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

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, Francisco Diez-Fuertes, Song-Lin Ding, Jamison McCorrison, Nicholas J. Schork, Soraya I. Shehata, Kimberly A. Smith, Susan M. Sunkin, Danny N. Tran, Pratap Venepally, Anna Marie Yanny, Frank J. Steemers, John W. Phillips, Amy Bernard, Christof Koch, Roger S. Lasken, Richard H. Scheuermann and Ed S. Lein ()
Additional contact information
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
Jonathan T. Ting: Allen Institute for Brain Science
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
Ed S. Lein: Allen Institute for Brain Science

Nature Communications, 2020, vol. 11, issue 1, 1-14

Abstract: 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.

Date: 2020
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DOI: 10.1038/s41467-020-14952-3

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