Molecular and cellular evolution of the amygdala across species analyzed by single-nucleus transcriptome profiling

Abstract The amygdala, or an amygdala-like structure, is found in the brains of all vertebrates and plays a critical role in survival and reproduction. However, the cellular architecture of the amygdala and how it has evolved remain elusive. Here, we generated single-nucleus RNA-sequencing data for...

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Main Authors: Bin Yu, Qianqian Zhang, Lin Lin, Xin Zhou, Wenji Ma, Shaonan Wen, Chunyue Li, Wei Wang, Qian Wu, Xiaoqun Wang, Xiao-Ming Li
Format: Article
Language:English
Published: Nature Publishing Group 2023-02-01
Series:Cell Discovery
Online Access:https://doi.org/10.1038/s41421-022-00506-y
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author Bin Yu
Qianqian Zhang
Lin Lin
Xin Zhou
Wenji Ma
Shaonan Wen
Chunyue Li
Wei Wang
Qian Wu
Xiaoqun Wang
Xiao-Ming Li
author_facet Bin Yu
Qianqian Zhang
Lin Lin
Xin Zhou
Wenji Ma
Shaonan Wen
Chunyue Li
Wei Wang
Qian Wu
Xiaoqun Wang
Xiao-Ming Li
author_sort Bin Yu
collection DOAJ
description Abstract The amygdala, or an amygdala-like structure, is found in the brains of all vertebrates and plays a critical role in survival and reproduction. However, the cellular architecture of the amygdala and how it has evolved remain elusive. Here, we generated single-nucleus RNA-sequencing data for more than 200,000 cells in the amygdala of humans, macaques, mice, and chickens. Abundant neuronal cell types from different amygdala subnuclei were identified in all datasets. Cross-species analysis revealed that inhibitory neurons and inhibitory neuron-enriched subnuclei of the amygdala were well-conserved in cellular composition and marker gene expression, whereas excitatory neuron-enriched subnuclei were relatively divergent. Furthermore, LAMP5 + interneurons were much more abundant in primates, while DRD2 + inhibitory neurons and LAMP5 + SATB2 + excitatory neurons were dominant in the human central amygdalar nucleus (CEA) and basolateral amygdalar complex (BLA), respectively. We also identified CEA-like neurons and their species-specific distribution patterns in chickens. This study highlights the extreme cell-type diversity in the amygdala and reveals the conservation and divergence of cell types and gene expression patterns across species that may contribute to species-specific adaptations.
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spelling doaj.art-026458dd92ee43adb569eca5438cd2602023-03-22T10:23:58ZengNature Publishing GroupCell Discovery2056-59682023-02-019112210.1038/s41421-022-00506-yMolecular and cellular evolution of the amygdala across species analyzed by single-nucleus transcriptome profilingBin Yu0Qianqian Zhang1Lin Lin2Xin Zhou3Wenji Ma4Shaonan Wen5Chunyue Li6Wei Wang7Qian Wu8Xiaoqun Wang9Xiao-Ming Li10Department of Neurobiology and Department of Neurology of the Second Affiliated Hospital, Zhejiang University School of MedicineState Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Biophysics, Chinese Academy of SciencesDepartment of Neurobiology and Department of Neurology of the Second Affiliated Hospital, Zhejiang University School of MedicineState Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal UniversityState Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Biophysics, Chinese Academy of SciencesState Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal UniversityDepartment of Neurobiology and Department of Neurology of the Second Affiliated Hospital, Zhejiang University School of MedicineState Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Biophysics, Chinese Academy of SciencesState Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal UniversityState Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Biophysics, Chinese Academy of SciencesDepartment of Neurobiology and Department of Neurology of the Second Affiliated Hospital, Zhejiang University School of MedicineAbstract The amygdala, or an amygdala-like structure, is found in the brains of all vertebrates and plays a critical role in survival and reproduction. However, the cellular architecture of the amygdala and how it has evolved remain elusive. Here, we generated single-nucleus RNA-sequencing data for more than 200,000 cells in the amygdala of humans, macaques, mice, and chickens. Abundant neuronal cell types from different amygdala subnuclei were identified in all datasets. Cross-species analysis revealed that inhibitory neurons and inhibitory neuron-enriched subnuclei of the amygdala were well-conserved in cellular composition and marker gene expression, whereas excitatory neuron-enriched subnuclei were relatively divergent. Furthermore, LAMP5 + interneurons were much more abundant in primates, while DRD2 + inhibitory neurons and LAMP5 + SATB2 + excitatory neurons were dominant in the human central amygdalar nucleus (CEA) and basolateral amygdalar complex (BLA), respectively. We also identified CEA-like neurons and their species-specific distribution patterns in chickens. This study highlights the extreme cell-type diversity in the amygdala and reveals the conservation and divergence of cell types and gene expression patterns across species that may contribute to species-specific adaptations.https://doi.org/10.1038/s41421-022-00506-y
spellingShingle Bin Yu
Qianqian Zhang
Lin Lin
Xin Zhou
Wenji Ma
Shaonan Wen
Chunyue Li
Wei Wang
Qian Wu
Xiaoqun Wang
Xiao-Ming Li
Molecular and cellular evolution of the amygdala across species analyzed by single-nucleus transcriptome profiling
Cell Discovery
title Molecular and cellular evolution of the amygdala across species analyzed by single-nucleus transcriptome profiling
title_full Molecular and cellular evolution of the amygdala across species analyzed by single-nucleus transcriptome profiling
title_fullStr Molecular and cellular evolution of the amygdala across species analyzed by single-nucleus transcriptome profiling
title_full_unstemmed Molecular and cellular evolution of the amygdala across species analyzed by single-nucleus transcriptome profiling
title_short Molecular and cellular evolution of the amygdala across species analyzed by single-nucleus transcriptome profiling
title_sort molecular and cellular evolution of the amygdala across species analyzed by single nucleus transcriptome profiling
url https://doi.org/10.1038/s41421-022-00506-y
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