Perioperative sleep deprivation activates the paraventricular thalamic nucleus resulting in persistent postoperative incisional pain in mice
BackgroundThe duration of postsurgical pain is closely correlated with perioperative stress. Most patients suffer short-term sleep disorder/deprivation before and/or after surgery, which leads to extended postsurgical pain by an undetermined mechanism. The paraventricular thalamus (PVT) is a critica...
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Frontiers Media S.A.
2022-12-01
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| Series: | Frontiers in Neuroanatomy |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnana.2022.1074310/full |
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| author | Lei Li Huijie Zhang Zhenli Zheng Zhenli Zheng Nan Ma Yidan Zhang Yaping Liu Yaping Liu Jingjing Zhang Songxue Su Weidong Zang Weidong Zang Jinping Shao Jinping Shao Jing Cao Jing Cao |
| author_facet | Lei Li Huijie Zhang Zhenli Zheng Zhenli Zheng Nan Ma Yidan Zhang Yaping Liu Yaping Liu Jingjing Zhang Songxue Su Weidong Zang Weidong Zang Jinping Shao Jinping Shao Jing Cao Jing Cao |
| author_sort | Lei Li |
| collection | DOAJ |
| description | BackgroundThe duration of postsurgical pain is closely correlated with perioperative stress. Most patients suffer short-term sleep disorder/deprivation before and/or after surgery, which leads to extended postsurgical pain by an undetermined mechanism. The paraventricular thalamus (PVT) is a critical area that contributes to the regulation of feeding, awakening, and emotional states. However, whether the middle PVT is involved in postoperative pain or the extension of postoperative pain caused by perioperative sleep deprivation has not yet been investigated.MethodsWe established a model of postoperative pain by plantar incision with perioperative rapid eye movement sleep deprivation (REMSD) 6 h/day for 3 consecutive days in mice. The excitability of the CaMKIIα+ neurons in the middle PVT (mPVTCaMKIIα) was detected by immunofluorescence and fiber photometry. The activation/inhibition of mPVTCaMKIIα neurons was conducted by chemogenetics.ResultsREMSD prolonged the duration of postsurgical pain and increased the excitability of mPVTCaMKIIα neurons. In addition, mPVTCaMKIIα neurons showed increased excitability in response to nociceptive stimuli or painful conditions. However, REMSD did not delay postsurgical pain recovery following the ablation of CaMKIIα neurons in the mPVT. The activation of mPVTCaMKIIα neurons prolonged the duration of postsurgical pain and elicited anxiety-like behaviors. In contrast, inhibition of mPVTCaMKIIα neurons reduced the postsurgical pain after REMSD.ConclusionOur data revealed that the CaMKIIα neurons in the mPVT are involved in the extension of the postsurgical pain duration induced by REMSD, and represented a novel potential target to treat postoperative pain induced by REMSD. |
| first_indexed | 2024-04-11T05:39:20Z |
| format | Article |
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| institution | Directory Open Access Journal |
| issn | 1662-5129 |
| language | English |
| last_indexed | 2024-04-11T05:39:20Z |
| publishDate | 2022-12-01 |
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| series | Frontiers in Neuroanatomy |
| spelling | doaj.art-91b5befe7fad4847a5fa33722e2366182022-12-22T08:01:06ZengFrontiers Media S.A.Frontiers in Neuroanatomy1662-51292022-12-011610.3389/fnana.2022.10743101074310Perioperative sleep deprivation activates the paraventricular thalamic nucleus resulting in persistent postoperative incisional pain in miceLei Li0Huijie Zhang1Zhenli Zheng2Zhenli Zheng3Nan Ma4Yidan Zhang5Yaping Liu6Yaping Liu7Jingjing Zhang8Songxue Su9Weidong Zang10Weidong Zang11Jinping Shao12Jinping Shao13Jing Cao14Jing Cao15Department of Anatomy, School of Basic Medical Sciences, Zhengzhou University, Zhengzhou, Henan, ChinaDepartment of Anatomy, School of Basic Medical Sciences, Zhengzhou University, Zhengzhou, Henan, ChinaDepartment of Anatomy, School of Basic Medical Sciences, Zhengzhou University, Zhengzhou, Henan, ChinaDepartment of Medical Record Management, The First Affiliated Hospital of Xinxiang Medical University, Xinxiang, ChinaDepartment of Anatomy, School of Basic Medical Sciences, Zhengzhou University, Zhengzhou, Henan, ChinaDepartment of Anatomy, School of Basic Medical Sciences, Zhengzhou University, Zhengzhou, Henan, ChinaDepartment of Anatomy, School of Basic Medical Sciences, Zhengzhou University, Zhengzhou, Henan, ChinaJiangsu