Resting state network plasticity related to picture naming in low-grade glioma patients before and after resection

Abstract

The dynamic connectome perspective states that brain functions arise from the functional integration of distributed and/or partly overlapping networks. Diffuse low-grade gliomas (DLGG) have a slow infiltrating character. Here we addressed whether and how anatomical disconnection following DLGG growth and resection might interfere with functional resting-state connectivity, specifically in relation to picture naming. Thirty-nine native French persons with a left DLGG were included. All underwent awake surgical resection of the tumor using direct brain electrostimulation to preserve critical eloquent regions. The anatomical disconnectivity risk following the DLGG volume and the resection, and the functional connectivity of resting-state fMRI images in relation to picture naming were evaluated prior to and three months after surgery. Resting-state connectivity patterns were compared with nineteen healthy controls. It was demonstrated that picture naming was strongly dependent on the semantic network that emerged from the integration and interaction of regions within multiple resting-state brain networks, in which their specific role could be explained in the light of the broader resting-state network they take part in. It emphasized the importance of a whole brain approach with specific clinical data input, during resting-state analysis in case of lesion. Adaptive plasticity was found in secondary regions, functionally connected to regions close to the tumor and/or cavity, marked by an increased connectivity of the right and left inferior parietal lobule with the left inferior temporal gyrus. In addition, an important role was identified for the superior parietal lobe, connected with the frontal operculum, suggesting functional compensation by means of attentional resources in order to name a picture via recruitment of the frontoparietal attention network.

Keywords: Connectivity; Glioma; Neurosurgery; Picture naming; Plasticity; Resting state.

Fig. 1

DLGG location density plot, with (a) Sum of DLGG masks pre-surgery, (b) sum of DLGG masks resection and (c) sum of DLGG masks residue. Each voxel's alue corresponds to the number of tumors in the specific location.

Fig. 2

Schematic representation of main functional connectivity (FC) patterns based on the four key-nodes that showed altered connectivity in relation to better picture naming (++ DO80) performance post-surgery (blue connections) as well as those that are different to controls (red connections). STG = superior temporal gyrus, ITG = inferior temporal gyrus. IPL = inferior parietal lobule. MFG = middle fonrtal gyrus, SPG = superior parietal lobule, ⇑ = increased (solid line), ⇓ = decreased (dotted line) connectivity, P = patients, C = Controls, LH = left-hemisphere, RH = right-hemisphere. Fig. 2a: altered connectivity of the STG. Fig. 2b: altered connectivity of the left MFG. Fig. 2c: altered connectivity of the network involving the right IPL. Fig. 2d: altered connectivity of the right SPL. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)