Conserved rules in embryonic development of cortical interneurons
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This review will focus on early aspects of cortical interneurons (cIN) development from specification to migration and final positioning in the human cerebral cortex. These mechanisms have been largely studied in the mouse model, which provides unique possibilities of genetic analysis, essential to dissect the molecular and cellular events involved in cortical development. An important goal here is to discuss the conservation and the potential divergence of these mechanisms, with a particular interest for the situation in the human embryo. We will thus cover recent works, but also revisit older studies in the light of recent data to better understand the developmental mechanisms underlying cIN differentiation in human. Because cIN are implicated in severe developmental disorders, understanding the molecular and cellular mechanisms controlling their differentiation might clarify some causes and potential therapeutic approaches to these important clinical conditions.
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Distinct basal ganglia existed in the last common ancestor of vertebrates over 500 million years ago.
“distinct basal ganglia were already present in the last common ancestor of vertebrates more than 500 million years ago3”
From Innovations present in the primate interneuron repertoire (2020) · cites this paper as [3]
The basal ganglia nuclei are thought to be deeply conserved, with lamprey retaining homologous nuclei, circuitry and basic cell types to mice.
“the subcortical nuclei comprising the basal ganglia are thought to be deeply conserved–so much so that the lamprey, which shares a last common ancestor with mammals more than 500 million years ago, retains nuclei, circuitry and basic cell types that are homologous to those in mice3.”
From Innovations present in the primate interneuron repertoire (2020) · cites this paper as [3]
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Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq
Zeisel, A., Muñoz-Manchado, A. B., Codeluppi, S., Lönnerberg, P., La Manno, G., Juréus, A., Marques, S., Munguba, H., He, L., Betsholtz, C., et al. (2015) · Science · doi:10.1126/science.aaa1934 · Cited by 3,124 · see citing works
Interneurons of the neocortical inhibitory system
Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., & Wu, C. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1519 · Cited by 2,954 · see citing works
Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances
Volpe, J. J. (2008) · The Lancet Neurology · doi:10.1016/s1474-4422(08)70294-1 · Cited by 2,420 · see citing works
Long-Distance Neuronal Migration in the Adult Mammalian Brain
Lois, C., & Álvarez-Buylla, A. (1994) · Science · doi:10.1126/science.8178174 · Cited by 2,331 · see citing works
GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits
Tremblay, R., Lee, S., & Rudy, B. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.033 · Cited by 2,033 · see citing works
Adult mouse cortical cell taxonomy revealed by single cell transcriptomics
Tasic, B., Menon, V., Nguyen, T. N., Kim, T. K., Jarsky, T., Yao, Z., Levi, B., Gray, L. T., Sorensen, S. A., Dolbeare, T., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4216 · Cited by 1,714 · see citing works
Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex
The Petilla Interneuron Nomenclature Group (PING) (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2402 · Cited by 1,491 · 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
Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons
Rudy, B., Fishell, G., Lee, S., & Hjerling‐Leffler, J. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20853 · Cited by 1,420 · see citing works
Kessaris, N., Fogarty, M., Iannarelli, P., Grist, M., Wegner, M., & Richardson, W. D. (2006) · Nature Neuroscience · doi:10.1038/nn1620 · Cited by 1,195 · see citing works
Cortical parvalbumin interneurons and cognitive dysfunction in schizophrenia
Lewis, D. A., Curley, A. A., Glausier, J. R., & Volk, D. W. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2011.10.004 · Cited by 1,071 · see citing works
A long, remarkable journey: Tangential migration in the telencephalon
Marín, Ó., & Rubenstein, J. L. R. (2001) · Nature reviews. Neuroscience · doi:10.1038/35097509 · Cited by 1,050 · see citing works
Excitatory/Inhibitory Balance and Circuit Homeostasis in Autism Spectrum Disorders
