Abstract
Neurons using gamma-aminobutyric acid (GABA) as their neurotransmitter are the main inhibitory neurons in the mature central nervous system (CNS) and show great variation in their form and function. GABAergic neurons are produced in all of the main domains of the CNS, where they develop from discrete regions of the neuroepithelium. Here, we review the gene expression and regulatory mechanisms controlling the main steps of GABAergic neuron development: early patterning of the proliferative neuroepithelium, production of postmitotic neural precursors, establishment of their identity and migration. By comparing the molecular regulation of these events across CNS, we broadly identify three regions utilizing distinct molecular toolkits for GABAergic fate determination: telencephalon–anterior diencephalon (DLX2 type), posterior diencephalon–midbrain (GATA2 type) and hindbrain–spinal cord (PTF1A and TAL1 types). Similarities and differences in the molecular regulatory mechanisms reveal the core determinants of a GABAergic neuron as well as provide insights into generation of the vast diversity of these neurons.
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Abbreviations
- AP:
-
Anterior-posterior
- bHLH:
-
Basic helix-loop-helix
- cb:
-
Cerebellum
- CGE:
-
Caudal ganglionic eminence
- CNS:
-
Central nervous system
- CoP:
-
Commissural pretectum (mixed GABAergic and glutamatergic)
- dI4, dI6, dILa:
-
Subpopulations of GABAergic neurons in dorsal spinal cord
- DV:
-
Dorso-ventral
- GABA:
-
Gamma-aminobutyric acid
- hb:
-
Hindbrain
- HD:
-
Homeodomain
- hyp:
-
Hypothalamus
- JcP:
-
Juxtacommissural pretectum (GABAergic)
- LGE:
-
Lateral ganglionic eminence
- mb:
-
Midbrain
- m1–m5:
-
Progenitor domains producing GABAergic neurons in midbrain
- MGE:
-
Medial ganglionic eminence
- MHB:
-
Midbrain–hindbrain boundary
- MZ:
-
Mantle zone
- OB:
-
Olfactory bulb
- p1:
-
Prosomere 1, pretectum
- p2:
-
Prosomere 2, thalamus
- p3:
-
Prosomere 3, prethalamus
- PcP:
-
Precommissural pretectum (glutamatergic)
- POA:
-
Preoptic area
- pTHr:
-
Rostral thalamus (GABAergic)
- pTHc:
-
Caudal thalamus (glutamatergic)
- sc:
-
Spinal cord
- SNpr:
-
Substantia nigra pars reticulata
- SVS:
-
Subcortical visual shell nuclei
- SVZ:
-
Subventricular zone
- tel:
-
Telencephalon
- TF:
-
Transcription factor
- V0–V2:
-
Subpopulations of GABAergic neurons in ventral spinal cord
- VTA:
-
Ventral tegmental area
- VZ:
-
Ventricular zone
- ZF:
-
Zinc finger
- ZLI:
-
Zona limitans intrathalamica
References
Kiecker C, Lumsden A (2012) The role of organizers in patterning the nervous system. Annu Rev Neurosci 35:347–367
Dessaud E, McMahon AP, Briscoe J (2008) Pattern formation in the vertebrate neural tube: a sonic hedgehog morphogen-regulated transcriptional network. Development 135(15):2489–2503
Guillemot F (2007) Spatial and temporal specification of neural fates by transcription factor codes. Development 134(21):3771–3780
Doe CQ (2008) Neural stem cells: balancing self-renewal with differentiation. Development 135(9):1575–1587
Lee SK, Pfaff SL (2003) Synchronization of neurogenesis and motor neuron specification by direct coupling of bHLH and homeodomain transcription factors. Neuron 38(5):731–745
Castro DS, Skowronska-Krawczyk D, Armant O, Donaldson IJ, Parras C, Hunt C, Critchley JA, Nguyen L, Gossler A, Gottgens B, Matter JM, Guillemot F (2006) Proneural bHLH and Brn proteins coregulate a neurogenic program through cooperative binding to a conserved DNA motif. Dev Cell 11(6):831–844
Zhou JX, Huang S (2011) Understanding gene circuits at cell-fate branch points for rational cell reprogramming. Trends Genet TIG 27(2):55–62
Ronan JL, Wu W, Crabtree GR (2013) From neural development to cognition: unexpected roles for chromatin. Nat Rev Genet 14(5):347–359
Rouaux C, Arlotta P (2010) Fezf2 directs the differentiation of corticofugal neurons from striatal progenitors in vivo. Nat Neurosci 13(11):1345–1347
Molyneaux BJ, Arlotta P, Hirata T, Hibi M, Macklis JD (2005) Fezl is required for the birth and specification of corticospinal motor neurons. Neuron 47(6):817–831
Jeong JY, Einhorn Z, Mathur P, Chen L, Lee S, Kawakami K, Guo S (2007) Patterning the zebrafish diencephalon by the conserved zinc-finger protein Fezl. Development 134(1):127–136
Hobert O, Carrera I, Stefanakis N (2010) The molecular and gene regulatory signature of a neuron. Trends Neurosci 33(10):435–445
Holmberg J, Hansson E, Malewicz M, Sandberg M, Perlmann T, Lendahl U, Muhr J (2008) SoxB1 transcription factors and Notch signaling use distinct mechanisms to regulate proneural gene function and neural progenitor differentiation. Development 135(10):1843–1851
Kadkhodaei B, Ito T, Joodmardi E, Mattsson B, Rouillard C, Carta M, Muramatsu S, Sumi-Ichinose C, Nomura T, Metzger D, Chambon P, Lindqvist E, Larsson NG, Olson L, Bjorklund A, Ichinose H, Perlmann T (2009) Nurr1 is required for maintenance of maturing and adult midbrain dopamine neurons. J Neurosci Off J Soc Neurosci 29(50):15923–15932
Liu C, Maejima T, Wyler SC, Casadesus G, Herlitze S, Deneris ES (2010) Pet-1 is required across different stages of life to regulate serotonergic function. Nat Neurosci 13(10):1190–1198
Flames N, Pla R, Gelman DM, Rubenstein JL, Puelles L, Marin O (2007) Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J Neurosci Off J Soc Neurosci 27(36):9682–9695
Yun K, Potter S, Rubenstein JL (2001) Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon. Development 128(2):193–205
