A wide diversity of cortical GABAergic interneurons derives from the embryonic preoptic area
Open accessAbstract
GABA-containing (GABAergic) interneurons comprise a very heterogeneous group of cells that are crucial for cortical function. Different classes of interneurons specialize in targeting specific subcellular domains of excitatory pyramidal cells or other interneurons, which provides cortical circuits with an enormous capability for information processing. As in other regions of the CNS, cortical interneuron diversity is thought to emerge from the genetic specification of different groups of progenitor cells within the subpallium. Most cortical interneurons originate from two main regions, the medial and the caudal ganglionic eminences (MGE and CGE, respectively). In addition, it has been shown that progenitors in the embryonic preoptic area (POA) also produce a small population of cortical GABAergic interneurons. Here, we show that the contribution of the POA to the complement of cortical GABAergic interneurons is larger than previously believed. Using genetic fate mapping and in utero transplantation experiments, we demonstrate that Dbx1-expressing progenitor cells in the POA give rise to a small but highly diverse cohort of cortical interneurons, with some neurochemical and electrophysiological characteristics that were previously attributed to MGE- or CGE-derived interneurons. There are, however, some features that seem to distinguish POA-derived interneurons from MGE- or CGE-derived cells, such as their preferential laminar location. These results indicate that the mechanisms controlling the specification of different classes of cortical interneurons might be more complex than previously expected. Together with earlier findings, our results also suggest that the POA generates nearly 10% of the GABAergic interneurons in the cerebral cortex of the mouse.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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 MGE and adjacent POA generate virtually all SST+ and PV+ cortical interneurons.
“The MGE and adjacent POA generate virtually all interneurons in the SST+ and PV+ classes”
From Development and Functional Diversification of Cortical Interneurons (2018) · cites this paper as Gelman et al., 2011
The POA is estimated to produce approximately 10% of neocortical and hippocampal interneurons.
“The POA is estimated to produce ~10% of neocortical and hippocampal interneurons”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [389]
Mature cortical interneurons derived from the POA are highly diverse, consisting of small fractions of PV-, SST-, NPY-, and reelin-expressing interneurons.
“Mature cortical interneurons derived from the POA are highly diverse consisting of small fractions of PV-, SST-, NPY-, and reelin-expressing interneurons”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [389]
GIFM studies using Dbx1-Cre mice revealed that the ventral POA region generates minor populations of deep PV- and SST-expressing interneurons.
“GIFM studies using Dbx1-Cre mice revealed that the ventral POA region generates minor populations of deep PV- and SST-expressing interneurons”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [389]
Most interneuron precursors emerging from the POA do not rely on downstream activation of Lhx6 to specify PV and SST interneurons.
“most interneuron precursors emerging from the POA do not rely on downstream activation of Lhx6 to specify PV and SST interneurons”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [389]
Two subdomains are found in the POA based on nonoverlapping expression profiles for Dbx1 and Nkx5.1.
