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.

AIMS: We aimed to clarify the relationship between alterations in functional networks and glioma-related epilepsy (GRE) in patients with different molecular diagnoses. METHODS: We enrolled 160 patients with prefrontal gliomas and different histories of GRE. The patients were grouped based on the latest pathological glioma classification and GRE history. Graph theory analysis was applied to reveal alterations in the sensorimotor networks among various subgroups. Binary logistic regression was used to identify risk factors for preoperative GRE onset. RESULTS: Decreasing shortest path length was found in patients with GRE, regardless of the chromosome 1p/19q status. Nodes located in the premotor and supplementary motor areas showed decreased nodal betweenness centrality and vulnerability in patients with GRE and chromosome 1p/19q intact. Additionally, the node on the primary motor area showed decreased nodal vulnerability but the node on the sensory-related thalamus increased in patients with GRE and chromosome 1p/19q co-deletion. Decreased shortest path length, grade 2, and decreased nodal betweenness centrality of the premotor area were risk factors for GRE. CONCLUSION: Decreased shortest path length was a characteristic alteration in GRE and prefrontal glioma. Alterations in global properties were similar, but nodal properties were different in patients with GRE and different chromosome 1p/19q statuses.

Association of homotopic areas in the right hemisphere with language deficits in the short term after tumor resection.

OBJECTIVE: It is important to identify language deficit and recovery in the week following a tumor resection procedure. The homotopic Broca's area and the superior longitudinal fasciculus in the right hemisphere participate in language functional compensation. However, the nodes in these structures, as well as their contributions to language rehabilitation, remain unknown. In this study, the authors investigated the association of homotopic areas in the right hemisphere with language deficit. METHODS: The authors retrospectively reviewed the records of 50 right-handed patients with left hemispheric lower-grade glioma that had been surgically treated between June 2020 and May 2022. The patients were divided into normal and aphasia groups based on their postoperative aphasia quotient (AQ) from the Western Aphasia Battery. Preoperative (within 24 hours before surgery) and postoperative (7 days after tumor resection) diffusion tensor images were used to reveal alterations of structural networks by using graphic theory analysis. The shortest distance between the glioma and the nodes belonging to the language network (SDTN) was quantitatively assessed. Pearson's correlation and causal mediation analyses were used to identify correlations and mediator factors among SDTN, topological properties, and AQs. RESULTS: Postoperative nodal local efficiency of the node dorsal Brodmann area (BA) 44 (A44d; p = 0.0330), nodal clustering coefficient of the nodes A44d (p = 0.0402) and dorsal lateral BA6 (A6dl; p = 0.0097), and nodal degree centrality (p = 0.0058) of the node medial BA7 (A7m) were higher in the normal group than in the aphasia group. SDTN was positively correlated with postoperative AQ (r = 0.457, p = 0.0009) and ΔAQ (r = 0.588, p < 0.0001). The nodal local efficiency of node A44d and the nodal efficiency, nodal betweenness centrality, and degree centrality of node A7m were mediators of SDTN and postoperative AQs. CONCLUSIONS: The decreased ability of nodes A44d, A6dl, and A7m to convey information in the right hemisphere was associated with short-term language deficits after tumor resection. A smaller SDTN induced a worsened postoperative language deficit through a significant decrease in the ability to convey information from these three nodes.

Decreasing distance from tumor to the language network causes language deficit.

Preoperative language deficits are associated with alterations in the language networks of patients with gliomas. This study investigated how gliomas affect language performance by altering the language network. Ninety patients with lower-grade gliomas were included, and their preoperative language performance was evaluated using the Western Aphasia Battery. We also calculated the topological properties based on resting state functional magnetic resonance imaging. All patients were classified according to aphasia quotient (AQ) into the aphasia (AQ < 93.8), mild anomia (AQ > 93.8 and naming section <9.8), and normal groups (AQ > 93.8). The shortest distance from the tumor to the language network (SDTN) was evaluated to identify the effect on language performance induced by the tumor. One-way analysis of variance and post hoc analysis with Sidak correction were used to analyze the differences in topological properties among the three groups. Causal mediation analysis was used to identify indirectly affected mediators. Compared with the mild anomia group, longer shortest path length (p = .0016), lower vulnerability (p = .0331), and weaker nodal efficiencies of three nodes (right caudal Brodmann area [BA] 45, right caudal BA 22, and left BA 41/42, all p < .05) were observed in the aphasia group. The SDTN mediated nodal degree centrality and nodal vulnerability (left rostroventral BA 39), which negatively affected the AQs. Conventional language eloquent and mirrored areas participated in the language network alterations induced by gliomas. The SDTN was a mediator that affected the preoperative language status in patients with gliomas.

Contralesional Cortical and Network Features Associated with Preoperative Language Deficit in Glioma Patients.

