Cortical arealization of interneurons defines shared and distinct molecular programs in developing human and macaque brains
Abstract Cortical interneurons generated from ganglionic eminence via a long-distance journey of tangential migration display evident cellular and molecular differences across brain regions, which seeds the heterogeneous cortical circuitry in primates. However, whether such regional specifications i...
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Nature Portfolio
2025-01-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-025-56058-8 |
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| author | Xiangling Feng Yingjie Gao Fan Chu Yuwen Shan Meicheng Liu Yaoyi Wang Ying Zhu Qing Lu Mingfeng Li |
| author_facet | Xiangling Feng Yingjie Gao Fan Chu Yuwen Shan Meicheng Liu Yaoyi Wang Ying Zhu Qing Lu Mingfeng Li |
| author_sort | Xiangling Feng |
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| description | Abstract Cortical interneurons generated from ganglionic eminence via a long-distance journey of tangential migration display evident cellular and molecular differences across brain regions, which seeds the heterogeneous cortical circuitry in primates. However, whether such regional specifications in interneurons are intrinsically encoded or gained through interactions with the local milieu remains elusive. Here, we recruit 685,692 interneurons from cerebral cortex and subcortex including ganglionic eminence within the developing human and macaque species. Our integrative and comparative analyses reveal that less transcriptomic alteration is accompanied by interneuron migration within the ganglionic eminence subdivisions, in contrast to the dramatic changes observed in cortical tangential migration, which mostly characterize the transcriptomic specification for different destinations and for species divergence. Moreover, the in-depth survey of temporal regulation illustrates species differences in the developmental dynamics of cell types, e.g., the employment of CRH in primate interneurons during late-fetal stage distinguishes from their postnatal emergence in mice, and our entropy quantifications manifest the interneuron diversities gradually increase along the developmental ages in human and macaque cerebral cortices. Overall, our analyses depict the spatiotemporal features appended to cortical interneurons, providing a new proxy for understanding the relationship between cellular diversity and functional progression. |
| format | Article |
| id | doaj-art-d00108d1ce4f45e28e33dcb1ca6aab62 |
| institution | Kabale University |
| issn | 2041-1723 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Nature Portfolio |
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| series | Nature Communications |
| spelling | doaj-art-d00108d1ce4f45e28e33dcb1ca6aab622025-01-19T12:30:09ZengNature PortfolioNature Communications2041-17232025-01-0116111810.1038/s41467-025-56058-8Cortical arealization of interneurons defines shared and distinct molecular programs in developing human and macaque brainsXiangling Feng0Yingjie Gao1Fan Chu2Yuwen Shan3Meicheng Liu4Yaoyi Wang5Ying Zhu6Qing Lu7Mingfeng Li8Department of Pharmacology, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and TechnologyDepartment of Pharmacology, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and TechnologyDepartment of Pharmacology, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and TechnologyNational Demonstration Center for Experimental Basic Medical Education, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and TechnologyNational Demonstration Center for Experimental Basic Medical Education, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and TechnologyState Key Laboratory of Medical Neurobiology, MOE Frontiers Center for Brain Science, Institutes of Brain Science, and Department of Neurosurgery, Huashan Hospital, Fudan UniversityState Key Laboratory of Medical Neurobiology, MOE Frontiers Center for Brain Science, Institutes of Brain Science, and Department of Neurosurgery, Huashan Hospital, Fudan UniversityDepartment of Pharmacology, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and TechnologyDepartment of Pharmacology, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and TechnologyAbstract Cortical interneurons generated from ganglionic eminence via a long-distance journey of tangential migration display evident cellular and molecular differences across brain regions, which seeds the heterogeneous cortical circuitry in primates. However, whether such regional specifications in interneurons are intrinsically encoded or gained through interactions with the local milieu remains elusive. Here, we recruit 685,692 interneurons from cerebral cortex and subcortex including ganglionic eminence within the developing human and macaque species. Our integrative and comparative analyses reveal that less transcriptomic alteration is accompanied by interneuron migration within the ganglionic eminence subdivisions, in contrast to the dramatic changes observed in cortical tangential migration, which mostly characterize the transcriptomic specification for different destinations and for species divergence. Moreover, the in-depth survey of temporal regulation illustrates species differences in the developmental dynamics of cell types, e.g., the employment of CRH in primate interneurons during late-fetal stage distinguishes from their postnatal emergence in mice, and our entropy quantifications manifest the interneuron diversities gradually increase along the developmental ages in human and macaque cerebral cortices. Overall, our analyses depict the spatiotemporal features appended to cortical interneurons, providing a new proxy for understanding the relationship between cellular diversity and functional progression.https://doi.org/10.1038/s41467-025-56058-8 |
| spellingShingle | Xiangling Feng Yingjie Gao Fan Chu Yuwen Shan Meicheng Liu Yaoyi Wang Ying Zhu Qing Lu Mingfeng Li Cortical arealization of interneurons defines shared and distinct molecular programs in developing human and macaque brains Nature Communications |
| title | Cortical arealization of interneurons defines shared and distinct molecular programs in developing human and macaque brains |
| title_full | Cortical arealization of interneurons defines shared and distinct molecular programs in developing human and macaque brains |
| title_fullStr | Cortical arealization of interneurons defines shared and distinct molecular programs in developing human and macaque brains |
| title_full_unstemmed | Cortical arealization of interneurons defines shared and distinct molecular programs in developing human and macaque brains |
| title_short | Cortical arealization of interneurons defines shared and distinct molecular programs in developing human and macaque brains |
| title_sort | cortical arealization of interneurons defines shared and distinct molecular programs in developing human and macaque brains |
| url | https://doi.org/10.1038/s41467-025-56058-8 |
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