“Two subdomains are found in the POA based on nonoverlapping expression profiles for Dbx1 and Nkx5.1”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [389]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Interneurons of the hippocampus
Freund, T. F., & Buzsáki, G. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:4 · Cited by 3,423 · see citing works
Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus
Srinivas, S., Watanabe, T., Lin, C.-S., William, C. M., Tanabe, Y., Jessell, T. M., & Costantini, F. (2001) · BMC Developmental Biology · doi:10.1186/1471-213x-1-4 · Cited by 3,121 · 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
Neuronal specification in the spinal cord: inductive signals and transcriptional codes
Jessell, T. M. (2000) · Nature Reviews Genetics · doi:10.1038/35049541 · Cited by 2,089 · see citing works
Neuronal 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
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
Briscoe, J., Pierani, A., Jessell, T. M., & Ericson, J. (2000) · Cell · doi:10.1016/s0092-8674(00)80853-3 · Cited by 1,111 · see citing works
Self-citationA 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
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
Defined types of cortical interneurone structure space and spike timing in the hippocampus
Somogyi, P., & Klausberger, T. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2004.078915 · Cited by 927 · 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
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
Dessaud, É., McMahon, A. P., & Briscoe, J. (2008) · Development · doi:10.1242/dev.009324 · Cited by 735 · 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
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
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
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
Self-citationMiyoshi, 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
DeFelipe, J. (1997) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(97)10013-8 · Cited by 550 · 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
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
Self-citationGsh2 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
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
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
Kawaguchi, Y., & Kondo, S. (2002) · Journal of Neurocytology · doi:10.1023/a:1024126110356 · Cited by 395 · see citing works
Control of Interneuron Fate in the Developing Spinal Cord by the Progenitor Homeodomain Protein Dbx1
Pierani, A., Moran-Rivard, L., Sunshine, M. J., Littman, D. R., Goulding, M., & Jessell, T. M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00212-4 · Cited by 379 · see citing works
Self-citationLiodis, 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
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
Transcriptional networks regulating neuronal identity in the developing spinal cord
Lee, S., & Pfaff, S. L. (2001) · Nature Neuroscience · doi:10.1038/nn750 · Cited by 290 · see citing works
Preferential Origin and Layer Destination of GAD65-GFP Cortical Interneurons
López‐Bendito, G. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh072 · Cited by 288 · 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
Self-citationNóbrega-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
Medina, L. M., Legáz, I., González, G. G., Castro, F. D., Rubenstein, J. L. R., & Puelles, L. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20141 · Cited by 238 · 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
A 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
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
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
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
Layer acquisition by cortical GABAergic interneurons is independent of Reelin signaling
Pla, R., Borrell, V., Flames, N., & Marín, O. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0245-06.2006 · Cited by 151 · see citing works
Self-citationIdentification of distinct telencephalic progenitor pools for neuronal diversity in the amygdala
Hirata, T., Li, P., Lanuza, G. M., Cocas, L. A., Huntsman, M. M., & Corbin, J. G. (2009) · Nature Neuroscience · doi:10.1038/nn.2241 · Cited by 151 · see citing works
Vucurovic, 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
Griveau, A., Borello, U., Causeret, F., Tissir, F., Boggetto, N., Karaz, S., & Pierani, A. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000440 · Cited by 124 · see citing works
Self-citationThree classes of GABAergic interneurons in neocortex and neostriatum.
Kubota, Y., & Kawaguchi, Y. (1994) · PubMed · Cited by 89 · 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
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
Self-citationTeissier, A., Waclaw, R. R., Griveau, A., Campbell, K., & Pierani, A. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr122 · Cited by 39 · see citing works
Self-citationSoriano, E., del Rı́o, J. A., Ferrer, I., Auladell, C., de Lecea, L., & Alcántara, S. (1992) · Neuroscience Letters · doi:10.1016/0304-3940(92)90360-j · Cited by 37 · see citing works
Flagged first, then by citations
1 of the 51 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Interneuron cell types are fit to function
Kepecs, A., & Fishell, G. (2014) · Nature · doi:10.1038/nature12983 · Cited by 1,110 · see citing works
Hippocampal GABAergic Inhibitory Interneurons
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
Development and Functional Diversification of Cortical Interneurons
Lim, L., Mi, D., Llorca, A., & Marín, O. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.009 · Cited by 714 · see citing works
“…Nr2f1 and Nr2f2 influence neuronal specification by regulating cell-cycle dynamics (Naka et al., 2008), which may explain why factors involved in the regulation of the cell cycle have also been involved in the regulation of interneuron diversity (Glickstein et al., 2007; Petros et al., 2015).”