Nelson, S. B., & Valakh, V. (2015) · Neuron · doi:10.1016/j.neuron.2015.07.033 · Cited by 1,001 · see citing works
The origin and specification of cortical interneurons
Wonders, C. P., & Anderson, S. A. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1954 · Cited by 980 · 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
Sussel, L., Marin, O., Kimura, S., & Rubenstein, J. L. R. (1999) · Development · doi:10.1242/dev.126.15.3359 · Cited by 873 · see citing works
Corridors of migrating neurons in the human brain and their decline during infancy
Sanai, N., Nguyen, T., Ihrie, R. A., Mirzadeh, Z., Tsai, H.-H., Wong, M., Gupta, N., Berger, M. S., Huang, E., Garcia-Verdugo, J.-M., et al. (2011) · Nature · doi:10.1038/nature10487 · Cited by 849 · see citing works
New insights into the classification and nomenclature of cortical GABAergic interneurons
DeFelipe, J., López-Cruz, P. L., Benavides-Piccione, R., Bielza, C., Larrañaga, P., Anderson, S., Burkhalter, A., Cauli, B., Fairén, A., Feldmeyer, D., et al. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3444 · Cited by 833 · see citing works
Puelles, L., & Rubenstein, J. L. R. (1993) · Trends in Neurosciences · doi:10.1016/0166-2236(93)90080-6 · Cited by 784 · 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
Wichterle, H., Turnbull, D. H., Nery, S., Fishell, G., & Alvarez-Buylla, A. (2001) · Development · doi:10.1242/dev.128.19.3759 · Cited by 722 · 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
Smart, I. H. M. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.1.37 · Cited by 687 · see citing works
Modes of neuronal migration in the developing cerebral cortex
Nadarajah, B., & Parnavelas, J. G. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn845 · Cited by 683 · see citing works
Balancing Plasticity/Stability Across Brain Development
Takesian, A. E., & Hensch, T. K. (2013) · Progress in Brain Research · doi:10.1016/b978-0-444-63327-9.00001-1 · Cited by 667 · 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
Patterns of neuronal migration in the embryonic cortex
Kriegstein, A. R., & Noctor, S. C. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.05.001 · Cited by 648 · see citing works
Mash1regulates neurogenesis in the ventral telencephalon
Casarosa, S., Schuurmans, C. J., & Guillemot, F. (1999) · Development · doi:10.1242/dev.126.3.525 · Cited by 639 · see citing works
Origins of Cortical Interneuron Subtypes
Xu, Q., Cobos, I., De La Cruz, E., Rubenstein, J. L., & Anderson, S. A. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.5667-03.2004 · Cited by 639 · see citing works
Fode, C., Ma, Q., Casarosa, S., Ang, S.-L., Anderson, D. J., & Guillemot, F. (2000) · Genes & Development · doi:10.1101/gad.14.1.67 · Cited by 624 · see citing works
Lee, S., Hjerling-Leffler, J., Zagha, E., Fishell, G., & Rudy, B. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1869-10.2010 · Cited by 600 · see citing works
The temporal and spatial origins of cortical interneurons predict their physiological subtype
Butt, S. J. B., Fuccillo, M., Nery, S., Noctor, S., Kriegstein, A., Corbin, J. G., & Fishell, G. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.034 · Cited by 587 · see citing works
McBain, C. J., & Fisahn, A. (2001) · Nature Reviews Neuroscience · doi:10.1038/35049047 · Cited by 581 · see citing works
Fate mapping Nkx2.1‐lineage cells in the mouse telencephalon
Xu, Q., Tam, M., & Anderson, S. A. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21529 · Cited by 560 · see citing works
Flames, N., Pla, R., Gelman, D. M., Rubenstein, J. L. R., Puelles, L., & Marín, O. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2750-07.2007 · Cited by 560 · see citing works
Miyoshi, G., Hjerling-Leffler, J., Karayannis, T., Sousa, V. H., Butt, S. J. B., Battiste, J., Johnson, J. E., Machold, R. P., & Fishell, G. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4515-09.2010 · Cited by 559 · see citing works
The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations
Nery, S., Fishell, G., & Corbin, J. G. (2002) · Nature Neuroscience · doi:10.1038/nn971 · Cited by 558 · see citing works
The Evolution of the Brain, the Human Nature of Cortical Circuits, and Intellectual Creativity
DeFelipe, J. (2011) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2011.00029 · Cited by 527 · see citing works
Young neurons from medial ganglionic eminence disperse in adult and embryonic brain
Wichterle, H., Garcia-Verdugo, J. M., Herrera, D. G., & Alvarez-Buylla, A. (1999) · Nature Neuroscience · doi:10.1038/8131 · Cited by 506 · see citing works
