Decoupled temporal variability and signal synchronization of spontaneous brain activity in loss of consciousness: An fMRI study in anesthesia.
Two aspects of the low frequency fluctuations of spontaneous brain activity have been proposed which reflect the complex and dynamic features of resting-state activity, namely temporal variability and signal synchronization. The relationship between them, especially its role in consciousness, nevertheless remains unclear. Our study examined the temporal variability and signal synchronization of spontaneous brain activity, as well as their relationship during loss of consciousness. We applied an intra-subject design of resting-state functional magnetic resonance imaging (rs-fMRI) in two conditions: during wakefulness, and under anesthesia with clinical unconsciousness. In addition, an independent group of patients with disorders of consciousness (DOC) was included in order to test the reliability of our findings. We observed a global reduction in the temporal variability, local and distant brain signal synchronization for subjects during anesthesia. Importantly, we found a link between temporal variability and both local and distant signal synchronizations during wakefulness: the higher the degree of temporal variability, the higher its intra-regional homogeneity and inter-regional functional connectivity. In contrast, this link was broken down under anesthesia, implying a decoupling between temporal variability and signal synchronization; this decoupling was reproduced in patients with DOC. Our results suggest that there exist some as yet unclear physiological mechanisms of consciousness which "couple" the two mathematically independent measures, temporal variability and signal synchronization of spontaneous brain activity. Our findings not only extend our current knowledge of the neural correlates of anesthetic-induced unconsciousness, but have implications for both computational neural modeling and clinical practice, such as in the diagnosis of loss of consciousness in patients with DOC.
Department of Anesthesiology, Huashan Hospital, Fudan University, Shanghai 200040, PR China; Institute of Mental Health Research, University of Ottawa, Ottawa, ON K1Z 7K4, Canada. Electronic address: Dr.Zirui.Huang@gmail.com.
Zirui
Z
Huang
Department of Anesthesiology, Huashan Hospital, Fudan University, Shanghai 200040, PR China. Electronic address: snapzhang@aliyun.com.
Jun
J
Zhang
Department of Neurosurgery, Huashan Hospital, Fudan University, Shanghai 200040, PR China.
Jinsong
J
Wu
Institute of Mental Health Research, University of Ottawa, Ottawa, ON K1Z 7K4, Canada.
Pengmin
P
Qin
Department of Neurosurgery, Huashan Hospital, Fudan University, Shanghai 200040, PR China.
Xuehai
X
Wu
Department of Anesthesiology, Huashan Hospital, Fudan University, Shanghai 200040, PR China.
Zhiyao
Z
Wang
Center for Cognition and Brain Disorders, Hangzhou Normal University, Hangzhou 310003, PR China; Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments, Hangzhou Normal University, Hangzhou 310015, PR China; School of Life Science, South China Normal University, Guangzhou 510613, PR China.
Rui
R
Dai
Department of Radiology, Huashan Hospital, Fudan University, Shanghai 200040, PR China.
Yuan
Y
Li
Department of Anesthesiology, Huashan Hospital, Fudan University, Shanghai 200040, PR China.
Weimin
W
Liang
Department of Neurosurgery, Huashan Hospital, Fudan University, Shanghai 200040, PR China.
Ying
Y
Mao
Department of Radiology, Huashan Hospital, Fudan University, Shanghai 200040, PR China.
Zhong
Z
Yang
Center for Cognition and Brain Disorders, Hangzhou Normal University, Hangzhou 310003, PR China; Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments, Hangzhou Normal University, Hangzhou 310015, PR China.
Jianfeng
J
Zhang
Institute of Mental Health Research, University of Ottawa, Ottawa, ON K1Z 7K4, Canada.
Annemarie
A
Wolff
Institute of Mental Health Research, University of Ottawa, Ottawa, ON K1Z 7K4, Canada; Center for Cognition and Brain Disorders, Hangzhou Normal University, Hangzhou 310003, PR China; Zhejiang Key Laboratory for Research in Assessment of Cognitive Impairments, Hangzhou Normal University, Hangzhou 310015, PR China.
Georg
G
Northoff
D000328:Adult; D000465:Algorithms; D000758:Anesthesia; D001921:Brain / Q000503:physiopathology*; D001931:Brain Mapping; D003244:Consciousness Disorders / Q000175:diagnosis / Q000473:pathology; D058407:Electroencephalography Phase Synchronization; D005260:Female; D006801:Humans; D008279:Magnetic Resonance Imaging / Q000379:methods*; D008297:Male; D008875:Middle Aged; D008959:Models, Neurological; D009434:Neural Pathways / Q000502:physiology; D019635:Neurosurgical Procedures; D015203:Reproducibility of Results; D012146:Rest / Q000502:physiology; D012815:Signal Processing, Computer-Assisted; D014474:Unconsciousness / Q000473:pathology*; D014851:Wakefulness / Q000502:physiology
Anesthesia; Consciousness; Resting-state; Signal synchronization; Temporal variability; fMRI