Complex Oscillatory Waves Emerging from Cortical Organoids Model Early Human Brain Network Development
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Abstract
Structural and transcriptional changes during early brain maturation follow fixed developmental programs defined by genetics. However, whether this is true for functional network activity remains unknown, primarily due to experimental inaccessibility of the initial stages of the living human brain. Here, we developed human cortical organoids that dynamically change cellular populations during maturation and exhibited consistent increases in electrical activity over the span of several months. The spontaneous network formation displayed periodic and regular oscillatory events that were dependent on glutamatergic and GABAergic signaling. The oscillatory activity transitioned to more spatiotemporally irregular patterns, and synchronous network events resembled features similar to those observed in preterm human electroencephalography. These results show that the development of structured network activity in a human neocortex model may follow stable genetic programming. Our approach provides opportunities for investigating and manipulating the role of network activity in the developing human cortex.
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Neural organoids in vitro or following transplantation show highly correlated activity indicative of circuit immaturity.
“This is in contrast with data obtained using neural organoids in vitro or following transplantation (Mansour et al., 2018, Trujillo et al., 2019), which show highly correlated activity indicative of circuit immaturity.”
From Xenotransplanted human cortical neurons reveal species-specific development and functional integration into mouse visual circuits (2019) · cites this paper as Trujillo et al., 2019
The Discussion reports highly synchronous, stereotypical activity in in-vitro cortical organoids at two months, and the Results liken synchronized events to preterm infant EEG. But the Discussion says activity becomes more variable as the organoids develop, so the source does not support describing their activity as uniformly highly correlated or their circuits as uniformly immature. This paper studies in-vitro organoids; the transplantation study has a separate citation. (LLM, conf=0.86)
Experimental — accuracy not yet measuredHuman brain organoids can replicate the complex brain microenvironment better than 2D in vitro models.
“With their 3D structures and cell components resembling the human brain, these organoids can replicate the complex brain microenvironment better than 2D in vitro models (15–17, 19)”
From Understanding monocyte-driven neuroinflammation in Alzheimer’s disease using human cortical organoid microphysiological systems (2025) · cites this paper as [17]
The Introduction describes organoids as three-dimensional models that mimic human brain development at the cellular and molecular levels, and the Results describe brain-like cell types and layered structures. Our copy does not establish that organoids replicate the brain microenvironment better than 2D in vitro models; searches for that comparison found no supporting passage. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe cells projected on the UMAP space were annotated using canonical marker genes for neurons, progenitors, intermediate progenitors, astrocytes, other glial cells, and monocytes.
“The cells projected on the UMAP space were annotated using canonical marker genes for neurons, progenitors, intermediate progenitors, astrocytes, other glial cells, and monocytes (17, 84, 85).”
From Understanding monocyte-driven neuroinflammation in Alzheimer’s disease using human cortical organoid microphysiological systems (2025) · cites this paper as [17]
The Results section (‘Generation of functional cortical organoids’; page unavailable) says cells were classified using gene markers into progenitors, intermediate progenitors, glial cells, and two neuronal classes. STAR METHODS (‘Methods Details’; page unavailable) describes plotting the clusters on UMAP. The copy does not report monocytes or astrocytes as separate annotated classes, so it does not support the full list in the claim. (LLM, conf=0.88)
Experimental — accuracy not yet measuredHuman brain organoids are 3D cultures derived from human pluripotent stem cells and recapitulate native brain cellular components, cytoarchitecture, and exhibit neural activity.
“Human brain organoids are 3D cultures derived from human pluripotent stem cells and recapitulate native brain cellular components, cytoarchitecture, and exhibit neural activity.22–24”
From Tubular human brain organoids to model microglia-mediated neuroinflammation (2021) · cites this paper as [24]
Human brain organoids are a scaled-down, three-dimensional model of the human brain, mimicking various developmental features, including generation of new neurons by their conversion from radial glia and incorporation into neuronal network.
“Human brain organoids are emerging as a scaled-down, three-dimensional model of the human brain, mimicking various developmental features, including generation of new neurons by their conversion from radial glia20 and incorporation into neuronal network21.”
