Higher-order sensorimotor circuit of the brain's global network supports human consciousness.

Affiliation

Qin P(1), Wu X(2), Wu C(3), Wu H(4), Zhang J(5), Huang Z(6), Weng X(7), Zang D(8), Qi Z(9), Tang W(10), Hiromi T(9), Tan J(9), Tanabe S(6), Fogel S(11), Hudetz AG(6), Yang Y(12), Stamatakis EA(13), Mao Y(14), Northoff G(15).
Author information:
(1)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 510335, China. Electronic address: [Email]
(2)Pazhou Lab, Guangzhou 510335, China; Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University, Shanghai, China; Shanghai Clinical Medical Center of Neurosurgery, Shanghai Key laboratory of Brain Function Restoration and Neural Regeneration, Neurosurgical Institute of Fudan University, Shanghai, 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, China.
(3)Research Center for Brain and Consciousness, Taipei Medical University, Taipei, Taiwan; Graduate Institute of Humanities in Medicine, Taipei Medical University, Taipei, Taiwan; Shuang-Ho Hospital, Taipei Medical University, New Taipei, Taiwan.
(4)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.
(5)Department of Anesthesiology, Fudan University Shanghai Cancer center, Shanghai, China.
(6)Department of Anesthesiology and Center for Consciousness Science, University of Michigan, Ann Arbor, MI, USA.
(7)Institute for Brain Research and Rehabilitation, South China Normal University, Guangzhou, Guangdong, China.
(8)Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University, Shanghai, China; Shanghai Clinical Medical Center of Neurosurgery, Shanghai Key laboratory of Brain Function Restoration and Neural Regeneration, Neurosurgical Institute of Fudan University, Shanghai, 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, China.
(9)Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University, Shanghai, China.
(10)Radiology Department, Shanghai Huashan Hospital, Fudan University, Shanghai, China.
(11)School of Psychology, University of Ottawa, Ottawa, Canada.
(12)Neuroimaging Research Branch, National Institute on Drug Abuse, Intramural Research Programs, National Institutes of Health, Baltimore, USA.
(13)Division of Anaesthesia, School of Clinical Medicine, University of Cambridge, Cambridge, UK.
(14)Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University, Shanghai, China. Electronic address: [Email]
(15)Institute of Mental Health Research, University of Ottawa, Ottawa, Ontario, Canada; Mental Health Centre, Zhejiang University School of Medicine, Hangzhou, China.

Abstract

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.