Abstract

Simple SummaryBeyond intraoperative electrostimulation mapping in awake patients (the gold-standard for brain tumor surgery), non-invasive FNI/TMS can be repeated before and after resection(s). These techniques enable longitudinal investigation of neural reorganization, especially in low-grade gliomas, which can generate neuroplasticity in patients with usually no or slight neurological deficits, despite neoplasm within “eloquent” structures. Here, data gained from perioperative FNI/TMS mapping methods are reviewed, in order to decipher mechanisms underpinning functional cerebral reshaping induced by the tumor and its possible relapse, (re)operation(s), and postoperative rehabilitation. Heterogeneous spatiotemporal patterns of rearrangement across patients and in a single patient over time were evidenced, with structural changes as well as modifications of intra-hemispheric and inter-hemispheric functional connectivity. Such various fingerprints of neural reconfiguration were correlated to different levels of cognitive compensation. Serial multimodal studies exploring neuroplasticity might lead to new management strategies based upon multistage therapeutic approaches adapted to the individual profile of functional reallocation.Intraoperative direct electrostimulation mapping (DEM) is currently the gold-standard for glioma surgery, since functional-based resection allows an optimization of the onco-functional balance (increased resection with preserved quality of life). Besides intrasurgical awake mapping of conation, cognition, and behavior, preoperative mapping by means of functional neuroimaging (FNI) and transcranial magnetic stimulation (TMS) has increasingly been utilized for surgical selection and planning. However, because these techniques suffer from several limitations, particularly for direct functional mapping of subcortical white matter pathways, DEM remains crucial to map neural connectivity. On the other hand, non-invasive FNI and TMS can be repeated before and after surgical resection(s), enabling longitudinal investigation of brain reorganization, especially in slow-growing tumors like low-grade gliomas. Indeed, these neoplasms generate neuroplastic phenomena in patients with usually no or only slight neurological deficits at diagnosis, despite gliomas involving the so-called “eloquent” structures. Here, data gained from perioperative FNI/TMS mapping methods are reviewed, in order to decipher mechanisms underpinning functional cerebral reshaping induced by the tumor and its possible relapse, (re)operation(s), and postoperative rehabilitation. Heterogeneous spatiotemporal patterns of rearrangement across patients and in a single patient over time have been evidenced, with structural changes as well as modifications of intra-hemispheric (in the ipsi-lesional and/or contra-lesional hemisphere) and inter-hemispheric functional connectivity. Such various fingerprints of neural reconfiguration were correlated to different levels of cognitive compensation. Serial multimodal studies exploring neuroplasticity might lead to new management strategies based upon multistage therapeutic approaches adapted to the individual profile of functional reallocation.

Highlights

  • The main purpose in glioma surgery is to optimize the extent of resection (EOR) while preserving or even improving the quality of life (QoL)

  • Regarding diffusion tractography imaging (DTI), beyond its high false-positive rate evidenced by an international tractography investigation [8], due to a marked inter-algorithm variability, especially in glioma patients [9], this technique is intrinsically a structural imaging modality not able to map the function of white matter (WM) tracts

  • With the ultimate goal to predict before surgery how the brain will be able to dynamically reshape according to the EOR achieved at the expense of interactive cortico-subcortical networks in a given patient at this moment, perioperative non-invasive functional neuroimaging (FNI) and transcranial magnetic stimulation (TMS)

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Summary

Introduction

The main purpose in glioma surgery is to optimize the extent of resection (EOR) while preserving or even improving the quality of life (QoL). The principle is to identify and preserve the eloquent neural networks subserving movement execution and control, visuospatial function, language, cognition (e.g., attention, semantics, or executive functions), and behavior (e.g., theory of mind), by means of direct electrostimulation mapping (DEM) in awake patients, at both cortical and axonal levels [13] This original philosophy resulted in a significant increase of survival and a decrease of disabling persistent deficits, including for gliomas within structures previously considered inoperable [14]. Another atlas of essential nodal architecture of the connectome was elaborated, reporting a normalized dataset of 1821 cortical and subcortical functional DEM-driven responses collected in awake LGG patients, and revealing the critical structures in 16 functional domains [30] These atlases may be helpful for preoperative planning of glioma resection, to distinguish compensable areas hat can be removed from critical areas that must be spared. With the ultimate goal to predict before surgery how the brain will be able to dynamically reshape (or not) according to the EOR achieved at the expense of interactive cortico-subcortical networks in a given patient at this moment, perioperative non-invasive FNI and TMS mapping may provide unique information based upon longitudinal investigations, complementary to the intrasurgical DEM data, which can be collected only in real time within the operating theater

Preoperative Structural Changes in Glioma Patients
Preoperative Reorganization of the Motor Network
Preoperative Reorganization of the Language Network
Preoperative Reorganization of Other Networks
Functional Compensation after LGG Surgery
Postoperative Reorganization of Motor Network
Serial fMRI before and after
Postoperative Reorganization of the Language Network
Findings
Conclusions and Perspectives
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