Scholpp S, Lumsden A (2010) Building a bridal chamber: development of the thalamus. Trends Neurosci 33(8):373–380
Virolainen SM, Achim K, Peltopuro P, Salminen M, Partanen J (2012) Transcriptional regulatory mechanisms underlying the GABAergic neuron fate in different diencephalic prosomeres. Development 139(20):3795–3805
Vue TY, Bluske K, Alishahi A, Yang LL, Koyano-Nakagawa N, Novitch B, Nakagawa Y (2009) Sonic hedgehog signaling controls thalamic progenitor identity and nuclei specification in mice. J Neurosci Off J Soc Neurosci 29(14):4484–4497
Kala K, Haugas M, Lillevali K, Guimera J, Wurst W, Salminen M, Partanen J (2009) Gata2 is a tissue-specific post-mitotic selector gene for midbrain GABAergic neurons. Development 136(2):253–262
Nakatani T, Minaki Y, Kumai M, Ono Y (2007) Helt determines GABAergic over glutamatergic neuronal fate by repressing Ngn genes in the developing mesencephalon. Development 134(15):2783–2793
Hashimoto M, Hibi M (2012) Development and evolution of cerebellar neural circuits. Dev Growth Differ 54(3):373–389
Lahti L, Achim K, Partanen J (2013) Molecular regulation of GABAergic neuron differentiation and diversity in the developing midbrain. Acta Physiol (Oxf) 207(4):616–627
Zordan P, Croci L, Hawkes R, Consalez GG (2008) Comparative analysis of proneural gene expression in the embryonic cerebellum. Dev Dyn Off Publ Am Assoc Anat 237(6):1726–1735
Lebel M, Mo R, Shimamura K, Hui CC (2007) Gli2 and Gli3 play distinct roles in the dorsoventral patterning of the mouse hindbrain. Dev Biol 302(1):345–355
Cordes SP (2001) Molecular genetics of cranial nerve development in mouse. Nat Rev Neurosci 2(9):611–623
Briscoe J, Pierani A, Jessell TM, Ericson J (2000) A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101(4):435–445
Lewis KE (2006) How do genes regulate simple behaviours? Understanding how different neurons in the vertebrate spinal cord are genetically specified. Philos Trans R Soc Lond B Biol Sci 361(1465):45–66
Vieira C, Pombero A, Garcia-Lopez R, Gimeno L, Echevarria D, Martinez S (2010) Molecular mechanisms controlling brain development: an overview of neuroepithelial secondary organizers. Int J Dev Biol 54(1):7–20
Beccari L, Marco-Ferreres R, Bovolenta P (2013) The logic of gene regulatory networks in early vertebrate forebrain patterning. Mech Dev 130(2–3):95–111
Puelles L, Rubenstein JL (1993) Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization. Trends Neurosci 16(11):472–479
Puelles L, Rubenstein JL (2003) Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci 26(9):469–476
Shimamura K, Hartigan DJ, Martinez S, Puelles L, Rubenstein JL (1995) Longitudinal organization of the anterior neural plate and neural tube. Development 121(12):3923–3933
Briscoe J, Novitch BG (2008) Regulatory pathways linking progenitor patterning, cell fates and neurogenesis in the ventral neural tube. Philos Trans R Soc Lond B Biol Sci 363(1489):57–70
Briscoe J (2009) Making a grade: Sonic hedgehog signalling and the control of neural cell fate. EMBO J 28(5):457–465
Guillemot F (2005) Cellular and molecular control of neurogenesis in the mammalian telencephalon. Curr Opin Cell Biol 17(6):639–647
Gelman DM, Marín O, Rubenstein JLR (2012) The Generation of cortical interneurons. In: Noebels JL, Avoli M, Rogawski MA et al (eds) Jasper's basic mechanisms of the epilepsies [Internet], 4th edn. National Center for Biotechnology Information (USA), Bethesda, MD. http://www.ncbi.nlm.nih.gov/books/NBK98190/
Xu Q, Cobos I, De La Cruz E, Rubenstein JL, Anderson SA (2004) Origins of cortical interneuron subtypes. J Neurosci Off J Soc Neurosci 24(11):2612–2622
Fogarty M, Grist M, Gelman D, Marin O, Pachnis V, Kessaris N (2007) Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex. J Neurosci Off J Soc Neurosci 27(41):10935–10946
Miyoshi G, Fishell G (2011) GABAergic interneuron lineages selectively sort into specific cortical layers during early postnatal development. Cereb Cortex 21(4):845–852
Sussel L, Marin O, Kimura S, Rubenstein JL (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(15):3359–3370
Pleasure SJ, Anderson S, Hevner R, Bagri A, Marin O, Lowenstein DH, Rubenstein JL (2000) Cell migration from the ganglionic eminences is required for the development of hippocampal GABAergic interneurons. Neuron 28(3):727–740
Gelman D, Griveau A, Dehorter N, Teissier A, Varela C, Pla R, Pierani A, Marin O (2011) A wide diversity of cortical GABAergic interneurons derives from the embryonic preoptic area. J Neurosci Off J Soc Neurosci 31(46):16570–16580
Gelman DM, Martini FJ, Nobrega-Pereira S, Pierani A, Kessaris N, Marin O (2009) The embryonic preoptic area is a novel source of cortical GABAergic interneurons. J Neurosci Off J Soc Neurosci 29(29):9380–9389
Wang B, Long JE, Flandin P, Pla R, Waclaw RR, Campbell K, Rubenstein JL (2013) Loss of Gsx1 and Gsx2 function rescues distinct phenotypes in Dlx1/2 mutants. J Comp Neurol 521(7):1561–1584
Shimogori T, Lee DA, Miranda-Angulo A, Yang Y, Wang H, Jiang L, Yoshida AC, Kataoka A, Mashiko H, Avetisyan M, Qi L, Qian J, Blackshaw S (2010) A genomic atlas of mouse hypothalamic development. Nat Neurosci 13(6):767–775
Toresson H, Potter SS, Campbell K (2000) Genetic control of dorsal-ventral identity in the telencephalon: opposing roles for Pax6 and Gsh2. Development 127(20):4361–4371
Carney RS, Cocas LA, Hirata T, Mansfield K, Corbin JG (2009) Differential regulation of telencephalic pallial–subpallial boundary patterning by Pax6 and Gsh2. Cereb Cortex 19(4):745–759
