The first neurons of the human cerebral cortex
Abstract
We describe a distinctive, widespread population of neurons situated beneath the pial surface of the human embryonic forebrain even before complete closure of the neural tube. These 'predecessor' cells include the first neurons seen in the primordium of the cerebral cortex, before the onset of local neurogenesis. Morphological analysis, combined with the study of centrosome location, regional transcription factors and patterns of mitosis and neurogenesis, indicates that predecessor cells invade the cortical primordium by tangential migration from the subpallium. These neurons, described here for the first time, precede all other known cell types of the developing cortex.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The developing human CNS has derived features including expanded proliferative zones and diverse neural stem/progenitor cell subtypes with enhanced proliferative capacity that facilitate brain expansion, especially neocortical expansion.
“the developing human CNS possesses certain divergent and highly derived features, such as expanded proliferative zones and diverse subtypes of neural stem and progenitor cells with enhanced proliferative capacities that facilitate brain expansion, especially of the neocortex (Bae et al., 2015; Bystron et al., 2006; Dehay et al., 2015; Gulden and Sestan, 2014; Howard et al., 2008; Lui et al., 2011;”
From The Cellular and Molecular Landscapes of the Developing Human Central Nervous System (2016) · cites this paper as Bystron et al., 2006
Cites
Noctor, S. C., Martínez-Cerdeño, V., Ivic, L., & Kriegstein, A. R. (2004) · Nature Neuroscience · doi:10.1038/nn1172 · Cited by 2,229 · see citing works
Interneuron Migration from Basal Forebrain to Neocortex: Dependence on <i>Dlx</i> Genes
Anderson, S. A., Eisenstat, D. D., Shi, L., & Rubenstein, J. L. R. (1997) · Science · doi:10.1126/science.278.5337.474 · Cited by 1,462 · see citing works
Englund, C., Fink, A., Lau, C., Pham, D., Daza, R. A. M., Bulfone, A., Kowalczyk, T., & Hevner, R. F. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2899-04.2005 · Cited by 1,261 · see citing works
Neuronal migration, with special reference to developing human brain: a review
Sidman, R. L., & RAKIC, P. T. (1973) · Brain Research · doi:10.1016/0006-8993(73)90617-3 · Cited by 1,251 · see citing works
Haubensak, W. E., Attardo, A., Denk, W. T., & Huttner, W. Β. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308600100 · Cited by 1,004 · see citing works
C ELL M IGRATION IN THE F OREBRAIN
Marín, Ó., & Rubenstein, J. L. R. (2003) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.041002.131058 · Cited by 917 · see citing works
Tbr1 regulates differentiation of the preplate and layer 6
Hevner, R. F., Shi, L., Justice, N., Hsueh, Y.-P., Sheng, M., Smiga, S., Bulfone, A., Goffinet, A. M., Campagnoni, A. T., & Rubenstein, J. L. R. (2001) · Neuron · doi:10.1016/s0896-6273(01)00211-2 · Cited by 857 · see citing works
Lavdas, A. A., Grigoriou, M., Pachnis, V., & Parnavelas, J. G. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-18-07881.1999 · Cited by 765 · see citing works
Embryonic vertebrate central nervous system: Revised terminology
Angevine, J. B., Bodian, D., Coulombre, A. J., Edds, M. V., Hamburger, V., Jacobson, M., Lyser, K. M., Prestige, M. C., Sidman, R. L., Varon, S. S., et al. (1970) · The Anatomical Record · doi:10.1002/ar.1091660214 · Cited by 727 · see citing works
Origin of GABAergic neurons in the human neocortex
Letinić, K., Zoncu, R., & RAKIC, P. T. (2002) · Nature · doi:10.1038/nature00779 · Cited by 718 · see citing works
Two modes of radial migration in early development of the cerebral cortex
Nadarajah, B., Brunstrom, J. E., Grutzendler, J., Wong, R., & Pearlman, A. L. (2001) · Nature Neuroscience · doi:10.1038/83967 · Cited by 689 · see citing works
Distinct cortical migrations from the medial and lateral ganglionic eminences
Anderson, S. A., Marín, Ó., Horn, C., Jennings, K., & Rubenstein, J. L. R. (2001) · Development · doi:10.1242/dev.128.3.353 · Cited by 651 · see citing works
Multiple origins of Cajal-Retzius cells at the borders of the developing pallium
Bielle, F., Griveau, A., Narboux‐Nême, N., Vigneau, S., Sigrist, M., Arber, S., Wassef, M., & Pierani, A. (2005) · Nature Neuroscience · doi:10.1038/nn1511 · Cited by 450 · see citing works
