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Chemogenetic Activation of Astrocytes in the Basolateral Amygdala Contributes to Fear Memory Formation by Modulating the Amygdala–Prefrontal Cortex Communication

The basolateral amygdala (BLA) is one of the key brain areas involved in aversive learning, especially fear memory formation. Studies of aversive learning in the BLA have largely focused on neuronal function, while the role of BLA astrocytes in aversive learning remains largely unknown. In this stud...

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Autores principales: Lei, Zhuogui, Xie, Li, Li, Cheuk Hin, Lam, Yuk Yan, Ramkrishnan, Aruna Surendran, Fu, Zhongqi, Zeng, Xianlin, Liu, Shu, Iqbal, Zafar, Li, Ying
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9181030/
https://www.ncbi.nlm.nih.gov/pubmed/35682767
http://dx.doi.org/10.3390/ijms23116092
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author Lei, Zhuogui
Xie, Li
Li, Cheuk Hin
Lam, Yuk Yan
Ramkrishnan, Aruna Surendran
Fu, Zhongqi
Zeng, Xianlin
Liu, Shu
Iqbal, Zafar
Li, Ying
author_facet Lei, Zhuogui
Xie, Li
Li, Cheuk Hin
Lam, Yuk Yan
Ramkrishnan, Aruna Surendran
Fu, Zhongqi
Zeng, Xianlin
Liu, Shu
Iqbal, Zafar
Li, Ying
author_sort Lei, Zhuogui
collection PubMed
description The basolateral amygdala (BLA) is one of the key brain areas involved in aversive learning, especially fear memory formation. Studies of aversive learning in the BLA have largely focused on neuronal function, while the role of BLA astrocytes in aversive learning remains largely unknown. In this study, we manipulated the BLA astrocytes by expressing the Gq-coupled receptor hM3q and discovered that astrocytic Gq modulation during fear conditioning promoted auditorily cued fear memory but did not affect less stressful memory tasks or induce anxiety-like behavior. Moreover, chemogenetic activation of BLA astrocytes during memory retrieval had no effect on fear memory expression. In addition, astrocytic Gq activation increased c-Fos expression in the BLA and the medial prefrontal cortex (mPFC) during fear conditioning, but not in the home cage. Combining these results with retrograde virus tracing, we found that the activity of mPFC-projecting BLA neurons showed significant enhancement after astrocytic Gq activation during fear conditioning. Electrophysiology recordings showed that activating astrocytic Gq in the BLA promoted spike-field coherence and phase locking percentage, not only within the BLA but also between the BLA and the mPFC. Finally, direct chemogenetic activation of mPFC-projecting BLA neurons during fear conditioning enhanced cued fear memory. Taken together, our data suggest that astrocytes in the BLA may contribute to aversive learning by modulating amygdala–mPFC communication.
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spelling pubmed-91810302022-06-10 Chemogenetic Activation of Astrocytes in the Basolateral Amygdala Contributes to Fear Memory Formation by Modulating the Amygdala–Prefrontal Cortex Communication Lei, Zhuogui Xie, Li Li, Cheuk Hin Lam, Yuk Yan Ramkrishnan, Aruna Surendran Fu, Zhongqi Zeng, Xianlin Liu, Shu Iqbal, Zafar Li, Ying Int J Mol Sci Article The basolateral amygdala (BLA) is one of the key brain areas involved in aversive learning, especially fear memory formation. Studies of aversive learning in the BLA have largely focused on neuronal function, while the role of BLA astrocytes in aversive learning remains largely unknown. In this study, we manipulated the BLA astrocytes by expressing the Gq-coupled receptor hM3q and discovered that astrocytic Gq modulation during fear conditioning promoted auditorily cued fear memory but did not affect less stressful memory tasks or induce anxiety-like behavior. Moreover, chemogenetic activation of BLA astrocytes during memory retrieval had no effect on fear memory expression. In addition, astrocytic Gq activation increased c-Fos expression in the BLA and the medial prefrontal cortex (mPFC) during fear conditioning, but not in the home cage. Combining these results with retrograde virus tracing, we found that the activity of mPFC-projecting BLA neurons showed significant enhancement after astrocytic Gq activation during fear conditioning. Electrophysiology recordings showed that activating astrocytic Gq in the BLA promoted spike-field coherence and phase locking percentage, not only within the BLA but also between the BLA and the mPFC. Finally, direct chemogenetic activation of mPFC-projecting BLA neurons during fear conditioning enhanced cued fear memory. Taken together, our data suggest that astrocytes in the BLA may contribute to aversive learning by modulating amygdala–mPFC communication. MDPI 2022-05-29 /pmc/articles/PMC9181030/ /pubmed/35682767 http://dx.doi.org/10.3390/ijms23116092 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Lei, Zhuogui
Xie, Li
Li, Cheuk Hin
Lam, Yuk Yan
Ramkrishnan, Aruna Surendran
Fu, Zhongqi
Zeng, Xianlin
Liu, Shu
Iqbal, Zafar
Li, Ying
Chemogenetic Activation of Astrocytes in the Basolateral Amygdala Contributes to Fear Memory Formation by Modulating the Amygdala–Prefrontal Cortex Communication
title Chemogenetic Activation of Astrocytes in the Basolateral Amygdala Contributes to Fear Memory Formation by Modulating the Amygdala–Prefrontal Cortex Communication
title_full Chemogenetic Activation of Astrocytes in the Basolateral Amygdala Contributes to Fear Memory Formation by Modulating the Amygdala–Prefrontal Cortex Communication
title_fullStr Chemogenetic Activation of Astrocytes in the Basolateral Amygdala Contributes to Fear Memory Formation by Modulating the Amygdala–Prefrontal Cortex Communication
title_full_unstemmed Chemogenetic Activation of Astrocytes in the Basolateral Amygdala Contributes to Fear Memory Formation by Modulating the Amygdala–Prefrontal Cortex Communication
title_short Chemogenetic Activation of Astrocytes in the Basolateral Amygdala Contributes to Fear Memory Formation by Modulating the Amygdala–Prefrontal Cortex Communication
title_sort chemogenetic activation of astrocytes in the basolateral amygdala contributes to fear memory formation by modulating the amygdala–prefrontal cortex communication
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9181030/
https://www.ncbi.nlm.nih.gov/pubmed/35682767
http://dx.doi.org/10.3390/ijms23116092
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