Genetics of human brain development.

Silbereis, J. C., Pochareddy, S., Zhu, Y., Li, M. & Sestan, N. The cellular and molecular landscapes of the developing human central nervous system. Neuron 89, 248–268 (2016).

pubmed: 26796689 pmcid: 4959909 doi: 10.1016/j.neuron.2015.12.008

Jayaraman, D., Bae, B. I. & Walsh, C. A. The genetics of primary microcephaly. Annu. Rev. Genom. Hum. Genet. 19, 177–200 (2018).

doi: 10.1146/annurev-genom-083117-021441

Lizarraga, S. B. et al. Cdk5rap2 regulates centrosome function and chromosome segregation in neuronal progenitors. Development 137, 1907–1917 (2010).

pubmed: 20460369 pmcid: 2867323 doi: 10.1242/dev.040410

Pulvers, J. N. et al. Mutations in mouse Aspm (abnormal spindle-like microcephaly associated) cause not only microcephaly but also major defects in the germline. Proc. Natl Acad. Sci. USA 107, 16595–16600 (2010).

pubmed: 20823249 pmcid: 2944708 doi: 10.1073/pnas.1010494107

Gruber, R. et al. MCPH1 regulates the neuroprogenitor division mode by coupling the centrosomal cycle with mitotic entry through the Chk1-Cdc25 pathway. Nat. Cell Biol. 13, 1325–1334 (2011).

pubmed: 21947081 doi: 10.1038/ncb2342

Barrera, J. A. et al. CDK5RAP2 regulates centriole engagement and cohesion in mice. Dev. Cell 18, 913–926 (2010).

pubmed: 20627074 pmcid: 3078807 doi: 10.1016/j.devcel.2010.05.017

Sousa, A. M. M., Meyer, K. A., Santpere, G., Gulden, F. O. & Sestan, N. Evolution of the human nervous system function, structure, and development. Cell 170, 226–247 (2017).

pubmed: 28708995 pmcid: 5647789 doi: 10.1016/j.cell.2017.06.036

Cadwell, C. R., Bhaduri, A., Mostajo-Radji, M. A., Keefe, M. G. & Nowakowski, T. J. Development and arealization of the cerebral cortex. Neuron 103, 980–1004 (2019).

pubmed: 31557462 pmcid: 9245854 doi: 10.1016/j.neuron.2019.07.009

Lancaster, M. A. et al. Cerebral organoids model human brain development and microcephaly. Nature 501, 373–379 (2013). This study pioneers a 3D cerebral organoid model derived from hPS cells to recapitulate human-specific features of brain development and model human brain disorders (microcephaly).

pubmed: 23995685 doi: 10.1038/nature12517

Pollen, A. A., Kilik, U., Lowe, C. B. & Camp, J. G. Human-specific genetics: new tools to explore the molecular and cellular basis of human evolution. Nat. Rev. Genet. https://doi.org/10.1038/s41576-022-00568-4 (2023).

doi: 10.1038/s41576-022-00568-4 pubmed: 36737647 pmcid: 9897628

Sullivan, P. F. & Geschwind, D. H. Defining the genetic, genomic, cellular, and diagnostic architectures of psychiatric disorders. Cell 177, 162–183 (2019).

pubmed: 30901538 pmcid: 6432948 doi: 10.1016/j.cell.2019.01.015

Klingler, E., Francis, F., Jabaudon, D. & Cappello, S. Mapping the molecular and cellular complexity of cortical malformations. Science 371, eaba4517 (2021).

pubmed: 33479124 doi: 10.1126/science.aba4517

Cuomo, A. S. E., Nathan, A., Raychaudhuri, S., MacArthur, D. G. & Powell, J. E. Single-cell genomics meets human genetics. Nat. Rev. Genet. 24, 535–549 (2023).

pubmed: 37085594 doi: 10.1038/s41576-023-00599-5

Kelley, K. W. & Pasca, S. P. Human brain organogenesis: toward a cellular understanding of development and disease. Cell 185, 42–61 (2022).

pubmed: 34774127 doi: 10.1016/j.cell.2021.10.003

Eichmuller, O. L. & Knoblich, J. A. Human cerebral organoids — a new tool for clinical neurology research. Nat. Rev. Neurol. 18, 661–680 (2022).

pubmed: 36253568 pmcid: 9576133 doi: 10.1038/s41582-022-00723-9

Andrews, M. G., Subramanian, L., Salma, J. & Kriegstein, A. R. How mechanisms of stem cell polarity shape the human cerebral cortex. Nat. Rev. Neurosci. 23, 711–724 (2022).

pubmed: 36180551 doi: 10.1038/s41583-022-00631-3

Cardenas, A. et al. Evolution of cortical neurogenesis in amniotes controlled by Robo signaling levels. Cell 174, 590–606.e21 (2018).

pubmed: 29961574 pmcid: 6063992 doi: 10.1016/j.cell.2018.06.007

Rakic, P. Evolution of the neocortex: a perspective from developmental biology. Nat. Rev. Neurosci. 10, 724–735 (2009).

pubmed: 19763105 pmcid: 2913577 doi: 10.1038/nrn2719

Corbin, J. G., Nery, S. & Fishell, G. Telencephalic cells take a tangent: non-radial migration in the mammalian forebrain. Nat. Neurosci. 4 (Suppl), 1177–1182 (2001).

pubmed: 11687827 doi: 10.1038/nn749

Ma, T. et al. Subcortical origins of human and monkey neocortical interneurons. Nat. Neurosci. 16, 1588–1597 (2013).

pubmed: 24097041 doi: 10.1038/nn.3536

Paredes, M. F. et al. Extensive migration of young neurons into the infant human frontal lobe. Science 354, aaf7073 (2016).

pubmed: 27846470 pmcid: 5436574 doi: 10.1126/science.aaf7073

Shi, Y. et al. Mouse and human share conserved transcriptional programs for interneuron development. Science 374, eabj6641 (2021).

pubmed: 34882453 doi: 10.1126/science.abj6641

Song, H. & Poo, M. The cell biology of neuronal navigation. Nat. Cell Biol. 3, E81–E88 (2001).

pubmed: 11231595 doi: 10.1038/35060164

Petanjek, Z. et al. Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc. Natl Acad. Sci. USA 108, 13281–13286 (2011).

pubmed: 21788513 pmcid: 3156171 doi: 10.1073/pnas.1105108108

Zhu, Y. et al. Spatiotemporal transcriptomic divergence across human and macaque brain development. Science 362, eaat8077 (2018).

pubmed: 30545855 pmcid: 6900982 doi: 10.1126/science.aat8077

Yeung, M. S. et al. Dynamics of oligodendrocyte generation and myelination in the human brain. Cell 159, 766–774 (2014).

pubmed: 25417154 doi: 10.1016/j.cell.2014.10.011

Masuda, T., Sankowski, R., Staszewski, O. & Prinz, M. Microglia heterogeneity in the single-cell era. Cell Rep. 30, 1271–1281 (2020).

pubmed: 32023447 doi: 10.1016/j.celrep.2020.01.010

Vanderhaeghen, P. & Polleux, F. Developmental mechanisms underlying the evolution of human cortical circuits. Nat. Rev. Neurosci. 24, 213–232 (2023).

pubmed: 36792753 pmcid: 10064077 doi: 10.1038/s41583-023-00675-z

Benito-Kwiecinski, S. et al. An early cell shape transition drives evolutionary expansion of the human forebrain. Cell 184, 2084–2102.e19 (2021). This study compares forebrain organoids of great apes and humans and reveals mechanisms of prolonged expansion of neuroepithelial cells in humans.

