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Chapter 8 - Ontogeny of Thalamic GABAergic Neurons

from Section 4: - Development

Published online by Cambridge University Press:  12 August 2022

By
Alessio Delogu
Edited by
Michael M. Halassa
Michael M. Halassa
Affiliation:
Massachusetts Institute of Technology
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Summary

GABAergic interneurons are present in the thalamus of amniotes to provide local inhibition and potentially contribute to the pacing of thalamocortical network activity. However, it has long been known that the density of GABAergic interneurons varies greatly between thalamocortical subdivisions among animal species. In mammals, the GABAergic interneurons that are invariantly found in the visual areas of the thalamus are very rare in other sensory and associative regions in rodents but not in carnivores and primates. Are GABAergic interneurons dispensable for the faithful relay of sensory information? Are there different interneuron types allocated to thalamocortical hierarchies and sensory modalities? Are thalamic interneurons the product of evolutionarily conserved differentiation programmes, or do they represent examples of convergence and novelty in evolution? Important clues for answering these open questions may come from an understanding of the genesis of thalamic GABAergic neurons in different species. Neuronal cell fate in the embryonic thalamic primordium is overwhelmingly of the glutamatergic type. Recent research identified multiple extra-thalamic sources of thalamic interneurons, suggesting that the correct cellular assembly of the thalamus also depends on the species-specific maturation of other regions of the brain.

Keywords

GABAinterneuronsprosomeresforebrainmidbrainneurogenesiscell fatelineage identitytranscription factorsintergeniculate leafletthalamocortical nuclei
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Chapter
Information
The Thalamus , pp. 163 - 186
Publisher: Cambridge University Press
Print publication year: 2022

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References

Achim, K., Peltopuro, P., Lahti, L., Li, J., Salminen, M., and Partanen, J. (2012). Distinct developmental origins and regulatory mechanisms for GABAergic neurons associated with dopaminergic nuclei in the ventral mesodiencephalic region. Development 139, 2360–2370.Google Scholar
Achim, K., Peltopuro, P., Lahti, L., Tsai, H.H., Zachariah, A., Astrand, M., Salminen, M., Rowitch, D., and Partanen, J. (2013). The role of Tal2 and Tal1 in the differentiation of midbrain GABAergic neuron precursors. Biol Open 2, 990–997.Google Scholar
Acuna-Goycolea, C., Brenowitz, S.D., and Regehr, W.G. (2008). Active dendritic conductances dynamically regulate GABA release from thalamic interneurons. Neuron 57, 420–431.CrossRefGoogle ScholarPubMed
Agoston, Z., and Schulte, D. (2009). Meis2 competes with the Groucho co-repressor Tle4 for binding to Otx2 and specifies tectal fate without induction of a secondary midbrain-hindbrain boundary organizer. Development 136, 3311–3322.Google Scholar
Albuixech-Crespo, B., Lopez-Blanch, L., Burguera, D., Maeso, I., Sanchez-Arrones, L., Moreno-Bravo, J.A., Somorjai, I., Pascual-Anaya, J., Puelles, E., Bovolenta, P., et al. (2017). Molecular regionalization of the developing amphioxus neural tube challenges major partitions of the vertebrate brain. PLoS Biol 15, e2001573.CrossRefGoogle ScholarPubMed
Altman, J., and Bayer, S.A. (1988a). Development of the rat thalamus: I. Mosaic organization of the thalamic neuroepithelium. J Comp Neurol 275, 346–377.Google Scholar
Altman, J., and Bayer, S.A. (1988b). Development of the rat thalamus: II. Time and site of origin and settling pattern of neurons derived from the anterior lobule of the thalamic neuroepithelium. J Comp Neurol 275, 378–405.Google Scholar
Altman, J., and Bayer, S.A. (1988c). Development of the rat thalamus: III. Time and site of origin and settling pattern of neurons of the reticular nucleus. J Comp Neurol 275, 406–428.Google Scholar
Altman, J., and Bayer, S.A. (1989a). Development of the rat thalamus: IV. The intermediate lobule of the thalamic neuroepithelium, and the time and site of origin and settling pattern of neurons of the ventral nuclear complex. J Comp Neurol 284, 534–566.CrossRefGoogle ScholarPubMed
Altman, J., and Bayer, S.A. (1989b). Development of the rat thalamus: V. The posterior lobule of the thalamic neuroepithelium and the time and site of origin and settling pattern of neurons of the medial geniculate body. J Comp Neurol 284, 567–580.Google Scholar
Altman, J., and Bayer, S.A. (1989c). Development of the rat thalamus: VI. The posterior lobule of the thalamic neuroepithelium and the time and site of origin and settling pattern of neurons of the lateral geniculate and lateral posterior nuclei. J Comp Neurol 284, 581–601.Google Scholar
An, K., Zhao, H., Miao, Y., Xu, Q., Li, Y.F., Ma, Y.Q., Shi, Y.M., Shen, J.W., Meng, J.J., Yao, Y.G., et al. (2020). A circadian rhythm-gated subcortical pathway for nighttime-light-induced depressive-like behaviors in mice. Nat Neurosci 23, 869–880.Google Scholar
Anderson, S.A., Eisenstat, D.D., Shi, L., and Rubenstein, J.L. (1997a). Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278, 474–476.Google Scholar
Anderson, S.A., Qiu, M., Bulfone, A., Eisenstat, D.D., Meneses, J., Pedersen, R., and Rubenstein, J.L. (1997b). Mutations of the homeobox genes Dlx-1 and Dlx-2 disrupt the striatal subventricular zone and differentiation of late born striatal neurons. Neuron 19, 27–37.CrossRefGoogle ScholarPubMed
Angevine, J.B., Jr. (1970). Time of neuron origin in the diencephalon of the mouse. An autoradiographic study. J Comp Neurol 139, 129–187.CrossRefGoogle ScholarPubMed
Anton-Bolanos, N., Espinosa, A., and Lopez-Bendito, G. (2018). Developmental interactions between thalamus and cortex: a true love reciprocal story. Curr Opin Neurobiol 52, 33–41.Google Scholar
Anton-Bolanos, N., Sempere-Ferrandez, A., Guillamon-Vivancos, T., Martini, F.J., Perez-Saiz, L., Gezelius, H., Filipchuk, A., Valdeolmillos, M., and Lopez-Bendito, G. (2019). Prenatal activity from thalamic neurons governs the emergence of functional cortical maps in mice. Science 364, 987–990.CrossRefGoogle ScholarPubMed
Arcelli, P., Frassoni, C., Regondi, M.C., De Biasi, S., and Spreafico, R. (1997). GABAergic neurons in mammalian thalamus: a marker of thalamic complexity? Brain Research Bulletin 42, 27–37.CrossRefGoogle ScholarPubMed
Arimura, N., Dewa, K.I., Okada, M., Yanagawa, Y., Taya, S.I., and Hoshino, M. (2019). Comprehensive and cell-type-based characterization of the dorsal midbrain during development. Genes Cells 24, 41–59.CrossRefGoogle ScholarPubMed
Babb, R.S. (1980). The pregeniculate nucleus of the monkey (Macaca mulatta). I. A study at the light microscopy level. J Comp Neurol 190, 651–672.Google Scholar
Bakken, T.E., van Velthoven, C.T.J., Menon, V., Hodge, R.D., Yao, Z., Nguyen, T.N., Graybuck, L.T., Horwitz, G.D., Bertagnolli, D., Goldy, J., et al. (2020). Single-cell RNA-seq uncovers shared and distinct axes of variation in dorsal LGN neurons in mice, non-human primates and humans. bioRxiv.Google Scholar
Batini, C., Guegan, M., Palestini, M., and Thomasset, M. (1991). The immunocytochemical distribution of calbindin-D28k and parvalbumin in identified neurons of the pulvinar-lateralis posterior complex of the cat. Neurosci Lett 130, 203–207.Google Scholar
Beier, C., Zhang, Z., Yurgel, M., and Hattar, S. (2020). The projections of ipRGCs and conventional RGCs to retinorecipient brain nuclei. bioRxiv.CrossRefGoogle Scholar
Benson, D.L., Isackson, P.J., Gall, C.M., and Jones, E.G. (1992). Contrasting patterns in the localization of glutamic acid decarboxylase and Ca2+/calmodulin protein kinase gene expression in the rat central nervous system. Neuroscience 46, 825–849.CrossRefGoogle ScholarPubMed
Benson, D.L., Isackson, P.J., Hendry, S.H., and Jones, E.G. (1991). Differential gene expression for glutamic acid decarboxylase and type II calcium-calmodulin-dependent protein kinase in basal ganglia, thalamus, and hypothalamus of the monkey. J Neurosci 11, 1540–1564.Google Scholar
