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Distinctive Regulation of Emotional Behaviors and Fear-Related Gene Expression Responses in Two Extended Amygdala Subnuclei With Similar Molecular Profiles

The central nucleus of the amygdala (CeA) and the lateral division of the bed nucleus of the stria terminalis (BNST) are the two major nuclei of the central extended amygdala that plays essential roles in threat processing, responsible for emotional states such as fear and anxiety. While some studie...

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Autores principales: Ueda, Shuhei, Hosokawa, Masahito, Arikawa, Koji, Takahashi, Kiyofumi, Fujiwara, Mao, Kakita, Manami, Fukada, Taro, Koyama, Hiroaki, Horigane, Shin-ichiro, Itoi, Keiichi, Kakeyama, Masaki, Matsunaga, Hiroko, Takeyama, Haruko, Bito, Haruhiko, Takemoto-Kimura, Sayaka
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8446640/
https://www.ncbi.nlm.nih.gov/pubmed/34539345
http://dx.doi.org/10.3389/fnmol.2021.741895
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author Ueda, Shuhei
Hosokawa, Masahito
Arikawa, Koji
Takahashi, Kiyofumi
Fujiwara, Mao
Kakita, Manami
Fukada, Taro
Koyama, Hiroaki
Horigane, Shin-ichiro
Itoi, Keiichi
Kakeyama, Masaki
Matsunaga, Hiroko
Takeyama, Haruko
Bito, Haruhiko
Takemoto-Kimura, Sayaka
author_facet Ueda, Shuhei
Hosokawa, Masahito
Arikawa, Koji
Takahashi, Kiyofumi
Fujiwara, Mao
Kakita, Manami
Fukada, Taro
Koyama, Hiroaki
Horigane, Shin-ichiro
Itoi, Keiichi
Kakeyama, Masaki
Matsunaga, Hiroko
Takeyama, Haruko
Bito, Haruhiko
Takemoto-Kimura, Sayaka
author_sort Ueda, Shuhei
collection PubMed
description The central nucleus of the amygdala (CeA) and the lateral division of the bed nucleus of the stria terminalis (BNST) are the two major nuclei of the central extended amygdala that plays essential roles in threat processing, responsible for emotional states such as fear and anxiety. While some studies suggested functional differences between these nuclei, others showed anatomical and neurochemical similarities. Despite their complex subnuclear organization, subnuclei-specific functional impact on behavior and their underlying molecular profiles remain obscure. We here constitutively inhibited neurotransmission of protein kinase C-δ-positive (PKCδ+) neurons—a major cell type of the lateral subdivision of the CeA (CeL) and the oval nucleus of the BNST (BNSTov)—and found striking subnuclei-specific effects on fear- and anxiety-related behaviors, respectively. To obtain molecular clues for this dissociation, we conducted RNA sequencing in subnuclei-targeted micropunch samples. The CeL and the BNSTov displayed similar gene expression profiles at the basal level; however, both displayed differential gene expression when animals were exposed to fear-related stimuli, with a more robust expression change in the CeL. These findings provide novel insights into the molecular makeup and differential engagement of distinct subnuclei of the extended amygdala, critical for regulation of threat processing.
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spelling pubmed-84466402021-09-18 Distinctive Regulation of Emotional Behaviors and Fear-Related Gene Expression Responses in Two Extended Amygdala Subnuclei With Similar Molecular Profiles Ueda, Shuhei Hosokawa, Masahito Arikawa, Koji Takahashi, Kiyofumi Fujiwara, Mao Kakita, Manami Fukada, Taro Koyama, Hiroaki Horigane, Shin-ichiro Itoi, Keiichi Kakeyama, Masaki Matsunaga, Hiroko Takeyama, Haruko Bito, Haruhiko Takemoto-Kimura, Sayaka Front Mol Neurosci Molecular Neuroscience The central nucleus of the amygdala (CeA) and the lateral division of the bed nucleus of the stria terminalis (BNST) are the two major nuclei of the central extended amygdala that plays essential roles in threat processing, responsible for emotional states such as fear and anxiety. While some studies suggested functional differences between these nuclei, others showed anatomical and neurochemical similarities. Despite their complex subnuclear organization, subnuclei-specific functional impact on behavior and their underlying molecular profiles remain obscure. We here constitutively inhibited neurotransmission of protein kinase C-δ-positive (PKCδ+) neurons—a major cell type of the lateral subdivision of the CeA (CeL) and the oval nucleus of the BNST (BNSTov)—and found striking subnuclei-specific effects on fear- and anxiety-related behaviors, respectively. To obtain molecular clues for this dissociation, we conducted RNA sequencing in subnuclei-targeted micropunch samples. The CeL and the BNSTov displayed similar gene expression profiles at the basal level; however, both displayed differential gene expression when animals were exposed to fear-related stimuli, with a more robust expression change in the CeL. These findings provide novel insights into the molecular makeup and differential engagement of distinct subnuclei of the extended amygdala, critical for regulation of threat processing. Frontiers Media S.A. 2021-09-03 /pmc/articles/PMC8446640/ /pubmed/34539345 http://dx.doi.org/10.3389/fnmol.2021.741895 Text en Copyright © 2021 Ueda, Hosokawa, Arikawa, Takahashi, Fujiwara, Kakita, Fukada, Koyama, Horigane, Itoi, Kakeyama, Matsunaga, Takeyama, Bito and Takemoto-Kimura. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Molecular Neuroscience
Ueda, Shuhei
Hosokawa, Masahito
Arikawa, Koji
Takahashi, Kiyofumi
Fujiwara, Mao
Kakita, Manami
Fukada, Taro
Koyama, Hiroaki
Horigane, Shin-ichiro
Itoi, Keiichi
Kakeyama, Masaki
Matsunaga, Hiroko
Takeyama, Haruko
Bito, Haruhiko
Takemoto-Kimura, Sayaka
Distinctive Regulation of Emotional Behaviors and Fear-Related Gene Expression Responses in Two Extended Amygdala Subnuclei With Similar Molecular Profiles
title Distinctive Regulation of Emotional Behaviors and Fear-Related Gene Expression Responses in Two Extended Amygdala Subnuclei With Similar Molecular Profiles
title_full Distinctive Regulation of Emotional Behaviors and Fear-Related Gene Expression Responses in Two Extended Amygdala Subnuclei With Similar Molecular Profiles
title_fullStr Distinctive Regulation of Emotional Behaviors and Fear-Related Gene Expression Responses in Two Extended Amygdala Subnuclei With Similar Molecular Profiles
title_full_unstemmed Distinctive Regulation of Emotional Behaviors and Fear-Related Gene Expression Responses in Two Extended Amygdala Subnuclei With Similar Molecular Profiles
title_short Distinctive Regulation of Emotional Behaviors and Fear-Related Gene Expression Responses in Two Extended Amygdala Subnuclei With Similar Molecular Profiles
title_sort distinctive regulation of emotional behaviors and fear-related gene expression responses in two extended amygdala subnuclei with similar molecular profiles
topic Molecular Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8446640/
https://www.ncbi.nlm.nih.gov/pubmed/34539345
http://dx.doi.org/10.3389/fnmol.2021.741895
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