A transcriptomic taxonomy of mouse brain-wide spinal projecting neurons

The brain controls nearly all bodily functions via spinal projecting neurons (SPNs) that carry command signals from the brain to the spinal cord. However, a comprehensive molecular characterization of brain-wide SPNs is still lacking. Here we transcriptionally profiled a total of 65,002 SPNs, identi...

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Published in:	Nature (London) Vol. 624; no. 7991; pp. 403 - 414
Main Authors:	Winter, Carla C., Jacobi, Anne, Su, Junfeng, Chung, Leeyup, van Velthoven, Cindy T. J., Yao, Zizhen, Lee, Changkyu, Zhang, Zicong, Yu, Shuguang, Gao, Kun, Duque Salazar, Geraldine, Kegeles, Evgenii, Zhang, Yu, Tomihiro, Makenzie C., Zhang, Yiming, Yang, Zhiyun, Zhu, Junjie, Tang, Jing, Song, Xuan, Donahue, Ryan J., Wang, Qing, McMillen, Delissa, Kunst, Michael, Wang, Ning, Smith, Kimberly A., Romero, Gabriel E., Frank, Michelle M., Krol, Alexandra, Kawaguchi, Riki, Geschwind, Daniel H., Feng, Guoping, Goodrich, Lisa V., Liu, Yuanyuan, Tasic, Bosiljka, Zeng, Hongkui, He, Zhigang
Format:	Journal Article
Language:	English
Published:	London Nature Publishing Group UK 14-12-2023 Nature Publishing Group
Subjects:	38/90 38/91 631/378 631/378/1687 64/60 Animals Brain Brain - cytology Brain - metabolism Cerebellum Cerebellum - cytology Cerebral Cortex - cytology Electrophysiology Functional morphology Functionals Gene Expression Profiling Homeobox Humanities and Social Sciences Hypothalamus Labeling Mesencephalon Mesencephalon - cytology Mice multidisciplinary Neural Pathways Neurons Neurons - metabolism Neuropeptides Neurotransmitter Agents Populations Proteins Red nucleus Reticular formation Reticular Formation - cytology Reticulospinal tracts Science Science (multidisciplinary) Spinal cord Spinal Cord - cytology Spinal Cord - metabolism Taxonomy Transcriptomics
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Summary:	The brain controls nearly all bodily functions via spinal projecting neurons (SPNs) that carry command signals from the brain to the spinal cord. However, a comprehensive molecular characterization of brain-wide SPNs is still lacking. Here we transcriptionally profiled a total of 65,002 SPNs, identified 76 region-specific SPN types, and mapped these types into a companion atlas of the whole mouse brain 1 . This taxonomy reveals a three-component organization of SPNs: (1) molecularly homogeneous excitatory SPNs from the cortex, red nucleus and cerebellum with somatotopic spinal terminations suitable for point-to-point communication; (2) heterogeneous populations in the reticular formation with broad spinal termination patterns, suitable for relaying commands related to the activities of the entire spinal cord; and (3) modulatory neurons expressing slow-acting neurotransmitters and/or neuropeptides in the hypothalamus, midbrain and reticular formation for ‘gain setting’ of brain–spinal signals. In addition, this atlas revealed a LIM homeobox transcription factor code that parcellates the reticulospinal neurons into five molecularly distinct and spatially segregated populations. Finally, we found transcriptional signatures of a subset of SPNs with large soma size and correlated these with fast-firing electrophysiological properties. Together, this study establishes a comprehensive taxonomy of brain-wide SPNs and provides insight into the functional organization of SPNs in mediating brain control of bodily functions. In this study, the authors develop a comprehensive taxonomy of brain-wide SPNs, identifying several novel subsets via their transcriptional signatures.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23
ISSN:	0028-0836 1476-4687
DOI:	10.1038/s41586-023-06817-8