Bentivoglio, M., Spreafico, R., Minciacchi, D., and Macchi, G. (1991). GABAergic interneurons and neuropil of the intralaminar thalamus: an immunohistochemical study in the rat and the cat, with notes in the monkey. Exp Brain Res 87, 85–95.Google Scholar
Bickford, M.E., Carden, W.B., and Patel, N.C. (1999). Two types of interneurons in the cat visual thalamus are distinguished by morphology, synaptic connections, and nitric oxide synthase content. J Comp Neurol 413, 83–100.3.0.CO;2-E>CrossRefGoogle ScholarPubMed
Bickford, M.E., Slusarczyk, A., Dilger, E.K., Krahe, T.E., Kucuk, C., and Guido, W. (2010). Synaptic development of the mouse dorsal lateral geniculate nucleus. J Comp Neurol 518, 622–635.Google Scholar
Blasiak, T., and Lewandowski, M.H. (2003). Dorsal raphe nucleus modulates neuronal activity in rat intergeniculate leaflet. Behav Brain Res 138, 179–185.CrossRefGoogle ScholarPubMed
Blitz, D.M., and Regehr, W.G. (2005). Timing and specificity of feed-forward inhibition within the LGN. Neuron 45, 917–928.CrossRefGoogle ScholarPubMed
Bluske, K.K., Kawakami, Y., Koyano-Nakagawa, N., and Nakagawa, Y. (2009). Differential activity of Wnt/beta-catenin signaling in the embryonic mouse thalamus. Dev Dyn 238, 3297–3309.Google Scholar
Bluske, K.K., Vue, T.Y., Kawakami, Y., Taketo, M.M., Yoshikawa, K., Johnson, J.E., and Nakagawa, Y. (2012). beta-Catenin signaling specifies progenitor cell identity in parallel with Shh signaling in the developing mammalian thalamus. Development 139, 2692–2702.Google Scholar
Bokor, H., Frere, S.G., Eyre, M.D., Slezia, A., Ulbert, I., Luthi, A., and Acsady, L. (2005). Selective GABAergic control of higher-order thalamic relays. Neuron 45, 929–940.Google Scholar
Born, G., and Schmidt, M. (2007). GABAergic pathways in the rat subcortical visual system: a comparative study in vivo and in vitro. Eur J Neurosci 26, 1183–1192.CrossRefGoogle ScholarPubMed
Braak, H., and Bachmann, A. (1985). The percentage of projection neurons and interneurons in the human lateral geniculate nucleus. Hum Neurobiol 4, 91–95.Google Scholar
Braak, H., and Braak, E. (1984). Neuronal types in the lateral geniculate nucleus of man. A Golgi-pigment study. Cell Tissue Res 237, 509–520.Google ScholarPubMed
Braak, H., and Weinel, U. (1985). The percentage of projection neurons and local circuit neurons in different nuclei of the human thalamus. J Hirnforsch 26, 525–530.Google Scholar
Bradley, C.K., Takano, E.A., Hall, M.A., Gothert, J.R., Harvey, A.R., Begley, C.G., and van Eekelen, J.A. (2006). The essential haematopoietic transcription factor Scl is also critical for neuronal development. Eur J Neurosci 23, 1677–1689.CrossRefGoogle ScholarPubMed
Brooks, J.M., Su, J., Levy, C., Wang, J.S., Seabrook, T.A., Guido, W., and Fox, M.A. (2013). A molecular mechanism regulating the timing of corticogeniculate innervation. Cell Rep 5, 573–581.Google Scholar
Brown, N.L., Patel, S., Brzezinski, J., and Glaser, T. (2001). Math5 is required for retinal ganglion cell and optic nerve formation. Development 128, 2497–2508.Google Scholar
Bucher, K., Sofroniew, M.V., Pannell, R., Impey, H., Smith, A.J., Torres, E.M., Dunnett, S.B., Jin, Y., Baer, R., and Rabbitts, T.H. (2000). The T cell oncogene Tal2 is necessary for normal development of the mouse brain. Dev Biol 227, 533–544.CrossRefGoogle Scholar
Bulfone, A., Puelles, L., Porteus, M.H., Frohman, M.A., Martin, G.R., and Rubenstein, J.L. (1993). Spatially restricted expression of Dlx-1, Dlx-2 (Tes-1), Gbx-2, and Wnt-3 in the embryonic day 12.5 mouse forebrain defines potential transverse and longitudinal segmental boundaries. J Neurosci 13, 3155–3172.Google Scholar
Butler, A.B. (2008). Evolution of the thalamus: a morphological and functional review. In Thalamus & Related Systems (Cambridge University Press), pp. 35–58.Google Scholar
Butt, S.J., Sousa, V.H., Fuccillo, M.V., Hjerling-Leffler, J., Miyoshi, G., Kimura, S., and Fishell, G. (2008). The requirement of Nkx2-1 in the temporal specification of cortical interneuron subtypes. Neuron 59, 722–732.CrossRefGoogle ScholarPubMed
Bylund, M., Andersson, E., Novitch, B.G., and Muhr, J. (2003). Vertebrate neurogenesis is counteracted by Sox1-3 activity. Nat Neurosci 6, 1162–1168.Google Scholar
Cajal, S.R.y. (1911). Histologie du Systeme Nerveux de l’ Homme et des Vertebres, Vol 2 (Maloine).Google Scholar
Campbell, P.W., Govindaiah, G., Masterson, S.P., Bickford, M.E., and Guido, W. (2020). Synaptic properties of the feedback connections from the thalamic reticular nucleus to the dorsal lateral geniculate nucleus. J Neurophysiol 124, 404–417.CrossRefGoogle Scholar
Carden, W.B., and Bickford, M.E. (2002). Synaptic inputs of class III and class V interneurons in the cat pulvinar nucleus: differential integration of RS and RL inputs. Vis Neurosci 19, 51–59.CrossRefGoogle ScholarPubMed
Carney, R.S., Cocas, L.A., Hirata, T., Mansfield, K., and Corbin, J.G. (2009). Differential regulation of telencephalic pallial-subpallial boundary patterning by Pax6 and Gsh2. Cereb Cortex 19, 745–759.Google Scholar
Casarosa, S., Fode, C., and Guillemot, F. (1999). Mash1 regulates neurogenesis in the ventral telencephalon. Development 126, 525–534.Google Scholar
Castro, D.S., Martynoga, B., Parras, C., Ramesh, V., Pacary, E., Johnston, C., Drechsel, D., Lebel-Potter, M., Garcia, L.G., Hunt, C., et al. (2011). A novel function of the proneural factor Ascl1 in progenitor proliferation identified by genome-wide characterization of its targets. Genes Dev 25, 930–945.Google Scholar
Celio, M.R. (1986). Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. Science 231, 995–997.Google Scholar
Celio, M.R., and Heizmann, C.W. (1981). Calcium-binding protein parvalbumin as a neuronal marker. Nature 293, 300–302.CrossRefGoogle ScholarPubMed
Charalambakis, N.E., Govindaiah, G., Campbell, P.W., and Guido, W. (2019). Developmental remodeling of thalamic interneurons requires retinal signaling. J Neurosci 39, 3856–3866.Google Scholar
Cheadle, L., Tzeng, C.P., Kalish, B.T., Harmin, D.A., Rivera, S., Ling, E., Nagy, M.A., Hrvatin, S., Hu, L., Stroud, H., et al. (2018). Visual experience-dependent expression of Fn14 is required for retinogeniculate refinement. Neuron 99, 525–539, e510.Google Scholar
Clark, A.S., Schwartz, M.L., and Goldman-Rakic, P.S. (1989). GABA-immunoreactive neurons in the mediodorsal nucleus of the monkey thalamus. J Chem Neuroanat 2, 259–267.Google Scholar
Clarke, L.E., and Barres, B.A. (2013). Emerging roles of astrocytes in neural circuit development. Nat Rev Neurosci 14, 311–321.Google Scholar
Cobos, I., Broccoli, V., and Rubenstein, J.L. (2005). The vertebrate ortholog of Aristaless is regulated by Dlx genes in the developing forebrain. J Comp Neurol 483, 292–303.Google Scholar
Colonnese, M.T., and Phillips, M.A. (2018). Thalamocortical function in developing sensory circuits. Curr Opin Neurobiol 52, 72–79.Google Scholar
Corbin, J.G., Rutlin, M., Gaiano, N., and Fishell, G. (2003). Combinatorial function of the homeodomain proteins Nkx2.1 and Gsh2 in ventral telencephalic patterning. Development 130, 4895–4906.Google Scholar
Cox, C.L., and Sherman, S.M. (2000). Control of dendritic outputs of inhibitory interneurons in the lateral geniculate nucleus. Neuron 27, 597–610.Google Scholar
Crossley, P.H., Martinez, S., and Martin, G.R. (1996). Midbrain development induced by FGF8 in the chick embryo. Nature 380, 66–68.CrossRefGoogle ScholarPubMed
Cucchiaro, J.B., Uhlrich, D.J., and Sherman, S.M. (1993). Ultrastructure of synapses from the pretectum in the A-laminae of the cat’s lateral geniculate nucleus. J Comp Neurol 334, 618–630.Google Scholar
Delogu, A., Sellers, K., Zagoraiou, L., Bocianowska-Zbrog, A., Mandal, S., Guimera, J., Rubenstein, J.L., Sugden, D., Jessell, T., and Lumsden, A. (2012). Subcortical visual shell nuclei targeted by ipRGCs develop from a Sox14+-GABAergic progenitor and require Sox14 to regulate daily activity rhythms. Neuron 75, 648–662.Google Scholar
Demeulemeester, H., Arckens, L., Vandesande, F., Orban, G.A., Heizmann, C.W., and Pochet, R. (1991). Calcium binding proteins as molecular markers for cat geniculate neurons. Exp Brain Res 83, 513–520.Google Scholar