Generating Neuronal Diversity in the Mammalian Cerebral Cortex
Lodato, S., & Arlotta, P. (2015) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100814-125353 · Cited by 389 · 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
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
Erbb4 Deletion from Fast-Spiking Interneurons Causes Schizophrenia-like Phenotypes
del Pino, I., García-Frigola, C., Dehorter, N., Brotons-Mas, J. R., Alvarez-Salvado, E., Martínez de Lagrán, M., Ciceri, G., Gabaldón, M. V., Moratal, D., Dierssen, M., et al. (2013) · Neuron · doi:10.1016/j.neuron.2013.07.010 · Cited by 314 · see citing works
Self-citationCortical interneuron development: a tale of time and space
Hu, J. S., Vogt, D., Sandberg, M., & Rubenstein, J. L. (2017) · Development · doi:10.1242/dev.132852 · Cited by 189 · 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
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
Reelin and neuropsychiatric disorders
Ishii, K., Kubo, K.-I., & Nakajima, K. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00229 · Cited by 185 · see citing works
Development and specification of GABAergic cortical interneurons
Kelsom, C., & Lu, W. (2013) · Cell & Bioscience · doi:10.1186/2045-3701-3-19 · Cited by 171 · see citing works
Assembloid CRISPR screens reveal impact of disease genes in human neurodevelopment
Meng, X., Yao, D., Imaizumi, K., Chen, X., Kelley, K. W., Reis, N., Thete, M. V., McKinney, A. A., Kulkarni, S., Panagiotakos, G., et al. (2023) · Nature · doi:10.1038/s41586-023-06564-w · Cited by 145 · 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
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
Inhibitory Interneurons and their Circuit Motifs in the Many Layers of the Barrel Cortex
Feldmeyer, D., Qi, G., Emmenegger, V., & Staiger, J. F. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.05.027 · Cited by 134 · 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
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
Neuronal nitric oxide synthase expressing neurons: a journey from birth to neuronal circuits
Tricoire, L., & Vitalis, T. (2012) · Frontiers in Neural Circuits · doi:10.3389/fncir.2012.00082 · Cited by 126 · see citing works
Mossink, B., Negwer, M., Schubert, D., & Nadif Kasri, N. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03714-5 · Cited by 114 · see citing works
The Epigenome in Neurodevelopmental Disorders
Reichard, J., & Zimmer‐Bensch, G. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.776809 · Cited by 112 · see citing works
Modulation of apoptosis controls inhibitory interneuron number in the cortex
Denaxa, M., Neves, G., Rabinowitz, A., Kemlo, S., Liodis, P., Burrone, J., & Pachnis, V. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.01.064 · Cited by 112 · see citing works
Genetic dissection of GABAergic neural circuits in mouse neocortex
Taniguchi, H. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00008 · Cited by 106 · see citing works
New Insights Into Cholinergic Neuron Diversity
Ahmed, N. Y., Knowles, R., & Dehorter, N. (2019) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2019.00204 · Cited by 108 · see citing works
Self-citationGABAergic Restriction of Network Dynamics Regulates Interneuron Survival in the Developing Cortex
Duan, Z. R. S., Che, A., Chu, P., Modol, L., Bollmann, Y., Babij, R., Fetcho, R. N., Otsuka, T., Fuccillo, M. V., Liston, C., et al. (2020) · Neuron · doi:10.1016/j.neuron.2019.10.008 · Cited by 102 · see citing works
Npas1 + -Nkx2.1 + Neurons Are an Integral Part of the Cortico-pallido-cortical Loop
Abecassis, Z. A., Berceau, B. L., Win, P. H., García, D., Xenias, H. S., Cui, Q., Pamukcu, A., Cherian, S., Hernández, V. M., Chon, U., et al. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1199-19.2019 · Cited by 93 · see citing works
Diversity and Function of Somatostatin-Expressing Interneurons in the Cerebral Cortex
Riedemann, T. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20122952 · Cited by 94 · see citing works