pubmed: 33765444 pmcid: 8054913 doi: 10.1016/j.cell.2021.02.050

Kanton, S. et al. Organoid single-cell genomic atlas uncovers human-specific features of brain development. Nature 574, 418–422 (2019).

pubmed: 31619793 doi: 10.1038/s41586-019-1654-9

Iwata, R., Casimir, P. & Vanderhaeghen, P. Mitochondrial dynamics in postmitotic cells regulate neurogenesis. Science 369, 858–862 (2020).

pubmed: 32792401 doi: 10.1126/science.aba9760

Marchetto, M. C. et al. Species-specific maturation profiles of human, chimpanzee and bonobo neural cells. eLife 8, e37527 (2019).

pubmed: 30730291 pmcid: 6366899 doi: 10.7554/eLife.37527

Sorrells, S. F. et al. Immature excitatory neurons develop during adolescence in the human amygdala. Nat. Commun. 10, 2748 (2019).

pubmed: 31227709 pmcid: 6588589 doi: 10.1038/s41467-019-10765-1

Zhou, Y. et al. Molecular landscapes of human hippocampal immature neurons across lifespan. Nature 607, 527–533 (2022).

pubmed: 35794479 pmcid: 9316413 doi: 10.1038/s41586-022-04912-w

Zhong, S. et al. Decoding the development of the human hippocampus. Nature 577, 531–536 (2020).

pubmed: 31942070 doi: 10.1038/s41586-019-1917-5

Wang, L. et al. A cross-species proteomic map of synapse development reveals neoteny during human postsynaptic density maturation. Preprint at bioRxiv https://doi.org/10.1101/2022.10.24.513541 (2022).

doi: 10.1101/2022.10.24.513541 pubmed: 36656775 pmcid: 9836620

Iwata, R. et al. Mitochondria metabolism sets the species-specific tempo of neuronal development. Science 379, eabn4705 (2023).

pubmed: 36705539 doi: 10.1126/science.abn4705

Wang, X., Tsai, J. W., LaMonica, B. & Kriegstein, A. R. A new subtype of progenitor cell in the mouse embryonic neocortex. Nat. Neurosci. 14, 555–561 (2011).

pubmed: 21478886 pmcid: 3083489 doi: 10.1038/nn.2807

Hansen, D. V., Lui, J. H., Parker, P. R. & Kriegstein, A. R. Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464, 554–561 (2010).

pubmed: 20154730 doi: 10.1038/nature08845

Nowakowski, T. J. et al. Spatiotemporal gene expression trajectories reveal developmental hierarchies of the human cortex. Science 358, 1318–1323 (2017).

pubmed: 29217575 pmcid: 5991609 doi: 10.1126/science.aap8809

Bilgic, M. et al. Truncated radial glia as a common precursor in the late corticogenesis of gyrencephalic mammals. Preprint at bioRxiv https://doi.org/10.1101/2022.05.05.490846 (2023).

doi: 10.1101/2022.05.05.490846 pubmed: 36824894 pmcid: 9948962

Huang, W. et al. Origins and proliferative states of human oligodendrocyte precursor cells. Cell 182, 594–608.e11 (2020).

pubmed: 32679030 pmcid: 7415734 doi: 10.1016/j.cell.2020.06.027

Allen, D. E. et al. Fate mapping of neural stem cell niches reveals distinct origins of human cortical astrocytes. Science 376, 1441–1446 (2022).

pubmed: 35587512 pmcid: 9233096 doi: 10.1126/science.abm5224

Delgado, R. N. et al. Individual human cortical progenitors can produce excitatory and inhibitory neurons. Nature 601, 397–403 (2022).

pubmed: 34912114 doi: 10.1038/s41586-021-04230-7

Ma, S. et al. Molecular and cellular evolution of the primate dorsolateral prefrontal cortex. Science 377, eabo7257 (2022).

pubmed: 36007006 pmcid: 9614553 doi: 10.1126/science.abo7257

Krienen, F. M. et al. Innovations present in the primate interneuron repertoire. Nature 586, 262–269 (2020).

pubmed: 32999462 pmcid: 7957574 doi: 10.1038/s41586-020-2781-z

Schmitz, M. T. et al. The development and evolution of inhibitory neurons in primate cerebrum. Nature 603, 871–877 (2022).

pubmed: 35322231 pmcid: 8967711 doi: 10.1038/s41586-022-04510-w

Molnar, Z., Luhmann, H. J. & Kanold, P. O. Transient cortical circuits match spontaneous and sensory-driven activity during development. Science 370, eabb2153 (2020).

pubmed: 33060328 pmcid: 8050953 doi: 10.1126/science.abb2153

Kostovic, I. & Rakic, P. Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J. Comp. Neurol. 297, 441–470 (1990).

pubmed: 2398142 doi: 10.1002/cne.902970309

Zoghbi, H. Y. & Bear, M. F. Synaptic dysfunction in neurodevelopmental disorders associated with autism and intellectual disabilities. Cold Spring Harb. Perspect. Biol. 4, a009886 (2012).

pubmed: 22258914 pmcid: 3282414 doi: 10.1101/cshperspect.a009886

Tessier-Lavigne, M. & Goodman, C. S. The molecular biology of axon guidance. Science 274, 1123–1133 (1996).

pubmed: 8895455 doi: 10.1126/science.274.5290.1123

Poo, M. M. Transcriptome, connectome and neuromodulation of the primate brain. Cell 185, 2636–2639 (2022).

pubmed: 35732175 doi: 10.1016/j.cell.2022.05.011

Zhou, Y. et al. Atypical behaviour and connectivity in SHANK3-mutant macaques. Nature 570, 326–331 (2019).

pubmed: 31189958 doi: 10.1038/s41586-019-1278-0

Liu, Z. et al. Autism-like behaviours and germline transmission in transgenic monkeys overexpressing MeCP2. Nature 530, 98–102 (2016).

pubmed: 26808898 doi: 10.1038/nature16533

Romero, I. G. Seeing humans through an evolutionary lens. Science 380, 360–361 (2023).

pubmed: 37104588 doi: 10.1126/science.adh0745

Whalen, S. et al. Machine learning dissection of human accelerated regions in primate neurodevelopment. Neuron 111, 857–873.e8 (2023).

pubmed: 36640767 doi: 10.1016/j.neuron.2022.12.026

Keough, K. C. et al. Three-dimensional genome rewiring in loci with human accelerated regions. Science 380, eabm1696 (2023). This study reveals that HARs interact with brain developmental genes through structural variants that alter 3D genome folding and cause enhancer adaptations, a mechanism underlying the rapid evolution of HARs.

pubmed: 37104607 doi: 10.1126/science.abm1696

Pollard, K. S. et al. An RNA gene expressed during cortical development evolved rapidly in humans. Nature 443, 167–172 (2006).

pubmed: 16915236 doi: 10.1038/nature05113

Espinos, A., Fernandez-Ortuno, E., Negri, E. & Borrell, V. Evolution of genetic mechanisms regulating cortical neurogenesis. Dev. Neurobiol. 82, 428–453 (2022).

pubmed: 35670518 pmcid: 9543202 doi: 10.1002/dneu.22891

Girskis, K. M. et al. Rewiring of human neurodevelopmental gene regulatory programs by human accelerated regions. Neuron 109, 3239–3251.e7 (2021).

pubmed: 34478631 pmcid: 8542612 doi: 10.1016/j.neuron.2021.08.005

Boyd, J. L. et al. Human-chimpanzee differences in a FZD8 enhancer alter cell-cycle dynamics in the developing neocortex. Curr. Biol. 25, 772–779 (2015).

