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Cell diversity and network dynamics in photosensitive human brain organoids

Author

Listed:
  • Giorgia Quadrato

    (Harvard University
    Stanley Center for Psychiatric Research, Broad Institute of Harvard and MIT)

  • Tuan Nguyen

    (Harvard University
    Stanley Center for Psychiatric Research, Broad Institute of Harvard and MIT)

  • Evan Z. Macosko

    (Stanley Center for Psychiatric Research, Broad Institute of Harvard and MIT
    Harvard Medical School)

  • John L. Sherwood

    (Harvard University
    Stanley Center for Psychiatric Research, Broad Institute of Harvard and MIT)

  • Sung Min Yang

    (Harvard University)

  • Daniel R. Berger

    (Harvard University)

  • Natalie Maria

    (Harvard University)

  • Jorg Scholvin

    (MIT Media Lab and McGovern Institute, MIT)

  • Melissa Goldman

    (Harvard Medical School)

  • Justin P. Kinney

    (LeafLabs, LLC)

  • Edward S. Boyden

    (MIT Media Lab and McGovern Institute, MIT)

  • Jeff W. Lichtman

    (Harvard University)

  • Ziv M. Williams

    (Massachusetts General Hospital, Harvard Medical School)

  • Steven A. McCarroll

    (Stanley Center for Psychiatric Research, Broad Institute of Harvard and MIT
    Harvard Medical School)

  • Paola Arlotta

    (Harvard University
    Stanley Center for Psychiatric Research, Broad Institute of Harvard and MIT)

Abstract

In vitro models of the developing brain such as three-dimensional brain organoids offer an unprecedented opportunity to study aspects of human brain development and disease. However, the cells generated within organoids and the extent to which they recapitulate the regional complexity, cellular diversity and circuit functionality of the brain remain undefined. Here we analyse gene expression in over 80,000 individual cells isolated from 31 human brain organoids. We find that organoids can generate a broad diversity of cells, which are related to endogenous classes, including cells from the cerebral cortex and the retina. Organoids could be developed over extended periods (more than 9 months), allowing for the establishment of relatively mature features, including the formation of dendritic spines and spontaneously active neuronal networks. Finally, neuronal activity within organoids could be controlled using light stimulation of photosensitive cells, which may offer a way to probe the functionality of human neuronal circuits using physiological sensory stimuli.

Suggested Citation

  • Giorgia Quadrato & Tuan Nguyen & Evan Z. Macosko & John L. Sherwood & Sung Min Yang & Daniel R. Berger & Natalie Maria & Jorg Scholvin & Melissa Goldman & Justin P. Kinney & Edward S. Boyden & Jeff W., 2017. "Cell diversity and network dynamics in photosensitive human brain organoids," Nature, Nature, vol. 545(7652), pages 48-53, May.
    • Handle: RePEc:nat:nature:v:545:y:2017:i:7652:d:10.1038_nature22047
    DOI: 10.1038/nature22047
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    Citations

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    Cited by:

    1. Elaine T. Lim & Yingleong Chan & Pepper Dawes & Xiaoge Guo & Serkan Erdin & Derek J. C. Tai & Songlei Liu & Julia M. Reichert & Mannix J. Burns & Ying Kai Chan & Jessica J. Chiang & Katharina Meyer & , 2022. "Orgo-Seq integrates single-cell and bulk transcriptomic data to identify cell type specific-driver genes associated with autism spectrum disorder," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Alessandro Fiorenzano & Edoardo Sozzi & Marcella Birtele & Janko Kajtez & Jessica Giacomoni & Fredrik Nilsson & Andreas Bruzelius & Yogita Sharma & Yu Zhang & Bengt Mattsson & Jenny Emnéus & Daniella , 2021. "Single-cell transcriptomics captures features of human midbrain development and dopamine neuron diversity in brain organoids," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    3. Yuge Wang & Hongyu Zhao, 2022. "Non-linear archetypal analysis of single-cell RNA-seq data by deep autoencoders," PLOS Computational Biology, Public Library of Science, vol. 18(4), pages 1-31, April.
    4. 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.
    5. Maisumu Gulimiheranmu & Shuang Li & Junmei Zhou, 2021. "In Vitro Recapitulation of Neuropsychiatric Disorders with Pluripotent Stem Cells-Derived Brain Organoids," IJERPH, MDPI, vol. 18(23), pages 1-14, November.
    6. Madison N. Wilson & Martin Thunemann & Xin Liu & Yichen Lu & Francesca Puppo & Jason W. Adams & Jeong-Hoon Kim & Mehrdad Ramezani & Donald P. Pizzo & Srdjan Djurovic & Ole A. Andreassen & Abed AlFatah, 2022. "Multimodal monitoring of human cortical organoids implanted in mice reveal functional connection with visual cortex," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    7. Tal Sharf & Tjitse Molen & Stella M. K. Glasauer & Elmer Guzman & Alessio P. Buccino & Gabriel Luna & Zhuowei Cheng & Morgane Audouard & Kamalini G. Ranasinghe & Kiwamu Kudo & Srikantan S. Nagarajan &, 2022. "Functional neuronal circuitry and oscillatory dynamics in human brain organoids," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    8. Anna Pagliaro & Roxy Finger & Iris Zoutendijk & Saskia Bunschuh & Hans Clevers & Delilah Hendriks & Benedetta Artegiani, 2023. "Temporal morphogen gradient-driven neural induction shapes single expanded neuroepithelium brain organoids with enhanced cortical identity," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

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