Cajal–Retzius cells and the development of the neocortex
Marín‐Padilla, M. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01164-8 · Cited by 444 · see citing works
Zhu, C., Zhao, J. H., Bibikova, M. V., Leverson, J. D., Bossy‐Wetzel, E., Fan, J., Abraham, R. T., & Jiang, W. B. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e05-02-0167 · Cited by 433 · see citing works
Bulfone, A., Smiga, S., Shimamura, K., Peterson, A. S., Puelles, L., & Rubenstein, J. L. R. (1995) · Neuron · doi:10.1016/0896-6273(95)90065-9 · Cited by 425 · see citing works
Nucleokinesis in Neuronal Migration
Tsai, L., & Gleeson, J. G. (2005) · Neuron · doi:10.1016/j.neuron.2005.04.013 · Cited by 357 · see citing works
Bellion, A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1030-05.2005 · Cited by 354 · see citing works
Telencephalic cells take a tangent: non-radial migration in the mammalian forebrain
Corbin, J. G., Nery, S. V., & Fishell, G. (2001) · Nature Neuroscience · doi:10.1038/nn749 · Cited by 293 · see citing works
DLX-1, DLX-2, and DLX-5 expression define distinct stages of basal forebrain differentiation
Eisenstat, D. D., Liu, J. K., Mione, M., Zhong, W., Yu, G. K., Anderson, S. A., Ghattas, I. R., Puelles, L., & Rubenstein, J. L. R. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19991115)414:2 · Cited by 286 · see citing works
Four-Dimensional Migratory Coordinates of GABAergic Interneurons in the Developing Mouse Cortex
Ang, E. S. B. C., Haydar, T. F., Gluncic, V., & Rakic, P. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-13-05805.2003 · Cited by 282 · see citing works
Par6α signaling controls glial-guided neuronal migration
Solecki, D. J., Model, L. S., Gaetz, J., Kapoor, T. M., & Hatten, M. E. (2004) · Nature Neuroscience · doi:10.1038/nn1332 · Cited by 281 · see citing works
Meyer, G., Soria, J. M., Martinez-Galan, J. R., Mart�n-Clemente, B., & Fair�n, A. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980810)397:4 · Cited by 228 · see citing works
Cell and molecular mechanisms involved in the migration of cortical interneurons
Métin, C., Baudoin, J., Rakić, S., & Parnavelas, J. G. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04630.x · Cited by 216 · see citing works
Embryonic and Early Fetal Development of the Human Neocortex
Meyer, G., Schaaps, J. P., Moreau, L., & Goffinet, A. M. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-05-01858.2000 · Cited by 215 · see citing works
Whitlock, K. E., & Westerfield, M. (2000) · Development · doi:10.1242/dev.127.17.3645 · Cited by 214 · see citing works
Iacopetti, P., Michelini, M., Stuckmann, I., Oback, B. J., Aaku‐Saraste, E., & Huttner, W. Β. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.8.4639 · Cited by 208 · see citing works
Expression of p73 and Reelin in the Developing Human Cortex
Meyer, G., Pérez‐García, C. G., Ábrahám, H., & Caput, D. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-12-04973.2002 · Cited by 204 · see citing works
The embryonic human brain : an atlas of developmental stages
O’Rahilly, R., & Müller, F. (2006) · Cited by 203 · see citing works
Hevner, R. F., Neogi, T., Englund, C., Daza, R. A. M., & Fink, A. (2003) · Developmental Brain Research · doi:10.1016/s0165-3806(02)00641-7 · Cited by 197 · see citing works
Kohtz, J. D., Baker, D. P., Corte, G., & Fishell, G. (1998) · Development · doi:10.1242/dev.125.24.5079 · Cited by 181 · see citing works
Neurogenic Radial Glial Cells in Reptile, Rodent and Human: from Mitosis to Migration
Weissman, T. A. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.6.550 · Cited by 158 · see citing works
Meyer, G. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.8.765 · Cited by 155 · see citing works
Emerging Complexity of Layer I in Human Cerebral Cortex
Rakić, S. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.10.1072 · Cited by 152 · see citing works
Progenitor cells of the olfactory receptor neuron lineage
Calof, A. L., Bonnin, A., Crocker, C. E., Kawauchi, S., Murray, R. C., Shou, J., & Wu, H. (2002) · Microscopy Research and Technique · doi:10.1002/jemt.10147 · Cited by 147 · see citing works
A Transient Population of Neurons Pioneers the Olfactory Pathway in the Zebrafish
Whitlock, K. E., & Westerfield, M. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-21-08919.1998 · Cited by 129 · see citing works
