Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy
Abstract
Dlx homeodomain transcription factors are essential during embryonic development for the production of forebrain GABAergic interneurons. Here we show that Dlx1 is also required for regulating the functional longevity of cortical and hippocampal interneurons in the adult brain. We demonstrate preferential Dlx1 expression in a subset of cortical and hippocampal interneurons which, in postnatal Dlx1 mutants, show a time-dependent reduction in number. This reduction preferentially affects calretinin(+) (bipolar cells) and somatostatin(+) subtypes (for example, bitufted cells), whereas parvalbumin(+) subpopulations (basket cells and chandelier cells) seem to be unaffected. Cell transplantation analysis demonstrates that interneuron loss reflects cell-autonomous functions of Dlx1. The decrease in the number of interneurons was associated with a reduction of GABA-mediated inhibitory postsynaptic current in neocortex and hippocampus in vitro and cortical dysrhythmia in vivo. Dlx1 mutant mice show generalized electrographic seizures and histological evidence of seizure-induced reorganization, linking the Dlx1 mutation to delayed-onset epilepsy associated with interneuron loss.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Dlx1 is critically required for maturation of some classes of cortical interneurons.
“a transcription factor that is critically required for the maturation of some classes of cortical interneurons (Cobos et al., 2005)”
From Development and Functional Diversification of Cortical Interneurons (2018) · cites this paper as Cobos et al., 2005
Cites
Modification of seizure activity by electrical stimulation: II. Motor seizure
Racine, R. J. (1972) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(72)90177-0 · Cited by 7,173 · see citing works
Theta oscillations in the hippocampus
Buzsáki, G. (2002) · Neuron · doi:10.1016/s0896-6273(02)00586-x · Cited by 3,332 · 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
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
Self-citationGABAergic cell subtypes and their synaptic connections in rat frontal cortex
Kawaguchi, Y. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.6.476 · Cited by 1,416 · see citing works
Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo
Klausberger, T., Magill, P. J., Márton, L. F., Roberts, J. D. B., Cobden, P. M., Buzsáki, G., & Somogyi, P. (2003) · Nature · doi:10.1038/nature01374 · Cited by 1,345 · see citing works
Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex
Gupta, A., Wang, Y., & Markram, H. (2000) · Science · doi:10.1126/science.287.5451.273 · Cited by 1,036 · 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
Self-citationKindling and status epilepticus models of epilepsy: rewiring the brain
Morimoto, K., Fahnestock, M. L., & Racine, R. J. (2004) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2004.03.009 · Cited by 840 · 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
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
Kitamura, K., Yanazawa, M., Sugiyama, N., Miura, H., Iizuka‐Kogo, A., Kusaka, M., Omichi, K., Suzuki, R., Fukui, Y., Kamiirisa, K., et al. (2002) · Nature Genetics · doi:10.1038/ng1009 · Cited by 708 · see citing works
Interneuron Diversity series: Rhythm and mood in perisomatic inhibition
Freund, T. F. (2003) · Trends in Neurosciences · doi:10.1016/s0166-2236(03)00227-3 · Cited by 641 · 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
Self-citationHistology Of The Nervous System
Cajal, S. R. Y., Azoulay, D. L., swanson, N., & Swanson, L. W. (1995) · doi:10.1093/oso/9780195074017.001.0001 · Cited by 634 · see citing works
Origin and Molecular Specification of Striatal Interneurons
Marín, Ó., Anderson, S. A., & Rubenstein, J. L. R. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06063.2000 · Cited by 627 · see citing works
Self-citationJones, E. G. (1975) · The Journal of Comparative Neurology · doi:10.1002/cne.901600204 · Cited by 602 · see citing works
Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy
