Anterior precuneus related to the recovery of consciousness

Hang Wu; Zengxin Qi; Xuehai Wu; Jun Zhang; Changwei Wu; Zirui Huang; Di Zang; Stuart Fogel; Sean Tanabe; Anthony G Hudetz; Georg Northoff; Ying Mao; Pengmin Qin

doi:10.1016/j.nicl.2022.102951

Anterior precuneus related to the recovery of consciousness

Neuroimage Clin. 2022:33:102951. doi: 10.1016/j.nicl.2022.102951. Epub 2022 Jan 30.

Authors

Hang Wu¹, Zengxin Qi², Xuehai Wu³, Jun Zhang⁴, Changwei Wu⁵, Zirui Huang⁶, Di Zang², Stuart Fogel⁷, Sean Tanabe⁶, Anthony G Hudetz⁶, Georg Northoff⁸, Ying Mao⁹, Pengmin Qin¹⁰

Affiliations

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.
² 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.
³ 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; Pazhou Lab, Guangzhou 510335, China.
⁴ Department of Anesthesiology, Fudan University Shanghai Cancer Center Shanghai, 200433, China.
⁵ Research Center for Brain and Consciousness, Taipei Medical University, Taipei 11031, Taiwan; Graduate Institute of Humanities in Medicine, Taipei Medical University, Taipei 11031, Taiwan; Shuang-Ho Hospital, Taipei Medical University, New Taipei 23561, Taiwan.
⁶ Department of Anesthesiology and Center for Consciousness Science, University of Michigan, Ann Arbor, MI 48105, USA.
⁷ School of Psychology, University of Ottawa, Ottawa, ON K1N 6N5, Canada.
⁸ Institute of Mental Health Research, University of Ottawa, Ottawa, Ontario, ON K1Z 7K4, Canada; Mental Health Centre, Zhejiang University School of Medicine, Hangzhou 310058, China.
⁹ 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. Electronic address: maoying@fudan.edu.cn.
¹⁰ 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: qin.pengmin@m.scnu.edu.cn.

Abstract

The neural mechanism that enables the recovery of consciousness in patients with unresponsive wakefulness syndrome (UWS) remains unclear. The aim of the current study is to characterize the cortical hub regions related to the recovery of consciousness. In the current fMRI study, voxel-wise degree centrality analysis was adopted to identify the cortical hubs related to the recovery of consciousness, for which a total of 27 UWS patients were recruited, including 13 patients who emerged from UWS (UWS-E), and 14 patients who remained in UWS (UWS-R) at least three months after the experiment performance. Furthermore, other recoverable unconscious states were adopted as validation groups, including three independent N3 sleep datasets (n = 12, 9, 9 respectively) and three independent anesthesia datasets (n = 27, 14, 6 respectively). Spatial similarity of the hub characteristic with the validation groups between the UWS-E and UWS-R was compared using the dice coefficient. Finally, with the cortical regions persistently shown as hubs across UWS-E and validation states, functional connectivity analysis was further performed to explore the connectivity patterns underlying the recovery of consciousness. The results identified four cortical hubs in the UWS-E, which showed significantly higher degree centrality for UWS-E than UWS-R, including the anterior precuneus, left inferior parietal lobule, left inferior frontal gyrus, and left middle frontal gyrus, of which the degree centrality value also positively correlated with the patients' Glasgow Outcome Scale (GOS) score that assessed global brain functioning outcome after a brain injury. Furthermore, the anterior precuneus was found with significantly higher similarity of hub characteristics as well as functional connectivity patterns between UWS-E and the validation groups. The results suggest that the recovery of consciousness may be relevant to the integrity of cortical hubs in the recoverable unconscious states, especially the anterior precuneus. The identified cortical hub regions could serve as potential treatment targets for patients with UWS.

Keywords: Anesthesia; Anterior precuneus; Degree centrality; N3 sleep; Recovery of consciousness; Unresponsive wakefulness syndrome.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Brain Injuries*
Consciousness Disorders / diagnostic imaging
Consciousness*
Humans
Magnetic Resonance Imaging
Parietal Lobe / diagnostic imaging
Wakefulness