Functional Mapping before and after Low-Grade Glioma Surgery: A New Way to Decipher Various Spatiotemporal Patterns of Individual Neuroplastic Potential in Brain Tumor Patients

Abstract

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.

Contralesional functional network reorganization of the insular cortex in diffuse low-grade glioma patients

“…Since, the glioma is commonly thought to disrupt functional networks and decrease FC 25,32,33 . Hence, the increasing FC implied that network reorganization occurred similar to what other studies have shown 3,10,19,20 . No significant sensorimotor and abnormal mental status were found in our patients.…”

“…However, this does not mean that the insular lobe is insignificant. The reason for the lack of serious neurological deficits is thought to be related to an increase in contralesional homotopic compensation that frequently increases functional connectivity (FC) in the contralesional hemisphere accompanied with decreases in FC within the ipsilateral damaged network 2,19 . A previous study indicated that diffuse insular low-grade gliomas (DLGGs) cause contralateral hemispheric compensation by increasing the volume of the contralateral insular cortex 11 .…”

Role of Preoperative Assessment in Predicting Tumor-Induced Plasticity in Patients with Diffuse Gliomas

“…A careful preoperative assessment seems of paramount importance to identify good candidates for the surgery and tailor brain mapping at the individual scale [ 20 , 62 , 63 ]. Several studies suggest that the local growth of gliomas affect the global brain functional organization by causing impaired communication of large-scale networks for cognition and behavior [ 2 , 64 ]. The insult to the subcortical white matter structural connectivity is correlated with a decline in cognitive functions, confirming that axonal bundles represent a major limitation in neuroplasticity [ 64 , 65 ].…”

Brain Mapping-Aided SupraTotal Resection (SpTR) of Brain Tumors: The Role of Brain Connectivity

“…This opens up the doors to the concept of onco-functional balance. According to this, surgical resection is guided by pre-operative assessment and intraoperative functional mapping and it takes account of the considerable structural-functional variability and the individual neural dynamics across glioma patients, in order to significantly increase patient’s OS and to decrease the rate of neurological impairments and the consequent disability ( 17 , 29 ). This rising concept paves the way even for the treatment of tumors within brain structures previously considered inoperable ( 17 ).…”

“…A careful preoperative selection of patients who can benefit from surgery is mandatory in order to meet the most favorable onco-functional balance ( 17 ).…”