GABAergic interneuron origin of schizophrenia pathophysiology
Nakazawa, K., Zsiros, V., Jiang, Z., Nakao, K., Kolata, S., Zhang, S., & Belforte, J. E. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.01.022 · Cited by 498 · 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
Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon
Yun, K., Potter, S., & Rubenstein, J. L. R. (2001) · Development · doi:10.1242/dev.128.2.193 · Cited by 449 · see citing works
Direct Evidence for Homotypic, Glia-Independent Neuronal Migration
Wichterle, H., García‐Verdugo, J. M., & Álvarez-Buylla, A. (1997) · Neuron · doi:10.1016/s0896-6273(00)80317-7 · Cited by 416 · see citing works
Fogarty, M., Grist, M., Gelman, D., Marín, O., Pachnis, V., & Kessaris, N. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1629-07.2007 · Cited by 412 · see citing works
Dynamics of Cell Migration from the Lateral Ganglionic Eminence in the Rat
Carlos, J., López‐Mascaraque, L., & Valverde, F. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-19-06146.1996 · Cited by 403 · see citing works
Miyoshi, G., Butt, S. J. B., Takebayashi, H., & Fishell, G. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1807-07.2007 · Cited by 400 · see citing works
Origin and Route of Tangentially Migrating Neurons in the Developing Neocortical Intermediate Zone
Tamamaki, N., Fujimori, K. E., & Takauji, R. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-21-08313.1997 · Cited by 394 · see citing works
The origin and migration of cortical neurones: new vistas
Parnavelas, J. G. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01553-8 · Cited by 393 · see citing works
Extensive migration of young neurons into the infant human frontal lobe
Paredes, M. F., James, D., Gil-Perotin, S., Kim, H., Cotter, J. A., Ng, C., Sandoval, K., Rowitch, D. H., Xu, D., McQuillen, P. S., et al. (2016) · Science · doi:10.1126/science.aaf7073 · Cited by 391 · see citing works
Genetic control of dorsal-ventral identity in the telencephalon: opposing roles for Pax6 and Gsh2
Toresson, H., Potter, S. S., & Campbell, K. (2000) · Development · doi:10.1242/dev.127.20.4361 · Cited by 387 · see citing works
The genetics of early telencephalon patterning: some assembly required
Hébert, J. M., & Fishell, G. (2008) · Nature reviews. Neuroscience · doi:10.1038/nrn2463 · Cited by 377 · see citing works
Liodis, P., Denaxa, M., Grigoriou, M., Akufo-Addo, C., Yanagawa, Y., & Pachnis, V. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3055-06.2007 · Cited by 377 · see citing works
Petryniak, M. A., Potter, G. B., Rowitch, D. H., & Rubenstein, J. L. R. (2007) · Neuron · doi:10.1016/j.neuron.2007.06.036 · Cited by 371 · see citing works
Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling
Polleux, F., Whitford, K. L., Dijkhuizen, P. A., Vitalis, T., & Ghosh, A. (2002) · Development · doi:10.1242/dev.129.13.3147 · Cited by 361 · see citing works
Molecular mechanisms underlying cell fate specification in the developing telencephalon
Schuurmans, C. J., & Guillemot, F. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00286-6 · Cited by 339 · see citing works
The requirement of Nkx2-1 in the temporal specification of cortical interneuron subtypes
Butt, S. J. B., Sousa, V. H., Fuccillo, M. V., Hjerling-Leffler, J., Miyoshi, G., Kimura, S., & Fishell, G. (2008) · Neuron · doi:10.1016/j.neuron.2008.07.031 · Cited by 330 · see citing works
Non-epithelial stem cells and cortical interneuron production in the human ganglionic eminences
Hansen, D. V., Lui, J. H., Flandin, P., Yoshikawa, K., Rubenstein, J. L., Alvarez-Buylla, A., & Kriegstein, A. R. (2013) · Nature Neuroscience · doi:10.1038/nn.3541 · Cited by 328 · see citing works
Anderson, S. A. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.6.646 · Cited by 325 · see citing works
Subcortical origins of human and monkey neocortical interneurons
Ma, T., Wang, C., Wang, L., Zhou, X., Tian, M., Zhang, Q., Zhang, Y., Li, J., Liu, Z., Cai, Y., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3536 · Cited by 322 · see citing works
Wang, C., Liu, F., Liu, Y.-Y., Zhao, C.-H., You, Y., Wang, L., Zhang, J., Wei, B. K., Ma, T., Zhang, Q., et al. (2011) · Cell Research · doi:10.1038/cr.2011.83 · Cited by 309 · see citing works
Grigoriou, M. E., Tucker, A. S., Sharpe, P. T., & Pachnis, V. (1998) · Development · doi:10.1242/dev.125.11.2063 · Cited by 307 · see citing works
Genetic and activity-dependent mechanisms underlying interneuron diversity
