Innovations present in the primate interneuron repertoire

Fenna M. Krienen, Melissa Goldman, Qiangge Zhang, Ricardo C. H. 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 NemeshDavid Kulp, Monika Burns, Victor Tkachev, Richard Smith, Christopher A. Walsh, Jordane Dimidschstein, Bernardo Rudy, Leslie S. Kean, Sabina Berretta, Gord Fishell, Guoping Feng, Steven A. McCarroll

Research output: Contribution to journalArticlepeer-review

11 Scopus citations

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.

Original languageEnglish (US)
Pages (from-to)262-269
Number of pages8
JournalNature
Volume586
Issue number7828
DOIs
StatePublished - Oct 8 2020
Externally publishedYes

ASJC Scopus subject areas

  • General

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