Alterations of degree centrality and functional connectivity in classic trigeminal neuralgia

Abstract

Objectives: Recent neuroimaging studies have indicated a wide range of structural and regional functional alterations in patients with classic trigeminal neuralgia (CTN). However, few studies have focused on the intrinsic functional characteristics of network organization in the whole brain. Therefore, the present study aimed to characterize the potential intrinsic dysconnectivity pattern of the whole brain functional networks at the voxel level using the degree centrality (DC) analysis in CTN patients.

Methods: Thirty-four patients with CTN and twenty-nine well-matched healthy controls (HCs) participated in this study. All subjects underwent resting-state functional magnetic resonance imaging (rs-MRI) examination and clinical and neuropsychologic assessments. DC is a graph theory-based measurement that represents the overall functional connectivity (FC) numbers between one voxel and other brain voxels. We first investigated brain regions exhibiting abnormal DC, and further identified their perturbation on FC with other brain regions using a seed-based FC analysis in patients with CTN. In addition, correlation analyses were performed to evaluate the relationship between the abnormal DC value and clinical variables in CTN patients.

Results: Compared with the HCs, the patients with CTN exhibited significantly greater DC values in the right pallidum and right putamen, and lower DC values in the right lingual gyrus, right calcarine sulcus, left paracentral lobule, and left midcingulate cortex. A further seed-based FC analysis revealed that the right lingual gyrus showed decreased FC within the visual network and with other core brain networks, including the sensorimotor network, default mode network, and salience network, relative to HCs. Additionally, the left midcingulate cortex exhibited decreased FC within the middle cingulate cortex and the visual network in CTN patients. Moreover, the DC value in the left midcingulate cortex was negatively correlated with the illness duration.

Conclusion: The present study shows that CTN patients exhibited specific functional connectivity network alterations in the basal ganglia, visual network, and salience network, which may reflect the aberrant neural network communication in pain processing and modulation. These findings may provide novel insight for understanding the mechanisms of pain chronicity in CTN patients.

Keywords: classic trigeminal neuralgia; degree centrality; functional connectivity; neuropathic pain; resting-state functional MRI.

FIGURE 1

Altered DC in CTN patients. Compared with HCs, the patients with CTN showed greater DC values in the right pallidum and right putamen, and lower DC values in the right lingual gyrus, right calcarine sulcus, left paracentral lobule, and left midcingulate cortex (p < 0.05, FDR corrected). The warm colors indicate a higher DC value whereas the cooler colors indicate a lower DC value. The color bar indicates T-value. DC, degree centrality; CTN, classic trigeminal neuralgia; HCs, healthy control subjects; FDR, false discovery rate.

FIGURE 2

Altered right lingual gyrus FC in CTN patients. Compared with HCs, the CTN patients exhibited significantly decreased FC between the right lingual gyrus and sensorimotor network, default mode network, and salient network. The significance threshold was set at p < 0.05 with FDR correction (cluster extent threshold >100 voxels). The cooler colors indicate a lower FC value. The color indicates T-value. FC, functional connectivity; CTN, classic trigeminal neuralgia; HCs, healthy control subjects; FDR, false discovery rate.

FIGURE 3

Altered left midcingulate cortex FC in CTN patients. The CTN patients showed significantly decreased FC between the left midcingulate cortex and visual network, left paracentral lobule compared with HCs (p < 0.05, FDR corrected, cluster >100 voxels). FC, functional connectivity; CTN, classic trigeminal neuralgia; HCs, healthy control subjects; FDR, false discovery rate.

FIGURE 4

Correlation between DC alterations and clinical variables in CTN patients. DC in the left MCC was negatively associated with the illness duration. DC, degree centrality; CTN, classic trigeminal neuralgia; MCC, midcingulate cortex.