Tangential Migration in Neocortical Development
Jiménez, D., López‐Mascaraque, L., Valverde, F., & Carlos, J. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0586 · Cited by 119 · see citing works
Kohtz, J. D., Lee, H. Y., Gaiano, N., Segal, J., Ng, E., Larson, T., Baker, D. P., Garber, E. A., Williams, K. P., & Fishell, G. (2001) · Development · doi:10.1242/dev.128.12.2351 · Cited by 119 · see citing works
Cortical Specification of Mice and Men
Kennedy, H., & Dehay, C. (1993) · Cerebral Cortex · doi:10.1093/cercor/3.3.171 · Cited by 109 · see citing works
SUPRAVITAL DNA SYNTHESIS IN THE DEVELOPING HUMAN AND MOUSE BRAIN
RAKIC, P. T., & Sidman, R. L. (1968) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-196804000-00006 · Cited by 102 · see citing works
Olfactory Structures in Staged Human Embryos
Müller, F., & O’Rahilly, R. (2004) · Cells Tissues Organs · doi:10.1159/000081720 · Cited by 83 · see citing works
Time of Origin and Early Fate of Preplate Cells in the Cerebral Cortex of the Rat
Valverde, F., Carlos, J., & López‐Mascaraque, L. (1995) · Cerebral Cortex · doi:10.1093/cercor/5.6.483 · Cited by 67 · see citing works
A New Model for Olfactory Placode Development
Whitlock, K. E. (2004) · Brain Behavior and Evolution · doi:10.1159/000079742 · Cited by 62 · see citing works
Bystron, I., Molnár, Z., Otellin, V. A., & Blakemore, C. B. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4770-04.2005 · Cited by 40 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Evolution of the neocortex: a perspective from developmental biology
Rakic, P. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2719 · Cited by 1,565 · see citing works
Development of the human cerebral cortex: Boulder Committee revisited
Bystron, I., Blakemore, C., & Rakic, P. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2252 · Cited by 977 · see citing works
Self-citationThe Cellular and Molecular Landscapes of the Developing Human Central Nervous System
Silbereis, J. C., Pochareddy, S., Zhu, Y., Li, M., & Sestan, N. (2016) · Neuron · doi:10.1016/j.neuron.2015.12.008 · Cited by 818 · see citing works
Cell-cycle control and cortical development
Dehay, C., & Kennedy, H. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2097 · Cited by 655 · see citing works
Chambers, S. M., Qi, Y., Mica, Y., Lee, G., Zhang, X., Niu, L., Bilsland, J., Cao, L., Stevens, E. B., Whiting, P. J., et al. (2012) · Nature Biotechnology · doi:10.1038/nbt.2249 · Cited by 605 · see citing works
Espuny-Camacho, I., Michelsen, K. A., Gall, D., Linaro, D., Hasche, A., Bonnefont, J., Bali, C., Orduz, D., Bilheu, A., Herpoel, A., et al. (2013) · Neuron · doi:10.1016/j.neuron.2012.12.011 · Cited by 568 · see citing works
Eze, U. C., Bhaduri, A., Haeussler, M., Nowakowski, T. J., & Kriegstein, A. R. (2021) · Nature Neuroscience · doi:10.1038/s41593-020-00794-1 · Cited by 427 · see citing works
Schizophrenia: a tale of two critical periods for prefrontal cortical development
Selemon, L. D., & Zecevic, N. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.115 · Cited by 336 · see citing works
Nowakowski, T. J., Pollen, A. A., Sandoval-Espinosa, C., & Kriegstein, A. R. (2016) · Neuron · doi:10.1016/j.neuron.2016.09.005 · Cited by 347 · see citing works
Human pluripotent stem cell-derived neural constructs for predicting neural toxicity
Schwartz, M. P., Hou, Z., Propson, N. E., Zhang, J., Engstrom, C. J., Costa, V. S., Jiang, P., Nguyen, B. K., Bolin, J. M., Daly, W., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1516645112 · Cited by 325 · see citing works
Johnson, M. A., Weick, J. P., Pearce, R. A., & Zhang, S.-C. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4562-06.2007 · Cited by 318 · see citing works
Retinoic acid signaling and neuronal differentiation
Janesick, A., Wu, S. C., & Blumberg, B. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1815-9 · Cited by 295 · see citing works
The radial edifice of cortical architecture: From neuronal silhouettes to genetic engineering
RAKIC, P. T. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.02.010 · Cited by 252 · see citing works
Bayatti, N., Moss, J. A., Sun, L. Y., Ambrose, P. M., Ward, J. F. H., Lindsay, S., & Clowry, G. J. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm184 · Cited by 227 · see citing works
Neuronal migration in the adult brain: are we there yet?