Cossart, R., Dinocourt, C., Hirsch, J. C., Merchán-Pérez, Á., DeFelipe, J., Ben‐Ari, Y., Esclapez, M., & Bernard, C. (2001) · Nature Neuroscience · doi:10.1038/82900 · Cited by 597 · see citing works
Loss of silent-chromatin looping and impaired imprinting of DLX5 in Rett syndrome
Horike, S., Cai, S., Miyano, M., Cheng, J., & Kohwi-shigematsu, T. (2004) · Nature Genetics · doi:10.1038/ng1491 · Cited by 585 · see citing works
McBain, C. J., & Fisahn, A. (2001) · Nature Reviews Neuroscience · doi:10.1038/35049047 · Cited by 581 · see citing works
Alcántara, S., Ruiz, M., D’Arcangelo, G., Ezan, F., de Lecea, L., Curran, T., Sotelo, C., & Soriano, E. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-19-07779.1998 · Cited by 568 · 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
Developmental functions of theDistal-less/Dlx homeobox genes
Panganiban, G. E. F., & Rubenstein, J. L. R. (2002) · Development · doi:10.1242/dev.129.19.4371 · Cited by 522 · see citing works
Self-citationYoung 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
Interneuron Diversity series: Inhibitory interneurons and network oscillations in vitro
Whittington, M. A., & Traub, R. D. (2003) · Trends in Neurosciences · doi:10.1016/j.tins.2003.09.016 · Cited by 497 · see citing works
Wang, Y., Toledo‐Rodriguez, M., Gupta, A., Wu, C., Silberberg, G., Luo, J., & Markram, H. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.073353 · Cited by 491 · see citing works
Three distinct families of GABAergic neurons in rat visual cortex
Gonchar, Y. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.4.347 · Cited by 481 · see citing works
Qiu, M. S., Bulfone, A., Ghattas, I. R., Meneses, J. J., Christensen, L., Sharpe, P. T., Presley, R., Pedersen, R. A., & Rubenstein, J. L. R. (1997) · Developmental Biology · doi:10.1006/dbio.1997.8556 · Cited by 460 · see citing works
Self-citationReduced Inhibition of Dentate Granule Cells in a Model of Temporal Lobe Epilepsy
Kobayashi, M., & Buckmaster, P. S. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-06-02440.2003 · Cited by 394 · see citing works
Qiu, M. S., Bulfone, A., Martı́nez, S., Meneses, J. J., Shimamura, K., Pedersen, R. A., & Rubenstein, J. L. R. (1995) · Genes & Development · doi:10.1101/gad.9.20.2523 · Cited by 374 · see citing works
Self-citationDeFelipe, J. (1993) · Cerebral Cortex · doi:10.1093/cercor/3.4.273 · Cited by 365 · 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
Maccaferri, G., David, J., Roberts, B., Szucs, P., Cottingham, C. A., & Somogyi, P. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.t01-3-00091.x · Cited by 357 · see citing works
Multiple facets of GABAergic neurons and synapses: multiple fates of GABA signalling in epilepsies
Cossart, R., Bernard, C., & Ben‐Ari, Y. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.11.011 · Cited by 340 · see citing works
A model of hippocampal memory encoding and retrieval: GABAergic control of synaptic plasticity
Paulsen, O., & Moser, E. I. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01205-8 · Cited by 338 · see citing works
Powell, E. M., Campbell, D. B., Stanwood, G. D., Davis, C., Noebels, J. L., & Levitt, P. R. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-02-00622.2003 · Cited by 333 · see citing works
Self-citationLevitt, P. R., Eagleson, K. L., & Powell, E. M. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.05.008 · Cited by 331 · see citing works
T HE B IOLOGY OF E PILEPSY G ENES
Noebels, J. L. (2003) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.010302.081210 · Cited by 296 · 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
Self-citationYun, 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
Self-citationNeurotrophins and activity-dependent plasticity of cortical interneurons
Marty, S., da, M., & Berninger, B. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)01026-0 · Cited by 221 · see citing works
Expression from a Dlx Gene Enhancer Marks Adult Mouse Cortical GABAergic Neurons
Stühmer, T. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.1.75 · Cited by 198 · see citing works
Baraban, S. C., & Tallent, M. K. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.01.008 · Cited by 187 · see citing works
