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Cerebellar Development and Neurogenesis in Zebrafish

  • Jan KaslinEmail author
  • Michael BrandEmail author
Living reference work entry
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Abstract

Cerebellar organization and function have been studied in numerous species of fish. Fish models such as goldfish, weakly electric fish, and sharks have led to important findings about the cerebellar architecture, cerebellar circuit physiology, and brain evolution. However, most of the studied fish models are not well suited for developmental and genetic studies of the cerebellum. The rapid transparent ex utero development in zebrafish allows direct access and precise visualization of all the major events in cerebellar development. Furthermore, the zebrafish is amenable to high-throughput screening techniques and advanced forward and reverse genetics approaches allowing interrogation and identification of genes and molecules in cerebellar development. The superficial position of the cerebellar primordium and the cerebellum facilitates in vivo imaging and physiological measurements of individual cerebellar cells or circuits. In addition, cerebellar neurogenesis and regeneration can be studied in the adult animal. Taken together, these features have allowed zebrafish to emerge as a complete model for studies of molecular, cellular, and physiological mechanisms involved in cerebellar development, function, and repair at cell and circuit level.

Keywords

Zebrafish Teleost Fish Adult neurogenesis Mutant Eurydendroid cell Genetic model Cerebellar development Morphogenesis Mid-hindbrain-boundary Isthmic organizer In vivo imaging Cerebellar regeneration 

References

  1. Adolf B, Bellipanni G, Huber V, Bally-Cuif L (2004) atoh1.2 and beta3.1 are two new bHLH-encoding genes expressed in selective precursor cells of the zebrafish anterior hindbrain. Gene Expr Patterns 5(1):35–41PubMedCrossRefPubMedCentralGoogle Scholar
  2. Alonso JR, Arevalo R, Brinon JG, Lara J, Weruaga E, Aijon J (1992) Parvalbumin immunoreactive neurons and fibres in the teleost cerebellum. Anat Embryol 185(4):355–361PubMedCrossRefPubMedCentralGoogle Scholar
  3. Altman J, Bayer SA (1997) Development of the cerebellar system: in relation to its evolution, structure, and functions. CRC Press, Boca RatonGoogle Scholar
  4. Alvarado-Mallart RM (2005) The chick/quail transplantation model: discovery of the isthmic organizer center. Brain Res 49(2):109–113CrossRefGoogle Scholar
  5. Ambrosi G, Flace P, Lorusso L, Girolamo F, Rizzi A, Bosco L, Errede M, Virgintino D, Roncali L, Benagiano V (2007) Non-traditional large neurons in the granular layer of the cerebellar cortex. Eur J Histochem 51(Suppl 1):59–64PubMedPubMedCentralGoogle Scholar
  6. Ampatzis K, Dermon CR (2007) Sex differences in adult cell proliferation within the zebrafish (Danio rerio) cerebellum. Eur J Neurosci 25(4):1030–1040PubMedCrossRefPubMedCentralGoogle Scholar
  7. Bae YK, Kani S, Shimizu T, Tanabe K, Nojima H, Kimura Y, Higashijima S, Hibi M (2009) Anatomy of zebrafish cerebellum and screen for mutations affecting its development. Dev Biol 330(2):406–426PubMedCrossRefPubMedCentralGoogle Scholar
  8. Bell CC (2002) Evolution of cerebellum-like structures. Brain Behav Evol 59(5–6):312–326PubMedCrossRefPubMedCentralGoogle Scholar
  9. Bell CC, Han V, Sawtell NB (2008) Cerebellum-like structures and their implications for cerebellar function. Annu Rev Neurosci 31:1–24PubMedCrossRefPubMedCentralGoogle Scholar
  10. Belting HG, Hauptmann G, Meyer D, Abdelilah-Seyfried S, Chitnis A, Eschbach C, Soll I, Thisse C, Thisse B, Artinger KB, Lunde K, Driever W (2001) Spiel ohne grenzen/pou2 is required during establishment of the zebrafish midbrain-hindbrain boundary organizer. Development 128(21):4165–4176PubMedPubMedCentralGoogle Scholar
