Abnormal brain spontaneous neural activity in neuromyelitis optica spectrum disorder with neuropathic pain

Gendi Wang; Xiang Chen; Xiaoyuan Wang; Yinghui Duan; Hanqing Gao; Xiaopei Ji; Yunfei Zhu; Xuanyi Xiang; Hairong Ma; Yonggang Li; Qun Xue

doi:10.3389/fneur.2024.1408759

Abnormal brain spontaneous neural activity in neuromyelitis optica spectrum disorder with neuropathic pain

Front Neurol. 2024 Jun 12:15:1408759. doi: 10.3389/fneur.2024.1408759. eCollection 2024.

Authors

Gendi Wang^#^{1

2}, Xiang Chen^#³, Xiaoyuan Wang¹, Yinghui Duan¹, Hanqing Gao¹, Xiaopei Ji¹, Yunfei Zhu¹, Xuanyi Xiang¹, Hairong Ma⁴, Yonggang Li^{3

5

6}, Qun Xue^{1

7

8}

Affiliations

¹ Department of Neurology, The First Affiliated Hospital of Soochow University, Suzhou, China.
² Department of Neurology, Yancheng Third People's Hospital, Yancheng, China.
³ Department of Radiology, The First Affiliated Hospital of Soochow University, Suzhou, China.
⁴ Department of Neurology, Kunshan Hospital of Chinese Medicine, Suzhou, China.
⁵ Institute of Medical Imaging, Soochow University, Suzhou, China.
⁶ National Clinical Research Center for Hematologic Diseases, The First Affiliated Hospital of Soochow University, Suzhou, China.
⁷ Medical College of Soochow University, Suzhou, China.
⁸ Jiangsu Key Laboratory of Clinical Immunology, Jiangsu Institute of Clinical Immunology, The First Affiliated Hospital of Soochow University, Suzhou, China.

^# Contributed equally.

Abstract

Background: Neuropathic pain is one of the most common symptoms in neuromyelitis optica spectrum disorder (NMOSD). Notwithstanding, its underlying mechanism remains obscure.

Methods: The amplitude of low-frequency fluctuations (ALFF) metric was employed to investigate spontaneous neural activity alterations via resting-state functional magnetic resonance imaging (rs-MRI) data from a 3.0 T MRI scanner, in a sample of 26 patients diagnosed with NMOSD with neuropathic pain (NMOSD-WNP), 20 patients with NMOSD but without neuropathic pain (NMOSD-WoNP), and 38 healthy control (HC) subjects matched for age and sex without the comorbidity of depressive or anxious symptoms.

Results: It was observed that patients with NMOSD-WNP displayed a significant ALFF decrease in the left amygdala and right anterior insula, relative to both patients with NMOSD-WoNP and HC subjects. Furthermore, ALFF values in the left amygdala were negatively correlated with the scores of the Douleur Neuropathique en 4 Questions and McGill Pain Questionnaire (both sensory and affective descriptors) in patients with NMOSD-WNP. Additionally, there were negative correlations between the ALFF values in the right anterior insula and the duration of pain and the number of relapses in patients with NMOSD-WNP.

Conclusion: The present study characterizes spontaneous neural activity changes in brain regions associated with sensory and affective processing of pain and its modulation, which underscore the central aspects in patients with NMOSD-WNP. These findings might contribute to a better understanding of the pathophysiologic basis of neuropathic pain in NMOSD.

Keywords: amplitude of low-frequency fluctuations; amygdala; anterior insula; neuromyelitis optica spectrum disorder; neuropathic pain.

Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This work was mainly supported by the Jiangsu Provincial Key Research and Development Program (Social Development) Clinical Frontier Technology Key Project (BE2019666); the National Natural Science Foundation of China (BK20211075); the Program for Gusu Medical Talent of Suzhou City (GSWS2020009); the Translational Research Grant of NCRCH (2020WSB06); and Jiangsu Provincial Key Medical Discipline (JSDW202242).