Prox1 Regulates the Subtype-Specific Development of Caudal Ganglionic Eminence-Derived GABAergic Cortical Interneurons
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Neurogliaform (RELN+) and bipolar (VIP+) GABAergic interneurons of the mammalian cerebral cortex provide critical inhibition locally within the superficial layers. While these subtypes are known to originate from the embryonic caudal ganglionic eminence (CGE), the specific genetic programs that direct their positioning, maturation, and integration into the cortical network have not been elucidated. Here, we report that in mice expression of the transcription factor Prox1 is selectively maintained in postmitotic CGE-derived cortical interneuron precursors and that loss of Prox1 impairs the integration of these cells into superficial layers. Moreover, Prox1 differentially regulates the postnatal maturation of each specific subtype originating from the CGE (RELN, Calb2/VIP, and VIP). Interestingly, Prox1 promotes the maturation of CGE-derived interneuron subtypes through intrinsic differentiation programs that operate in tandem with extrinsically driven neuronal activity-dependent pathways. Thus Prox1 represents the first identified transcription factor specifically required for the embryonic and postnatal acquisition of CGE-derived cortical interneuron properties. SIGNIFICANCE STATEMENT: Despite the recognition that 30% of GABAergic cortical interneurons originate from the caudal ganglionic eminence (CGE), to date, a specific transcriptional program that selectively regulates the development of these populations has not yet been identified. Moreover, while CGE-derived interneurons display unique patterns of tangential and radial migration and preferentially populate the superficial layers of the cortex, identification of a molecular program that controls these events is lacking.Here, we demonstrate that the homeodomain transcription factor Prox1 is expressed in postmitotic CGE-derived cortical interneuron precursors and is maintained into adulthood. We found that Prox1 function is differentially required during both embryonic and postnatal stages of development to direct the migration, differentiation, circuit integration, and maintenance programs within distinct subtypes of CGE-derived interneurons.
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For CGE, the Ntng1 HPF supertype does not express canonical pan-CGE marker Prox1 nor its subclass markers Vip, Sncg or Lamp5.
“For CGE, the Ntng1 HPF supertype does not express canonical pan-CGE marker Prox1 (Miyoshi et al., 2015; Rubin and Kessaris, 2013) nor its subclass markers Vip, Sncg or Lamp5”
From A taxonomy of transcriptomic cell types across the isocortex and hippocampal formation (2021) · cites this paper as Miyoshi et al., 2015
Prox1 is differentially required embryonically and postnatally for CGE-derived interneuron migration and differentiation/circuit integration, respectively.
“Loss-of-function studies indicate that Prox1 is differentially required embryonically and postnatally for CGE-derived interneuron migration and differentiation/circuit integration, respectively”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [797]
Prox1 is present in the SVZs of all GEs, but its expression is selectively maintained in CGE-derived and downregulated in MGE-derived interneuron precursors.
“while the homeodomain transcription factor Prox1 is present in the SVZs of all GEs, its expression is selectively maintained in CGE-derived, and downregulated in MGE-derived, interneuron precursors”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [797]
Transcription factors such as Gsx2, CoupTF1/2, and SP8 are enriched within the CGE and have been implicated in the generation, migration, specification, and maturation of CGE-derived interneurons.