Corbin JG, Rutlin M, Gaiano N, Fishell G (2003) Combinatorial function of the homeodomain proteins Nkx2.1 and Gsh2 in ventral telencephalic patterning. Development 130(20):4895–4906
Pei Z, Wang B, Chen G, Nagao M, Nakafuku M, Campbell K (2011) Homeobox genes Gsx1 and Gsx2 differentially regulate telencephalic progenitor maturation. Proc Natl Acad Sci USA 108(4):1675–1680
Waclaw RR, Wang B, Pei Z, Ehrman LA, Campbell K (2009) Distinct temporal requirements for the homeobox gene Gsx2 in specifying striatal and olfactory bulb neuronal fates. Neuron 63(4):451–465
Letinic K, Zoncu R, Rakic P (2002) Origin of GABAergic neurons in the human neocortex. Nature 417(6889):645–649
Petanjek Z, Kostovic I, Esclapez M (2009) Primate-specific origins and migration of cortical GABAergic neurons. Front Neuroanat 3:26
Cai Y, Zhang Y, Shen Q, Rubenstein JL, Yang Z (2013) A subpopulation of individual neural progenitors in the mammalian dorsal pallium generates both projection neurons and interneurons in vitro. Stem Cells 31(6):1193–1201
Kohwi M, Petryniak MA, Long JE, Ekker M, Obata K, Yanagawa Y, Rubenstein JL, Alvarez-Buylla A (2007) A subpopulation of olfactory bulb GABAergic interneurons is derived from Emx1- and Dlx5/6-expressing progenitors. J Neurosci Off J Soc Neurosci 27(26):6878–6891
Nakagawa Y, Shimogori T (2012) Diversity of thalamic progenitor cells and postmitotic neurons. Eur J Neurosci 35(10):1554–1562
Hirata T, Nakazawa M, Muraoka O, Nakayama R, Suda Y, Hibi M (2006) Zinc-finger genes Fez and Fez-like function in the establishment of diencephalon subdivisions. Development 133(20):3993–4004
Jeong Y, Dolson DK, Waclaw RR, Matise MP, Sussel L, Campbell K, Kaestner KH, Epstein DJ (2011) Spatial and temporal requirements for sonic hedgehog in the regulation of thalamic interneuron identity. Development 138(3):531–541
Achim K, Peltopuro P, Lahti L, Li J, Salminen M, Partanen J (2012) Distinct developmental origins and regulatory mechanisms for GABAergic neurons associated with dopaminergic nuclei in the ventral mesodiencephalic region. Development 139(13):2360–2370
Arber S (2012) Motor circuits in action: specification, connectivity, and function. Neuron 74(6):975–989
Karunaratne A, Hargrave M, Poh A, Yamada T (2002) GATA proteins identify a novel ventral interneuron subclass in the developing chick spinal cord. Dev Biol 249(1):30–43
Smith E, Hargrave M, Yamada T, Begley CG, Little MH (2002) Coexpression of SCL and GATA3 in the V2 interneurons of the developing mouse spinal cord. Dev Dyn Off Publ Am Assoc Anat 224(2):231–237
Zhou Y, Yamamoto M, Engel JD (2000) GATA2 is required for the generation of V2 interneurons. Development 127(17):3829–3838
Panayi H, Panayiotou E, Orford M, Genethliou N, Mean R, Lapathitis G, Li S, Xiang M, Kessaris N, Richardson WD, Malas S (2010) Sox1 is required for the specification of a novel p2-derived interneuron subtype in the mouse ventral spinal cord. J Neurosci Off J Soc Neurosci 30(37):12274–12280
Li S, Misra K, Matise MP, Xiang M (2005) Foxn4 acts synergistically with Mash1 to specify subtype identity of V2 interneurons in the spinal cord. Proc Natl Acad Sci USA 102(30):10688–10693
Del Barrio MG, Taveira-Marques R, Muroyama Y, Yuk DI, Li S, Wines-Samuelson M, Shen J, Smith HK, Xiang M, Rowitch D, Richardson WD (2007) A regulatory network involving Foxn4, Mash1 and delta-like 4/Notch1 generates V2a and V2b spinal interneurons from a common progenitor pool. Development 134(19):3427–3436
Pierani A, Brenner-Morton S, Chiang C, Jessell TM (1999) A sonic hedgehog-independent, retinoid-activated pathway of neurogenesis in the ventral spinal cord. Cell 97(7):903–915
Vallstedt A, Muhr J, Pattyn A, Pierani A, Mendelsohn M, Sander M, Jessell TM, Ericson J (2001) Different levels of repressor activity assign redundant and specific roles to Nkx6 genes in motor neuron and interneuron specification. Neuron 31(5):743–755
Alvarez FJ, Jonas PC, Sapir T, Hartley R, Berrocal MC, Geiman EJ, Todd AJ, Goulding M (2005) Postnatal phenotype and localization of spinal cord V1-derived interneurons. J Comp Neurol 493(2):177–192
Sapir T, Geiman EJ, Wang Z, Velasquez T, Mitsui S, Yoshihara Y, Frank E, Alvarez FJ, Goulding M (2004) Pax6 and engrailed 1 regulate two distinct aspects of Renshaw cell development. J Neurosci Off J Soc Neurosci 24(5):1255–1264
Lanuza GM, Gosgnach S, Pierani A, Jessell TM, Goulding M (2004) Genetic identification of spinal interneurons that coordinate left–right locomotor activity necessary for walking movements. Neuron 42(3):375–386
Pierani A, Moran-Rivard L, Sunshine MJ, Littman DR, Goulding M, Jessell TM (2001) Control of interneuron fate in the developing spinal cord by the progenitor homeodomain protein Dbx1. Neuron 29(2):367–384
Gribble SL, Nikolaus OB, Dorsky RI (2007) Regulation and function of Dbx genes in the zebrafish spinal cord. Dev Dyn Off Publ Am Assoc Anat 236(12):3472–3483
Matise MP, Joyner AL (1997) Expression patterns of developmental control genes in normal and Engrailed-1 mutant mouse spinal cord reveal early diversity in developing interneurons. J Neurosci Off J Soc Neurosci 17(20):7805–7816
Gross MK, Dottori M, Goulding M (2002) Lbx1 specifies somatosensory association interneurons in the dorsal spinal cord. Neuron 34(4):535–549
Kriks S, Lanuza GM, Mizuguchi R, Nakafuku M, Goulding M (2005) Gsh2 is required for the repression of Ngn1 and specification of dorsal interneuron fate in the spinal cord. Development 132(13):2991–3002
