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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| Format: | Article |
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Frontiers Media S.A.
2021-09-01
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| Series: | Frontiers in Molecular Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnmol.2021.741895/full |
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| author | Shuhei Ueda Shuhei Ueda Masahito Hosokawa Masahito Hosokawa Masahito Hosokawa Koji Arikawa Kiyofumi Takahashi Mao Fujiwara Manami Kakita Manami Kakita Manami Kakita Taro Fukada Taro Fukada Hiroaki Koyama Shin-ichiro Horigane Shin-ichiro Horigane Keiichi Itoi Masaki Kakeyama Masaki Kakeyama Hiroko Matsunaga Haruko Takeyama Haruko Takeyama Haruko Takeyama Haruko Takeyama Haruhiko Bito Sayaka Takemoto-Kimura Sayaka Takemoto-Kimura Sayaka Takemoto-Kimura |
| author_facet | Shuhei Ueda Shuhei Ueda Masahito Hosokawa Masahito Hosokawa Masahito Hosokawa Koji Arikawa Kiyofumi Takahashi Mao Fujiwara Manami Kakita Manami Kakita Manami Kakita Taro Fukada Taro Fukada Hiroaki Koyama Shin-ichiro Horigane Shin-ichiro Horigane Keiichi Itoi Masaki Kakeyama Masaki Kakeyama Hiroko Matsunaga Haruko Takeyama Haruko Takeyama Haruko Takeyama Haruko Takeyama Haruhiko Bito Sayaka Takemoto-Kimura Sayaka Takemoto-Kimura Sayaka Takemoto-Kimura |
| author_sort | Shuhei Ueda |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-17T06:21:32Z |
| format | Article |
| id | doaj.art-34c256e6b13c42328ff4728d539f59cb |
| institution | Directory Open Access Journal |
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| language | English |
| last_indexed | 2024-12-17T06:21:32Z |
| publishDate | 2021-09-01 |
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| record_format | Article |
| series | Frontiers in Molecular Neuroscience |
| spelling | doaj.art-34c256e6b13c42328ff4728d539f59cb2022-12-21T22:00:23ZengFrontiers Media S.A.Frontiers in Molecular Neuroscience1662-50992021-09-011410.3389/fnmol.2021.741895741895Distinctive Regulation of Emotional Behaviors and Fear-Related Gene Expression Responses in Two Extended Amygdala Subnuclei With Similar Molecular ProfilesShuhei Ueda0Shuhei Ueda1Masahito Hosokawa2Masahito Hosokawa3Masahito Hosokawa4Koji Arikawa5Kiyofumi Takahashi6Mao Fujiwara7Manami Kakita8Manami Kakita9Manami Kakita10Taro Fukada11Taro Fukada12Hiroaki Koyama13Shin-ichiro Horigane14Shin-ichiro Horigane15Keiichi Itoi16Masaki Kakeyama17Masaki Kakeyama18Hiroko Matsunaga19Haruko Takeyama20Haruko Takeyama21Haruko Takeyama22Haruko Takeyama23Haruhiko Bito24Sayaka Takemoto-Kimura25Sayaka Takemoto-Kimura26Sayaka Takemoto-Kimura27Department of Neuroscience I, Research Institute of Environmental Medicine, Nagoya University, Nagoya, JapanMolecular/Cellular Neuroscience, Nagoya University Graduate School of Medicine, Nagoya University, Nagoya, JapanResearch Organization for Nano and Life Innovation, Waseda University, Tokyo, JapanDepartment of Life Science and Medical Bioscience, Waseda University, Tokyo, JapanPrecursory Research for Embryonic Science and Technology, Japan Science and Technology Agency, Tokyo, JapanResearch Organization for Nano and Life Innovation, Waseda University, Tokyo, JapanResearch Organization for Nano and Life Innovation, Waseda University, Tokyo, JapanDepartment of Neuroscience I, Research Institute of Environmental Medicine, Nagoya University, Nagoya, JapanDepartment of Neuroscience I, Research Institute of Environmental Medicine, Nagoya University, Nagoya, JapanLaboratory for Systems Neurosciences and Preventive Medicine, Faculty of Human Sciences, Waseda University, Tokorozawa, JapanResearch Institute for Environmental Medical Sciences, Waseda University, Tokorozawa, JapanDepartment of Neuroscience I, Research Institute of Environmental Medicine, Nagoya University, Nagoya, JapanMolecular/Cellular Neuroscience, Nagoya University Graduate School of Medicine, Nagoya University, Nagoya, JapanDepartment of Neurochemistry, Graduate School of Medicine, The University of Tokyo, Tokyo, JapanDepartment of Neuroscience I, Research Institute of Environmental Medicine, Nagoya University, Nagoya, JapanMolecular/Cellular Neuroscience, Nagoya University Graduate School of Medicine, Nagoya University, Nagoya, JapanDepartment of Nursing, Tohoku Fukushi University, Sendai, JapanLaboratory for Systems Neurosciences and Preventive Medicine, Faculty of Human Sciences, Waseda University, Tokorozawa, JapanResearch Institute for Environmental Medical Sciences, Waseda University, Tokorozawa, JapanResearch Organization for Nano and Life Innovation, Waseda University, Tokyo, JapanResearch Organization for Nano and Life Innovation, Waseda University, Tokyo, JapanDepartment of Life Science and Medical Bioscience, Waseda University, Tokyo, Japan0Computational Bio Big-Data Open Innovation Laboratory, National Institute of Advanced Industrial Science and Technology, Tokyo, Japan1Institute for Advanced Research of Biosystem Dynamics, Waseda Research Institute for Science and Engineering, Waseda University, Tokyo, JapanDepartment of Neurochemistry, Graduate School of Medicine, The University of Tokyo, Tokyo, JapanDepartment of Neuroscience I, Research Institute of Environmental Medicine, Nagoya University, Nagoya, JapanMolecular/Cellular Neuroscience, Nagoya University Graduate School of Medicine, Nagoya University, Nagoya, JapanPrecursory Research for Embryonic Science and Technology, Japan Science and Technology Agency, Tokyo, JapanThe 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.https://www.frontiersin.org/articles/10.3389/fnmol.2021.741895/fullcentral extended amygdalagene expressionfearanxietycentral nucleus of the amygdalabed nucleus of the stria terminalis |
| spellingShingle | Shuhei Ueda Shuhei Ueda Masahito Hosokawa Masahito Hosokawa Masahito Hosokawa Koji Arikawa Kiyofumi Takahashi Mao Fujiwara Manami Kakita Manami Kakita Manami Kakita Taro Fukada Taro Fukada Hiroaki Koyama Shin-ichiro Horigane Shin-ichiro Horigane Keiichi Itoi Masaki Kakeyama Masaki Kakeyama Hiroko Matsunaga Haruko Takeyama Haruko Takeyama Haruko Takeyama Haruko Takeyama Haruhiko Bito Sayaka Takemoto-Kimura Sayaka Takemoto-Kimura Sayaka Takemoto-Kimura Distinctive Regulation of Emotional Behaviors and Fear-Related Gene Expression Responses in Two Extended Amygdala Subnuclei With Similar Molecular Profiles Frontiers in Molecular Neuroscience central extended amygdala gene expression fear anxiety central nucleus of the amygdala bed nucleus of the stria terminalis |
| 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 | central extended amygdala gene expression fear anxiety central nucleus of the amygdala bed nucleus of the stria terminalis |
| url | https://www.frontiersin.org/articles/10.3389/fnmol.2021.741895/full |
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