Contralesional macrostructural plasticity of the insular cortex in patients with glioma

Abstract

ObjectiveTo assess the homotopic structural plasticity in case of unilateral damage of the insula.MethodsTo detect changes in gray matter volumes of the contralesional insula from structural MRIs, we used voxel-based morphometry (VBM) in a sample of 84 patients with a diffuse low-grade glioma invading the left insula (insL group; n = 47) or the right insula (insR group; n = 37).ResultsThe region of interest–based VBM analysis highlighted a large cluster of voxels with gray matter volume increase in the contralesional insula in both patient groups (k = 2,214 voxels for insL and k = 879 voxels for insR, p < 0.05, family-wise error corrected) compared with 24 age-matched healthy controls. Gray matter volume was increased for the entire insula (t69 = 3.63, p = 0.0016 for insL; t59 = 3.54, p = 0.0024 for insR, Bonferroni corrected), whereas no significant changes were found in 2 control regions for both patient groups. Furthermore, an increase of 24.6% and 31.6% in the gray matter volume was observed in the insula-related VBM cluster for insL and insR patients, respectively, compared with healthy controls (t69 = 7.39, p = 2.59 × 10−10 and t59 = 7.51, p = 3.61 × 10−10).ConclusionsThe reported results demonstrate that slow-growing but massive lesion infiltration of the insula induces marked increase of gray matter volume in the contralateral one. Our findings give support for a homotopic reorganization that might be a physiologic basis for the high level of functional compensation observed in patients with glioma.

Restructuring of contralateral gray matter volume associated with cognition in patients with unilateral temporal lobe glioma before and after surgery

“…Some studies have suggested that localized tumors can affect the function of distant part of the brain (Liu et al, 2019;Park, Kim, Kim, Kim, & Shim, 2015;Zhang et al, 2016). Indeed, structural changes in the regions distant from brain tumor have also been confirmed by some studies (Almairac et al, 2018;Bouwen et al, 2018). These structural changes have been correlated with cognition decline (Bouwen et al, 2018), though cognitive functions are not always caused by the alternation in the brain, sometimes the cognitive function recovers over time (Voytek et al, 2010), which may be attributed to the brain plasticity.…”

“…Therefore, the present study was initiated to investigate the alteration in contralateral GM volume before and after surgery, and the relationship between the alterations in contralateral GM volume with cognitive function in unilateral temporal lobe glioma patients. We hypothesized that contralateral GM volume compensates for damaged glioma and the compensatory brain structure may be a structural basis of cognitive function compensation (Almairac et al, ; Bouwen et al, ; Duffau, ; Duffau, ).…”

“…Currently, surgical resection, followed by radiation therapy and adjuvant chemotherapy is the standard of care for patients with glioma (Duffau & Taillandier, 2015); however, in spite of these treatments, 5-year survival rates (5%) remain poor (Ghinda, Wu, Duncan, & Northoff, 2018). To our knowledge, focal deficits caused by glioma are not restricted to the area where the tumor is located and where it has caused local damage; however, it may impact the global dysfunctioning of the brain (Almairac, Duffau, & Herbet, 2018;Hart, Romero-Garcia, Price, & Suckling, 2019;Maesawa et al, 2015). Some studies have suggested that localized tumors can affect the function of distant part of the brain (Liu et al, 2019;Park, Kim, Kim, Kim, & Shim, 2015;Zhang et al, 2016).…”

“…This method has been successfully used to detect structural changes of cerebral GM and WM in patients with Alzheimer's disease, acute focal cerebral infarction and depression (Ashburner & Friston, 2000;Dang et al, 2013;Liu et al, 2014;Matsuda, 2016). Furthermore, Almairac et al found that patients with unilateral insular low-grade glioma exhibited noticeable increase in GM volume only in the contralateral insular lobe (Almairac et al, 2018), indicating a plastic compensatory mechanism in the distant brain regions. Conceivably, these changes in human brain may be related to cognitive changes in patients with glioma (Derks, Reijneveld, & Douw, 2014).…”

“…We hypothesized that contralateral GM volume compensates for damaged glioma and the compensatory brain structure may be a structural basis of cognitive function compensation (Almairac et al, 2018;Bouwen et al, 2018;Duffau, 2005;Duffau, 2006…”