“a number of transcription factors such as Gsx2, CoupTF1/2, and SP8 are enriched within the CGE and have been implicated in the generation, migration, specification, and maturation of CGE-derived interneurons”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [797]
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Shrestha, S., & Offer, S. M. (2016) · Medical Epigenetics · doi:10.1159/000444713 · Cited by 8,949 · see citing works
A robust and high-throughput Cre reporting and characterization system for the whole mouse brain
Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., Ng, L. L., Palmiter, R. D., Hawrylycz, M. J., Jones, A. R., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2467 · Cited by 6,907 · 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
Parvalbumin neurons and gamma rhythms enhance cortical circuit performance
Sohal, V. S., Zhang, F., Yizhar, O., & Deisseroth, K. (2009) · Nature · doi:10.1038/nature07991 · Cited by 2,606 · see citing works
A gene expression atlas of the central nervous system based on bacterial artificial chromosomes
Gong, S., Zheng, C., Doughty, M. L., Losos, K., Didkovsky, N., Schambra, U. B., Nowak, N. J., Joyner, A., Leblanc, G., Hatten, M. E., et al. (2003) · Nature · doi:10.1038/nature02033 · Cited by 2,108 · see citing works
Self-citationNeuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations
Klausberger, T., & Somogyi, P. (2008) · Science · doi:10.1126/science.1149381 · Cited by 2,050 · see citing works
A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex
Taniguchi, H., He, M., Wu, P., Kim, S., Paik, R., Sugino, K., Kvitsani, D., Fu, Y., Lu, J., Lin, Y., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.026 · Cited by 1,828 · see citing works
Self-citationHow Inhibition Shapes Cortical Activity
Isaacson, J. S., & Scanziani, M. (2011) · Neuron · doi:10.1016/j.neuron.2011.09.027 · Cited by 1,678 · see citing works
Neuronal subtype specification in the cerebral cortex
Molyneaux, B. J., Arlotta, P., Menezes, J. R. L., & Macklis, J. D. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2151 · Cited by 1,632 · see citing works
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
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
Development and Evolution of the Human Neocortex
Lui, J. H., Hansen, D. V., & Kriegstein, A. R. (2011) · Cell · doi:10.1016/j.cell.2011.06.030 · Cited by 1,342 · 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
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
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
Self-citationA cellular mechanism for cortical associations: an organizing principle for the cerebral cortex
Larkum, M. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2012.11.006 · Cited by 755 · 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
Self-citationThe Endocannabinoid System Controls Key Epileptogenic Circuits in the Hippocampus
Monory, K., Massa, F., Egertová, M., Eder, M., Blaudzun, H., Westenbroek, R., Kelsch, W., Jacob, W., Marsch, R., Ekker, M., et al. (2006) · Neuron · doi:10.1016/j.neuron.2006.07.006 · Cited by 706 · 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
Activity-dependent regulation of inhibitory synapse development by Npas4
Lin, Y., Bloodgood, B. L., Hauser, J. L., Lapan, A. D., Koon, A. C., Kim, T.-K., Hu, L. S., Malik, A. N., & Greenberg, M. E. (2008) · Nature · doi:10.1038/nature07319 · 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
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
Self-citationThe 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
Self-citationLymphatic vascular defects promoted by Prox1 haploinsufficiency cause adult-onset obesity
Harvey, N. L., Srinivasan, R. S., Dillard, M. E., Johnson, N. C., Witte, M. H., Boyd, K. L., Sleeman, M. W., & Oliver, G. C. (2005) · Nature Genetics · doi:10.1038/ng1642 · Cited by 580 · see citing works
Self-citationFate 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
Self-citationThe 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
Self-citationNeuronal Activity-Regulated Gene Transcription in Synapse Development and Cognitive Function
West, A. E., & Greenberg, M. E. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005744 · Cited by 532 · see citing works
Distinct behavioural and network correlates of two interneuron types in prefrontal cortex
Kvitsiani, D., Ranade, S., Hangya, B., Taniguchi, H., Huang, J. Z., & Kepecs, A. (2013) · Nature · doi:10.1038/nature12176 · Cited by 516 · see citing works
Self-citationMice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy
Cobos, I., Calcagnotto, M. E., Vilaythong, A. J., Thwin, M. T., Noebels, J. L., Baraban, S. C., & Rubenstein, J. L. R. (2005) · Nature Neuroscience · doi:10.1038/nn1499 · Cited by 502 · see citing works
Buzsáki, G., Kaila, K., & Raichle, M. E. (2007) · Neuron · doi:10.1016/j.neuron.2007.11.008 · Cited by 449 · see citing works
Functional maps of neocortical local circuitry.
