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Transcriptomic evidence that von Economo neurons are regionally specialized extratelencephalic-projecting excitatory neurons

Author

Listed:
  • Rebecca D. Hodge

    (Allen Institute for Brain Science)

  • Jeremy A. Miller

    (Allen Institute for Brain Science)

  • Mark Novotny

    (J. Craig Venter Institute)

  • Brian E. Kalmbach

    (Allen Institute for Brain Science
    University of Washington)

  • Jonathan T. Ting

    (Allen Institute for Brain Science
    University of Washington)

  • Trygve E. Bakken

    (Allen Institute for Brain Science)

  • Brian D. Aevermann

    (J. Craig Venter Institute)

  • Eliza R. Barkan

    (Allen Institute for Brain Science)

  • Madeline L. Berkowitz-Cerasano

    (University of Washington)

  • Charles Cobbs

    (The Ben and Catherine Ivy Center for Advanced Brain Tumor Treatment, Swedish Neuroscience Institute)

  • Francisco Diez-Fuertes

    (J. Craig Venter Institute)

  • Song-Lin Ding

    (Allen Institute for Brain Science)

  • Jamison McCorrison

    (J. Craig Venter Institute)

  • Nicholas J. Schork

    (J. Craig Venter Institute)

  • Soraya I. Shehata

    (Allen Institute for Brain Science)

  • Kimberly A. Smith

    (Allen Institute for Brain Science)

  • Susan M. Sunkin

    (Allen Institute for Brain Science)

  • Danny N. Tran

    (J. Craig Venter Institute)

  • Pratap Venepally

    (J. Craig Venter Institute)

  • Anna Marie Yanny

    (Allen Institute for Brain Science)

  • Frank J. Steemers

    (Illumina, Inc.)

  • John W. Phillips

    (Allen Institute for Brain Science)

  • Amy Bernard

    (Allen Institute for Brain Science)

  • Christof Koch

    (Allen Institute for Brain Science)

  • Roger S. Lasken

    (J. Craig Venter Institute)

  • Richard H. Scheuermann

    (J. Craig Venter Institute
    University of California)

  • Ed S. Lein

    (Allen Institute for Brain Science)

Abstract

von Economo neurons (VENs) are bipolar, spindle-shaped neurons restricted to layer 5 of human frontoinsula and anterior cingulate cortex that appear to be selectively vulnerable to neuropsychiatric and neurodegenerative diseases, although little is known about other VEN cellular phenotypes. Single nucleus RNA-sequencing of frontoinsula layer 5 identifies a transcriptomically-defined cell cluster that contained VENs, but also fork cells and a subset of pyramidal neurons. Cross-species alignment of this cell cluster with a well-annotated mouse classification shows strong homology to extratelencephalic (ET) excitatory neurons that project to subcerebral targets. This cluster also shows strong homology to a putative ET cluster in human temporal cortex, but with a strikingly specific regional signature. Together these results suggest that VENs are a regionally distinctive type of ET neuron. Additionally, we describe the first patch clamp recordings of VENs from neurosurgically-resected tissue that show distinctive intrinsic membrane properties relative to neighboring pyramidal neurons.

Suggested Citation

  • Rebecca D. Hodge & Jeremy A. Miller & Mark Novotny & Brian E. Kalmbach & Jonathan T. Ting & Trygve E. Bakken & Brian D. Aevermann & Eliza R. Barkan & Madeline L. Berkowitz-Cerasano & Charles Cobbs & F, 2020. "Transcriptomic evidence that von Economo neurons are regionally specialized extratelencephalic-projecting excitatory neurons," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-14952-3
    DOI: 10.1038/s41467-020-14952-3
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    Cited by:

    1. Junhao Li & Manoj K. Jaiswal & Jo-Fan Chien & Alexey Kozlenkov & Jinyoung Jung & Ping Zhou & Mahammad Gardashli & Luc J. Pregent & Erica Engelberg-Cook & Dennis W. Dickson & Veronique V. Belzil & Eran, 2023. "Divergent single cell transcriptome and epigenome alterations in ALS and FTD patients with C9orf72 mutation," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    2. Stefano Berto & Alex H. Treacher & Emre Caglayan & Danni Luo & Jillian R. Haney & Michael J. Gandal & Daniel H. Geschwind & Albert A. Montillo & Genevieve Konopka, 2022. "Association between resting-state functional brain connectivity and gene expression is altered in autism spectrum disorder," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    3. Jia-Ru Wei & Zhao-Zhe Hao & Chuan Xu & Mengyao Huang & Lei Tang & Nana Xu & Ruifeng Liu & Yuhui Shen & Sarah A. Teichmann & Zhichao Miao & Sheng Liu, 2022. "Identification of visual cortex cell types and species differences using single-cell RNA sequencing," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    4. Songren Wei & Meng Luo & Pingping Wang & Rui Chen & Xiyun Jin & Chang Xu & Chenyang Li & Xiaoyu Lin & Zhaochun Xu & Hongxin Liu & Rui Cheng & Wenyi Yang & Yideng Cai & Guangfu Xue & Peng Huang & Zhiga, 2025. "Charting the spatial transcriptome of the human cerebral cortex at single-cell resolution," Nature Communications, Nature, vol. 16(1), pages 1-20, December.

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