Posterior basolateral amygdala to ventral hippocampal CA1 drives approach behaviour to exert an anxiolytic effect
The basolateral amygdala (BLA) and ventral hippocampal CA1 (vCA1) are cellularly and functionally diverse along their anterior–posterior and superficial-deep axes. Here, we find that anterior BLA (aBLA) and posterior BLA (pBLA) innervate deep-layer calbindin1-negative (Calb1−) and superficial-layer...
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| Published in | Nature communications Vol. 11; no. 1; pp. 183 - 15 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
10.01.2020
Nature Publishing Group Nature Portfolio |
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| Abstract | The basolateral amygdala (BLA) and ventral hippocampal CA1 (vCA1) are cellularly and functionally diverse along their anterior–posterior and superficial-deep axes. Here, we find that anterior BLA (aBLA) and posterior BLA (pBLA) innervate deep-layer calbindin1-negative (Calb1−) and superficial-layer calbindin1-positive neurons (Calb1+) in vCA1, respectively. Photostimulation of pBLA–vCA1 inputs has an anxiolytic effect in mice, promoting approach behaviours during conflict exploratory tasks. By contrast, stimulating aBLA–vCA1 inputs induces anxiety-like behaviour resulting in fewer approaches. During conflict stages of the elevated plus maze task vCA1
Calb1+
neurons are preferentially activated at the open-to-closed arm transition, and photostimulation of vCA1
Calb1+
neurons at decision-making zones promotes approach with fewer retreats. In the APP/PS1 mouse model of Alzheimer’s disease, which shows anxiety-like behaviour, photostimulating the pBLA–vCA1
Calb1+
circuit ameliorates the anxiety in a Calb1-dependent manner. These findings suggest the pBLA–vCA1
Calb1+
circuit from heterogeneous BLA–vCA1 connections drives approach behaviour to reduce anxiety-like behaviour.
Projections from the anterior and posterior basolateral amygdala (pBLA) to the ventral hippocampus CA1 (vCA1) are heterogenous. Here the authors show that activating the pathway from pBLA to vCA1 calbindin 1 positive neurons has an anxiolytic effect in approach-avoidance tasks in mice. |
|---|---|
| AbstractList | The basolateral amygdala (BLA) and ventral hippocampal CA1 (vCA1) are cellularly and functionally diverse along their anterior-posterior and superficial-deep axes. Here, we find that anterior BLA (aBLA) and posterior BLA (pBLA) innervate deep-layer calbindin1-negative (Calb1-) and superficial-layer calbindin1-positive neurons (Calb1+) in vCA1, respectively. Photostimulation of pBLA-vCA1 inputs has an anxiolytic effect in mice, promoting approach behaviours during conflict exploratory tasks. By contrast, stimulating aBLA-vCA1 inputs induces anxiety-like behaviour resulting in fewer approaches. During conflict stages of the elevated plus maze task vCA1Calb1+ neurons are preferentially activated at the open-to-closed arm transition, and photostimulation of vCA1Calb1+ neurons at decision-making zones promotes approach with fewer retreats. In the APP/PS1 mouse model of Alzheimer's disease, which shows anxiety-like behaviour, photostimulating the pBLA-vCA1Calb1+ circuit ameliorates the anxiety in a Calb1-dependent manner. These findings suggest the pBLA-vCA1Calb1+ circuit from heterogeneous BLA-vCA1 connections drives approach behaviour to reduce anxiety-like behaviour.The basolateral amygdala (BLA) and ventral hippocampal CA1 (vCA1) are cellularly and functionally diverse along their anterior-posterior and superficial-deep axes. Here, we find that anterior BLA (aBLA) and posterior BLA (pBLA) innervate deep-layer calbindin1-negative (Calb1-) and superficial-layer calbindin1-positive neurons (Calb1+) in vCA1, respectively. Photostimulation of pBLA-vCA1 inputs has an anxiolytic effect in mice, promoting approach behaviours during conflict exploratory tasks. By contrast, stimulating aBLA-vCA1 inputs induces anxiety-like behaviour resulting in fewer approaches. During conflict stages of the elevated plus maze task vCA1Calb1+ neurons are preferentially activated at the open-to-closed arm transition, and photostimulation of vCA1Calb1+ neurons at decision-making zones promotes approach with fewer retreats. In the APP/PS1 mouse model of Alzheimer's disease, which shows anxiety-like behaviour, photostimulating the pBLA-vCA1Calb1+ circuit ameliorates the anxiety in a Calb1-dependent manner. These findings suggest the pBLA-vCA1Calb1+ circuit from heterogeneous BLA-vCA1 connections drives approach behaviour to reduce anxiety-like behaviour. The basolateral