Helms AW, Johnson JE (2003) Specification of dorsal spinal cord interneurons. Curr Opin Neurobiol 13(1):42–49
Fujiyama T, Yamada M, Terao M, Terashima T, Hioki H, Inoue YU, Inoue T, Masuyama N, Obata K, Yanagawa Y, Kawaguchi Y, Nabeshima Y, Hoshino M (2009) Inhibitory and excitatory subtypes of cochlear nucleus neurons are defined by distinct bHLH transcription factors, Ptf1a and Atoh1. Development 136(12):2049–2058
Farkas LM, Huttner WB (2008) The cell biology of neural stem and progenitor cells and its significance for their proliferation versus differentiation during mammalian brain development. Curr Opin Cell Biol 20(6):707–715
Castro DS, Martynoga B, Parras C, Ramesh V, Pacary E, Johnston C, Drechsel D, Lebel-Potter M, Garcia LG, Hunt C, Dolle D, Bithell A, Ettwiller L, Buckley N, Guillemot F (2011) A novel function of the proneural factor Ascl1 in progenitor proliferation identified by genome-wide characterization of its targets. Genes Dev 25(9):930–945
Kageyama R, Ohtsuka T, Kobayashi T (2008) Roles of Hes genes in neural development. Dev Growth Differ 50(Suppl 1):S97–S103
Bylund M, Andersson E, Novitch BG, Muhr J (2003) Vertebrate neurogenesis is counteracted by So1–3 activity. Nat Neurosci 6(11):1162–1168
Graham V, Khudyakov J, Ellis P, Pevny L (2003) SOX2 functions to maintain neural progenitor identity. Neuron 39(5):749–765
Casarosa S, Fode C, Guillemot F (1999) Mash1 regulates neurogenesis in the ventral telencephalon. Development 126(3):525–534
Parras CM, Schuurmans C, Scardigli R, Kim J, Anderson DJ, Guillemot F (2002) Divergent functions of the proneural genes Mash1 and Ngn2 in the specification of neuronal subtype identity. Genes Dev 16(3):324–338
Fode C, Ma Q, Casarosa S, Ang SL, Anderson DJ, Guillemot F (2000) A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev 14(1):67–80
Peltopuro P, Kala K, Partanen J (2010) Distinct requirements for Ascl1 in subpopulations of midbrain GABAergic neurons. Dev Biol 343(1–2):63–70
Kataoka A, Shimogori T (2008) Fgf8 controls regional identity in the developing thalamus. Development 135(17):2873–2881
Guimera J, Weisenhorn DV, Wurst W (2006) Megane/Heslike is required for normal GABAergic differentiation in the mouse superior colliculus. Development 133(19):3847–3857
Miyoshi G, Bessho Y, Yamada S, Kageyama R (2004) Identification of a novel basic helix-loop-helix gene, Heslike, and its role in GABAergic neurogenesis. J Neurosci Off J Soc Neurosci 24(14):3672–3682
Guimera J, Vogt Weisenhorn D, Echevarria D, Martinez S, Wurst W (2006) Molecular characterization, structure and developmental expression of Megane bHLH factor. Gene 377:65–76
Delogu A, Sellers K, Zagoraiou L, Bocianowska-Zbrog A, Mandal S, Guimera J, Rubenstein JL, Sugden D, Jessell T, 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(4):648–662
Mizuguchi R, Kriks S, Cordes R, Gossler A, Ma Q, Goulding M (2006) Ascl1 and Gsh1/2 control inhibitory and excitatory cell fate in spinal sensory interneurons. Nat Neurosci 9(6):770–778
Sudarov A, Turnbull RK, Kim EJ, Lebel-Potter M, Guillemot F, Joyner AL (2011) Ascl1 genetics reveals insights into cerebellum local circuit assembly. J Neurosci Off J Soc Neurosci 31(30):11055–11069
Wildner H, Muller T, Cho SH, Brohl D, Cepko CL, Guillemot F, Birchmeier C (2006) dILA neurons in the dorsal spinal cord are the product of terminal and non-terminal asymmetric progenitor cell divisions, and require Mash1 for their development. Development 133(11):2105–2113
Grimaldi P, Parras C, Guillemot F, Rossi F, Wassef M (2009) Origins and control of the differentiation of inhibitory interneurons and glia in the cerebellum. Dev Biol 328(2):422–433
Lundell TG, Zhou Q, Doughty ML (2009) Neurogenin1 expression in cell lineages of the cerebellar cortex in embryonic and postnatal mice. Dev Dyn Off Publ Am Assoc Anat 238(12):3310–3325
Florio M, Leto K, Muzio L, Tinterri A, Badaloni A, Croci L, Zordan P, Barili V, Albieri I, Guillemot F, Rossi F, Consalez GG (2012) Neurogenin 2 regulates progenitor cell-cycle progression and Purkinje cell dendritogenesis in cerebellar development. Development 139(13):2308–2320
Henke RM, Savage TK, Meredith DM, Glasgow SM, Hori K, Dumas J, MacDonald RJ, Johnson JE (2009) Neurog2 is a direct downstream target of the Ptf1a–Rbpj transcription complex in dorsal spinal cord. Development 136(17):2945–2954
Peng CY, Yajima H, Burns CE, Zon LI, Sisodia SS, Pfaff SL, Sharma K (2007) Notch and MAML signaling drives Scl-dependent interneuron diversity in the spinal cord. Neuron 53(6):813–827
Glasgow SM, Henke RM, Macdonald RJ, Wright CV, Johnson JE (2005) Ptf1a determines GABAergic over glutamatergic neuronal cell fate in the spinal cord dorsal horn. Development 132(24):5461–5469
Muroyama Y, Fujiwara Y, Orkin SH, Rowitch DH (2005) Specification of astrocytes by bHLH protein SCL in a restricted region of the neural tube. Nature 438(7066):360–363
Cheng L, Samad OA, Xu Y, Mizuguchi R, Luo P, Shirasawa S, Goulding M, Ma Q (2005) Lbx1 and Tlx3 are opposing switches in determining GABAergic versus glutamatergic transmitter phenotypes. Nat Neurosci 8(11):1510–1515
Eisenstat DD, Liu JK, Mione M, Zhong W, Yu G, Anderson SA, Ghattas I, Puelles L, Rubenstein JL (1999) DLX-1, DLX-2, and DLX-5 expression define distinct stages of basal forebrain differentiation. J Comp Neurol 414(2):217–237
Stuhmer T, Puelles L, Ekker M, Rubenstein JL (2002) Expression from a Dlx gene enhancer marks adult mouse cortical GABAergic neurons. Cereb Cortex 12(1):75–85