Demeulemeester, H., Vandesande, F., Orban, G.A., Heizmann, C.W., and Pochet, R. (1989). Calbindin D-28K and parvalbumin immunoreactivity is confined to two separate neuronal subpopulations in the cat visual cortex, whereas partial coexistence is shown in the dorsal lateral geniculate nucleus. Neurosci Lett 99, 6–11.Google Scholar
Di Giovannantonio, L.G., Di Salvio, M., Omodei, D., Prakash, N., Wurst, W., Pierani, A., Acampora, D., and Simeone, A. (2014). Otx2 cell-autonomously determines dorsal mesencephalon versus cerebellum fate independently of isthmic organizing activity. Development 141, 377–388.Google Scholar
Dixon, G., and Harper, C.G. (2001). Quantitative analysis of glutamic acid decarboxylase-immunoreactive neurons in the anterior thalamus of the human brain. Brain Res 923, 39–44.Google Scholar
Edwards, M.A., Caviness, V.S., Jr., and Schneider, G.E. (1986). Development of cell and fiber lamination in the mouse superior colliculus. J Comp Neurol 248, 395–409.CrossRefGoogle ScholarPubMed
El-Danaf, R.N., Krahe, T.E., Dilger, E.K., Bickford, M.E., Fox, M.A., and Guido, W. (2015). Developmental remodeling of relay cells in the dorsal lateral geniculate nucleus in the absence of retinal input. Neural Dev 10, 19.CrossRefGoogle ScholarPubMed
Erisir, A., Van Horn, S.C., Bickford, M.E., and Sherman, S.M. (1997). Immunocytochemistry and distribution of parabrachial terminals in the lateral geniculate nucleus of the cat: a comparison with corticogeniculate terminals. J Comp Neurol 377, 535–549.Google Scholar
Evangelio, M., García-Amado, M., and Clascá, F. (2018). Thalamocortical projection neuron and interneuron numbers in the visual thalamic nuclei of the adult C57BL/6 mouse. Frontiers in Neuroanatomy 12, 27.Google Scholar
Famiglietti, E.V., Jr. (1970). Dendro-dendritic synapses in the lateral geniculate nucleus of the cat. Brain Res 20, 181–191.Google Scholar
Famiglietti, E.V., Jr., and Peters, A. (1972). The synaptic glomerulus and the intrinsic neuron in the dorsal lateral geniculate nucleus of the cat. J Comp Neurol 144, 285–334.Google Scholar
Feig, S., and Harting, J.K. (1994). Ultrastructural studies of the primate lateral geniculate nucleus: morphology and spatial relationships of axon terminals arising from the retina, visual cortex (area 17), superior colliculus, parabigeminal nucleus, and pretectum of Galago crassicaudatus. J Comp Neurol 343, 17–34.Google Scholar
Fernandez, D.C., Fogerson, P.M., Lazzerini Ospri, L., Thomsen, M.B., Layne, R.M., Severin, D., Zhan, J., Singer, J.H., Kirkwood, A., Zhao, H., et al. (2018). Light affects mood and learning through distinct retina-brain pathways. Cell 175, 71–84 e18.Google Scholar
Fernandez, D.C., Komal, R., Langel, J., Ma, J., Duy, P.Q., Penzo, M.A., Zhao, H., and Hattar, S. (2020). Retinal innervation tunes circuits that drive nonphotic entrainment to food. Nature 581, 194–198.Google Scholar
Fitzpatrick, D., Diamond, I.T., and Raczkowski, D. (1989). Cholinergic and monoaminergic innervation of the cat’s thalamus: comparison of the lateral geniculate nucleus with other principal sensory nuclei. J Comp Neurol 288, 647–675.CrossRefGoogle ScholarPubMed
Fitzpatrick, D., Penny, G.R., and Schmechel, D.E. (1984). Glutamic acid decarboxylase-immunoreactive neurons and terminals in the lateral geniculate nucleus of the cat. J Neurosci 4, 1809–1829.Google Scholar
Fogarty, M., Grist, M., Gelman, D., Marin, O., Pachnis, V., and Kessaris, N. (2007). Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex. J Neurosci 27, 10935–10946.CrossRefGoogle ScholarPubMed
Frangeul, L., Pouchelon, G., Telley, L., Lefort, S., Luscher, C., and Jabaudon, D. (2016). A cross-modal genetic framework for the development and plasticity of sensory pathways. Nature 538, 96–98.CrossRefGoogle ScholarPubMed
Gabbott, P.L., and Bacon, S.J. (1994). Two types of interneuron in the dorsal lateral geniculate nucleus of the rat: a combined NADPH diaphorase histochemical and GABA immunocytochemical study. J Comp Neurol 350, 281–301.Google Scholar
Garcia-Lopez, R., Vieira, C., Echevarria, D., and Martinez, S. (2004). Fate map of the diencephalon and the zona limitans at the 10-somites stage in chick embryos. Dev Biol 268, 514–530.Google Scholar
Geisert, E.E., Jr. (1980). Cortical projections of the lateral geniculate nucleus in the cat. J Comp Neurol 190, 793–812.Google Scholar
Gelman, D., Griveau, A., Dehorter, N., Teissier, A., Varela, C., Pla, R., Pierani, A., and Marin, O. (2011). A wide diversity of cortical GABAergic interneurons derives from the embryonic preoptic area. J Neurosci 31, 16570–16580.CrossRefGoogle ScholarPubMed
Gelman, D.M., Martini, F.J., Nobrega-Pereira, S., Pierani, A., Kessaris, N., and Marin, O. (2009). The embryonic preoptic area is a novel source of cortical GABAergic interneurons. J Neurosci 29, 9380–9389.Google Scholar
Golden, J.A., Zitz, J.C., McFadden, K., and Cepko, C.L. (1997). Cell migration in the developing chick diencephalon. Development 124, 3525–3533.Google Scholar
Golding, B., Pouchelon, G., Bellone, C., Murthy, S., Di Nardo, A.A., Govindan, S., Ogawa, M., Shimogori, T., Lüscher, C., Dayer, A., et al. (2014). Retinal input directs the recruitment of inhibitory interneurons into thalamic visual circuits. Neuron 81, 1057–1069.Google Scholar
Gonzalo-Ruiz, A., Sanz, J.M., and Lieberman, A.R. (1996). Immunohistochemical studies of localization and co-localization of glutamate, aspartate and GABA in the anterior thalamic nuclei, retrosplenial granular cortex, thalamic reticular nucleus and mammillary nuclei of the rat. J Chem Neuroanat 12, 77–84.Google Scholar
Govindaiah, , and Cox, C.L. (2004). Synaptic activation of metabotropic glutamate receptors regulates dendritic outputs of thalamic interneurons. Neuron 41, 611–623.CrossRefGoogle ScholarPubMed
Graham, V., Khudyakov, J., Ellis, P., and Pevny, L. (2003). SOX2 functions to maintain neural progenitor identity. Neuron 39, 749–765.Google Scholar
Grant, E., Hoerder-Suabedissen, A., and Molnar, Z. (2016). The regulation of corticofugal fiber targeting by retinal inputs. Cereb Cortex 26, 1336–1348.Google Scholar
Grimes, W.N., Zhang, J., Graydon, C.W., Kachar, B., and Diamond, J.S. (2010). Retinal parallel processors: more than 100 independent microcircuits operate within a single interneuron. Neuron 65, 873–885.Google Scholar
Guillery, R.W. (1966). A study of Golgi preparations from the dorsal lateral geniculate nucleus of the adult cat. J Comp Neurol 128, 21–50.Google Scholar
Guillery, R.W. (1969). The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus of the cat. Z Zellforsch Mikrosk Anat 96, 1–38.Google Scholar
Guillery, R.W., and Sherman, S.M. (2002). Thalamic relay functions and their role in corticocortical communication: generalizations from the visual system. Neuron 33, 163–175.Google Scholar
Guimera, J., Vogt Weisenhorn, D., Echevarria, D., Martinez, S., and Wurst, W. (2006a). Molecular characterization, structure and developmental expression of Megane bHLH factor. Gene 377, 65–76.Google Scholar
Guimera, J., Weisenhorn, D.V., and Wurst, W. (2006b). Megane/Heslike is required for normal GABAergic differentiation in the mouse superior colliculus. Development 133, 3847–3857.CrossRefGoogle ScholarPubMed
Guler, A.D., Ecker, J.L., Lall, G.S., Haq, S., Altimus, C.M., Liao, H.W., Barnard, A.R., Cahill, H., Badea, T.C., Zhao, H., et al. (2008). Melanopsin cells are the principal conduits for rod-cone input to non-image-forming vision. Nature 453, 102–105.CrossRefGoogle ScholarPubMed
Guo, Q., and Li, J.Y.H. (2019). Defining developmental diversification of diencephalon neurons through single cell gene expression profiling. Development 146.Google Scholar
Hamos, J.E., Van Horn, S.C., Raczkowski, D., Uhlrich, D.J., and Sherman, S.M. (1985). Synaptic connectivity of a local circuit neurone in lateral geniculate nucleus of the cat. Nature 317, 618–621.Google Scholar
Harrington, M.E., and Rusak, B. (1986). Lesions of the thalamic intergeniculate leaflet alter hamster circadian rhythms. J Biol Rhythms 1, 309–325.Google Scholar
Harris, R.M., and Hendrickson, A.E. (1987). Local circuit neurons in the rat ventrobasal thalamus–a GABA immunocytochemical study. Neuroscience 21, 229–236.Google Scholar