Thomson, A. M. (2007) · Frontiers in Neuroscience · doi:10.3389/neuro.01.1.1.002.2007 · Cited by 434 · see citing works
GABAergic Interneurons Shape the Functional Maturation of the Cortex
Le Magueresse, C., & Monyer, H. (2013) · Neuron · doi:10.1016/j.neuron.2013.01.011 · Cited by 425 · see citing works
Neural stem cells: balancing self-renewal with differentiation
Doe, C. Q. (2008) · Development · doi:10.1242/dev.014977 · Cited by 420 · see citing works
Guiding Neuronal Cell Migrations
Marin, O., Valiente, M., Ge, X., & Tsai, L.-H. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a001834 · Cited by 417 · 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
Choksi, S. P., Southall, T. D., Bossing, T., Edoff, K., de Wit, E., Fischer, B., van Steensel, B., Micklem, G., & Brand, A. H. (2006) · Developmental Cell · doi:10.1016/j.devcel.2006.09.015 · Cited by 410 · see citing works
Dyer, M. A., Livesey, F. J., Cepko, C. L., & Oliver, G. C. (2003) · Nature Genetics · doi:10.1038/ng1144 · Cited by 406 · see citing works
Self-citationMiyoshi, 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
Self-citationTranscriptional co-regulation of neuronal migration and laminar identity in the neocortex
Kwan, K. Y., Šestan, N., & Anton, E. S. (2012) · Development · doi:10.1242/dev.069963 · Cited by 388 · see citing works
Bortone, D., & Polleux, F. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.034 · Cited by 387 · see citing works
The determination of projection neuron identity in the developing cerebral cortex
Leone, D. P., Srinivasan, K., Chen, B., Alcamo, E., & McConnell, S. K. (2008) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2008.05.006 · Cited by 382 · 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
Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex
Kubota, Y., Hattori, R., & Yui, Y. (1994) · Brain Research · doi:10.1016/0006-8993(94)91060-x · Cited by 365 · see citing works
Identified sources and targets of slow inhibition in the neocortex
Tamás, G., Simon, A. L., & Szabadics, J. (2003) · Science · doi:10.1126/science.1082053 · Cited by 359 · 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
Self-citationFranco, S. J., Martínez‐Garay, I., Gil, C., Harkins-Perry, S. R., & Müller, U. (2011) · Neuron · doi:10.1016/j.neuron.2011.01.003 · Cited by 329 · see citing works
Characterization of Nkx6-2-Derived Neocortical Interneuron Lineages
Sousa, V. H., Miyoshi, G., Hjerling-Leffler, J., Karayannis, T., & Fishell, G. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp038 · Cited by 328 · see citing works
Self-citationShimogori, T., Banuchi, V., Ng, H., Strauss, J. B., & Grove, E. (2004) · Development · doi:10.1242/dev.01428 · Cited by 317 · see citing works
Neuronal activity is required for the development of specific cortical interneuron subtypes
De Marco García, N. V., Karayannis, T., & Fishell, G. (2011) · Nature · doi:10.1038/nature09865 · Cited by 294 · see citing works
Self-citationThe 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
Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order
Yoshida, M., Assimacopoulos, S., Jones, K. R., & Grove, E. A. (2006) · Development · doi:10.1242/dev.02209 · Cited by 275 · see citing works
Cortical Plasticity Induced by Inhibitory Neuron Transplantation
Southwell, D. G., Froemke, R. C., Alvarez-Buylla, A., Stryker, M. P., & Gandhi, S. P. (2010) · Science · doi:10.1126/science.1183962 · Cited by 271 · see citing works
Dlx transcription factors promote migration through repression of axon and dendrite growth
Cobos, I., Borello, U., & Rubenstein, J. L. R. (2007) · Neuron · doi:10.1016/j.neuron.2007.05.024 · Cited by 246 · see citing works
Lavado, A., Lagutin, O. V., Chow, L. M. L., Baker, S. J., & Oliver, G. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000460 · Cited by 238 · see citing works
Self-citationWaclaw, 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
López-Bendito, G., Sánchez-Alcañiz, J. A., Pla, R., Borrell, V., Picó, E., Valdeolmillos, M., & Marín, O. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4651-07.2008 · Cited by 236 · see citing works
Kubota, Y., Shigematsu, N., Karube, F., Sekigawa, A., Kato, S., Yamaguchi, N., Hirai, Y., Morishima, M., & Kawaguchi, Y. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq252 · Cited by 235 · see citing works
Miyoshi, G., & Fishell, G. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq155 · Cited by 230 · see citing works
Self-citationChapter 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
Self-citationNKX2.1 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
Shaping Our Minds: Stem and Progenitor Cell Diversity in the Mammalian Neocortex
Franco, S. J., & Müller, U. (2013) · Neuron · doi:10.1016/j.neuron.2012.12.022 · Cited by 219 · see citing works
Torii, M.-A., Matsuzaki, F., Osumi, N., Kaibuchi, K., Nakamura, S., Casarosa, S., Guillemot, F., & Nakafuku, M. (1999) · Development · doi:10.1242/dev.126.3.443 · Cited by 217 · see citing works
Self-citationA spatial bias for the origins of interneuron subgroups within the medial ganglionic eminence
Wonders, C. P., Taylor, L. A., Welagen, J., Mbata, I. C., Xiang, J., & Anderson, S. A. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.11.018 · 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 · cited 1× · see citing works
“…migration, and maturation of MGE-derived lineages (Sussel et al., 1999; Liodis et al., 2007; Butt et al., 2008; Du et al., 2008; Zhao et al., 2008; Azim et al., 2009; Batista-Brito et al., 2009; Balamotis et al., 2012; Close et al., 2012; Denaxa et al., 2012; Narboux-Nême et al., 2012).”