Self-citationErbel-Sieler, C., Dudley, C., Zhou, Y., Wu, X., Estill, S. J., Han, T., Diaz-Arrastia, R., Brunskill, E. W., Potter, S. S., & McKnight, S. L. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0405310101 · Cited by 178 · 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
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
Self-citationHistology of the Nervous System
Guillery, R. W. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)80029-4 · Cited by 76 · see citing works
Gonchar, Y., Turney, S. G., Price, J. L., & Burkhalter, A. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1425 · Cited by 52 · see citing works
McBain, C. J., Eaton, J., Brown, T. M., et al. (1992) · Brain Research · doi:10.1016/0006-8993(92)91683-6 · Cited by 42 · see citing works
Saino‐Saito, S., Berlin, R., & Baker, H. A. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10611 · Cited by 31 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
Palop, J. J., Chin, J., Roberson, E. D., Wang, J., Thwin, M. T., Bien-Ly, N., Yoo, J., Ho, K. O., Yu, G.-Q., Kreitzer, A., et al. (2007) · Neuron · doi:10.1016/j.neuron.2007.07.025 · Cited by 1,653 · see citing works
Self-citationThree 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
Autism spectrum disorders: developmental disconnection syndromes
Geschwind, D. H., & Levitt, P. (2007) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2007.01.009 · Cited by 1,411 · see citing works
Interneuron cell types are fit to function
Kepecs, A., & Fishell, G. (2014) · Nature · doi:10.1038/nature12983 · Cited by 1,110 · 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
Self-citationThe 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
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
Postnatal NMDA receptor ablation in corticolimbic interneurons confers schizophrenia-like phenotypes
Belforte, J. E., Zsiros, V., Sklar, E. R., Jiang, Z., Yu, G., Li, Y., Quinlan, E. M., & Nakazawa, K. (2010) · Nature Neuroscience · doi:10.1038/nn.2447 · Cited by 752 · see citing works
Feng, J., Bi, C., Clark, B. S., Mady, R., Shah, P., & Kohtz, J. D. (2006) · Genes & Development · doi:10.1101/gad.1416106 · Cited by 712 · 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
Mechanisms of epileptogenesis: a convergence on neural circuit dysfunction
Goldberg, E. M., & Coulter, D. A. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3482 · Cited by 542 · 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
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
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
Bortone, D., & Polleux, F. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.034 · Cited by 387 · see citing works
Gonchar, Y. (2008) · Frontiers in Neuroanatomy · doi:10.3389/neuro.05.003.2007 · Cited by 369 · 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
Self-citationCheah, C. S., Yu, F. H., Westenbroek, R. E., Kalume, F. K., Oakley, J. C., Potter, G. B., Rubenstein, J. L., & Catterall, W. A. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1211591109 · Cited by 336 · see citing works
Self-citationGenetic 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
Hashemi, E., Ariza, J., Rogers, H., Noctor, S. C., & Martínez-Cerdeño, V. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw021 · Cited by 322 · 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
CXCR4 and CXCR7 Have Distinct Functions in Regulating Interneuron Migration
Wang, Y., Li, G., Stanco, A., Long, J. E., Crawford, D., Potter, G. B., Pleasure, S. J., Behrens, T., & Rubenstein, J. L. R. (2011) · Neuron · doi:10.1016/j.neuron.2010.12.005 · Cited by 290 · see citing works
Self-citationA Blueprint for the Spatiotemporal Origins of Mouse Hippocampal Interneuron Diversity
Tricoire, L., Pelkey, K. A., Erkkila, B. E., Jeffries, B. W., Yuan, X., & McBain, C. J. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0323-11.2011 · Cited by 292 · see citing works
Pyramidal cell regulation of interneuron survival sculpts cortical networks
Wong, F. K., Bercsenyi, K., Sreenivasan, V., Portalés, A., Fernández-Otero, M., & Marín, O. (2018) · Nature · doi:10.1038/s41586-018-0139-6 · Cited by 286 · see citing works
