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Review
. 2022 Mar 2:12:855587.
doi: 10.3389/fonc.2022.855587. eCollection 2022.

White Matter Tracts and Diffuse Lower-Grade Gliomas: The Pivotal Role of Myelin Plasticity in the Tumor Pathogenesis, Infiltration Patterns, Functional Consequences and Therapeutic Management

Hugues Duffau  1   2
Affiliations
Review

White Matter Tracts and Diffuse Lower-Grade Gliomas: The Pivotal Role of Myelin Plasticity in the Tumor Pathogenesis, Infiltration Patterns, Functional Consequences and Therapeutic Management

Hugues Duffau. Front Oncol. .

Abstract

For many decades, interactions between diffuse lower-grade glioma (LGG) and brain connectome were neglected. However, the neoplasm progression is intimately linked to its environment, especially the white matter (WM) tracts and their myelin status. First, while the etiopathogenesis of LGG is unclear, this tumor seems to appear during the adolescence, and it is mostly located within anterior and associative cerebral areas. Because these structures correspond to those which were myelinated later in the brain maturation process, WM myelination could play a role in the development of LGG. Second, WM fibers and the myelin characteristics also participate in LGG diffusion, since glioma cells migrate along the subcortical pathways, especially when exhibiting a demyelinated phenotype, which may result in a large invasion of the parenchyma. Third, such a migratory pattern can induce functional (neurological, cognitive and behavioral) disturbances, because myelinated WM tracts represent the main limitation of neuroplastic potential. These parameters are critical for tailoring an individualized therapeutic strategy, both (i) regarding the timing of active treatment(s) which must be proposed earlier, before a too wide glioma infiltration along the WM bundles, (ii) and regarding the anatomic extent of surgical resection and irradiation, which should take account of the subcortical connectivity. Therefore, the new science of connectomics must be integrated in LGG management, based upon an improved understanding of the interplay across glioma dissemination within WM and reactional neural networks reconfiguration, in order to optimize long-term oncological and functional outcomes. To this end, mechanisms of activity-dependent myelin plasticity should be better investigated.

Keywords: brain connectome; brain mapping; cognition; lower-grade glioma; myelin; neural networks; neuroplasticity; white matter tracts.

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Conflict of interest statement

The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Correlations between the degree of infiltration of WM tracts by the LGG and cognitive deteriorations: (A) Preoperative voxel-based lesion symptom map for semantic fluency, evidencing significant relationship between the inferior fronto-occipital fasciculus infiltrated voxels by LGG and deficit of language semantics [from (78) with permission]; (B) Voxel-based lesion symptom of postsurgical lasting anomia performed on residual infiltration map, showing correlations between postoperative lexical retrieval troubles and LGG invasion of the left inferior longitudinal fasciculus [from (79) with permission]; (C) Significant relationship between postoperative residual tumor volume in the arcuate fasciculus and decreased low-level mentalizing accuracy [from (80) with permission]; (D) Disconnectome analysis demonstrating a significant link between postoperative persistent deficit of executive functions and the residual LGG infiltration volume in the superior longitudinal fasciculus [from (81) with permission]. ***Statistically significant.
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