Long JE, Garel S, Alvarez-Dolado M, Yoshikawa K, Osumi N, Alvarez-Buylla A, Rubenstein JL (2007) Dlx-dependent and -independent regulation of olfactory bulb interneuron differentiation. J Neurosci Off J Soc Neurosci 27(12):3230–3243
Long JE, Swan C, Liang WS, Cobos I, Potter GB, Rubenstein JL (2009) Dlx1&2 and Mash1 transcription factors control striatal patterning and differentiation through parallel and overlapping pathways. J Comp Neurol 512(4):556–572
Zerucha T, Stuhmer T, Hatch G, Park BK, Long Q, Yu G, Gambarotta A, Schultz JR, Rubenstein JL, Ekker M (2000) A highly conserved enhancer in the Dlx5/Dlx6 intergenic region is the site of cross-regulatory interactions between Dlx genes in the embryonic forebrain. J Neurosci Off J Soc Neurosci 20(2):709–721
Poitras L, Ghanem N, Hatch G, Ekker M (2007) The proneural determinant MASH1 regulates forebrain Dlx1/2 expression through the I12b intergenic enhancer. Development 134(9):1755–1765
Potter GB, Petryniak MA, Shevchenko E, McKinsey GL, Ekker M, Rubenstein JL (2009) Generation of Cre-transgenic mice using Dlx1/Dlx2 enhancers and their characterization in GABAergic interneurons. Mol Cell Neurosci 40(2):167–186
Panganiban G, Rubenstein JL (2002) Developmental functions of the distal-less/Dlx homeobox genes. Development 129(19):4371–4386
Anderson SA, Qiu M, Bulfone A, Eisenstat DD, Meneses J, Pedersen R, Rubenstein JL (1997) Mutations of the homeobox genes Dlx-1 and Dlx-2 disrupt the striatal subventricular zone and differentiation of late born striatal neurons. Neuron 19(1):27–37
Anderson SA, Eisenstat DD, Shi L, Rubenstein JL (1997) Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278(5337):474–476
Colasante G, Collombat P, Raimondi V, Bonanomi D, Ferrai C, Maira M, Yoshikawa K, Mansouri A, Valtorta F, Rubenstein JL, Broccoli V (2008) Arx is a direct target of Dlx2 and thereby contributes to the tangential migration of GABAergic interneurons. J Neurosci Off J Soc Neurosci 28(42):10674–10686
Ghanem N, Yu M, Long J, Hatch G, Rubenstein JL, Ekker M (2007) Distinct cis-regulatory elements from the Dlx1/Dlx2 locus mark different progenitor cell populations in the ganglionic eminences and different subtypes of adult cortical interneurons. J Neurosci Off J Soc Neurosci 27(19):5012–5022
Cobos I, Calcagnotto ME, Vilaythong AJ, Thwin MT, Noebels JL, Baraban SC, Rubenstein JL (2005) Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat Neurosci 8(8):1059–1068
McKinsey GL, Lindtner S, Trzcinski B, Visel A, Pennacchio LA, Huylebroeck D, Higashi Y, Rubenstein JL (2013) Dlx1&2-dependent expression of Zfhx1b (Sip1, Zeb2) regulates the fate switch between cortical and striatal interneurons. Neuron 77(1):83–98
Fulp CT, Cho G, Marsh ED, Nasrallah IM, Labosky PA, Golden JA (2008) Identification of Arx transcriptional targets in the developing basal forebrain. Hum Mol Genet 17(23):3740–3760
Herberth B, Minko K, Csillag A, Jaffredo T, Madarasz E (2005) SCL, GATA-2 and Lmo2 expression in neurogenesis. Int J Dev Neurosci Off J Int Soc Dev Neurosci 23(5):449–463
Achim K, Peltopuro P, Lahti L, Tsai H, Zachariah A, Åstrand M, Salminen M, Rowitch D, Partanen J (2013) The role of Tal2 and Tal1 in the differentiation of midbrain GABAergic neuron precursors. Biol Open. doi:10.1242/bio.20135041
Ogilvy S, Ferreira R, Piltz SG, Bowen JM, Gottgens B, Green AR (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(20):7206–7219
Joshi K, Lee S, Lee B, Lee JW, Lee SK (2009) LMO4 controls the balance between excitatory and inhibitory spinal V2 interneurons. Neuron 61(6):839–851
Minaki Y, Nakatani T, Mizuhara E, Inoue T, Ono Y (2008) Identification of a novel transcriptional corepressor, Corl2, as a cerebellar Purkinje cell-selective marker. Gene Expr Patterns GEP 8(6):418–423
Hoshino M, Nakamura S, Mori K, Kawauchi T, Terao M, Nishimura YV, Fukuda A, Fuse T, Matsuo N, Sone M, Watanabe M, Bito H, Terashima T, Wright CV, Kawaguchi Y, Nakao K, Nabeshima Y (2005) Ptf1a, a bHLH transcriptional gene, defines GABAergic neuronal fates in cerebellum. Neuron 47(2):201–213
Pascual M, Abasolo I, Mingorance-Le Meur A, Martinez A, Del Rio JA, Wright CV, Real FX, Soriano E (2007) Cerebellar GABAergic progenitors adopt an external granule cell-like phenotype in the absence of Ptf1a transcription factor expression. Proc Natl Acad Sci USA 104(12):5193–5198
Yamada M, Terao M, Terashima T, Fujiyama T, Kawaguchi Y, Nabeshima Y, Hoshino M (2007) Origin of climbing fiber neurons and their developmental dependence on Ptf1a. J Neurosci Off J Soc Neurosci 27(41):10924–10934
Cheng L, Arata A, Mizuguchi R, Qian Y, Karunaratne A, Gray PA, Arata S, Shirasawa S, Bouchard M, Luo P, Chen CL, Busslinger M, Goulding M, Onimaru H, Ma Q (2004) Tlx3 and Tlx1 are post-mitotic selector genes determining glutamatergic over GABAergic cell fates. Nat Neurosci 7(5):510–517
Huang M, Huang T, Xiang Y, Xie Z, Chen Y, Yan R, Xu J, Cheng L (2008) Ptf1a, Lbx1 and Pax2 coordinate glycinergic and peptidergic transmitter phenotypes in dorsal spinal inhibitory neurons. Dev Biol 322(2):394–405
Meredith DM, Borromeo MD, Deering TG, Casey B, Savage TK, Mayer PR, Hoang C, Tung KC, Kumar M, Shen C, Swift GH, Macdonald RJ, Johnson JE (2013) Program specificity for Ptf1a in pancreas versus neural tube development correlates with distinct collaborating cofactors and chromatin accessibility. Mol Cell Biol 33(16):3166–3179
