Contralesional Sensorimotor Network Participates in Motor Functional Compensation in Glioma Patients

Abstract

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.

Keywords: brain reorganization; glioma; graph theory; resting-state functional magnetic resonance images; topological property.

Figure 1

Tumor location and global properties of patients with left hemispheric gliomas. (A) Overlapping results of gliomas in the left hemisphere. The value of the color bar represents the number of patients with tumors located in a same region. (B) Differences in global topological properties of the sensorimotor network in the contralesional hemisphere among the three groups.

Figure 2

Tumor location and global properties of patients with right hemispheric gliomas. (A) Overlapping results of gliomas in the right hemisphere. The value of the color bar represents the number of patients with tumors located in a same region. (B) Differences in global topological properties of the sensorimotor network in the contralesional hemisphere among the three groups.

Figure 3

Differences in nodal topological properties of the sensorimotor network in the contralesional hemisphere among the three groups, with left hemisphere glioma. Orange node (No. 1), caudal dorsolateral Brodmann area (BA) 6 (A6cdl); pink node (No. 2), upper limb of BA 4 (A4ul); red node (No. 3), tongue and larynx of BA 4 (A4tl); light blue node (No. 4), lower limb region of BA 4 (A4ll); green node (No. 5), upper limb, head, and face regions of BA 1/2/3 (A1/2/3ulhf); purple node (No. 6), tongue and larynx of BA 1/2/3 (A1_2_3tonIa); and dark blue node (No. 7), premotor-related thalamus (mPMtha).

Figure 4

Differences in nodal topological properties of the sensorimotor network in the contralesional hemisphere among the three groups, with right hemisphere glioma. Orange node (No. 1), caudal dorsolateral Brodmann area (BA) 6 (A6cdl); pink node (No. 2), upper limb of BA 4 (A4ul); red node (No. 3), tongue and larynx of BA 4 (A4tl); light blue node (No. 4), lower limb region of BA 4 (A4ll); green node (No. 5), upper limb, head, and face regions of BA 1/2/3 (A1/2/3ulhf); purple node (No. 6), tongue and larynx of BA 1/2/3 (A1_2_3tonIa); yellow node (No. 7), trunk region of BA 1/2/3 (A1_2_3tru); and dark blue node (No. 8), premotor-related thalamus (mPMtha).