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Complex activity and short-term plasticity of human cerebral organoids reciprocally connected with axons

Author

Listed:
  • Tatsuya Osaki

    (The University of Tokyo
    The University of Tokyo)

  • Tomoya Duenki

    (The University of Tokyo
    The University of Tokyo
    The University of Tokyo
    The University of Tokyo)

  • Siu Yu A. Chow

    (The University of Tokyo
    The University of Tokyo)

  • Yasuhiro Ikegami

    (The University of Tokyo
    The University of Tokyo)

  • Romain Beaubois

    (The University of Tokyo
    The University of Tokyo
    UMR5218, University of Bordeaux)

  • Timothée Levi

    (The University of Tokyo
    The University of Tokyo
    UMR5218, University of Bordeaux)

  • Nao Nakagawa-Tamagawa

    (The University of Tokyo
    Kagoshima University)

  • Yoji Hirano

    (The University of Tokyo
    Kyushu University
    University of Miyazaki)

  • Yoshiho Ikeuchi

    (The University of Tokyo
    The University of Tokyo
    The University of Tokyo
    The University of Tokyo)

Abstract

An inter-regional cortical tract is one of the most fundamental architectural motifs that integrates neural circuits to orchestrate and generate complex functions of the human brain. To understand the mechanistic significance of inter-regional projections on development of neural circuits, we investigated an in vitro neural tissue model for inter-regional connections, in which two cerebral organoids are connected with a bundle of reciprocally extended axons. The connected organoids produced more complex and intense oscillatory activity than conventional or directly fused cerebral organoids, suggesting the inter-organoid axonal connections enhance and support the complex network activity. In addition, optogenetic stimulation of the inter-organoid axon bundles could entrain the activity of the organoids and induce robust short-term plasticity of the macroscopic circuit. These results demonstrated that the projection axons could serve as a structural hub that boosts functionality of the organoid-circuits. This model could contribute to further investigation on development and functions of macroscopic neuronal circuits in vitro.

Suggested Citation

  • Tatsuya Osaki & Tomoya Duenki & Siu Yu A. Chow & Yasuhiro Ikegami & Romain Beaubois & Timothée Levi & Nao Nakagawa-Tamagawa & Yoji Hirano & Yoshiho Ikeuchi, 2024. "Complex activity and short-term plasticity of human cerebral organoids reciprocally connected with axons," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46787-7
    DOI: 10.1038/s41467-024-46787-7
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    1. Seok-Jun Hong & Reinder Vos de Wael & Richard A. I. Bethlehem & Sara Lariviere & Casey Paquola & Sofie L. Valk & Michael P. Milham & Adriana Di Martino & Daniel S. Margulies & Jonathan Smallwood & Bor, 2019. "Atypical functional connectome hierarchy in autism," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    2. M. Angeles Rabadan & Estanislao Daniel De La Cruz & Sneha B. Rao & Yannan Chen & Cheng Gong & Gregg Crabtree & Bin Xu & Sander Markx & Joseph A. Gogos & Rafael Yuste & Raju Tomer, 2022. "An in vitro model of neuronal ensembles," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. Madeline A. Lancaster & Magdalena Renner & Carol-Anne Martin & Daniel Wenzel & Louise S. Bicknell & Matthew E. Hurles & Tessa Homfray & Josef M. Penninger & Andrew P. Jackson & Juergen A. Knoblich, 2013. "Cerebral organoids model human brain development and microcephaly," Nature, Nature, vol. 501(7467), pages 373-379, September.
    4. Uwe Frey & Richard G. M. Morris, 1997. "Synaptic tagging and long-term potentiation," Nature, Nature, vol. 385(6616), pages 533-536, February.
    5. Fikri Birey & Jimena Andersen & Christopher D. Makinson & Saiful Islam & Wu Wei & Nina Huber & H. Christina Fan & Kimberly R. Cordes Metzler & Georgia Panagiotakos & Nicholas Thom & Nancy A. O’Rourke , 2017. "Assembly of functionally integrated human forebrain spheroids," Nature, Nature, vol. 545(7652), pages 54-59, May.
    6. 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.
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    Cited by:

    1. Romain Beaubois & Jérémy Cheslet & Tomoya Duenki & Giuseppe De Venuto & Marta Carè & Farad Khoyratee & Michela Chiappalone & Pascal Branchereau & Yoshiho Ikeuchi & Timothée Levi, 2024. "BiœmuS: A new tool for neurological disorders studies through real-time emulation and hybridization using biomimetic Spiking Neural Network," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

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