Electrophysiological characteristics of CM-pf in diagnosis and outcome of patients with disorders of consciousness

Jianghong He; Haoran Zhang; Yuanyuan Dang; Yutong Zhuang; Qianqian Ge; Yi Yang; Long Xu; Xiaoyu Xia; Steven Laureys; Shan Yu; Wangming Zhang

doi:10.1016/j.brs.2023.09.021

Electrophysiological characteristics of CM-pf in diagnosis and outcome of patients with disorders of consciousness

Brain Stimul. 2023 Sep-Oct;16(5):1522-1532. doi: 10.1016/j.brs.2023.09.021. Epub 2023 Sep 29.

Authors

Jianghong He¹, Haoran Zhang², Yuanyuan Dang³, Yutong Zhuang⁴, Qianqian Ge⁵, Yi Yang⁵, Long Xu⁵, Xiaoyu Xia⁶, Steven Laureys⁷, Shan Yu⁸, Wangming Zhang⁹

Affiliations

¹ Neurosurgery Center, The National Key Clinical Specialty, The Engineering Technology Research Center of Education Ministry of China on Diagnosis and Treatment of Cerebrovascular Disease, Guangdong Provincial Key Laboratory on Brain Function Repair and Regeneration, The Neurosurgery Institute of Guangdong Province, Zhujiang Hospital, Southern Medical University, China; Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, 100070, China.
² Laboratory of Brain Atlas and Brain-inspired Intelligence, Institute of Automation, Chinese Academy of Sciences, Beijing, 100190, China; School of Future Technology, University of Chinese Academy of Sciences, Beijing, 100049, China.
³ Department of Neurosurgery, The First Medical Center of Chinese PLA General Hospital, Beijing, 100853, China.
⁴ Department of Neurosurgery, The Second School of Clinical Medicine, Southern Medical University, Guangzhou, China.
⁵ Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, 100070, China.
⁶ Department of Neurosurgery, The Seventh Medical Center of PLA General Hospital, Beijing, 100700, China.
⁷ CERVO Brain Research Centre, Laval University, Canada; Coma Science Group, GIGA Consciousness Research Unit, Liège University Hospital, Belgium; International Consciousness Science Institute, Hangzhou Normal University, Hangzhou, Zhejiang, China.
⁸ Laboratory of Brain Atlas and Brain-inspired Intelligence, Institute of Automation, Chinese Academy of Sciences, Beijing, 100190, China; School of Future Technology, University of Chinese Academy of Sciences, Beijing, 100049, China. Electronic address: shan.yu@nlpr.ia.ac.cn.
⁹ Neurosurgery Center, The National Key Clinical Specialty, The Engineering Technology Research Center of Education Ministry of China on Diagnosis and Treatment of Cerebrovascular Disease, Guangdong Provincial Key Laboratory on Brain Function Repair and Regeneration, The Neurosurgery Institute of Guangdong Province, Zhujiang Hospital, Southern Medical University, China. Electronic address: wzhang@vip.126.com.

PMID: 37778457
DOI: 10.1016/j.brs.2023.09.021

Abstract

Background: Deep brain stimulation (DBS) in the centromedian-parafascicular complex (CM-pf) has been reported as a potential therapeutic option for disorders of consciousness (DoC). However, the lack of understanding of its electrophysiological characteristics limits the improvement of therapeutic effect.

Objective: To investigate the CM-pf electrophysiological characteristics underlying disorders of consciousness (DoC) and its recovery.

Methods: We collected the CM-pf electrophysiological signals from 23 DoC patients who underwent central thalamus DBS (CT-DBS) surgery. Five typical electrophysiological features were extracted, including neuronal firing properties, multiunit activity (MUA) properties, signal stability, spike-MUA synchronization strength (syncMUA), and the background noise level. Their correlations with the consciousness level, the outcome, and the primary clinical factors of DoC were analyzed.

Results: 11 out of 23 patients (0/2 chronic coma, 5/13 unresponsive wakefulness syndrome/vegetative state (UWS/VS), 6/8 minimally conscious state minus (MCS-)) exhibited an improvement in the level of consciousness after CT-DBS. In CM-pf, significantly stronger gamma band syncMUA strength and alpha band normalized MUA power were found in MCS- patients. In addition, higher firing rates, stronger high-gamma band MUA power and alpha band normalized power, and more stable theta oscillation were correlated with better outcomes. Besides, we also identified electrophysiological properties that are correlated with clinical factors, including etiologies, age, and duration of DoC.

Conclusion: We provide comprehensive analyses of the electrophysiological characteristics of CM-pf in DoC patients. Our results support the 'mesocircuit' hypothesis, one proposed mechanism of DoC recovery, and reveal CM-pf electrophysiological features that are crucial for understanding the pathogenesis of DoC, predicting its recovery, and explaining the effect of clinical factors on DoC.

Keywords: Central thalamus (CT); Centromedian-parafascicular complex (CM-pf); Deep brain stimulation (DBS); Disorders of consciousness (DoC); Multiunit activity (MUA).

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Consciousness
Consciousness Disorders* / diagnosis
Consciousness Disorders* / etiology
Consciousness Disorders* / therapy
Electrophysiological Phenomena
Humans
Persistent Vegetative State* / diagnosis
Thalamus