Ghashghaei, H. T., Lai, C., & Anton, E. S. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2074 · Cited by 192 · see citing works
Tubulin-related cortical dysgeneses: microtubule dysfunction underlying neuronal migration defects
Jaglin, X. H., & Chelly, J. (2009) · Trends in Genetics · doi:10.1016/j.tig.2009.10.003 · Cited by 194 · see citing works
Reillo, I., & Borrell, V. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr284 · Cited by 177 · see citing works
Collin, G., & van den Heuvel, M. P. (2013) · The Neuroscientist · doi:10.1177/1073858413503712 · Cited by 198 · see citing works
The development of the neural crest in the human
O’Rahilly, R., & Müller, F. (2007) · Journal of Anatomy · doi:10.1111/j.1469-7580.2007.00773.x · Cited by 174 · see citing works
An Adaptive Threshold in Mammalian Neocortical Evolution
Lewitus, É., Kelava, I., Kalinka, A. T., Tomančák, P., & Huttner, W. Β. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1002000 · Cited by 162 · see citing works
Neural Stem Cells: Historical Perspective and Future Prospects
Breunig, J. J., Haydar, T. F., & RAKIC, P. T. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.005 · Cited by 161 · see citing works
Renewed focus on the developing human neocortex
Clowry, G. J., Molnár, Z., & RAKIC, P. T. (2010) · Journal of Anatomy · doi:10.1111/j.1469-7580.2010.01281.x · Cited by 141 · see citing works
Nat, R., Nilbratt, M., Narkilahti, S., Winblad, B. G., Hovatta, O., & Nordberg, A. K. (2006) · Glia · doi:10.1002/glia.20463 · Cited by 139 · see citing works
Comparative aspects of cortical neurogenesis in vertebrates
Cheung, A. F. P., Pollen, A. A., Tavare, A. N., DeProto, J., & Molnár, Z. (2007) · Journal of Anatomy · doi:10.1111/j.1469-7580.2007.00769.x · Cited by 137 · see citing works
Cerebral cortical development in rodents and primates
Molnár, Z., & Clowry, G. J. (2012) · Progress in brain research · doi:10.1016/b978-0-444-53860-4.00003-9 · Cited by 130 · see citing works
A Single-Cell Roadmap of Lineage Bifurcation in Human ESC Models of Embryonic Brain Development
Yao, Z., Mich, J. K., Ku, S., Menon, V., Krostag, A.-R., Martinez, R. A., Furchtgott, L., Mulholland, H., Bort, S. J., Fuqua, M. A., et al. (2016) · Cell stem cell · doi:10.1016/j.stem.2016.09.011 · Cited by 127 · see citing works
Growth of Thalamocortical Fibers to the Somatosensory Cortex in the Human Fetal Brain
Krsnik, Ž., Majić, V., Vasung, L., Huang, H., & Kostović, I. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00233 · Cited by 127 · see citing works
A 2020 view of tension-based cortical morphogenesis
Essen, D. C. V. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2016830117 · Cited by 124 · see citing works
Sestan, N., & State, M. W. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.015 · Cited by 127 · see citing works
Kostović, I., & JUDAS, M. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.04.018 · Cited by 119 · see citing works
Is this a brain which I see before me? Modeling human neural development with pluripotent stem cells
Suzuki, I. K., & Vanderhaeghen, P. (2015) · Development · doi:10.1242/dev.120568 · Cited by 110 · see citing works
Six1 is essential for early neurogenesis in the development of olfactory epithelium
Ikeda, K., Ookawara, S., Sato, S., Ando, Z., Kageyama, R., & Kawakami, K. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.08.020 · Cited by 113 · see citing works
Thinking out of the dish: what to learn about cortical development using pluripotent stem cells
van den Ameele, J., Tiberi, L., Vanderhaeghen, P., & Espuny-Camacho, I. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.03.005 · Cited by 110 · see citing works
