Innovations present in the primate interneuron repertoire
Primates and rodents, which descended from a common ancestor around 90 million years ago , 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...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Springer Science and Business Media LLC
2021
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| Online Access: | https://hdl.handle.net/1721.1/130409 |
| _version_ | 1826193021471817728 |
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| author | Krienen, Fenna M. Goldman, Melissa Zhang, Qiangge C. H. del Rosario, Ricardo Florio, Marta Machold, Robert Saunders, Arpiar Levandowski, Kirsten Zaniewski, Heather Schuman, Benjamin Wu, Carolyn Lutservitz, Alyssa Mullally, Christopher D. Reed, Nora Bien, Elizabeth Bortolin, Laura Fernandez-Otero, Marian Lin, Jessica D. Wysoker, Alec Nemesh, James Kulp, David Burns, Monika Tkachev, Victor Smith, Richard Walsh, Christopher A. Dimidschstein, Jordane Rudy, Bernardo S. Kean, Leslie Berretta, Sabina Fishell, Gord Feng, Guoping McCarroll, Steven A. |
| author2 | McGovern Institute for Brain Research at MIT |
| author_facet | McGovern Institute for Brain Research at MIT Krienen, Fenna M. Goldman, Melissa Zhang, Qiangge C. H. del Rosario, Ricardo Florio, Marta Machold, Robert Saunders, Arpiar Levandowski, Kirsten Zaniewski, Heather Schuman, Benjamin Wu, Carolyn Lutservitz, Alyssa Mullally, Christopher D. Reed, Nora Bien, Elizabeth Bortolin, Laura Fernandez-Otero, Marian Lin, Jessica D. Wysoker, Alec Nemesh, James Kulp, David Burns, Monika Tkachev, Victor Smith, Richard Walsh, Christopher A. Dimidschstein, Jordane Rudy, Bernardo S. Kean, Leslie Berretta, Sabina Fishell, Gord Feng, Guoping McCarroll, Steven A. |
| author_sort | Krienen, Fenna M. |
| collection | MIT |
| description | Primates and rodents, which descended from a common ancestor around 90 million years ago , 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. |
| first_indexed | 2024-09-23T09:32:24Z |
| format | Article |
| id | mit-1721.1/130409 |
| institution | Massachusetts Institute of Technology |
| language | English |
| last_indexed | 2024-09-23T09:32:24Z |
| publishDate | 2021 |
| publisher | Springer Science and Business Media LLC |
| record_format | dspace |
| spelling | mit-1721.1/1304092022-09-26T12:08:41Z Innovations present in the primate interneuron repertoire Krienen, Fenna M. Goldman, Melissa Zhang, Qiangge C. H. del Rosario, Ricardo Florio, Marta Machold, Robert Saunders, Arpiar Levandowski, Kirsten Zaniewski, Heather Schuman, Benjamin Wu, Carolyn Lutservitz, Alyssa Mullally, Christopher D. Reed, Nora Bien, Elizabeth Bortolin, Laura Fernandez-Otero, Marian Lin, Jessica D. Wysoker, Alec Nemesh, James Kulp, David Burns, Monika Tkachev, Victor Smith, Richard Walsh, Christopher A. Dimidschstein, Jordane Rudy, Bernardo S. Kean, Leslie Berretta, Sabina Fishell, Gord Feng, Guoping McCarroll, Steven A. McGovern Institute for Brain Research at MIT Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences Primates and rodents, which descended from a common ancestor around 90 million years ago , 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. 2021-04-08T14:25:34Z 2021-04-08T14:25:34Z 2020-09 2019-07 2021-04-07T13:33:08Z Article http://purl.org/eprint/type/JournalArticle 0028-0836 1476-4687 https://hdl.handle.net/1721.1/130409 Krienen, Fenna M. et al. "Innovations present in the primate interneuron repertoire." Nature 586, 7828 (September 2020): 262–269. © 2020 The Author(s) en http://dx.doi.org/10.1038/s41586-020-2781-z Nature Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf Springer Science and Business Media LLC other univ website |
| spellingShingle | Krienen, Fenna M. Goldman, Melissa Zhang, Qiangge C. H. del Rosario, Ricardo Florio, Marta Machold, Robert Saunders, Arpiar Levandowski, Kirsten Zaniewski, Heather Schuman, Benjamin Wu, Carolyn Lutservitz, Alyssa Mullally, Christopher D. Reed, Nora Bien, Elizabeth Bortolin, Laura Fernandez-Otero, Marian Lin, Jessica D. Wysoker, Alec Nemesh, James Kulp, David Burns, Monika Tkachev, Victor Smith, Richard Walsh, Christopher A. Dimidschstein, Jordane Rudy, Bernardo S. Kean, Leslie Berretta, Sabina Fishell, Gord Feng, Guoping McCarroll, Steven A. Innovations present in the primate interneuron repertoire |
| title | Innovations present in the primate interneuron repertoire |
| title_full | Innovations present in the primate interneuron repertoire |
| title_fullStr | Innovations present in the primate interneuron repertoire |
| title_full_unstemmed | Innovations present in the primate interneuron repertoire |
| title_short | Innovations present in the primate interneuron repertoire |
| title_sort | innovations present in the primate interneuron repertoire |
| url | https://hdl.handle.net/1721.1/130409 |
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