Specification of Cerebellar and Precerebellar Neurons

  • Mikio HoshinoEmail author
  • Satoshi Miyashita
  • Yusuke Seto
  • Mayumi Yamada
Living reference work entry


The cerebellum is thought to participate in the regulation of movement and is comprised of various types of neurons in the cerebellar cortex and nuclei. Each type of neurons has morphologically, immunohistochemically, and electrophysiologically distinct characteristics. In addition, there are two precerebellar afferent systems, the mossy fiber (MF) system and the climbing fiber (CF) system. MF neurons are located in various nuclei throughout the brainstem and send their axons to cerebellar granule cells, whereas CF neurons reside exclusively in the inferior olivary nucleus (ION) and project to Purkinje cells. Recently developed genetic lineage-tracing methods as well as gene-transfer technologies have accelerated the studies on the molecular machinery to specify neuronal subtypes in the cerebellum and the precerebellar systems.


Cerebellum bHLH Transcription factor Atoh1 Ptf1a Ngn1 Ascl1 Olig3 Pax6 Rhombomere Neuroepithelium Roof plate Rhombic lip (RL) Ventricular zone (VZ) Glutamatergic neuron GABAergic neuron Cerebellar nucleus (CN) CN-Glu neuron CN-GABA-ION neuron CN-GABA-interneuron Lineage trace In utero electroporation Null mutant Precerebellar systems Climbing fiber (CF) neuron Mossy fiber (MF) neuron Hindbrain Pontine gray nucleus (PGN) Reticulotegmental nucleus (RTN) Lateral reticular nucleus (LRN) External cuneate nucleus (ECN) Inferior olive nucleus (ION) Wnt-1 BMP Specification Subtype Cochlear nucleus Dorsal Grafting study Mitotic Postmitotic Granule cell Purkinje cell Golgi cell Stellate cell Basket cell 


  1. Altman J, Bayer SA (1987) Development of the precerebellar nuclei in the rat. I–IV. J Comp Neurol 257:477–552PubMedCrossRefPubMedCentralGoogle Scholar
  2. Ambrosiani J, Armengol JA, Martinez S, Puelles L (1996) The avian inferior olive derives from the alar neuroepithelium of the rhombomeres 7 and 8: an analysis by using chick-quail chimeric embryos. Neuroreport 7:1285–1288PubMedCrossRefPubMedCentralGoogle Scholar
  3. Aruga J, Minowa O, Yaginuma H, Kuno J, Nagai T, Noda T, Mikoshiba K (1998) Mouse Zic1 is involved in cerebellar development. J Neurosci 18:284–293PubMedCrossRefPubMedCentralGoogle Scholar
  4. Batini C, Compoint C, Buisseret-Delmas C, Daniel H, Guegan M (1992) Cerebellar nuclei and the nucleocortical projections in the rat: retrograde tracing coupled to GABA and glutamate immunohistochemistry. J Comp Neurol 315:74–84PubMedCrossRefPubMedCentralGoogle Scholar
  5. Ben-Arie N, Bellen HJ, Armstrong DL, McCall AE, Gordadze PR, Guo Q, Matzuk MM, Zoghbi HY (1997) Math1 is essential for genesis of cerebellar granule neurons. Nature 390:169–172PubMedCrossRefPubMedCentralGoogle Scholar
  6. Ben-Arie N, Hassan BA, Bermingham NA, Malicki DM, Armstrong D, Matzuk M, Bellen HJ, Zoghbi HY (2000) Functional conservation of atonal and Math1 in the CNS and PNS. Development 127:1039–1048PubMedPubMedCentralGoogle Scholar
  7. Bermingham NA, Hassan BA, Wang VY, Fernandez M, Banfi S, Bellen HJ, Fritzsch B, Zoghbi HY (2001) Proprioceptor pathway development is dependent on Math1. Neuron 30:411–422PubMedCrossRefPubMedCentralGoogle Scholar
  8. Bloch-Gallego E, Ezan F, Tessier-Lavigne M, Sotelo C (1999) Floor plate and netrin-1 are involved in the migration and survival of inferior olivary neurons. J Neurosci 19:4407–4420PubMedCrossRefPubMedCentralGoogle Scholar
