Innovations present in the primate interneuron repertoire

Fenna M. Krienen (), Melissa Goldman, Qiangge Zhang, Ricardo del Rosario, Marta Florio, Robert Machold, Arpiar Saunders, Kirsten Levandowski, Heather Zaniewski, Benjamin Schuman, Carolyn Wu, Alyssa Lutservitz, Christopher D. Mullally, Nora Reed, Elizabeth Bien, Laura Bortolin, Marian Fernandez-Otero, Jessica D. Lin, Alec Wysoker, James Nemesh, David Kulp, Monika Burns, Victor Tkachev, Richard Smith, Christopher A. Walsh, Jordane Dimidschstein, Bernardo Rudy, Leslie Kean, Sabina Berretta, Gord Fishell, Guoping Feng and Steven A. McCarroll ()
Additional contact information
Fenna M. Krienen: Harvard Medical School
Melissa Goldman: Harvard Medical School
Qiangge Zhang: Broad Institute of MIT and Harvard
Ricardo del Rosario: Broad Institute of MIT and Harvard
Marta Florio: Harvard Medical School
Robert Machold: New York University
Arpiar Saunders: Harvard Medical School
Kirsten Levandowski: Broad Institute of MIT and Harvard
Heather Zaniewski: Broad Institute of MIT and Harvard
Benjamin Schuman: New York University
Carolyn Wu: Massachusetts Institute of Technology
Alyssa Lutservitz: Harvard Medical School
Christopher D. Mullally: Harvard Medical School
Nora Reed: Harvard Medical School
Elizabeth Bien: Harvard Medical School
Laura Bortolin: Harvard Medical School
Marian Fernandez-Otero: Broad Institute of MIT and Harvard
Jessica D. Lin: Broad Institute of MIT and Harvard
Alec Wysoker: Broad Institute of MIT and Harvard
James Nemesh: Broad Institute of MIT and Harvard
David Kulp: Broad Institute of MIT and Harvard
Monika Burns: Massachusetts Institute of Technology
Victor Tkachev: Boston Children’s Hospital
Richard Smith: Boston Children’s Hospital
Christopher A. Walsh: Boston Children’s Hospital
Jordane Dimidschstein: Broad Institute of MIT and Harvard
Bernardo Rudy: New York University
Leslie Kean: Boston Children’s Hospital
Sabina Berretta: Massachusetts Institute of Technology
Gord Fishell: Broad Institute of MIT and Harvard
Guoping Feng: Broad Institute of MIT and Harvard
Steven A. McCarroll: Harvard Medical School

Nature, 2020, vol. 586, issue 7828, 262-269

Abstract: Abstract Primates and rodents, which descended from a common ancestor around 90 million years ago1, exhibit profound differences in behaviour and cognitive capacity; the cellular basis for these differences is unknown. Here we use single-nucleus RNA sequencing to profile RNA expression in 188,776 individual interneurons across homologous brain regions from three primates (human, macaque and marmoset), a rodent (mouse) and a weasel (ferret). Homologous interneuron types—which were readily identified by their RNA-expression patterns—varied in abundance and RNA expression among ferrets, mice and primates, but varied less among primates. Only a modest fraction of the genes identified as ‘markers’ of specific interneuron subtypes in any one species had this property in another species. In the primate neocortex, dozens of genes showed spatial expression gradients among interneurons of the same type, which suggests that regional variation in cortical contexts shapes the RNA expression patterns of adult neocortical interneurons. We found that an interneuron type that was previously associated with the mouse hippocampus—the ‘ivy cell’, which has neurogliaform characteristics—has become abundant across the neocortex of humans, macaques and marmosets but not mice or ferrets. We also found a notable subcortical innovation: an abundant striatal interneuron type in primates that had no molecularly homologous counterpart in mice or ferrets. These interneurons expressed a unique combination of genes that encode transcription factors, receptors and neuropeptides and constituted around 30% of striatal interneurons in marmosets and humans.

Date: 2020
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DOI: 10.1038/s41586-020-2781-z

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