Vascular Influence on Ventral Telencephalic Progenitors and Neocortical Interneuron Production
Tan, X., Liu, W. A., Zhang, X., Shi, W., Ren, S., Li, Z., Brown, K. N., & Shi, S. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.02.023 · Cited by 83 · see citing works
Spatio-temporal extension in site of origin for cortical calretinin neurons in primates
Hladnik, A., Džaja, D., Darmopil, S., Jovanov-MiloÅ¡ević, N., & Petanjek, Z. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00050 · Cited by 72 · 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
Orduz, D., Benamer, N., Ortolani, D., Coppola, E., Vigier, L., Pierani, A., & Angulo, M. C. (2019) · Nature Communications · doi:10.1038/s41467-019-11904-4 · Cited by 75 · see citing works
Self-citationHuman pallial MGE-type GABAergic interneuron cell therapy for chronic focal epilepsy
Bershteyn, M., Bröer, S., Parekh, M. B., Maury, Y., Havlicek, S., Kriks, S., Fuentealba, L. C., Lee, S., Zhou, R., Subramanyam, G., et al. (2023) · Cell stem cell · doi:10.1016/j.stem.2023.08.013 · Cited by 75 · see citing works
Rubin, A. N., & Kessaris, N. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077339 · Cited by 69 · see citing works
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
The serotonin 5-HT3 receptor: a novel neurodevelopmental target
Engel, M., Smidt, M. P., & van Hooft, J. A. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00076 · Cited by 70 · see citing works
Developmental specification of forebrain cholinergic neurons
Allaway, K. C., & Machold, R. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2016.11.007 · Cited by 68 · see citing works
Dissociable Roles of Pallidal Neuron Subtypes in Regulating Motor Patterns
Cui, Q., Pamukcu, A., Cherian, S., Chang, I. Y. M., Berceau, B. L., Xenias, H. S., Higgs, M. H., Rajamanickam, S., Chen, Y., Du, X., et al. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2210-20.2021 · Cited by 61 · see citing works
Pai, E. L.-L., Vogt, D. L., Clemente-Perez, A., McKinsey, G. L., Cho, F. S., Hu, J. S., Wimer, M., Paul, A., Darbandi, S. F., Pla, R., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.01.031 · Cited by 63 · see citing works
Self-citationButt, S. J. B., Stacey, J. A., Teramoto, Y., & Vagnoni, C. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.03.011 · Cited by 61 · see citing works
Interneuron Transplantation as a Treatment for EpilepsyPreprint
Hunt, R. F., & Baraban, S. C. (2015) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a022376 · Cited by 67 · 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
Dual midbrain and forebrain origins of thalamic inhibitory interneurons
Jager, P., Moore, G., Calpin, P., Durmishi, X., Salgarella, I., Menage, L., Kita, Y., Wang, Y., Kim, D. W., Blackshaw, S., et al. (2021) · eLife · doi:10.7554/elife.59272 · Cited by 61 · see citing works
Cell and circuit complexity of the external globus pallidus
Courtney, C. D., Pamukcu, A., & Chan, C. S. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01368-7 · 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
Early GABAergic circuitry in the cerebral cortex
Luhmann, H. J., Kirischuk, S., Sinning, A., & Kilb, W. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.12.014 · Cited by 59 · see citing works
Development and Organization of the Evolutionarily Conserved Three-Layered Olfactory Cortex
Klingler, E. (2017) · eNeuro · doi:10.1523/eneuro.0193-16.2016 · Cited by 58 · see citing works
Mechanisms regulating GABAergic neuron development
Achim, K., Salminen, M., & Partanen, J. M. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1501-3 · Cited by 56 · see citing works
Puelles, L., Morales-Delgado, N., Merchán, P., Castro‐Robles, B., Martinez-de-la-Torre, M., Dı́az, C., & Ferrán, J. L. (2015) · Brain Structure and Function · doi:10.1007/s00429-015-1086-8 · Cited by 55 · 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
Interneuron development and dysfunction
Yang, J., Yang, X. W., & Tang, K. (2021) · FEBS Journal · doi:10.1111/febs.15872 · Cited by 52 · 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