pubmed: 25702574 pmcid: 4366288 doi: 10.1016/j.cub.2015.01.041

Lui, J. H. et al. Radial glia require PDGFD–PDGFRβ signalling in human but not mouse neocortex. Nature 515, 264–268 (2014).

pubmed: 25391964 pmcid: 4231536 doi: 10.1038/nature13973

Suzuki, I. K. et al. Human-specific NOTCH2NL genes expand cortical neurogenesis through Delta/Notch regulation. Cell 173, 1370–1384.e16 (2018).

pubmed: 29856955 pmcid: 6092419 doi: 10.1016/j.cell.2018.03.067

Fiddes, I. T. et al. Human-specific NOTCH2NL genes affect notch signaling and cortical neurogenesis. Cell 173, 1356–1369.e22 (2018).

pubmed: 29856954 pmcid: 5986104 doi: 10.1016/j.cell.2018.03.051

Pollen, A. A. et al. Establishing cerebral organoids as models of human-specific brain evolution. Cell 176, 743–756.e17 (2019).

pubmed: 30735633 pmcid: 6544371 doi: 10.1016/j.cell.2019.01.017

Van Heurck, R. et al. CROCCP2 acts as a human-specific modifier of cilia dynamics and mTOR signaling to promote expansion of cortical progenitors. Neuron 111, 65–80.e6 (2023).

pubmed: 36334595 pmcid: 9831670 doi: 10.1016/j.neuron.2022.10.018

Keeney, J. G. et al. DUF1220 protein domains drive proliferation in human neural stem cells and are associated with increased cortical volume in anthropoid primates. Brain Struct. Funct. 220, 3053–3060 (2015).

pubmed: 24957859 doi: 10.1007/s00429-014-0814-9

Johansson, P. A. et al. A cis-acting structural variation at the ZNF558 locus controls a gene regulatory network in human brain development. Cell Stem Cell 29, 52–69.e8 (2022).

pubmed: 34624206 doi: 10.1016/j.stem.2021.09.008

Florio, M. et al. Human-specific gene ARHGAP11B promotes basal progenitor amplification and neocortex expansion. Science 347, 1465–1470 (2015).

pubmed: 25721503 doi: 10.1126/science.aaa1975

Namba, T. et al. Human-specific ARHGAP11B acts in mitochondria to expand neocortical progenitors by glutaminolysis. Neuron 105, 867–881.e9 (2020).

pubmed: 31883789 doi: 10.1016/j.neuron.2019.11.027

Kalebic, N. et al. Human-specific ARHGAP11B induces hallmarks of neocortical expansion in developing ferret neocortex. eLife 7, e41241 (2018).

pubmed: 30484771 pmcid: 6303107 doi: 10.7554/eLife.41241

Heide, M. et al. Human-specific ARHGAP11B increases size and folding of primate neocortex in the fetal marmoset. Science 369, 546–550 (2020).

pubmed: 32554627 doi: 10.1126/science.abb2401

Fischer, J. et al. Human-specific ARHGAP11B ensures human-like basal progenitor levels in hominid cerebral organoids. EMBO Rep. 23, e54728 (2022).

pubmed: 36381990 pmcid: 9646322 doi: 10.15252/embr.202254728

Ju, X. C. et al. The hominoid-specific gene TBC1D3 promotes generation of basal neural progenitors and induces cortical folding in mice. eLife 5, e18197 (2016).

pubmed: 27504805 pmcid: 5028191 doi: 10.7554/eLife.18197

Hou, Q. Q., Xiao, Q., Sun, X. Y., Ju, X. C. & Luo, Z. G. TBC1D3 promotes neural progenitor proliferation by suppressing the histone methyltransferase G9a. Sci. Adv. 7, eaba8053 (2021).

pubmed: 33523893 pmcid: 7810367 doi: 10.1126/sciadv.aba8053

Liu, J. et al. The primate-specific gene TMEM14B marks outer radial glia cells and promotes cortical expansion and folding. Cell Stem Cell 21, 635–649.e8 (2017).

pubmed: 29033352 doi: 10.1016/j.stem.2017.08.013

Pinson, A. et al. Human TKTL1 implies greater neurogenesis in frontal neocortex of modern humans than Neanderthals. Science 377, eabl6422 (2022).

pubmed: 36074851 doi: 10.1126/science.abl6422

Luria, V., Ma, S., Shibata, M., Pattabiraman, K. & Sestan, N. Molecular and cellular mechanisms of human cortical connectivity. Curr. Opin. Neurobiol. 80, 102699 (2023).

pubmed: 36921362 doi: 10.1016/j.conb.2023.102699

Enard, W. et al. Molecular evolution of FOXP2, a gene involved in speech and language. Nature 418, 869–872 (2002).

pubmed: 12192408 doi: 10.1038/nature01025

Enard, W. et al. A humanized version of Foxp2 affects cortico-basal ganglia circuits in mice. Cell 137, 961–971 (2009).

pubmed: 19490899 doi: 10.1016/j.cell.2009.03.041

Charrier, C. et al. Inhibition of SRGAP2 function by its human-specific paralogs induces neoteny during spine maturation. Cell 149, 923–935 (2012).

pubmed: 22559944 pmcid: 3357949 doi: 10.1016/j.cell.2012.03.034

Fossati, M. et al. SRGAP2 and its human-specific paralog co-regulate the development of excitatory and inhibitory synapses. Neuron 91, 356–369 (2016).

pubmed: 27373832 pmcid: 5385270 doi: 10.1016/j.neuron.2016.06.013

Dennis, M. Y. et al. Evolution of human-specific neural SRGAP2 genes by incomplete segmental duplication. Cell 149, 912–922 (2012).

pubmed: 22559943 pmcid: 3365555 doi: 10.1016/j.cell.2012.03.033

Schmidt, E. R. E. et al. A human-specific modifier of cortical connectivity and circuit function. Nature 599, 640–644 (2021).

pubmed: 34707291 pmcid: 9161439 doi: 10.1038/s41586-021-04039-4

Ataman, B. et al. Evolution of osteocrin as an activity-regulated factor in the primate brain. Nature 539, 242–247 (2016).

pubmed: 27830782 pmcid: 5499253 doi: 10.1038/nature20111

Shibata, M. et al. Hominini-specific regulation of CBLN2 increases prefrontal spinogenesis. Nature 598, 489–494 (2021).

pubmed: 34599306 pmcid: 9018127 doi: 10.1038/s41586-021-03952-y

Gu, Z. et al. Control of species-dependent cortico-motoneuronal connections underlying manual dexterity. Science 357, 400–404 (2017).

pubmed: 28751609 pmcid: 5774341 doi: 10.1126/science.aan3721

Luo, X. et al. 3D genome of macaque fetal brain reveals evolutionary innovations during primate corticogenesis. Cell 184, 723–740.e21 (2021).

pubmed: 33508230 doi: 10.1016/j.cell.2021.01.001

Xue, J. R. et al. The functional and evolutionary impacts of human-specific deletions in conserved elements. Science 380, eabn2253 (2023). This study identifies over 10,000 human-specific deletions in genomic regions highly conserved in other vertebrates, suggesting evolutionary mechanisms driving traits unique to humans.

pubmed: 37104592 pmcid: 10202372 doi: 10.1126/science.abn2253

McLean, C. Y. et al. Human-specific loss of regulatory DNA and the evolution of human-specific traits. Nature 471, 216–219 (2011).

pubmed: 21390129 pmcid: 3071156 doi: 10.1038/nature09774

Linker, S. B. et al. Human-specific regulation of neural maturation identified by cross-primate transcriptomics. Curr. Biol. 32, 4797–4807 e4795 (2022).

