Chronic Stress Oppositely Regulates Tonic Inhibition in Thy1-Expressing and Non-expressing Neurons in Amygdala
Chronic or prolonged exposure to stress ranks among the most important socioenvironmental factors contributing to the development of neuropsychiatric diseases, a process generally associated with loss of inhibitory tone in amygdala. Recent studies have identified distinct neuronal circuits within th...
Main Authors: | , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Frontiers Media S.A.
2020-04-01
|
Series: | Frontiers in Neuroscience |
Subjects: | |
Online Access: | https://www.frontiersin.org/article/10.3389/fnins.2020.00299/full |
id |
doaj-a00dd025167c4f518fd1144e72051f8a |
---|---|
record_format |
Article |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Han-Qing Pan Han-Qing Pan Wen-Hua Zhang Wen-Hua Zhang Cai-Zhi Liao Cai-Zhi Liao Ye He Zhi-Ming Xiao Xia Qin Xia Qin Wei-Zhu Liu Wei-Zhu Liu Na Wang Jia-Xin Zou Jia-Xin Zou Xiao-Xuan Liu Xiao-Xuan Liu Bing-Xing Pan Bing-Xing Pan |
spellingShingle |
Han-Qing Pan Han-Qing Pan Wen-Hua Zhang Wen-Hua Zhang Cai-Zhi Liao Cai-Zhi Liao Ye He Zhi-Ming Xiao Xia Qin Xia Qin Wei-Zhu Liu Wei-Zhu Liu Na Wang Jia-Xin Zou Jia-Xin Zou Xiao-Xuan Liu Xiao-Xuan Liu Bing-Xing Pan Bing-Xing Pan Chronic Stress Oppositely Regulates Tonic Inhibition in Thy1-Expressing and Non-expressing Neurons in Amygdala Frontiers in Neuroscience chronic stress amygdala tonic inhibition Thy1 neuronal excitability corticosterone |
author_facet |
Han-Qing Pan Han-Qing Pan Wen-Hua Zhang Wen-Hua Zhang Cai-Zhi Liao Cai-Zhi Liao Ye He Zhi-Ming Xiao Xia Qin Xia Qin Wei-Zhu Liu Wei-Zhu Liu Na Wang Jia-Xin Zou Jia-Xin Zou Xiao-Xuan Liu Xiao-Xuan Liu Bing-Xing Pan Bing-Xing Pan |
author_sort |
Han-Qing Pan |
title |
Chronic Stress Oppositely Regulates Tonic Inhibition in Thy1-Expressing and Non-expressing Neurons in Amygdala |
title_short |
Chronic Stress Oppositely Regulates Tonic Inhibition in Thy1-Expressing and Non-expressing Neurons in Amygdala |
title_full |
Chronic Stress Oppositely Regulates Tonic Inhibition in Thy1-Expressing and Non-expressing Neurons in Amygdala |
title_fullStr |
Chronic Stress Oppositely Regulates Tonic Inhibition in Thy1-Expressing and Non-expressing Neurons in Amygdala |
title_full_unstemmed |
Chronic Stress Oppositely Regulates Tonic Inhibition in Thy1-Expressing and Non-expressing Neurons in Amygdala |
title_sort |
chronic stress oppositely regulates tonic inhibition in thy1-expressing and non-expressing neurons in amygdala |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Neuroscience |
issn |
1662-453X |
publishDate |
2020-04-01 |
description |
Chronic or prolonged exposure to stress ranks among the most important socioenvironmental factors contributing to the development of neuropsychiatric diseases, a process generally associated with loss of inhibitory tone in amygdala. Recent studies have identified distinct neuronal circuits within the basolateral amygdala (BLA) engaged in different emotional processes. However, the potential circuit involved in stress-induced dysregulation of inhibitory tones in BLA remains elusive. Here, a transgenic mouse model expressing yellow fluorescent protein under control of the Thy1 promoter was used to differentiate subpopulations of projection neurons (PNs) within the BLA. We observed that the tonic inhibition in amygdala neurons expressing and not expressing Thy1 (Thy1+/−) was oppositely regulated by chronic social defeat stress (CSDS). In unstressed control mice, the tonic inhibitory currents were significantly stronger in Thy1- PNs than their Thy1+ counterparts. CSDS markedly reduced the currents in Thy1- projection neurons (PNs), but increased that in Thy1+ ones. By contrast, CSDS failed to affect both the phasic A-type γ-aminobutyric acid receptor (GABAAR) currents and GABABR currents in these two PN populations. Moreover, chronic corticosterone administration was sufficient to mimic the effect of CSDS on the tonic inhibition of Thy1+ and Thy1- PNs. As a consequence, the suppression of tonic GABAAR currents on the excitability of Thy1- PNs was weakened by CSDS, but enhanced in Thy1+ PNs. The differential regulation of chronic stress on the tonic inhibition in Thy1+ and Thy1- neurons may orchestrate cell-specific adaptation of amygdala neurons to chronic stress. |
topic |
chronic stress amygdala tonic inhibition Thy1 neuronal excitability corticosterone |
url |
https://www.frontiersin.org/article/10.3389/fnins.2020.00299/full |
work_keys_str_mv |
AT hanqingpan chronicstressoppositelyregulatestonicinhibitioninthy1expressingandnonexpressingneuronsinamygdala AT hanqingpan chronicstressoppositelyregulatestonicinhibitioninthy1expressingandnonexpressingneuronsinamygdala AT wenhuazhang chronicstressoppositelyregulatestonicinhibitioninthy1expressingandnonexpressingneuronsinamygdala AT wenhuazhang chronicstressoppositelyregulatestonicinhibitioninthy1expressingandnonexpressingneuronsinamygdala AT caizhiliao chronicstressoppositelyregulatestonicinhibitioninthy1expressingandnonexpressingneuronsinamygdala AT caizhiliao chronicstressoppositelyregulatestonicinhibitioninthy1expressingandnonexpressingneuronsinamygdala AT yehe chronicstressoppositelyregulatestonicinhibitioninthy1expressingandnonexpressingneuronsinamygdala AT zhimingxiao chronicstressoppositelyregulatestonicinhibitioninthy1expressingandnonexpressingneuronsinamygdala AT xiaqin chronicstressoppositelyregulatestonicinhibitioninthy1expressingandnonexpressingneuronsinamygdala AT xiaqin chronicstressoppositelyregulatestonicinhibitioninthy1expressingandnonexpressingneuronsinamygdala AT weizhuliu chronicstressoppositelyregulatestonicinhibitioninthy1expressingandnonexpressingneuronsinamygdala AT weizhuliu chronicstressoppositelyregulatestonicinhibitioninthy1expressingandnonexpressingneuronsinamygdala AT nawang chronicstressoppositelyregulatestonicinhibitioninthy1expressingandnonexpressingneuronsinamygdala AT jiaxinzou chronicstressoppositelyregulatestonicinhibitioninthy1expressingandnonexpressingneuronsinamygdala AT jiaxinzou chronicstressoppositelyregulatestonicinhibitioninthy1expressingandnonexpressingneuronsinamygdala AT xiaoxuanliu chronicstressoppositelyregulatestonicinhibitioninthy1expressingandnonexpressingneuronsinamygdala AT xiaoxuanliu chronicstressoppositelyregulatestonicinhibitioninthy1expressingandnonexpressingneuronsinamygdala AT bingxingpan chronicstressoppositelyregulatestonicinhibitioninthy1expressingandnonexpressingneuronsinamygdala AT bingxingpan chronicstressoppositelyregulatestonicinhibitioninthy1expressingandnonexpressingneuronsinamygdala |
_version_ |
1724595707754577920 |
spelling |
doaj-a00dd025167c4f518fd1144e72051f8a2020-11-25T03:25:48ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2020-04-011410.3389/fnins.2020.00299514596Chronic Stress Oppositely Regulates Tonic Inhibition in Thy1-Expressing and Non-expressing Neurons in AmygdalaHan-Qing Pan0Han-Qing Pan1Wen-Hua Zhang2Wen-Hua Zhang3Cai-Zhi Liao4Cai-Zhi Liao5Ye He6Zhi-Ming Xiao7Xia Qin8Xia Qin9Wei-Zhu Liu10Wei-Zhu Liu11Na Wang12Jia-Xin Zou13Jia-Xin Zou14Xiao-Xuan Liu15Xiao-Xuan Liu16Bing-Xing Pan17Bing-Xing Pan18Department of Biological Science, School of Life Sciences, Nanchang