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

• Published in: NeuroImage (Orlando, Fla.) Vol. 231; p. 117850
• Main Authors: Qin, Pengmin, Wu, Xuehai, Wu, Changwei, Wu, Hang, Zhang, Jun, Huang, Zirui, Weng, Xuchu, Zang, Di, Qi, Zengxin, Tang, Weijun, Hiromi, Tanikawa, Tan, Jiaxing, Tanabe, Sean, Fogel, Stuart, Hudetz, Anthony G., Yang, Yihong, Stamatakis, Emmanuel A, Mao, Ying, Northoff, Georg
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.05.2021; Elsevier Limited; Elsevier
• Subjects: Anesthesia; Brain; Brain injury; Brain mapping; Consciousness; Cortex (cingulate); Datasets; Degree centrality; Disorders of consciousness; Electroencephalography; Functional magnetic resonance imaging; Higher-order sensorimotor circuit; Inferior parietal lobule; Investigations; Neural networks; Rapid eye movement sleep; REM sleep; Sensorimotor integration; Sleep; Sleep and wakefulness; Somatosensory cortex; Supplementary motor area; Temporal cortex; Temporal gyrus; Unconsciousness; Higher-order sensorimotor circuit; Anesthesia; Inferior parietal lobule; Degree centrality; Rapid eye movement sleep; Disorders of consciousness
• ISSN: 1053-8119; 1095-9572
• DOI: 10.1016/j.neuroimage.2021.117850

•Adopted multiple altered consciousness states to study the neural correlates of consciousness.•Sensorimotor cortex shows reduced degree centrality during unconsciousness.•Connections between sensory and motor regions correlate with levels of consciousness.•REM-sleep showed a similar sensorimotor integration pattern as the awake state. 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.