The neuroanatomy of prematurity: Normal brain development and the impact of preterm birth
Ortinau, C. M., & Neil, J. J. (2014) · Clinical Anatomy · doi:10.1002/ca.22430 · Cited by 109 · see citing works
Consciousness in the cradle: on the emergence of infant experience
Bayne, T., Frohlich, J., Cusack, R., Moser, J., & Naci, L. (2023) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2023.08.018 · Cited by 106 · see citing works
Mühlebner, A., Bongaarts, A., Sarnat, H. B., Scholl, T. O., & Aronica, E. (2019) · Journal of Anatomy · doi:10.1111/joa.12956 · Cited by 96 · see citing works
Kostović, I. (2020) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2020.101883 · Cited by 102 · see citing works
Radial glia cells in the developing human brain
Howard, B. M., Mo, Z., Filipovic, R., Moore, A. R., Antic, S. D., & Zecevic, N. (2008) · The Neuroscientist · doi:10.1177/1073858407313512 · Cited by 97 · see citing works
Review: Cortical construction in autism spectrum disorder: columns, connectivity and the subplate
Hutsler, J. J., & Casanova, M. F. (2016) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12227 · Cited by 94 · see citing works
Human Cerebral Organoids and Fetal Brain Tissue Share Proteomic Similarities
Nascimento, J. M., Saia-Cereda, V. M., Sartore, R., da Costa, R. M., Schitine, C., Freitas, H. R., Murgu, M., Reis, R. A. D. M., Rehen, S. K., & Martins‐de‐Souza, D. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00303 · Cited by 88 · see citing works
Is Pax6 Critical for Neurogenesis in the Human Fetal Brain?
Mo, Z., & Zečević, N. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm181 · Cited by 80 · see citing works
Saito, T., Hanai, S., Takashima, S., Nakagawa, E., Okazaki, S., Inoue, T., Miyata, R., Hoshino, K., Akashi, T., Sasaki, M., et al. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq125 · Cited by 76 · see citing works
Comparative Aspects of Subplate Zone Studied with Gene Expression in Sauropsids and Mammals
Wang, W. Z., Oeschger, F. M., Montiel, J. F., García-Moreno, F., Hoerder-Suabedissen, A., Krubitzer, L., Ek, C. J., Saunders, N. R., Reim, K., Villalón, A., et al. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq278 · Cited by 76 · see citing works
Composition of the migratory mass during development of the olfactory nerve
Miller, A. M., Treloar, H. B., & Greer, C. A. (2010) · The Journal of Comparative Neurology · doi:10.1002/cne.22497 · Cited by 78 · see citing works
Significant features in the early prenatal development of the human brain
O’Rahilly, R., & Müller, F. (2008) · Annals of Anatomy - Anatomischer Anzeiger · doi:10.1016/j.aanat.2008.01.001 · Cited by 77 · see citing works
Pulvers, J. N., & Huttner, W. Β. (2009) · Development · doi:10.1242/dev.033498 · Cited by 77 · see citing works
Teissier, A., Griveau, A., Vigier, L., Piolot, T., Borello, U., & Pierani, A. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0776-10.2010 · Cited by 77 · see citing works
Evolution of Cerebral Cortical Development
Molnár, Z. (2011) · Brain Behavior and Evolution · doi:10.1159/000327325 · Cited by 71 · see citing works
Kirischuk, S., Luhmann, H. J., & Kilb, W. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.06.009 · Cited by 67 · see citing works
Judáš, M., Sedmak, G., & Pletikos, M. (2010) · Journal of Anatomy · doi:10.1111/j.1469-7580.2010.01283.x · Cited by 65 · see citing works
Costa, M. R., Kessaris, N., Richardson, W. D., Götz, M., & Hedin‐Pereira, C. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2418-07.2007 · Cited by 67 · see citing works
Ikeda, K., Kageyama, R., Suzuki, Y., & Kawakami, K. (2010) · The International Journal of Developmental Biology · doi:10.1387/ijdb.093041ki · Cited by 66 · see citing works
