Identifying patients with cognitive motor dissociation using resting-state temporal stability
Hang Wu,
Qiuyou Xie,
Jiahui Pan,
Qimei Liang,
Yue Lan,
Yequn Guo,
Junrong Han,
Musi Xie,
Yueyao Liu,
Liubei Jiang,
Xuehai Wu,
Yuanqing Li,
Pengmin Qin
Affiliations
Hang Wu
Key Laboratory of Brain, Cognition and Education Sciences, Ministry of Education, School of Psychology, Center for Studies of Psychological Application, and Guangdong Key Laboratory of Mental Health and Cognitive Science, South China Normal University, Guangzhou, Guangdong, 510631, China
Qiuyou Xie
Joint Center for disorders of consciousness, Department of Rehabilitation Medicine, Zhujiang Hospital, Southern Medical University, Guangzhou, 510220, China; Centre for Hyperbaric Oxygen and Neurorehabilitation, Guangzhou General Hospital of Guangzhou Military Command, Guangzhou, 510010, China
Jiahui Pan
School of Software, South China Normal University, Foshan, 528225, China; Pazhou Lab, Guangzhou, 510330, China
Qimei Liang
Joint Center for disorders of consciousness, Department of Rehabilitation Medicine, Zhujiang Hospital, Southern Medical University, Guangzhou, 510220, China
Yue Lan
Joint Center for disorders of consciousness, Department of Rehabilitation Medicine, Zhujiang Hospital, Southern Medical University, Guangzhou, 510220, China
Yequn Guo
Centre for Hyperbaric Oxygen and Neurorehabilitation, Guangzhou General Hospital of Guangzhou Military Command, Guangzhou, 510010, China
Junrong Han
Key Laboratory of Brain, Cognition and Education Science, Ministry of Education, China; Institute for Brain Research and Rehabilitation, and Guangdong Key Laboratory of Mental Health and Cognitive Science, South China Normal University, 510631 Guangzhou, China
Musi Xie
Key Laboratory of Brain, Cognition and Education Sciences, Ministry of Education, School of Psychology, Center for Studies of Psychological Application, and Guangdong Key Laboratory of Mental Health and Cognitive Science, South China Normal University, Guangzhou, Guangdong, 510631, China
Yueyao Liu
Key Laboratory of Brain, Cognition and Education Sciences, Ministry of Education, School of Psychology, Center for Studies of Psychological Application, and Guangdong Key Laboratory of Mental Health and Cognitive Science, South China Normal University, Guangzhou, Guangdong, 510631, China
Liubei Jiang
Key Laboratory of Brain, Cognition and Education Sciences, Ministry of Education, School of Psychology, Center for Studies of Psychological Application, and Guangdong Key Laboratory of Mental Health and Cognitive Science, South China Normal University, Guangzhou, Guangdong, 510631, China
Xuehai Wu
Pazhou Lab, Guangzhou, 510330, China; Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University, Shanghai, 200433, China; Neurosurgical Institute of Fudan University, Shanghai Clinical Medical Center of Neurosurgery, Shanghai Key laboratory of Brain Function Restoration and Neural Regeneration, Shanghai, 200433, China; State Key Laboratory of Medical Neurobiology and MOE Frontiers Center for Brain Science, School of Basic Medical Sciences and Institutes of Brain Science, Fudan University, Shanghai, 200433, China; Corresponding authors at: Xuehai Wu, Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University, Shanghai, 200433, China. Yuanqing Li, School of Automation Science and Engineering, South China University of Technology, Guangzhou, 510640, China. Pengmin Qin, Key Laboratory of Brain, Cognition and Education Sciences, Ministry of Education; School of Psychology, Center for Studies of Psychological Application, and Guangdong Key Laboratory of Mental Health and Cognitive Science, South China Normal University, Guangzhou, Guangdong, 510631, China
Yuanqing Li
Pazhou Lab, Guangzhou, 510330, China; School of Automation Science and Engineering, South China University of Technology, Guangzhou 510640, China; Corresponding authors at: Xuehai Wu, Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University, Shanghai, 200433, China. Yuanqing Li, School of Automation Science and Engineering, South China University of Technology, Guangzhou, 510640, China. Pengmin Qin, Key Laboratory of Brain, Cognition and Education Sciences, Ministry of Education; School of Psychology, Center for Studies of Psychological Application, and Guangdong Key Laboratory of Mental Health and Cognitive Science, South China Normal University, Guangzhou, Guangdong, 510631, China
Pengmin Qin
Key Laboratory of Brain, Cognition and Education Sciences, Ministry of Education, School of Psychology, Center for Studies of Psychological Application, and Guangdong Key Laboratory of Mental Health and Cognitive Science, South China Normal University, Guangzhou, Guangdong, 510631, China; Pazhou Lab, Guangzhou, 510330, China; Corresponding authors at: Xuehai Wu, Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University, Shanghai, 200433, China. Yuanqing Li, School of Automation Science and Engineering, South China University of Technology, Guangzhou, 510640, China. Pengmin Qin, Key Laboratory of Brain, Cognition and Education Sciences, Ministry of Education; School of Psychology, Center for Studies of Psychological Application, and Guangdong Key Laboratory of Mental Health and Cognitive Science, South China Normal University, Guangzhou, Guangdong, 510631, China
Using task-dependent neuroimaging techniques, recent studies discovered a fraction of patients with disorders of consciousness (DOC) who had no command-following behaviors but showed a clear sign of awareness as healthy controls, which was defined as cognitive motor dissociation (CMD). However, existing task-dependent approaches might fail when CMD patients have cognitive function (e.g., attention, memory) impairments, in which patients with covert awareness cannot perform a specific task accurately and are thus wrongly considered unconscious, which leads to false-negative findings. Recent studies have suggested that sustaining a stable functional organization over time, i.e., high temporal stability, is crucial for supporting consciousness. Thus, temporal stability could be a powerful tool to detect the patient's cognitive functions (e.g., consciousness), while its alteration in the DOC and its capacity for identifying CMD were unclear. The resting-state fMRI (rs-fMRI) study included 119 participants from three independent research sites. A sliding-window approach was used to investigate global and regional temporal stability, which measured how stable the brain's functional architecture was across time. The temporal stability was compared in the first dataset (36/16 DOC/controls), and then a Support Vector Machine (SVM) classifier was built to discriminate DOC from controls. Furthermore, the generalizability of the SVM classifier was tested in the second independent dataset (35/21 DOC/controls). Finally, the SVM classifier was applied to the third independent dataset, where patients underwent rs-fMRI and brain-computer interface assessment (4/7 CMD/potential non-CMD), to test its performance in identifying CMD. Our results showed that global and regional temporal stability was impaired in DOC patients, especially in regions of the cingulo-opercular task control network, default-mode network, fronto-parietal task control network, and salience network. Using temporal stability as the feature, the SVM model not only showed good performance in the first dataset (accuracy = 90%), but also good generalizability in the second dataset (accuracy = 84%). Most importantly, the SVM model generalized well in identifying CMD in the third dataset (accuracy = 91%). Our preliminary findings suggested that temporal stability could be a potential tool to assist in diagnosing CMD. Furthermore, the temporal stability investigated in this study also contributed to a deeper understanding of the neural mechanism of consciousness.