Lower-grade Gliomas anchored in eloquent areas cause varying degrees of language impairment. Except for a tumor's features, contralesional compensation may explain these differences. Therefore, studying changes in the contralateral hemisphere can provide insights into the underlying mechanisms of language function compensation in patients with gliomas. This study included 60 patients with eloquent-area or near-eloquent-area gliomas. The participants were grouped according to the degree of language defect. T1 and diffusion tensor imaging were obtained. The contralesional cortical volume and the subcortical network were compared between groups. Patients with unimpaired language function showed elevated cortical volume in the midline areas of the frontal and temporal lobes. In subcortical networks, the group also had the highest global efficiency and shortest global path length. Ten nodes had intergroup differences in nodal efficiency, among which four nodes were in the motor area and four nodes were in the language area. Linear correlation was observed between the efficiency of the two nodes and the patient's language function score. Functional compensation in the contralesional hemisphere may alleviate language deficits in patients with gliomas. Structural compensation mainly occurs in the contralesional midline area in the frontal and temporal lobes, and manifests as an increase in cortical volume and subcortical network efficiency.

Contralesional Sensorimotor Network Participates in Motor Functional Compensation in Glioma Patients.

Background: Some gliomas in sensorimotor areas induce motor deficits, while some do not. Cortical destruction and reorganization contribute to this phenomenon, but detailed reasons remain unclear. This study investigated the differences of the functional connectivity and topological properties in the contralesional sensorimotor network (cSMN) between patients with motor deficit and those with normal motor function. Methods: We retrospectively reviewed 65 patients (32 men) between 2017 and 2020. The patients were divided into four groups based on tumor laterality and preoperative motor status (deficit or non-deficit). Thirty-three healthy controls (18 men) were enrolled after matching for sex, age, and educational status. Graph theoretical measurement was applied to reveal alterations of the topological properties of the cSMN by analyzing resting-state functional MRI. Results: The results for patients with different hemispheric gliomas were similar. The clustering coefficient, local efficiency, transitivity, and vulnerability of the cSMN significantly increased in the non-deficit group and decreased in the deficit group compared to the healthy group (p < 0.05). Moreover, the nodes of the motor-related thalamus showed a significantly increased nodal efficiency and nodal local efficiency in the non-deficit group and decreased in the deficit group compared with the healthy group (p < 0.05). Conclusions: We posited the existence of two stages of alterations of the preoperative motor status. In the compensatory stage, the cSMN sacrificed stability to acquire high efficiency and to compensate for impaired motor function. With the glioma growing and the motor function being totally damaged, the cSMN returned to a stable state and maintained healthy hemispheric motor function, but with low efficiency.

Increasing nodal vulnerability and nodal efficiency implied recovery time prolonging in patients with supplementary motor area syndrome.

Supplementary motor area (SMA) syndrome is a surgery-related complication that commonly occurs after removing SMA glioma, and needs weeks to recover. However, susceptible factors of patients suffering from SMA syndrome remain unknown. Graphic theory was applied to reveal topological properties of sensorimotor network (SMN) by processing resting-state functional magnetic resonance images in 66 patients with SMA gliomas. Patients were classified into SMA and non-SMA groups based on whether they suffered from SMA syndrome. We collected recovery time and used causal mediation analysis to find association between topological properties and recovery time. Compared with the non-SMA group, higher vulnerability (left: p = .0018; right: p = .0033) and lower fault tolerance (left: p = .0022; right: p = .0248) of the whole SMN were found in the SMA group. Moreover, higher nodal properties of lesional-hemispheric cingulate cortex (nodal efficiency: left, p = .0389; right, p = .0169; nodal vulnerability: left, p = .0185; right, p = .0085) and upper limb region of primary motor cortex (PMC; nodal efficiency: left, p = .0132; right, p = .0001; nodal vulnerability: left, p = .0091; right, p = .0209) were found in the SMA group. Nodal efficiency and nodal vulnerability of cingulate cortex and upper limb region of PMC were important predictors for SMA syndrome occurring and recovery time prolonging. Neurosurgeons should carefully deal with upper limb region of PMC and cingulate cortex, and protect them if these two region were unnecessary to damage during SMA glioma resection.

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

BACKGROUND: Glioma-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. METHODS: Sixty-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. RESULTS: All 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)]. CONCLUSIONS: The 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 STATEMENT: Glioma 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.

Intra-operative mapping and language protection in glioma.

ABSTRACT: The demand for acquiring different languages has increased with increasing globalization. However, knowledge of the modification of the new language in the neural language network remains insufficient. Although many details of language function have been detected based on the awake intra-operative mapping results, the language neural network of the bilingual or multilingual remains unclear, which raises difficulties in clinical practice to preserve patients' full language ability in neurosurgery. In this review, we present a summary of the current findings regarding the structure of the language network and its evolution as the number of acquired languages increased in glioma patients. We then discuss a new insight into the awake intra-operative mapping protocol to reduce surgical risks during the preservation of language function in multilingual patients with glioma.