  11. 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(6656):169–172PubMedCrossRefPubMedCentralGoogle Scholar
  12. Brand M, Heisenberg CP, Jiang YJ, Beuchle D, Lun K, Furutani-Seiki M, Granato M, Haffter P, Hammerschmidt M, Kane DA, Kelsh RN, Mullins MC, Odenthal J, van Eeden FJ, Nusslein-Volhard C (1996) Mutations in zebrafish genes affecting the formation of the boundary between midbrain and hindbrain. Development 123:179–190PubMedPubMedCentralGoogle Scholar
  13. Broccoli V, Boncinelli E, Wurst W (1999) The caudal limit of Otx2 expression positions the isthmic organizer. Nature 401(6749):164–168PubMedCrossRefPubMedCentralGoogle Scholar
  14. Buckles GR, Thorpe CJ, Ramel MC, Lekven AC (2004) Combinatorial Wnt control of zebrafish midbrain-hindbrain boundary formation. Mech Dev 121(5):437–447PubMedCrossRefPubMedCentralGoogle Scholar
  15. Burgess S, Reim G, Chen W, Hopkins N, Brand M (2002) The zebrafish spiel-ohne-grenzen (spg) gene encodes the POU domain protein Pou2 related to mammalian Oct4 and is essential for formation of the midbrain and hindbrain, and for pre-gastrula morphogenesis. Development 129(4):905–916PubMedPubMedCentralGoogle Scholar
  16. Butler AB, Hodos W (2005) Comparative vertebrate neuroanatomy, 2nd edn. Wiley, New YorkCrossRefGoogle Scholar
  17. Butts T, Hanzel M, Wingate RJ (2014a) Transit amplification in the amniote cerebellum evolved via a heterochronic shift in NeuroD1 expression. Development 141(14):2791–2795.  https://doi.org/10.1242/dev.101758CrossRefPubMedPubMedCentralGoogle Scholar
  18. Butts T, Modrell MS, Baker CV, Wingate RJ (2014b) The evolution of the vertebrate cerebellum: absence of a proliferative external granule layer in a non-teleost ray-finned fish. Evol Dev 16(2):92–100.  https://doi.org/10.1111/ede.12067CrossRefPubMedPubMedCentralGoogle Scholar
  19. Canning CA, Lee L, Irving C, Mason I, Jones CM (2007) Sustained interactive Wnt and FGF signaling is required to maintain isthmic identity. Dev Biol 305(1):276–286PubMedCrossRefPubMedCentralGoogle Scholar
  20. Carletti B, Rossi F (2008) Neurogenesis in the cerebellum. Neuroscientist 14(1):91–100PubMedCrossRefPubMedCentralGoogle Scholar
  21. Chaplin N, Tendeng C, Wingate RJ (2010) Absence of an external germinal layer in zebrafish and shark reveals a distinct, anamniote ground plan of cerebellum development. J Neurosci 30(8):3048–3057PubMedPubMedCentralCrossRefGoogle Scholar
  22. Costagli A, Kapsimali M, Wilson SW, Mione M (2002) Conserved and divergent patterns of Reelin expression in the zebrafish central nervous system. J Comp Neurol 450(1):73–93PubMedCrossRefPubMedCentralGoogle Scholar
  23. Crook J, Hendrickson A, Robinson FR (2006) Co-localization of glycine and gaba immunoreactivity in interneurons in Macaca monkey cerebellar cortex. Neuroscience 141(4):1951–1959PubMedCrossRefPubMedCentralGoogle Scholar
  24. Dahmane N, Ruiz i Altaba A (1999) Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126(14):3089–3100PubMedPubMedCentralGoogle Scholar
  25. Delgado L, Schmachtenberg O (2008) Immunohistochemical localization of GABA, GAD65, and the receptor subunits GABAAalpha1 and GABAB1 in the zebrafish cerebellum. Cerebellum 7(3):444–450PubMedCrossRefPubMedCentralGoogle Scholar
  26. Devor A (2000) Is the cerebellum like cerebellar-like structures? Brain Res 34(3):149–156CrossRefGoogle Scholar
  27. Elsen GE, Choi LY, Millen KJ, Grinblat Y, Prince VE (2008) Zic1 and Zic4 regulate zebrafish roof plate specification and hindbrain ventricle morphogenesis. Dev Biol 314(2):376–392PubMedCrossRefPubMedCentralGoogle Scholar