  9. Cambronero F, Puelles L (2000) Rostrocaudal nuclear relationships in the avian medulla oblongata: a fate map with quail chick chimeras. J Comp Neurol 427:522–545PubMedCrossRefPubMedCentralGoogle Scholar
  10. Carletti B, Rossi F (2008) Neurogenesis in the cerebellum. Neuroscientist 14:91–100PubMedCrossRefPubMedCentralGoogle Scholar
  11. Carletti B, Grimaldi P, Magrassi L, Rossi F (2002) Specification of cerebellar progenitors after heterotopic-heterochronic transplantation to the embryonic CNS in vivo and in vitro. J Neurosci 22:7132–7146PubMedCrossRefPubMedCentralGoogle Scholar
  12. Chan-Palay V, Palay SL, Brown JT, Van Itallie C (1977) Sagittal organization of olivocerebellar and reticulocerebellar projections: autoradiographic studies with 35S-methionine. Exp Brain Res 30:561–576PubMedCrossRefPubMedCentralGoogle Scholar
  13. Chizhikov V, Millen KJ (2003) Development and malformations of the cerebellum in mice. Mol Genet Metab 80:54–65PubMedCrossRefPubMedCentralGoogle Scholar
  14. Chizhikov VV, Lindgren AG, Currle DS, Rose MF, Monuki ES, Millen KJ (2006) The roof plate regulates cerebellar cell-type specification and proliferation. Development 133:2793–2804CrossRefGoogle Scholar
  15. Cramer KS, Fraser SE, Rubel EW (2000) Embryonic origins of auditory brain-stem nuclei in the chick hindbrain. Dev Biol 224:138–151PubMedCrossRefPubMedCentralGoogle Scholar
  16. De Luca A, Parmigiani E, Tosatto G, Martire S, Hoshino M, Buffor A, Leto K, Rossi F (2015) Exogenous Sonic Hedgehog modulates the pool of GABAergic interneurons during cerebellar development. Cerebellum 14:72–85PubMedCrossRefPubMedCentralGoogle Scholar
  17. De Zeeuw CI, Berrebi AS (1995) Postsynaptic targets of Purkinje cell terminals in the cerebellar and vestibular nuclei of the rat. Eur J Neurosci 7:2322–2333PubMedCrossRefPubMedCentralGoogle Scholar
  18. Englund C, Kowalczyk T, Daza RA, Dagan A, Lau C, Rose MF, Hevner RF (2006) Unipolar brush cells of the cerebellum are produced in the rhombic lip and migrate through developing white matter. J Neurosci 26:9184–9195CrossRefGoogle Scholar
  19. Farago AF, Awatramani RB, Dymecki SM (2006) Assembly of the brainstem cochlear nuclear complex is revealed by intersectional and subtractive genetic fate maps. Neuron 50:205–218PubMedCrossRefPubMedCentralGoogle Scholar
  20. Feng X, Juan AH, Wang HA, Ko KD, Zare H, Sartorelli V (2016) Polycomb Ezh2 controls the fate of GABAergic neurons in the embryonic cerebellum. Development 143:1971–1980PubMedPubMedCentralCrossRefGoogle Scholar
  21. Fleming JT, He W, Hao C, Ketova T, Pan FC, Wright CC, Litingtung Y, Chaing C (2013) The Purkinje neuron act as a central regulator of spatially and functionally distinct cerebellar precursors. Dev Cell 27:278–292PubMedCrossRefPubMedCentralGoogle Scholar
  22. Flora A, Garcia JJ, Thaller C, Zoghbi HY (2007) The E-protein Tcf4 interacts with Math1 to regulate differentiation of a specific subset of neuronal progenitors. Proc Natl Acad Sci U S A 104:15382–15387PubMedPubMedCentralCrossRefGoogle Scholar
  23. 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 136:2049–2058PubMedCrossRefPubMedCentralGoogle Scholar
  24. 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 328:422–433PubMedCrossRefPubMedCentralGoogle Scholar
