ACx-projecting cholinergic neurons in the NB influence the BLA ensembles to modulate the discrimination of auditory fear memory
Abstract Animals need discriminating auditory fear memory (DAFM) to survive, but the related neural circuits of DAFM remain largely unknown. Our study shows that DAFM depends on acetylcholine (ACh) signal in the auditory cortex (ACx), which is projected from the nucleus basalis (NB). At the encoding...
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| Format: | Article |
| Language: | English |
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Nature Publishing Group
2023-03-01
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| Series: | Translational Psychiatry |
| Online Access: | https://doi.org/10.1038/s41398-023-02384-8 |
| _version_ | 1797863500837552128 |
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| author | Yan Yan Da Song Yue Jin Yujun Deng Chunjian Wang Tao Huang Yuanhong Tang Yu Yang Yun Zhang Zhe Wang Zhifang Dong Yuetian Wang Juan Zhao Junjun Ni Hui Li Jun Zhang Yiran Lang Yili Wu Hong Qing Zhenzhen Quan |
| author_facet | Yan Yan Da Song Yue Jin Yujun Deng Chunjian Wang Tao Huang Yuanhong Tang Yu Yang Yun Zhang Zhe Wang Zhifang Dong Yuetian Wang Juan Zhao Junjun Ni Hui Li Jun Zhang Yiran Lang Yili Wu Hong Qing Zhenzhen Quan |
| author_sort | Yan Yan |
| collection | DOAJ |
| description | Abstract Animals need discriminating auditory fear memory (DAFM) to survive, but the related neural circuits of DAFM remain largely unknown. Our study shows that DAFM depends on acetylcholine (ACh) signal in the auditory cortex (ACx), which is projected from the nucleus basalis (NB). At the encoding stage, optogenetic inhibition of cholinergic projections of NB-ACx obfuscates distinct tone-responsive neurons of ACx recognizing from fear-paired tone to fear-unpaired tone signals, while simultaneously regulating the neuronal activity and reactivation of basal lateral amygdala (BLA) engram cells at the retrieval stage. This NBACh-ACx-BLA neural circuit for the modulation of DAFM is especially dependent on the nicotinic ACh receptor (nAChR). A nAChR antagonist reduces DAFM and diminishes the increased magnitude of ACx tone-responsive neuronal activity during the encoding stage. Our data suggest a critical role of NBACh-ACx-BLA neural circuit in DAFM: manipulation of the NB cholinergic projection to the ACx via nAChR during the encoding stage affects the activation of ACx tone-responsive neuron clusters and the BLA engram cells during the retrieval stage, thus modulating the DAFM. |
| first_indexed | 2024-04-09T22:36:29Z |
| format | Article |
| id | doaj.art-cf84139c4aea44f2841dbf16a2eefcba |
| institution | Directory Open Access Journal |
| issn | 2158-3188 |
| language | English |
| last_indexed | 2024-04-09T22:36:29Z |
| publishDate | 2023-03-01 |
| publisher | Nature Publishing Group |
| record_format | Article |
| series | Translational Psychiatry |
| spelling | doaj.art-cf84139c4aea44f2841dbf16a2eefcba2023-03-22T12:27:10ZengNature Publishing GroupTranslational Psychiatry2158-31882023-03-0113111210.1038/s41398-023-02384-8ACx-projecting cholinergic neurons in the NB influence the BLA ensembles to modulate the discrimination of auditory fear memoryYan Yan0Da Song1Yue Jin2Yujun Deng3Chunjian Wang4Tao Huang5Yuanhong Tang6Yu Yang7Yun Zhang8Zhe Wang9Zhifang Dong10Yuetian Wang11Juan Zhao12Junjun Ni13Hui Li14Jun Zhang15Yiran Lang16Yili Wu17Hong Qing18Zhenzhen Quan19Key Laboratory of Molecular Medicine and Biotherapy, School of Life Science, Beijing Institute of TechnologyKey Laboratory of Molecular Medicine and Biotherapy, School of Life Science, Beijing Institute of TechnologyKey Laboratory of Molecular Medicine and Biotherapy, School of Life Science, Beijing Institute of TechnologyKey Laboratory of Molecular Medicine and Biotherapy, School of Life Science, Beijing Institute of TechnologyKey Laboratory of Molecular Medicine and Biotherapy, School of Life Science, Beijing Institute of TechnologyKey Laboratory of Molecular Medicine and Biotherapy, School of Life Science, Beijing Institute of TechnologyKey Laboratory of Molecular Medicine and Biotherapy, School of Life Science, Beijing Institute of TechnologyShandong Key Laboratory of Behavioral Medicine, Shandong Collaborative Innovation Center for Diagnosis, Treatment & Behavioral Interventions of Mental Disorders, School