The disrupted topological properties of structural networks showed recovery in ischemic stroke patients: a longitudinal design study

Abstract

Introduction Stroke is one of the leading causes of substantial disability worldwide. Previous studies have shown brain functional and structural alterations in adults with stroke. However, few studies have examined the longitudinal reorganization in whole-brain structural networks in stroke. Methods Here, we applied graph theoretical analysis to investigate the longitudinal topological organization of white matter networks in 20 ischemic stroke patients with a one-month interval between two timepoints. Two sets of clinical scores, Fugl-Meyer motor assessment (FMA) and neurological deficit scores (NDS), were assessed for all patients on the day the image data were collected. Results The stroke patients exhibited significant increases in FMA scores and significant reductions in DNS between the two timepoints. All groups exhibited small-world organization (σ > 1) in the brain structural network, including a high clustering coefficient (γ > 1) and a low normalized characteristic path length (λ ≈ 1). However, compared to healthy controls, stroke patients showed significant decrease in nodal characteristics at the first timepoint, primarily in the right supplementary motor area, right middle temporal gyrus, right inferior parietal lobe, right postcentral gyrus and left posterior cingulate gyrus. Longitudinal results demonstrated that altered nodal characteristics were partially restored one month later. Additionally, significant correlations between the nodal characteristics of the right supplementary motor area and the clinical scale scores (FMA and NDS) were observed in stroke patients. Similar behavioral-neuroimaging correlations were found in the right inferior parietal lobe. Conclusion Altered topological properties may be an effect of stroke, which can be modulated during recovery. The longitudinal results and the neuroimaging-behavioral relationship may provide information for understanding brain recovery from stroke. Future studies should detect whether observed changes in structural topological properties can predict the recovery of daily cognitive function in stroke.

Development and Testing of SPIDER-NET: An Interactive Tool for Brain Connectogram Visualization, Sub-Network Exploration and Graph Metrics Quantification

“…The example of application presented in this study highlighted the impact of graph-based metrics in connectivity analysis. Both local and global metrics derived from the whole-brain networks of Case 1 and Case 2 differed from HC one, as expected ( Crofts et al, 2011 ; Cheng et al, 2019 ; Li et al, 2021 ). This quantitative result mirrored the differences qualitatively observed with connectograms.…”

Frequency-Specific Changes of Amplitude of Low-Frequency Fluctuations in Patients with Acute Basal Ganglia Ischemic Stroke

“…The research of Nierhaus and colleagues has showed increased functional connectivity between the caudate nucleus and red nucleus in patients with poststroke motor disturbance [ 47 ]. Li et al who used graph-based theoretical approach found that the nodal efficiency of acute stroke patients with unimanual motor deficits was reduced in the caudate [ 48 ]. However, correlation results in the current study showed that there was a significant negative correlation between FMA scores and fALFF value of the right caudate.…”

Brain’s Energy After Stroke: From a Cellular Perspective Toward Behavior

“…Neuroimaging technics allow the description of network reorganización after a stroke. The majority of recent studies report the conservation of small-world definition for the network state, but with a deterioration of specific small-world indices in acute ( Caliandro et al, 2017 ; Shi et al, 2021 ) and subacute stages of the stroke ( Wang et al, 2010 ; Zhang et al, 2017 ; Li et al, 2021 ). Interestingly, the preservation ( Bonilha et al, 2016 ) and recovery ( Caliandro et al, 2017 ; Li et al, 2021 ) of optimal small-world properties of the network correlate positively with the improvement of cognitive and motor functions, suggesting that small-world indices restoration could be a proxy for predicting neurological recovery ( Vecchio et al, 2019 ).…”

“…The majority of recent studies report the conservation of small-world definition for the network state, but with a deterioration of specific small-world indices in acute ( Caliandro et al, 2017 ; Shi et al, 2021 ) and subacute stages of the stroke ( Wang et al, 2010 ; Zhang et al, 2017 ; Li et al, 2021 ). Interestingly, the preservation ( Bonilha et al, 2016 ) and recovery ( Caliandro et al, 2017 ; Li et al, 2021 ) of optimal small-world properties of the network correlate positively with the improvement of cognitive and motor functions, suggesting that small-world indices restoration could be a proxy for predicting neurological recovery ( Vecchio et al, 2019 ). Studies in animal models ( van Meer et al, 2012 ) have complemented these findings, showing that the initial small-worldness (an excessive clustering and wiring of the network) evolves to an optimal small-world topology in the chronic stage.…”

“…This damage to the cortical control network could disrupt a small-world organization, which has an impact on energy efficiency and the selective and flexible control ( Gerloff and Hallett, 2010 ; Rehme and Grefkes, 2013 ; Li et al, 2021 ).…”