Hori K, Cholewa-Waclaw J, Nakada Y, Glasgow SM, Masui T, Henke RM, Wildner H, Martarelli B, Beres TM, Epstein JA, Magnuson MA, Macdonald RJ, Birchmeier C, Johnson JE (2008) A nonclassical bHLH Rbpj transcription factor complex is required for specification of GABAergic neurons independent of Notch signaling. Genes Dev 22(2):166–178
Graw J (2010) Eye development. Curr Top Dev Biol 90:343–386
Fujitani Y, Fujitani S, Luo H, Qiu F, Burlison J, Long Q, Kawaguchi Y, Edlund H, MacDonald RJ, Furukawa T, Fujikado T, Magnuson MA, Xiang M, Wright CV (2006) Ptf1a determines horizontal and amacrine cell fates during mouse retinal development. Development 133(22):4439–4450
Jusuf PR, Almeida AD, Randlett O, Joubin K, Poggi L, Harris WA (2011) Origin and determination of inhibitory cell lineages in the vertebrate retina. J Neurosci Off J Soc Neurosci 31(7):2549–2562
Nakhai H, Sel S, Favor J, Mendoza-Torres L, Paulsen F, Duncker GI, Schmid RM (2007) Ptf1a is essential for the differentiation of GABAergic and glycinergic amacrine cells and horizontal cells in the mouse retina. Development 134(6):1151–1160
Dullin JP, Locker M, Robach M, Henningfeld KA, Parain K, Afelik S, Pieler T, Perron M (2007) Ptf1a triggers GABAergic neuronal cell fates in the retina. BMC Dev Biol 7:110
Lamb TD, Collin SP, Pugh EN Jr (2007) Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup. Nat Rev Neurosci 8(12):960–976
Livesey FJ, Cepko CL (2001) Vertebrate neural cell-fate determination: lessons from the retina. Nat Rev Neurosci 2(2):109–118
Winden KD, Oldham MC, Mirnics K, Ebert PJ, Swan CH, Levitt P, Rubenstein JL, Horvath S, Geschwind DH (2009) The organization of the transcriptional network in specific neuronal classes. Mol Syst Biol 5:291
Holmberg J, Perlmann T (2012) Maintaining differentiated cellular identity. Nat Rev Genet 13(6):429–439
Zhou QP, Le TN, Qiu X, Spencer V, de Melo J, Du G, Plews M, Fonseca M, Sun JM, Davie JR, Eisenstat DD (2004) Identification of a direct Dlx homeodomain target in the developing mouse forebrain and retina by optimization of chromatin immunoprecipitation. Nucleic Acids Res 32(3):884–892
Hobert O, Westphal H (2000) Functions of LIM-homeobox genes. Trends Genet TIG 16(2):75–83
Pillai A, Mansouri A, Behringer R, Westphal H, Goulding M (2007) Lhx1 and Lhx5 maintain the inhibitory-neurotransmitter status of interneurons in the dorsal spinal cord. Development 134(2):357–366
Zhao Y, Kwan KM, Mailloux CM, Lee WK, Grinberg A, Wurst W, Behringer RR, Westphal H (2007) LIM-homeodomain proteins Lhx1 and Lhx5, and their cofactor Ldb1, control Purkinje cell differentiation in the developing cerebellum. Proc Natl Acad Sci USA 104(32):13182–13186
Moreno N, Bachy I, Retaux S, Gonzalez A (2004) LIM-homeodomain genes as developmental and adult genetic markers of Xenopus forebrain functional subdivisions. J Comp Neurol 472(1):52–72
Shibata M, Nakao H, Kiyonari H, Abe T, Aizawa S (2011) MicroRNA-9 regulates neurogenesis in mouse telencephalon by targeting multiple transcription factors. J Neurosci Off J Soc Neurosci 31(9):3407–3422
Schaefer A, O’Carroll D, Tan CL, Hillman D, Sugimori M, Llinas R, Greengard P (2007) Cerebellar neurodegeneration in the absence of microRNAs. J Exp Med 204(7):1553–1558
Sun AX, Crabtree GR, Yoo AS (2013) MicroRNAs: regulators of neuronal fate. Curr Opin Cell Biol 25(2):215–221
He M, Liu Y, Wang X, Zhang MQ, Hannon GJ, Huang ZJ (2012) Cell-type-based analysis of microRNA profiles in the mouse brain. Neuron 73(1):35–48
Hatten ME (1999) Central nervous system neuronal migration. Annu Rev Neurosci 22:511–539
Marin O, Rubenstein JL (2003) Cell migration in the forebrain. Annu Rev Neurosci 26:441–483
de Castro F, Bribian A (2005) The molecular orchestra of the migration of oligodendrocyte precursors during development. Brain Res Brain Res Rev 49(2):227–241
Ghashghaei HT, Lai C, Anton ES (2007) Neuronal migration in the adult brain: are we there yet? Nat Rev Neurosci 8(2):141–151
Chedotal A, Rijli FM (2009) Transcriptional regulation of tangential neuronal migration in the developing forebrain. Curr Opin Neurobiol 19(2):139–145
Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5(10):793–807
Klausberger T, Somogyi P (2008) Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321(5885):53–57
Baudoin JP, Viou L, Launay PS, Luccardini C, Espeso Gil S, Kiyasova V, Irinopoulou T, Alvarez C, Rio JP, Boudier T, Lechaire JP, Kessaris N, Spassky N, Metin C (2012) Tangentially migrating neurons assemble a primary cilium that promotes their reorientation to the cortical plate. Neuron 76(6):1108–1122
Marin O, Yaron A, Bagri A, Tessier-Lavigne M, Rubenstein JL (2001) Sorting of striatal and cortical interneurons regulated by semaphorin-neuropilin interactions. Science 293(5531):872–875
Flames N, Long JE, Garratt AN, Fischer TM, Gassmann M, Birchmeier C, Lai C, Rubenstein JL, Marin O (2004) Short- and long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron 44(2):251–261
Stumm RK, Zhou C, Ara T, Lazarini F, Dubois-Dalcq M, Nagasawa T, Hollt V, Schulz S (2003) CXCR4 regulates interneuron migration in the developing neocortex. J Neurosci Off J Soc Neurosci 23(12):5123–5130
Yozu M, Tabata H, Nakajima K (2005) The caudal migratory stream: a novel migratory stream of interneurons derived from the caudal ganglionic eminence in the developing mouse forebrain. J Neurosci Off J Soc Neurosci 25(31):7268–7277
