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Dynamics of language reorganization after left temporo-parietal and frontal stroke

Published on Mar 1, 2020in Brain11.814
· DOI :10.1093/BRAIN/AWAA023
Anika Stockert5
Estimated H-index: 5
(Leipzig University),
Max Wawrzyniak4
Estimated H-index: 4
(Leipzig University)
+ 6 AuthorsDorothee Saur27
Estimated H-index: 27
(Leipzig University)
Abstract
The loss and recovery of language functions are still incompletely understood. This longitudinal functional MRI study investigated the neural mechanisms underlying language recovery in patients with post-stroke aphasia putting particular emphasis on the impact of lesion site. To identify patterns of language-related activation, an auditory functional MRI sentence comprehension paradigm was administered to patients with circumscribed lesions of either left frontal (n = 17) or temporo-parietal (n = 17) cortex. Patients were examined repeatedly during the acute ( 6 months, t3) post-stroke; healthy age-matched control subjects (n = 17) were tested once. The separation into two patient groups with circumscribed lesions allowed for a direct comparison of the contributions of distinct lesion-dependent network components to language reorganization between both groups. We hypothesized that activation of left hemisphere spared and perilesional cortex as well as lesion-homologue cortex in the right hemisphere varies between patient groups and across time. In addition, we expected that domain-general networks serving cognitive control independently contribute to language recovery. First, we found a global network disturbance in the acute phase that is characterized by reduced functional MRI language activation including areas distant to the lesion (i.e. diaschisis) and subsequent subacute network reactivation (i.e. resolution of diaschisis). These phenomena were driven by temporo-parietal lesions. Second, we identified a lesion-independent sequential activation pattern with increased activity of perilesional cortex and bilateral domain-general networks in the subacute phase followed by reorganization of left temporal language areas in the chronic phase. Third, we observed involvement of lesion-homologue cortex only in patients with frontal but not temporo-parietal lesions. Fourth, irrespective of lesion location, language reorganization predominantly occurred in pre-existing networks showing comparable activation in healthy controls. Finally, we detected different relationships of performance and activation in language and domain-general networks demonstrating the functional relevance for language recovery. Our findings highlight that the dynamics of language reorganization clearly depend on lesion location and hence open new perspectives for neurobiologically motivated strategies of language rehabilitation, such as individually-tailored targeted application of neuro-stimulation.
  • References (80)
  • Citations (5)
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References80
Newest
#1Rodolphe Nenert (UAB: University of Alabama at Birmingham)H-Index: 10
#2Jane B. Allendorfer (UAB: University of Alabama at Birmingham)H-Index: 15
Last. Jerzy P. Szaflarski (UAB: University of Alabama at Birmingham)H-Index: 51
view all 9 authors...
BACKGROUND: Recovery from stroke-induced aphasia is typically protracted and involves complex functional reorganization. The relative contributions of the lesioned and non-lesioned hemispheres to this process have been examined in several cross-sectional studies but longitudinal studies involving several time-points and large numbers of subjects are scarce. OBJECTIVE: The aim of this study was to address the gaps in the literature by longitudinally studying the evolution of post-stroke lateraliz...
2 CitationsSource
#1Joshua S. Siegel (WashU: Washington University in St. Louis)H-Index: 15
#2Benjamin A. Seitzman (WashU: Washington University in St. Louis)H-Index: 6
Last. Maurizio CorbettaH-Index: 5
view all 9 authors...
Abstract Studies of stroke have identified local reorganization in perilesional tissue. However, because the brain is highly networked, strokes also broadly alter the brain's global network organization. Here, we assess brain network structure longitudinally in adult stroke patients using resting state fMRI. The topology and boundaries of cortical regions remain grossly unchanged across recovery. In contrast, the modularity of brain systems i.e. the degree of integration within and segregation b...
23 CitationsSource
#1Joseph C. Griffis (UAB: University of Alabama at Birmingham)H-Index: 8
#2Rodolphe Nenert (UAB: University of Alabama at Birmingham)H-Index: 10
Last. Jerzy P. Szaflarski (UAB: University of Alabama at Birmingham)H-Index: 51
view all 4 authors...
Abstract The preservation of near-typical function in distributed brain networks is associated with less severe deficits in chronic stroke patients. However, it remains unclear how task-evoked responses in networks that support complex cognitive functions such as semantic processing relate to the post-stroke brain anatomy. Here, we used recently developed methods for the analysis of multimodal MRI data to investigate the relationship between regional tissue concentration and functional MRI activ...
9 CitationsSource
#1Gesa Hartwigsen (MPG: Max Planck Society)H-Index: 19
#2Dorothee Saur (Leipzig University)H-Index: 27
Abstract The role of left and right hemisphere brain regions in language recovery after stroke-induced aphasia remains controversial. Here, we summarize how neuroimaging studies increase the current understanding of functional interactions, reorganization and plasticity in the language network. We first discuss the temporal dynamics across the time course of language recovery, with a main focus on longitudinal studies from the acute to the chronic phase after stroke. These studies show that the ...
17 CitationsSource
#1Fatemeh Geranmayeh (Hammersmith Hospital)H-Index: 12
#2Tsz Wing Chau (Hammersmith Hospital)H-Index: 1
Last. Adam Hampshire (Hammersmith Hospital)H-Index: 33
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: We hypothesized that the recovery of speech production after left hemisphere stroke not only depends on the integrity of language-specialized brain systems, but also on 'domain-general' brain systems that have much broader functional roles. The presupplementary motor area/dorsal anterior cingulate forms part of the cingular-opercular network, which has a broad role in cognition and learning. Consequently, we have previously suggested that variability in the recovery of speech production after ...
