Yiping Xie , Zui Shen , Xixiao Zhu , Yushuang Pan , Haiju Sun , Mengdi Xie , Qiuzhu Gong , Qunqi Hu , Jie Chen , Zemin Wu , Shuting Zhou , Boyu Liu , Xiaofen He , Boyi Liu , Xiaomei Shao , Jianqiao Fang
{"title":"与慢性神经病理性疼痛诱发的抑郁样而非焦虑样行为相关的下边缘-基底外侧杏仁核回路以及电针的抗抑郁作用","authors":"Yiping Xie , Zui Shen , Xixiao Zhu , Yushuang Pan , Haiju Sun , Mengdi Xie , Qiuzhu Gong , Qunqi Hu , Jie Chen , Zemin Wu , Shuting Zhou , Boyu Liu , Xiaofen He , Boyi Liu , Xiaomei Shao , Jianqiao Fang","doi":"10.1016/j.brainresbull.2024.111092","DOIUrl":null,"url":null,"abstract":"<div><div>Chronic pain, such as neuropathic pain, can lead to anxiety, depression, and other negative emotions, thereby forming comorbidities and increasing the risk of chronic pain over time. Both the infralimbic amygdala (IL) and the basolateral amygdala (BLA) are significantly associated with negative emotions and pain, and they are known to have reciprocal connections. However, the role of IL-BLA circuit pathways in neuropathic pain-induced anxiety and depression remains unexplored. Electroacupuncture (EA) is frequently employed in the treatment of chronic pain and emotional disorders. However, The mechanism by which EA mediates its analgesic and emotion-alleviating effects via the IL-BLA circuit remains uncertain. Here, we used chemogenetic manipulation combined with behavioral tests to detect pain induced anxiety-like and depression-like behaviors. We observed that activation of the IL-BLA circuit by chemogenetic activation induced depression-like behavior of mice. Additionally, we discovered that chemogenetic activation of the IL-BLA circuit successfully prevented the beneficial effects of EA on depression-like behavior brought on by chronic pain in mice with spared nerve injury (SNI). We discovered that SNI-induced depression-like behavior could be mitigated by inhibiting the circuit, and EA had a comparable depressive-relieving effect. Furthermore, the IL-BLA circuit's activation or inhibition had no effect on the anxiety-like feelings brought on by SNI. Overall, our findings identify a specific neural circuit that selectively regulates pain-induced depression-like emotions, without affecting pain-induced anxiety-like emotions. This discovery offers a precise target for future treatments of comorbid pain and depression and provides a plausible explanation for the efficacy of EA in treating depression-like emotions associated with chronic pain.</div></div>","PeriodicalId":9302,"journal":{"name":"Brain Research Bulletin","volume":"218 ","pages":"Article 111092"},"PeriodicalIF":3.5000,"publicationDate":"2024-10-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Infralimbic-basolateral amygdala circuit associated with depression-like not anxiety-like behaviors induced by chronic neuropathic pain and the antidepressant effects of electroacupuncture\",\"authors\":\"Yiping Xie , Zui Shen , Xixiao Zhu , Yushuang Pan , Haiju Sun , Mengdi Xie , Qiuzhu Gong , Qunqi Hu , Jie Chen , Zemin Wu , Shuting Zhou , Boyu Liu , Xiaofen He , Boyi Liu , Xiaomei Shao , Jianqiao Fang\",\"doi\":\"10.1016/j.brainresbull.2024.111092\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<div><div>Chronic pain, such as neuropathic pain, can lead to anxiety, depression, and other negative emotions, thereby forming comorbidities and increasing the risk of chronic pain over time. Both the infralimbic amygdala (IL) and the basolateral amygdala (BLA) are significantly associated with negative emotions and pain, and they are known to have reciprocal connections. However, the role of IL-BLA circuit pathways in neuropathic pain-induced anxiety and depression remains unexplored. Electroacupuncture (EA) is frequently employed in the treatment of chronic pain and emotional disorders. However, The mechanism by which EA mediates its analgesic and emotion-alleviating effects via the IL-BLA circuit remains uncertain. Here, we used chemogenetic manipulation combined with behavioral tests to detect pain induced anxiety-like and depression-like behaviors. We observed that activation of the IL-BLA circuit by chemogenetic activation induced depression-like behavior of mice. Additionally, we discovered that chemogenetic activation of the IL-BLA circuit successfully prevented the beneficial effects of EA on depression-like behavior brought on by chronic pain in mice with spared nerve injury (SNI). We discovered that SNI-induced depression-like behavior could be mitigated by inhibiting the circuit, and EA had a comparable depressive-relieving effect. Furthermore, the IL-BLA circuit's activation or inhibition had no effect on the anxiety-like feelings brought on by SNI. Overall, our findings identify a specific neural circuit that selectively regulates pain-induced depression-like emotions, without affecting pain-induced anxiety-like emotions. This discovery offers a precise target for future treatments of comorbid pain and depression and provides a plausible explanation for the efficacy of EA in treating depression-like emotions associated with chronic pain.