Zimmer G, Rudolph J, Landmann J, Gerstmann K, Steinecke A, Gampe C, Bolz J (2011) Bidirectional ephrinB3/EphA4 signaling mediates the segregation of medial ganglionic eminence- and preoptic area-derived interneurons in the deep and superficial migratory stream. J Neurosci Off J Soc Neurosci 31(50):18364–18380
Marin O (2013) Cellular and molecular mechanisms controlling the migration of neocortical interneurons. Eur J Neurosci 38(1):2019–2029
Marin O, Rubenstein JL (2001) A long, remarkable journey: tangential migration in the telencephalon. Nat Rev Neurosci 2(11):780–790
Lavdas AA, Grigoriou M, Pachnis V, Parnavelas JG (1999) The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J Neurosci Off J Soc Neurosci 19(18):7881–7888
Wichterle H, Garcia-Verdugo JM, Herrera DG, Alvarez-Buylla A (1999) Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat Neurosci 2(5):461–466
Li G, Adesnik H, Li J, Long J, Nicoll RA, Rubenstein JL, Pleasure SJ (2008) Regional distribution of cortical interneurons and development of inhibitory tone are regulated by Cxcl12/Cxcr4 signaling. J Neurosci Off J Soc Neurosci 28(5):1085–1098
Lopez-Bendito G, Sanchez-Alcaniz JA, Pla R, Borrell V, Pico E, Valdeolmillos M, Marin O (2008) Chemokine signaling controls intracortical migration and final distribution of GABAergic interneurons. J Neurosci Off J Soc Neurosci 28(7):1613–1624
Tiveron MC, Rossel M, Moepps B, Zhang YL, Seidenfaden R, Favor J, Konig N, Cremer H (2006) Molecular interaction between projection neuron precursors and invading interneurons via stromal-derived factor 1 (CXCL12)/CXCR4 signaling in the cortical subventricular zone/intermediate zone. J Neurosci Off J Soc Neurosci 26(51):13273–13278
Sessa A, Mao CA, Colasante G, Nini A, Klein WH, Broccoli V (2010) Tbr2-positive intermediate (basal) neuronal progenitors safeguard cerebral cortex expansion by controlling amplification of pallial glutamatergic neurons and attraction of subpallial GABAergic interneurons. Genes Dev 24(16):1816–1826
Zarbalis K, Choe Y, Siegenthaler JA, Orosco LA, Pleasure SJ (2012) Meningeal defects alter the tangential migration of cortical interneurons in Foxc1hith/hith mice. Neural Dev 7:2
Pla R, Borrell V, Flames N, Marin O (2006) Layer acquisition by cortical GABAergic interneurons is independent of Reelin signaling. J Neurosci Off J Soc Neurosci 26(26):6924–6934
Fairen A, Cobas A, Fonseca M (1986) Times of generation of glutamic acid decarboxylase immunoreactive neurons in mouse somatosensory cortex. J Comp Neurol 251(1):67–83
Valcanis H, Tan SS (2003) Layer specification of transplanted interneurons in developing mouse neocortex. J Neurosci Off J Soc Neurosci 23(12):5113–5122
Hevner RF, Daza RA, Englund C, Kohtz J, Fink A (2004) Postnatal shifts of interneuron position in the neocortex of normal and reeler mice: evidence for inward radial migration. Neuroscience 124(3):605–618
Lodato S, Rouaux C, Quast KB, Jantrachotechatchawan C, Studer M, Hensch TK, Arlotta P (2011) Excitatory projection neuron subtypes control the distribution of local inhibitory interneurons in the cerebral cortex. Neuron 69(4):763–779
Wang Y, Li G, Stanco A, Long JE, Crawford D, Potter GB, Pleasure SJ, Behrens T, Rubenstein JL (2011) CXCR4 and CXCR7 have distinct functions in regulating interneuron migration. Neuron 69(1):61–76
Cobos I, Broccoli V, Rubenstein JL (2005) The vertebrate ortholog of Aristaless is regulated by Dlx genes in the developing forebrain. J Comp Neurol 483(3):292–303
Colombo E, Collombat P, Colasante G, Bianchi M, Long J, Mansouri A, Rubenstein JL, Broccoli V (2007) Inactivation of Arx, the murine ortholog of the X-linked lissencephaly with ambiguous genitalia gene, leads to severe disorganization of the ventral telencephalon with impaired neuronal migration and differentiation. J Neurosci Off J Soc Neurosci 27(17):4786–4798
Kitamura K, Yanazawa M, Sugiyama N, Miura H, Iizuka-Kogo A, Kusaka M, Omichi K, Suzuki R, Kato-Fukui Y, Kamiirisa K, Matsuo M, Kamijo S, Kasahara M, Yoshioka H, Ogata T, Fukuda T, Kondo I, Kato M, Dobyns WB, Yokoyama M, Morohashi K (2002) Mutation of ARX causes abnormal development of forebrain and testes in mice and X-linked lissencephaly with abnormal genitalia in humans. Nat Genet 32(3):359–369
Friocourt G, Parnavelas JG (2011) Identification of Arx targets unveils new candidates for controlling cortical interneuron migration and differentiation. Front Cell Neurosci. doi:10.3389/fncel.2011.00028
Kanatani S, Yozu M, Tabata H, Nakajima K (2008) COUP-TFII is preferentially expressed in the caudal ganglionic eminence and is involved in the caudal migratory stream. J Neurosci Off J Soc Neurosci 28(50):13582–13591
Nobrega-Pereira S, Kessaris N, Du T, Kimura S, Anderson SA, Marin O (2008) Postmitotic Nkx2-1 controls the migration of telencephalic interneurons by direct repression of guidance receptors. Neuron 59(5):733–745
Le TN, Du G, Fonseca M, Zhou QP, Wigle JT, Eisenstat DD (2007) Dlx homeobox genes promote cortical interneuron migration from the basal forebrain by direct repression of the semaphorin receptor neuropilin-2. J Biol Chem 282(26):19071–19081
Liodis P, Denaxa M, Grigoriou M, Akufo-Addo C, Yanagawa Y, Pachnis V (2007) Lhx6 activity is required for the normal migration and specification of cortical interneuron subtypes. J Neurosci Off J Soc Neurosci 27(12):3078–3089
Du T, Xu Q, Ocbina PJ, Anderson SA (2008) NKX2.1 specifies cortical interneuron fate by activating Lhx6. Development 135(8):1559–1567
Zhao Y, Flandin P, Long JE, Cuesta MD, Westphal H, Rubenstein JL (2008) Distinct molecular pathways for development of telencephalic interneuron subtypes revealed through analysis of Lhx6 mutants. J Comp Neurol 510(1):79–99