Peyre, E., Silva, C. G., & Nguyen, L. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00129 · Cited by 51 · 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
Generation of diverse cortical inhibitory interneurons
Sultan, K. T., & Shi, S. (2017) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.306 · Cited by 48 · see citing works
Hoch, R. V., Lindtner, S., Price, J. D., & Rubenstein, J. L. R. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.06.043 · Cited by 48 · see citing works
The Combinatorial Creature: Cortical Phenotypes within and across Lifetimes
Krubitzer, L. A., & Prescott, T. J. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.08.002 · Cited by 47 · see citing works
From Progenitors to Progeny: Shaping Striatal Circuit Development and Function
Knowles, R., Dehorter, N., & Ellender, T. J. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0620-21.2021 · Cited by 45 · see citing works
Self-citationMining the jewels of the cortex’s crowning mystery
Ibrahim, L. A., Schuman, B., Bandler, R. C., Rudy, B., & Fishell, G. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.04.005 · Cited by 48 · see citing works
Kanatani, S., Honda, T., Aramaki, M., Hayashi, K., Kubo, K., Ishida, M., Tanaka, D. H., Kawauchi, T., Sekine, K., Kusuzawa, S., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1420701112 · Cited by 45 · see citing works
Regionalized differentiation of CRH, TRH, and GHRH peptidergic neurons in the mouse hypothalamus
Morales-Delgado, N., Castro‐Robles, B., Ferrán, J. L., Martı́nez-de-la-Torre, M., Puelles, L., & Dı́az, C. (2013) · Brain Structure and Function · doi:10.1007/s00429-013-0554-2 · Cited by 44 · see citing works
Winterer, J., Lukacsovich, D., Que, L., Sartori, A. M., Luo, W., & Földy, C. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14549 · Cited by 40 · see citing works
Pai, E. L.-L., Chen, J., Darbandi, S. F., Cho, F. S., Chen, J., Lindtner, S., Chu, J. S. F., Paz, J. T., Vogt, D. L., Paredes, M. F., et al. (2020) · eLife · doi:10.7554/elife.54903 · Cited by 43 · see citing works
Parvalbumin - Positive Neurons in the Neocortex: A Review
Druga, R., Salaj, M., & Al‐Redouan, A. (2023) · Physiological Research · doi:10.33549/physiolres.935005 · Cited by 42 · see citing works
Origin, Development, and Synaptogenesis of Cortical Interneurons
Llorca, A., & Deogracias, R. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.929469 · Cited by 40 · see citing works
Spatial enhancer activation influences inhibitory neuron identity during mouse embryonic development
Dvoretskova, E., Ho, M. C., Kittke, V., Neuhaus, F., Vitali, I., Lam, D. D., Delgado, I., Feng, C., Torres, M., Winkelmann, J., et al. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01611-9 · Cited by 34 · see citing works
The origin of neocortical nitric oxide synthase-expressing inhibitory neurons
Jaglin, X. H., Hjerling‐Leffler, J., Fishell, G., & Batista‐Brito, R. (2012) · Frontiers in Neural Circuits · doi:10.3389/fncir.2012.00044 · Cited by 34 · see citing works
Developmental Genes and Malformations in the Hypothalamus
Dı́az, C., & Puelles, L. (2020) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2020.607111 · Cited by 33 · see citing works
Cellular birthdate predicts laminar and regional cholinergic projection topography in the forebrain
Allaway, K. C., Muñoz, W., Tremblay, R., Sherer, M., Herron, J., Rudy, B., Machold, R. P., & Fishell, G. (2020) · eLife · doi:10.7554/elife.63249 · Cited by 32 · see citing works
Regulation of the E/I-balance by the neural matrisome
Mueller-Buehl, C., Wegrzyn, D., Bauch, J., & Faissner, A. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1102334 · Cited by 32 · see citing works
Human pluripotent stem cell (hPSC) and organoid models of autism: opportunities and limitations
Kilpatrick, S., Irwin, C. L., & Singh, K. K. (2023) · Translational Psychiatry · doi:10.1038/s41398-023-02510-6 · Cited by 34 · see citing works
Frazer, S., Otomo, K., & Dayer, A. G. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.147 · Cited by 32 · see citing works