  28. Elsen GE, Choi LY, Prince VE, Ho RK (2009) The autism susceptibility gene met regulates zebrafish cerebellar development and facial motor neuron migration. Dev Biol 335(1):78–92PubMedPubMedCentralCrossRefGoogle Scholar
  29. 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(36):9184–9195PubMedPubMedCentralCrossRefGoogle Scholar
  30. Finger TE (1978) Efferent neurons of the teleost cerebellum. Brain Res 153(3):608–614PubMedCrossRefPubMedCentralGoogle Scholar
  31. Finger TE (1983) Organization of the teleost cerebellum. In: Northcutt RG, Davis RE (eds) Fish neurobiology. Brain stem and sense organs, vol 1. University of Michigan Press, Ann Arbor, pp 261–284Google Scholar
  32. Fink AJ, Englund C, Daza RA, Pham D, Lau C, Nivison M, Kowalczyk T, Hevner RF (2006) Development of the deep cerebellar nuclei: transcription factors and cell migration from the rhombic lip. J Neurosci 26(11):3066–3076PubMedPubMedCentralCrossRefGoogle Scholar
  33. Folgueira M, Anadon R, Yanez J (2006) Afferent and efferent connections of the cerebellum of a salmonid, the rainbow trout (Oncorhynchus mykiss): a tract-tracing study. J Comp Neurol 497(4):542–565PubMedCrossRefPubMedCentralGoogle Scholar
  34. Foucher I, Mione M, Simeone A, Acampora D, Bally-Cuif L, Houart C (2006) Differentiation of cerebellar cell identities in absence of Fgf signalling in zebrafish Otx morphants. Development 133(10):1891–1900PubMedCrossRefPubMedCentralGoogle Scholar
  35. Gibbs MA, Northmore DP (1996) The role of torus longitudinalis in equilibrium orientation measured with the dorsal light reflex. Brain Behav Evol 48(3):115–120PubMedCrossRefPubMedCentralGoogle Scholar
  36. Gona AG (1976) Autoradiographic studies of cerebellar histogenesis in the bullfrog tadpole during metamorphosis: the external granular layer. J Comp Neurol 165:77–87PubMedCrossRefPubMedCentralGoogle Scholar
  37. Hans S, Kaslin J, Freudenreich D, Brand M (2009) Temporally-controlled site-specific recombination in zebrafish. PLoS One 4(2):e4640PubMedPubMedCentralCrossRefGoogle Scholar
  38. Hoshino M (2006) Molecular machinery governing GABAergic neuron specification in the cerebellum. Cerebellum 5(3):193–198PubMedCrossRefPubMedCentralGoogle Scholar
  39. 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):201–213PubMedCrossRefPubMedCentralGoogle Scholar
  40. Housden BE, Muhar M, Gemberling M, Gersbach CA, Stainier DYR, Seydoux G, Mohr SE, Zuber J, Perrimon N (2016) Loss-of-function genetic tools for animal models: cross-species and cross-platform differences. Nat Rev Genet 18:24.  https://doi.org/10.1038/nrg.2016.118CrossRefPubMedPubMedCentralGoogle Scholar
  41. Ikenaga T, Yoshida M, Uematsu K (2002) Efferent connections of the cerebellum of the goldfish, Carassius auratus. Brain Behav Evol 60(1):36–51PubMedCrossRefPubMedCentralGoogle Scholar
  42. Ikenaga T, Yoshida M, Uematsu K (2005) Morphology and immunohistochemistry of efferent neurons of the goldfish corpus cerebelli. J Comp Neurol 487(3):300–311PubMedCrossRefPubMedCentralGoogle Scholar
  43. Ikenaga T, Yoshida M, Uematsu K (2006) Cerebellar efferent neurons in teleost fish. Cerebellum 5(4):268–274PubMedPubMedCentralCrossRefGoogle Scholar
  44. Ito H, Yoshimoto M (1990) Cytoarchitecture and fiber connections of the nucleus lateralis valvulae in the carp (Cyprinus carpio). J Comp Neurol 298(4):385–399PubMedCrossRefPubMedCentralGoogle Scholar
  45. Jaszai J, Reifers F, Picker A, Langenberg T, Brand M (2003) Isthmus-to-midbrain transformation in the absence of midbrain-hindbrain organizer activity. Development 130(26):6611–6623PubMedCrossRefPubMedCentralGoogle Scholar
  46. Joyner AL (1996) Engrailed, Wnt and Pax genes regulate midbrain – hindbrain development. Trends Genet 12(1):15–20PubMedCrossRefPubMedCentralGoogle Scholar
