Genetic and activity-dependent mechanisms underlying interneuron diversity
Abstract
The proper construction of neural circuits requires the generation of diverse cell types, their distribution to defined regions, and their specific and appropriate wiring. A major objective in neurobiology has been to understand the molecular determinants that link neural birth to terminal specification and functional connectivity, a task that is especially daunting in the case of cortical interneurons. Considerable evidence supports the idea that an interplay of intrinsic and environmental signalling is crucial to the sequential steps of interneuron specification, including migration, selection of a settling position, morphogenesis and synaptogenesis. However, when and how these influences merge to support the appropriate terminal differentiation of different classes of interneurons remains uncertain. In this Review, we discuss a wealth of recent findings that have advanced our understanding of the developmental mechanisms that contribute to the diversification of interneurons and suggest areas of particular promise for further investigation.
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Interneurons are generated from progenitors located in the ventral forebrain in transient structures called ganglionic eminences and migrate tangentially to the cortex through different migratory streams.
“Interneurons are generated from progenitors located in the ventral forebrain in transient structures called ganglionic eminences and migrate tangentially to the cortex through different migratory streams85–87.”
From Consequences of trisomy 21 for brain development in Down syndrome (2024) · cites this paper as [87]
Interneuron diversity does not emerge in response to activity-dependent mechanisms in the cortex, but is established early before cells reach the cortex by specific transcriptional programs that unfold over weeks.
“This suggests that interneuron diversity does not emerge in response to activity-dependent mechanisms in the cortex (1, 9), but rather is established early, before these cells reach the cortex, by specific transcriptional programs that then unfold over the course of several weeks.”
From Early emergence of cortical interneuron diversity in the mouse embryo (2018) · cites this paper as [9]
Cites
Hebb, D. O. (2005) · doi:10.4324/9781410612403 · Cited by 9,825 · see citing works
Shrestha, S., & Offer, S. M. (2016) · Medical Epigenetics · doi:10.1159/000444713 · Cited by 8,949 · see citing works
indicated, N. A. (1950) · Journal of Consulting Psychology · doi:10.1037/h0049612 · Cited by 6,984 · see citing works
Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq
Zeisel, A., Muñoz-Manchado, A. B., Codeluppi, S., Lönnerberg, P., La Manno, G., Juréus, A., Marques, S., Munguba, H., He, L., Betsholtz, C., et al. (2015) · Science · doi:10.1126/science.aaa1934 · Cited by 3,124 · see citing works
Monyer, H., Burnashev, N., Laurie, D. J., Sakmann, B., & Seeburg, P. H. (1994) · Neuron · doi:10.1016/0896-6273(94)90210-0 · Cited by 2,989 · 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
GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits
Tremblay, R., Lee, S., & Rudy, B. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.033 · Cited by 2,033 · see citing works
Adult mouse cortical cell taxonomy revealed by single cell transcriptomics
Tasic, B., Menon, V., Nguyen, T. N., Kim, T. K., Jarsky, T., Yao, Z., Levi, B., Gray, L. T., Sorensen, S. A., Dolbeare, T., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4216 · Cited by 1,714 · see citing works
Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex
The Petilla Interneuron Nomenclature Group (PING) (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2402 · Cited by 1,491 · see citing works
Interneuron Migration from Basal Forebrain to Neocortex: Dependence on <i>Dlx</i> Genes
Anderson, S. A., Eisenstat, D. D., Shi, L., & Rubenstein, J. L. R. (1997) · Science · doi:10.1126/science.278.5337.474 · Cited by 1,462 · see citing works
GABA: A Pioneer Transmitter That Excites Immature Neurons and Generates Primitive Oscillations