Luskin MB (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11(1):173–189
Luskin MB, Boone MS (1994) Rate and pattern of migration of lineally-related olfactory bulb interneurons generated postnatally in the subventricular zone of the rat. Chem Senses 19(6):695–714
Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264(5162):1145–1148
Hakanen J, Duprat S, Salminen M (2011) Netrin1 is required for neural and glial precursor migrations into the olfactory bulb. Dev Biol 355(1):101–114
Cobos I, Borello U, Rubenstein JL (2007) Dlx transcription factors promote migration through repression of axon and dendrite growth. Neuron 54(6):873–888
Alberti S, Krause SM, Kretz O, Philippar U, Lemberger T, Casanova E, Wiebel FF, Schwarz H, Frotscher M, Schutz G, Nordheim A (2005) Neuronal migration in the murine rostral migratory stream requires serum response factor. Proc Natl Acad Sci USA 102(17):6148–6153
Vasudevan A, Won C, Li S, Erdelyi F, Szabo G, Kim KS (2012) Dopaminergic neurons modulate GABA neuron migration in the embryonic midbrain. Development 139(17):3136–3141
Crandall JE, McCarthy DM, Araki KY, Sims JR, Ren JQ, Bhide PG (2007) Dopamine receptor activation modulates GABA neuron migration from the basal forebrain to the cerebral cortex. J Neurosci Off J Soc Neurosci 27(14):3813–3822
Horton S, Meredith A, Richardson JA, Johnson JE (1999) Correct coordination of neuronal differentiation events in ventral forebrain requires the bHLH factor MASH1. Mol Cell Neurosci 14(4–5):355–369
Chen L, Guo Q, Li JY (2009) Transcription factor Gbx2 acts cell-nonautonomously to regulate the formation of lineage-restriction boundaries of the thalamus. Development 136(8):1317–1326
Mastick GS, Andrews GL (2001) Pax6 regulates the identity of embryonic diencephalic neurons. Mol Cell Neurosci 17(1):190–207
Zhao GY, Li ZY, Zou HL, Hu ZL, Song NN, Zheng MH, Su CJ, Ding YQ (2008) Expression of the transcription factor GATA3 in the postnatal mouse central nervous system. Neurosci Res 61(4):420–428
Agarwala S, Sanders TA, Ragsdale CW (2001) Sonic hedgehog control of size and shape in midbrain pattern formation. Science 291(5511):2147–2150
Blaess S, Corrales JD, Joyner AL (2006) Sonic hedgehog regulates Gli activator and repressor functions with spatial and temporal precision in the mid/hindbrain region. Development 133(9):1799–1809
Puelles E, Annino A, Tuorto F, Usiello A, Acampora D, Czerny T, Brodski C, Ang SL, Wurst W, Simeone A (2004) Otx2 regulates the extent, identity and fate of neuronal progenitor domains in the ventral midbrain. Development 131(9):2037–2048
Waite MR, Skidmore JM, Billi AC, Martin JF, Martin DM (2011) GABAergic and glutamatergic identities of developing midbrain Pitx2 neurons. Dev Dyn Off Publ Am Assoc Anat 240(2):333–346
Lorente-Canovas B, Marin F, Corral-San-Miguel R, Hidalgo-Sanchez M, Ferran JL, Puelles L, Aroca P (2012) Multiple origins, migratory paths and molecular profiles of cells populating the avian interpeduncular nucleus. Dev Biol 361(1):12–26
Waite MR, Skaggs K, Kaviany P, Skidmore JM, Causeret F, Martin JF, Martin DM (2012) Distinct populations of GABAergic neurons in mouse rhombomere 1 express but do not require the homeodomain transcription factor PITX2. Mol Cell Neurosci 49(1):32–43
Sgaier SK, Lao Z, Villanueva MP, Berenshteyn F, Stephen D, Turnbull RK, Joyner AL (2007) Genetic subdivision of the tectum and cerebellum into functionally related regions based on differential sensitivity to engrailed proteins. Development 134(12):2325–2335
Sillitoe RV, Stephen D, Lao Z, Joyner AL (2008) Engrailed homeobox genes determine the organization of Purkinje cell sagittal stripe gene expression in the adult cerebellum. J Neurosci Off J Soc Neurosci 28(47):12150–12162
Wilson SL, Kalinovsky A, Orvis GD, Joyner AL (2011) Spatially restricted and developmentally dynamic expression of engrailed genes in multiple cerebellar cell types. Cerebellum 10(3):356–372
Chizhikov VV, Lindgren AG, Currle DS, Rose MF, Monuki ES, Millen KJ (2006) The roof plate regulates cerebellar cell-type specification and proliferation. Development 133(15):2793–2804
Kim EJ, Battiste J, Nakagawa Y, Johnson JE (2008) Ascl1 (Mash1) lineage cells contribute to discrete cell populations in CNS architecture. Mol Cell Neurosci 38(4):595–606
Maricich SM, Herrup K (1999) Pax-2 expression defines a subset of GABAergic interneurons and their precursors in the developing murine cerebellum. J Neurobiol 41(2):281–294
Helms AW, Battiste J, Henke RM, Nakada Y, Simplicio N, Guillemot F, Johnson JE (2005) Sequential roles for Mash1 and Ngn2 in the generation of dorsal spinal cord interneurons. Development 132(12):2709–2719
Moran-Rivard L, Kagawa T, Saueressig H, Gross MK, Burrill J, Goulding M (2001) Evx1 is a postmitotic determinant of v0 interneuron identity in the spinal cord. Neuron 29(2):385–399
Acknowledgments
We thank Laura Lahti and Maarja Haugas for comments on this manuscript. Our work was supported by the Academy of Finland, Sigrid Juselius Foundation, Finnish Parkinson’s Foundation and the University of Helsinki.
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Achim, K., Salminen, M. & Partanen, J. Mechanisms regulating GABAergic neuron development. Cell. Mol. Life Sci. 71, 1395–1415 (2014). https://doi.org/10.1007/s00018-013-1501-3
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DOI: https://doi.org/10.1007/s00018-013-1501-3