Hashikawa, T., Rausell, E., Molinari, M., and Jones, E.G. (1991). Parvalbumin- and calbindin-containing neurons in the monkey medial geniculate complex: differential distribution and cortical layer specific projections. Brain Res 544, 335–341.Google Scholar
Hattar, S., Kumar, M., Park, A., Tong, P., Tung, J., Yau, K.W., and Berson, D.M. (2006). Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J Comp Neurol 497, 326–349.Google Scholar
He, J., Xu, X., Monavarfeshani, A., Banerjee, S., Fox, M.A., and Xie, H. (2019). Retinal-input-induced epigenetic dynamics in the developing mouse dorsal lateral geniculate nucleus. Epigenetics Chromatin 12, 13.Google Scholar
Hendry, S.H., Jones, E.G., Emson, P.C., Lawson, D.E., Heizmann, C.W., and Streit, P. (1989). Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities. Exp Brain Res 76, 467–472.Google Scholar
Henke, R.M., Meredith, D.M., Borromeo, M.D., Savage, T.K., and Johnson, J.E. (2009). Ascl1 and Neurog2 form novel complexes and regulate Delta-like3 (Dll3) expression in the neural tube. Dev Biol 328, 529–540.Google Scholar
Herberth, B., Minko, K., Csillag, A., Jaffredo, T., and Madarasz, E. (2005). SCL, GATA-2 and Lmo2 expression in neurogenesis. Int J Dev Neurosci 23, 449–463.Google Scholar
Herron, P., Baskerville, K.A., Chang, H.T., and Doetsch, G.S. (1997). Distribution of neurons immunoreactive for parvalbumin and calbindin in the somatosensory thalamus of the raccoon. J Comp Neurol 388, 120–129.Google Scholar
Hirata, T., Nakazawa, M., Muraoka, O., Nakayama, R., Suda, Y., and Hibi, M. (2006). Zinc-finger genes Fez and Fez-like function in the establishment of diencephalon subdivisions. Development 133, 3993–4004.CrossRefGoogle ScholarPubMed
Hirsch, J.A., Wang, X., Sommer, F.T., and Martinez, L.M. (2015). How inhibitory circuits in the thalamus serve vision. Annu Rev Neurosci 38, 309–329.Google Scholar
Hong, Y.K., and Chen, C. (2011). Wiring and rewiring of the retinogeniculate synapse. Curr Opin Neurobiol 21, 228–237.Google Scholar
Hsieh-Li, H.M., Witte, D.P., Szucsik, J.C., Weinstein, M., Li, H., and Potter, S.S. (1995). Gsh-2, a murine homeobox gene expressed in the developing brain. Mech Dev 50, 177–186.Google Scholar
Huang, L., Xi, Y., Peng, Y., Yang, Y., Huang, X., Fu, Y., Tao, Q., Xiao, J., Yuan, T., An, K., et al. (2019). A visual circuit related to habenula underlies the antidepressive effects of light therapy. Neuron 102, 128–142 e128.Google Scholar
Huang, X., Huang, P., Huang, L., Hu, Z., Liu, X., Shen, J., Xi, Y., Yang, Y., Fu, Y., Tao, Q., et al. (2021). A visual circuit related to the nucleus reuniens for the spatial-memory-promoting effects of light treatment. Neuron 109, 347–362 e347.Google Scholar
Huberman, A.D., Feller, M.B., and Chapman, B. (2008). Mechanisms underlying development of visual maps and receptive fields. Annu Rev Neurosci 31, 479–509.Google Scholar
Hunt, C.A., Pang, D.Z., and Jones, E.G. (1991). Distribution and density of GABA cells in intralaminar and adjacent nuclei of monkey thalamus. Neuroscience 43, 185–196.Google Scholar
Ilinsky, I.A., Ambardekar, A.V., and Kultas-Ilinsky, K. (1999). Organization of projections from the anterior pole of the nucleus reticularis thalami (NRT) to subdivisions of the motor thalamus: light and electron microscopic studies in the rhesus monkey. J Comp Neurol 409, 369–384.3.0.CO;2-H>CrossRefGoogle ScholarPubMed
Inamura, N., Ono, K., Takebayashi, H., Zalc, B., and Ikenaka, K. (2011). Olig2 lineage cells generate GABAergic neurons in the prethalamic nuclei, including the zona incerta, ventral lateral geniculate nucleus and reticular thalamic nucleus. Dev Neurosci 33, 118–129.Google Scholar
Inverardi, F., Beolchi, M.S., Ortino, B., Moroni, R.F., Regondi, M.C., Amadeo, A., and Frassoni, C. (2007). GABA immunoreactivity in the developing rat thalamus and Otx2 homeoprotein expression in migrating neurons. Brain Res Bull 73, 64–74.Google Scholar
Jager, P., Moore, G., Calpin, P., Durmishi, X., Salgarella, I., Menage, L., Kita, Y., Wang, Y., Kim, D.W., Blackshaw, S., et al. (2021). Dual midbrain and forebrain origins of thalamic inhibitory interneurons. eLife 10.Google Scholar
Jager, P., Ye, Z., Yu, X., Zagoraiou, L., Prekop, H.T., Partanen, J., Jessell, T.M., Wisden, W., Brickley, S.G., and Delogu, A. (2016). Tectal-derived interneurons contribute to phasic and tonic inhibition in the visual thalamus. Nat Commun 7, 13579.Google Scholar
Janik, D., and Mrosovsky, N. (1994). Intergeniculate leaflet lesions and behaviorally-induced shifts of circadian rhythms. Brain Res 651, 174–182.Google Scholar
Jeong, Y., Dolson, D.K., Waclaw, R.R., Matise, M.P., Sussel, L., Campbell, K., Kaestner, K.H., and Epstein, D.J. (2011). Spatial and temporal requirements for sonic hedgehog in the regulation of thalamic interneuron identity. Development 138, 531–541.Google Scholar
Johnson, R.F., Moore, R.Y., and Morin, L.P. (1989). Lateral geniculate lesions alter circadian activity rhythms in the hamster. Brain Res Bull 22, 411–422.Google Scholar
Jones, E. (2002). Dichronous appearance and unusual origins of GABA neurons during development of the mammalian thalamus. Thalamus & Related Systems 1, 283–288.Google Scholar
Jones, E.G. (2007). The Thalamus (Cambridge University Press).Google Scholar
Jones, E.G., and Hendry, S.H. (1989). Differential calcium binding protein immunoreactivity distinguishes classes of relay neurons in monkey thalamic nuclei. Eur J Neurosci 1, 222–246.Google Scholar
Kala, K., Haugas, M., Lillevali, K., Guimera, J., Wurst, W., Salminen, M., and Partanen, J. (2009). Gata2 is a tissue-specific post-mitotic selector gene for midbrain GABAergic neurons. Development 136, 253–262.CrossRefGoogle ScholarPubMed
Kalish, B.T., Cheadle, L., Hrvatin, S., Nagy, M.A., Rivera, S., Crow, M., Gillis, J., Kirchner, R., and Greenberg, M.E. (2018). Single-cell transcriptomics of the developing lateral geniculate nucleus reveals insights into circuit assembly and refinement. Proc Natl Acad Sci USA 115, E1051–E1060.Google Scholar
Kataoka, A., and Shimogori, T. (2008). Fgf8 controls regional identity in the developing thalamus. Development 135, 2873–2881.Google Scholar
Kessaris, N., Fogarty, M., Iannarelli, P., Grist, M., Wegner, M., and Richardson, W.D. (2006). Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat Neurosci 9, 173–179.Google Scholar
Kiecker, C., and Lumsden, A. (2004). Hedgehog signaling from the ZLI regulates diencephalic regional identity. Nat Neurosci 7, 1242–1249.Google Scholar
Kim, D.W., Washington, P.W., Wang, Z.Q., Lin, S.H., Sun, C., Ismail, B.T., Wang, H., Jiang, L., and Blackshaw, S. (2020). The cellular and molecular landscape of hypothalamic patterning and differentiation from embryonic to late postnatal development. Nat Commun 11, 4360.CrossRefGoogle ScholarPubMed
Kimura, S., Hara, Y., Pineau, T., Fernandez-Salguero, P., Fox, C.H., Ward, J.M., and Gonzalez, F.J. (1996). The T/ebp null mouse: thyroid-specific enhancer-binding protein is essential for the organogenesis of the thyroid, lung, ventral forebrain, and pituitary. Genes Dev 10, 60–69.Google Scholar
Kitamura, K., Miura, H., Yanazawa, M., Miyashita, T., and Kato, K. (1997). Expression patterns of Brx1 (Rieg gene), Sonic hedgehog, Nkx2.2, Dlx1 and Arx during zona limitans intrathalamica and embryonic ventral lateral geniculate nuclear formation. Mech Dev 67, 83–96.Google Scholar
Kobayashi, D., Kobayashi, M., Matsumoto, K., Ogura, T., Nakafuku, M., and Shimamura, K. (2002). Early subdivisions in the neural plate define distinct competence for inductive signals. Development 129, 83–93.Google Scholar
Kornhauser, J.M., Leonard, M.W., Yamamoto, M., LaVail, J.H., Mayo, K.E., and Engel, J.D. (1994). Temporal and spatial changes in GATA transcription factor expression are coincident with development of the chicken optic tectum. Brain Res Mol Brain Res 23, 100–110.Google Scholar
Kultas-Ilinsky, K., Yi, H., and Ilinsky, I.A. (1995). Nucleus reticularis thalami input to the anterior thalamic nuclei in the monkey: a light and electron microscopic study. Neurosci Lett 186, 25–28.Google Scholar
Lazzaro, D., Price, M., de Felice, M., and Di Lauro, R. (1991). The transcription factor TTF-1 is expressed at the onset of thyroid and lung morphogenesis and in restricted regions of the foetal brain. Development 113, 1093–1104.Google Scholar