Ben-Ari, Y., Gaiarsa, J.-L., Tyzio, R., & Khazipov, R. (2007) · Physiological Reviews · doi:10.1152/physrev.00017.2006 · Cited by 1,304 · see citing works
Interneuron dysfunction in psychiatric disorders
Marín, O. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3155 · Cited by 1,190 · see citing works
Changing subunit composition of heteromeric NMDA receptors during development of rat cortex
Sheng, M., Cummings, J., Roldan, L. A., Jan, Y. N., & Jan, L. Y. (1994) · Nature · doi:10.1038/368144a0 · Cited by 1,170 · see citing works
Regulation of Gene Expression in Hippocampal Neurons by Distinct Calcium Signaling Pathways
Bading, H., Ginty, D. D., & Greenberg, M. E. (1993) · Science · doi:10.1126/science.8097060 · Cited by 1,157 · 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
Self-citationGABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis
LoTurco, J. J., Owens, D. F., Heath, M. J. S., Davis, M. B. E., & Kriegstein, A. R. (1995) · Neuron · doi:10.1016/0896-6273(95)90008-x · Cited by 1,064 · 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
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
Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks
Buzsáki, G., & Chrobak, J. J. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80012-3 · Cited by 878 · 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
Mechanisms underlying spontaneous patterned activity in developing neural circuits
Blankenship, A. G., & Feller, M. B. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2759 · Cited by 851 · 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-citationFlavell, S. W., & Greenberg, M. E. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.31.060407.125631 · Cited by 832 · see citing works
Electrical activity in early neuronal development
Spitzer, N. C. (2006) · Nature · doi:10.1038/nature05300 · Cited by 779 · see citing works
A disinhibitory circuit mediates motor integration in the somatosensory cortex
Lee, S., Kruglikov, I., Huang, Z. J., Fishell, G., & Rudy, B. (2013) · Nature Neuroscience · doi:10.1038/nn.3544 · Cited by 758 · see citing works
Self-citationEpigenomic Signatures of Neuronal Diversity in the Mammalian Brain
Mo, A., Mukamel, E. A., Davis, F. P., Luo, C., Henry, G. L., Picard, S., Urich, M. A., Nery, J. R., Sejnowski, T. J., Lister, R., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.05.018 · Cited by 739 · see citing works
Neuronal activity modifies the DNA methylation landscape in the adult brain
Guo, J. U., Ma, D. K., Mo, H., Ball, M. P., Jang, M.-H., Bonaguidi, M. A., Balazer, J. A., Eaves, H. L., Xie, B., Ford, E., et al. (2011) · Nature Neuroscience · doi:10.1038/nn.2900 · Cited by 669 · see citing works
Greer, P. L., & Greenberg, M. E. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.002 · Cited by 661 · see citing works
Chattopadhyaya, B., Di Cristo, G., Higashiyama, H., Knott, G. W., Kuhlman, S. J., Welker, E., & Huang, Z. J. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.1851-04.2004 · Cited by 596 · see citing works
Weissman, T. A., Riquelme, P. A., Ivic, L., Flint, A. C., & Kriegstein, A. R. (2004) · Neuron · doi:10.1016/j.neuron.2004.08.015 · Cited by 579 · 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
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
Neuronal Activity-Dependent Cell Survival Mediated by Transcription Factor MEF2
Mao, Z., Bonni, A., Xia, F., Nadal-Vicens, M. F., & Greenberg, M. E. (1999) · Science · doi:10.1126/science.286.5440.785 · Cited by 505 · see citing works
Mice 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
Large-scale oscillatory calcium waves in the immature cortex
Garaschuk, O., Linn, J., Eilers, J., & Konnerth, A. (2000) · Nature Neuroscience · doi:10.1038/74823 · Cited by 493 · see citing works
Raj, B., & Blencowe, B. J. (2015) · Neuron · doi:10.1016/j.neuron.2015.05.004 · Cited by 475 · 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
Spiegel, I., Mardinly, A. R., Gabel, H. W., Bazinet, J. E., Couch, C. H., Tzeng, C. P., Harmin, D. A., & Greenberg, M. E. (2014) · Cell · doi:10.1016/j.cell.2014.03.058 · Cited by 416 · see citing works
Intracellular Ca2+ Fluctuations Modulate the Rate of Neuronal Migration