BackgroundSelf-citationLi, G., Adesnik, H., Li, J., Long, J., Nicoll, R. A., Rubenstein, J. L. R., & Pleasure, S. J. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4602-07.2008 · Cited by 209 · see citing works
Machoň, O., Backman, M., Machoňová, O., Kozmík, Z., Vacı́k, T., Andersen, L., & Krauss, S. J. K. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.08.038 · Cited by 208 · 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
Cellular and molecular mechanisms controlling the migration of neocortical interneurons
Marín, Ó. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12225 · Cited by 206 · 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
Karalay, Ö., Doberauer, K., Vadodaria, K. C., Knobloch, M., Berti, L., Miquelajauregui, A., Schwark, M., Jagasia, R., Taketo, M. M., Tarabykin, V., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1013456108 · Cited by 201 · see citing works
Generation of interneuron diversity in the mouse cerebral cortex
Gelman, D. M., & Marín, O. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07267.x · Cited by 188 · 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
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
Battiste, J. D., Helms, A. W., Kim, E. J., Savage, T. K., Lagace, D. C., Mandyam, C. D., Eisch, A. J., Miyoshi, G., & Johnson, J. E. B. (2006) · Development · doi:10.1242/dev.02727 · Cited by 178 · see citing works
Self-citationFlandin, 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
Synaptic interactions of late-spiking neocortical neurons in layer 1
Chu, Z., Galarreta, M., & Hestrin, S. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-01-00096.2003 · Cited by 172 · see citing works
Miller, M. W. (1985) · Developmental Brain Research · doi:10.1016/0165-3806(85)90040-9 · Cited by 171 · 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
Inan, M., Welagen, J., & Anderson, S. A. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhr148 · Cited by 161 · see citing works
Distinction between Color Photoreceptor Cell Fates Is Controlled by Prospero in Drosophila
Cook, T. A., Franck Pichaud, N., Sonneville, R., Papatsenko, D., & Desplan, C. (2003) · Developmental Cell · doi:10.1016/s1534-5807(03)00156-4 · Cited by 160 · see citing works
Fairén, A., Cobas, A., & Fonseca, M. (1986) · Journal of Comparative Neurology · doi:10.1002/cne.902510105 · Cited by 158 · see citing works
Miyoshi, G., & Fishell, G. (2012) · Neuron · doi:10.1016/j.neuron.2012.04.025 · Cited by 157 · see citing works
Self-citationIwano, T., Masuda, A., Kiyonari, H., Enomoto, H., & Matsuzaki, F. (2012) · Development · doi:10.1242/dev.080002 · Cited by 155 · see citing works
Self-citationThe Logic of Inhibitory Connectivity in the Neocortex
Fino, É., Packer, A. M., & Yuste, R. (2012) · The Neuroscientist · doi:10.1177/1073858412456743 · Cited by 151 · see citing works
Colasante, G., Collombat, P., Raimondi, V., Bonanomi, D., Ferrai, C., Maira, M., Yoshikawa, K., Mansouri, A., Valtorta, F., Rubenstein, J. L. R., et al. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1283-08.2008 · Cited by 150 · see citing works
Prox1 expression patterns in the developing and adult murine brain
Lavado, A., & Oliver, G. C. (2006) · Developmental Dynamics · doi:10.1002/dvdy.21024 · Cited by 146 · see citing works
Self-citationGil, C., Franco, S. J., Martínez‐Garay, I., Espinosa, A., Harkins-Perry, S. R., & Müller, U. (2013) · Neuron · doi:10.1016/j.neuron.2013.06.040 · Cited by 143 · see citing works
Origin and molecular specification of globus pallidus neurons
Nóbrega-Pereira, S., Gelman, D., Bartolini, G., Pla, R., Pierani, A., & Marín, O. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4023-09.2010 · Cited by 142 · see citing works
Close, J., Xu, H., De Marco García, N., Batista-Brito, R., Rossignol, E., Rudy, B., & Fishell, G. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.3583-12.2012 · Cited by 141 · see citing works
Self-citationVucurovic, K., Gallopin, T., Ferezou, I., Rancillac, A., Chameau, P., van Hooft, J. A., Geoffroy, H., Monyer, H., Rossier, J., & Vitalis, T. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhp310 · Cited by 139 · 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
