A common neuronal ensemble in nucleus accumbens regulates pain-like behaviour and sleep
Abstract A comorbidity of chronic pain is sleep disturbance. Here, we identify a dual-functional ensemble that regulates both pain-like behaviour induced by chronic constrictive injury or complete Freund’s adjuvant, and sleep wakefulness, in the nucleus accumbens (NAc) in mice. Specifically, a selec...
| Main Authors: | , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2023-08-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-40450-3 |
| _version_ | 1797558046610685952 |
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| author | Haiyan Sun Zhilin Li Zhentong Qiu Yu Shen Qingchen Guo Su-Wan Hu Hai-Lei Ding Shuming An Jun-Li Cao |
| author_facet | Haiyan Sun Zhilin Li Zhentong Qiu Yu Shen Qingchen Guo Su-Wan Hu Hai-Lei Ding Shuming An Jun-Li Cao |
| author_sort | Haiyan Sun |
| collection | DOAJ |
| description | Abstract A comorbidity of chronic pain is sleep disturbance. Here, we identify a dual-functional ensemble that regulates both pain-like behaviour induced by chronic constrictive injury or complete Freund’s adjuvant, and sleep wakefulness, in the nucleus accumbens (NAc) in mice. Specifically, a select population of NAc neurons exhibits increased activity either upon nociceptive stimulation or during wakefulness. Experimental activation of the ensemble neurons exacerbates pain-like (nociceptive) responses and reduces NREM sleep, while inactivation of these neurons produces the opposite effects. Furthermore, NAc ensemble primarily consists of D1 neurons and projects divergently to the ventral tegmental area (VTA) and preoptic area (POA). Silencing an ensemble innervating VTA neurons selectively increases nociceptive responses without affecting sleep, whereas inhibiting ensemble-innervating POA neurons decreases NREM sleep without affecting nociception. These results suggest a common NAc ensemble that encodes chronic pain and controls sleep, and achieves the modality specificity through its divergent downstream circuit targets. |
| first_indexed | 2024-03-10T17:24:54Z |
| format | Article |
| id | doaj.art-f7861fd6906c4753aac8517e135cea6e |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-10T17:24:54Z |
| publishDate | 2023-08-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-f7861fd6906c4753aac8517e135cea6e2023-11-20T10:13:40ZengNature PortfolioNature Communications2041-17232023-08-0114111910.1038/s41467-023-40450-3A common neuronal ensemble in nucleus accumbens regulates pain-like behaviour and sleepHaiyan Sun0Zhilin Li1Zhentong Qiu2Yu Shen3Qingchen Guo4Su-Wan Hu5Hai-Lei Ding6Shuming An7Jun-Li Cao8Jiangsu Province Key Laboratory of Anesthesiology & Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical UniversityJiangsu Province Key Laboratory of Anesthesiology & Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical UniversityJiangsu Province Key Laboratory of Anesthesiology & Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical UniversityJiangsu Province Key Laboratory of Anesthesiology & Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical UniversityJiangsu Province Key Laboratory of Anesthesiology & Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical UniversityJiangsu Province Key Laboratory of Anesthesiology & Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical UniversityJiangsu Province Key Laboratory of Anesthesiology & Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical UniversityJiangsu Province Key Laboratory of Anesthesiology & Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical UniversityJiangsu Province Key Laboratory of Anesthesiology & Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, NMPA Key Laboratory for Research and Evaluation of Narcotic and Psychotropic Drugs, Xuzhou Medical UniversityAbstract A comorbidity of chronic pain is sleep disturbance. Here, we identify a dual-functional ensemble that regulates both pain-like behaviour induced by chronic constrictive injury or complete Freund’s adjuvant, and sleep wakefulness, in the nucleus accumbens (NAc) in mice. Specifically, a select population of NAc neurons exhibits increased activity either upon nociceptive stimulation or during wakefulness. Experimental activation of the ensemble neurons exacerbates pain-like (nociceptive) responses and reduces NREM sleep, while inactivation of these neurons produces the opposite effects. Furthermore, NAc ensemble primarily consists of D1 neurons and projects divergently to the ventral tegmental area (VTA) and preoptic area (POA). Silencing an ensemble innervating VTA neurons selectively increases nociceptive responses without affecting sleep, whereas inhibiting ensemble-innervating POA neurons decreases NREM sleep without affecting nociception. These results suggest a common NAc ensemble that encodes chronic pain and controls sleep, and achieves the modality specificity through its divergent downstream circuit targets.https://doi.org/10.1038/s41467-023-40450-3 |
| spellingShingle | Haiyan Sun Zhilin Li Zhentong Qiu Yu Shen Qingchen Guo Su-Wan Hu Hai-Lei Ding Shuming An Jun-Li Cao A common neuronal ensemble in nucleus accumbens regulates pain-like behaviour and sleep Nature Communications |
| title | A common neuronal ensemble in nucleus accumbens regulates pain-like behaviour and sleep |
| title_full | A common neuronal ensemble in nucleus accumbens regulates pain-like behaviour and sleep |
| title_fullStr | A common neuronal ensemble in nucleus accumbens regulates pain-like behaviour and sleep |
| title_full_unstemmed | A common neuronal ensemble in nucleus accumbens regulates pain-like behaviour and sleep |
| title_short | A common neuronal ensemble in nucleus accumbens regulates pain-like behaviour and sleep |
| title_sort | common neuronal ensemble in nucleus accumbens regulates pain like behaviour and sleep |
| url | https://doi.org/10.1038/s41467-023-40450-3 |
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