Wamsley, B., & Fishell, G. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.30 · Cited by 290 · 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
The embryonic preoptic area is a novel source of cortical GABAergic interneurons
Gelman, D. M., Martini, F. J., Nóbrega-Pereira, S., Pierani, A., Kessaris, N., & Marín, O. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.0604-09.2009 · Cited by 280 · see citing works
Contributions of cortical subventricular zone to the development of the human cerebral cortex
Zecevic, N., Chen, Y., & Filipovic, R. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20714 · Cited by 269 · see citing works
Inta, D., Alfonso, J., von Engelhardt, J., Kreuzberg, M. M., Meyer, A. H., van Hooft, J. A., & Monyer, H. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807059105 · Cited by 267 · see citing works
Comparative aspects of cerebral cortical development
Molnár, Z., Métin, C., Stoykova, A., Tarabykin, V. S., Price, D. J., Francis, F., Meyer, G., Dehay, C., & Kennedy, H. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04611.x · Cited by 266 · see citing works
Self-citationEctopic expression of the Dlx genes induces glutamic acid decarboxylase and Dlx expression
Stühmer, T., Anderson, S. A., Ekker, M., & Rubenstein, J. L. R. (2002) · Development · doi:10.1242/dev.129.1.245 · Cited by 257 · see citing works
Nóbrega-Pereira, S., Kessaris, N., Du, T., Kimura, S., Anderson, S. A., & Marín, O. (2008) · Neuron · doi:10.1016/j.neuron.2008.07.024 · Cited by 256 · see citing works
Yun, K., Fischman, S., Johnson, J. E. B., de Angelis, M. H., Weinmaster, G., & Rubenstein, J. L. R. (2002) · Development · doi:10.1242/dev.129.21.5029 · Cited by 255 · see citing works
Waclaw, R. R., Allen, Z. J., Bell, S. M., Erdélyi, F., Szabó, G., Potter, S. S., & Campbell, K. (2006) · Neuron · doi:10.1016/j.neuron.2006.01.018 · Cited by 237 · see citing works
Prenatal development of GABA‐ergic neurons in the neocortex of the rat
van Eden, C. G., Mrzljak, L., Voorn, P., & Uylings, H. B. M. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902890204 · Cited by 236 · see citing works
Mechanisms of Inhibition within the Telencephalon: “Where the Wild Things Are”
Fishell, G., & Rudy, B. (2011) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-061010-113717 · Cited by 233 · 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
Chapter 3 The Developmental Integration of Cortical Interneurons into a Functional Network
Batista‐Brito, R., & Fishell, G. (2009) · Current Topics in Developmental Biology · doi:10.1016/s0070-2153(09)01203-4 · Cited by 223 · see citing works
NKX2.1 specifies cortical interneuron fate by activatingLhx6
Du, T., Xu, Q., Ocbina, P. J. R., & Anderson, S. A. (2008) · Development · doi:10.1242/dev.015123 · Cited by 220 · see citing works
Ventricle-directed migration in the developing cerebral cortex
Nadarajah, B., Alifragis, P., Wong, R., & Parnavelas, J. G. (2002) · Nature Neuroscience · doi:10.1038/nn813 · Cited by 219 · see citing works
Xu, Q., Guo, L., Moore, H., Waclaw, R. R., Campbell, K., & Anderson, S. A. (2010) · Neuron · doi:10.1016/j.neuron.2010.01.004 · Cited by 218 · 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
Self-citationFérézou, I., Cauli, B., Hill, E. L., Rossier, J., Hamel, E., & Lambolez, B. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-17-07389.2002 · Cited by 215 · 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
The Cell-Intrinsic Requirement of Sox6 for Cortical Interneuron Development
Batista-Brito, R., Rossignol, E., Hjerling-Leffler, J., Denaxa, M., Wegner, M., Lefebvre, V., Pachnis, V., & Fishell, G. (2009) · Neuron · doi:10.1016/j.neuron.2009.08.005 · Cited by 214 · see citing works
The Proneural Gene Mash1 Specifies an Early Population of Telencephalic Oligodendrocytes
Parras, C., Hunt, C., Sugimori, M., Nakafuku, M., Rowitch, D., & Guillemot, F. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0126-07.2007 · Cited by 211 · see citing works
Zhao, Y., Flandin, P., Long, J. E., Cuesta, M. D., Westphal, H., & Rubenstein, J. L. R. (2008) · Journal of Comparative Neurology · doi:10.1002/cne.21772 · Cited by 207 · see citing works
SOX6 controls dorsal progenitor identity and interneuron diversity during neocortical development
Azim, E., Jabaudon, D., Fame, R. M., & Macklis, J. D. (2009) · Nature Neuroscience · doi:10.1038/nn.2387 · Cited by 202 · see citing works
Puelles, L. (2001) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2001.0973 · Cited by 196 · see citing works
Horton, S. E., Meredith, A. L., Richardson, J. A., & Johnson, J. E. B. (1999) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.1999.0791 · Cited by 194 · see citing works