amygdala (BLA) and ventral hippocampal CA1 (vCA1) are cellularly and functionally diverse along their anterior-posterior and superficial-deep axes. Here, we find that anterior BLA (aBLA) and posterior BLA (pBLA) innervate deep-layer calbindin1-negative (Calb1-) and superficial-layer calbindin1-positive neurons (Calb1+) in vCA1, respectively. Photostimulation of pBLA-vCA1 inputs has an anxiolytic effect in mice, promoting approach behaviours during conflict exploratory tasks. By contrast, stimulating aBLA-vCA1 inputs induces anxiety-like behaviour resulting in fewer approaches. During conflict stages of the elevated plus maze task vCA1 neurons are preferentially activated at the open-to-closed arm transition, and photostimulation of vCA1 neurons at decision-making zones promotes approach with fewer retreats. In the APP/PS1 mouse model of Alzheimer's disease, which shows anxiety-like behaviour, photostimulating the pBLA-vCA1 circuit ameliorates the anxiety in a Calb1-dependent manner. These findings suggest the pBLA-vCA1 circuit from heterogeneous BLA-vCA1 connections drives approach behaviour to reduce anxiety-like behaviour. The basolateral amygdala (BLA) and ventral hippocampal CA1 (vCA1) are cellularly and functionally diverse along their anterior–posterior and superficial-deep axes. Here, we find that anterior BLA (aBLA) and posterior BLA (pBLA) innervate deep-layer calbindin1-negative (Calb1−) and superficial-layer calbindin1-positive neurons (Calb1+) in vCA1, respectively. Photostimulation of pBLA–vCA1 inputs has an anxiolytic effect in mice, promoting approach behaviours during conflict exploratory tasks. By contrast, stimulating aBLA–vCA1 inputs induces anxiety-like behaviour resulting in fewer approaches. During conflict stages of the elevated plus maze task vCA1 Calb1+ neurons are preferentially activated at the open-to-closed arm transition, and photostimulation of vCA1 Calb1+ neurons at decision-making zones promotes approach with fewer retreats. In the APP/PS1 mouse model of Alzheimer’s disease, which shows anxiety-like behaviour, photostimulating the pBLA–vCA1 Calb1+ circuit ameliorates the anxiety in a Calb1-dependent manner. These findings suggest the pBLA–vCA1 Calb1+ circuit from heterogeneous BLA–vCA1 connections drives approach behaviour to reduce anxiety-like behaviour. The basolateral amygdala (BLA) and ventral hippocampal CA1 (vCA1) are cellularly and functionally diverse along their anterior–posterior and superficial-deep axes. Here, we find that anterior BLA (aBLA) and posterior BLA (pBLA) innervate deep-layer calbindin1-negative (Calb1−) and superficial-layer calbindin1-positive neurons (Calb1+) in vCA1, respectively. Photostimulation of pBLA–vCA1 inputs has an anxiolytic effect in mice, promoting approach behaviours during conflict exploratory tasks. By contrast, stimulating aBLA–vCA1 inputs induces anxiety-like behaviour resulting in fewer approaches. During conflict stages of the elevated plus maze task vCA1 Calb1+ neurons are preferentially activated at the open-to-closed arm transition, and photostimulation of vCA1 Calb1+ neurons at decision-making zones promotes approach with fewer retreats. In the APP/PS1 mouse model of Alzheimer’s disease, which shows anxiety-like behaviour, photostimulating the pBLA–vCA1 Calb1+ circuit ameliorates the anxiety in a Calb1-dependent manner. These findings suggest the pBLA–vCA1 Calb1+ circuit from heterogeneous BLA–vCA1 connections drives approach behaviour to reduce anxiety-like behaviour. Projections from the anterior and posterior basolateral amygdala (pBLA) to the ventral hippocampus CA1 (vCA1) are heterogenous. Here the authors show that activating the pathway from pBLA to vCA1 calbindin 1 positive neurons has an anxiolytic effect in approach-avoidance tasks in mice. Projections from the anterior and posterior basolateral amygdala (pBLA) to the ventral hippocampus CA1 (vCA1) are heterogenous. Here the authors show that activating the pathway from pBLA to vCA1 calbindin 1 positive neurons has an anxiolytic effect in approach-avoidance tasks in mice. The basolateral amygdala (BLA) and ventral hippocampal CA1 (vCA1) are cellularly and functionally diverse along their anterior–posterior and superficial-deep axes. Here, we find that anterior BLA (aBLA) and posterior BLA (pBLA) innervate deep-layer calbindin1-negative (Calb1−) and superficial-layer calbindin1-positive neurons (Calb1+) in vCA1, respectively. Photostimulation of pBLA–vCA1 inputs has an anxiolytic effect in mice, promoting approach behaviours during conflict exploratory tasks. By contrast, stimulating