of Mental Health, Jining Medical UniversityAdvanced Innovation Center for Human Brain Protection, Capital Medical University; The National Clinical Research Center for Geriatric Disease, Xuanwu Hospital, Capital Medical UniversityAdvanced Innovation Center for Human Brain Protection, Capital Medical University; The National Clinical Research Center for Geriatric Disease, Xuanwu Hospital, Capital Medical UniversityMinistry of Education Key Laboratory of Child Development and Disorders, National Research Center for Child Health and Disorders, Chongqing Key Laboratory of Translational Medical Research in Cognitive Development and Learning and Memory Disorders, Children’s Hospital of Chongqing Medical UniversityKey Laboratory of Molecular Medicine and Biotherapy, School of Life Science, Beijing Institute of TechnologyKey Laboratory of Molecular Medicine and Biotherapy, School of Life Science, Beijing Institute of TechnologyKey Laboratory of Molecular Medicine and Biotherapy, School of Life Science, Beijing Institute of TechnologyKey Laboratory of Molecular Medicine and Biotherapy, School of Life Science, Beijing Institute of TechnologyKey Laboratory of Molecular Medicine and Biotherapy, School of Life Science, Beijing Institute of TechnologyBeijing Advanced Innovation Center for Intelligent Robots and Systems, Beijing Institute of TechnologyShandong Key Laboratory of Behavioral Medicine, Shandong Collaborative Innovation Center for Diagnosis, Treatment & Behavioral Interventions of Mental Disorders, School of Mental Health, Jining Medical UniversityKey Laboratory of Molecular Medicine and Biotherapy, School of Life Science, Beijing Institute of TechnologyKey Laboratory of Molecular Medicine and Biotherapy, School of Life Science, Beijing Institute of TechnologyAbstract Animals need discriminating auditory fear memory (DAFM) to survive, but the related neural circuits of DAFM remain largely unknown. Our study shows that DAFM depends on acetylcholine (ACh) signal in the auditory cortex (ACx), which is projected from the nucleus basalis (NB). At the encoding stage, optogenetic inhibition of cholinergic projections of NB-ACx obfuscates distinct tone-responsive neurons of ACx recognizing from fear-paired tone to fear-unpaired tone signals, while simultaneously regulating the neuronal activity and reactivation of basal lateral amygdala (BLA) engram cells at the retrieval stage. This NBACh-ACx-BLA neural circuit for the modulation of DAFM is especially dependent on the nicotinic ACh receptor (nAChR). A nAChR antagonist reduces DAFM and diminishes the increased magnitude of ACx tone-responsive neuronal activity during the encoding stage. Our data suggest a critical role of NBACh-ACx-BLA neural circuit in DAFM: manipulation of the NB cholinergic projection to the ACx via nAChR during the encoding stage affects the activation of ACx tone-responsive neuron clusters and the BLA engram cells during the retrieval stage, thus modulating the DAFM.https://doi.org/10.1038/s41398-023-02384-8 |
| spellingShingle | Yan Yan Da Song Yue Jin Yujun Deng Chunjian Wang Tao Huang Yuanhong Tang Yu Yang Yun Zhang Zhe Wang Zhifang Dong Yuetian Wang Juan Zhao Junjun Ni Hui Li Jun Zhang Yiran Lang Yili Wu Hong Qing Zhenzhen Quan ACx-projecting cholinergic neurons in the NB influence the BLA ensembles to modulate the discrimination of auditory fear memory Translational Psychiatry |
| title | ACx-projecting cholinergic neurons in the NB influence the BLA ensembles to modulate the discrimination of auditory fear memory |
| title_full | ACx-projecting cholinergic neurons in the NB influence the BLA ensembles to modulate the discrimination of auditory fear memory |
| title_fullStr | ACx-projecting cholinergic neurons in the NB influence the BLA ensembles to modulate the discrimination of auditory fear memory |
| title_full_unstemmed | ACx-projecting cholinergic neurons in the NB influence the BLA ensembles to modulate the discrimination of auditory fear memory |
| title_short | ACx-projecting cholinergic neurons in the NB influence the BLA ensembles to modulate the discrimination of auditory fear memory |
| title_sort | acx projecting cholinergic neurons in the nb influence the bla ensembles to modulate the discrimination of auditory fear memory |
| url | https://doi.org/10.1038/s41398-023-02384-8 |
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