Integration of GABAergic interneurons into cortical cell assemblies: lessons from embryos and adults
Bartolini, G., Ciceri, G., & Marín, O. (2013) · Neuron · doi:10.1016/j.neuron.2013.08.014 · Cited by 185 · see citing works
Xu, Q., Wonders, C. P., & Anderson, S. A. (2005) · Development · doi:10.1242/dev.02090 · Cited by 184 · see citing works
A wide diversity of cortical GABAergic interneurons derives from the embryonic preoptic area
Gelman, D., Griveau, A., Dehorter, N., Teissier, A., Varela, C., Pla, R., Pierani, A., & Marín, O. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.4068-11.2011 · Cited by 179 · see citing works
Flandin, P., Kimura, S., & Rubenstein, J. L. R. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4228-09.2010 · Cited by 176 · see citing works
Layer Specification of Transplanted Interneurons in Developing Mouse Neocortex
Valcanis, H., & Tan, S.-S. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-12-05113.2003 · Cited by 175 · see citing works
Common Origins of Hippocampal Ivy and Nitric Oxide Synthase Expressing Neurogliaform Cells
Tricoire, L., Pelkey, K. A., Daw, M. I., Sousa, V. H., Miyoshi, G., Jeffries, B., Cauli, B., Fishell, G., & McBain, C. J. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5123-09.2010 · Cited by 171 · see citing works
Tanaka, D. H., Nakaya, Y., Yanagawa, Y., Obata, K., & Murakami, F. (2003) · Development · doi:10.1242/dev.00825 · Cited by 169 · see citing works
Kanatani, S., Yozu, M., Tabata, H., & Nakajima, K. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.2132-08.2008 · Cited by 163 · see citing works
Cobos, I., Puelles, L., & Martı́nez, S. (2001) · Developmental Biology · doi:10.1006/dbio.2001.0422 · Cited by 157 · see citing works
Long, J. E., Swan, C. H., Liang, W. S., Cobos, I., Potter, G. B., & Rubenstein, J. L. R. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21854 · Cited by 156 · see citing works
Yun, K., Garel, S., Fischman, S., & Rubenstein, J. L. R. (2003) · Journal of Comparative Neurology · doi:10.1002/cne.10685 · Cited by 156 · see citing works
Interneurons in the developing human neocortex
Zečević, N., Hu, F., & Jakovčevski, I. (2010) · Developmental Neurobiology · doi:10.1002/dneu.20812 · Cited by 153 · 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
GABA and glutamate in schizophrenia: A 7 T 1H-MRS study
Marsman, A., Mandl, R. C. W., Klomp, D. W. J., Bohlken, M. M., Boer, V. O., Андрейченко, А. Е., Cahn, W., Kahn, R. S., Luijten, P. R., & Pol, H. E. H. (2014) · NeuroImage Clinical · doi:10.1016/j.nicl.2014.10.005 · Cited by 151 · see citing works
Alifragis, P., Liapi, A., & Parnavelas, J. G. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1245-04.2004 · Cited by 143 · see citing works
Cobas, A., Fairén, A., Álvarez-Bolado, G., & ́nchez, M. P. S. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90127-a · Cited by 137 · see citing works
Development of GABA‐immunoreactivity in the neocortex of the mouse
del Rı́o, J. A., Soriano, E., & Ferrer, I. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903260403 · Cited by 136 · see citing works
Miyoshi, G., Young, A., Petros, T., Karayannis, T., McKenzie Chang, M., Lavado, A., Iwano, T., Nakajima, M., Taniguchi, H., Huang, Z. J., et al. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.1164-15.2015 · Cited by 135 · see citing works
Corbin, J. G., Rutlin, M. L., Gaiano, N., & Fishell, G. (2003) · Development · doi:10.1242/dev.00717 · Cited by 131 · see citing works
Modes and Mishaps of Neuronal Migration in the Mammalian Brain
Métin, C., Vallee, R. B., RAKIC, P. T., & Bhide, P. G. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3860-08.2008 · Cited by 131 · see citing works
Self-citationDlx-Dependent and -Independent Regulation of Olfactory Bulb Interneuron Differentiation
Long, J. E., Garel, S., Álvarez‐Dolado, M., Yoshikawa, K., Osumi, N., Álvarez-Buylla, A., & Rubenstein, J. L. R. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.5265-06.2007 · Cited by 131 · see citing works
Origins of Cortical GABAergic Neurons in the Cynomolgus Monkey
Petanjek, Z., Berger, B., & Esclapez, M. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn078 · Cited by 130 · see citing works
Lhx6 directly regulates Arx and CXCR7 to determine cortical interneuron fate and laminar position
Vogt, D., Hunt, R. F., Mandal, S., Sandberg, M., Silberberg, S. N., Nagasawa, T., Yang, Z., Baraban, S. C., & Rubenstein, J. L. R. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.030 · Cited by 129 · see citing works