Prox1 Regulates the Notch1-Mediated Inhibition of Neurogenesis
Kaltezioti, V., Kouroupi, G., Oikonomaki, M., Mantouvalou, E., Στεργιόπουλος, Α., CHARONIS, A. S., Rohrer, H., Matsas, R., & Politis, P. K. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000565 · Cited by 126 · see citing works
Genetic programs controlling cortical interneuron fate
Kessaris, N., Magno, L., Rubin, A. N., & Oliveira, M. G. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.12.012 · Cited by 122 · see citing works
Cell-Autonomous Roles of ARX in Cell Proliferation and Neuronal Migration during Corticogenesis
Friocourt, G., Kanatani, S., Tabata, H., Yozu, M., Takahashi, T., Antypa, M., Raguénès, O., Chelly, J., Férec, C., Nakajima, K., et al. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1067-08.2008 · Cited by 121 · see citing works
β-catenin–mediated Wnt signaling regulates neurogenesis in the ventral telencephalon
Gulácsi, A., & Anderson, S. A. (2008) · Nature Neuroscience · doi:10.1038/nn.2226 · Cited by 119 · 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
Sensory inputs control the integration of neurogliaform interneurons into cortical circuits
De Marco García, N. V., Priya, R., Tuncdemir, S. N., Fishell, G., & Karayannis, T. (2015) · Nature Neuroscience · doi:10.1038/nn.3946 · Cited by 117 · see citing works
Self-citationLaminar fate of cortical GABAergic interneurons is dependent on both birthdate and phenotype
Rymar, V. V., & Sadikot, A. F. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21250 · Cited by 116 · 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
Molecular Neuroanatomy's “Three Gs”: A Primer
Dymecki, S. M., & Kim, J. C. (2007) · Neuron · doi:10.1016/j.neuron.2007.03.009 · Cited by 110 · see citing works
Maturation-Promoting Activity of SATB1 in MGE-Derived Cortical Interneurons
Denaxa, M., Kalaitzidou, M., Garefalaki, A., Achimastou, A., Lasrado, R., Maes, T., & Pachnis, V. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.10.003 · Cited by 105 · see citing works
Martínez‐Cerdeño, V., Noctor, S. C., Espinosa, A., Ariza, J., Parker, P. R. L., Orasji, S. S., Daadi, M. M., Bankiewicz, K. S., Álvarez-Buylla, A., & Kriegstein, A. R. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.01.004 · Cited by 104 · see citing works
Sessa, A., Mao, C., Colasante, G., Nini, A., Klein, W. H., & Broccoli, V. (2010) · Genes & Development · doi:10.1101/gad.575410 · Cited by 101 · see citing works
The vertebrate ortholog of Aristaless is regulated by Dlx genes in the developing forebrain
Cobos, I., Broccoli, V., & Rubenstein, J. L. R. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20405 · Cited by 90 · see citing works
Molecules and Mechanisms Involved in the Generation and Migration of Cortical Interneurons
Hernandez-Miranda, L. R., Parnavelas, J. G., & Chiara, F. (2010) · ASN NEURO · doi:10.1042/an20090053 · Cited by 90 · see citing works
Miquelajáuregui, A., de Putte, T. V., Polyakov, A. S., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0609863104 · 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
Balamotis, M. A., Tamberg, N., Woo, Y. J., Li, J., Davy, B., Kohwi-shigematsu, T., & Kohwi, Y. (2011) · Molecular and Cellular Biology · doi:10.1128/mcb.05917-11 · Cited by 84 · see citing works
Inada, H., Watanabe, M., Uchida, T., Ishibashi, H., Wake, H., Nemoto, T., Yanagawa, Y., Fukuda, A., & Nabekura, J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027048 · Cited by 83 · 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
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
Rubin, A. N., & Kessaris, N. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077339 · Cited by 69 · see citing works
Lineage-dependent circuit assembly in the neocortex
Gao, P., Sultan, K. T., Zhang, X., & Shi, S. (2013) · Development · doi:10.1242/dev.087668 · Cited by 64 · see citing works
New dimensions of interneuronal specialization unmasked by principal cell heterogeneity
Krook-Magnuson, E., Varga, C., Lee, S.-H., & Soltesz, I. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2011.10.005 · Cited by 63 · see citing works