  47. Kani S, Bae YK, Shimizu T, Tanabe K, Satou C, Parsons MJ, Scott E, Higashijima S, Hibi M (2010) Proneural gene-linked neurogenesis in zebrafish cerebellum. Dev Biol 343(1–2):1–17PubMedCrossRefPubMedCentralGoogle Scholar
  48. Kaslin J, Ganz J, Geffarth M, Grandel H, Hans S, Brand M (2009) Stem cells in the adult zebrafish cerebellum: initiation and maintenance of a novel stem cell niche. J Neurosci 29(19):6142–6153.  https://doi.org/10.1523/JNEUROSCI.0072-09.2009CrossRefPubMedPubMedCentralGoogle Scholar
  49. Kaslin J, Kroehne V, Benato F, Argenton F, Brand M (2013) Development and specification of cerebellar stem and progenitor cells in zebrafish: from embryo to adult. Neural Dev 8:9.  https://doi.org/10.1186/1749-8104-8-9CrossRefPubMedPubMedCentralGoogle Scholar
  50. Kaslin J, Kroehne V, Ganz J, Hans S, Brand M (2017) Distinct roles of neuroepithelial-like and radial glia-like stem and progenitor cells in cerebellar regeneration. Development 144(8):1462–1471.  https://doi.org/10.1242/dev.144907CrossRefPubMedPubMedCentralGoogle Scholar
  51. Katahira T, Sato T, Sugiyama S, Okafuji T, Araki I, Funahashi J, Nakamura H (2000) Interaction between Otx2 and Gbx2 defines the organizing center for the optic tectum. Mech Dev 91(1–2):43–52PubMedCrossRefPubMedCentralGoogle Scholar
  52. Katsuyama Y, Oomiya Y, Dekimoto H, Motooka E, Takano A, Kikkawa S, Hibi M, Terashima T (2007) Expression of zebrafish ROR alpha gene in cerebellar-like structures. Dev Dyn 236(9):2694–2701PubMedCrossRefPubMedCentralGoogle Scholar
  53. Kim CH, Bae YK, Yamanaka Y, Yamashita S, Shimizu T, Fujii R, Park HC, Yeo SY, Huh TL, Hibi M, Hirano T (1997) Overexpression of neurogenin induces ectopic expression of HuC in zebrafish. Neurosci Lett 239(2–3):113–116PubMedCrossRefPubMedCentralGoogle Scholar
  54. Koster RW, Fraser SE (2001) Direct imaging of in vivo neuronal migration in the developing cerebellum. Curr Biol 11(23):1858–1863PubMedCrossRefPubMedCentralGoogle Scholar
  55. Koster RW, Fraser SE (2006) FGF signaling mediates regeneration of the differentiating cerebellum through repatterning of the anterior hindbrain and reinitiation of neuronal migration. J Neurosci 26(27):7293–7304PubMedPubMedCentralCrossRefGoogle Scholar
  56. Laine J, Axelrad H (1994) The candelabrum cell: a new interneuron in the cerebellar cortex. J Comp Neurol 339(2):159–173PubMedCrossRefPubMedCentralGoogle Scholar
  57. Langenberg T, Dracz T, Oates AC, Heisenberg CP, Brand M (2006) Analysis and visualization of cell movement in the developing zebrafish brain. Dev Dyn 235(4):928–933PubMedCrossRefPubMedCentralGoogle Scholar
  58. Lekven AC, Buckles GR, Kostakis N, Moon RT (2003) Wnt1 and wnt10b function redundantly at the zebrafish midbrain-hindbrain boundary. Dev Biol 254(2):172–187PubMedCrossRefPubMedCentralGoogle Scholar
  59. Leucht C, Stigloher C, Wizenmann A, Klafke R, Folchert A, Bally-Cuif L (2008) MicroRNA-9 directs late organizer activity of the midbrain-hindbrain boundary. Nat Neurosci 11(6):641–648PubMedCrossRefPubMedCentralGoogle Scholar
  60. Li M, Zhao L, Page-McCaw PS, Chen W (2016) Zebrafish genome engineering using the CRISPR-Cas9 system. Trends Genet 32(12):815–827.  https://doi.org/10.1016/j.tig.2016.10.005CrossRefPubMedPubMedCentralGoogle Scholar
  61. Lindsey BW, Douek AM, Loosli F, Kaslin J (2018a) A whole brain staining, embedding, and clearing pipeline for adult zebrafish to visualize cell proliferation and morphology in 3-dimensions. Front Neurosci 11(750).  https://doi.org/10.3389/fnins.2017.00750
  62. Lindsey BW, Hall ZJ, Heuze A, Joly JS, Tropepe V, Kaslin J (2018b) The role of neuro-epithelial-like and radial-glial stem and progenitor cells in development, plasticity, and repair. Prog Neurobiol 11(17):30185–30185Google Scholar