COUP - TF Genes, Human Diseases, and the Development of the Central Nervous System in Murine Models
Yang, X. W., Feng, S., & Tang, K. (2017) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2016.12.002 · Cited by 30 · see citing works
Multiple embryonic origins of nitric oxide synthase-expressing GABAergic neurons of the neocortex
Magno, L., Oliveira, M. G., Mucha, M. W., Rubin, A. N., & Kessaris, N. (2012) · Frontiers in Neural Circuits · doi:10.3389/fncir.2012.00065 · Cited by 31 · see citing works
Chen, Y.-J. J., Vogt, D. L., Wang, Y., Visel, A., Silberberg, S. N., Nicholas, C. R., Danjo, T., Pollack, J. L., Pennacchio, L. A., Anderson, S. A., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0061956 · Cited by 30 · see citing works
Bucher, E., Collins, J. M., King, A. E., Vickers, J. C., & Kirkcaldie, M. (2021) · Brain Structure and Function · doi:10.1007/s00429-021-02327-3 · Cited by 29 · see citing works
Vogt, D. L., Wu, P., Sorrells, S. F., Arnold, C. M., Álvarez-Buylla, A., & Rubenstein, J. L. R. (2015) · Journal of Visualized Experiments · doi:10.3791/52740 · Cited by 29 · see citing works
Regulation of neuronal survival by DNA methyltransferases
Zimmer‐Bensch, G., & Symmank, J. (2017) · Neural Regeneration Research · doi:10.4103/1673-5374.219027 · Cited by 28 · see citing works
The Generation of Cortical Interneurons
Gelman, D. M., Marín, Ó., & Rubenstein, J. L. R. (2012) · Oxford University Press eBooks · doi:10.1093/med/9780199746545.003.0061 · Cited by 28 · see citing works
Self-citationNeuron–Oligodendrocyte Communication in Myelination of Cortical GABAergic Cells
Mazuir, E., Fricker, D., & Sol‐Foulon, N. (2021) · Life · doi:10.3390/life11030216 · Cited by 25 · see citing works
Generating neural diversity through spatial and temporal patterning
Sen, S. (2022) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2022.06.002 · Cited by 28 · see citing works
Elucidating the developmental trajectories of GABAergic cortical interneuron subtypes
Miyoshi, G. (2018) · Neuroscience Research · doi:10.1016/j.neures.2018.09.012 · Cited by 28 · see citing works
Transcriptomic and spatial organization of telencephalic GABAergic neurons
van Velthoven, C. T. J., Gao, Y., Kunst, M., Lee, C., McMillen, D., Chakka, A. B., Casper, T., Clark, M., Chakrabarty, R., Daniel, S. F., et al. (2025) · Nature · doi:10.1038/s41586-025-09296-1 · Cited by 30 · see citing works
Development, Diversity, and Death of MGE-Derived Cortical Interneurons
Williams, R. H., & Riedemann, T. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22179297 · Cited by 24 · see citing works
Brandão, J. A., & Romcy-Pereira, R. N. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00149 · Cited by 26 · see citing works
Defining the nature of human pluripotent stem cell-derived interneurons via single-cell analysis
Allison, T. F., Langerman, J., Sabri, S., Otero‐García, M., Lund, A. J., Huang, J. C., Wei, X., Samarasinghe, R. A., Polioudakis, D., Módy, I., et al. (2021) · Stem Cell Reports · doi:10.1016/j.stemcr.2021.08.006 · Cited by 25 · see citing works
The Embryonic Septum and Ventral Pallium, New Sources of Olfactory Cortex Cells
Ceci, M. L., Pedraza, M., & Carlos, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0044716 · Cited by 25 · see citing works
Transplantation of GABAergic interneurons for cell-based therapy
Spatazza, J., Mancia, W., & Álvarez-Buylla, A. (2017) · Progress in brain research · doi:10.1016/bs.pbr.2016.11.005 · Cited by 23 · see citing works
Impaired Organization of GABAergic Neurons Following Prenatal Hypoxia
Nisimov, H., Orenbuch, A., Pleasure, S. J., & Golan, H. M. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.05.021 · Cited by 24 · see citing works
Hippocampal CA1 Somatostatin Interneurons Originate in the Embryonic MGE/POA
Asgarian, Z., Magno, L., Ktena, N., Harris, K. D., & Kessaris, N. (2019) · Stem Cell Reports · doi:10.1016/j.stemcr.2019.09.008 · Cited by 24 · see citing works