Stenman, J. M., Yu, R. T., Evans, R. M., & Campbell, K. (2003) · Development · doi:10.1242/dev.00328 · Cited by 129 · see citing works
Bakhshi, K., & Chance, S. A. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.06.028 · Cited by 128 · see citing works
Tanaka, D. H., Maekawa, K., Yanagawa, Y., Obata, K., & Murakami, F. (2006) · Development · doi:10.1242/dev.02382 · Cited by 128 · see citing works
Jakovcevski, I., Mayer, N., & Zecevic, N. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq245 · Cited by 124 · see citing works
Potter, G. B., Petryniak, M. A., Shevchenko, E., McKinsey, G. L., Ekker, M., & Rubenstein, J. L. R. (2008) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2008.10.003 · Cited by 122 · 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
de Diego, I., Smith‐Fernández, A., & Fairén, A. (1994) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1994.tb00593.x · Cited by 117 · see citing works
The COUP-TF nuclear receptors regulate cell migration in the mammalian basal forebrain
Tripodi, M., Filosa, A., Armentano, M., & Studer, M. (2004) · Development · doi:10.1242/dev.01530 · Cited by 117 · see citing works
Lodato, S., Tomassy, G. S., De Leonibus, E., Uzcategui, Y. G., Andolfi, G., Armentano, M., Touzot, A., Gaztelu, J. M., Arlotta, P., Menendez de la Prida, L., et al. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.6580-10.2011 · Cited by 112 · see citing works
Cerebral vascular regulation and brain injury in preterm infants
Brew, N., Walker, D. W., & Wong, F. Y. (2014) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00487.2013 · Cited by 111 · see citing works
Genetic interplay between the transcription factors Sp8 and Emx2 in the patterning of the forebrain
Zembrzycki, A., Griesel, G., Stoykova, A., & Mansouri, A. (2007) · Neural Development · doi:10.1186/1749-8104-2-8 · Cited by 108 · see citing works
Fertuzinhos, S., Krsnik, Ž., Kawasawa, Y. I., Rašin, M.-R., Kwan, K. Y., Chen, J.-G., Judaš, M., Hayashi, M., & Šestan, N. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp009 · Cited by 106 · see citing works
Localisation of amino acid neurotransmitters during postnatal development of the rat retina
Fletcher, E. L., & Kalloniatis, M. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970421)380:4 · Cited by 99 · see citing works
del R�o, M. R., & DeFelipe, J. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960603)369:3 · Cited by 97 · see citing works
The DLX1and DLX2 genes and susceptibility to autism spectrum disorders
Liu, X., Novosedlik, N., Wang, A., Hudson, M. L., Cohen, I. L., Chudley, A. E., Forster‐Gibson, C., Lewis, M. E. S., & Holden, J. J. A. (2008) · European Journal of Human Genetics · doi:10.1038/ejhg.2008.148 · Cited by 93 · see citing works
Development and evolution of the subpallium
Moreno, N., González, A., & Rétaux, S. (2009) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2009.04.007 · Cited by 87 · see citing works
Rubin, A. N., Alfonsi, F., Humphreys, M. P., Choi, C. K. P., Rocha, S. F., & Kessaris, N. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.6178-09.2010 · Cited by 87 · see citing works
Conserved pattern of tangential neuronal migration during forebrain development
Métin, C., Alvarez, C., Moudoux, D., Vitalis, T., Pieau, C., & Molnár, Z. (2007) · Development · doi:10.1242/dev.02869 · Cited by 86 · see citing works
Self-citationVaccarino, F. M., Grigorenko, E. L., Smith, K. M., & Stevens, H. E. (2008) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-008-0653-8 · Cited by 84 · see citing works
Serotonin receptor 3A controls interneuron migration into the neocortex
Murthy, S. S., Niquille, M., Hurni, N., Limoni, G., Frazer, S. L., Chameau, P. J. P., van Hooft, J. A., Vitalis, T., & Dayer, A. G. (2014) · Nature Communications · doi:10.1038/ncomms6524 · Cited by 81 · see citing works
Yu, X., & Zečević, N. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5249-10.2011 · Cited by 79 · see citing works
Ma, T., Zhang, Q., Cai, Y., You, Y., Rubenstein, J. L. R., & Yang, Z. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhr296 · Cited by 79 · see citing works
Temporal sequence of neurotransmitter expression by developing neurons of fetal monkey visual cortex
Huntley, G. W., Hendry, S. H. C., Killackey, H. P., Chalupa, L. M., & Jones, E. G. (1988) · Developmental Brain Research · doi:10.1016/0165-3806(88)90154-x · Cited by 78 · see citing works