  63. Liu A, Joyner AL (2001) Early anterior/posterior patterning of the midbrain and cerebellum. Annu Rev Neurosci 24:869–896PubMedCrossRefPubMedCentralGoogle Scholar
  64. Louvi A, Alexandre P, Metin C, Wurst W, Wassef M (2003) The isthmic neuroepithelium is essential for cerebellar midline fusion. Development 130(22):5319–5330PubMedCrossRefPubMedCentralGoogle Scholar
  65. Lumsden A, Krumlauf R (1996) Patterning the vertebrate neuraxis. Science 274(5290):1109–1115PubMedCrossRefPubMedCentralGoogle Scholar
  66. Lun K, Brand M (1998) A series of no isthmus (noi) alleles of the zebrafish pax2.1 gene reveals multiple signaling events in development of the midbrain-hindbrain boundary. Development 125(16):3049–3062PubMedPubMedCentralGoogle Scholar
  67. Machold R, Fishell G (2005) Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron 48(1):17–24PubMedCrossRefPubMedCentralGoogle Scholar
  68. Martinez S, Alvarado-Mallart RM (1989) Rostral cerebellum originates from the caudal portion of the so-called ‘mesencephalic’ vesicle: a study using chick/quail chimeras. Eur J Neurosci 1(6):549–560PubMedCrossRefPubMedCentralGoogle Scholar
  69. Matsui H, Namikawa K, Babaryka A, Koster RW (2014) Functional regionalization of the teleost cerebellum analyzed in vivo. Proc Natl Acad Sci U S A 111(32):11846–11851.  https://doi.org/10.1073/pnas.1403105111CrossRefPubMedPubMedCentralGoogle Scholar
  70. McFarland KA, Topczewska JM, Weidinger G, Dorsky RI, Appel B (2008) Hh and Wnt signaling regulate formation of olig2+ neurons in the zebrafish cerebellum. Dev Biol 318(1):162–171PubMedPubMedCentralCrossRefGoogle Scholar
  71. Meek J (1983) Functional anatomy of the tectum mesencephali of the goldfish. An explorative analysis of the functional implications of the laminar structural organization of the tectum. Brain Res 287(3):247–297PubMedCrossRefPubMedCentralGoogle Scholar
  72. Meek J (1992) Comparative aspects of cerebellar organization. From mormyrids to mammals. Eur J Morphol 30(1):37–51PubMedPubMedCentralGoogle Scholar
  73. Meek J (1998) Holosteans and teleosts. In: Nieuwenhuys R, ten Donkelaar HJ, Nicholson C (eds) The central nervous system of vertebrates. Springer, BerlinGoogle Scholar
  74. Meek J, Yang JY, Han VZ, Bell CC (2008) Morphological analysis of the mormyrid cerebellum using immunohistochemistry, with emphasis on the unusual neuronal organization of the valvula. J Comp Neurol 510(4):396–421PubMedPubMedCentralCrossRefGoogle Scholar
  75. Millet S, Campbell K, Epstein DJ, Losos K, Harris E, Joyner AL (1999) A role for Gbx2 in repression of Otx2 and positioning the mid/hindbrain organizer. Nature 401(6749):161–164PubMedCrossRefPubMedCentralGoogle Scholar
  76. Mugnaini E, Sekerkova G, Martina M (2011) The unipolar brush cell: a remarkable neuron finally receiving the deserved attention. Brain Res Rev 66:220–245.  https://doi.org/10.1016/j.brainresrev.2010.10.001PubMedCrossRefPubMedCentralGoogle Scholar
  77. Murakami T, Morita Y (1987) Morphology and distribution of the projection neurons in the cerebellum in a teleost, Sebastiscus marmoratus. J Comp Neurol 256(4):607–623PubMedCrossRefPubMedCentralGoogle Scholar
  78. Nieuwenhuys R, Pouwels E, Smulders-Kersten E (1974) The neuronal organization of cerebellar lobe C1 in the mormyrid fish Gnathonemus petersii (teleostei). Z Anat Entwicklungsgesch 144(3):315–336PubMedCrossRefPubMedCentralGoogle Scholar
  79. Northmore DP, Williams B, Vanegas H (1983) The teleostean torus longitudinalis: responses related to eye movements, visuotopic mapping, and functional relations with the optic tectum. J Comp Physiol A 150:39–50CrossRefGoogle Scholar
