Brain white matter plasticity and functional reorganization underlying the central pathogenesis of trigeminal neuralgia.

Tian Tian,Shun Zhang,Jing Xu,Jingjing Shi,Yuanyuan Qin,Linying Guo,Chengxia Liu,Wenzhen Zhu

doi:10.1038/srep36030

Tian Tian, Shun Zhang + Show 6 more

Open Access

https://doi.org/10.1038/srep36030

Copy DOI

Abstract

Peripheral nerve damage does not fully explain the pathogenesis of trigeminal neuralgia (TN). Central nervous system changes can follow trigeminal nerve dysfunction. We hypothesized that brain white matter and functional connectivity changes in TN patients were involved in pain perception, modulation, the cognitive-affective system, and motor function; moreover, changes in functional reorganization were correlated with white matter alterations. Twenty left TN patients and twenty-two healthy controls were studied. Diffusion kurtosis imaging was analyzed to extract diffusion and kurtosis parameters, and functional connectivity density (FCD) mapping was used to explore the functional reorganization in the brain. In the patient group, we found lower axial kurtosis and higher axial diffusivity in tracts participated in sensory, cognitive-affective, and modulatory aspects of pain, such as the corticospinal tract, superior longitudinal fasciculus, anterior thalamic radiation, inferior longitudinal fasciculus, inferior fronto-occipital fasciculus, cingulated gyrus, forceps major and uncinate fasciculus. Patients exhibited complex FCD reorganization of hippocampus, striatum, thalamus, precentral gyrus, precuneus, prefrontal cortex and inferior parietal lobule in multiple modulatory networks that played crucial roles in pain perception, modulation, cognitive-affective system, and motor function. Further, the correlated structural-functional changes may be responsible for the persistence of long-term recurrent pain and sensory-related dysfunction in TN.

Highlights

Many neuroimaging studies have used highly sensitive MRI methods to evaluate the structural or functional brain changes in Trigeminal neuralgia (TN) patients
There were no significant differences in fractional anisotropy (FA), radial diffusivity (RD), and mean diffusivity (MD) between the two groups
We found that the left hippocampus was a component of the reward-emotion network; that the caudate and putamen were parts of the striatal network; that the precuneus, bilateral prefrontal cortex (PFC), and right angular gyrus were parts of the default mode network (DMN); and that the right supramarginal gyrus was part of the sensorimotor network (SMN)

Summary

Introduction

Many neuroimaging studies have used highly sensitive MRI methods to evaluate the structural or functional brain changes in TN patients. Previous studies have addressed morphological changes occurring in grey matter volume[13] and in the cortical thickness of central structures[14,15] These abnormal brain regions in TN patients have been associated with pain perception, modulation, the cognitive-affective system, and motor function, further reflecting the maladaptive brain plasticity due to long-term nociceptive inputs. Functional connectivity density (FCD) mapping is a newly developed data-driven method to identify the distribution of functional connectivity regions in the human brain. This ultrafast technique allows the calculation of functional connectivity maps in brain networks, overcoming the limitations of seed-based approaches for functional study[25]. The correlated brain structural-functional changes may be responsible for the persistence of long-term recurrent pain and sensory-related dysfunction in TN patients

Methods

Results

Conclusion