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Revealing single-neuron and network-activity interaction by combining high-density microelectrode array and optogenetics

Author

Listed:
  • Toki Kobayashi

    (The University of Tokyo)

  • Kenta Shimba

    (The University of Tokyo)

  • Taiyo Narumi

    (The University of Tokyo)

  • Takahiro Asahina

    (National Institute of Information and Communications Technology)

  • Kiyoshi Kotani

    (The University of Tokyo)

  • Yasuhiko Jimbo

    (The University of Tokyo)

Abstract

The synchronous activity of neuronal networks is considered crucial for brain function. However, the interaction between single-neuron activity and network-wide activity remains poorly understood. This study explored this interaction within cultured networks of rat cortical neurons. Employing a combination of high-density microelectrode array recording and optogenetic stimulation, we established an experimental setup enabling simultaneous recording and stimulation at a precise single-neuron level that can be scaled to the level of the whole network. Leveraging our system, we identified a network burst-dependent response change in single neurons, providing a possible mechanism for the network-burst-dependent loss of information within the network and consequent cognitive impairment during epileptic seizures. Additionally, we directly recorded a leader neuron initiating a spontaneous network burst and characterized its firing properties, indicating that the bursting activity of hub neurons in the brain can initiate network-wide activity. Our study offers valuable insights into brain networks characterized by a combination of bottom-up self-organization and top-down regulation.

Suggested Citation

  • Toki Kobayashi & Kenta Shimba & Taiyo Narumi & Takahiro Asahina & Kiyoshi Kotani & Yasuhiko Jimbo, 2024. "Revealing single-neuron and network-activity interaction by combining high-density microelectrode array and optogenetics," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53505-w
    DOI: 10.1038/s41467-024-53505-w
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    1. Brandon Lieberthal & Allison M Gardner, 2021. "Connectivity, reproduction number, and mobility interact to determine communities’ epidemiological superspreader potential in a metapopulation network," PLOS Computational Biology, Public Library of Science, vol. 17(3), pages 1-22, March.
    2. Michael Zabolocki & Kasandra McCormack & Mark Hurk & Bridget Milky & Andrew P. Shoubridge & Robert Adams & Jenne Tran & Anita Mahadevan-Jansen & Philipp Reineck & Jacob Thomas & Mark R. Hutchinson & C, 2020. "BrainPhys neuronal medium optimized for imaging and optogenetics in vitro," Nature Communications, Nature, vol. 11(1), pages 1-19, December.
    3. Jérémie Barral & Xiao-Jing Wang & Alex D. Reyes, 2019. "Propagation of temporal and rate signals in cultured multilayer networks," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
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