Cortical distribution of GABAergic interneurons is determined by migration time and brain size
Fazzari, P., Mortimer, N., Yabut, O., Vogt, D. L., & Pla, R. (2020) · Development · doi:10.1242/dev.185033 · Cited by 21 · see citing works
Self-citationA Composite Sketch of Fast-Spiking Parvalbumin-Positive Neurons
Bartholomé, O., Bonardeaux, O. D. L. B., Neirinckx, V., & Rogister, B. (2020) · Cerebral Cortex Communications · doi:10.1093/texcom/tgaa026 · Cited by 21 · see citing works
Deciphering inhibitory neuron development: The paths to diversity
Bandler, R. C., & Mayer, C. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102691 · Cited by 20 · see citing works
Interneuron Progenitor Transplantation to Treat CNS Dysfunction
Chohan, M. O., & Moore, H. M. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00064 · Cited by 22 · see citing works
Ansen-Wilson, L. J., & Lipinski, R. J. (2016) · NeuroToxicology · doi:10.1016/j.neuro.2016.12.002 · Cited by 22 · see citing works
Symmank, J., Gölling, V., Gerstmann, K., & Zimmer‐Bensch, G. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy063 · Cited by 22 · see citing works
Being superficial: a developmental viewpoint on cortical layer 1 wiring
Genescu, I., & Garel, S. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.10.003 · Cited by 20 · see citing works
Zimmer‐Bensch, G. (2018) · Brain Research · doi:10.1016/j.brainres.2018.09.001 · Cited by 21 · see citing works
Progress of Induced Pluripotent Stem Cell Technologies to Understand Genetic Epilepsy
Sterlini, B., Fruscione, F., Baldassari, S., Benfenati, F., Zara, F., & Corradi, A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21020482 · Cited by 19 · see citing works
Transcranial Magnetic Stimulation and Neocortical Neurons: The Micro-Macro Connection
Tian, D., & Izumi, S. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.866245 · Cited by 18 · see citing works
Cortical interneuron specification and diversification in the era of big data
Kessaris, N., & Denaxa, M. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102703 · Cited by 17 · see citing works
- Authors
- Gelman, D., Griveau, A., Dehorter, N., Teissier, A., Varela, C., Pla, R., Pierani, A., & Marín, O.
- Affiliations
- Consejo Superior de Investigaciones Científicas (ES)
- Centre National de la Recherche Scientifique (FR)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2011-11-16
- Volume
- 31
- Issue
- 46
- Pages
- 16570-16580
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6633309
- OpenAlex
- W1994924452
- Cited by
- 179
- References
- 51
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 10 · 2023: 14 · 2022: 11 · 2021: 16 · 2020: 23 · 2019: 12 · 2018: 13 · 2017: 18 · 2016: 10 · 2015: 13 · 2014: 8 · 2013: 14 · 2012: 9
- FWCI
- 3.26
- 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)
- Americanae (AECID Library) (publishedVersion, other-oa)
- HAL (submittedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- ANU Open Research (Australian National University) (submittedVersion)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, cc-by-nc-sa)
- Funders
- Association pour la Recherche sur le Cancer
- European Commission (005139)
- Centre National de la Recherche Scientifique
- Ministerio de Ciencia e Innovación (CSD2007-00023)
- 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
- GABAergic interneurons, medial ganglionic eminence, caudal ganglionic eminence, interneuron specification, laminar distribution, mouse cortex, fate mapping, in utero transplantation
- MeSH terms
- Animals, Animals, Newborn, Bacterial Proteins, Bromodeoxyuridine, Cell Movement, Electric Stimulation, Embryo, Mammalian, gamma-Aminobutyric Acid, Indoles, Interneurons, Luminescent Proteins, Membrane Potentials, Mice, Transgenic, Nerve Tissue Proteins, Preoptic Area, Proteins, Somatosensory Cortex, Homeodomain Proteins, Patch-Clamp Techniques, Gene Expression Regulation, Developmental, RNA, Untranslated, Green Fluorescent Proteins, Mice, Neural Stem Cells, In Vitro Techniques
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