Key Laboratory of Neuropsychiatric Diseases and Institute of Neuroscience, Soochow University, Suzhou, ChinaDepartment of Anatomy, School of Basic Medical Sciences, Zhengzhou University, Zhengzhou, Henan, ChinaDepartment of Anatomy, School of Basic Medical Sciences, Zhengzhou University, Zhengzhou, Henan, ChinaDepartment of Anatomy, School of Basic Medical Sciences, Zhengzhou University, Zhengzhou, Henan, ChinaNeuroscience Research Institute, Zhengzhou University Academy of Medical Sciences, Zhengzhou, Henan, ChinaDepartment of Anatomy, School of Basic Medical Sciences, Zhengzhou University, Zhengzhou, Henan, ChinaNeuroscience Research Institute, Zhengzhou University Academy of Medical Sciences, Zhengzhou, Henan, ChinaDepartment of Anatomy, School of Basic Medical Sciences, Zhengzhou University, Zhengzhou, Henan, ChinaNeuroscience Research Institute, Zhengzhou University Academy of Medical Sciences, Zhengzhou, Henan, ChinaBackgroundThe duration of postsurgical pain is closely correlated with perioperative stress. Most patients suffer short-term sleep disorder/deprivation before and/or after surgery, which leads to extended postsurgical pain by an undetermined mechanism. The paraventricular thalamus (PVT) is a critical area that contributes to the regulation of feeding, awakening, and emotional states. However, whether the middle PVT is involved in postoperative pain or the extension of postoperative pain caused by perioperative sleep deprivation has not yet been investigated.MethodsWe established a model of postoperative pain by plantar incision with perioperative rapid eye movement sleep deprivation (REMSD) 6 h/day for 3 consecutive days in mice. The excitability of the CaMKIIα+ neurons in the middle PVT (mPVTCaMKIIα) was detected by immunofluorescence and fiber photometry. The activation/inhibition of mPVTCaMKIIα neurons was conducted by chemogenetics.ResultsREMSD prolonged the duration of postsurgical pain and increased the excitability of mPVTCaMKIIα neurons. In addition, mPVTCaMKIIα neurons showed increased excitability in response to nociceptive stimuli or painful conditions. However, REMSD did not delay postsurgical pain recovery following the ablation of CaMKIIα neurons in the mPVT. The activation of mPVTCaMKIIα neurons prolonged the duration of postsurgical pain and elicited anxiety-like behaviors. In contrast, inhibition of mPVTCaMKIIα neurons reduced the postsurgical pain after REMSD.ConclusionOur data revealed that the CaMKIIα neurons in the mPVT are involved in the extension of the postsurgical pain duration induced by REMSD, and represented a novel potential target to treat postoperative pain induced by REMSD.https://www.frontiersin.org/articles/10.3389/fnana.2022.1074310/fullpostsurgical painparaventricular thalamic nucleus (PVT)CaMKIIα neuronsperioperative sleep deprivationstress |
| spellingShingle | Lei Li Huijie Zhang Zhenli Zheng Zhenli Zheng Nan Ma Yidan Zhang Yaping Liu Yaping Liu Jingjing Zhang Songxue Su Weidong Zang Weidong Zang Jinping Shao Jinping Shao Jing Cao Jing Cao Perioperative sleep deprivation activates the paraventricular thalamic nucleus resulting in persistent postoperative incisional pain in mice Frontiers in Neuroanatomy postsurgical pain paraventricular thalamic nucleus (PVT) CaMKIIα neurons perioperative sleep deprivation stress |
| title | Perioperative sleep deprivation activates the paraventricular thalamic nucleus resulting in persistent postoperative incisional pain in mice |
| title_full | Perioperative sleep deprivation activates the paraventricular thalamic nucleus resulting in persistent postoperative incisional pain in mice |
| title_fullStr | Perioperative sleep deprivation activates the paraventricular thalamic nucleus resulting in persistent postoperative incisional pain in mice |
| title_full_unstemmed | Perioperative sleep deprivation activates the paraventricular thalamic nucleus resulting in persistent postoperative incisional pain in mice |
| title_short | Perioperative sleep deprivation activates the paraventricular thalamic nucleus resulting in persistent postoperative incisional pain in mice |
| title_sort | perioperative sleep deprivation activates the paraventricular thalamic nucleus resulting in persistent postoperative incisional pain in mice |
| topic | postsurgical pain paraventricular thalamic nucleus (PVT) CaMKIIα neurons perioperative sleep deprivation stress |
| url | https://www.frontiersin.org/articles/10.3389/fnana.2022.1074310/full |
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