Abstract
Cerebral lesions may cause degeneration and neuroplastic reorganization in both the ipsi- and the contralesional hemisphere, presumably creating an imbalance of primarily inhibitory interhemispheric influences produced via transcallosal pathways. The two hemispheres are thought to mutually hamper neuroplastic reorganization of the other hemisphere. The results of preceding degeneration and neuroplastic reorganization of white matter may be reflected by Diffusion Tensor Imaging-derived diffusivity parameters such as fractional anisotropy (FA). In this study, we applied Diffusion Tensor Imaging (DTI) to contrast the white matter status of the contralesional hemisphere of young lesioned brains with and without contralateral influences by comparing patients after hemispherotomy to those who had not undergone neurosurgery. DTI was applied to 43 healthy controls (26 females, mean age ± SD: 25.07 ± 11.33 years) and two groups of in total 51 epilepsy patients with comparable juvenile brain lesions (32 females, mean age ± SD: 25.69 ± 12.77 years) either after hemispherotomy (30 of 51 patients) or without neurosurgery (21 of 51 patients), respectively. FA values were compared between these groups using the unbiased tract-based spatial statistics approach. A voxel-wise ANCOVA controlling for age at scan yielded significant group differences in FA. A post hoc t-test between hemispherotomy patients and healthy controls revealed widespread supra-threshold voxels in the contralesional hemisphere of hemispherotomy patients indicating comparatively higher FA values (p < 0.05, FWE-corrected). The non-surgery group, in contrast, showed extensive supra-threshold voxels indicating lower FA values in the contralesional hemisphere as compared to healthy controls (p < 0.05, FWE-corrected). Whereas lower FA values are suggestive of pronounced contralesional degeneration in the non-surgery group, higher FA values in the hemispherotomy group may be interpreted as a result of preceding plastic remodeling. We conclude that, whether juvenile brain lesions are associated with contralesional degeneration or reorganization partly depends on the ipsilesional hemisphere. Contralesional reorganization as observed in hemispherotomy patients was most likely enabled by the complete neurosurgical deafferentation of the ipsilesional hemisphere and, thereby, the disinhibition of the neuroplastic potential of the contralesional hemisphere. The main argument of this study is that hemispherotomy may be seen as a major plastic stimulus and as a prerequisite for contralesional neuroplastic remodeling in patients with juvenile brain lesions.
Highlights
Cerebral lesions may cause two types of structural changes in the brain: degeneration and neuroplastic reorganization (Rossini et al, 2003; Murphy and Corbett, 2009; Dodd et al, 2017)
The voxel-wise analysis of covariance (ANCOVA) controlling for scanner update and age at scan as covariates yielded significant effects of the group factor (p < 0.05): clusters were widely distributed in the contralesional hemisphere, whereas they only covered frontal areas and cerebral peduncle in the lesional hemisphere
Clusters indicating comparatively higher fractional anisotropy (FA) values in the hemispherotomy group were only found in small parts of the brainstem
Summary
Cerebral lesions may cause two types of structural changes in the brain: degeneration and neuroplastic reorganization (Rossini et al, 2003; Murphy and Corbett, 2009; Dodd et al, 2017) Both degeneration and neuroplastic reorganization can occur in the ipsilesional hemisphere or the contralesional, intact hemisphere (Buetefisch, 2015; Dodd et al, 2017). We used DTI to evaluate contralesional white matter changes after extended unilateral early brain lesions in the absence or presence of the ipsilesional hemisphere by comparing epilepsy patients who had undergone transsylvian functional hemispherotomy (hemispherotomy group) to nonsurgical patients with similar pathologies (non-surgery group). That neuroplastic reorganization as indicated by higher FA could be observed in both patient groups, but was more pronounced in the hemispherotomy group, and within this group, in patients with earlier disease onset
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