aBLA–vCA1 inputs induces anxiety-like behaviour resulting in fewer approaches. During conflict stages of the elevated plus maze task vCA1Calb1+ neurons are preferentially activated at the open-to-closed arm transition, and photostimulation of vCA1Calb1+ neurons at decision-making zones promotes approach with fewer retreats. In the APP/PS1 mouse model of Alzheimer’s disease, which shows anxiety-like behaviour, photostimulating the pBLA–vCA1Calb1+ circuit ameliorates the anxiety in a Calb1-dependent manner. These findings suggest the pBLA–vCA1Calb1+ circuit from heterogeneous BLA–vCA1 connections drives approach behaviour to reduce anxiety-like behaviour.Projections from the anterior and posterior basolateral amygdala (pBLA) to the ventral hippocampus CA1 (vCA1) are heterogenous. Here the authors show that activating the pathway from pBLA to vCA1 calbindin 1 positive neurons has an anxiolytic effect in approach-avoidance tasks in mice. |
| ArticleNumber | 183 |
| Author | Wu, Dongqin Xiong, Rui Zhang, Xiaohui Wang, Xin Ke, Dan Zhang, Si Liu, Gongping Jiang, Tao Zeng, Wenbo Lei, Huiyang Guo, Jing Gao, Di Li, Shihong Yang, Ying Li, Ruining Gao, Yang Li, Honglian Pi, Guilin Yang, Xifei Luo, Min–Hua Wang, Jian–Zhi Wang, Yali Yin, Taoyuan He, Ting Yu, Huiling |
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Technology – sequence: 4 givenname: Yali surname: Wang fullname: Wang, Yali organization: Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Ministry of Education of China and Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Department of Physiology and Neurology, Key Laboratory for Brain Research of Henan Province, Xinxiang Medical University – sequence: 5 givenname: Huiyang orcidid: 0000-0002-9157-7301 surname: Lei fullname: Lei, Huiyang organization: Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Ministry of Education of China and Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology – sequence: 6 givenname: Wenbo orcidid: 0000-0002-1334-2726 surname: Zeng fullname: Zeng, Wenbo organization: State Key Laboratory of Virology, CAS Center for Excellence in Brain Science and Intelligence Technology (CEBSIT), Wuhan Institute of Virology, Chinese Academy of Sciences – sequence: 7 givenname: Yang orcidid: 0000-0003-1707-9053 surname: Gao fullname: Gao, Yang organization: Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Ministry of Education of China and Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology – sequence: 8 givenname: Huiling orcidid: 0000-0003-3098-9692 surname: Yu fullname: Yu, Huiling organization: Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Ministry of Education of China and Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology – sequence: 9 givenname: Rui orcidid: 0000-0003-3268-9618 surname: Xiong fullname: Xiong, Rui organization: Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Ministry of Education of China and Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology – sequence: 10 givenname: Tao surname: Jiang fullname: Jiang, Tao organization: Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Ministry of Education of China and Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology – sequence: 11 givenname: Shihong orcidid: 0000-0002-2241-9609 surname: Li fullname: Li, Shihong organization: Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Ministry of Education of China and Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology – sequence: 12 givenname: Xin orcidid: 0000-0001-7440-3150 surname: Wang fullname: Wang, Xin organization: Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Ministry of Education of China and Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology – sequence: 13 givenname: Jing surname: Guo fullname: Guo, Jing organization: Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Ministry of Education of China and Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology – sequence: 14 givenname: Si orcidid: 0000-0003-2615-8650 surname: Zhang fullname: Zhang, Si organization: Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Ministry of Education of China and Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology – sequence: 15 givenname: Taoyuan orcidid: 0000-0003-0838-9746 surname: Yin fullname: Yin, Taoyuan organization: Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Ministry of Education of China and Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology – sequence: 16 givenname: Ting orcidid: 0000-0001-6171-8225 surname: He fullname: He, Ting organization: Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Ministry