Posterior Basolateral Amygdala is a Critical Amygdaloid Area for Temporal Lobe Epilepsy

Abstract The amygdaloid complex consists of multiple nuclei and is a key node in controlling temporal lobe epilepsy (TLE) in both human and animal model studies. However, the specific nucleus in the amygdaloid complex and the neural circuitry governing seizures remain unknown. Here, it is discovered...

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Main Authors: Yan‐Hui Sun, Bo‐Wu Hu, Li‐Heng Tan, Lin Lin, Shu‐Xia Cao, Tan‐Xia Wu, Hao Wang, Bin Yu, Qin Wang, Hong Lian, Jiadong Chen, Xiao‐Ming Li
Format: Article
Language:English
Published: Wiley 2024-12-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202407525
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author Yan‐Hui Sun
Bo‐Wu Hu
Li‐Heng Tan
Lin Lin
Shu‐Xia Cao
Tan‐Xia Wu
Hao Wang
Bin Yu
Qin Wang
Hong Lian
Jiadong Chen
Xiao‐Ming Li
author_facet Yan‐Hui Sun
Bo‐Wu Hu
Li‐Heng Tan
Lin Lin
Shu‐Xia Cao
Tan‐Xia Wu
Hao Wang
Bin Yu
Qin Wang
Hong Lian
Jiadong Chen
Xiao‐Ming Li
author_sort Yan‐Hui Sun
collection DOAJ
description Abstract The amygdaloid complex consists of multiple nuclei and is a key node in controlling temporal lobe epilepsy (TLE) in both human and animal model studies. However, the specific nucleus in the amygdaloid complex and the neural circuitry governing seizures remain unknown. Here, it is discovered that activation of glutamatergic neurons in the posterior basolateral amygdala (pBLA) induces severe seizures and even mortality. The pBLA glutamatergic neurons project collateral connections to multiple brain regions, including the insular cortex (IC), bed nucleus of the stria terminalis (BNST), and central amygdala (CeA). Stimulation of pBLA‐targeted IC neurons triggers seizures, whereas ablation of IC neurons suppresses seizures induced by activating pBLA glutamatergic neurons. GABAergic neurons in the BNST and CeA establish feedback inhibition on pBLA glutamatergic neurons. Deleting GABAergic neurons in the BNST or CeA leads to sporadic seizures, highlighting their role in balancing pBLA activity. Furthermore, pBLA neurons receive glutamatergic inputs from the ventral hippocampal CA1 (vCA1). Ablation of pBLA glutamatergic neurons mitigates both acute and chronic seizures in the intrahippocampal kainic acid‐induced mouse model of TLE. Together, these findings identify the pBLA as a pivotal nucleus in the amygdaloid complex for regulating epileptic seizures in TLE.