</div></div>\",\"PeriodicalId\":9302,\"journal\":{\"name\":\"Brain Research Bulletin\",\"volume\":\"218 \",\"pages\":\"Article 111092\"},\"PeriodicalIF\":3.5000,\"publicationDate\":\"2024-10-05\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Brain Research Bulletin\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://www.sciencedirect.com/science/article/pii/S0361923024002260\",\"RegionNum\":3,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q2\",\"JCRName\":\"NEUROSCIENCES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Brain Research Bulletin","FirstCategoryId":"3","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0361923024002260","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
引用次数: 0
摘要
慢性疼痛,如神经性疼痛,可导致焦虑、抑郁和其他负面情绪,从而形成合并症,并随着时间的推移增加慢性疼痛的风险。下边缘杏仁核(IL)和基底外侧杏仁核(BLA)都与负面情绪和疼痛密切相关,而且已知它们之间存在相互联系。然而,IL-BLA回路通路在神经病理性疼痛诱发的焦虑和抑郁中的作用仍未得到探讨。电针(EA)经常被用于治疗慢性疼痛和情绪障碍。然而,EA通过IL-BLA回路介导其镇痛和缓解情绪作用的机制仍不确定。在这里,我们使用化学遗传学操作结合行为测试来检测疼痛诱导的焦虑样和抑郁样行为。我们观察到,通过化学基因激活 IL-BLA 回路会诱发小鼠的抑郁样行为。此外,我们还发现,化学基因激活 IL-BLA 环路成功地阻止了 EA 对神经损伤(SNI)小鼠因慢性疼痛而产生的抑郁样行为的有益影响。我们发现,SNI诱导的抑郁样行为可以通过抑制该回路得到缓解,而EA具有类似的抑郁缓解效果。此外,IL-BLA回路的激活或抑制对SNI引起的焦虑样感觉没有影响。总之,我们的研究结果发现了一个特定的神经回路,它能选择性地调节疼痛引起的抑郁样情绪,而不影响疼痛引起的焦虑样情绪。这一发现为未来治疗合并疼痛和抑郁提供了一个精确的靶点,并为 EA 有效治疗与慢性疼痛相关的抑郁样情绪提供了一个合理的解释。
Infralimbic-basolateral amygdala circuit associated with depression-like not anxiety-like behaviors induced by chronic neuropathic pain and the antidepressant effects of electroacupuncture
Chronic pain, such as neuropathic pain, can lead to anxiety, depression, and other negative emotions, thereby forming comorbidities and increasing the risk of chronic pain over time. Both the infralimbic amygdala (IL) and the basolateral amygdala (BLA) are significantly associated with negative emotions and pain, and they are known to have reciprocal connections. However, the role of IL-BLA circuit pathways in neuropathic pain-induced anxiety and depression remains unexplored. Electroacupuncture (EA) is frequently employed in the treatment of chronic pain and emotional disorders. However, The mechanism by which EA mediates its analgesic and emotion-alleviating effects via the IL-BLA circuit remains uncertain. Here, we used chemogenetic manipulation combined with behavioral tests to detect pain induced anxiety-like and depression-like behaviors. We observed that activation of the IL-BLA circuit by chemogenetic activation induced depression-like behavior of mice. Additionally, we discovered that chemogenetic activation of the IL-BLA circuit successfully prevented the beneficial effects of EA on depression-like behavior brought on by chronic pain in mice with spared nerve injury (SNI). We discovered that SNI-induced depression-like behavior could be mitigated by inhibiting the circuit, and EA had a comparable depressive-relieving effect. Furthermore, the IL-BLA circuit's activation or inhibition had no effect on the anxiety-like feelings brought on by SNI. Overall, our findings identify a specific neural circuit that selectively regulates pain-induced depression-like emotions, without affecting pain-induced anxiety-like emotions. This discovery offers a precise target for future treatments of comorbid pain and depression and provides a plausible explanation for the efficacy of EA in treating depression-like emotions associated with chronic pain.
期刊介绍:
The Brain Research Bulletin (BRB) aims to publish novel work that advances our knowledge of molecular and cellular mechanisms that underlie neural network properties associated with behavior, cognition and other brain functions during neurodevelopment and in the adult. Although clinical research is out of the Journal''s scope, the BRB also aims to publish translation research that provides insight into biological mechanisms and processes associated with neurodegeneration mechanisms, neurological diseases and neuropsychiatric disorders. The Journal is especially interested in research using novel methodologies, such as optogenetics, multielectrode array recordings and life imaging in wild-type and genetically-modified animal models, with the goal to advance our understanding of how neurons, glia and networks function in vivo.