Le, T.N., Zhou, Q.P., Cobos, I., Zhang, S., Zagozewski, J., Japoni, S., Vriend, J., Parkinson, T., Du, G., Rubenstein, J.L., et al. (2017). GABAergic interneuron differentiation in the basal forebrain is mediated through direct regulation of glutamic acid decarboxylase isoforms by Dlx homeobox transcription factors. J Neurosci 37, 8816–8829.Google Scholar
Leist, M., Datunashvilli, M., Kanyshkova, T., Zobeiri, M., Aissaoui, A., Cerina, M., Romanelli, M.N., Pape, H.C., and Budde, T. (2016). Two types of interneurons in the mouse lateral geniculate nucleus are characterized by different h-current density. Sci Rep 6, 24904.Google Scholar
Letinic, K., and Kostovic, I. (1997). Transient fetal structure, the gangliothalamic body, connects telencephalic germinal zone with all thalamic regions in the developing human brain. J Comp Neurol 384, 373–395.Google Scholar
Letinic, K., and Rakic, P. (2001). Telencephalic origin of human thalamic GABAergic neurons. Nat Neurosci 4, 931–936.Google Scholar
Letinic, K., Zoncu, R., and Rakic, P. (2002). Origin of GABAergic neurons in the human neocortex. Nature 417, 645–649.Google Scholar
Lewandowski, M.H., and Usarek, A. (2002). Effects of intergeniculate leaflet lesions on circadian rhythms in the mouse. Behav Brain Res 128, 13–17.Google Scholar
Li, J., Wang, C., Zhang, Z., Wen, Y., An, L., Liang, Q., Xu, Z., Wei, S., Li, W., Guo, T., et al. (2018). Transcription Factors Sp8 and Sp9 coordinately regulate olfactory bulb interneuron development. Cereb Cortex 28, 3278–3294.Google Scholar
Lima, R.R., Pinato, L., Nascimento, R.B., Engelberth, R.C., Nascimento, E.S., Cavalcante, J.C., Britto, L.R., Costa, M.S., and Cavalcante, J.S. (2012). Retinal projections and neurochemical characterization of the pregeniculate nucleus of the common marmoset (Callithrix jacchus). J Chem Neuroanat 44, 34–44.Google Scholar
Lindtner, S., Catta-Preta, R., Tian, H., Su-Feher, L., Price, J.D., Dickel, D.E., Greiner, V., Silberberg, S.N., McKinsey, G.L., McManus, M.T., et al. (2019). Genomic resolution of DLX-orchestrated transcriptional circuits driving development of forebrain GABAergic neurons. Cell Rep 28, 2048–2063 e2048.Google Scholar
Liu, J.K., Ghattas, I., Liu, S., Chen, S., and Rubenstein, J.L. (1997). Dlx genes encode DNA-binding proteins that are expressed in an overlapping and sequential pattern during basal ganglia differentiation. Dev Dyn 210, 498–512.Google Scholar
Long, J.E., Cobos, I., Potter, G.B., and Rubenstein, J.L. (2009). Dlx1&2 and Mash1 transcription factors control MGE and CGE patterning and differentiation through parallel and overlapping pathways. Cereb Cortex 19 Suppl 1, i96–106.Google Scholar
Long, J.E., Garel, S., Alvarez-Dolado, M., Yoshikawa, K., Osumi, N., Alvarez-Buylla, A., and Rubenstein, J.L. (2007). Dlx-dependent and -independent regulation of olfactory bulb interneuron differentiation. J Neurosci 27, 3230–3243.Google Scholar
Long, J.E., Swan, C., Liang, W.S., Cobos, I., Potter, G.B., and Rubenstein, J.L. (2009). Dlx1&2 and Mash1 transcription factors control striatal patterning and differentiation through parallel and overlapping pathways. J Comp Neurol 512, 556–572.Google Scholar
Lumsden, A., and Krumlauf, R. (1996). Patterning the vertebrate neuraxis. Science 274, 1109–1115.Google Scholar
Majorossy, K., and Kiss, A. (1976). Types of interneurons and their participation in the neuronal network of the medial geniculate body. Exp Brain Res 26, 19–37.Google Scholar
Makrides, N., Panayiotou, E., Fanis, P., Karaiskos, C., Lapathitis, G., and Malas, S. (2018). Sequential role of SOXB2 factors in GABAergic neuron specification of the dorsal midbrain. Front Mol Neurosci 11, 152.Google Scholar
Marchant, E.G., Watson, N.V., and Mistlberger, R.E. (1997). Both neuropeptide Y and serotonin are necessary for entrainment of circadian rhythms in mice by daily treadmill running schedules. J Neurosci 17, 7974–7987.Google Scholar
Martinez-Ferre, A., and Martinez, S. (2009). The development of the thalamic motor learning area is regulated by Fgf8 expression. J Neurosci 29, 13389–13400.Google Scholar
Martinez-Ferre, A., and Martinez, S. (2012). Molecular regionalization of the diencephalon. Front Neurosci 6, 73.Google Scholar
Martinez-Ferre, A., Navarro-Garberi, M., Bueno, C., and Martinez, S. (2013). Wnt signal specifies the intrathalamic limit and its organizer properties by regulating Shh induction in the alar plate. J Neurosci 33, 3967–3980.Google Scholar
Mattes, B., Weber, S., Peres, J., Chen, Q., Davidson, G., Houart, C., and Scholpp, S. (2012). Wnt3 and Wnt3a are required for induction of the mid-diencephalic organizer in the caudal forebrain. Neural Dev 7, 12.Google Scholar
McCauley, A.K., Carden, W.B., and Godwin, D.W. (2003). Brain nitric oxide synthase expression in the developing ferret lateral geniculate nucleus: analysis of time course, localization, and synaptic contacts. J Comp Neurol 462, 342–354.Google Scholar
McCormick, D.A., and Pape, H.C. (1988). Acetylcholine inhibits identified interneurons in the cat lateral geniculate nucleus. Nature 334, 246–248.Google Scholar
Meng, X.W., Ohara, P.T., and Ralston, H.J., 3rd (1996). Nitric oxide synthase immunoreactivity distinguishes a sub-population of GABA-immunoreactive neurons in the ventrobasal complex of the cat. Brain Res 728, 111–115.Google Scholar
Meyer-Bernstein, E.L., and Morin, L.P. (1996). Differential serotonergic innervation of the suprachiasmatic nucleus and the intergeniculate leaflet and its role in circadian rhythm modulation. J Neurosci 16, 2097–2111.CrossRefGoogle ScholarPubMed
Minocha, S., Valloton, D., Arsenijevic, Y., Cardinaux, J.R., Guidi, R., Hornung, J.P., and Lebrand, C. (2017). Nkx2.1 regulates the generation of telencephalic astrocytes during embryonic development. Sci Rep 7, 43093.Google Scholar
Minocha, S., Valloton, D., Ypsilanti, A.R., Fiumelli, H., Allen, E.A., Yanagawa, Y., Marin, O., Chedotal, A., Hornung, J.P., and Lebrand, C. (2015). Nkx2.1-derived astrocytes and neurons together with Slit2 are indispensable for anterior commissure formation. Nat Commun 6, 6887.Google Scholar
Miyoshi, G., Bessho, Y., Yamada, S., and Kageyama, R. (2004). Identification of a novel basic helix-loop-helix gene, Heslike, and its role in GABAergic neurogenesis. J Neurosci 24, 3672–3682.Google Scholar
Mojsilovic, J., and Zecevic, N. (1991). Early development of the human thalamus: Golgi and Nissl study. Early Hum Dev 27, 119–144.Google Scholar
Molinari, M., Leggio, M.G., Dell’Anna, M.E., Giannetti, S., and Macchi, G. (1994). Chemical compartmentation and relationships between calcium-binding protein immunoreactivity and layer-specific cortical caudate-projecting cells in the anterior intralaminar nuclei of the cat. Eur J Neurosci 6, 299–312.Google Scholar
Montero, V.M. (1986). Localization of gamma-aminobutyric acid (GABA) in type 3 cells and demonstration of their source to F2 terminals in the cat lateral geniculate nucleus: a Golgi-electron-microscopic GABA-immunocytochemical study. J Comp Neurol 254, 228–245.Google Scholar
Montero, V.M. (1989). The GABA-immunoreactive neurons in the interlaminar regions of the cat lateral geniculate nucleus: light and electron microscopic observations. Exp Brain Res 75, 497–512.Google Scholar
Montero, V.M. (1991). A quantitative study of synaptic contacts on interneurons and relay cells of the cat lateral geniculate nucleus. Exp Brain Res 86, 257–270.Google Scholar
Montero, V.M., and Singer, W. (1985). Ultrastructural identification of somata and neural processes immunoreactive to antibodies against glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the cat. Exp Brain Res 59, 151–165.Google Scholar
Montero, V.M., and Zempel, J. (1985). Evidence for two types of GABA-containing interneurons in the A-laminae of the cat lateral geniculate nucleus: a double-label HRP and GABA-immunocytochemical study. Exp Brain Res 60, 603–609.Google Scholar
Montero, V.M., and Zempel, J. (1986). The proportion and size of GABA-immunoreactive neurons in the magnocellular and parvocellular layers of the lateral geniculate nucleus of the rhesus monkey. Exp Brain Res 62, 215–223.Google Scholar