University, Nanchang, ChinaLaboratory of Fear and Anxiety Disorders, Institutes of Life Science, Nanchang University, Nanchang, ChinaDepartment of Biological Science, School of Life Sciences, Nanchang University, Nanchang, ChinaLaboratory of Fear and Anxiety Disorders, Institutes of Life Science, Nanchang University, Nanchang, ChinaDepartment of Biological Science, School of Life Sciences, Nanchang University, Nanchang, ChinaLaboratory of Fear and Anxiety Disorders, Institutes of Life Science, Nanchang University, Nanchang, ChinaCenter for Medical Experiments, Nanchang University, Nanchang, ChinaLaboratory of Fear and Anxiety Disorders, Institutes of Life Science, Nanchang University, Nanchang, ChinaDepartment of Biological Science, School of Life Sciences, Nanchang University, Nanchang, ChinaLaboratory of Fear and Anxiety Disorders, Institutes of Life Science, Nanchang University, Nanchang, ChinaDepartment of Biological Science, School of Life Sciences, Nanchang University, Nanchang, ChinaLaboratory of Fear and Anxiety Disorders, Institutes of Life Science, Nanchang University, Nanchang, ChinaDepartment of Physiology, Mudanjiang Medical University, Mudanjiang, ChinaDepartment of Biological Science, School of Life Sciences, Nanchang University, Nanchang, ChinaLaboratory of Fear and Anxiety Disorders, Institutes of Life Science, Nanchang University, Nanchang, ChinaDepartment of Biological Science, School of Life Sciences, Nanchang University, Nanchang, ChinaLaboratory of Fear and Anxiety Disorders, Institutes of Life Science, Nanchang University, Nanchang, ChinaDepartment of Biological Science, School of Life Sciences, Nanchang University, Nanchang, ChinaLaboratory of Fear and Anxiety Disorders, Institutes of Life Science, Nanchang University, Nanchang, ChinaChronic or prolonged exposure to stress ranks among the most important socioenvironmental factors contributing to the development of neuropsychiatric diseases, a process generally associated with loss of inhibitory tone in amygdala. Recent studies have identified distinct neuronal circuits within the basolateral amygdala (BLA) engaged in different emotional processes. However, the potential circuit involved in stress-induced dysregulation of inhibitory tones in BLA remains elusive. Here, a transgenic mouse model expressing yellow fluorescent protein under control of the Thy1 promoter was used to differentiate subpopulations of projection neurons (PNs) within the BLA. We observed that the tonic inhibition in amygdala neurons expressing and not expressing Thy1 (Thy1+/−) was oppositely regulated by chronic social defeat stress (CSDS). In unstressed control mice, the tonic inhibitory currents were significantly stronger in Thy1- PNs than their Thy1+ counterparts. CSDS markedly reduced the currents in Thy1- projection neurons (PNs), but increased that in Thy1+ ones. By contrast, CSDS failed to affect both the phasic A-type γ-aminobutyric acid receptor (GABAAR) currents and GABABR currents in these two PN populations. Moreover, chronic corticosterone administration was sufficient to mimic the effect of CSDS on the tonic inhibition of Thy1+ and Thy1- PNs. As a consequence, the suppression of tonic GABAAR currents on the excitability of Thy1- PNs was weakened by CSDS, but enhanced in Thy1+ PNs. The differential regulation of chronic stress on the tonic inhibition in Thy1+ and Thy1- neurons may orchestrate cell-specific adaptation of amygdala neurons to chronic stress.https://www.frontiersin.org/article/10.3389/fnins.2020.00299/fullchronic stressamygdalatonic inhibitionThy1neuronal excitabilitycorticosterone |