From Therapeutically viable generation of neurons with antisense oligonucleotide suppression of PTB (2021) · cites this paper as [21]
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Maturation and circuit integration of transplanted human cortical organoids
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Human organoids in basic research and clinical applications
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Induced pluripotent stem cells (iPSCs): molecular mechanisms of induction and applications
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Materials-Driven Soft Wearable Bioelectronics for Connected Healthcare
Gong, S. P., Yan, L., Yin, J., Levin, A., & Cheng, W. (2024) · Chemical Reviews · doi:10.1021/acs.chemrev.3c00502 · Cited by 424 · see citing works
Brain organoids for the study of human neurobiology at the interface of in vitro and in vivo
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SARS-CoV-2 infects human neural progenitor cells and brain organoids
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Self-citationHuman cerebral organoids — a new tool for clinical neurology research
Eichmüller, O. L., & Knoblich, J. A. (2022) · Nature Reviews Neurology · doi:10.1038/s41582-022-00723-9 · Cited by 260 · see citing works
Multi-lineage human iPSC-derived platforms for disease modeling and drug discovery
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Identification of neural oscillations and epileptiform changes in human brain organoids
Samarasinghe, R. A., Miranda, O. A., Buth, J. E., Mitchell, S. A., Ferando, I., Watanabe, M., Allison, T. F., Kurdian, A., Fotion, N. N., Gandal, M. J., et al. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00906-5 · Cited by 278 · see citing works
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Prefrontal Cortex Development in Health and Disease: Lessons from Rodents and Humans
Chini, M., & Hanganu-Opatz, I. L. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2020.10.017 · Cited by 253 · see citing works
Park, Y., Franz, C. K., Ryu, H., Luan, H., Cotton, K. Y., Kim, J. U., Chung, T. S., Zhao, S., Vázquez‐Guardado, A., Yang, D. S., et al. (2021) · Science Advances · doi:10.1126/sciadv.abf9153 · Cited by 287 · see citing works
Brain organoid reservoir computing for artificial intelligence
Cai, H., Ao, Z., Tian, C., Wu, Z., Liu, H., Tchieu, J. H., Gu, M., Mackie, K., & Guo, F. (2023) · Nature Electronics · doi:10.1038/s41928-023-01069-w · Cited by 314 · see citing works
Organoid intelligence (OI): the new frontier in biocomputing and intelligence-in-a-dish
Smirnova, L., Caffo, B. S., Gracias, D. H., Huang, Q., Pantoja, I. E. M., Tang, B., Zack, D. J., Berlinicke, C. A., Boyd, J. L., Harris, T. D., et al. (2023) · Frontiers in Science · doi:10.3389/fsci.2023.1017235 · Cited by 290 · see citing works
Self-citationGetting to the cores of autism
Iakoucheva, L. M., Muotri, A. R., & Sebat, J. (2019) · Cell · doi:10.1016/j.cell.2019.07.037 · Cited by 260 · see citing works
Self-citationChallenges of Organoid Research
Andrews, M., & Kriegstein, A. (2022) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-111020-090812 · Cited by 216 · see citing works
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Synthetic Analyses of Single-Cell Transcriptomes from Multiple Brain Organoids and Fetal Brain
Tanaka, Y., Çakır, B., Xiang, Y., Sullivan, G. J., & Park, I. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.01.038 · Cited by 238 · see citing works
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Functional neuronal circuitry and oscillatory dynamics in human brain organoids
Sharf, T., van der Molen, T., Glasauer, S. M. K., Guzman, E., Buccino, A. P., Luna, G., Cheng, Z., Audouard, M., Ranasinghe, K. G., Kudo, K., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-32115-4 · Cited by 242 · see citing works
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Linaro, D., Vermaercke, B., Iwata, R., Ramaswamy, A., Davis, B. A., Boubakar, L., Libé-Philippot, B., Bilheu, A., Bruyne, L. D., Gall, D., et al. (2019) · doi:10.1101/626218 · Cited by 210 · see citing works
“This is in contrast with data obtained using neural organoids in vitro or following transplantation (Mansour et al., 2018; Trujillo et al., 2019), which show highly correlated activity indicative of circuit immaturity.”
