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

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 (≤1 week, t1), subacute (1–2 weeks, t2) and chronic phase (>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.

The domain-general multiple demand (MD) network does not support core aspects of language comprehension: a large-scale fMRI investigation

“…The MD network might be especially plastic in this way, given that it flexibly supports diverse behaviors and modulates its responses based on current task demands (e.g., Freedman et al, 2001;Cromer et al, 2010;Jackson et al, 2016;Kumano et al, 2016). Recent behavioral (e.g., Martin & Allen, 2008;Corbett et al, 2009;El Hachioui et al, 2014;Bonini & Radanovic, 2015;Villard & Kiran, 2016;Simic et al, 2017;Wall et al, 2017) and neuroimaging (e.g., Brownsett et al, 2014;Geranmayeh et al, 2016Geranmayeh et al, , 2017Sims et al, 2016;Meier et al, 2016;Stockert et al, 2020) studies have begun to suggest a possible role for the MD network in recovery from aphasia (see Hartwigsen, 2018, for a review). Related evidence comes from increases in the MD network's activity during language processing in aging (e.g., Wingfield & Grossman, 2006).…”

Variables and Mechanisms Affecting Response to Language Treatment in Multilingual People with Aphasia

“…The mechanisms underlying treatment-related improvement in aphasia have been studied in recent years, but much is still not well understood [16,17]. The evidence suggests that neuroplasticity allows for reorganization of portions of the neuronal networks, and that regions adjacent to or homologous to the affected regions take on language-related processing [18,19]. Similar processes can be assumed to account for changes observed in multilingual PWA, but an additional consideration is required.…”

Language networks in aphasia and health: a 1000 participant Activation Likelihood Estimate analysis

“…Only five papers, representing six of the 64 PSA groups, repeated functional neuroimaging longitudinally at multiple timepoints (Cardebat et al, 2003;Radman et al, 2016;Long et al, 2017;Nenert et al, 2018;Stockert et al, 2020). When counting the 'earliest' timepoint at which each PSA group was scanned, only 9/64 groups had mean times post-stroke less than 6 months (Cardebat et al, 2003;Mattioli et al, 2014;Geranmayeh et al, 2016;Radman et al, 2016;Long et al, 2017;Qiu et al, 2017;Nenert et al, 2018;Stockert et al, 2020). Accordingly, there were too few groups to contrast PSA before versus after six months (Eickhoff et al, 2016).…”

“…Despite its size and clear results, inevitably this study has limitations. First, we did not have information regarding lesion location and thus were unable to investigate how this might influence activation patterns post-stroke (Stockert et al, 2020). Second, it is important to be cautious about decreased neurovascular coupling post-stroke, which itself could generate false differences between patients and controls.…”