Moore, R.Y. (1989). The geniculohypothalamic tract in monkey and man. Brain Res 486, 190–194.Google Scholar
Moore, R.Y., Weis, R., and Moga, M.M. (2000). Efferent projections of the intergeniculate leaflet and the ventral lateral geniculate nucleus in the rat. J Comp Neurol 420, 398–418.Google Scholar
Moreno-Juan, V., Filipchuk, A., Anton-Bolanos, N., Mezzera, C., Gezelius, H., Andres, B., Rodriguez-Malmierca, L., Susin, R., Schaad, O., Iwasato, T., et al. (2017). Prenatal thalamic waves regulate cortical area size prior to sensory processing. Nat Commun 8, 14172.Google Scholar
Morest, D.K. (1971). Dendrodendritic synapses of cells that have axons: the fine structure of the Golgi type II cell in the medial geniculate body of the cat. Z Anat Entwicklungsgesch 133, 216–246.Google Scholar
Morgan, J.L., and Lichtman, J.W. (2020). An individual interneuron participates in many kinds of inhibition and innervates much of the mouse visual thalamus. Neuron 106, 468–481 e462.Google Scholar
Mori, S., Sugawara, S., Kikuchi, T., Tanji, M., Narumi, O., Stoykova, A., Nishikawa, S.I., and Yokota, Y. (1999). The leukemic oncogene tal-2 is expressed in the developing mouse brain. Brain Res Mol Brain Res 64, 199–210.Google Scholar
Morin, L.P., and Blanchard, J. (1995). Organization of the hamster intergeniculate leaflet: NPY and ENK projections to the suprachiasmatic nucleus, intergeniculate leaflet and posterior limitans nucleus. Vis Neurosci 12, 57–67.Google Scholar
Morin, L.P., and Blanchard, J.H. (2005). Descending projections of the hamster intergeniculate leaflet: relationship to the sleep/arousal and visuomotor systems. J Comp Neurol 487, 204–216.Google Scholar
Munkle, M.C., Waldvogel, H.J., and Faull, R.L. (2000). The distribution of calbindin, calretinin and parvalbumin immunoreactivity in the human thalamus. J Chem Neuroanat 19, 155–173.Google Scholar
Nakatani, T., Minaki, Y., Kumai, M., and Ono, Y. (2007). Helt determines GABAergic over glutamatergic neuronal fate by repressing Ngn genes in the developing mesencephalon. Development 134, 2783–2793.Google Scholar
Nardelli, J., Thiesson, D., Fujiwara, Y., Tsai, F.Y., and Orkin, S.H. (1999). Expression and genetic interaction of transcription factors GATA-2 and GATA-3 during development of the mouse central nervous system. Dev Biol 210, 305–321.Google Scholar
Nobrega-Pereira, S., Kessaris, N., Du, T., Kimura, S., Anderson, S.A., and Marin, O. (2008). Postmitotic Nkx2-1 controls the migration of telencephalic interneurons by direct repression of guidance receptors. Neuron 59, 733–745.Google Scholar
Ogilvy, S., Ferreira, R., Piltz, S.G., Bowen, J.M., Gottgens, B., and Green, A.R. (2007). The SCL +40 enhancer targets the midbrain together with primitive and definitive hematopoiesis and is regulated by SCL and GATA proteins. Mol Cell Biol 27, 7206–7219.Google Scholar
Ohara, P.T., Chazal, G., and Ralston, H.J., 3rd (1989). Ultrastructural analysis of GABA-immunoreactive elements in the monkey thalamic ventrobasal complex. J Comp Neurol 283, 541–558.Google Scholar
Ohara, P.T., Lieberman, A.R., Hunt, S.P., and Wu, J.Y. (1983). Neural elements containing glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the rat; immunohistochemical studies by light and electron microscopy. Neuroscience 8, 189–211.Google Scholar
Ottersen, O.P., and Storm-Mathisen, J. (1984). GABA-containing neurons in the thalamus and pretectum of the rodent. An immunocytochemical study. Anat Embryol (Berl) 170, 197–207.Google Scholar
Palestini, M., Guegan, M., Saavedra, H., Thomasset, M., and Batini, C. (1993). Glutamate, GABA, calbindin-D28k and parvalbumin immunoreactivity in the pulvinar-lateralis posterior complex of the cat: relation to the projection to the Clare-Bishop area. Neurosci Lett 160, 89–92.CrossRefGoogle Scholar
Pan, Y., and Monje, M. (2020). Activity shapes neural circuit form and function: a historical perspective. J Neurosci 40, 944–954.Google Scholar
Pandolfi, P.P., Roth, M.E., Karis, A., Leonard, M.W., Dzierzak, E., Grosveld, F.G., Engel, J.D., and Lindenbaum, M.H. (1995). Targeted disruption of the GATA3 gene causes severe abnormalities in the nervous system and in fetal liver haematopoiesis. Nat Genet 11, 40–44.CrossRefGoogle ScholarPubMed
Parras, C.M., Schuurmans, C., Scardigli, R., Kim, J., Anderson, D.J., and Guillemot, F. (2002). Divergent functions of the proneural genes Mash1 and Ngn2 in the specification of neuronal subtype identity. Genes Dev 16, 324–338.Google Scholar
Pasik, P., Pasik, T., Hamori, J., and Szentagothai, J. (1973). Golgi type II interneurons in the neuronal circuit of the monkey lateral geniculate nucleus. Exp Brain Res 17, 18–34.Google Scholar
Pei, Z., Wang, B., Chen, G., Nagao, M., Nakafuku, M., and Campbell, K. (2011). Homeobox genes Gsx1 and Gsx2 differentially regulate telencephalic progenitor maturation. Proc Natl Acad Sci USA 108, 1675–1680.Google Scholar
Peltopuro, P., Kala, K., and Partanen, J. (2010). Distinct requirements for Ascl1 in subpopulations of midbrain GABAergic neurons. Dev Biol 343, 63–70.Google Scholar
Penny, G.R., Conley, M., Schmechel, D.E., and Diamond, I.T. (1984). The distribution of glutamic acid decarboxylase immunoreactivity in the diencephalon of the opossum and rabbit. J Comp Neurol 228, 38–56.Google Scholar
Penny, G.R., Fitzpatrick, D., Schmechel, D.E., and Diamond, I.T. (1983). Glutamic acid decarboxylase-immunoreactive neurons and horseradish peroxidase-labeled projection neurons in the ventral posterior nucleus of the cat and Galago senegalensis. J Neurosci 3, 1868–1887.Google Scholar
Perez-Balaguer, A., Puelles, E., Wurst, W., and Martinez, S. (2009). Shh dependent and independent maintenance of basal midbrain. Mech Dev 126, 301–313.Google Scholar
Peters, A., and Palay, S.L. (1966). The morphology of laminae A and A1 of the dorsal nucleus of the lateral geniculate body of the cat. J Anat 100, 451–486.Google Scholar
Petryniak, M.A., Potter, G.B., Rowitch, D.H., and Rubenstein, J.L. (2007). Dlx1 and Dlx2 control neuronal versus oligodendroglial cell fate acquisition in the developing forebrain. Neuron 55, 417–433.Google Scholar
Pleasure, S.J., Anderson, S., Hevner, R., Bagri, A., Marin, O., Lowenstein, D.H., and Rubenstein, J.L. (2000). Cell migration from the ganglionic eminences is required for the development of hippocampal GABAergic interneurons. Neuron 28, 727–740.Google Scholar
Poitras, L., Ghanem, N., Hatch, G., and Ekker, M. (2007). The proneural determinant MASH1 regulates forebrain Dlx1/2 expression through the I12b intergenic enhancer. Development 134, 1755–1765.Google Scholar
Puelles, L. (2019). Survey of midbrain, diencephalon, and hypothalamus neuroanatomic terms whose prosomeric definition conflicts with columnar tradition. Front Neuroanat 13, 20.Google Scholar
Puelles, L., Diaz, C., Stuhmer, T., Ferran, J.L., Martinez-de la Torre, M., and Rubenstein, J.L.R. (2020). LacZ-reporter mapping of Dlx5/6 expression and genoarchitectural analysis of the postnatal mouse prethalamus. J Comp Neurol 529, 367–420.Google Scholar
Puelles, L., Harrison, M., Paxinos, G., and Watson, C. (2013). A developmental ontology for the mammalian brain based on the prosomeric model. Trends Neurosci 36, 570–578.Google Scholar
Puelles, L., and Rubenstein, J.L. (1993). Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization. Trends Neurosci 16, 472–479.Google Scholar
Puelles, L., and Rubenstein, J.L. (2003). Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci 26, 469–476.Google Scholar
Quinlan, R., Graf, M., Mason, I., Lumsden, A., and Kiecker, C. (2009). Complex and dynamic patterns of Wnt pathway gene expression in the developing chick forebrain. Neural Dev 4, 35.Google Scholar
Rakić, P., and Sidman, R.L. (1969). Telencephalic origin of pulvinar neurons in the fetal human brain. Z Anat Entwicklungsgesch 129, 53–82.Google Scholar
Rausell, E., Bae, C.S., Vinuela, A., Huntley, G.W., and Jones, E.G. (1992). Calbindin and parvalbumin cells in monkey VPL thalamic nucleus: distribution, laminar cortical projections, and relations to spinothalamic terminations. J Neurosci 12, 4088–4111.Google Scholar
Rikhye, R.V., Wimmer, R.D., and Halassa, M.M. (2018). Toward an integrative theory of thalamic function. Annu Rev Neurosci 41, 163–183.Google Scholar
