbi.nlm.nih.gov/pubmed/28444235
http://dx.doi.org/10.1093/brain/awx086
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author Hope, Thomas M. H.
Leff, Alex P.
Prejawa, Susan
Bruce, Rachel
Haigh, Zula
Lim, Louise
Ramsden, Sue
Oberhuber, Marion
Ludersdorfer, Philipp
Crinion, Jenny
Seghier, Mohamed L.
Price, Cathy J.
author_facet Hope, Thomas M. H.
Leff, Alex P.
Prejawa, Susan
Bruce, Rachel
Haigh, Zula
Lim, Louise
Ramsden, Sue
Oberhuber, Marion
Ludersdorfer, Philipp
Crinion, Jenny
Seghier, Mohamed L.
Price, Cathy J.
author_sort Hope, Thomas M. H.
collection PubMed
description Stroke survivors with acquired language deficits are commonly thought to reach a ‘plateau’ within a year of stroke onset, after which their residual language skills will remain stable. Nevertheless, there have been reports of patients who appear to recover over years. Here, we analysed longitudinal change in 28 left-hemisphere stroke patients, each more than a year post-stroke when first assessed—testing each patient’s spoken object naming skills and acquiring structural brain scans twice. Some of the patients appeared to improve over time while others declined; both directions of change were associated with, and predictable given, structural adaptation in the intact right hemisphere of the brain. Contrary to the prevailing view that these patients’ language skills are stable, these results imply that real change continues over years. The strongest brain–behaviour associations (the ‘peak clusters’) were in the anterior temporal lobe and the precentral gyrus. Using functional magnetic resonance imaging, we confirmed that both regions are actively involved when neurologically normal control subjects name visually presented objects, but neither appeared to be involved when the same participants used a finger press to make semantic association decisions on the same stimuli. This suggests that these regions serve word-retrieval or articulatory functions in the undamaged brain. We teased these interpretations apart by reference to change in other tasks. Consistent with the claim that the real change is occurring here, change in spoken object naming was correlated with change in two other similar tasks, spoken action naming and written object naming, each of which was independently associated with structural adaptation in similar (overlapping) right hemisphere regions. Change in written object naming, which requires word-retrieval but not articulation, was also significantly more correlated with both (i) change in spoken object naming; and (ii) structural adaptation in the two peak clusters, than was change in another task—auditory word repetition—which requires articulation but not word retrieval. This suggests that the changes in spoken object naming reflected variation at the level of word-retrieval processes. Surprisingly, given their qualitatively similar activation profiles, hypertrophy in the anterior temporal region was associated with improving behaviour, while hypertrophy in the precentral gyrus was associated with declining behaviour. We predict that either or both of these regions might be fruitful targets for neural stimulation studies (suppressing the precentral region and/or enhancing the anterior temporal region), aiming to encourage recovery or arrest decline even years after stroke occurs.
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spelling pubmed-54452562017-05-31 Right hemisphere structural adaptation and changing language skills years after left hemisphere stroke Hope, Thomas M. H. Leff, Alex P. Prejawa, Susan Bruce, Rachel Haigh, Zula Lim, Louise Ramsden, Sue Oberhuber, Marion Ludersdorfer, Philipp Crinion, Jenny Seghier, Mohamed L. Price, Cathy J. Brain Original Articles Stroke survivors with acquired language deficits are commonly thought to reach a ‘plateau’ within a year of stroke onset, after which their residual language skills will remain stable. Nevertheless, there have been reports of patients who appear to recover over years. Here, we analysed longitudinal change in 28 left-hemisphere stroke patients, each more than a year post-stroke when first assessed—testing each patient’s spoken object naming skills and acquiring structural brain scans twice. Some of the patients appeared to improve over time while others declined; both directions of change were associated with, and predictable given, structural adaptation in the intact right hemisphere of the brain. Contrary to the prevailing view that these patients’ language skills are stable, these results imply that real change continues over years. The strongest brain–behaviour associations (the ‘peak clusters’) were in the anterior temporal lobe and the precentral gyrus. Using functional magnetic resonance imaging, we confirmed that both regions are actively involved when neurologically normal control subjects name visually presented objects, but neither appeared to be involved when the same participants used a finger press to make semantic association decisions on the same stimuli. This suggests that these regions serve word-retrieval or articulatory functions in the undamaged brain. We teased these interpretations apart by reference to change in other tasks. Consistent with the claim that the real change is occurring here, change in spoken object naming was correlated with change in two other similar tasks, spoken action naming and written object naming, each of which was independently associated with structural adaptation in similar (overlapping) right hemisphere regions. Change in written object naming, which requires word-retrieval but not articulation, was also significantly more correlated with both (i) change in spoken object naming; and (ii) structural adaptation in the two peak clusters, than was change in another task—auditory word repetition—which requires articulation but not word retrieval. This suggests that the changes in spoken object naming reflected variation at the level of word-retrieval processes. Surprisingly, given their qualitatively similar activation profiles, hypertrophy in the anterior temporal region was associated with improving behaviour, while hypertrophy in the precentral gyrus was associated with declining behaviour. We predict that either or both of these regions might be fruitful targets for neural stimulation studies (suppressing the precentral region and/or enhancing the anterior temporal region), aiming to encourage recovery or arrest decline even years after stroke occurs. Oxford University Press 2017-06 2017-04-24 /pmc/articles/PMC5445256/ /pubmed/28444235 http://dx.doi.org/10.1093/brain/awx086 Text en © The Author (2017). Published by Oxford University Press on behalf of the Guarantors of Brain. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Hope, Thomas M. H.
Leff, Alex P.
Prejawa, Susan
Bruce, Rachel
Haigh, Zula
Lim, Louise
Ramsden, Sue
Oberhuber, Marion
Ludersdorfer, Philipp
Crinion, Jenny
Seghier, Mohamed L.
Price, Cathy J.
Right hemisphere structural adaptation and changing language skills years after left hemisphere stroke
title Right hemisphere structural adaptation and changing language skills years after left hemisphere stroke
title_full Right hemisphere structural adaptation and changing language skills years after left hemisphere stroke
title_fullStr Right hemisphere structural adaptation and changing language skills years after left hemisphere stroke
title_full_unstemmed Right hemisphere structural adaptation and changing language skills years after left hemisphere stroke
title_short Right hemisphere structural adaptation and changing language skills years after left hemisphere stroke
title_sort right hemisphere structural adaptation and changing language skills years after left hemisphere stroke
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5445256/
https://www.ncbi.nlm.nih.gov/pubmed/28444235
http://dx.doi.org/10.1093/brain/awx086
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