Absence of Perilesional Neuroplastic Recruitment in Chronic Poststroke Aphasia.
Journal
Neurology
ISSN: 1526-632X
Titre abrégé: Neurology
Pays: United States
ID NLM: 0401060
Informations de publication
Date de publication:
12 07 2022
12 07 2022
Historique:
received:
04
10
2021
accepted:
25
02
2022
pubmed:
5
5
2022
medline:
14
7
2022
entrez:
4
5
2022
Statut:
ppublish
Résumé
A prominent theory proposes that neuroplastic recruitment of perilesional tissue supports aphasia recovery, especially when language-capable cortex is spared by smaller lesions. This theory has rarely been tested directly and findings have been inconclusive. We tested the perilesional plasticity hypothesis using 2 fMRI tasks in 2 groups of patients with previous aphasia diagnosis. Two cohorts totaling 82 patients with chronic left-hemisphere stroke with previous aphasia diagnosis and 82 control participants underwent fMRI using either a naming task or a reliable semantic decision task. Individualized perilesional tissue was defined by dilating anatomical lesions and language regions were defined using meta-analyses. Mixed modeling examined differences in activity between groups. Relationships with lesion size and aphasia severity were examined. Patients exhibited reduced activity in perilesional language tissue relative to controls in both tasks. Although a few cortical regions exhibited greater activity irrespective of distance from the lesion, or only when distant from the lesion, no regions exhibited increased activity only when near the lesion. Larger lesions were associated with reduced language activity irrespective of distance from the lesion. Using the reliable fMRI task, reduced language activity was related to aphasia severity independent of lesion size. We found no evidence for neuroplastic recruitment of perilesional tissue in aphasia beyond its typical role in language. Rather, our findings are consistent with alternative hypotheses that changes in left-hemisphere activation during recovery relate to normalization of language network dysfunction and possibly recruitment of alternate cortical processors. These findings clarify left-hemisphere neuroplastic mechanisms supporting language recovery after stroke.
Sections du résumé
BACKGROUND AND OBJECTIVES
A prominent theory proposes that neuroplastic recruitment of perilesional tissue supports aphasia recovery, especially when language-capable cortex is spared by smaller lesions. This theory has rarely been tested directly and findings have been inconclusive. We tested the perilesional plasticity hypothesis using 2 fMRI tasks in 2 groups of patients with previous aphasia diagnosis.
METHODS
Two cohorts totaling 82 patients with chronic left-hemisphere stroke with previous aphasia diagnosis and 82 control participants underwent fMRI using either a naming task or a reliable semantic decision task. Individualized perilesional tissue was defined by dilating anatomical lesions and language regions were defined using meta-analyses. Mixed modeling examined differences in activity between groups. Relationships with lesion size and aphasia severity were examined.
RESULTS
Patients exhibited reduced activity in perilesional language tissue relative to controls in both tasks. Although a few cortical regions exhibited greater activity irrespective of distance from the lesion, or only when distant from the lesion, no regions exhibited increased activity only when near the lesion. Larger lesions were associated with reduced language activity irrespective of distance from the lesion. Using the reliable fMRI task, reduced language activity was related to aphasia severity independent of lesion size.
DISCUSSION
We found no evidence for neuroplastic recruitment of perilesional tissue in aphasia beyond its typical role in language. Rather, our findings are consistent with alternative hypotheses that changes in left-hemisphere activation during recovery relate to normalization of language network dysfunction and possibly recruitment of alternate cortical processors. These findings clarify left-hemisphere neuroplastic mechanisms supporting language recovery after stroke.
Identifiants
pubmed: 35508398
pii: WNL.0000000000200382
doi: 10.1212/WNL.0000000000200382
pmc: PMC9280993
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e119-e128Subventions
Organisme : NCATS NIH HHS
ID : KL2 TR000102
Pays : United States
Organisme : NCATS NIH HHS
ID : TL1 TR001431
Pays : United States
Organisme : NINDS NIH HHS
ID : U10 NS086513
Pays : United States
Organisme : NIDCD NIH HHS
ID : K99 DC018828
Pays : United States
Organisme : NIDCD NIH HHS
ID : R01 DC014960
Pays : United States
Organisme : NICHD NIH HHS
ID : K12 HD093427
Pays : United States
Informations de copyright
Copyright © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Academy of Neurology.