Taléns‐Visconti, R., Sánchez-Vera, I., Kostic, J., Aragó, M. A. P., Erceg, S., Stojković, M., & Guerri, C. (2010) · Stem Cells and Development · doi:10.1089/scd.2010.0037 · Cited by 65 · see citing works
Normal Development of the Fetal Brain by MRI
Glenn, O. A. (2009) · Seminars in Perinatology · doi:10.1053/j.semperi.2009.04.009 · Cited by 60 · see citing works
ATP-Dependent Chromatin Remodeling During Cortical Neurogenesis
Sokpor, G., Castro-Hernández, R., Rosenbusch, J., Staiger, J. F., & Tuoc, T. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00226 · Cited by 60 · see citing works
Anstötz, M., Cosgrove, K. E., Hack, I., Mugnaini, E., Maccaferri, G., & Lübke, J. H. R. (2013) · Brain Structure and Function · doi:10.1007/s00429-013-0627-2 · Cited by 64 · see citing works
Lamadrid-Romero, M., Solís, K. H., Cruz-Reséndiz, M. S., Pérez, J. E., Díaz, N. F., Flores‐Herrera, H., Garcı́a-López, G., Perichart, O., Reyes-Muñoz, E., Arenas‐Huertero, F., et al. (2017) · Neuroscience Research · doi:10.1016/j.neures.2017.08.003 · Cited by 58 · see citing works
Control of tangential/non-radial migration of neurons in the developing cerebral cortex
Nakajima, K. (2007) · Neurochemistry International · doi:10.1016/j.neuint.2007.05.006 · Cited by 56 · see citing works
Vasung, L., Rollins, C. K., Yun, H. J., Velasco‐Annis, C., Zhang, J., Wagstyl, K., Evans, A. C., Warfield, S. K., Feldman, H. A., Grant, P. E., et al. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz200 · Cited by 51 · see citing works
Regulation of Six1 expression by evolutionarily conserved enhancers in tetrapods
Sato, S., Ikeda, K., Shioi, G., Nakao, K., Yajima, H., & Kawakami, K. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.05.023 · Cited by 48 · see citing works
Krefft, O., Jabali, A., Iefremova, V., Koch, P., & Ladewig, J. (2018) · Journal of Visualized Experiments · doi:10.3791/56768 · Cited by 50 · see citing works
Carney, R. S. E., Bystron, I., López‐Bendito, G., & Molnár, Z. (2007) · Brain Structure and Function · doi:10.1007/s00429-007-0142-4 · Cited by 46 · see citing works
Transcriptional and Post-Transcriptional Mechanisms of the Development of Neocortical Lamination
Popovitchenko, T., & Rašin, M. (2017) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2017.00102 · Cited by 45 · see citing works
The importance of tracing developmental trajectories for clinical child neuropsychology
Annaz, D., Karmiloff‐Smith, A., & Thomas, M. S. C. (2008) · BIROn (Birkbeck, University of London) · Cited by 42 · see citing works
Using brain organoids to study human neurodevelopment, evolution and disease
Kyrousi, C., & Cappello, S. (2019) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.347 · Cited by 40 · see citing works
Neurogenesis in primates versus rodents and the value of non-human primate models
Zhang, R., Quan, H., Wang, Y., & Luo, F. (2023) · National Science Review · doi:10.1093/nsr/nwad248 · Cited by 42 · see citing works
Uniform neural tissue models produced on synthetic hydrogels using standard culture techniques
Barry, C., Schmitz, M. T., Propson, N. E., Hou, Z., Zhang, J., Nguyen, B. K., Bolin, J. M., Jiang, P., McIntosh, B. E., Probasco, M. D., et al. (2017) · Experimental Biology and Medicine · doi:10.1177/1535370217715028 · Cited by 40 · see citing works
The heterogeneity of human Cajal-Retzius neurons
Meyer, G., & González‐Gómez, M. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.08.059 · Cited by 37 · see citing works
Species-Specific miRNAs in Human Brain Development and Disease
Prodromidou, K., & Matsas, R. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00559 · Cited by 37 · see citing works