pubmed: 36228612 doi: 10.1016/j.cub.2022.09.028

Pinson, A., Maricic, T., Zeberg, H., Paabo, S. & Huttner, W. B. Response to comment on “Human TKTL1 implies greater neurogenesis in frontal neocortex of modern humans than Neanderthals”. Science 379, eadf2212 (2023).

pubmed: 36893240 doi: 10.1126/science.adf2212

Herai, R. H., Semendeferi, K. & Muotri, A. R. Comment on “Human TKTL1 implies greater neurogenesis in frontal neocortex of modern humans than Neanderthals”. Science 379, eadf0602 (2023).

pubmed: 36893252 doi: 10.1126/science.adf0602

Atkinson, E. G. et al. No evidence for recent selection at FOXP2 among diverse human populations. Cell 174, 1424–1435.e15 (2018).

pubmed: 30078708 pmcid: 6128738 doi: 10.1016/j.cell.2018.06.048

Fisher, S. E. Human genetics: the evolving story of FOXP2. Curr. Biol. 29, R65–R67 (2019).

pubmed: 30668952 doi: 10.1016/j.cub.2018.11.047

Benjamin, K. J. M. et al. Genetic and environmental contributions to ancestry differences in gene expression in the human brain. Preprint at bioRxiv https://doi.org/10.1101/2023.03.28.534458 (2023).

doi: 10.1101/2023.03.28.534458 pubmed: 37425961 pmcid: 10327178

Schoeler, T. et al. Participation bias in the UK Biobank distorts genetic associations and downstream analyses. Nat. Hum. Behav. https://doi.org/10.1038/s41562-023-01579-9 (2023).

doi: 10.1038/s41562-023-01579-9 pubmed: 37106081 pmcid: 10365993

Fatumo, S. et al. A roadmap to increase diversity in genomic studies. Nat. Med. 28, 243–250 (2022).

pubmed: 35145307 doi: 10.1038/s41591-021-01672-4

Liao, W. W. et al. A draft human pangenome reference. Nature 617, 312–324 (2023).

pubmed: 37165242 pmcid: 10172123 doi: 10.1038/s41586-023-05896-x

Bolognesi, B. & Lehner, B. Protein overexpression: reaching the limit. eLife 7, e39804 (2018).

pubmed: 30095407 pmcid: 6086656 doi: 10.7554/eLife.39804

Fair, T. & Pollen, A. A. Genetic architecture of human brain evolution. Curr. Opin. Neurobiol. 80, 102710 (2023).

pubmed: 37003107 doi: 10.1016/j.conb.2023.102710

Juriloff, D. M. & Harris, M. J. Insights into the etiology of mammalian neural tube closure defects from developmental, genetic and evolutionary studies. J. Dev. Biol. 6, 22 (2018).

pubmed: 30134561 pmcid: 6162505 doi: 10.3390/jdb6030022

Greene, N. D. & Copp, A. J. Neural tube defects. Annu. Rev. Neurosci. 37, 221–242 (2014).

pubmed: 25032496 pmcid: 4486472 doi: 10.1146/annurev-neuro-062012-170354

Karzbrun, E. et al. Human neural tube morphogenesis in vitro by geometric constraints. Nature 599, 268–272 (2021). This study develops a chip-based system that enables self-organization of 3D hPS cell culture into specific spatial structure and cell fate patterns to model neural tube morphogenesis.

pubmed: 34707290 pmcid: 8828633 doi: 10.1038/s41586-021-04026-9

Abdel Fattah, A. R. et al. Actuation enhances patterning in human neural tube organoids. Nat. Commun. 12, 3192 (2021).

pubmed: 34045434 pmcid: 8159931 doi: 10.1038/s41467-021-22952-0

Li, R. et al. Recapitulating cortical development with organoid culture in vitro and modeling abnormal spindle-like (ASPM related primary) microcephaly disease. Protein Cell 8, 823–833 (2017).

pubmed: 29058117 pmcid: 5676597 doi: 10.1007/s13238-017-0479-2

Gabriel, E. et al. CPAP promotes timely cilium disassembly to maintain neural progenitor pool. EMBO J. 35, 803–819 (2016).

pubmed: 26929011 pmcid: 4972140 doi: 10.15252/embj.201593679

Zhang, W. et al. Modeling microcephaly with cerebral organoids reveals a WDR62-CEP170-KIF2A pathway promoting cilium disassembly in neural progenitors. Nat. Commun. 10, 2612 (2019).

pubmed: 31197141 pmcid: 6565620 doi: 10.1038/s41467-019-10497-2

Xu, D., Zhang, F., Wang, Y., Sun, Y. & Xu, Z. Microcephaly-associated protein WDR62 regulates neurogenesis through JNK1 in the developing neocortex. Cell Rep. 6, 104–116 (2014).

pubmed: 24388750 doi: 10.1016/j.celrep.2013.12.016

Zhou, Z. W. et al. DNA damage response in microcephaly development of MCPH1 mouse model. DNA Repair. 12, 645–655 (2013).

pubmed: 23683352 doi: 10.1016/j.dnarep.2013.04.017

Esk, C. et al. A human tissue screen identifies a regulator of ER secretion as a brain-size determinant. Science 370, 935–941 (2020). This study combines CRISPR–Cas9-based loss-of-function screening with barcoded cell lineage tracing technologies to simultaneously evaluate 172 microcephaly risk genes in human cerebral brain organoids. It reveals that endoplasmic reticulum secretion affects tissue integrity and brain size and that its dysregulation leads to microcephaly phenotypes.

pubmed: 33122427 doi: 10.1126/science.abb5390

Montgomery, S. H. & Mundy, N. I. Microcephaly genes evolved adaptively throughout the evolution of eutherian mammals. BMC Evol. Biol. 14, 120 (2014).

pubmed: 24898820 pmcid: 4055943 doi: 10.1186/1471-2148-14-120

Li, Y. et al. Induction of expansion and folding in human cerebral organoids. Cell Stem Cell 20, 385–396.e3 (2017).

pubmed: 28041895 doi: 10.1016/j.stem.2016.11.017

Eichmuller, O. L. et al. Amplification of human interneuron progenitors promotes brain tumors and neurological defects. Science 375, eabf5546 (2022). This study utilizes a tuberous sclerosis complex patient-derived brain organoid model and gene editing technology to identify mTOR-driven overproliferation of a specific interneuron progenitor subpopulation in the caudal ganglionic eminence as the cellular and molecular mechanisms underlying the disease pathology.

pubmed: 35084981 pmcid: 7613689 doi: 10.1126/science.abf5546

Anastasaki, C. et al. Human iPSC-derived neurons and cerebral organoids establish differential effects of germline NF1 gene mutations. Stem Cell Rep. 14, 541–550 (2020).

doi: 10.1016/j.stemcr.2020.03.007

Wegscheid, M. L. et al. Patient-derived iPSC-cerebral organoid modeling of the 17q11.2 microdeletion syndrome establishes CRLF3 as a critical regulator of neurogenesis. Cell Rep. 36, 109315 (2021).

pubmed: 34233200 pmcid: 8278229 doi: 10.1016/j.celrep.2021.109315

Papes, F. et al. Transcription Factor 4 loss-of-function is associated with deficits in progenitor proliferation and cortical neuron content. Nat. Commun. 13, 2387 (2022).

pubmed: 35501322 pmcid: 9061776 doi: 10.1038/s41467-022-29942-w

de Jong, J. O. et al. Cortical overgrowth in a preclinical forebrain organoid model of CNTNAP2-associated autism spectrum disorder. Nat. Commun. 12, 4087 (2021).