  25. Hashimoto M, Mikoshiba K (2003) Mediolateral compartmentalization of the cerebellum is determined on the “birth date” of Purkinje cells. J Neurosci 23:11342–11351PubMedCrossRefPubMedCentralGoogle Scholar
  26. Hatanaka Y, Zhu Y, Torigoe M, Kita Y, Murakami F (2016) From migration to settlement: the pathways, migration modes and dynamics of neurons in the developing brain. Proc Jpn Acad Ser B Phys Biol Sci 92:1–19PubMedPubMedCentralCrossRefGoogle Scholar
  27. Hoshino M (2006) Molecular machinery governing GABAergic neuron specification in the cerebellum. Cerebellum 5:193–198PubMedCrossRefPubMedCentralGoogle Scholar
  28. 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 47:201–213CrossRefGoogle Scholar
  29. Huang Y, Zhang Q, Song NN, Zhang L, Sun YL, Hu L, Chen JY, Zhu W, Li J, Ding YQ (2016) Lrp5/6 are required for cerebellar development and for suppressing TH expression in Purkinje cells via β-catenin. Mol Brain 9:7PubMedPubMedCentralCrossRefGoogle Scholar
  30. Huard JM, Forster CC, Carter ML, Sicinski P, Ross ME (1999) Cerebellar histogenesis is disturbed in mice lacking cyclin D2. Development 126:1927–1935PubMedPubMedCentralGoogle Scholar
  31. Ivanova A, Yuasa S (1998) Neuronal migration and differentiation in the development of the mouse dorsal cochlear nucleus. Dev Neurosci 20:495–511PubMedCrossRefPubMedCentralGoogle Scholar
  32. Jankovski A, Rossi F, Sotelo C (1996) Neuronal precursors in the postnatal mouse cerebellum are fully committed cells: evidence from heterochronic transplantations. Eur J Neurosci 8:2308–2319PubMedCrossRefPubMedCentralGoogle Scholar
  33. Jin K, Jiang H, Xiao D, Zou M, Zhu J, Xiang M (2015) Tfap2a and 2b act downstream of Ptf1a to promote amacrine cell differentiation during retinogenesis. Mol Brain 8:28PubMedPubMedCentralCrossRefGoogle Scholar
  34. Ju J, Liu Q, Zhang Y, Liu Y, Jiang M, Zhang L, He X, Peng C, Zheng T, Lu QR, Li H (2017) Olig2 regulates Purkinje cell generation in the early developing mouse cerebellum. Sci Rep 6:30711CrossRefGoogle Scholar
  35. Kawauchi D, Taniguchi H, Watanabe H, Saito T, Murakami F (2006) Direct visualization of nucleogenesis by precerebellar neurons: involvement of ventricle-directed, radial fibre-associated migration. Development 133:1113–1123PubMedCrossRefGoogle Scholar
  36. Kobayashi H, Kawauchi D, Hashimoto Y, Ogata T, Murakami F (2013) The control of precerebellar neuron migration by RNA-binding protein Csde1. Neuroscience 253:292–303PubMedCrossRefGoogle Scholar
  37. Kobayashi H, Saragai S, Naito A, Ichio K, Kawauchi D, Murakami F (2015) Calm1 signaling pathway is essential for the migration of mouse precerebellar neurons. Development 142:375–384PubMedCrossRefGoogle Scholar
  38. Kyriakopoulou K, de Diego I, Wassef M, Karagogeos D (2002) A combination of chain and neurophilic migration involving the adhesion molecule TAG-1 in the caudal medulla. Development 129:287–296PubMedGoogle Scholar
  39. Landsberg RL, Awatramani RB, Hunter NL, Farago AF, DiPietrantonio HJ, Rodriguez CI, Dymecki SM (2005) Hindbrain rhombic lip is comprised of discrete progenitor cell populations allocated by Pax6. Neuron 48:933–947PubMedCrossRefGoogle Scholar
  40. Lee KJ, Dietrich P, Jessell TM (2000) Genetic ablation reveals that the roof plate is essential for dorsal interneuron specification. Nature 403:734–740PubMedCrossRefPubMedCentralGoogle Scholar
