A transcriptomic taxonomy of mouse brain-wide spinal projecting neurons

Carla C. Winter, Anne Jacobi (), Junfeng Su, Leeyup Chung, Cindy T. J. van Velthoven, Zizhen Yao, Changkyu Lee, Zicong Zhang, Shuguang Yu, Kun Gao, Geraldine Duque Salazar, Evgenii Kegeles, Yu Zhang, Makenzie C. Tomihiro, Yiming Zhang, Zhiyun Yang, Junjie Zhu, Jing Tang, Xuan Song, Ryan J. Donahue, Qing Wang, Delissa McMillen, Michael Kunst, Ning Wang, Kimberly A. Smith, Gabriel E. Romero, Michelle M. Frank, Alexandra Krol, Riki Kawaguchi, Daniel H. Geschwind, Guoping Feng, Lisa V. Goodrich, Yuanyuan Liu, Bosiljka Tasic, Hongkui Zeng () and Zhigang He ()
Additional contact information
Carla C. Winter: F. M. Kirby Neurobiology Center, Boston Children’s Hospital
Anne Jacobi: F. M. Kirby Neurobiology Center, Boston Children’s Hospital
Junfeng Su: F. M. Kirby Neurobiology Center, Boston Children’s Hospital
Leeyup Chung: F. M. Kirby Neurobiology Center, Boston Children’s Hospital
Cindy T. J. van Velthoven: Allen Institute for Brain Science
Zizhen Yao: Allen Institute for Brain Science
Changkyu Lee: Allen Institute for Brain Science
Zicong Zhang: F. M. Kirby Neurobiology Center, Boston Children’s Hospital
Shuguang Yu: F. M. Kirby Neurobiology Center, Boston Children’s Hospital
Kun Gao: University of California Los Angeles
Geraldine Duque Salazar: F. M. Kirby Neurobiology Center, Boston Children’s Hospital
Evgenii Kegeles: F. M. Kirby Neurobiology Center, Boston Children’s Hospital
Yu Zhang: F. M. Kirby Neurobiology Center, Boston Children’s Hospital
Makenzie C. Tomihiro: F. M. Kirby Neurobiology Center, Boston Children’s Hospital
Yiming Zhang: F. M. Kirby Neurobiology Center, Boston Children’s Hospital
Zhiyun Yang: F. M. Kirby Neurobiology Center, Boston Children’s Hospital
Junjie Zhu: F. M. Kirby Neurobiology Center, Boston Children’s Hospital
Jing Tang: F. M. Kirby Neurobiology Center, Boston Children’s Hospital
Xuan Song: F. M. Kirby Neurobiology Center, Boston Children’s Hospital
Ryan J. Donahue: F. M. Kirby Neurobiology Center, Boston Children’s Hospital
Qing Wang: University of California Los Angeles
Delissa McMillen: Allen Institute for Brain Science
Michael Kunst: Allen Institute for Brain Science
Ning Wang: Allen Institute for Brain Science
Kimberly A. Smith: Allen Institute for Brain Science
Gabriel E. Romero: Harvard Medical School
Michelle M. Frank: Harvard Medical School
Alexandra Krol: Massachusetts Institute of Technology
Riki Kawaguchi: University of California Los Angeles
Daniel H. Geschwind: University of California Los Angeles
Guoping Feng: Massachusetts Institute of Technology
Lisa V. Goodrich: Harvard Medical School
Yuanyuan Liu: Somatosensation and Pain Unit, National Institute of Dental and Craniofacial Research, National Center for Complementary and Integrative Health, National Institutes of Health
Bosiljka Tasic: Allen Institute for Brain Science
Hongkui Zeng: Allen Institute for Brain Science
Zhigang He: F. M. Kirby Neurobiology Center, Boston Children’s Hospital

Nature, 2023, vol. 624, issue 7991, 403-414

Abstract: Abstract 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 brain1. 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.

Date: 2023
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DOI: 10.1038/s41586-023-06817-8

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