pubmed: 34471112 pmcid: 8410758 doi: 10.1038/s41467-021-24358-4

Baala, L. et al. Homozygous silencing of T-box transcription factor EOMES leads to microcephaly with polymicrogyria and corpus callosum agenesis. Nat. Genet. 39, 454–456 (2007).

pubmed: 17353897 doi: 10.1038/ng1993

Bershteyn, M. et al. Human iPSC-derived cerebral organoids model cellular features of lissencephaly and reveal prolonged mitosis of outer radial glia. Cell Stem Cell 20, 435–449.e4 (2017).

pubmed: 28111201 pmcid: 5667944 doi: 10.1016/j.stem.2016.12.007

Lim, J. S. et al. Brain somatic mutations in MTOR cause focal cortical dysplasia type II leading to intractable epilepsy. Nat. Med. 21, 395–400 (2015).

pubmed: 25799227 doi: 10.1038/nm.3824

Bizzotto, S. & Walsh, C. A. Genetic mosaicism in the human brain: from lineage tracing to neuropsychiatric disorders. Nat. Rev. Neurosci. 23, 275–286 (2022).

pubmed: 35322263 doi: 10.1038/s41583-022-00572-x

Fry, A. E., Cushion, T. D. & Pilz, D. T. The genetics of lissencephaly. Am. J. Med. Genet. C. Semin. Med. Genet. 166C, 198–210 (2014).

pubmed: 24862549 doi: 10.1002/ajmg.c.31402

Iefremova, V. et al. An organoid-based model of cortical development identifies non-cell-autonomous defects in Wnt signaling contributing to Miller-Dieker syndrome. Cell Rep. 19, 50–59 (2017).

pubmed: 28380362 doi: 10.1016/j.celrep.2017.03.047

Karzbrun, E., Kshirsagar, A., Cohen, S. R., Hanna, J. H. & Reiner, O. Human brain organoids on a chip reveal the physics of folding. Nat. Phys. 14, 515–522 (2018).

pubmed: 29760764 pmcid: 5947782 doi: 10.1038/s41567-018-0046-7

Bamba, Y., Kanemura, Y., Okano, H. & Yamasaki, M. Visualization of migration of human cortical neurons generated from induced pluripotent stem cells. J. Neurosci. Methods 289, 57–63 (2017).

pubmed: 28694214 doi: 10.1016/j.jneumeth.2017.07.004

Gleeson, J. G. et al. Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell 92, 63–72 (1998).

pubmed: 9489700 doi: 10.1016/S0092-8674(00)80899-5

Des Portes, V. et al. A novel CNS gene required for neuronal migration and involved in X-linked subcortical laminar heterotopia and lissencephaly syndrome. Cell 92, 51–61 (1998).

pubmed: 9489699 doi: 10.1016/S0092-8674(00)80898-3

Niehaus, I. et al. Cerebral organoids expressing mutant actin genes reveal cellular mechanism underlying microcephalic cortical malformation. Preprint at bioRxiv https://doi.org/10.1101/2022.12.07.519435 (2022).

doi: 10.1101/2022.12.07.519435

Klaus, J. et al. Altered neuronal migratory trajectories in human cerebral organoids derived from individuals with neuronal heterotopia. Nat. Med. 25, 561–568 (2019).

pubmed: 30858616 doi: 10.1038/s41591-019-0371-0

Birey, F. et al. Assembly of functionally integrated human forebrain spheroids. Nature 545, 54–59 (2017). This study pioneers an assembloid approach fusing spheroids to model different brain regions and perturbations in human interneuron migration patterns in Timothy syndrome patients.

pubmed: 28445465 pmcid: 5805137 doi: 10.1038/nature22330

Birey, F. et al. Dissecting the molecular basis of human interneuron migration in forebrain assembloids from Timothy syndrome. Cell Stem Cell 29, 248–264.e7 (2022).

pubmed: 34990580 doi: 10.1016/j.stem.2021.11.011

Qian, X. et al. Sliced human cortical organoids for modeling distinct cortical layer formation. Cell Stem Cell 26, 766–781.e9 (2020). This study develops a slicing method for large organoids to prevent interior cell death for long-term maintenance to recapitulate late-stage neurodevelopmental features, such as distinct cortical layer segregation and emergence of human-specific astrocytes.

pubmed: 32142682 pmcid: 7366517 doi: 10.1016/j.stem.2020.02.002

Avansini, S. H. et al. Junctional instability in neuroepithelium and network hyperexcitability in a focal cortical dysplasia human model. Brain 145, 1962–1977 (2022).

pubmed: 34957478 doi: 10.1093/brain/awab479

Xu, R. et al. OLIG2 Drives abnormal neurodevelopmental phenotypes in human iPSC-based organoid and chimeric mouse models of Down syndrome. Cell Stem Cell 24, 908–926.e8 (2019).

pubmed: 31130512 pmcid: 6944064 doi: 10.1016/j.stem.2019.04.014

Morelli, K. H. et al. MECP2-related pathways are dysregulated in a cortical organoid model of myotonic dystrophy. Sci. Transl Med. 14, eabn2375 (2022).

pubmed: 35767654 pmcid: 9645119 doi: 10.1126/scitranslmed.abn2375

Paulsen, B. et al. Autism genes converge on asynchronous development of shared neuron classes. Nature 602, 268–273 (2022). This study generates cortical organoid models with different ASD-associated mutations to reveal their convergent mechanisms in changing the timing of human neuronal development.

pubmed: 35110736 pmcid: 8852827 doi: 10.1038/s41586-021-04358-6

Van Battum, E. Y., Brignani, S. & Pasterkamp, R. J. Axon guidance proteins in neurological disorders. Lancet Neurol. 14, 532–546 (2015).

pubmed: 25769423 doi: 10.1016/S1474-4422(14)70257-1

Paul, L. K. et al. Agenesis of the corpus callosum: genetic, developmental and functional aspects of connectivity. Nat. Rev. Neurosci. 8, 287–299 (2007).

pubmed: 17375041 doi: 10.1038/nrn2107

Martins-Costa, C. et al. ARID1B controls transcriptional programs of axon projection in the human corpus callosum. Preprint at bioRxiv https://doi.org/10.1101/2023.05.04.539362 (2023).

doi: 10.1101/2023.05.04.539362

Willsey, H. R., Willsey, A. J., Wang, B. & State, M. W. Genomics, convergent neuroscience and progress in understanding autism spectrum disorder. Nat. Rev. Neurosci. 23, 323–341 (2022).

pubmed: 35440779 doi: 10.1038/s41583-022-00576-7

Zhang, Z., Wang, X., Park, S., Song, H. & Ming, G. L. Development and application of brain region-specific organoids for investigating psychiatric disorders. Biol. Psychiatry 93, 594–605 (2023).

pubmed: 36759261 doi: 10.1016/j.biopsych.2022.12.015

Khan, T. A. et al. Neuronal defects in a human cellular model of 22q11.2 deletion syndrome. Nat. Med. 26, 1888–1898 (2020).

pubmed: 32989314 pmcid: 8525897 doi: 10.1038/s41591-020-1043-9

Zhang, Z. et al. The fragile X mutation impairs homeostatic plasticity in human neurons by blocking synaptic retinoic acid signaling. Sci. Transl Med. 10, eaar4338 (2018).

pubmed: 30068571 pmcid: 6317709 doi: 10.1126/scitranslmed.aar4338

Kang, Y. et al. A human forebrain organoid model of fragile X syndrome exhibits altered neurogenesis and highlights new treatment strategies. Nat. Neurosci. 24, 1377–1391 (2021).

pubmed: 34413513 pmcid: 8484073 doi: 10.1038/s41593-021-00913-6

Yildirim, M. et al. Label-free three-photon imaging of intact human cerebral organoids for tracking early events in brain development and deficits in Rett syndrome. eLife 10, eaar4338 (2022).

