The neural correlates of arousal: Ventral posterolateral nucleus-global transient co-activation

Junrong Han; Qiuyou Xie; Xuehai Wu; Zirui Huang; Sean Tanabe; Stuart Fogel; Anthony G Hudetz; Hang Wu; Georg Northoff; Ying Mao; Sheng He; Pengmin Qin

doi:10.1016/j.celrep.2023.113633

The neural correlates of arousal: Ventral posterolateral nucleus-global transient co-activation

Cell Rep. 2024 Jan 23;43(1):113633. doi: 10.1016/j.celrep.2023.113633. Epub 2023 Dec 29.

Authors

Junrong Han¹, Qiuyou Xie², Xuehai Wu³, Zirui Huang⁴, Sean Tanabe⁴, Stuart Fogel⁵, Anthony G Hudetz⁴, Hang Wu⁶, Georg Northoff⁷, Ying Mao⁸, Sheng He⁹, Pengmin Qin¹⁰

Affiliations

¹ Key Laboratory of Brain, Cognition and Education Sciences, Ministry of Education, Institute for Brain Research and Rehabilitation, Guangdong Key Laboratory of Mental Health and Cognitive Science, South China Normal University, Guangzhou 510631, China.
² Department of Rehabilitation Medicine, Zhujiang Hospital, Southern Medical University, Guangzhou 510280, Guangdong, China; Joint Research Centre for Disorders of Consciousness, Guangzhou, Guangdong, China.
³ Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University, Shanghai, China.
⁴ Department of Anesthesiology, Center for Consciousness Science, University of Michigan, Ann Arbor, MI, USA.
⁵ School of Psychology, University of Ottawa, Ottawa, ON, Canada.
⁶ Center for Studies of Psychological Application, School of Psychology, South China Normal University, Guangzhou 510631, Guangdong, China.
⁷ Institute of Mental Health Research, University of Ottawa, Ottawa, ON, Canada; Mental Health Centre, Zhejiang University School of Medicine, Hangzhou, China.
⁸ Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University, Shanghai, China. Electronic address: [email protected].
⁹ State Key Laboratory of Brain and Cognitive Science, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China. Electronic address: [email protected].
¹⁰ Center for Studies of Psychological Application, School of Psychology, South China Normal University, Guangzhou 510631, Guangdong, China; Pazhou Lab, Guangzhou 510335, China. Electronic address: [email protected].

PMID: 38159279
DOI: 10.1016/j.celrep.2023.113633

Abstract

Arousal and awareness are two components of consciousness whose neural mechanisms remain unclear. Spontaneous peaks of global (brain-wide) blood-oxygenation-level-dependent (BOLD) signal have been found to be sensitive to changes in arousal. By contrasting BOLD signals at different arousal levels, we find decreased activation of the ventral posterolateral nucleus (VPL) during transient peaks in the global signal in low arousal and awareness states (non-rapid eye movement sleep and anesthesia) compared to wakefulness and in eyes-closed compared to eyes-open conditions in healthy awake individuals. Intriguingly, VPL-global co-activation remains high in patients with unresponsive wakefulness syndrome (UWS), who exhibit high arousal without awareness, while it reduces in rapid eye movement sleep, a state characterized by low arousal but high awareness. Furthermore, lower co-activation is found in individuals during N3 sleep compared to patients with UWS. These results demonstrate that co-activation of VPL and global activity is critical to arousal but not to awareness.

Keywords: CP: Neuroscience; arousal; fMRI; global activity; thalamus; transient co-activation.

Publication types

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

MeSH terms

Arousal / physiology
Brain / physiology
Electroencephalography
Humans
Sleep* / physiology
Ventral Thalamic Nuclei*
Wakefulness / physiology