ResultShell microelectrode arrays (MEAs) for brain organoids
Huang, Q., Tang, B.-H., Romero, J. C., Yang, Y., Elsayed, S. K., Pahapale, G. J., Lee, T.-J., Pantoja, I. E. M., Han, F., Berlinicke, C. J., et al. (2022) · bioRxiv · doi:10.1126/sciadv.abq5031 · Cited by 195 · see citing works
Organoids: a systematic review of ethical issues
de Jongh, D., Massey, E. K., Berishvili, E., Fonseca, L. M., Lebreton, F., Bellofatto, K., Bignard, J., Seißler, J., Buerck, L. W.-V., Honarpisheh, M. M., et al. (2022) · Stem Cell Research & Therapy · doi:10.1186/s13287-022-02950-9 · Cited by 208 · see citing works
Zika Virus Targets Glioblastoma Stem Cells through a SOX2-Integrin αvβ5 Axis
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Self-citationSchaworonkow, N., & Voytek, B. (2020) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2020.100895 · Cited by 190 · see citing works
Self-citationEthical issues related to brain organoid research
Hyun, I., Scharf-Deering, J. C., & Lunshof, J. E. (2020) · Brain Research · doi:10.1016/j.brainres.2020.146653 · Cited by 186 · see citing works
An increase of inhibition drives the developmental decorrelation of neural activity
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Brain organoids: an ensemble of bioassays to investigate human neurodevelopment and disease
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The role of gamma oscillations in central nervous system diseases: Mechanism and treatment
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The Edge of Sentience: Risk and Precaution in Humans, Other Animals, and AI
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An integrated transcriptomic cell atlas of human neural organoids
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One-Stop Microfluidic Assembly of Human Brain Organoids To Model Prenatal Cannabis Exposure
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Moral Limits of Brain Organoid Research
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Self-citationModelling human brain development and disease with organoids
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Are there islands of awareness?
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Reintroduction of the archaic variant of NOVA1 in cortical organoids alters neurodevelopment
Trujillo, C. A., Rice, E. S., Schaefer, N. K., Chaim, I. A., Wheeler, E. C., Madrigal, A. A., Buchanan, J., Preißl, S., Wang, A., Negraes, P. D., et al. (2021) · Science · doi:10.1126/science.aax2537 · Cited by 146 · see citing works
Self-citationThe role of manganese dysregulation in neurological disease: emerging evidence
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Cortical organoids model early brain development disrupted by 16p11.2 copy number variants in autism
Urresti, J., Zhang, P., Losada, P. M., Yu, N., Negraes, P. D., Trujillo, C. A., Antaki, D., Amar, M., Chau, K. K., Pramod, A. B., et al. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01243-6 · Cited by 133 · see citing works
Self-citationBrain Organoids and the Study of Neurodevelopment
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Self-citationThe Ethics of Cerebral Organoid Research: Being Conscious of Consciousness
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Transplantation of Human Brain Organoids: Revisiting the Science and Ethics of Brain Chimeras
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Microglia-like Cells Promote Neuronal Functions in Cerebral Organoids
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Advancing models of neural development with biomaterials
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Neuropathogenesis-on-chips for neurodegenerative diseases
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Developmental GABA polarity switch and neuronal plasticity in Bioengineered Neuronal Organoids
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Connectomics of human electrophysiology
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Human cerebral organoids establish subcortical projections in the mouse brain after transplantation
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Self-citationMapping the Ethical Issues of Brain Organoid Research and Application
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Ethical Challenges in Organoid Use
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Nicheformer: a foundation model for single-cell and spatial omics
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Human cerebral organoids and consciousness: a double-edged sword
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Multiscale 3D phenotyping of human cerebral organoids
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Past, Present, and Future of Brain Organoid Technology.
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Self-citationAdvancing Drug Discovery for Neurological Disorders Using iPSC-Derived Neural Organoids
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Tubular human brain organoids to model microglia-mediated neuroinflammation
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Innovations in 3D Tissue Models of Human Brain Physiology and Diseases
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Transcription and Beyond: Delineating FOXG1 Function in Cortical Development and Disorders
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Bio‐Inspired 3D Artificial Neuromorphic Circuits
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Human neuronal maturation comes of age: cellular mechanisms and species differences
