The micro and macro interactions in acute autoimmune encephalitis: a study of resting-state EEG

Xin Luo; Jie Liao; Hong Liu; Qiulin Tang; Hua Luo; Xiu Chen; Jianghai Ruan

doi:10.3389/fneur.2023.1181629

The micro and macro interactions in acute autoimmune encephalitis: a study of resting-state EEG

Front Neurol. 2023 Jun 8:14:1181629. doi: 10.3389/fneur.2023.1181629. eCollection 2023.

Authors

Xin Luo^#^{1

2}, Jie Liao^#^{1

2}, Hong Liu^{1

2}, Qiulin Tang^{1

2}, Hua Luo^{1

2}, Xiu Chen^{1

2}, Jianghai Ruan^{1

2}

Affiliations

¹ Department of Neurology, The Affiliated Hospital of Southwest Medical University, Luzhou, China.
² Laboratory of Neurological Diseases and Brain Function, Luzhou, China.

^# Contributed equally.

Abstract

Objective: Early recognition of autoimmune encephalitis (AIE) is often difficult and time-consuming. Understanding how the micro-level (antibodies) and macro-level (EEG) couple with each other may help rapidly diagnose and appropriately treat AIE. However, limited studies focused on brain oscillations involving micro- and macro-interactions in AIE from a neuro-electrophysiological perspective. Here, we investigated brain network oscillations in AIE using Graph theoretical analysis of resting state EEG.

Methods: AIE Patients (n = 67) were enrolled from June 2018 to June 2022. Each participant underwent a ca.2-hour 19-channel EEG examination. Five 10-second resting state EEG epochs with eyes closed were extracted for each participant. The functional networks based on the channels and Graph theory analysis were carried out.

Results: Compared with the HC group, significantly decreased FC across whole brain regions at alpha and beta bands were found in AIE patients. In addition, the local efficiency and clustering coefficient of the delta band was higher in AIE patients than in the HC group (P < 0.05). AIE patients had a smaller world index (P < 0.05) and higher shortest path length (P < 0.001) in the alpha band than those of the control group. Also, the AIE patients' global efficiency, local efficiency, and clustering coefficients decreased in the alpha band (P < 0.001). Different types of antibodies (antibodies against ion channels, antibodies against synaptic excitatory receptors, antibodies against synaptic inhibitory receptors, and multiple antibodies positive) showed distinct graph parameters. Moreover, the graph parameters differed in the subgroups by intracranial pressure. Correlation analysis revealed that magnetic resonance imaging abnormalities were related to global efficiency, local efficiency, and clustering coefficients in the theta, alpha, and beta bands, but negatively related to the shortest path length.

Conclusion: These findings add to our understanding of how brain FC and graph parameters change and how the micro- (antibodies) scales interact with the macro- (scalp EEG) scale in acute AIE. The clinical traits and subtypes of AIE may be suggested by graph properties. Further longitudinal cohort studies are needed to explore the associations between these graph parameters and recovery status, and their possible applications in AIE rehabilitation.

Keywords: acute autoimmune encephalitis; electroencephalography; graph analysis; phase lock value; resting-state brain network.

Grants and funding

This work was supported by the Youth Program of the National Natural Science Foundation of China (81804198), Strategic Cooperation Project between Sichuan University and Luzhou Government (2021CDLZ-10).