20 CitationsSource
#1Laura M. Skipper-Kallal (GUMC: Georgetown University Medical Center)H-Index: 7
#2Elizabeth H. LaceyH-Index: 8
Last. Peter E. TurkeltaubH-Index: 29
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Language network reorganization in aphasia may depend on the degree of damage in critical language areas, making it difficult to determine how reorganization impacts performance. Prior studies on remapping of function in aphasia have not accounted for the location of the lesion relative to critical language areas. They rectified this problem by using a multimodal approach, combining multivariate lesion-symptom mapping and fMRI in chronic aphasia to understand the independent contributions to nam...
12 CitationsSource
#1Joseph C. Griffis (UAB: University of Alabama at Birmingham)H-Index: 8
#2Rodolphe Nenert (UAB: University of Alabama at Birmingham)H-Index: 10
Last. Jerzy P. Szaflarski (UAB: University of Alabama at Birmingham)H-Index: 51
view all 7 authors...
Current theories of language recovery after stroke are limited by a reliance on small studies. Here, we aimed to test predictions of current theory and resolve inconsistencies regarding right hemispheric contributions to long-term recovery. We first defined the canonical semantic network in 43 healthy controls. Then, in a group of 43 patients with chronic post-stroke aphasia, we tested whether activity in this network predicted performance on measures of semantic comprehension, naming, and fluen...
13 CitationsSource
#1Heather Flowers (U of T: University of Toronto)H-Index: 8
#2Stacey A. SkoretzH-Index: 5
Last. Rosemary Martino (U of T: University of Toronto)H-Index: 16
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Abstract Objectives To conduct a systematic review to elucidate the frequency, recovery, and associated outcomes for poststroke aphasia over the long-term. Data Sources Using the Cochrane Stroke Strategy, we searched 10 databases, 13 journals, 3 conferences, and the gray literature. Study Selection Our a priori protocol criteria included unselected samples of adult stroke patients from randomized controlled trials or consecutive cohorts. Two independent reviewers rated abstracts and articles for...
39 CitationsSource
#1Joshua S. Siegel (WashU: Washington University in St. Louis)H-Index: 15
#2Lenny Ramsey (WashU: Washington University in St. Louis)H-Index: 11
Last. Maurizio CorbettaH-Index: 76
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Abstract Deficits following stroke are classically attributed to focal damage, but recent evidence suggests a key role of distributed brain network disruption. We measured resting functional connectivity (FC), lesion topography, and behavior in multiple domains (attention, visual memory, verbal memory, language, motor, and visual) in a cohort of 132 stroke patients, and used machine-learning models to predict neurological impairment in individual subjects. We found that visual memory and verbal ...
113 CitationsSource
#1Anika Stockert (Leipzig University)H-Index: 5
#2Dorothee Kümmerer (University Medical Center Freiburg)H-Index: 12
Last. Dorothee Saur (Leipzig University)H-Index: 27
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Background: Post-stroke loss and recovery of language functions evolves in time and space. A high functional dynamic can be observed in the first days and weeks after stroke, which has been associated with reorganisation processes in the left-lateralised language network, its right-hemisphere homologues and in the vicinity of the lesion site. With the advances in in vivo neuroimaging techniques, mapping changes in the language network over time (e.g., lesion extent, structural integrity of grey ...
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Cited By5
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#1Christian Grefkes (University of Cologne)H-Index: 45
#2Gereon R. Fink (University of Cologne)H-Index: 98
Stroke is a leading cause of acquired, permanent disability worldwide. Although the treatment of acute stroke has been improved considerably, the majority of patients to date are left disabled with a considerable impact on functional independence and quality of life. As the absolute number of stroke survivors is likely to further increase due to the demographic changes in our aging societies, new strategies are needed in order to improve neurorehabilitation. The most critical driver of functiona...
Source
#1Gesa Hartwigsen (MPG: Max Planck Society)H-Index: 19
#2Anika Stockert (Leipzig University)H-Index: 5
Last. Dorothee Saur (Leipzig University)H-Index: 27
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Language is sustained by large-scale networks in the human brain. Stroke often severely affects function and network dynamics. However, the adaptive potential of the brain to compensate for lesions is poorly understood. A key question is whether upregulation of the right hemisphere is adaptive for language recovery. Targeting the potential for short-term reorganization in the lesioned brain, we applied 'virtual lesions' over left anterior or posterior inferior frontal gyrus (IFG) in post-stroke ...
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#1Jiangwen Yin (Shihezi University)H-Index: 4
#2Xuejiao Liu (First Affiliated Hospital of Wenzhou Medical University)
Last. Sheng Wang (USTC: University of Science and Technology of China)H-Index: 3
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Aim. Connexin 43 (Cx43) has been identified to be important for cerebral ischemia/reperfusion (I/R) injury as well as protection from it. This study was aimed at investigating the relationship between phosphorylated Cx43 (p-Cx43), transforming growth factor-β1 (TGF-β1)/Smad2/3 signaling pathway, and isoflurane postconditioning (ISPOC), which has effects on brain injury in rats with cerebral ischemia/reperfusion (I/R) injury. Methods. The middle cerebral artery occlusion (MCAO) model was induced ...
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#1Evgeniia Diachek (Vandy: Vanderbilt University)H-Index: 3
#1Evgeniia Diachek (Vandy: Vanderbilt University)H-Index: 1
Last. Evelina Fedorenko (MIT: Massachusetts Institute of Technology)H-Index: 34
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Aside from the core language-specific left-lateralized fronto-temporal network, language comprehension sometimes additionally recruits a domain-general bilateral fronto-parietal network implicated in executive functions: the multiple demand (MD) network. However, the nature of the MD network9s contributions to language comprehension remains debated. To illuminate the role of this network in language processing, we conducted a large-scale fMRI investigation using data from 30 diverse word and sen...
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