Different Synaptic Plasticity After Physiological and Psychological Stress in the Anterior Insular Cortex in an Observational Fear Mouse Model

Post-traumatic stress disorder (PTSD) can be triggered not only in people who have personally experienced traumatic events but also in those who witness them. Physiological and psychological stress can have different effects on neural activity, but little is known about the underlying mechanisms. Th...

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Main Authors: Wenlong Shi, Yuan Fu, Tianyao Shi, Wenxia Zhou
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-05-01
Series:Frontiers in Synaptic Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnsyn.2022.851015/full
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author Wenlong Shi
Yuan Fu
Yuan Fu
Tianyao Shi
Wenxia Zhou
Wenxia Zhou
author_facet Wenlong Shi
Yuan Fu
Yuan Fu
Tianyao Shi
Wenxia Zhou
Wenxia Zhou
author_sort Wenlong Shi
collection DOAJ
description Post-traumatic stress disorder (PTSD) can be triggered not only in people who have personally experienced traumatic events but also in those who witness them. Physiological and psychological stress can have different effects on neural activity, but little is known about the underlying mechanisms. There is ample evidence that the insular cortex, especially the anterior insular cortex (aIC), is critical to both the sensory and emotional experience of pain. It is therefore worthwhile to explore the effects of direct and indirect stress on the synaptic plasticity of the aIC. Here, we used a mouse model of observational fear to mimic direct suffering (Demonstrator, DM) and witnessing (Observer, OB) of traumatic events. After observational fear training, using a 64-channel recording system, we showed that both DM and OB mice exhibited a decreased ratio of paired-pulse with intervals of 50 ms in the superficial layers of the aIC but not in the deep layers. We found that theta-burst stimulation (TBS)–induced long-term potentiation (LTP) in OB mice was significantly higher than in DM mice, and the recruitment of synaptic responses occurred only in OB mice. Compared with naive mice, OB mice showed stronger recruitment and higher amplitude in the superficial layers of the aIC. We also used low-frequency stimulation (LFS) to induce long-term depression (LTD). OB mice showed greater LTD in both the superficial and deep layers of the aIC than naive mice, but no significant difference was found between OB and DM mice. These results provide insights into the changes in synaptic plasticity in the aIC after physiological and psychological stress, and suggest that different types of stress may have different mechanisms. Furthermore, identification of the possible causes of the differences in stress could help treat stress-related disorders.
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spelling doaj.art-370f2f1446284e92a92c48007a43963f2022-12-22T00:11:40ZengFrontiers Media S.A.Frontiers in Synaptic Neuroscience1663-35632022-05-011410.3389/fnsyn.2022.851015851015Different Synaptic Plasticity After Physiological and Psychological Stress in the Anterior Insular Cortex in an Observational Fear Mouse ModelWenlong Shi0Yuan Fu1Yuan Fu2Tianyao Shi3Wenxia Zhou4Wenxia Zhou5State Key Laboratory of Toxicology and Medical Countermeasures, Beijing Institute of Pharmacology and Toxicology, Beijing, ChinaState Key Laboratory of Toxicology and Medical Countermeasures, Beijing Institute of Pharmacology and Toxicology, Beijing, ChinaNanjing University of Chinese Medicine, Nanjing, ChinaState Key Laboratory of Toxicology and Medical Countermeasures, Beijing Institute of Pharmacology and Toxicology, Beijing, ChinaState Key Laboratory of Toxicology and Medical Countermeasures, Beijing Institute of Pharmacology and Toxicology, Beijing, ChinaNanjing University of Chinese Medicine, Nanjing, ChinaPost-traumatic stress disorder (PTSD) can be triggered not only in people who have personally experienced traumatic events but also in those who witness them. Physiological and psychological stress can have different effects on neural activity, but little is known about the underlying mechanisms. There is ample evidence that the insular cortex, especially the anterior insular cortex (aIC), is critical to both the sensory and emotional experience of pain. It is therefore worthwhile to explore the effects of direct and indirect stress on the synaptic plasticity of the aIC. Here, we used a mouse model of observational fear to mimic direct suffering (Demonstrator, DM) and witnessing (Observer, OB) of traumatic events. After observational fear training, using a 64-channel recording system, we showed that both DM and OB mice exhibited a decreased ratio of paired-pulse with intervals of 50 ms in the superficial layers of the aIC but not in the deep layers. We found that theta-burst stimulation (TBS)–induced long-term potentiation (LTP) in OB mice was significantly higher than in DM mice, and the recruitment of synaptic responses occurred only in OB mice. Compared with naive mice, OB mice showed stronger recruitment and higher amplitude in the superficial layers of the aIC. We also used low-frequency stimulation (LFS) to induce long-term depression (LTD). OB mice showed greater LTD in both the superficial and deep layers of the aIC than naive mice, but no significant difference was found between OB and DM mice. These results provide insights into the changes in synaptic plasticity in the aIC after physiological and psychological stress, and suggest that different types of stress may have different mechanisms. Furthermore, identification of the possible causes of the differences in stress could help treat stress-related disorders.https://www.frontiersin.org/articles/10.3389/fnsyn.2022.851015/fullpsychological stressphysiological stressanterior insular cortexlong-term potentiationlong-term depressionmultielectrode array
spellingShingle Wenlong Shi
Yuan Fu
Yuan Fu
Tianyao Shi
Wenxia Zhou
Wenxia Zhou
Different Synaptic Plasticity After Physiological and Psychological Stress in the Anterior Insular Cortex in an Observational Fear Mouse Model
Frontiers in Synaptic Neuroscience
psychological stress
physiological stress
anterior insular cortex
long-term potentiation
long-term depression
multielectrode array
title Different Synaptic Plasticity After Physiological and Psychological Stress in the Anterior Insular Cortex in an Observational Fear Mouse Model
title_full Different Synaptic Plasticity After Physiological and Psychological Stress in the Anterior Insular Cortex in an Observational Fear Mouse Model
title_fullStr Different Synaptic Plasticity After Physiological and Psychological Stress in the Anterior Insular Cortex in an Observational Fear Mouse Model
title_full_unstemmed Different Synaptic Plasticity After Physiological and Psychological Stress in the Anterior Insular Cortex in an Observational Fear Mouse Model
title_short Different Synaptic Plasticity After Physiological and Psychological Stress in the Anterior Insular Cortex in an Observational Fear Mouse Model
title_sort different synaptic plasticity after physiological and psychological stress in the anterior insular cortex in an observational fear mouse model
topic psychological stress
physiological stress
anterior insular cortex
long-term potentiation
long-term depression
multielectrode array
url https://www.frontiersin.org/articles/10.3389/fnsyn.2022.851015/full
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