Références
Brain. 2006 Jun;129(Pt 6):1371-84
pubmed: 16638796
Stroke. 2020 Sep;51(9):2872-2884
pubmed: 32757757
Brain. 2014 Jan;137(Pt 1):242-54
pubmed: 24163248
Hum Brain Mapp. 2017 Apr;38(4):2051-2066
pubmed: 28083891
Stroke. 1995 Nov;26(11):2135-44
pubmed: 7482662
Brain. 2020 Mar 1;143(3):844-861
pubmed: 32068789
J Speech Lang Hear Res. 2019 Nov 22;62(11):3907-3922
pubmed: 31756155
Brain. 2005 May;128(Pt 5):1122-38
pubmed: 15728652
Neuroimage. 2006 Jul 1;31(3):1116-28
pubmed: 16545965
J Cereb Blood Flow Metab. 2000 Jan;20(1):45-52
pubmed: 10616792
J Neurophysiol. 1998 Apr;79(4):2119-48
pubmed: 9535973
J Speech Lang Hear Res. 2019 Nov 22;62(11):3937-3946
pubmed: 31756153
Neurobiol Lang (Camb). 2021;2(1):22-82
pubmed: 33884373
Cortex. 2015 Feb;63:296-316
pubmed: 25460496
Curr Neurol Neurosci Rep. 2015 Nov;15(11):72
pubmed: 26396038
Exp Neurol. 2008 Jul;212(1):207-12
pubmed: 18501349
Neuroimage. 2002 Jan;15(1):1-15
pubmed: 11771969
Proc Natl Acad Sci U S A. 2013 Oct 8;110(41):16616-21
pubmed: 24062451
Behav Neurol. 2011;24(2):117-22
pubmed: 21606572
Top Stroke Rehabil. 2005 Summer;12(3):11-26
pubmed: 16110424
Neuroimage. 2012 Apr 2;60(2):854-63
pubmed: 22227052
Curr Opin Neurobiol. 1999 Dec;9(6):740-7
pubmed: 10607636
Neuroimage Clin. 2016 Mar 24;16:399-408
pubmed: 28879081
J Neurol Neurosurg Psychiatry. 1999 Feb;66(2):155-61
pubmed: 10071093
Hum Brain Mapp. 2018 Aug;39(8):3285-3307
pubmed: 29665223
Cereb Cortex. 2010 May;20(5):1013-9
pubmed: 19687294
Brain. 2014 Oct;137(Pt 10):2632-48
pubmed: 24974382
Neuroimage. 2008 Feb 15;39(4):2038-46
pubmed: 18096407
J Neurosci. 2002 Oct 1;22(19):8597-606
pubmed: 12351733
Comput Biomed Res. 1996 Jun;29(3):162-73
pubmed: 8812068
J Commun Disord. 2014 Sep-Oct;51:43-50
pubmed: 25092638
Brain Lang. 2006 Jul;98(1):118-23
pubmed: 16564566
Nat Neurosci. 2009 May;12(5):535-40
pubmed: 19396166
Curr Neurol Neurosci Rep. 2008 Nov;8(6):475-83
pubmed: 18957184
Nat Rev Neurol. 2020 Jan;16(1):43-55
pubmed: 31772339
J Neurosci. 2010 Sep 1;30(35):11558-64
pubmed: 20810877
Neuroimage. 2013 Nov 15;82:403-15
pubmed: 23747961
Ann Neurol. 1999 Apr;45(4):430-8
pubmed: 10211466
Nat Methods. 2011 Jun 26;8(8):665-70
pubmed: 21706013
Neurol Res Pract. 2020 Jun 16;2:17
pubmed: 33324923
J Stroke Cerebrovasc Dis. 2011 Jul-Aug;20(4):336-45
pubmed: 20719532