Duff, B. J., Macritchie, K., Moorhead, T. W. J., Lawrie, S. M., & Blackwood, D. (2013) · Schizophrenia Research · doi:10.1016/j.schres.2013.03.015 · Cited by 78 · see citing works
Diversity of Cortical Interneurons in Primates: The Role of the Dorsal Proliferative Niche
Radonjić, N. V., Ayoub, A. E., Memi, F., Yu, X., Maroof, A., Jakovcevski, I., Anderson, S. A., Rakic, P., & Zecevic, N. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.11.026 · Cited by 74 · see citing works
Uchida, T., Furukawa, T., Iwata, S., Yanagawa, Y., & Fukuda, A. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.13 · Cited by 73 · see citing works
Wilson, M. T., & Snow, D. M. (2000) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20000828)424:3 · Cited by 72 · see citing works
Rubin, A. N., & Kessaris, N. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077339 · Cited by 69 · see citing works
Reconstructing the ancestral vertebrate brain
Sugahara, F., Murakami, Y., Pascual‐Anaya, J., & Kuratani, S. (2017) · Development Growth & Differentiation · doi:10.1111/dgd.12347 · Cited by 68 · see citing works
Moreno, N., González, A., & Rétaux, S. (2008) · Developmental Neurobiology · doi:10.1002/dneu.20603 · Cited by 67 · see citing works
Meyer, G. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.12.1225 · Cited by 65 · see citing works
Puzzolo, E., & Mallamaci, A. (2010) · Neural Development · doi:10.1186/1749-8104-5-8 · Cited by 61 · see citing works
Early Expression of GABA-containing Neurons in the Prefrontal and Visual Cortices of Rhesus Monkeys
Schwartz, M. L., & Meinecke, D. L. (1992) · Cerebral Cortex · doi:10.1093/cercor/2.1.16 · Cited by 55 · see citing works
Cai, Y., Zhang, Q., Wang, C., Zhang, Y., Ma, T., Zhou, X., Tian, M., Rubenstein, J. L. R., & Yang, Z. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23186 · Cited by 53 · see citing works
Alzu’bi, A., Lindsay, S., Kerwin, J. M., Looi, S. J., Khalil, F., & Clowry, G. J. (2016) · Brain Structure and Function · doi:10.1007/s00429-016-1343-5 · Cited by 52 · see citing works
Carrera, I., Ferreiro‐Galve, S., Sueiro, C., Anadón, R., & Rodríguez‐Moldes, I. (2007) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2007.10.013 · Cited by 51 · see citing works
Close, J., Yao, Z., Levi, B. P., Miller, J. A., Bakken, T. E., Menon, V., Ting, J. T., Wall, A., Krostag, A.-R., Thomsen, E. R., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.02.014 · Cited by 51 · see citing works
Prenatal development of GABA-immunoreactive neurons in the human striate cortex
Yan, X., Zheng, D.-S., & Garey, L. J. (1992) · Developmental Brain Research · doi:10.1016/0165-3806(92)90179-z · Cited by 50 · see citing works
Migratory pathways of GABAergic interneurons when they enter the neocortex
Tanaka, D. H., & Nakajima, K. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08111.x · Cited by 49 · see citing works
MacDonald, R. B., Debiais‐Thibaud, M., Talbot, J. C., & Ekker, M. (2010) · Developmental Dynamics · doi:10.1002/dvdy.22365 · Cited by 48 · see citing works
Tyson, J. A., Goldberg, E. M., Maroof, A. M., Xu, Q., Petros, T. J., & Anderson, S. A. (2015) · Development · doi:10.1242/dev.111526 · Cited by 46 · see citing works
Dlx2 Progenitor Migration in Wild Type and Nkx2.1 Mutant Telencephalon
Nery, S. V. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.9.895 · Cited by 46 · see citing works
Willi-Monnerat, S., Migliavacca, E., Surdez, D., Delorenzi, M., Luthi‐Carter, R., & Terskikh, A. V. (2008) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2008.01.009 · Cited by 45 · see citing works
New Pool of Cortical Interneuron Precursors in the Early Postnatal Dorsal White Matter
Riccio, O., Murthy, S. S., Szabó, G., Vutskits, L., Kiss, J. Z., Vitalis, T., Lebrand, C., & Dayer, A. G. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr086 · Cited by 45 · see citing works
COUP-TFII Expressing Interneurons in Human Fetal Forebrain
Reinchisi, G., Ijichi, K., Glidden, N. C., Jakovčevski, I., & Zečević, N. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr359 · Cited by 43 · see citing works
Tangential migration of cells from the basal to the dorsal telencephalic regions in the chick
Tuorto, F., Alifragis, P., Failla, V., Parnavelas, J. G., & Gulisano, M. (2003) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2003.03059.x · Cited by 36 · see citing works
Chapter 6 The origin and migration of cortical neurons
Parnavelas, J. G., Alifragis, P., & Nadarajah, B. (2002) · Progress in brain research · doi:10.1016/s0079-6123(02)36008-4 · Cited by 35 · see citing works
Clowry, G. J. (2014) · Journal of Anatomy · doi:10.1111/joa.12198 · Cited by 34 · see citing works
