Electroencephalography-based biological and functional characteristics of spinal cord injury patients with neuropathic pain and numbness

Dezheng Wang; Xinting Zhang; Chen Xin; Chongfeng Wang; Shouwei Yue; Dongju Guo; Wei Wang; Yang Zhang; Fangzhou Xu

doi:10.3389/fnins.2024.1356858

Electroencephalography-based biological and functional characteristics of spinal cord injury patients with neuropathic pain and numbness

Front Neurosci. 2024 May 1:18:1356858. doi: 10.3389/fnins.2024.1356858. eCollection 2024.

Authors

Dezheng Wang^#^{1

2}, Xinting Zhang^#³, Chen Xin², Chongfeng Wang⁴, Shouwei Yue², Dongju Guo², Wei Wang², Yang Zhang^{1

2}, Fangzhou Xu⁴

Affiliations

¹ Rehabilitation and Physical Therapy Department, Shandong University of Traditional Chinese Medicine Affiliated Hospital, Jinan, China.
² Rehabilitation Center, Qilu Hospital of Shandong University, Jinan, Shandong, China.
³ Department of Pediatrics, Qilu Hospital of Shandong University, Jinan, China.
⁴ International School for Optoelectronic Engineering, Qilu University of Technology (Shandong Academy of Sciences), Jinan, China.

^# Contributed equally.

Abstract

Objectives: To identify potential treatment targets for spinal cord injury (SCI)-related neuropathic pain (NP) by analysing the differences in electroencephalogram (EEG) and brain network connections among SCI patients with NP or numbness.

Participants and methods: The EEG signals during rest, as well as left- and right-hand and feet motor imagination (MI), were recorded. The power spectral density (PSD) of the θ (4-8 Hz), α (8-12 Hz), and β (13-30 Hz) bands was calculated by applying Continuous Wavelet Transform (CWT) and Modified S-transform (MST) to the data. We used 21 electrodes as network nodes and performed statistical measurements of the phase synchronisation between two brain regions using a phase-locking value, which captures nonlinear phase synchronisation.

Results: The specificity of the MST algorithm was higher than that of the CWT. Widespread non-lateralised event-related synchronization was observed in both groups during the left- and right-hand MI. The PWP (patients with pain) group had lower θ and α bands PSD values in multiple channels of regions including the frontal, premotor, motor, and temporal regions compared with the PWN (patients with numbness) group (all p < 0.05), but higher β band PSD values in multiple channels of regions including the frontal, premotor, motor, and parietal region compared with the PWN group (all p < 0.05). During left-hand and feet MI, in the lower frequency bands (θ and α bands), the brain network connections of the PWP group were significantly weaker than the PWN group except for the frontal region. Conversely, in the higher frequency bands (β band), the brain network connections of the PWP group were significantly stronger in all regions than the PWN group.

Conclusion: The differences in the power of EEG and network connectivity in the frontal, premotor, motor, and temporal regions are potential biological and functional characteristics that can be used to distinguish NP from numbness. The differences in brain network connections between the two groups suggest that the distinct mechanisms for pain and numbness.

Keywords: biological and functional characteristics; electroencephalogram; motor imagination; neuropathic pain; numbness; spinal cord injury.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. The project is supported in part by the Fundamental Research Funds for the Central Universities (No. 2022JC013), the Natural Science Foundation of Shandong Province of China (No. ZR202102200383), the Program for Youth Innovative Research Team in the University of Shandong Province in China (No. 2019KJN010), the Introduce Innovative Teams of 2021 “New High School 20 Items” Project (No. 2021GXRC071), the Clinical Research Cross-Project of Shandong University (No. 2020SDUCRCB004), the National Natural Science Foundation of China (No. 82172535), Key Program of the National Natural Science Foundation of China (No. 82330064), Natural Science Foundation of Shandong Province (No. ZR2022MF289), National Natural Science Foundation of China (No. 62271293), Graduate Education and Teaching Reform Project of Qilu University of Technology (Shandong Academy of Sciences) in 2023, and Talent Training and Teaching Reform Project of Qilu University of Technology in 2022 (No. P202204).