Komuro, H., & RAKIC, P. T. (1996) · Neuron · doi:10.1016/s0896-6273(00)80159-2 · Cited by 406 · see citing works
Yu, C., Power, J., Barnea, G., O'Donnell, S., Brown, H. E. V., Osborne, J., Axel, R., & Gogos, J. A. (2004) · Neuron · doi:10.1016/s0896-6273(04)00224-7 · Cited by 392 · see citing works
Bortone, D., & Polleux, F. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.034 · Cited by 387 · 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
DeFelipe, J. (1993) · Cerebral Cortex · doi:10.1093/cercor/3.4.273 · Cited by 365 · see citing works
Intrinsically determined cell death of developing cortical interneurons
Southwell, D. G., Paredes, M. F., Galvao, R. P., Jones, D. L., Froemke, R. C., Sebe, J. Y., Alfaro-Cervello, C., Tang, Y., Garcia-Verdugo, J. M., Rubenstein, J. L., et al. (2012) · Nature · doi:10.1038/nature11523 · Cited by 365 · 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-citationChattopadhyaya, B., Cristo, G. D., Wu, C. Z., Knott, G. W., Kuhlman, S. J., Fu, Y., Palmiter, R. D., & Huang, Z. J. (2007) · Neuron · doi:10.1016/j.neuron.2007.05.015 · Cited by 326 · see citing works
Anderson, S. A. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.6.646 · Cited by 325 · 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-citationLerea, L. S., & McNamara, J. O. (1993) · Neuron · doi:10.1016/0896-6273(93)90239-n · Cited by 284 · see citing works
Sequential Generation of Two Distinct Synapse-Driven Network Patterns in Developing Neocortex
Allène, C., Cattani, A., Ackman, J. B., Bonifazi, P., Aniksztejn, L., Ben-Ari, Y., & Cossart, R. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.3733-08.2008 · Cited by 281 · see citing works
The spatial and temporal origin of chandelier cells in mouse neocortex
Taniguchi, H., Lu, J., & Huang, Z. J. (2013) · Science · doi:10.1126/science.1227622 · Cited by 278 · see citing works
Yang, J.-W., Hanganu-Opatz, I. L., Sun, J.-J., & Luhmann, H. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5646-08.2009 · Cited by 276 · see citing works
Genome-wide identification and characterization of functional neuronal activity–dependent enhancers
Malik, A. N., Vierbuchen, T., Hemberg, M., Rubin, A. A., Ling, E., Couch, C. H., Stroud, H., Spiegel, I., Farh, K. K., Harmin, D. A., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3808 · Cited by 267 · see citing works
Early Gamma Oscillations Synchronize Developing Thalamus and Cortex
Minlebaev, M., Colonnese, M., Tsintsadze, T., Sirota, A., & Khazipov, R. (2011) · Science · doi:10.1126/science.1210574 · Cited by 257 · 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
Lodato, S., Rouaux, C., Quast, K. B., Jantrachotechatchawan, C., Studer, M., Hensch, T. K., & Arlotta, P. (2011) · Neuron · doi:10.1016/j.neuron.2011.01.015 · Cited by 244 · see citing works
Mechanisms of Inhibition within the Telencephalon: “Where the Wild Things Are”
Fishell, G., & Rudy, B. (2011) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-061010-113717 · Cited by 233 · see citing works
Self-citationEarly somatostatin interneuron connectivity mediates the maturation of deep layer cortical circuits
Tuncdemir, S. N., Wamsley, B., Stam, F. J., Osakada, F., Goulding, M., Callaway, E. M., Rudy, B., & Fishell, G. (2016) · Neuron · doi:10.1016/j.neuron.2015.11.020 · Cited by 224 · see citing works
Self-citationA Noncanonical Release of GABA and Glutamate Modulates Neuronal Migration
Manent, J.-B., Demarque, M., Jorquera, I., Pellegrino, C., Ben-Ari, Y., Aniksztejn, L., & Represa, A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0553-05.2005 · Cited by 220 · see citing works
NKX2.1 specifies cortical interneuron fate by activatingLhx6
Du, T., Xu, Q., Ocbina, P. J. R., & Anderson, S. A. (2008) · Development · doi:10.1242/dev.015123 · Cited by 220 · see citing works
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
Inhibitory neurons in human cortical circuits: substrate for cognitive dysfunction in schizophrenia
Lewis, D. A. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.11.003 · Cited by 217 · 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
Self-citationNeuronal activity during development: permissive or instructive?