Development of Layer 1 Neurons in the Mouse Neocortex
Ma, J., Yao, X.-H., Fu, Y., & Yu, Y. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht114 · Cited by 57 · 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
Directing neuron-specific transgene expression in the mouse CNS
Miyoshi, G., & Fishell, G. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.08.013 · Cited by 49 · see citing works
Self-citationMigratory 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
Characterization and Distribution of Reelin-Positive Interneuron Subtypes in the Rat Barrel Cortex
Pohlkamp, T., Dávid, C., Cauli, B., Gallopin, T., Bouché, E., Karagiannis, A., May, P., Herz, J., Frotscher, M., Staiger, J. F., et al. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht161 · Cited by 45 · see citing works
Intrinsic and extrinsic mechanisms control the termination of cortical interneuron migration
Inamura, N., Kimura, T., Tada, S., Kurahashi, T., Yanagida, M., Yanagawa, Y., Ikenaka, K., & Murakami, F. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.3446-11.2012 · Cited by 43 · see citing works
Functional adaptation of cortical interneurons to attenuated activity is subtype-specific
Karayannis, T., García, N. V. D. M., & Fishell, G. (2012) · Frontiers in Neural Circuits · doi:10.3389/fncir.2012.00066 · Cited by 20 · see citing works
Self-citationSpecification of GABAergic Neocortical Interneurons
Miyoshi, G., Machold, R. P., & Fishell, G. (2013) · Springer eBooks · doi:10.1007/978-4-431-54496-8_5 · Cited by 14 · see citing works
Self-citationNarboux‐Nême, N., Goïame, R., Mattéi, M., Cohen‐Tannoudji, M., & Wassef, M. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.6068-11.2012 · Cited by 9 · see citing works
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A taxonomy of transcriptomic cell types across the isocortex and hippocampal formation
Yao, Z., van Velthoven, C. T. J., Nguyen, T. N., Goldy, J., Sedeno-Cortes, A. E., Baftizadeh, F., Bertagnolli, D., Casper, T., Chiang, M., Crichton, K., et al. (2021) · Cell · doi:10.1016/j.cell.2021.04.021 · Cited by 1,065 · see citing works
Sohal, V. S., & Rubenstein, J. L. R. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0426-0 · Cited by 988 · see citing works
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Pelkey, K. A., Chittajallu, R., Craig, M. T., Tricoire, L., Wester, J. C., & McBain, C. J. (2017) · Physiological Reviews · doi:10.1152/physrev.00007.2017 · Cited by 889 · see citing works
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John Lin, C.-C., Yu, K., Hatcher, A., Huang, T.-W., Lee, H. K., Carlson, J., Weston, M. C., Chen, F., Zhang, Y., Zhu, W., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4493 · Cited by 525 · see citing works
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Lee, D.-S., Luo, C., Zhou, J., Chandran, S., Rivkin, A., Bartlett, A., Nery, J. R., Fitzpatrick, C., O’Connor, C., Dixon, J. R., et al. (2019) · Nature Methods · doi:10.1038/s41592-019-0547-z · Cited by 340 · see citing works
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Cardin, J. A. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.07.015 · Cited by 254 · see citing works
Cortical interneuron specification: the juncture of genes, time and geometry
Bandler, R. C., Mayer, C., & Fishell, G. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.10.003 · Cited by 125 · see citing works
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Batista-Brito, R., Vinck, M., Ferguson, K. A., Chang, J. T., Laubender, D., Lur, G., Mossner, J. M., Hernandez, V. G., Ramakrishnan, C., Deisseroth, K., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.07.034 · Cited by 135 · see citing works
Zheng, Y., Fan, W., Zhang, X., & Dong, E. (2016) · Epigenetics · doi:10.1080/15592294.2016.1146850 · Cited by 111 · see citing works
Frazer, S., Prados, J., Niquille, M., Cadilhac, C., Markopoulos, F., Gomez, L., Tomasello, U., Telley, L., Holtmaat, A., Jabaudon, D., et al. (2017) · Nature Communications · doi:10.1038/ncomms14219 · Cited by 72 · see citing works
“2), and glucose (22), and equilibrated with 95% O2/5% CO2, pH 7.”