Nakajima, M., Görlich, A., & Heintz, N. (2014) · Cell · doi:10.1016/j.cell.2014.09.020 · Cited by 262 · see citing works
Shining a light on CNTNAP2: Complex functions to complex disorders
Rodenas-Cuadrado, P., Ho, J., & Vernes, S. C. (2014) · European Journal of Human Genetics · doi:10.1038/ejhg.2013.100 · Cited by 272 · see citing works
Oskvig, D. B., Elkahloun, A. G., Johnson, K. R., Phillips, T. M., & Herkenham, M. (2012) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2012.01.015 · Cited by 248 · see citing works
Inhibitory Interneurons Regulate Temporal Precision and Correlations in Cortical Circuits
Cardin, J. A. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.07.015 · Cited by 254 · 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
Miyoshi, G., & Fishell, G. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq155 · Cited by 230 · see citing works
Three hypotheses for developmental defects that may underlie some forms of autism spectrum disorder
Rubenstein, J. L. (2010) · Current Opinion in Neurology · doi:10.1097/wco.0b013e328336eb13 · 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
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
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
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
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
Self-citationBrain adaptation and alternative developmental trajectories
Johnson, M. H., Jones, E. J. H., & Gliga, T. (2015) · Development and Psychopathology · doi:10.1017/s0954579415000073 · Cited by 213 · 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
Tepe, B., Hill, M. C., Pekarek, B. T., Hunt, P. J., Martin, T. J., Martin, J. F., & Arenkiel, B. R. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.11.034 · Cited by 183 · see citing works
Adenosine receptor antagonists including caffeine alter fetal brain development in mice
Silva, C. G., Métin, C., Fazeli, W., Machado, N. J., Darmopil, S., Launay, P.-S., Ghestem, A., Nesa, M.-P., Bassot, E., Szabó, E., et al. (2013) · Science Translational Medicine · doi:10.1126/scitranslmed.3006258 · Cited by 177 · see citing works
Inan, M., Welagen, J., & Anderson, S. A. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhr148 · Cited by 161 · see citing works
Genomic Perspectives of Transcriptional Regulation in Forebrain Development
Nord, A. S., Pattabiraman, K., Visel, A., & Rubenstein, J. L. R. (2015) · Neuron · doi:10.1016/j.neuron.2014.11.011 · Cited by 152 · see citing works
Self-citationColasante, 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
Self-citationClose, 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
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
Self-citationMiyoshi, 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
The organization of the transcriptional network in specific neuronal classes
Winden, K. D., Oldham, M. C., Mirnics, K., Ebert, P. J., Swan, C. H., Levitt, P., Rubenstein, J. L., Horvath, S., & Geschwind, D. H. (2009) · Molecular Systems Biology · doi:10.1038/msb.2009.46 · Cited by 112 · see citing works
Self-citationRossignol, E., Kruglikov, I., van den Maagdenberg, A. M. J. M., Rudy, B., & Fishell, G. (2013) · Annals of Neurology · doi:10.1002/ana.23913 · Cited by 112 · 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
Leung, L., Andrews-Zwilling, Y., Yoon, S. Y., Jain, S., Ring, K., Dai, J., Wang, M. M., Tong, L., Walker, D., & Huang, Y. (2012) · PLoS ONE · doi:10.1371/journal.pone.0053569 · Cited by 109 · see citing works
GABAergic 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
Selective cortical interneuron and GABA deficits in cyclin D2-null mice
Glickstein, S. B., Moore, H., Slowinska, B., Racchumi, J., Suh, M., Chuhma, N., & Ross, M. E. (2007) · Development · doi:10.1242/dev.008524 · Cited by 89 · see citing works
The role of interneurons in autism and Tourette Syndrome
Rapanelli, M., Frick, L. R., & Pittenger, C. (2017) · Trends in Neurosciences · doi:10.1016/j.tins.2017.05.004 · Cited by 93 · see citing works
Loss of Gsx1 and Gsx2 function rescues distinct phenotypes in Dlx1/2 mutants
Wang, B., Long, J. E., Flandin, P., Pla, R., Waclaw, R. R., Campbell, K., & Rubenstein, J. L. R. (2013) · Journal of Comparative Neurology · doi:10.1002/cne.23242 · Cited by 85 · 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