of Education of China and Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology – sequence: 17 givenname: Dan surname: Ke fullname: Ke, Dan organization: Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Ministry of Education of China and Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology – sequence: 18 givenname: Ruining orcidid: 0000-0003-1236-0057 surname: Li fullname: Li, Ruining organization: Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Ministry of Education of China and Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology – sequence: 19 givenname: Honglian surname: Li fullname: Li, Honglian organization: Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Ministry of Education of China and Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology – sequence: 20 givenname: Gongping surname: Liu fullname: Liu, Gongping organization: Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Ministry of Education of China and Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology – sequence: 21 givenname: Xifei orcidid: 0000-0002-9000-7016 surname: Yang fullname: Yang, Xifei organization: Key Laboratory of Modern Toxicology of Shenzhen, Shenzhen Centre for Disease Control and Prevention – sequence: 22 givenname: Min–Hua orcidid: 0000-0001-9352-0643 surname: Luo fullname: Luo, Min–Hua organization: State Key Laboratory of Virology, CAS Center for Excellence in Brain Science and Intelligence Technology (CEBSIT), Wuhan Institute of Virology, Chinese Academy of Sciences – sequence: 23 givenname: Xiaohui surname: Zhang fullname: Zhang, Xiaohui organization: State Key Laboratory of Cognitive Neuroscience & Learning and IDG/McGovern Institute for Brain Research, Beijing Normal University – sequence: 24 givenname: Ying orcidid: 0000-0002-9479-4766 surname: Yang fullname: Yang, Ying email: yingyang@hust.edu.cn organization: Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Ministry of Education of China and Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology – sequence: 25 givenname: Jian–Zhi orcidid: 0000-0002-0181-4415 surname: Wang fullname: Wang, Jian–Zhi email: wangjz@mail.hust.edu.cn organization: Department of Pathophysiology, School of Basic Medicine, Key Laboratory of Ministry of Education of China and Hubei Province for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Co–innovation Center of Neuroregeneration, Nantong University |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31924799$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | The Author(s) 2020 This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. |
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| DOI | 10.1038/s41467-019-13919-3 |
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| Snippet | The basolateral amygdala (BLA) and ventral hippocampal CA1 (vCA1) are cellularly and functionally diverse along their anterior–posterior and superficial-deep... The basolateral amygdala (BLA) and ventral hippocampal CA1 (vCA1) are cellularly and functionally diverse along their anterior-posterior and superficial-deep... Projections from the anterior and posterior basolateral amygdala (pBLA) to the ventral hippocampus CA1 (vCA1) are heterogenous. Here the authors show that... |
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| SubjectTerms | 13/1 13/109 14/19 38/35 631/378/3920 64/60 692/699/375/365/1283 692/699/476/1300 82/47 82/80 9/74 Alzheimer Disease - metabolism Alzheimer's disease Amygdala Animal behavior Animals Anti-Anxiety Agents - pharmacology Anxiety Approach behavior Basolateral Nuclear Complex - metabolism Behavior, Animal CA1 Region, Hippocampal - metabolism Calbindin Calbindin 1 - genetics Calbindin 1 - metabolism Choice Behavior - physiology Circuits Decision Making Hippocampus Humanities and Social Sciences Male Maze Learning - physiology Mice Mice, Inbred C57BL Mice, Knockout multidisciplinary Neurodegenerative diseases Neurons Neurons - physiology Posterior basolateral amygdala Presenilin 1 Proteomics Science Science (multidisciplinary) |
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| Title | Posterior basolateral amygdala to ventral hippocampal CA1 drives approach behaviour to exert an anxiolytic effect |
| URI | https://link.springer.com/article/10.1038/s41467-019-13919-3 https://www.ncbi.nlm.nih.gov/pubmed/31924799 https://www.proquest.com/docview/2342999575 https://www.proquest.com/docview/2336248102 https://pubmed.ncbi.nlm.nih.gov/PMC6954243 https://doaj.org/article/c8dce64f4e8c49f1836109d3e2d14530 |
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