Gomes, A. R. et al. Modeling Rett syndrome with human patient-specific forebrain organoids. Front. Cell Dev. Biol. 8, 610427 (2020).

pubmed: 33363173 pmcid: 7758289 doi: 10.3389/fcell.2020.610427

Samarasinghe, R. A. et al. Identification of neural oscillations and epileptiform changes in human brain organoids. Nat. Neurosci. 24, 1488–1500 (2021).

pubmed: 34426698 pmcid: 9070733 doi: 10.1038/s41593-021-00906-5

Miura, Y. et al. Generation of human striatal organoids and cortico-striatal assembloids from human pluripotent stem cells. Nat. Biotechnol. 38, 1421–1430 (2020).

pubmed: 33273741 pmcid: 9042317 doi: 10.1038/s41587-020-00763-w

Sun, A. X. et al. Potassium channel dysfunction in human neuronal models of Angelman syndrome. Science 366, 1486–1492 (2019).

pubmed: 31857479 pmcid: 7735558 doi: 10.1126/science.aav5386

Ye, F. et al. DISC1 regulates neurogenesis via modulating kinetochore attachment of Ndel1/Nde1 during mitosis. Neuron 96, 1041–1054.e5 (2017).

pubmed: 29103808 pmcid: 5731645 doi: 10.1016/j.neuron.2017.10.010

Srikanth, P. et al. Shared effects of DISC1 disruption and elevated WNT signaling in human cerebral organoids. Transl. Psychiatry 8, 77 (2018).

pubmed: 29643329 pmcid: 5895714 doi: 10.1038/s41398-018-0122-x

Stachowiak, E. K. et al. Cerebral organoids reveal early cortical maldevelopment in schizophrenia-computational anatomy and genomics, role of FGFR1. Transl. Psychiatry 7, 6 (2017).

pubmed: 30446636 pmcid: 5802550 doi: 10.1038/s41398-017-0054-x

Steinberg, D. J. et al. Modeling genetic epileptic encephalopathies using brain organoids. EMBO Mol. Med. 13, e13610 (2021).

pubmed: 34268881 pmcid: 8350905 doi: 10.15252/emmm.202013610

Eroglu, C. & Barres, B. A. Regulation of synaptic connectivity by glia. Nature 468, 223–231 (2010).

pubmed: 21068831 pmcid: 4431554 doi: 10.1038/nature09612

Madhavan, M. et al. Induction of myelinating oligodendrocytes in human cortical spheroids. Nat. Methods 15, 700–706 (2018).

pubmed: 30046099 pmcid: 6508550 doi: 10.1038/s41592-018-0081-4

Luhmann, H. J., Kanold, P. O., Molnar, Z. & Vanhatalo, S. Early brain activity: translations between bedside and laboratory. Prog. Neurobiol. 213, 102268 (2022).

pubmed: 35364141 pmcid: 9923767 doi: 10.1016/j.pneurobio.2022.102268

Fan, W., Christian, K. M., Song, H. & Ming, G. L. Applications of brain organoids for infectious diseases. J. Mol. Biol. 434, 167243 (2022).

pubmed: 34536442 doi: 10.1016/j.jmb.2021.167243

Hwang, H. M., Ku, R. Y. & Hashimoto-Torii, K. Prenatal environment that affects neuronal migration. Front. Cell Dev. Biol. 7, 138 (2019).

pubmed: 31380373 pmcid: 6652208 doi: 10.3389/fcell.2019.00138

Zhang, D. Y., Song, H. & Ming, G. L. Modeling neurological disorders using brain organoids. Semin. Cell Dev. Biol. 111, 4–14 (2021).

pubmed: 32561297 doi: 10.1016/j.semcdb.2020.05.026

Ming, G. L., Tang, H. & Song, H. Advances in Zika virus research: stem cell models, challenges, and opportunities. Cell Stem Cell 19, 690–702 (2016).

pubmed: 27912090 pmcid: 5218815 doi: 10.1016/j.stem.2016.11.014

Tang, H. et al. Zika virus infects human cortical neural progenitors and attenuates their growth. Cell Stem Cell 18, 587–590 (2016).

pubmed: 26952870 pmcid: 5299540 doi: 10.1016/j.stem.2016.02.016

Qian, X. et al. Brain-region-specific organoids using mini-bioreactors for modeling ZIKV exposure. Cell 165, 1238–1254 (2016). This study reports generation of different region-specific organoids from human iPS cells and modelling of Zika virus infection using forebrain organoids, showing that Zika virus specifically targets RGCs to cause microcephaly phenotypes.

pubmed: 27118425 pmcid: 4900885 doi: 10.1016/j.cell.2016.04.032

Li, C. et al. Zika virus disrupts neural progenitor development and leads to microcephaly in mice. Cell Stem Cell 19, 120–126 (2016).

pubmed: 27179424 doi: 10.1016/j.stem.2016.04.017

Xu, D., Li, C., Qin, C. F. & Xu, Z. Update on the animal models and underlying mechanisms for ZIKV-induced microcephaly. Annu. Rev. Virol. 6, 459–479 (2019).

pubmed: 31206355 doi: 10.1146/annurev-virology-092818-015740

Dang, J. et al. Zika virus depletes neural progenitors in human cerebral organoids through activation of the innate immune receptor TLR3. Cell Stem Cell 19, 258–265 (2016).

pubmed: 27162029 pmcid: 5116380 doi: 10.1016/j.stem.2016.04.014

Link, N. et al. Mutations in ANKLE2, a ZIKA virus target, disrupt an asymmetric cell division pathway in Drosophila neuroblasts to cause microcephaly. Dev. Cell 51, 713–729.e6 (2019).

pubmed: 31735666 pmcid: 6917859 doi: 10.1016/j.devcel.2019.10.009

Thomas, A. X. et al. ANKLE2-related microcephaly: a variable microcephaly syndrome resembling Zika infection. Ann. Clin. Transl. Neurol. 9, 1276–1288 (2022).

pubmed: 35871307 pmcid: 9380164 doi: 10.1002/acn3.51629

Yoon, K. J. et al. Zika-virus-encoded NS2A disrupts mammalian cortical neurogenesis by degrading Adherens junction proteins. Cell Stem Cell 21, 349–358.e6 (2017).

pubmed: 28826723 pmcid: 5600197 doi: 10.1016/j.stem.2017.07.014

Gabriel, E. et al. Recent Zika virus isolates induce premature differentiation of neural progenitors in human brain organoids. Cell Stem Cell 20, 397–406.e5 (2017).

pubmed: 28132835 doi: 10.1016/j.stem.2016.12.005

Onorati, M. et al. Zika virus disrupts phospho-TBK1 localization and mitosis in human neuroepithelial stem cells and radial glia. Cell Rep. 16, 2576–2592 (2016).

pubmed: 27568284 pmcid: 5135012 doi: 10.1016/j.celrep.2016.08.038

Smeland, O. B., Frei, O., Dale, A. M. & Andreassen, O. A. The polygenic architecture of schizophrenia — rethinking pathogenesis and nosology. Nat. Rev. Neurol. 16, 366–379 (2020).

pubmed: 32528109 doi: 10.1038/s41582-020-0364-0

Shibata, M. et al. Regulation of prefrontal patterning and connectivity by retinoic acid. Nature 598, 483–488 (2021).