The impact of (ab)normal maternal environment on cortical development
Vasistha, N. A., & Khodosevich, K. (2021) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2021.102054 · Cited by 36 · see citing works
Priddle, T. H., & Crow, T. J. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs181 · Cited by 35 · see citing works
Urzainqui, I. Q., Rodríguez‐Moldes, I., & Candal, E. (2012) · Brain Structure and Function · doi:10.1007/s00429-012-0486-2 · Cited by 34 · see citing works
A neural stem cell paradigm of pediatric hydrocephalus
Duy, P. Q., RAKIC, P. T., Alper, S. L., Robert, S. M., Kundishora, A. J., Butler, W. E., Walsh, C. A., Šestan, N., Geschwind, D. H., Jin, S. C., et al. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac341 · Cited by 32 · see citing works
Larsen, K. B., Lutterodt, M. C., Laursen, H. B., Græm, N., Pakkenberg, B., Møllgård, K., & Møller, M. (2010) · Developmental Neuroscience · doi:10.1159/000297602 · Cited by 33 · see citing works
Metabolic mechanisms of species-specific developmental tempo
Iwata, R., & Vanderhaeghen, P. (2024) · Developmental Cell · doi:10.1016/j.devcel.2024.05.027 · Cited by 32 · see citing works
The Initial Appearance of the Cranial Nerves and Related Neuronal Migration in Staged Human Embryos
Müller, F., & O’Rahilly, R. (2010) · Cells Tissues Organs · doi:10.1159/000320026 · Cited by 32 · see citing works
Pasquet, N., Douceau, S., Naveau, M., Lesept, F., Louessard, M., Lebouvier, L., Hommet, Y., Vivien, D., & Bardou, I. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy119 · Cited by 31 · see citing works
The Molecular and Genetic Mechanisms of Neocortex Development
Diaz, A. L., & Gleeson, J. G. (2009) · Clinics in Perinatology · doi:10.1016/j.clp.2009.06.008 · Cited by 32 · see citing works
Yoshinaga, S., Shin, M., Kitazawa, A., Ishii, K., Tanuma, M., Kasai, A., Hashimoto, H., Kubo, K., & Nakajima, K. (2021) · iScience · doi:10.1016/j.isci.2021.102277 · Cited by 27 · see citing works
Connectome development and a novel extension to the neurodevelopmental model of schizophrenia
Collin, G., & Keshavan, M. S. (2018) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2018.20.2/gcollin · Cited by 29 · see citing works
Tomasello, U., Klingler, E., Niquille, M., Mule, N., Santinha, A. J., de Vevey, L., Prados, J., Platt, R. J., Borrell, V., Jabaudon, D., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2022.110381 · Cited by 28 · see citing works
Tripathi, A., Khurshid, N., Kumar, P., & Iyengar, S. (2008) · Neuroscience Research · doi:10.1016/j.neures.2008.03.002 · Cited by 29 · see citing works
Breunig, J. J., Gate, D., Levy, R., Rodríguez, J., Kim, G. B., Danielpour, M., Svendsen, C. N., & Town, T. (2012) · Neural Development · doi:10.1186/1749-8104-7-26 · Cited by 29 · see citing works
Impact of maternal immune activation on dendritic spine development
Pękała, M., Doliwa, M., & Kalita, K. B. (2020) · Developmental Neurobiology · doi:10.1002/dneu.22804 · Cited by 26 · see citing works
Fetal Development of the Central Nervous System
Ashwell, K. W. S., & Mai, J. K. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-374236-0.10003-3 · Cited by 27 · see citing works
Korzhevsky, D. E., Karpenko, M. N., & Kirik, O. V. (2012) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-012-9556-4 · Cited by 27 · see citing works
Essen, D. C. V. (2022) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2022.06.007 · Cited by 26 · see citing works
Organization of the human fetal subpallium
Pauly, M.-C., Döbrössy, M. D., Nikkhah, G., Winkler, C., & Piroth, T. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2013.00054 · Cited by 26 · see citing works
