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Innovations present in the primate interneuron repertoire

Author

Listed:
  • Fenna M. Krienen

    (Harvard Medical School
    Broad Institute of MIT and Harvard)

  • Melissa Goldman

    (Harvard Medical School
    Broad Institute of MIT and Harvard)

  • Qiangge Zhang

    (Broad Institute of MIT and Harvard
    Massachusetts Institute of Technology)

  • Ricardo del Rosario

    (Broad Institute of MIT and Harvard)

  • Marta Florio

    (Harvard Medical School
    Broad Institute of MIT and Harvard)

  • Robert Machold

    (New York University)

  • Arpiar Saunders

    (Harvard Medical School
    Broad Institute of MIT and Harvard)

  • Kirsten Levandowski

    (Broad Institute of MIT and Harvard
    Massachusetts Institute of Technology)

  • Heather Zaniewski

    (Broad Institute of MIT and Harvard
    Massachusetts Institute of Technology)

  • Benjamin Schuman

    (New York University)

  • Carolyn Wu

    (Massachusetts Institute of Technology)

  • Alyssa Lutservitz

    (Harvard Medical School
    Broad Institute of MIT and Harvard)

  • Christopher D. Mullally

    (Harvard Medical School
    Broad Institute of MIT and Harvard)

  • Nora Reed

    (Harvard Medical School
    Broad Institute of MIT and Harvard)

  • Elizabeth Bien

    (Harvard Medical School
    Broad Institute of MIT and Harvard)

  • Laura Bortolin

    (Harvard Medical School
    Broad Institute of MIT and Harvard)

  • Marian Fernandez-Otero

    (Broad Institute of MIT and Harvard
    Massachusetts Institute of Technology)

  • 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
    Dana-Farber Cancer Institute
    Harvard Medical School)

  • Richard Smith

    (Boston Children’s Hospital
    Boston Children’s Hospital)

  • Christopher A. Walsh

    (Boston Children’s Hospital
    Boston Children’s Hospital)

  • Jordane Dimidschstein

    (Broad Institute of MIT and Harvard)

  • Bernardo Rudy

    (New York University
    New York University School of Medicine)

  • Leslie Kean

    (Boston Children’s Hospital
    Dana-Farber Cancer Institute
    Harvard Medical School)

  • Sabina Berretta

    (Massachusetts Institute of Technology
    McLean Hospital
    Harvard Medical School)

  • Gord Fishell

    (Broad Institute of MIT and Harvard
    Harvard Medical School)

  • Guoping Feng

    (Broad Institute of MIT and Harvard
    Massachusetts Institute of Technology)

  • Steven A. McCarroll

    (Harvard Medical School
    Broad Institute of MIT and Harvard)

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.

Suggested Citation

  • Fenna M. Krienen & Melissa Goldman & Qiangge Zhang & Ricardo del Rosario & Marta Florio & Robert Machold & Arpiar Saunders & Kirsten Levandowski & Heather Zaniewski & Benjamin Schuman & Carolyn Wu & A, 2020. "Innovations present in the primate interneuron repertoire," Nature, Nature, vol. 586(7828), pages 262-269, October.
  • Handle: RePEc:nat:nature:v:586:y:2020:i:7828:d:10.1038_s41586-020-2781-z
    DOI: 10.1038/s41586-020-2781-z
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    Citations

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    Cited by:

    1. Leonardo D. Garma & Lisbeth Harder & Juan M. Barba-Reyes & Sergio Marco Salas & Mónica Díez-Salguero & Mats Nilsson & Alberto Serrano-Pozo & Bradley T. Hyman & Ana B. Muñoz-Manchado, 2024. "Interneuron diversity in the human dorsal striatum," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. Yueqi Wang & Simone Chiola & Guang Yang & Chad Russell & Celeste J. Armstrong & Yuanyuan Wu & Jay Spampanato & Paisley Tarboton & H. M. Arif Ullah & Nicolas U. Edgar & Amelia N. Chang & David A. Harmi, 2022. "Modeling human telencephalic development and autism-associated SHANK3 deficiency using organoids generated from single neural rosettes," Nature Communications, Nature, vol. 13(1), pages 1-25, December.
    3. BaDoi N. Phan & Madelyn H. Ray & Xiangning Xue & Chen Fu & Robert J. Fenster & Stephen J. Kohut & Jack Bergman & Suzanne N. Haber & Kenneth M. McCullough & Madeline K. Fish & Jill R. Glausier & Qiao S, 2024. "Single nuclei transcriptomics in human and non-human primate striatum in opioid use disorder," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    4. Xuelong Yao & Zongyang Lu & Zhanying Feng & Lei Gao & Xin Zhou & Min Li & Suijuan Zhong & Qian Wu & Zhenbo Liu & Haofeng Zhang & Zeyuan Liu & Lizhi Yi & Tao Zhou & Xudong Zhao & Jun Zhang & Yong Wang , 2022. "Comparison of chromatin accessibility landscapes during early development of prefrontal cortex between rhesus macaque and human," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. Jia-Ru Wei & Zhao-Zhe Hao & Chuan Xu & Mengyao Huang & Lei Tang & Nana Xu & Ruifeng Liu & Yuhui Shen & Sarah A. Teichmann & Zhichao Miao & Sheng Liu, 2022. "Identification of visual cortex cell types and species differences using single-cell RNA sequencing," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    6. Arpiar Saunders & Kee Wui Huang & Cassandra Vondrak & Christina Hughes & Karina Smolyar & Harsha Sen & Adrienne C. Philson & James Nemesh & Alec Wysoker & Seva Kashin & Bernardo L. Sabatini & Steven A, 2022. "Ascertaining cells’ synaptic connections and RNA expression simultaneously with barcoded rabies virus libraries," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    7. Anthony G. Boghdadi & Joshua Spurrier & Leon Teo & Mingfeng Li & Mario Skarica & Benjamin Cao & William C. Kwan & Tobias D. Merson & Susan K. Nilsson & Nenad Sestan & Stephen M. Strittmatter & James A, 2021. "NogoA-expressing astrocytes limit peripheral macrophage infiltration after ischemic brain injury in primates," Nature Communications, Nature, vol. 12(1), pages 1-16, December.

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