Varga, C., Tamás, G., Barzó, P., Oláh, S., & Somogyi, P. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv045 · Cited by 34 · see citing works
Larimer, P., Spatazza, J., Espinosa, J. S., Tang, Y., Kaneko, M., Hasenstaub, A. R., Stryker, M. P., & Álvarez-Buylla, A. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.06.071 · Cited by 34 · see citing works
The Role of Sonic Hedgehog in the Specification of Human Cortical Progenitors In Vitro
Radonjić, N. V., Memi, F., Ortega, J. A., Glidden, N. C., Zhan, H., & Zečević, N. (2014) · Cerebral Cortex · doi:10.1093/cercor/bhu183 · Cited by 28 · see citing works
Sugahara, F., Murakami, Y., Adachi, N., & Kuratani, S. (2013) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2013.02.008 · Cited by 28 · see citing works
Prenatal development of calbindin D-28K in human visual cortex
Yan, X. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.1.57 · Cited by 25 · see citing works
Cai, Y., Zhang, Y., Shen, Q., Rubenstein, J. L. R., & Yang, Z. (2013) · Stem Cells · doi:10.1002/stem.1363 · Cited by 24 · see citing works
Best-laid schemes for interneuron origin of mice and men
Molnár, Z., & Butt, S. J. B. (2013) · Nature Neuroscience · doi:10.1038/nn.3557 · Cited by 17 · see citing works
Immunocytochemical localization of growth-associated protein GAP-43 in early human development
Milosevic, A., Kanazir, S., & Zečević, N. (1995) · Developmental Brain Research · doi:10.1016/0165-3806(94)00187-5 · Cited by 15 · see citing works
Fate determination of cerebral cortical GABAergic interneurons and their derivation from stem cells
DeBoer, E., & Anderson, S. A. (2015) · Brain Research · doi:10.1016/j.brainres.2015.12.031 · Cited by 13 · see citing works
Salaj, M., Druga, R., Cerman, J., Kubová, H., & Barinka, F. (2015) · Brain Research · doi:10.1016/j.brainres.2015.09.031 · Cited by 11 · see citing works
Broca's region revisited: Cytoarchitecture and intersubject variability
Amunts, K., Schleicher, A., B�rgel, U., Mohlberg, H., Uylings, H. B. M., & Zilles, K. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990920)412:2
Salin (1998) · doi:10.1002/(sici)1096-9861(19980720)397:1
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Innovations present in the primate interneuron repertoire
Krienen, F. M., Goldman, M., Zhang, Q., C. H. del Rosario, R., Florio, M., Machold, R., Saunders, A., Levandowski, K., Zaniewski, H., Schuman, B., et al. (2020) · Nature · doi:10.1038/s41586-020-2781-z · Cited by 381 · see citing works
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Krienen, F. M., Goldman, M., Zhang, Q., del Rosario, R., Florio, M., Machold, R., Saunders, A., Levandowski, K., Zaniewski, H., Schuman, B., et al. (2019) · doi:10.1101/709501 · Cited by 372 · see citing works
Franjic, D., Skarica, M., Ma, S., Arellano, J. I., Tebbenkamp, A. T. N., Choi, J., Xu, C., Li, Q., Morozov, Y. M., Andrijevic, D., et al. (2022) · Neuron · doi:10.1016/j.neuron.2021.10.036 · Cited by 308 · see citing works
Cellular and Molecular Mechanisms Linking Human Cortical Development and Evolution
Libé-Philippot, B., & Vanderhaeghen, P. (2021) · Annual Review of Genetics · doi:10.1146/annurev-genet-071719-020705 · Cited by 78 · see citing works
de Lombares, C., Heude, E., Alfama, G., Fontaine, A., Hassouna, R., Vernochet, C., de Chaumont, F., Olivo-Marin, C., Ey, E., Parnaudeau, S., et al. (2019) · Aging · doi:10.18632/aging.102141 · Cited by 52 · see citing works
- Authors
- Laclef, C., & Métin, C.
- Affiliations
- Inserm (FR)
- Corresponding author
- Métin, Christine
- ORCID
- Métin, Christine
- Venue
- Seminars in Cell & Developmental Biology
- Publisher
- Elsevier BV
- Published
- 2018-04
- Volume
- 76
- Pages
- 86-100
- ISSN
- 1084-9521 (ISSN-L)
- OpenAlex
- W2755139995
- Cited by
- 57
- References
- 171
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 8 · 2023: 6 · 2022: 9 · 2021: 6 · 2020: 6 · 2019: 6 · 2018: 9
- FWCI
- 0.87
- Type
- journal article
- Language
- en
- Open access
- Licence
- Locations
- Seminars in Cell and Developmental Biology (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- Funders
- Agence Nationale de la Recherche (ANR-14-CE13-0018)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Keywords
- cortical interneurons, embryonic development, interneuron specification, neuronal migration, human cerebral cortex, developmental disorders, interneuron differentiation
- MeSH terms
- Cell Differentiation, Cerebral Cortex, Humans, Interneurons
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