  41. Leto K, Carletti B, Williams IM, Magrassi L, Rossi F (2006) Different types of cerebellar GABAergic interneurons originate from a common pool of multipotent progenitor cells. J Neurosci 26:11682–11694PubMedCrossRefPubMedCentralGoogle Scholar
  42. Leto K, Bartolini A, Yanagawa Y, Obata K, Magrassi L, Schilling K, Rossi F (2009) Laminar fate and phenotype specification of cerebellar GABAergic interneurons. J Neurosci 29:7079–7091PubMedCrossRefPubMedCentralGoogle Scholar
  43. Li S, Qiu F, Xu A, Price SM, Xiang M (2004) Barhl1 regulates migration and survival of cerebellar granule cells by controlling expression of the neurotrophin-3 gene. J Neurosci 24:3104–3114PubMedCrossRefPubMedCentralGoogle Scholar
  44. Liu Z, Li H, Hu X, Yu L, Liu H, Han R, Colella R, Mower GD, Chen Y, Qiu M (2008) Control of precerebellar neuron development by Olig3 bHLH transcription factor. J Neurosci 28:10124–10133PubMedPubMedCentralCrossRefGoogle Scholar
  45. Lundell TG, Zhou Q, Doughty ML (2009) Neurogenin1 expression in cell lineages of the cerebellar cortex in embryonic and postnatal mice. Dev Dyn 238:3310–3325PubMedCrossRefPubMedCentralGoogle Scholar
  46. Machold R, Fishell G (2005) Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron 48:17–24CrossRefGoogle Scholar
  47. Machold RP, Kittell DJ, Fishell GJ (2007) Antagonism between Notch and bone morphogenetic protein receptor signaling regulates neurogenesis in the cerebellar rhombic lip. Neural Dev 2:5PubMedPubMedCentralCrossRefGoogle Scholar
  48. Maricich SM, Herrup K (1999) Pax-2 expression defines a subset of GABAergic interneurons and their precursors in the developing murine cerebellum. J Neurobiol 41:281–294PubMedCrossRefPubMedCentralGoogle Scholar
  49. Mathis L, Nicolas JF (2003) Progressive restriction of cell fates in relation to neuroepithelial cell mingling in the mouse cerebellum. Dev Biol 258:20–31PubMedCrossRefPubMedCentralGoogle Scholar
  50. Mathis L, Bonnerot C, Puelles L, Nicolas JF (1997) Retrospective clonal analysis of the cerebellum using genetic laacZ/lacZ mouse mosaics. Development 124:4089–4104Google Scholar
  51. Millet S, Bloch-Gallego E, Simeone A, Alvarado-Mallart RM (1996) The caudal limit of Otx2 gene expression as a marker of the midbrain/hindbrain boundary: a study using in situ hybridisation and chick/quail homotopic grafts. Development 122:3785–3797PubMedPubMedCentralGoogle Scholar
  52. Millonig JH, Millen KJ, Hatten ME (2000) The mouse Dreher gene Lmx1a controls formation of the roof plate in the vertebrate CNS. Nature 403:764–769PubMedCrossRefPubMedCentralGoogle Scholar
  53. 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 8:418–423PubMedCrossRefPubMedCentralGoogle Scholar
  54. Mizuhara E, Minaki Y, Nakatani T, Kumai M, Inoue T, Muguruma K, Sasai Y, Ono Y (2010) Purkinje cells originate from cerebellar ventricular zone progenitors positive for Neph3 and E-cadherin. Dev Biol 338:202–214PubMedCrossRefPubMedCentralGoogle Scholar
  55. Morales D, Hatten ME (2006) Molecular markers of neuronal progenitors in the embryonic cerebellar anlage. J Neurosci 26:12226–12236CrossRefGoogle Scholar
  56. Muguruma K, Nishiyama A, Ono Y, Miyawaki H, Mizuhara E, Hori S, Kakizuka A, Obata K, Yanagawa Y, Hirano T, Sasai Y (2010) Ontogeny-recapitulating generation and tissue integration of ES cell-derived Purkinje cells. Nat Neurosci 13:1171–1180PubMedCrossRefPubMedCentralGoogle Scholar
  57. Nichols DH, Bruce LL (2006) Migratory routes and fates of cells transcribing the Wnt-1 gene in the murine hindbrain. Dev Dyn 235:285–300PubMedCrossRefPubMedCentralGoogle Scholar