Crair, M. C. (1999) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)80011-7 · Cited by 203 · 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
The absence of a major Ca <sup>2+</sup> signaling pathway in GABAergic neurons of the hippocampus
Sík, A., Hájos, N., Gulácsi, A., Mody, I., & Freund, T. F. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.6.3245 · Cited by 186 · see citing works
Xu, Q., Wonders, C. P., & Anderson, S. A. (2005) · Development · doi:10.1242/dev.02090 · Cited by 184 · see citing works
A wide diversity of cortical GABAergic interneurons derives from the embryonic preoptic area
Gelman, D., Griveau, A., Dehorter, N., Teissier, A., Varela, C., Pla, R., Pierani, A., & Marín, O. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.4068-11.2011 · Cited by 179 · see citing works
Long, J. E., Cobos, I., Potter, G. B., & Rubenstein, J. L. R. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp045 · Cited by 178 · see citing works
Sensory experience regulates cortical inhibition by inducing IGF1 in VIP neurons
Mardinly, A. R., Spiegel, I., Patrizi, A., Centofante, E., Bazinet, J. E., Tzeng, C. P., Mandel-Brehm, C., Harmin, D. A., Adesnik, H., Fagiolini, M., et al. (2016) · Nature · doi:10.1038/nature17187 · Cited by 176 · see citing works
Connectivity of mouse somatosensory and prefrontal cortex examined with trans-synaptic tracing
DeNardo, L. A., Berns, D. S., DeLoach, K. E., & Luo, L. (2015) · Nature Neuroscience · doi:10.1038/nn.4131 · Cited by 173 · see citing works
Thalamic Network Oscillations Synchronize Ontogenetic Columns in the Newborn Rat Barrel Cortex
Yang, J., An, S., Sun, J., Reyes‐Puerta, V., Kindler, J., Berger, T. K., Kilb, W., & Luhmann, H. J. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs103 · Cited by 171 · see citing works
Tuning of fast-spiking interneuron properties by an activity-dependent transcriptional switch
Dehorter, N., Ciceri, G., Bartolini, G., Lim, L., del Pino, I., & Marín, O. (2015) · Science · doi:10.1126/science.aab3415 · Cited by 169 · see citing works
Major Effects of Sensory Experiences on the Neocortical Inhibitory Circuits
Jiao, Y., Zhang, C., Yanagawa, Y., & Sun, Q. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2478-06.2006 · Cited by 168 · see citing works
NMDA receptors inhibit synapse unsilencing during brain development
Adesnik, H., Li, G., During, M. J., Pleasure, S. J., & Nicoll, R. A. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0800946105 · Cited by 161 · see citing works
Inan, M., Welagen, J., & Anderson, S. A. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhr148 · Cited by 161 · see citing works
Attractive axon guidance involves asymmetric membrane transport and exocytosis in the growth cone
Tojima, T., Akiyama, H., Itofusa, R., Li, Y., Katayama, H., Miyawaki, A., & Kamiguchi, H. (2006) · Nature Neuroscience · doi:10.1038/nn1814 · Cited by 156 · see citing works
Flandin, P., Zhao, Y., Vogt, D., Jeong, J., Long, J., Potter, G., Westphal, H., & Rubenstein, J. L. R. (2011) · Neuron · doi:10.1016/j.neuron.2011.04.020 · Cited by 155 · see citing works
McKinsey, G. L., Lindtner, S., Trzcinski, B., Visel, A., Pennacchio, L. A., Huylebroeck, D., Higashi, Y., & Rubenstein, J. L. R. (2013) · Neuron · doi:10.1016/j.neuron.2012.11.035 · Cited by 153 · see citing works
Clonal production and organization of inhibitory interneurons in the neocortex
Brown, K. N., Chen, S., Han, Z., Lu, C.-H., Tan, X., Zhang, X.-J., Ding, L., Lopez-Cruz, A., Saur, D., Anderson, S. A., et al. (2011) · Science · doi:10.1126/science.1208884 · Cited by 152 · see citing works
Jones, E. G., Huntley, G. W., & Benson, D. L. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-02-00611.1994 · Cited by 141 · 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-citationCalcium Signaling in Synapse-to-Nucleus CommunicationPreprint
Hagenston, A. M., & Bading, H. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a004564 · Cited by 140 · 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
