Decreasing Shortest Path Length of the Sensorimotor Network Induces Frontal Glioma-Related Epilepsy

Abstract

BackgroundGlioma-related epilepsy (GRE) is a common symptom in patients with prefrontal glioma. Epilepsy onset is associated with functional network alterations. This study investigated alterations of functional networks in patients with prefrontal glioma and GRE.MethodsSixty-five patients with prefrontal lobe gliomas were retrospectively assessed and classified into GRE and non-GRE groups. Additionally, 25 healthy participants were enrolled after matching for general information. Imaging data were acquired within 72 h in pre-operation. The sensorimotor network was used to delineate alterations in functional connectivity (FC) and topological properties. One-way analysis of variance and post-hoc analysis with Bonferroni correction were used to calculate differences of FC and topological properties.ResultsAll significant alterations were solely found in the sensorimotor network. Irrespective of gliomas located in the left or right prefrontal lobes, the edge between medial Brodmann area 6 and caudal ventrolateral Brodmann area 6 decreased FC in the GRE group compared with the non-GRE group [p < 0.0001 (left glioma), p = 0.0002 (right glioma)]. Moreover, the shortest path length decrease was found in the GRE group compared with the non-GRE group [p = 0.0292 (left glioma) and p = 0.0129 (right glioma)].ConclusionsThe reduction of FC between the medial BA 6 (supplementary motor area) and caudal ventrolateral BA 6 in the ipsilateral hemisphere and the shortening of the path length of the sensorimotor network were characteristics alterations in patients with GRE onset. These findings fill in the gap which is the relationship between GRE onset and the alterations of functional networks in patients with prefrontal glioma.Significance StatementGlioma related epilepsy is the most common symptom of prefrontal glioma. It is important to identify characteristic alterations in functional networks in patients with GRE. We found that all significant alterations occurred in the sensorimotor network. Moreover, a decreased FC in the supplementary motor area and a shortening of the path’s length are additional characteristics of glioma-related epilepsy. We believe that our findings indicate new directions of research that will contribute to future investigations of glioma-related epilepsy onset.

Altered Structural and Functional Patterns Within Executive Control Network Distinguish Frontal Glioma-Related Epilepsy

“…Furthermore, some studies suggest that tumor invasion affects brain function over the whole network rather than isolated regions ( Vigneau et al, 2006 ; Xiang et al, 2010 ; Briganti et al, 2012 ). In particular, some studies indicated that tumor-related epilepsy induces topological changes in WM networks ( Zhou et al, 2022 ) and functional networks ( Fang et al, 2022 ). Therefore, the network-based features and the structural features outside the tumor lesion can reflect more information about glioma-related epilepsy.…”

“…Tumor invasion of the frontal lobe induces changes in the executive control network (ECN) ( Liu Y. et al, 2020 ). Similarly, the onset of epilepsy also leads to functional network alterations ( Cao et al, 2014 ; Fang et al, 2022 ). Therefore, an in-depth understanding of the structural and functional patterns of the ECN in glioma-associated epilepsy is required for the early differentiation and diagnosis of glioma seizures and the development of individualized intervention strategies.…”

“…Furthermore, idiopathic epilepsy reduces FC in networks (such as the salience network, default network, and ECN) ( Cao et al, 2014 ; Li et al, 2017 ). In particular, some studies indicate that tumor-related epilepsy induces topological changes in white matter (WM) networks ( Zhou et al, 2022 ) and functional networks ( Fang et al, 2022 ). Based on these findings, we hypothesize that tumor invasion of the frontal lobe, accompanied by epileptic seizures, will lead to disruption and reorganization of the ECN.…”

Neuroplasticity of Glioma Patients: Brain Structure and Topological Network

“…In addition, the changes in cerebral network caused by glioma and GRE are not completely clear. Around frontal and temporal GRE and in regard to graph theory analysis based on rs-fMRI, Fang et al found that both frontal lobe and temporal lobe GRE will cause changes in the topological properties of brain functions, and temporal lobe GRE can cause changes in the topological properties of visual networks (80) and language networks (81); prefrontal lobe GRE can cause changes in the topological properties of sensorimotor networks (82). Meanwhile, Zhou et al (83) identified altered topological properties of epilepsy-related white matter network in patients with frontal glioma.…”

Altering patterns of sensorimotor network in patients with different pathological diagnoses and glioma‐related epilepsy under the latest glioma classification of the central nervous system

“…Previous studies 9–12 have demonstrated that different tumor locations cause alterations in different functional networks near the tumor. For instance, increased functional connectivity (FC) of nodes located in the premotor area and decreased shortest path length of the sensorimotor network are specific alterations in patients with prefrontal glioma and GRE onset 13 …”