Innovations in Primate Interneuron Repertoire
Open accessPreprint — published as 10.1038/s41586-020-2781-z · Paper page
Abstract
Primates and rodents, which descended from a common ancestor more than 90 million years ago, exhibit profound differences in behavior and cognitive capacity. Modifications, specializations, and innovations to brain cell types may have occurred along each lineage. We used Drop-seq to profile RNA expression in more than 184,000 individual telencephalic interneurons from humans, macaques, marmosets, and mice. Conserved interneuron types varied significantly in abundance and RNA expression between mice and primates, but varied much more modestly among primates. In adult primates, the expression patterns of dozens of genes exhibited spatial expression gradients among neocortical interneurons, suggesting that adult neocortical interneurons are imprinted by their local cortical context. In addition, we found that an interneuron type previously associated with the mouse hippocampus—the “ivy cell”, which has neurogliaform characteristics—has become abundant across the neocortex of humans, macaques, and marmosets. The most striking innovation was subcortical: we identified an abundant striatal interneuron type in primates that had no molecularly homologous cell population in mouse striatum, cortex, thalamus, or hippocampus. These interneurons, which expressed a unique combination of transcription factors, receptors, and neuropeptides, including the neuropeptide TAC3 , constituted almost 30% of striatal interneurons in marmosets and humans. Understanding how gene and cell-type attributes changed or persisted over the evolutionary divergence of primates and rodents will guide the choice of models for human brain disorders and mutations and help to identify the cellular substrates of expanded cognition in humans and other primates.
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Emerging data indicate primate-unique cell types and profound differences in transcriptomic signatures between rodents and primates.
“Emerging data also indicate primate-unique cell types, and profound differences in transcriptomic signatures between rodents and primates (Krienen et al., 2019).”
From Guanfacine’s mechanism of action in treating prefrontal cortical disorders: Successful translation across species (2020) · cites this paper as Krienen et al., 2019
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Self-citation
- Authors
- Krienen, F. M., Goldman, M., Zhang, Q., del Rosario, R., Florio, M., Machold, R., Saunders, A., Levandowski, K., Zaniewski, H., Schuman, B., Wu, C., Lutservitz, A., Mullally, C. D., Reed, N., Bien, E., Bortolin, L., Fernandez-Otero, M., Lin, J., Wysoker, A., Nemesh, J., Kulp, D., Burns, M., Tkachev, V., Smith, R., Walsh, C. A., Dimidschstein, J., Rudy, B., Kean, L., Berretta, S., Fishell, G., Feng, G., & McCarroll, S. A.
- Affiliations
- Broad Institute (US)
- NYU Langone Health (US)
- McGovern Institute for Brain Research (US)
- Massachusetts Institute of Technology (US)
- Boston Children's Hospital (US)
- Harvard University (US)
- Corresponding author
- Krienen, Fenna M.
- ORCID
- Krienen, Fenna M.
- Goldman, Melissa
- Zhang, Qiangge
- Florio, Marta
- Machold, Robert
- Saunders, Arpiar
- Levandowski, Kirsten
- Zaniewski, Heather
- Schuman, Benjamin
- Mullally, Christopher D.
- Reed, Nora
- Bien, Elizabeth
- Lin, Jessica
- Kulp, David
- Tkachev, Victor
- Smith, Richard
- Walsh, Christopher A.
- Dimidschstein, Jordane
- Rudy, Bernardo
- Kean, Leslie
- Berretta, Sabina
- Fishell, Gord
- Feng, Guoping
- McCarroll, Steven A.
- Venue
- Nature
- Publisher
- openRxiv
- Published
- 2019-07-23
- Volume
- 586
- Issue
- 7828
- Pages
- 262-269
- ISSN
- 0028-0836 (ISSN-L)
- PMC
- PMC7957574
- OpenAlex
- W3091064804
- Cited by
- 372
- References
- 63
- Citations by year
- 2026: 50 · 2025: 64 · 2024: 66 · 2023: 66 · 2022: 46 · 2021: 53 · 2020: 22 · 2019: 3
- FWCI
- 14.98
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Locations
- Nature (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
- Funders
- Howard Hughes Medical Institute
- Broad Institute
- Stanley Center for Psychiatric Research, Broad Institute
- McGovern Institute for Brain Research, Massachusetts Institute of Technology
- National Institute of Mental Health (P50MH094271, U01MH114819)
- National Institute of Neurological Disorders and Stroke (R01NS107257, P01NS074972, R01NS110079, R01NS032457)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- neocortical interneurons, interneuron subtypes, primate evolution, single-nucleus RNA sequencing, striatal interneurons, neuropeptides, transcription factors, human brain evolution, comparative transcriptomics, marmoset, macaque, mice, ferrets
- MeSH terms
- Animals, Callithrix, Cerebral Cortex, Female, Ferrets, Hippocampus, Humans, Interneurons, Macaca, Male, Nerve Tissue Proteins, Primates, RNA, Species Specificity, Transcription Factors, Neostriatum, Mice, Lysosomal Membrane Proteins, LIM-Homeodomain Proteins
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