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Functional neuronal circuitry and oscillatory dynamics in human brain organoids

Human brain organoids replicate much of the cellular diversity and developmental anatomy of the human brain. However, the physiology of neuronal circuits within organoids remains under-explored. With high-density CMOS microelectrode arrays and shank electrodes, we captured spontaneous extracellular...

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Autores principales: Sharf, Tal, van der Molen, Tjitse, Glasauer, Stella M. K., Guzman, Elmer, Buccino, Alessio P., Luna, Gabriel, Cheng, Zhuowei, Audouard, Morgane, Ranasinghe, Kamalini G., Kudo, Kiwamu, Nagarajan, Srikantan S., Tovar, Kenneth R., Petzold, Linda R., Hierlemann, Andreas, Hansma, Paul K., Kosik, Kenneth S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9338020/
https://www.ncbi.nlm.nih.gov/pubmed/35906223
http://dx.doi.org/10.1038/s41467-022-32115-4
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author Sharf, Tal
van der Molen, Tjitse
Glasauer, Stella M. K.
Guzman, Elmer
Buccino, Alessio P.
Luna, Gabriel
Cheng, Zhuowei
Audouard, Morgane
Ranasinghe, Kamalini G.
Kudo, Kiwamu
Nagarajan, Srikantan S.
Tovar, Kenneth R.
Petzold, Linda R.
Hierlemann, Andreas
Hansma, Paul K.
Kosik, Kenneth S.
author_facet Sharf, Tal
van der Molen, Tjitse
Glasauer, Stella M. K.
Guzman, Elmer
Buccino, Alessio P.
Luna, Gabriel
Cheng, Zhuowei
Audouard, Morgane
Ranasinghe, Kamalini G.
Kudo, Kiwamu
Nagarajan, Srikantan S.
Tovar, Kenneth R.
Petzold, Linda R.
Hierlemann, Andreas
Hansma, Paul K.
Kosik, Kenneth S.
author_sort Sharf, Tal
collection PubMed
description Human brain organoids replicate much of the cellular diversity and developmental anatomy of the human brain. However, the physiology of neuronal circuits within organoids remains under-explored. With high-density CMOS microelectrode arrays and shank electrodes, we captured spontaneous extracellular activity from brain organoids derived from human induced pluripotent stem cells. We inferred functional connectivity from spike timing, revealing a large number of weak connections within a skeleton of significantly fewer strong connections. A benzodiazepine increased the uniformity of firing patterns and decreased the relative fraction of weakly connected edges. Our analysis of the local field potential demonstrate that brain organoids contain neuronal assemblies of sufficient size and functional connectivity to co-activate and generate field potentials from their collective transmembrane currents that phase-lock to spiking activity. These results point to the potential of brain organoids for the study of neuropsychiatric diseases, drug action, and the effects of external stimuli upon neuronal networks.
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spelling pubmed-93380202022-07-31 Functional neuronal circuitry and oscillatory dynamics in human brain organoids Sharf, Tal van der Molen, Tjitse Glasauer, Stella M. K. Guzman, Elmer Buccino, Alessio P. Luna, Gabriel Cheng, Zhuowei Audouard, Morgane Ranasinghe, Kamalini G. Kudo, Kiwamu Nagarajan, Srikantan S. Tovar, Kenneth R. Petzold, Linda R. Hierlemann, Andreas Hansma, Paul K. Kosik, Kenneth S. Nat Commun Article Human brain organoids replicate much of the cellular diversity and developmental anatomy of the human brain. However, the physiology of neuronal circuits within organoids remains under-explored. With high-density CMOS microelectrode arrays and shank electrodes, we captured spontaneous extracellular activity from brain organoids derived from human induced pluripotent stem cells. We inferred functional connectivity from spike timing, revealing a large number of weak connections within a skeleton of significantly fewer strong connections. A benzodiazepine increased the uniformity of firing patterns and decreased the relative fraction of weakly connected edges. Our analysis of the local field potential demonstrate that brain organoids contain neuronal assemblies of sufficient size and functional connectivity to co-activate and generate field potentials from their collective transmembrane currents that phase-lock to spiking activity. These results point to the potential of brain organoids for the study of neuropsychiatric diseases, drug action, and the effects of external stimuli upon neuronal networks. Nature Publishing Group UK 2022-07-29 /pmc/articles/PMC9338020/ /pubmed/35906223 http://dx.doi.org/10.1038/s41467-022-32115-4 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Sharf, Tal
van der Molen, Tjitse
Glasauer, Stella M. K.
Guzman, Elmer
Buccino, Alessio P.
Luna, Gabriel
Cheng, Zhuowei
Audouard, Morgane
Ranasinghe, Kamalini G.
Kudo, Kiwamu
Nagarajan, Srikantan S.
Tovar, Kenneth R.
Petzold, Linda R.
Hierlemann, Andreas
Hansma, Paul K.
Kosik, Kenneth S.
Functional neuronal circuitry and oscillatory dynamics in human brain organoids
title Functional neuronal circuitry and oscillatory dynamics in human brain organoids
title_full Functional neuronal circuitry and oscillatory dynamics in human brain organoids
title_fullStr Functional neuronal circuitry and oscillatory dynamics in human brain organoids
title_full_unstemmed Functional neuronal circuitry and oscillatory dynamics in human brain organoids
title_short Functional neuronal circuitry and oscillatory dynamics in human brain organoids
title_sort functional neuronal circuitry and oscillatory dynamics in human brain organoids
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9338020/
https://www.ncbi.nlm.nih.gov/pubmed/35906223
http://dx.doi.org/10.1038/s41467-022-32115-4
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