Functional cortical neurons and astrocytes from human pluripotent stem cells in 3D culture
Open accessAbstract
The human cerebral cortex develops through an elaborate succession of cellular events that, when disrupted, can lead to neuropsychiatric disease. The ability to reprogram somatic cells into pluripotent cells that can be differentiated in vitro provides a unique opportunity to study normal and abnormal corticogenesis. Here, we present a simple and reproducible 3D culture approach for generating a laminated cerebral cortex-like structure, named human cortical spheroids (hCSs), from pluripotent stem cells. hCSs contain neurons from both deep and superficial cortical layers and map transcriptionally to in vivo fetal development. These neurons are electrophysiologically mature, display spontaneous activity, are surrounded by nonreactive astrocytes and form functional synapses. Experiments in acute hCS slices demonstrate that cortical neurons participate in network activity and produce complex synaptic events. These 3D cultures should allow a detailed interrogation of human cortical development, function and disease, and may prove a versatile platform for generating other neuronal and glial subtypes in vitro.
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Human 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 [16]
Production of radial glial cells, intermediate progenitors, and deep- and superficial-layer neurons in an ordered temporal fashion has been reported by studies using all current protocols.
“The production of radial glial cells, intermediate progenitors, and deep- and superficial-layer neurons in an ordered temporal fashion has been reported by studies using all of the protocols currently in use2,3,5,25.”
From The use of brain organoids to investigate neural development and disease (2017) · cites this paper as [25]
Neurons fired action potentials spontaneously, there was evidence of synaptogenesis, and excitatory postsynaptic potentials were evoked by extracellular electrical stimulation, suggesting neuronal connectivity.
“Neurons fired action potentials spontaneously, there was evidence of synaptogenesis and excitatory postsynaptic potentials were evoked in response to extracellular electrical stimulation, suggesting neuronal connectivity.”
From The use of brain organoids to investigate neural development and disease (2017) · cites this paper as [25]
A degree of neuronal functional maturation was reported in dorsal telencephalon organoids allowed to develop for up to 180 days in vitro.
“A degree of neuronal functional maturation was reported in dorsal telencephalon organoids that were allowed to develop for up to 180 days in vitro25.”
From The use of brain organoids to investigate neural development and disease (2017) · cites this paper as [25]
Most protocols show transcriptional correlation with only early to mid-gestational stages of brain development.
“Most protocols show transcriptional correlation with only early to mid-gestational stages of brain development5,25,29.”
From The use of brain organoids to investigate neural development and disease (2017) · cites this paper as [25]
Transcriptomic profiles of organoid-derived neurons show greater neuronal maturation than those of 2D monolayer-derived neurons.
“Interestingly, the transcriptomic profiles of organoid-derived neurons show greater neuronal maturation than those of 2D monolayer-derived neurons25.”
From The use of brain organoids to investigate neural development and disease (2017) · cites this paper as [25]
Electrophysiological studies demonstrated functional synapses in several brain organoid models.
“In addition to these findings, electrophysiological studies have demonstrated functional synapses in several brain organoid models25,28, and electron microscopy has confirmed the presence of structurally defined synaptic junctions28.”
From The use of brain organoids to investigate neural development and disease (2017) · cites this paper as [25]
RNA-seq shows that transcriptional profiles of organoids cultured for up to 100 days are similar to those of developing human cortex at post-conceptional weeks 17-24.
“The results show that the transcriptional profiles of organoids cultured for up to 100 days are similar to those of developing human cortex at post-conceptional weeks 17–24 (REFS 25,29).”
From The use of brain organoids to investigate neural development and disease (2017) · cites this paper as [25]
The extrinsic organoid model shows promise for better reproducibility.
“The ‘extrinsic’ organoid model whereby patterning is influenced by externally added molecules rather than relying on intrinsic self-organization shows promise with regard to better reproducibility5,6,25.”
From The use of brain organoids to investigate neural development and disease (2017) · cites this paper as [25]
Human cortical spheroids are regionalized brain organoids whose generation is highly reliable.
“We derived 3D human cortical spheroids (hCS)19–21, which are regionalized brain organoids that show high reliability of differentiation22”
From Neuronal defects in a human cellular model of 22q11.2 deletion syndrome (2020) · cites this paper as [19]
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- Authors
- Paşca, A. M., Sloan, S. A., Clarke, L. E., Tian, Y., Makinson, C. D., Huber, N., Kim, C. H., Park, J.-Y., O'Rourke, N. A., Nguyen, K. D., Smith, S. J., Huguenard, J. R., Geschwind, D. H., Barres, B. A., & Paşca, S. P.
- Affiliations
- Stanford Medicine (US)
- University of California, Los Angeles (US)
- Yonsei University (KR)
- Stanford Blood Center (US)
- Allen Institute for Brain Science (US)
- ORCID
- Venue
- Nature Methods
- Published
- 2015-05-25
- Volume
- 12
- Issue
- 7
- Pages
- 671-678
- ISSN
- 1548-7091 (ISSN-L)
- 1548-7105
- PMC
- PMC4489980
- OpenAlex
- W1553983967
- Cited by
- 1,609
- References
- 44
- Citations by year
- 2026: 137 · 2025: 167 · 2024: 152 · 2023: 155 · 2022: 180 · 2021: 175 · 2020: 178 · 2019: 150 · 2018: 130 · 2017: 95 · 2016: 71 · 2015: 15
- FWCI
- 45.04
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Methods (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institutes of Health (5t32ns007280-35, 5r01mh094714-04)
- National Institute of Mental Health (F30MH106261, R21MH087898, 5R01MH094714, R33MH087898, R01-MH094714, R01MH099555, R01MH060233, R21MH099797, R01MH100900, R56MH060233, R37MH060233, T32MH020016)
- National Institute of General Medical Sciences (T32GM007365)
- National Institute of Neurological Disorders and Stroke (R01NS090911, R01NS075252, T32NS-007280, R01NS092474, R01NS081703, R01NS034774)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- cortical development, pluripotent stem cells, 3D cell culture, cortical neurons, astrocytes, spontaneous neuronal activity, cortical network activity, cortical lamination, in vitro brain models
- MeSH terms
- Astrocytes, Cells, Cultured, Cerebral Cortex, Humans, Synapses, Spheroids, Cellular, Pluripotent Stem Cells
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