  58. Nishida K, Nakayama K, Yoshimura S, Murakami F (2011) Role of Neph2 in pontine nuclei formation in the developing hindbrain. Mol Cell Neurosci 46:662–670PubMedCrossRefPubMedCentralGoogle Scholar
  59. Okada T, Keino-Masu K, Masu M (2007) Migration and nucleogenesis of mouse precerebellar neurons visualized by in utero electroporation of a green fluorescent protein gene. Neurosci Res 57:40–49PubMedCrossRefPubMedCentralGoogle Scholar
  60. Owa T, Taya S, Miyashita S, Yamashita M, Adachi T, Yamada K, Yokoyama M, Aida S, Nishioka T, Yukiko UI, Goitsuka R, Nakamura T, Inoue T, Kaibuchi K, Hoshino M (2018) Meis1 coordi-nates cerebellar granule cell development by regulating Pax6 transcription, BMP signaling and Atoh1 degradation. J Neurosci 38:1277–1294PubMedCrossRefPubMedCentralGoogle Scholar
  61. 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 U S A 104:5193–5198PubMedPubMedCentralCrossRefGoogle Scholar
  62. Pierce ET (1967) Histogenesis of the dorsal and ventral cochlear nuclei in the mouse. An autoradiographic study. J Comp Neurol 131:27–54PubMedCrossRefPubMedCentralGoogle Scholar
  63. Pierce ET (1973) Time of origin of neurons in the brain stem of the mouse. Prog Brain Res 40:53–65PubMedCrossRefPubMedCentralGoogle Scholar
  64. Ramon y Cajal S (1911) Histologie du Systeme Nerveux de l’Homme et des Vertebres. Maloine, ParisGoogle Scholar
  65. Rodriguez CI, Dymecki SM (2000) Origin of the precerebellar system. Neuron 27:475–486PubMedCrossRefPubMedCentralGoogle Scholar
  66. Ruigrok TJ, Cella F, Voogd J (1995) Connections of the lateral reticular nucleus to the lateral vestibular nucleus in the rat. An anterograde tracing study with Phaseolus vulgaris leucoagglutinin. Eur J Neurosci 7:1410–1413PubMedCrossRefPubMedCentralGoogle Scholar
  67. Sellick GS, Barker KT, Stolte-Dijkstra I, Fleischmann C, Coleman RJ, Garrett C, Gloyn AL, Edghill EL, Hattersley AT, Wellauer PK, Goodwin G, Houlston RS (2004) Mutations in PTF1A cause pancreatic and cerebellar agenesis. Nat Genet 36:1301–1305PubMedCrossRefPubMedCentralGoogle Scholar
  68. Seto Y, Nakatani T, Masuyama N, Taya S, Kumai M, Minaki Y, Hamaguchi A, Inoue YU, Inoue T, Miyashita S, Fujiyama T, Yamada M, Chapman H, Campbell K, Magnuson MA, Wright CV, Kawaguchi Y, Ikenaka K, Takebayashi H, Ishiwata S, Ono Y, Hoshino M (2014) Temporal identity transition from Purkinje cell progenitors to GABAergic interneuron progenitors in the cerebellum. Nat Commun 5:3337PubMedPubMedCentralCrossRefGoogle Scholar
  69. Shinohara M, Zhu Y, Murakami F (2013) Four-dimensional analysis of nucleogenesis of the pontine nucleus in the hindbrain. J Comp Neurol 521:3340–3357PubMedCrossRefPubMedCentralGoogle Scholar
  70. Storm R, Cholewa-Waclaw J, Reuter K, Brohl D, Sieber M, Treier M, Muller T, Birchmeier C (2009) The bHLH transcription factor Olig3 marks the dorsal neuroepithelium of the hindbrain and is essential for the development of brainstem nuclei. Development 136:295–305PubMedCrossRefPubMedCentralGoogle Scholar
  71. Sultan F, Czubayko U, Thier P (2003) Morphological classification of the rat lateral cerebellar nuclear neurons by principal component analysis. J Comp Neurol 455:139–155PubMedCrossRefPubMedCentralGoogle Scholar
  72. Tan K, Le Douarin NM (1991) Development of the nuclei and cell migration in the medulla oblongata. Application of the quail-chick chimera system. Anat Embryol (Berl) 183:321–343CrossRefGoogle Scholar