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
Self-citationLineage-specific laminar organization of cortical GABAergic interneurons
Ciceri, G., Dehorter, N., Sols, I., Huang, Z. J., Maravall, M., & Marín, O. (2013) · Nature Neuroscience · doi:10.1038/nn.3485 · Cited by 124 · see citing works
Electrical activity patterns and the functional maturation of the neocortex
Kilb, W., Kirischuk, S., & Luhmann, H. J. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07878.x · Cited by 124 · see citing works
Directed migration of cortical interneurons depends on the cell-autonomous action of Sip1
van den Berghe, V., Stappers, E., Vandesande, B., Dimidschstein, J., Kroes, R., Francis, A., Conidi, A., Lesage, F., Dries, R., Cazzola, S., et al. (2013) · Neuron · doi:10.1016/j.neuron.2012.11.009 · Cited by 120 · see citing works
Self-citationβ-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
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-citationMayer, C., Jaglin, X. H., Cobbs, L. V., Bandler, R. C., Streicher, C., Cepko, C. L., Hippenmeyer, S., & Fishell, G. (2015) · Neuron · doi:10.1016/j.neuron.2015.07.011 · Cited by 113 · see citing works
Self-citationWide dispersion and diversity of clonally related inhibitory interneurons
Harwell, C. C., Fuentealba, L. C., Gonzalez-Cerrillo, A., Parker, P. R. L., Gertz, C. C., Mazzola, E., Garcia, M. T., Alvarez-Buylla, A., Cepko, C. L., & Kriegstein, A. R. (2015) · Neuron · doi:10.1016/j.neuron.2015.07.030 · Cited by 106 · 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
Cohen, S. M., Ma, H., Kuchibhotla, K. V., Watson, B. O., Buzsáki, G., Froemke, R. C., & Tsien, R. W. (2016) · Neuron · doi:10.1016/j.neuron.2016.03.001 · Cited by 100 · see citing works
Mire, E., Mezzera, C., Leyva‐Díaz, E., et al. (2012) · Nature Neuroscience · doi:10.1038/nn.3160 · Cited by 98 · see citing works
Inhibitory Regulation of Dendritic Activity in vivo
Palmer, L. M., Murayama, M., & Larkum, M. E. (2012) · Frontiers in Neural Circuits · doi:10.3389/fncir.2012.00026 · Cited by 82 · see citing works
NPAS1 Represses the Generation of Specific Subtypes of Cortical Interneurons
Stanco, A., Pla, R., Vogt, D. L., Chen, Y., Mandal, S., Walker, J. M., Hunt, R. F., Lindtner, S., Erdman, C. A., Pieper, A. A., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.10.040 · Cited by 71 · see citing works
Exploring the dominant role of Cav1 channels in signalling to the nucleus
Ma, H., Cohen, S., Li, B., & Tsien, R. W. (2012) · Bioscience Reports · doi:10.1042/bsr20120099 · Cited by 68 · see citing works
Muñoz, W., Tremblay, R., & Rudy, B. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.11.042 · Cited by 65 · see citing works
Neves, G., Shah, M. M., Liodis, P., Achimastou, A., Denaxa, M., Roalfe, G., Sesay, A. K., Walker, M. C., & Pachnis, V. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs159 · Cited by 62 · see citing works
Cossart, R. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.10.003 · Cited by 60 · 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
Calcium Dynamics of Neocortical Ventricular Zone Cells
Owens, D. F., Flint, A. C., Dammerman, R. S., & Kriegstein, A. R. (2000) · Developmental Neuroscience · doi:10.1159/000017424 · Cited by 52 · see citing works
The role of firing patterns in neuronal development of sensory systems
Wong, R. (1993) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(93)90061-3 · Cited by 47 · see citing works
Miller, M. N., Okaty, B. W., Kato, S., & Nelson, S. B. (2010) · Developmental Neurobiology · doi:10.1002/dneu.20811 · Cited by 40 · see citing works
Mouse Embryonic Retina Delivers Information Controlling Cortical Neurogenesis
Bonetti, C., & Surace, E. M. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015211 · Cited by 28 · see citing works
Specification 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-citation
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Sohal, V. S., & Rubenstein, J. L. R. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0426-0 · Cited by 988 · 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