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spelling doaj-art-1a2c40ba3ac54dfd8eb1110ae1bab0102025-08-20T02:55:53ZengWileyAdvanced Science2198-38442024-12-011148n/an/a10.1002/advs.202407525Posterior Basolateral Amygdala is a Critical Amygdaloid Area for Temporal Lobe EpilepsyYan‐Hui Sun0Bo‐Wu Hu1Li‐Heng Tan2Lin Lin3Shu‐Xia Cao4Tan‐Xia Wu5Hao Wang6Bin Yu7Qin Wang8Hong Lian9Jiadong Chen10Xiao‐Ming Li11Department of Neurology and Department of Psychiatry of the Second Affiliated Hospital School of Medicine Zhejiang University Hangzhou 310058 ChinaDepartment of Neurology and Department of Psychiatry of the Second Affiliated Hospital School of Medicine Zhejiang University Hangzhou 310058 ChinaDepartment of Neurology and Department of Psychiatry of the Second Affiliated Hospital School of Medicine Zhejiang University Hangzhou 310058 ChinaDepartment of Neurology and Department of Psychiatry of the Second Affiliated Hospital School of Medicine Zhejiang University Hangzhou 310058 ChinaDepartment of Neurobiology of Sir Run Shaw Hospital Zhejiang University Hangzhou 310058 ChinaDepartment of Neurobiology of Sir Run Shaw Hospital Zhejiang University Hangzhou 310058 ChinaNanhu Brain‐computer Interface Institute Hangzhou 311100 ChinaKey Laboratory of Novel Targets Drug Study for Neural Repair of Zhejiang Province School of Medicine Hangzhou City University Hangzhou 310015 ChinaDepartment of Neurology and Department of Psychiatry of the Second Affiliated Hospital School of Medicine Zhejiang University Hangzhou 310058 ChinaResearch Center of System Medicine School of Basic Medical Sciences Zhejiang University Hangzhou 310058 ChinaDepartment of Neurology and Department of Psychiatry of the Second Affiliated Hospital School of Medicine Zhejiang University Hangzhou 310058 ChinaDepartment of Neurology and Department of Psychiatry of the Second Affiliated Hospital School of Medicine Zhejiang University Hangzhou 310058 ChinaAbstract The amygdaloid complex consists of multiple nuclei and is a key node in controlling temporal lobe epilepsy (TLE) in both human and animal model studies. However, the specific nucleus in the amygdaloid complex and the neural circuitry governing seizures remain unknown. Here, it is discovered that activation of glutamatergic neurons in the posterior basolateral amygdala (pBLA) induces severe seizures and even mortality. The pBLA glutamatergic neurons project collateral connections to multiple brain regions, including the insular cortex (IC), bed nucleus of the stria terminalis (BNST), and central amygdala (CeA). Stimulation of pBLA‐targeted IC neurons triggers seizures, whereas ablation of IC neurons suppresses seizures induced by activating pBLA glutamatergic neurons. GABAergic neurons in the BNST and CeA establish feedback inhibition on pBLA glutamatergic neurons. Deleting GABAergic neurons in the BNST or CeA leads to sporadic seizures, highlighting their role in balancing pBLA activity. Furthermore, pBLA neurons receive glutamatergic inputs from the ventral hippocampal CA1 (vCA1). Ablation of pBLA glutamatergic neurons mitigates both acute and chronic seizures in the intrahippocampal kainic acid‐induced mouse model of TLE. Together, these findings identify the pBLA as a pivotal nucleus in the amygdaloid complex for regulating epileptic seizures in TLE.https://doi.org/10.1002/advs.202407525feedback inhibitionneural circuitsposterior basolateral amygdalatemporal lobe epilepsy
spellingShingle Yan‐Hui Sun
Bo‐Wu Hu
Li‐Heng Tan
Lin Lin
Shu‐Xia Cao
Tan‐Xia Wu
Hao Wang
Bin Yu
Qin Wang
Hong Lian
Jiadong Chen
Xiao‐Ming Li
Posterior Basolateral Amygdala is a Critical Amygdaloid Area for Temporal Lobe Epilepsy
Advanced Science
feedback inhibition
neural circuits
posterior basolateral amygdala
temporal lobe epilepsy
title Posterior Basolateral Amygdala is a Critical Amygdaloid Area for Temporal Lobe Epilepsy
title_full Posterior Basolateral Amygdala is a Critical Amygdaloid Area for Temporal Lobe Epilepsy
title_fullStr Posterior Basolateral Amygdala is a Critical Amygdaloid Area for Temporal Lobe Epilepsy
title_full_unstemmed Posterior Basolateral Amygdala is a Critical Amygdaloid Area for Temporal Lobe Epilepsy
title_short Posterior Basolateral Amygdala is a Critical Amygdaloid Area for Temporal Lobe Epilepsy
title_sort posterior basolateral amygdala is a critical amygdaloid area for temporal lobe epilepsy
topic feedback inhibition
neural circuits
posterior basolateral amygdala
temporal lobe epilepsy
url https://doi.org/10.1002/advs.202407525
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