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...

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Main Authors: Han-Qing Pan, Wen-Hua Zhang, Cai-Zhi Liao, Ye He, Zhi-Ming Xiao, Xia Qin, Wei-Zhu Liu, Na Wang, Jia-Xin Zou, Xiao-Xuan Liu, Bing-Xing Pan
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
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language English
format Article
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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
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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