Radial glia in the ventral telencephalon
Turrero García, M., & Harwell, C. C. (2017) · FEBS Letters · doi:10.1002/1873-3468.12829 · Cited by 62 · see citing works
Conserved rules in embryonic development of cortical interneurons
Laclef, C., & Métin, C. (2018) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2017.09.017 · Cited by 57 · see citing works
Borges-Merjane, C., Kim, O., & Jonas, P. (2020) · Neuron · doi:10.1016/j.neuron.2019.12.022 · Cited by 60 · see citing works
Touzot, A., Ruiz-Reig, N., Vitalis, T., & Studer, M. (2016) · Development · doi:10.1242/dev.131102 · Cited by 56 · see citing works
Neurogliaform cortical interneurons derive from cells in the preoptic area
Niquille, M., Limoni, G., Markopoulos, F., Cadilhac, C., Prados, J., Holtmaat, A., & Dayer, A. (2018) · eLife · doi:10.7554/elife.32017 · Cited by 55 · see citing works
Emmenegger, V., Qi, G., Wang, H., & Feldmeyer, D. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhx352 · Cited by 26 · see citing works
Torigoe, M., Yamauchi, K., Kimura, T., Uemura, Y., & Murakami, F. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.3550-15.2016 · Cited by 21 · see citing works
- Authors
- Miyoshi, G., Young, A., Petros, T., Karayannis, T., McKenzie Chang, M., Lavado, A., Iwano, T., Nakajima, M., Taniguchi, H., Huang, Z. J., Heintz, N., Oliver, G., Matsuzaki, F., Machold, R. P., & Fishell, G.
- Affiliations
- New York University (US)
- St. Jude Children's Research Hospital (US)
- RIKEN (JP)
- Howard Hughes Medical Institute (US)
- Cold Spring Harbor Laboratory (US)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2015-09-16
- Volume
- 35
- Issue
- 37
- Pages
- 12869-12889
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC4571608
- OpenAlex
- W2218398206
- Cited by
- 135
- References
- 130
- Citations by year
- 2026: 5 · 2025: 12 · 2024: 14 · 2023: 8 · 2022: 8 · 2021: 23 · 2020: 12 · 2019: 11 · 2018: 11 · 2017: 22 · 2016: 7 · 2015: 2
- FWCI
- 5.68
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, other-oa)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- Simons Foundation
- New York State Stem Cell Science
- National Institutes of Health
- Japan Society for the Promotion of Science (25860141)
- National Institute of Mental Health (K99MH104595, R01MH071679)
- National Cancer Institute (P30CA021765)
- National Institute of Neurological Disorders and Stroke (F32NS074742, R01NS039007, R01NS081297, PPG-NS309889)
- 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 › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- Prox1, caudal ganglionic eminence, VIP interneurons, tangential migration, radial migration, superficial cortical layers, neural integration, postnatal maturation, activity-dependent development, transcriptional regulation
- MeSH terms
- Reelin Protein, Prospero-Related Homeobox 1 Protein, Animals, Cell Movement, Cerebral Cortex, Interneurons, Nerve Tissue Proteins, Serine Endopeptidases, Vasoactive Intestinal Peptide, Biomarkers, Cell Adhesion Molecules, Neuronal, Extracellular Matrix Proteins, Homeodomain Proteins, Gene Expression Regulation, Developmental, Cell Lineage, Gene Expression Profiling, Tumor Suppressor Proteins, Mice, Neurogenesis, GABAergic Neurons, Calbindin 2
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