Facultad de Ciencias Biológicas
Hontana, A. S. (2007) · Dialnet (Universidad de la Rioja) · Cited by 24 · see citing works
Heterogeneous growth of the insula shapes the human brain
Mallela, A. N., Deng, H., Gholipour, A., Warfield, S. K., & Goldschmidt, E. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2220200120 · Cited by 24 · see citing works
Ayachi, I. E., Fernandez, C., Baeza, N., de Paula, A. M., Pesheva, P., & Figarella-Branger, D. F. (2011) · The Journal of Comparative Neurology · doi:10.1002/cne.22632 · Cited by 22 · see citing works
Overview of the Development of the Human Brain and Spinal Cord
ten Donkelaar, H. J., Yamada, S., Shiota, K., & van der Vliet, T. (2014) · Springer eBooks · doi:10.1007/978-3-642-54687-7_1 · Cited by 22 · see citing works
Petanjek, Z., Banovac, I., Sedmak, D., & Hladnik, A. (2023) · Advances in neurobiology · doi:10.1007/978-3-031-36159-3_4 · Cited by 23 · see citing works
Espinosa, A. (2009) · Frontiers in Neuroanatomy · doi:10.3389/neuro.05.027.2009 · Cited by 19 · see citing works
Enduring Neuroprotective Effect of Subacute Neural Stem Cell Transplantation After Penetrating TBI
Kassi, A., Mahavadi, A. K., Clavijo, A., Caliz, D., Lee, S. W., Ahmed, A. I., Yokobori, S., Hu, Z., Spurlock, M. S., Wasserman, J. M., et al. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2018.01097 · Cited by 20 · see citing works
Layer I as a putative neurogenic niche in young adult guinea pig cerebrum
Xiong, K., Cai, Y., Zhang, X., Huang, J.-F., Liu, Z.-Y., Fu, G.-M., Feng, J., Clough, R. W., Patrylo, P. R., Luo, X., et al. (2010) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2010.06.009 · Cited by 19 · see citing works
Fate and manipulations of endogenous neural stem cells following brain ischemia
Leker, R. R. (2009) · Expert Opinion on Biological Therapy · doi:10.1517/14712590903130558 · Cited by 17 · see citing works
Eze, U. C., Bhaduri, A., Haeussler, M., Nowakowski, T. J., & Kriegstein, A. R. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.03.06.981423 · Cited by 17 · see citing works
Temporal differences of neurodevelopment processes between species
Iwata, R. (2021) · Neuroscience Research · doi:10.1016/j.neures.2021.08.004 · Cited by 16 · see citing works
Akiyama, S., Madan, N., Graham, G., Samura, O., Kitano, R., Yun, H. J., Craig, A. K., Nakamura, T., Hozawa, A., Grant, P. E., et al. (2022) · PLoS ONE · doi:10.1371/journal.pone.0263535 · Cited by 16 · see citing works
- Authors
- Bystron, I., Rakic, P., Molnár, Z., & Blakemore, C.
- Affiliations
- University of Oxford (GB)
- Yale University (US)
- Corresponding author
- Bystron, Irina
- Venue
- Nature Neuroscience
- Published
- 2006-06-18
- Volume
- 9
- Issue
- 7
- Pages
- 880-886
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W1969413827
- Cited by
- 183
- References
- 44
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 7 · 2023: 11 · 2022: 11 · 2021: 8 · 2020: 5 · 2019: 11 · 2018: 8 · 2017: 6 · 2016: 9 · 2015: 7 · 2014: 11 · 2013: 7 · 2012: 9
- FWCI
- 3.39
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Yale University
- Russian Foundation for Basic Research
- Medical Research Council
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Fetal and Pediatric Neurological Disorders
- Keywords
- cortical development, tangential migration, subpallium, transcription factors, mitosis, neurogenesis, neural tube closure
- MeSH terms
- Cell Differentiation, Cell Movement, Cerebral Cortex, Fetus, Humans, Immunohistochemistry, Nerve Tissue Proteins, Neurons, Stem Cells, Transcription Factors, Gene Expression, Body Patterning
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review