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A mesh microelectrode array for non-invasive electrophysiology within neural organoids
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Brainstem Organoids From Human Pluripotent Stem Cells
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Evolutionary conservation and divergence of the human brain transcriptome
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Human Brain Organoids and Consciousness
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Self-citationEmerging Bioelectronics for Brain Organoid Electrophysiology
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Rigor and reproducibility in human brain organoid research: Where we are and where we need to go
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Modelling epilepsy in the mouse: challenges and solutions
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Stretchable mesh microelectronics for the biointegration and stimulation of human neural organoids
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Recent Advances in Three-Dimensional Stem Cell Culture Systems and Applications
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Kim, M., Hwang, J. C., Min, S., Park, Y., Kim, S., Kim, E., Seo, H., Chung, W. G., Lee, J., Cho, S., et al. (2022) · Nano Letters · doi:10.1021/acs.nanolett.2c02790 · Cited by 68 · see citing works
Genome Editing in iPSC-Based Neural Systems: From Disease Models to Future Therapeutic Strategies
McTague, A., Rossignoli, G., Ferrini, A., Barral, S., & Kurian, M. A. (2021) · Frontiers in Genome Editing · doi:10.3389/fgeed.2021.630600 · Cited by 67 · see citing works
Zheng, X., Han, D., Liu, W., Wang, X., Pan, N., Wang, Y., & Chen, Z. (2023) · Theranostics · doi:10.7150/thno.80271 · Cited by 67 · see citing works
Sofosbuvir protects human brain organoids against SARS-CoV-2Preprint
Mesci, P., Macia, Á., Saleh, A., Martin‐Sancho, L., Yin, X., Snethlage, C. E., Avansini, S. H., Chanda, S. K., & Muotri, A. R. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.30.125856 · Cited by 67 · see citing works
Self-citationBrain organoids, consciousness, ethics and moral status
Jeziorski, J. J., Brandt, R., Evans, J. H., Campana, W. M., KALICHMAN, M. W., Thompson, E. T., Goldstein, L. S. B., Koch, C., & Muotri, A. R. (2022) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2022.03.020 · Cited by 67 · see citing works
Self-citationBrain organoids and organoid intelligence from ethical, legal, and social points of view
Härtung, T., Pantoja, I. E. M., & Smirnova, L. (2024) · Frontiers in Artificial Intelligence · doi:10.3389/frai.2023.1307613 · Cited by 66 · see citing works
Brain organoids as a model system for human neurodevelopment and disease
Setia, H., & Muotri, A. R. (2019) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2019.03.002 · Cited by 66 · see citing works
Self-citationLogan, S., Arzua, T., Yan, Y., Jiang, C., Liu, X., Yu, L., Liu, Q.-S., & Bai, X. (2020) · Cells · doi:10.3390/cells9051301 · Cited by 62 · see citing works
Advances in 3D neuronal microphysiological systems: towards a functional nervous system on a chip
Anderson, W. A., Bosak, A. J., Högberg, H. T., Härtung, T., & Moore, M. J. (2021) · In Vitro Cellular & Developmental Biology - Animal · doi:10.1007/s11626-020-00532-8 · Cited by 64 · see citing works
- Authors
- Trujillo, C. A., Gao, R., Negraes, P. D., Gu, J., Buchanan, J., Preissl, S., Wang, A., Wu, W., Haddad, G. G., Chaim, I. A., Domissy, A., Vandenberghe, M., Devor, A., Yeo, G. W., Voytek, B., & Muotri, A. R.
- Affiliations
- University of California San Diego (US)
- Harvard University (US)
- Corresponding author
- Muotri, Alysson R.
- ORCID
- Venue
- Cell Stem Cell
- Publisher
- Elsevier BV
- Published
- 2019-10
- Volume
- 25
- Issue
- 4
- Pages
- 558-569.e7
- ISSN
- 1875-9777 (ISSN-L)
- 1934-5909
- PMC
- PMC6778040
- OpenAlex
- W2970454553
- Cited by
- 974
- References
- 80
- Citations by year
- 2026: 131 · 2025: 148 · 2024: 186 · 2023: 110 · 2022: 131 · 2021: 131 · 2020: 98 · 2019: 32 · 2018: 5
- FWCI
- 57.13
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell stem cell (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- California Institute for Regenerative Medicine (DISC1-08825, DISC2-09649)
- Whitehall Foundation (2017-12-73)
- National Institutes of Health (U19MH1073671, R01MH108528, R01MH109885, R01MH100175, R56MH109587, R01MH094753)
- National Alliance for Research on Schizophrenia and Depression
- Simons Foundation Autism Research Initiative (345469)
- Natural Sciences and Engineering Research Council of Canada
- School of Medicine, University of California, San Diego
- University of California, San Diego
- Foundation for the National Institutes of Health (/NIGMS K12 GM068524, K12 GM068524, U19MH1073671)
- Kavli Institute for Brain and Mind, University of California, San Diego
- Spectrum Pharmaceuticals
- National Science Foundation (1736028)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- cortical organoids, human brain development, network activity, glutamatergic signaling, GABAergic neurotransmission, developmental programming, functional brain networks
- MeSH terms
- Biological Clocks, Cells, Cultured, Cerebellar Cortex, gamma-Aminobutyric Acid, Humans, Nerve Net, Synaptic Transmission, Organoids, Signal Transduction, Neocortex, Gene Expression Profiling, Neurogenesis, Induced Pluripotent Stem Cells, Single-Cell Analysis, Electromagnetic Radiation
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