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Investigation of acupuncture in improving sleep, cognitive and emotion based on attenuation of oxidative stress in prefrontal cortex in sleep-deprived rats

基于前额叶皮质氧化应激抑制效应探讨针刺对睡眠剥夺大鼠睡眠、认知及情绪的改善

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Abstract

Objective

To explore whether acupuncture can improve sleep disturbance, cognitive impairment and emotional disorders caused by sleep deprivation, and its association with the attenuation of oxidative stress injury in prefrontal cortex.

Methods

Fifty-two male Sprague-Dawley rats were randomly divided into a control group (n=10), a model group (n=14), a manual acupuncture (MA) group (n=14), and a sham-MA group (n=14). All the groups were established as sleep deprivation models via the modified multiple platform method, except for the control group. Rats in both the MA group and the sham-MA group received corresponding intervention, respectively. After modeling and intervention, the four groups received three behavioral tests, namely sleep monitoring, by comprehensive lab animal monitoring system (CLAMS), Morris water maze (MWM) test and open-field test (OFT), followed by oxygen free radical level test and Western blot (WB) detection for the expression levels of Bax and Bcl-2.

Results

The MA group derived more sleep time within 24 h than either the model group or the sham-MA group (both P<0.05). On MWM orientation navigation test day 1, there were no significant differences in escape latency among the control, MA and sham-MA groups (P>0.05), and the escape latency was significantly shorter in these three groups than that in the model group (all P<0.05). On test day 4, the escape latency was markedly shorter in the MA group than that in either the model group or the sham-MA group (both P<0.05); meanwhile, the MA group showed significantly better performance compared with these two groups in space probe test (both P<0.05). In OFT, compared with the control group, there was a significant decline in the horizontal movement score in the other three groups (all P<0.05), and the decrease was more significant in the model group and the sham-MA group than that in the MA group (both P<0.05). The superoxide dismutase (SOD) content was markedly higher and the malondialdehyde (MDA) content was markedly lower in the MA group than those in the model group and the sham-MA group (all P<0.05). Compared with the model group and the sham-MA group, the expression of Bax was significantly lower and the expression of Bcl-2 was significantly higher in the MA group (all P<0.05).

Conclusion

MA therapy can lengthen the sleep time in sleep-deprived rats and improve learning and memory impairments induced by sleep deprivation, and the underlying mechanism may be associated with the enhancement of antioxidant capacity in the prefrontal cortex and the inhibition of hippocampal neuronal apoptosis.

【摘要】

目的: 探究针刺是否可以改善慢性睡眠剥夺诱发的睡眠、情绪障碍及认知损害, 及其与前额叶皮质氧化应激损伤抑制的关系。方法: 将52只雄性Sprague-Dawley大鼠随机分入对照组(n=10), 模型组(n=14), 针刺组(n=14)及假针刺组(n=14)。除对照组外, 其余三组通过改良多平台水环境法建立慢性睡眠剥夺模型。针刺组及假针刺组大鼠分别接受相应干预。建模和干预后, 四组大鼠均接受三种行为测试, 即通过实验室动物能量代谢检测系统(CLAMS)进行睡眠行为监控, 莫里斯水迷宫测试(MWM)和旷场试验(OFT)。行为学实验后进行氧自由基水平检测, 并采用蛋白质免疫印迹法(WB)检测Bax及Bcl-2的表达水平。结果: 针刺组24 h内睡眠时间较模型组及假针刺组显著增长(均P<0.05)。MWM定向导航试验第1天, 对照组、针刺组和假针刺组的逃逸潜伏期无显著差异(P>0.05), 且均明显短于模型组(均P<0.05)。试验第4天, 针刺组逃逸潜伏期显著短于模型组及假针刺组(均P<0.05); 同时, 在空间探索试验中, 针刺组的表现也显著优于模型组及假针刺组(均P<0.05)。OFT中, 与对照组相比, 其他三组的水平运动得分显著下降(均P<0.05)。其中, 模型组及假针刺组的得分下降程度较针刺组更明显(均P<0.05)。与模型组及假针刺组比较, 针刺组超氧化物歧化酶(SOD)含量显著升高, 丙二醛(MDA)含量明显降低(均P<0.05)。与模型组及假针刺组比较, 针刺组Bax表达水平明显降低, Bcl-2表达水平显著升高(均P<0.05)。结论: 针刺疗法可延长睡眠剥夺大鼠睡眠时间, 改善睡眠剥夺引起的学习及记忆障碍, 其机制可能与增强前额叶皮质的抗氧化能力及抑制海马神经元凋亡有关。

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Acknowledgments

This work was supported by Natural Science Foundation of Shanghai (上海市自然科学基金项目, No. 1 7ZR1428100); Traditional Chinese Medicine Science and Technology Innovation Project of Shanghai Health and Family Planning Commission: Mobile Internet-based Guidance Platform of ‘Preventive Treatment of Insomnia’ (Chronic Disease Management) [上海市卫生和计划生育委员会中医药科技创新项目-基于移动互联网的失眠症 “治未病” 康复预防 (慢病管理) 指导平台, No. ZYKC20161016]; Special Project for Clinical Research, Shanghai Municipal Health Commission (上海市卫生和计划生育委员会临床研究专项, No. 20174Y0009).

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Authors and Affiliations

  1. Department of Nursing, School of International Medical Technology, Shanghai Sanda University, Shanghai, 201209, China

    Zhao Fei-yi  (赵非一), Xu Yan  (徐燕), Yue Li-ping  (岳立萍) & Chen Fang-lei  (陈方蕾)

  2. Institute of Acupuncture and Moxibustion, China Academy of Chinese Medical Sciences, Beijing, 100700, China

    Guo Sheng-nan  (郭盛楠)

  3. Shanghai Municipal Hospital of Traditional Chinese Medicine Affiliated to Shanghai University of Traditional Chinese Medicine, Shanghai, 200071, China

    Xu Hong  (许红), Wang Guo-hua  (王国华) & Chen Si-han  (陈思翰)

  4. School of Public Health, Shanghai University of Traditional Chinese Medicine, Shanghai, 201203, China

    Song Hua-ling  (宋花玲)

  5. Yangpu Hospital, Tongji University School of Medicine, Shanghai, 200090, China

    Fu Qiang-qiang  (付强强)

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  1. Zhao Fei-yi  (赵非一)
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Correspondence to Fu Qiang-qiang  (付强强).

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Author: Zhao Fei-yi, PhD candidate, lecturer, resident physician

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Fei-yi, Z., Sheng-nan, G., Yan, X. et al. Investigation of acupuncture in improving sleep, cognitive and emotion based on attenuation of oxidative stress in prefrontal cortex in sleep-deprived rats. J. Acupunct. Tuina. Sci. 19, 157–166 (2021). https://doi.org/10.1007/s11726-021-1240-1

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