Chronic post-stroke aphasia severity is determined by fragmentation of residual white matter networks

Abstract

Many stroke survivors with aphasia in the acute period experience spontaneous recovery within the first six months after the stroke. However, approximately 30–40% sustain permanent aphasia and the factors determining incomplete recovery are unclear. Suboptimal recovery may be influenced by disruption of areas seemingly spared by the stroke due to loss of white matter connectivity and network integrity. We reconstructed individual anatomical whole-brain connectomes from 90 left hemisphere stroke survivors using diffusion MR images. We measured the modularity of the residual white matter network organization, the probability of brain regions clustering together, and the degree of fragmentation of left hemisphere networks. Greater post-stroke left hemisphere network fragmentation and higher modularity index were associated with more severe chronic aphasia, controlling for the size of the stroke lesion. Even when the left hemisphere was relatively spared, subjects with disorganized community structure had significantly worse aphasia, particularly when key temporal lobe regions were isolated into segregated modules. These results suggest that white matter integrity and disorganization of neuronal networks could be important determinants of chronic aphasia severity. Connectome white matter organization measured through modularity and other topological features could be used as a personalized variable for clinical staging and aphasia treatment planning.

Structural disconnections explain brain network dysfunction after stroke

“…Our results also complement prior studies that have implicated WM damage and SDC as important factors in determining the severity of cognitive and behavioral deficits after stroke (Catani et al, 2012;Chechlacz et al, 2013;Corbetta et al, 2015;Forkel et al, 2014;Griffis et al, 2017b, Kuceyeski et al, 2015Marebwa et al, 2017;Thiebaut De Schotten et al, 2014;Yourganov et al, 2016). Speculatively, these relationships may be partially mediated by the large-scale functional disruptions precipitated by SDCs.…”

Brain networks and their relevance for stroke rehabilitation

“…In this regard, several studies promote the idea that stroke lesions lead to modular fragmentation and clustering resulting in weaker inter-modular integrations and a total decrease of information transfer and communicability especially remotely to the lesion. This has been shown both, in aphasia (Gleichgerrcht et al, 2015, Yourganov et al, 2016, Marebwa et al, 2017 and motor affection (Crofts et al, 2011, Kuceyeski et al, 2014 after stroke, supporting additionally the idea of secondary degeneration. This indicates a large effect on local and global networks induced by a focal brain lesion (Saenger et al, 2017, Foulon et al, 2018.…”

“…Hereby, the loss of specific white matter tracts measured with DTI usually leads to specific loss of functions, known as dysconnection syndromes (Catani et al, 2005, Thiebaut de Schotten et al, 2005. This is also seen in pure subcortical stroke lesions (Marebwa et al, 2017). In this regard, patients, in whom stroke lesions affect areas with a high overlap of association fibres are more likely to suffer from deficits in several cognitive domains depending on the affected white matter tracts (Corbetta et al, 2015).…”

Mapping Language Networks Using the Structural and Dynamic Brain Connectomes

“…Overall, their and our findings suggest that there is additional information from each modality that can leveraged to better understand the neurobiology of poststroke impairments and aphasia. Importantly, our findings suggest that CDLSM is particularly useful in improving predictions, indicating that connectome based studies, which are instrumental in expanding the understanding of the relationship between brain structural integrity and behavior ( Yourganov et al, 2016 ; Gleichgerrcht et al, 2017 ; Marebwa et al, 2017 ), can be even further improved by including connectome dynamics. To our knowledge, this is one of the first studies to assess structural connectome dynamics related to stroke recovery.…”