  73. Wang VY, Rose MF, Zoghbi HY (2005) Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron 48:31–43CrossRefGoogle Scholar
  74. Weisheit G, Gliem M, Endl E, Pfeffer PL, Busslinger M, Schilling K (2006) Postnatal development of the murine cerebellar cortex: formation and early dispersal of basket, stellate and Golgi neurons. Eur J Neurosci 24:466–478PubMedCrossRefPubMedCentralGoogle Scholar
  75. Wilson SW, Rubenstein JL (2000) Induction and dorsoventral patterning of the telencephalon. Neuron 28:641–651PubMedCrossRefPubMedCentralGoogle Scholar
  76. Wingate RJ, Hatten ME (1999) The role of the rhombic lip in avian cerebellum development. Development 126:4395–4404PubMedPubMedCentralGoogle Scholar
  77. 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 27:10924–10934CrossRefGoogle Scholar
  78. Yamada M, Seto Y, Taya S, Owa T, Inoue YU, Inoue T, Kawaguchi Y, Nabeshima Y, Hoshino M (2014) Specification of spatial identities of cerebellar neuron progenitors by Ptf1a and Atoh1 for proper production of GABAergic and glutamatergic neurons. J Neurosci 34:4786–4800PubMedCrossRefGoogle Scholar
  79. Yee KT, Simon HH, Tessier-Lavigne M, O’Leary DM (1999) Extension of long leading processes and neuronal migration in the mammalian brain directed by the chemoattractant netrin-1. Neuron 24:607–622PubMedCrossRefGoogle Scholar
  80. Yeung J, Goldowitz D (2017) Wls expression in the rhombic lip orchestrates the embryonic development of the mouse cerebellum. Neuroscience 354:30–42PubMedCrossRefPubMedCentralGoogle Scholar
  81. Yeung J, Ha TJ, Swanson DJ, Choi K, Tong Y, Goldowitz D (2014) Wls provides a new compartmental view of the rhombic lip in mouse cerebellar development. J Neurosci 34:12527–37PubMedCrossRefPubMedCentralGoogle Scholar
  82. Young RA (2011) Control of the embryonic stem cell state. Cell 144:940–954PubMedPubMedCentralCrossRefGoogle Scholar
  83. Zainolabidin N, Kamath SP, Thanawalla AR, Chen AI (2017) Distinct activities of Tfap2A and Tfap2B in the specification of GABAergic interneurons in the developing cerebellum. Front Mol Neurosci 10:281PubMedPubMedCentralCrossRefGoogle Scholar
  84. Zervas M, Millet S, Ahn S, Joyner AL (2004) Cell behaviors and genetic lineages of the mesencephalon and rhombomere 1. Neuron 43:345–357CrossRefGoogle Scholar
  85. 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 U S A 104:13182–13186PubMedPubMedCentralCrossRefGoogle Scholar
  86. Zordan P, Croci L, Hawkes R, Consalez GG (2008) Comparative analysis of proneural gene expression in the embryonic cerebellum. Dev Dyn 237:1726–1735CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Mikio Hoshino
    • 1
    Email author
  • Satoshi Miyashita
    • 1
  • Yusuke Seto
    • 1
    • 2
  • Mayumi Yamada
    • 1
    • 3
  1. 1.Department of Biochemistry and Cellular BiologyNational Institute of Neuroscience, National Center of Neurology and PsychiatryTokyoJapan
  2. 2.Laboratory of Developmental Systems, Institute for Frontier Life and Medical SciencesKyoto UniversityKyotoJapan
  3. 3.Laboratory of Brain Development and Regeneration, Graduate School of BiostudiesKyoto UniversityKyotoJapan

Section editors and affiliations

  • Roy V. Sillitoe
    • 1
  1. 1.Department of Pathology and ImmunologyBaylor College of Medicine, Jan and Dan Duncan Neurological Research InstituteHoustonUSA

Personalised recommendations