TY - JOUR
T1 - Higher-order sensorimotor circuit of the brain's global network supports human consciousness
AU - Qin, Pengmin
AU - Wu, Xuehai
AU - Wu, Changwei
AU - Wu, Hang
AU - Zhang, Jun
AU - Huang, Zirui
AU - Weng, Xuchu
AU - Zang, Di
AU - Qi, Zengxin
AU - Tang, Weijun
AU - Hiromi, Tanikawa
AU - Tan, Jiaxing
AU - Tanabe, Sean
AU - Fogel, Stuart
AU - Hudetz, Anthony G.
AU - Yang, Yihong
AU - Stamatakis, Emmanuel A.
AU - Mao, Ying
AU - Northoff, Georg
N1 - Funding Information:
This work was sponsored by grants from Key Realm R&D Program of Guangzhou ( 202007030005 to PQ), the National Natural Science Foundation of China (Grant 31971032, 31771249 to PQ; Grants 81571025 to XW), International Cooperation Project from Shanghai Science Foundation (No. 18410711300 to Xuehai Wu), Shanghai Science and Technology Development funds (No. 16JC1420100 to Y.M), Shanghai Municipal Science and Technology Major Project (No. 2018SHZDZX01 to Y.M), Natural Science Foundation and Major Basic Research Program of Shanghai ( 16JC1420100 ), Ministry of Science and Technology in Taiwan ( MOST 105-2628-B-038-013-MY3 ), National Science Foundation of China ( 31471072 ), Taiwan Ministry of Science and Technology ( 105-2410-H-038-006-MY3 , 105-2410-H-038-005-MY2 ); and Taipei Medical University ( 104-6402-006-110 ), and National Institute of General Medical Sciences of the National Institutes of Health ( R01-GM103894 , to AGH), Canadian Institutes of Health Research (CIHR), Michael Smith Foundation (EJLB-CIHR), The Hope for Depression Research Foundation (HDRF). This research project was also supported by the HBP Joint Platform to GN, funded from the European Union's Horizon 2020 Framework Program for research and Innovation under the specific Grant Agreement No 785907 (Human Brian Project SGA 2).
Publisher Copyright:
© 2021 The Authors
Copyright:
Copyright 2021 Elsevier B.V., All rights reserved.
PY - 2021/5/1
Y1 - 2021/5/1
N2 - Consciousness is a mental characteristic of the human mind, whose exact neural features remain unclear. We aimed to identify the critical nodes within the brain's global functional network that support consciousness. To that end, we collected a large fMRI resting state dataset with subjects in at least one of the following three consciousness states: preserved (including the healthy awake state, and patients with a brain injury history (BI) that is fully conscious), reduced (including the N1-sleep state, and minimally conscious state), and lost (including the N3-sleep state, anesthesia, and unresponsive wakefulness state). We also included a unique dataset of subjects in rapid eye movement sleep state (REM-sleep) to test for the presence of consciousness with minimum movements and sensory input. To identify critical nodes, i.e., hubs, within the brain's global functional network, we used a graph-theoretical measure of degree centrality conjoined with ROI-based functional connectivity. Using these methods, we identified various higher-order sensory and motor regions including the supplementary motor area, bilateral supramarginal gyrus (part of inferior parietal lobule), supragenual/dorsal anterior cingulate cortex, and left middle temporal gyrus, that could be important hubs whose degree centrality was significantly reduced when consciousness was reduced or absent. Additionally, we identified a sensorimotor circuit, in which the functional connectivity among these regions was significantly correlated with levels of consciousness across the different groups, and remained present in the REM-sleep group. Taken together, we demonstrated that regions forming a higher-order sensorimotor integration circuit are involved in supporting consciousness within the brain's global functional network. That offers novel and more mechanism-guided treatment targets for disorders of consciousness.
AB - Consciousness is a mental characteristic of the human mind, whose exact neural features remain unclear. We aimed to identify the critical nodes within the brain's global functional network that support consciousness. To that end, we collected a large fMRI resting state dataset with subjects in at least one of the following three consciousness states: preserved (including the healthy awake state, and patients with a brain injury history (BI) that is fully conscious), reduced (including the N1-sleep state, and minimally conscious state), and lost (including the N3-sleep state, anesthesia, and unresponsive wakefulness state). We also included a unique dataset of subjects in rapid eye movement sleep state (REM-sleep) to test for the presence of consciousness with minimum movements and sensory input. To identify critical nodes, i.e., hubs, within the brain's global functional network, we used a graph-theoretical measure of degree centrality conjoined with ROI-based functional connectivity. Using these methods, we identified various higher-order sensory and motor regions including the supplementary motor area, bilateral supramarginal gyrus (part of inferior parietal lobule), supragenual/dorsal anterior cingulate cortex, and left middle temporal gyrus, that could be important hubs whose degree centrality was significantly reduced when consciousness was reduced or absent. Additionally, we identified a sensorimotor circuit, in which the functional connectivity among these regions was significantly correlated with levels of consciousness across the different groups, and remained present in the REM-sleep group. Taken together, we demonstrated that regions forming a higher-order sensorimotor integration circuit are involved in supporting consciousness within the brain's global functional network. That offers novel and more mechanism-guided treatment targets for disorders of consciousness.
KW - Anesthesia
KW - Degree centrality
KW - Disorders of consciousness
KW - Higher-order sensorimotor circuit
KW - Inferior parietal lobule
KW - Rapid eye movement sleep
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U2 - 10.1016/j.neuroimage.2021.117850
DO - 10.1016/j.neuroimage.2021.117850
M3 - Article
C2 - 33582277
AN - SCOPUS:85101140797
SN - 1053-8119
VL - 231
JO - NeuroImage
JF - NeuroImage
M1 - 117850
ER -