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
Self-citationPangratz-Fuehrer, S., & Hestrin, S. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6655-10.2011 · Cited by 83 · see citing works
Revisiting enigmatic cortical calretinin-expressing interneurons
Cauli, B., Zhou, X., Tricoire, L., Toussay, X., & Staiger, J. F. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00052 · Cited by 86 · see citing works
Cajigas, I., Chakraborty, A., Swyter, K. R., Luo, H., Bastidas, M., Nigro, M., Morris, E. R., Chen, S., VanGompel, M. J. W., Leib, D., et al. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.07.024 · Cited by 82 · see citing works
Functional Access to Neuron Subclasses in Rodent and Primate Forebrain
Mehta, P., Kreeger, L., Wylie, D. C., Pattadkal, J. J., Lusignan, T., Davis, M. J., Turi, G. F., Li, W.-K., Whitmire, M. P., Chen, Y., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.02.011 · Cited by 67 · see citing works
TBR1 regulates autism risk genes in the developing neocortex
Notwell, J. H., Heavner, W. E., Darbandi, S. F., Katzman, S., McKenna, W. L., Ortiz-Londono, C. F., Tastad, D., Eckler, M. J., Rubenstein, J. L. R., McConnell, S. K., et al. (2016) · Genome Research · doi:10.1101/gr.203612.115 · Cited by 74 · see citing works
Self-citationZimmer, G., Rudolph, J., Landmann, J., Gerstmann, K., Steinecke, A., Gampe, C., & Bolz, J. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.4690-11.2011 · Cited by 68 · see citing works
An SNP in an ultraconserved regulatory element affects <i>Dlx5/Dlx6</i> regulation in the forebrain
Poitras, L., Yu, M., Lesage-Pelletier, C., MacDonald, R. B., Gagné, J.-P., Hatch, G., Kelly, I., Hamilton, S. P., Rubenstein, J. L. R., Poirier, G. G., et al. (2010) · Development · doi:10.1242/dev.051052 · Cited by 69 · 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
Inda, M. C., DeFelipe, J., & Munoz, A. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn057 · Cited by 51 · see citing works
Functional consequences of I56ii Dlx enhancer deletion in the developing mouse forebrain
Fazel Darbandi, S., Poitras, L., Monis, S., Lindtner, S., Yu, M., Hatch, G., Rubenstein, J. L., & Ekker, M. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.10.015 · Cited by 18 · see citing works
Self-citationNeuronal migration and its disorders affecting the CA3 region
Belvindrah, R., Nosten-Bertrand, M., & Francis, F. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00063 · Cited by 18 · see citing works
- Authors
- Cobos, I., Calcagnotto, M. E., Vilaythong, A. J., Thwin, M. T., Noebels, J. L., Baraban, S. C., & Rubenstein, J. L. R.
- Affiliations
- University of California, San Francisco (US)
- Baylor College of Medicine (US)
- Corresponding author
- Cobos, Inma
- Rubenstein, John L R
- Venue
- Nature Neuroscience
- Published
- 2005-07-10
- Volume
- 8
- Issue
- 8
- Pages
- 1059-1068
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W2005402594
- Cited by
- 502
- References
- 50
- Citations by year
- 2026: 8 · 2025: 10 · 2024: 15 · 2023: 15 · 2022: 20 · 2021: 17 · 2020: 14 · 2019: 20 · 2018: 25 · 2017: 28 · 2016: 16 · 2015: 23 · 2014: 30 · 2013: 38 · 2012: 31
- FWCI
- 15.31
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (R01MH49428, K05MH065670, R01MH049428)
- National Institute of Neurological Disorders and Stroke (R01 NS40272, R01NS040272, NS29709, R01NS029709)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD 24064, P30HD024064)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Epilepsy research and treatment
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- DLX1, GABAergic interneurons, interneuron loss, calretinin, somatostatin, parvalbumin, inhibitory postsynaptic currents, cell-autonomous function, cell transplantation, hippocampus, neocortex
- MeSH terms
- Aging, Animals, Behavior, Animal, Brain, Cell Count, Cerebral Cortex, Epilepsy, gamma-Aminobutyric Acid, Interneurons, Neural Inhibition, Neurons, Synapses, Transcription Factors, Apoptosis, Gene Deletion, Mice, Knockout, Homeodomain Proteins, Mice
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