pubmed: 34599305 pmcid: 9018119 doi: 10.1038/s41586-021-03953-x

Barbeito-Andres, J., Schuler-Faccini, L. & Garcez, P. P. Why is congenital Zika syndrome asymmetrically distributed among human populations? PLoS Biol. 16, e2006592 (2018).

pubmed: 30142150 pmcid: 6126861 doi: 10.1371/journal.pbio.2006592

Esposito, G., Azhari, A. & Borelli, J. L. Gene x environment interaction in developmental disorders: where do we stand and what’s next? Front. Psychol. 9, 2036 (2018).

pubmed: 30416467 pmcid: 6212589 doi: 10.3389/fpsyg.2018.02036

Seah, C., Huckins, L. M. & Brennand, K. J. Stem cell models for context-specific modeling in psychiatric disorders. Biol. Psychiatry 93, 642–650 (2022).

pubmed: 36658083 doi: 10.1016/j.biopsych.2022.09.033

Schrode, N. et al. Synergistic effects of common schizophrenia risk variants. Nat. Genet. 51, 1475–1485 (2019).

pubmed: 31548722 pmcid: 6778520 doi: 10.1038/s41588-019-0497-5

Singh, T. et al. Rare coding variants in ten genes confer substantial risk for schizophrenia. Nature 604, 509–516 (2022).

pubmed: 35396579 pmcid: 9805802 doi: 10.1038/s41586-022-04556-w

O’Neill, A. C. et al. Spatial centrosome proteome of human neural cells uncovers disease-relevant heterogeneity. Science 376, eabf9088 (2022).

pubmed: 35709258 doi: 10.1126/science.abf9088

Panagiotakos, G. & Pasca, S. P. A matter of space and time: emerging roles of disease-associated proteins in neural development. Neuron 110, 195–208 (2022).

pubmed: 34847355 doi: 10.1016/j.neuron.2021.10.035

Wang, Y. et al. Modeling human telencephalic development and autism-associated SHANK3 deficiency using organoids generated from single neural rosettes. Nat. Commun. 13, 5688 (2022).

pubmed: 36202854 pmcid: 9537523 doi: 10.1038/s41467-022-33364-z

Gandal, M. J. et al. Transcriptome-wide isoform-level dysregulation in ASD, schizophrenia, and bipolar disorder. Science 362, eaat8127 (2018).

pubmed: 30545856 pmcid: 6443102 doi: 10.1126/science.aat8127

Mirzaa, G. M. & Paciorkowski, A. R. Introduction: brain malformations. Am. J. Med. Genet. C. Semin. Med. Genet. 166C, 117–123 (2014).

pubmed: 24853778 doi: 10.1002/ajmg.c.31404

Gilmore, J. H., Knickmeyer, R. C. & Gao, W. Imaging structural and functional brain development in early childhood. Nat. Rev. Neurosci. 19, 123–137 (2018).

pubmed: 29449712 pmcid: 5987539 doi: 10.1038/nrn.2018.1

Duy, P. Q. et al. Brain ventricles as windows into brain development and disease. Neuron 110, 12–15 (2022).

pubmed: 34990576 pmcid: 9212067 doi: 10.1016/j.neuron.2021.12.009

Grasby, K. L. et al. The genetic architecture of the human cerebral cortex. Science 367, eaay6690 (2020).

pubmed: 32193296 pmcid: 7295264 doi: 10.1126/science.aay6690

Vinsland, E. & Linnarsson, S. Single-cell RNA-sequencing of mammalian brain development: insights and future directions. Development 149, dev200180 (2022).

pubmed: 35593486 doi: 10.1242/dev.200180

Zeng, H. What is a cell type and how to define it? Cell 185, 2739–2755 (2022).

pubmed: 35868277 pmcid: 9342916 doi: 10.1016/j.cell.2022.06.031

Tabula Sapiens Consortium et al. The Tabula Sapiens: a multiple-organ, single-cell transcriptomic atlas of humans. Science 376, eabl4896 (2022).

doi: 10.1126/science.abl4896

Rao, A., Barkley, D., Franca, G. S. & Yanai, I. Exploring tissue architecture using spatial transcriptomics. Nature 596, 211–220 (2021).

pubmed: 34381231 pmcid: 8475179 doi: 10.1038/s41586-021-03634-9

Haniffa, M. et al. A roadmap for the Human Developmental Cell Atlas. Nature 597, 196–205 (2021).

pubmed: 34497388 pmcid: 10337595 doi: 10.1038/s41586-021-03620-1

Stuart, T. & Satija, R. Integrative single-cell analysis. Nat. Rev. Genet. 20, 257–272 (2019).

pubmed: 30696980 doi: 10.1038/s41576-019-0093-7

Greener, J. G., Kandathil, S. M., Moffat, L. & Jones, D. T. A guide to machine learning for biologists. Nat. Rev. Mol. Cell Biol. 23, 40–55 (2022).

pubmed: 34518686 doi: 10.1038/s41580-021-00407-0

Gayoso, A. et al. A Python library for probabilistic analysis of single-cell omics data. Nat. Biotechnol. 40, 163–166 (2022).

pubmed: 35132262 doi: 10.1038/s41587-021-01206-w

Palla, G., Fischer, D. S., Regev, A. & Theis, F. J. Spatial components of molecular tissue biology. Nat. Biotechnol. 40, 308–318 (2022).

pubmed: 35132261 doi: 10.1038/s41587-021-01182-1

Millar, J. K. et al. Disruption of two novel genes by a translocation co-segregating with schizophrenia. Hum. Mol. Genet. 9, 1415–1423 (2000).

pubmed: 10814723 doi: 10.1093/hmg/9.9.1415

Sachs, N. A. et al. A frameshift mutation in disrupted in schizophrenia 1 in an American family with schizophrenia and schizoaffective disorder. Mol. Psychiatry 10, 758–764 (2005).

pubmed: 15940305 doi: 10.1038/sj.mp.4001667

Duan, X. et al. Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell 130, 1146–1158 (2007).

pubmed: 17825401 pmcid: 2002573 doi: 10.1016/j.cell.2007.07.010

Faulkner, R. L. et al. Development of hippocampal mossy fiber synaptic outputs by new neurons in the adult brain. Proc. Natl Acad. Sci. USA 105, 14157–14162 (2008).

pubmed: 18780780 pmcid: 2544594 doi: 10.1073/pnas.0806658105

Lee, H. et al. DISC1-mediated dysregulation of adult hippocampal neurogenesis in rats. Front. Syst. Neurosci. 9, 93 (2015).

pubmed: 26161071 pmcid: 4479724 doi: 10.3389/fnsys.2015.00093

Zhou, M. et al. mTOR Inhibition ameliorates cognitive and affective deficits caused by Disc1 knockdown in adult-born dentate granule neurons. Neuron 77, 647–654 (2013).

pubmed: 23439118 pmcid: 3586374 doi: 10.1016/j.neuron.2012.12.033

Chiang, C. H. et al. Integration-free induced pluripotent stem cells derived from schizophrenia patients with a DISC1 mutation. Mol. Psychiatry 16, 358–360 (2011).

pubmed: 21339753 pmcid: 4005725 doi: 10.1038/mp.2011.13

Wen, Z. et al. Synaptic dysregulation in a human iPS cell model of mental disorders. Nature 515, 414–418 (2014). This study pioneers the application of genome editing to establish the causality between genotype (a DISC1 mutation from patients) and phenotype (dysregulated synapse formation and gene expression) in patient-derived iPS cell modelling of psychiatric disorders.