Rinvik, E., Ottersen, O.P., and Storm-Mathisen, J. (1987). Gamma-aminobutyrate-like immunoreactivity in the thalamus of the cat. Neuroscience 21, 781–805.Google Scholar
Robertshaw, E., Matsumoto, K., Lumsden, A., and Kiecker, C. (2013). Irx3 and Pax6 establish differential competence for Shh-mediated induction of GABAergic and glutamatergic neurons of the thalamus. Proc Natl Acad Sci USA 110, E3919–3926.Google Scholar
Rubenstein, J.L., Martinez, S., Shimamura, K., and Puelles, L. (1994). The embryonic vertebrate forebrain: the prosomeric model. Science 266, 578–580.Google Scholar
Sabbagh, U., Govindaiah, G., Somaiya, R.D., Ha, R.V., Wei, J.C., Guido, W., and Fox, M.A. (2020). Diverse GABAergic neurons organize into subtype-specific sublaminae in the ventral lateral geniculate nucleus. J Neurochem 159, 479–497.Google Scholar
Sanchez-Vives, M.V., Bal, T., Kim, U., von Krosigk, M., and McCormick, D.A. (1996). Are the interlaminar zones of the ferret dorsal lateral geniculate nucleus actually part of the perigeniculate nucleus? J Neurosci 16, 5923–5941.Google Scholar
Sanders, T.A., Lumsden, A., and Ragsdale, C.W. (2002). Arcuate plan of chick midbrain development. J Neurosci 22, 10742–10750.Google Scholar
Saunders, A., Macosko, E.Z., Wysoker, A., Goldman, M., Krienen, F.M., de Rivera, H., Bien, E., Baum, M., Bortolin, L., Wang, S., et al. (2018). Molecular diversity and specializations among the cells of the adult mouse brain. Cell 174, 1015–1030, e1016.Google Scholar
Sawyer, S.F., Martone, M.E., and Groves, P.M. (1991). A GABA immunocytochemical study of rat motor thalamus: light and electron microscopic observations. Neuroscience 42, 103–124.Google Scholar
Scheibel, M.E., Davies, T.L., and Scheibel, A.B. (1972). On dendrodendritic relations in the dorsal thalamus of the adult cat. Exp Neurol 36, 519–529.Google Scholar
Scholpp, S., Delogu, A., Gilthorpe, J., Peukert, D., Schindler, S., and Lumsden, A. (2009). Her6 regulates the neurogenetic gradient and neuronal identity in the thalamus. Proc Natl Acad Sci USA 106, 19895–19900.Google Scholar
Scholpp, S., Wolf, O., Brand, M., and Lumsden, A. (2006). Hedgehog signalling from the zona limitans intrathalamica orchestrates patterning of the zebrafish diencephalon. Development 133, 855–864.Google Scholar
Seabrook, T.A., Burbridge, T.J., Crair, M.C., and Huberman, A.D. (2017). Architecture, function, and assembly of the mouse visual system. Annu Rev Neurosci 40, 499–538.Google Scholar
Seabrook, T.A., El-Danaf, R.N., Krahe, T.E., Fox, M.A., and Guido, W. (2013a). Retinal input regulates the timing of corticogeniculate innervation. J Neurosci 33, 10085–10097.Google Scholar
Seabrook, T.A., Krahe, T.E., Govindaiah, G., and Guido, W. (2013b). Interneurons in the mouse visual thalamus maintain a high degree of retinal convergence throughout postnatal development. Neural Dev 8, 24.Google Scholar
Sellers, K., Zyka, V., Lumsden, A.G., and Delogu, A. (2014). Transcriptional control of GABAergic neuronal subtype identity in the thalamus. Neural Dev 9, 14.Google Scholar
Shamim, H., Mahmood, R., Logan, C., Doherty, P., Lumsden, A., and Mason, I. (1999). Sequential roles for Fgf4, En1 and Fgf8 in specification and regionalisation of the midbrain. Development 126, 945–959.Google Scholar
Shatz, C.J. (1996). Emergence of order in visual system development. Proc Natl Acad Sci USA 93, 602–608.Google Scholar
Sherman, S.M. (2004). Interneurons and triadic circuitry of the thalamus. Trends Neurosci 27, 670–675.CrossRefGoogle ScholarPubMed
Sherman, S.M., and Guillery, R.W. (1998). On the actions that one nerve cell can have on another: distinguishing “drivers” from “modulators.” Proc Natl Acad Sci USA 95, 7121–7126.Google Scholar
Shi, H.Y., Xu, W., Guo, H., Dong, H., Qu, W.M., and Huang, Z.L. (2020). Lesion of intergeniculate leaflet GABAergic neurons attenuates sleep in mice exposed to light. Sleep 43.Google Scholar
Shi, W., Xianyu, A., Han, Z., Tang, X., Li, Z., Zhong, H., Mao, T., Huang, K., and Shi, S.H. (2017). Ontogenetic establishment of order-specific nuclear organization in the mammalian thalamus. Nat Neurosci 20, 516–528.Google Scholar
Shimamura, K., Hartigan, D.J., Martinez, S., Puelles, L., and Rubenstein, J.L. (1995). Longitudinal organization of the anterior neural plate and neural tube. Development 121, 3923–3933.Google Scholar
Simeone, A., Acampora, D., Pannese, M., D’Esposito, M., Stornaiuolo, A., Gulisano, M., Mallamaci, A., Kastury, K., Druck, T., Huebner, K., et al. (1994). Cloning and characterization of two members of the vertebrate Dlx gene family. Proc Natl Acad Sci USA 91, 2250–2254.Google Scholar
Smith, V.M., Jeffers, R.T., and Antle, M.C. (2015). Serotonergic enhancement of circadian responses to light: role of the raphe and intergeniculate leaflet. Eur J Neurosci 42, 2805–2817.Google Scholar
Smith, Y., Seguela, P., and Parent, A. (1987). Distribution of GABA-immunoreactive neurons in the thalamus of the squirrel monkey (Saimiri sciureus). Neuroscience 22, 579–591.Google Scholar
Sokhadze, G., Seabrook, T.A., and Guido, W. (2018). The absence of retinal input disrupts the development of cholinergic brainstem projections in the mouse dorsal lateral geniculate nucleus. Neural Dev 13, 27.Google Scholar
Song, H., Lee, B., Pyun, D., Guimera, J., Son, Y., Yoon, J., Baek, K., Wurst, W., and Jeong, Y. (2015). Ascl1 and Helt act combinatorially to specify thalamic neuronal identity by repressing Dlxs activation. Dev Biol 398, 280–291.Google Scholar
Spreafico, R., De Biasi, S., Battaglia, G., and Rustioni, A. (1992). GABA- and glutamate-containing neurons in the thalamus of rats and cats: an immunocytochemical study. Epilepsy Res Suppl 8, 107–115.Google Scholar
Spreafico, R., Frassoni, C., Arcelli, P., and De Biasi, S. (1994). GABAergic interneurons in the somatosensory thalamus of the guinea-pig: a light and ultrastructural immunocytochemical investigation. Neuroscience 59, 961–973.Google Scholar
Spreafico, R., Schmechel, D.E., Ellis, L.C., Jr., and Rustioni, A. (1983). Cortical relay neurons and interneurons in the N. ventralis posterolateralis of cats: a horseradish peroxidase, electron-microscopic, Golgi and immunocytochemical study. Neuroscience 9, 491–509.CrossRefGoogle Scholar
Steriade, M. (2004). Local gating of information processing through the thalamus. Neuron 41, 493–494.Google Scholar
Steriade, M., Domich, L., and Oakson, G. (1986). Reticularis thalami neurons revisited: activity changes during shifts in states of vigilance. J Neurosci 6, 68–81.Google Scholar
Sterling, P., and Davis, T.L. (1980). Neurons in cat lateral geniculate nucleus that concentrate exogenous [3H]-gamma-aminobutyric acid (GABA). J Comp Neurol 192, 737–749.Google Scholar
Stichel, C.C., Singer, W., and Heizmann, C.W. (1988). Light and electron microscopic immunocytochemical localization of parvalbumin in the dorsal lateral geniculate nucleus of the cat: evidence for coexistence with GABA. J Comp Neurol 268, 29–37.Google Scholar
Su, J., Charalambakis, N.E., Sabbagh, U., Somaiya, R.D., Monavarfeshani, A., Guido, W., and Fox, M.A. (2020). Retinal inputs signal astrocytes to recruit interneurons into visual thalamus. Proc Natl Acad Sci USA 117, 2671–2682.Google Scholar
Sussel, L., Marin, O., Kimura, S., and Rubenstein, J.L. (1999). Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 126, 3359–3370.Google Scholar
Szentagothai, J. (1967). Models of specific neuron arrays in thalamic relay nuclei. Acta Morphol Acad Sci Hung 15, 113–124.Google Scholar
Szucsik, J.C., Witte, D.P., Li, H., Pixley, S.K., Small, K.M., and Potter, S.S. (1997). Altered forebrain and hindbrain development in mice mutant for the Gsh-2 homeobox gene. Dev Biol 191, 230–242.Google Scholar
Tai, Y., Yi, H., Ilinsky, I.A., and Kultas-Ilinsky, K. (1995). Nucleus reticularis thalami connections with the mediodorsal thalamic nucleus: a light and electron microscopic study in the monkey. Brain Res Bull 38, 475–488.Google Scholar
Tombol, T. (1967). Short neurons and their synaptic relations in the specific thalamic nuclei. Brain Res 3, 307–326.Google Scholar
Toresson, H., Potter, S.S., and Campbell, K. (2000). Genetic control of dorsal-ventral identity in the telencephalon: opposing roles for Pax6 and Gsh2. Development 127, 4361–4371.Google Scholar