“led to very diverging views on the mechanisms controlling the generation of their diversity (Wamsley and Fishell, 2017),”
Temporal patterning of apical progenitors and their daughter neurons in the developing neocortex
Telley, L., Agirman, G., Prados, J., Amberg, N., Fièvre, S., Oberst, P., Bartolini, G., Vitali, I., Cadilhac, C., Hippenmeyer, S., et al. (2019) · Science · doi:10.1126/science.aav2522 · Cited by 423 · see citing works
Phenotypic variation of transcriptomic cell types in mouse motor cortex
Scala, F., Kobak, D., Bernabucci, M., Bernaerts, Y., Cadwell, C. R., Castro, J. R., Hartmanis, L., Jiang, X., Laturnus, S., Miranda, E., et al. (2021) · Nature · doi:10.1038/s41586-020-2907-3 · Cited by 398 · see citing works
Early emergence of cortical interneuron diversity in the mouse embryo
Mi, D., Li, Z., Lim, L., Li, M., Moissidis, M., Yang, Y., Gao, T., Hu, T. X., Pratt, T., Price, D. J., et al. (2018) · Science · doi:10.1126/science.aar6821 · Cited by 259 · see citing works
Neuronal circuits in barrel cortex for whisker sensory perception
Staiger, J. F., & Petersen, C. C. H. (2021) · Physiological Reviews · doi:10.1152/physrev.00019.2019 · Cited by 165 · 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
Optimization of interneuron function by direct coupling of cell migration and axonal targeting
Lim, L., Pakan, J. M. P., Selten, M. M., Marques-Smith, A., Llorca, A., Bae, S. E., Rochefort, N. L., & Marín, O. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0162-9 · Cited by 93 · see citing works
Rotaru, D. C., van Woerden, G. M., Wallaard, I., & Elgersma, Y. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.0083-18.2018 · Cited by 74 · see citing works
Shekhar, K., Whitney, I. E., Butrus, S., Peng, Y.-R., & Sanes, J. R. (2022) · eLife · doi:10.7554/elife.73809 · Cited by 68 · 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
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
Yamagata, T., Ogiwara, I., Mazaki, E., Yanagawa, Y., & Yamakawa, K. (2017) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2017.08.013 · Cited by 57 · see citing works
Micali, N., Kim, S.-K., Diaz-Bustamante, M., Stein-O’Brien, G., Seo, S., Shin, J.-H., Rash, B. G., Ma, S., Wang, Y., Olivares, N. A., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107599 · Cited by 31 · see citing works
Consequences of trisomy 21 for brain development in Down syndrome
Russo, M. L., Sousa, A. M. M., & Bhattacharyya, A. (2024) · Nature Reviews Neuroscience · doi:10.1038/s41583-024-00866-2 · Cited by 28 · see citing works
“…generation of interneurons contributes to the overall reduced neurogenesis in DS. Interneurons are generated from progenitors located in the ventral forebrain in transient structures called ganglionic eminences and migrate tangentially to the cortex through different migratory streams 85–87 .”
Wang, W. X., & Lefebvre, J. L. (2020) · doi:10.1101/2020.02.29.971366
- Authors
- Wamsley, B., & Fishell, G.
- Affiliations
- New York University (US)
- Corresponding author
- Fishell, Gord
- Venue
- Nature Reviews Neuroscience
- Published
- 2017-04-06
- Volume
- 18
- Issue
- 5
- Pages
- 299-309
- ISSN
- 1471-003X (ISSN-L)
- 1471-0048
- OpenAlex
- W2604871800
- Cited by
- 290
- References
- 107
- Citations by year
- 2026: 15 · 2025: 18 · 2024: 32 · 2023: 28 · 2022: 31 · 2021: 40 · 2020: 38 · 2019: 44 · 2018: 33 · 2017: 11
- FWCI
- 5.22
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature reviews. Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (P01NS074972, T32NS086750)
- 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
- cortical interneurons, interneuron specification, interneuron diversity, neural development, interneuron migration, functional connectivity, synaptogenesis, morphogenesis, cell fate determination
- MeSH terms
- Animals, Cell Differentiation, Cerebral Cortex, Humans, Interneurons, Neural Pathways, Neurogenesis
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