Nuancing the Limitations of Axonal Plasticity in World Health Organization Grade II Gliomas: White Matter Tracts Compensation Is Driven by Cortical Remodeling

Abstract

Diffuse World Health Organization grade II glioma (GIIG) is a slow-growing brain cancer that migrates along the white matter (WM) tracts. Neuroplastic changes were described in reaction to GIIG progression, opening the window to extensive cerebral surgical resection in patients able to resume an active life with no functional consequences. However, atlases of cortico-subcortical neural plasticity emphasized the limited potential of axonal reorganization. Yet, the removal of WM involved by GIIG can be possible, at least to some extent, without generating permanent neurological disturbances. Here, the aim was to discuss mechanisms underlying functional compensation which make feasible resection of the subcortical component of GIIG and to propose a new model of adaptative neural reconfiguration at the level of the axonal connectivity. In this model, 2 parts of the WM tracts are considered: (1) the stem of the bundle that represents the actual limitation of plastic potential, as supported by reproducible behavioral disorders elicited by intraoperative axonal electrostimulation mapping (ESM) and (2) the terminations/origins of the bundle that may no longer be critical in case of functional reallocation of the cortex to/from which these WM fibers run—thus inducing no behavioral troubles during direct ESM. Understanding that a certain degree of axonal compensation in specific portions of the tracts is driven by cortical remodeling may enable to rethink the concept of WM plasticity and to refine the preoperative estimation of extent of resection for GIIG. Identifying eloquent fibers by ESM, especially their convergence in the depth, is essential to achieve an individualized connectome-based resection.