Preoperative Acute Sleep Deprivation Causes Postoperative Pain Hypersensitivity and Abnormal Cerebral Function
Meimei Guo1 · Yuxiang Wu2 · Danhao Zheng3 · Lei Chen1,4 · Bingrui Xiong1 · Jinfeng Wu3 · Ke Li1 · Li Wang3 · Kangguang Lin5 · Zongze Zhang1 · Anne Manyande6 · Fuqiang Xu3 · Jie Wang3,7,8 · Mian Peng11 Department of Anesthesiology, Zhongnan Hospital of Wuhan University, Wuhan 430071, China
2 Department of Health and Kinesiology, School of Physical Education, Jianghan University, Wuhan 430056, China
3 State Key Laboratory of Magnetic Resonance and Atomic and Molecular Physics, National Center for Magnetic Resonance in Wuhan, Wuhan Institute of Physics and Mathematics, Innovation Academy for Precision Measurement Science and Technology, Chinese Academy of Sciences-Wuhan National Laboratory for Optoelectronics, Wuhan 430071, China
4 Department of Anesthesiology, Peking University Third Hospital, Beijing 100191, China
5 Department of Afective Disorders, The Afliated Brain Hospital of Guangzhou Medical University, Guangzhou 510000, China
6 School of Human and Social Sciences, University of West London, London W1S 3PR, UK
7 Institute of Neuroscience and Brain Disease; Xiangyang Central Hospital, Afliated Hospital of Hubei University of Arts and Science, Xiangyang 441000, China
8 University of Chinese Academy of Sciences, Beijing 100049, China
Abstract
Preoperative sleep loss can amplify post-operative mechanical hyperalgesia. However, the underlying mechanisms are still largely unknown. In the current study, rats were randomly allocated to a control group and an acute sleep deprivation (ASD) group which experienced 6 h ASD before surgery. Then the variations in cerebral function and activity were investigated with multi-modal techniques, such as nuclear magnetic resonance, functional magnetic resonance imaging, c-Fos immunofluorescence, and electrophysiology. The results indicated that ASD induced hyperalgesia, and the metabolic kinetics were remarkably decreased in the striatum and midbrain. The functional connectivity (FC) between the nucleus accumbens (NAc, a subregion of the ventral striatum) and the ventrolateral periaqueductal gray (vLPAG) was significantly reduced, and the c-Fos expression in the NAc and the vLPAG was suppressed. Furthermore, the electrophysiological recordings demonstrated that both the neuronal activity in the NAc and the vLPAG, and the coherence of the NAc-vLPAG were suppressed in both resting and task states. This study showed that neuronal activity in the NAc and the vLPAG were weakened and the FC between the NAc and the vLPAG was also suppressed in rats with ASD-induced hyperalgesia. This study highlights the importance of preoperative sleep management for surgical patients.
Keywords
Acute sleep deprivation; Incisional pain; Nucleus accumbens; Periaqueductal gray; Functional connectivity