Uchikawa, M., Kamachi, Y., and Kondoh, H. (1999). Two distinct subgroups of Group B Sox genes for transcriptional activators and repressors: their expression during embryonic organogenesis of the chicken. Mech Dev 84, 103–120.Google Scholar
Valerius, M.T., Li, H., Stock, J.L., Weinstein, M., Kaur, S., Singh, G., and Potter, S.S. (1995). Gsh-1: a novel murine homeobox gene expressed in the central nervous system. Dev Dyn 203, 337–351.Google Scholar
van Doorninck, J.H., van Der Wees, J., Karis, A., Goedknegt, E., Engel, J.D., Coesmans, M., Rutteman, M., Grosveld, F., and De Zeeuw, C.I. (1999). GATA-3 is involved in the development of serotonergic neurons in the caudal raphe nuclei. J Neurosci 19, RC12.Google Scholar
van Eekelen, J.A., Bradley, C.K., Gothert, J.R., Robb, L., Elefanty, A.G., Begley, C.G., and Harvey, A.R. (2003). Expression pattern of the stem cell leukaemia gene in the CNS of the embryonic and adult mouse. Neuroscience 122, 421–436.Google Scholar
Van Horn, S.C., Erisir, A., and Sherman, S.M. (2000). Relative distribution of synapses in the A-laminae of the lateral geniculate nucleus of the cat. J Comp Neurol 416, 509–520.Google Scholar
Vernay, B., Koch, M., Vaccarino, F., Briscoe, J., Simeone, A., Kageyama, R., and Ang, S.L. (2005). Otx2 regulates subtype specification and neurogenesis in the midbrain. J Neurosci 25, 4856–4867.Google Scholar
Vieira, C., and Martinez, S. (2006). Sonic hedgehog from the basal plate and the zona limitans intrathalamica exhibits differential activity on diencephalic molecular regionalization and nuclear structure. Neuroscience 143, 129–140.Google Scholar
Virolainen, S.M., Achim, K., Peltopuro, P., Salminen, M., and Partanen, J. (2012). Transcriptional regulatory mechanisms underlying the GABAergic neuron fate in different diencephalic prosomeres. Development 139, 3795–3805.Google Scholar
Vrang, N., Mrosovsky, N., and Mikkelsen, J.D. (2003). Afferent projections to the hamster intergeniculate leaflet demonstrated by retrograde and anterograde tracing. Brain Res Bull 59, 267–288.Google Scholar
Vue, T.Y., Aaker, J., Taniguchi, A., Kazemzadeh, C., Skidmore, J.M., Martin, D.M., Martin, J.F., Treier, M., and Nakagawa, Y. (2007). Characterization of progenitor domains in the developing mouse thalamus. J Comp Neurol 505, 73–91.Google Scholar
Vue, T.Y., Bluske, K., Alishahi, A., Yang, L.L., Koyano-Nakagawa, N., Novitch, B., and Nakagawa, Y. (2009). Sonic hedgehog signaling controls thalamic progenitor identity and nuclei specification in mice. J Neurosci 29, 4484–4497.Google Scholar
Waclaw, R.R., Wang, B., Pei, Z., Ehrman, L.A., and Campbell, K. (2009). Distinct temporal requirements for the homeobox gene Gsx2 in specifying striatal and olfactory bulb neuronal fates. Neuron 63, 451–465.Google Scholar
Waite, M.R., Skidmore, J.M., Billi, A.C., Martin, J.F., and Martin, D.M. (2011). GABAergic and glutamatergic identities of developing midbrain Pitx2 neurons. Dev Dyn 240, 333–346.Google Scholar
Wang, B., Waclaw, R.R., Allen, Z.J., 2nd, Guillemot, F., and Campbell, K. (2009). Ascl1 is a required downstream effector of Gsx gene function in the embryonic mouse telencephalon. Neural Dev 4, 5.Google Scholar
Wang, S., Eisenback, M., Datskovskaia, A., Boyce, M., and Bickford, M.E. (2002). GABAergic pretectal terminals contact GABAergic interneurons in the cat dorsal lateral geniculate nucleus. Neurosci Lett 323, 141–145.Google Scholar
Wang, S.W., Kim, B.S., Ding, K., Wang, H., Sun, D., Johnson, R.L., Klein, W.H., and Gan, L. (2001). Requirement for math5 in the development of retinal ganglion cells. Genes Dev 15, 24–29.Google Scholar
Wang, Y., Dye, C.A., Sohal, V., Long, J.E., Estrada, R.C., Roztocil, T., Lufkin, T., Deisseroth, K., Baraban, S.C., and Rubenstein, J.L. (2010). Dlx5 and Dlx6 regulate the development of parvalbumin-expressing cortical interneurons. J Neurosci 30, 5334–5345.Google Scholar
Wang, Y., Li, G., Stanco, A., Long, J.E., Crawford, D., Potter, G.B., Pleasure, S.J., Behrens, T., and Rubenstein, J.L. (2011). CXCR4 and CXCR7 have distinct functions in regulating interneuron migration. Neuron 69, 61–76.Google Scholar
Weber, A.J., and Kalil, R.E. (1983). The percentage of interneurons in the dorsal lateral geniculate nucleus of the cat and observations on several variables that affect the sensitivity of horseradish peroxidase as a retrograde marker. J Comp Neurol 220, 336–346.Google Scholar
Weber, A.J., Kalil, R.E., and Behan, M. (1989). Synaptic connections between corticogeniculate axons and interneurons in the dorsal lateral geniculate nucleus of the cat. J Comp Neurol 289, 156–164.Google Scholar
Weber, A.J., Kalil, R.E., and Hickey, T.L. (1986). Genesis of interneurons in the dorsal lateral geniculate nucleus of the cat. J Comp Neurol 252, 385–391.Google Scholar
Wei, S., Du, H., Li, Z., Tao, G., Xu, Z., Song, X., Shang, Z., Su, Z., Chen, H., Wen, Y., et al. (2019). Transcription factors Sp8 and Sp9 regulate the development of caudal ganglionic eminence-derived cortical interneurons. J Comp Neurol 527, 2860–2874.Google Scholar
Wende, C.Z., Zoubaa, S., Blak, A., Echevarria, D., Martinez, S., Guillemot, F., Wurst, W., and Guimera, J. (2015). Hairy/enhancer-of-split MEGANE and proneural MASH1 factors cooperate synergistically in midbrain GABAergic neurogenesis. PLoS One 10, e0127681.Google Scholar
Willett, R.T., and Greene, L.A. (2011). Gata2 is required for migration and differentiation of retinorecipient neurons in the superior colliculus. J Neurosci 31, 4444–4455.Google Scholar
Williams, S.R., Turner, J.P., Anderson, C.M., and Crunelli, V. (1996). Electrophysiological and morphological properties of interneurones in the rat dorsal lateral geniculate nucleus in vitro. J Physiol 490 (Pt 1), 129–147.Google Scholar
Wilson, J.R. (1986). Synaptic connections of relay and local circuit neurons in the monkey’s dorsal lateral geniculate nucleus. Neurosci Lett 66, 79–84.Google Scholar
Wong, S.Z.H., Scott, E.P., Mu, W., Guo, X., Borgenheimer, E., Freeman, M., Ming, G.L., Wu, Q.F., Song, H., and Nakagawa, Y. (2018). In vivo clonal analysis reveals spatiotemporal regulation of thalamic nucleogenesis. PLoS Biol 16, e2005211.Google Scholar
Xu, Q., Cobos, I., De La Cruz, E., Rubenstein, J.L., and Anderson, S.A. (2004). Origins of cortical interneuron subtypes. J Neurosci 24, 2612–2622.Google Scholar
Xu, Q., Tam, M., and Anderson, S.A. (2008). Fate mapping Nkx2.1-lineage cells in the mouse telencephalon. J Comp Neurol 506, 16–29.Google Scholar
Yoon, M.S., Puelles, L., and Redies, C. (2000). Formation of cadherin-expressing brain nuclei in diencephalic alar plate divisions. J Comp Neurol 427, 461–480.Google Scholar
Yun, K., Fischman, S., Johnson, J., Hrabe de Angelis, M., Weinmaster, G., and Rubenstein, J.L. (2002). Modulation of the notch signaling by Mash1 and Dlx1/2 regulates sequential specification and differentiation of progenitor cell types in the subcortical telencephalon. Development 129, 5029–5040.Google Scholar
Yun, K., Garel, S., Fischman, S., and Rubenstein, J.L. (2003). Patterning of the lateral ganglionic eminence by the Gsh1 and Gsh2 homeobox genes regulates striatal and olfactory bulb histogenesis and the growth of axons through the basal ganglia. J Comp Neurol 461, 151–165.Google Scholar
Yun, K., Potter, S., and Rubenstein, J.L. (2001). Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon. Development 128, 193–205.Google Scholar
Zeisel, A., Hochgerner, H., Lonnerberg, P., Johnsson, A., Memic, F., van der Zwan, J., Haring, M., Braun, E., Borm, L.E., La Manno, G., et al. (2018). Molecular Architecture of the Mouse Nervous System. Cell 174, 999–1014 e1022.Google Scholar
Zhang, Q., Zhang, Y., Wang, C., Xu, Z., Liang, Q., An, L., Li, J., Liu, Z., You, Y., He, M., et al. (2016). The zinc finger transcription factor Sp9 is required for the development of striatopallidal projection neurons. Cell Rep 16, 1431–1444.Google Scholar
Zhao, G.Y., Li, Z.Y., Zou, H.L., Hu, Z.L., Song, N.N., Zheng, M.H., Su, C.J., and Ding, Y.Q. (2008). Expression of the transcription factor GATA3 in the postnatal mouse central nervous system. Neurosci Res 61, 420–428.Google Scholar

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