pubmed: 25132547 pmcid: 4501856 doi: 10.1038/nature13716

Kang, E. et al. Interplay between a mental disorder risk gene and developmental polarity switch of GABA action leads to excitation-inhibition imbalance. Cell Rep. 28, 1419–1428 e1413 (2019).

pubmed: 31390557 pmcid: 6690484 doi: 10.1016/j.celrep.2019.07.024

Wang, X. et al. Structural interaction between DISC1 and ATF4 underlying transcriptional and synaptic dysregulation in an iPSC model of mental disorders. Mol. Psychiatry 26, 1346–1360 (2021).

pubmed: 31444471 doi: 10.1038/s41380-019-0485-2

Murai, K. et al. The TLX-miR-219 cascade regulates neural stem cell proliferation in neurodevelopment and schizophrenia iPSC model. Nat. Commun. 7, 10965 (2016).

pubmed: 26965827 pmcid: 4793043 doi: 10.1038/ncomms10965

Kang, E. et al. Rheb1 mediates DISC1-dependent regulation of new neuron development in the adult hippocampus. Neurogenesis 2, e1081715 (2015).

pubmed: 27606328 pmcid: 4973590 doi: 10.1080/23262133.2015.1081715

Kim, J. Y. et al. Interplay between DISC1 and GABA signaling regulates neurogenesis in mice and risk for schizophrenia. Cell 148, 1051–1064 (2012).

pubmed: 22385968 pmcid: 3294278 doi: 10.1016/j.cell.2011.12.037

Kang, E. et al. Interaction between FEZ1 and DISC1 in regulation of neuronal development and risk for schizophrenia. Neuron 72, 559–571 (2011).

pubmed: 22099459 pmcid: 3222865 doi: 10.1016/j.neuron.2011.09.032

Kim, J. Y. et al. DISC1 regulates new neuron development in the adult brain via modulation of AKT-mTOR signaling through KIAA1212. Neuron 63, 761–773 (2009).

pubmed: 19778506 pmcid: 3075620 doi: 10.1016/j.neuron.2009.08.008

Callicott, J. H. et al. DISC1 and SLC12A2 interaction affects human hippocampal function and connectivity. J. Clin. Investig. 123, 2961–2964 (2013).

pubmed: 23921125 pmcid: 3999052 doi: 10.1172/JCI67510

Kim, N. S. et al. Pharmacological rescue in patient iPSC and mouse models with a rare DISC1 mutation. Nat. Commun. 12, 1398 (2021).

pubmed: 33658519 pmcid: 7930023 doi: 10.1038/s41467-021-21713-3

Hong, Y., Yang, Q., Song, H. & Ming, G. L. Opportunities and limitations for studying neuropsychiatric disorders using patient-derived induced pluripotent stem cells. Mol. Psychiatry 28, 1430–1439 (2023).

pubmed: 36782062 doi: 10.1038/s41380-023-01990-8

Bennett, M. L., Song, H. & Ming, G. L. Microglia modulate neurodevelopment in human neuroimmune organoids. Cell Stem Cell 28, 2035–2036 (2021).

pubmed: 34861141 doi: 10.1016/j.stem.2021.11.005

Schafer, S. T. et al. An in vivo neuroimmune organoid model to study human microglia phenotypes. Cell 186, 2111–2126.e20 (2023).

pubmed: 37172564 doi: 10.1016/j.cell.2023.04.022

Ye, B. Approaches to vascularizing human brain organoids. PLoS Biol. 21, e3002141 (2023).

pubmed: 37155714 pmcid: 10194923 doi: 10.1371/journal.pbio.3002141

Revah, O. et al. Maturation and circuit integration of transplanted human cortical organoids. Nature 610, 319–326 (2022).

pubmed: 36224417 pmcid: 9556304 doi: 10.1038/s41586-022-05277-w

Jgamadze, D. et al. Structural and functional integration of human forebrain organoids with the injured adult rat visual system. Cell Stem Cell 30, 137–152.e7 (2023).

pubmed: 36736289 doi: 10.1016/j.stem.2023.01.004

Rifes, P. et al. Modeling neural tube development by differentiation of human embryonic stem cells in a microfluidic WNT gradient. Nat. Biotechnol. 38, 1265–1273 (2020). This study develops a microfluidic-based system for morphogen patterning of human iPS cells, generating neural tissue that exhibits progressive caudalization from the forebrain to the midbrain and hindbrain.

pubmed: 32451506 doi: 10.1038/s41587-020-0525-0

Deciphering Developmental Disorders Study. Large-scale discovery of novel genetic causes of developmental disorders. Nature 519, 223–228 (2015).

doi: 10.1038/nature14135

The PsychEncode Consortium. Revealing the brain’s molecular architecture. Science 362, 1262–1263 (2018).

doi: 10.1126/science.362.6420.1262

Rajewsky, N. et al. LifeTime and improving European healthcare through cell-based interceptive medicine. Nature 587, 377–386 (2020).

pubmed: 32894860 pmcid: 7656507 doi: 10.1038/s41586-020-2715-9

Ngai, J. BRAIN 2.0: transforming neuroscience. Cell 185, 4–8 (2022).

pubmed: 34995517 doi: 10.1016/j.cell.2021.11.037

Taylor, D. M. et al. The Pediatric Cell Atlas: defining the growth phase of human development at single-cell resolution. Dev. Cell 49, 10–29 (2019).

pubmed: 30930166 pmcid: 6616346 doi: 10.1016/j.devcel.2019.03.001

Kullo, I. J. et al. Polygenic scores in biomedical research. Nat. Rev. Genet. 23, 524–532 (2022).

pubmed: 35354965 pmcid: 9391275 doi: 10.1038/s41576-022-00470-z

Acosta, J. N., Falcone, G. J., Rajpurkar, P. & Topol, E. J. Multimodal biomedical AI. Nat. Med. 28, 1773–1784 (2022).

pubmed: 36109635 doi: 10.1038/s41591-022-01981-2

Wang, J. Y. & Doudna, J. A. CRISPR technology: a decade of genome editing is only the beginning. Science 379, eadd8643 (2023).

pubmed: 36656942 doi: 10.1126/science.add8643

Replogle, J. M. et al. Mapping information-rich genotype-phenotype landscapes with genome-scale Perturb-seq. Cell 185, 2559–2575.e28 (2022).

pubmed: 35688146 pmcid: 9380471 doi: 10.1016/j.cell.2022.05.013

Sadybekov, A. V. & Katritch, V. Computational approaches streamlining drug discovery. Nature 616, 673–685 (2023).

pubmed: 37100941 doi: 10.1038/s41586-023-05905-z

Paunovska, K., Loughrey, D. & Dahlman, J. E. Drug delivery systems for RNA therapeutics. Nat. Rev. Genet. 23, 265–280 (2022).

pubmed: 34983972 pmcid: 8724758 doi: 10.1038/s41576-021-00439-4

Schuster, J. et al. ZEB2 haploinsufficient Mowat-Wilson syndrome induced pluripotent stem cells show disrupted GABAergic transcriptional regulation and function. Front. Mol. Neurosci. 15, 988993 (2022).

pubmed: 36353360 pmcid: 9637781 doi: 10.3389/fnmol.2022.988993

Mellios, N. et al. MeCP2-regulated miRNAs control early human neurogenesis through differential effects on ERK and AKT signaling. Mol. Psychiatry 23, 1051–1065 (2018).

pubmed: 28439102 doi: 10.1038/mp.2017.86

Genetics of human brain development.

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Yi Zhou (Y)

Hongjun Song (H)

Guo-Li Ming (GL)

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