  80. O’Hara FP, Beck E, Barr LK, Wong LL, Kessler DS, Riddle RD (2005) Zebrafish Lmx1b.1 and Lmx1b.2 are required for maintenance of the isthmic organizer. Development 132(14):3163–3173PubMedPubMedCentralCrossRefGoogle Scholar
  81. 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(12):5193–5198PubMedPubMedCentralCrossRefGoogle Scholar
  82. Picker A, Brennan C, Reifers F, Clarke JD, Holder N, Brand M (1999) Requirement for the zebrafish mid-hindbrain boundary in midbrain polarisation, mapping and confinement of the retinotectal projection. Development 126(13):2967–2978PubMedPubMedCentralGoogle Scholar
  83. Pouwels E (1978) On the development of the cerebellum of the trout, Salmo gairdneri. IV. Development of the pattern of connectivity. Anat Embryol 153(1):55–65PubMedCrossRefPubMedCentralGoogle Scholar
  84. Raible F, Brand M (2004) Divide et Impera – the midbrain-hindbrain boundary and its organizer. Trends Neurosci 27(12):727–734PubMedCrossRefPubMedCentralGoogle Scholar
  85. Reifers F, Bohli H, Walsh EC, Crossley PH, Stainier DY, Brand M (1998) Fgf8 is mutated in zebrafish acerebellar (ace) mutants and is required for maintenance of midbrain-hindbrain boundary development and somitogenesis. Development 125(13):2381–2395PubMedPubMedCentralGoogle Scholar
  86. Reim G, Brand M (2002) Spiel-ohne-grenzen/pou2 mediates regional competence to respond to Fgf8 during zebrafish early neural development. Development 129(4):917–933PubMedPubMedCentralGoogle Scholar
  87. Rhinn M, Brand M (2001) The midbrain--hindbrain boundary organizer. Curr Opin Neurobiol 11(1):34–42PubMedCrossRefPubMedCentralGoogle Scholar
  88. Rhinn M, Lun K, Luz M, Werner M, Brand M (2005) Positioning of the midbrain-hindbrain boundary organizer through global posteriorization of the neuroectoderm mediated by Wnt8 signaling. Development 132(6):1261–1272PubMedCrossRefPubMedCentralGoogle Scholar
  89. Rhinn M, Picker A, Brand M (2006) Global and local mechanisms of forebrain and midbrain patterning. Curr Opin Neurobiol 16(1):5–12PubMedCrossRefPubMedCentralGoogle Scholar
  90. Rhinn M, Lun K, Ahrendt R, Geffarth M, Brand M (2009) Zebrafish gbx1 refines the midbrain-hindbrain boundary border and mediates the Wnt8 posteriorization signal. Neural Dev 4:12PubMedPubMedCentralCrossRefGoogle Scholar
  91. Rieger S, Senghaas N, Walch A, Koster RW (2009) Cadherin-2 controls directional chain migration of cerebellar granule neurons. PLoS Biol 7(11):e1000240PubMedPubMedCentralCrossRefGoogle Scholar
  92. Scott EK (2009) The Gal4/UAS toolbox in zebrafish: new approaches for defining behavioral circuits. J Neurochem 110(2):441–456PubMedCrossRefPubMedCentralGoogle Scholar
  93. Sgaier SK, Millet S, Villanueva MP, Berenshteyn F, Song C, Joyner AL (2005) Morphogenetic and cellular movements that shape the mouse cerebellum; insights from genetic fate mapping. Neuron 45(1):27–40PubMedPubMedCentralGoogle Scholar
  94. 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):2325–2335PubMedPubMedCentralCrossRefGoogle Scholar
  95. Simeone A (2000) Positioning the isthmic organizer where Otx2 and Gbx2meet. Trends Genet 16(6):237–240PubMedCrossRefPubMedCentralGoogle Scholar
  96. Simmich J, Staykov E, Scott E (2012) Zebrafish as an appealing model for optogenetic studies. Prog Brain Res 196:145–162.  https://doi.org/10.1016/B978-0-444-59426-6.00008-2CrossRefPubMedPubMedCentralGoogle Scholar
  97. Takacs J, Markova L, Borostyankoi Z, Gorcs TJ, Hamori J (1999) Metabotrop glutamate receptor type 1a expressing unipolar brush cells in the cerebellar cortex of different species: a comparative quantitative study. J Neurosci Res 55(6):733–748PubMedCrossRefPubMedCentralGoogle Scholar
  98. Tour E, Pillemer G, Gruenbaum Y, Fainsod A (2002) Gbx2 interacts with Otx2 and patterns the anterior-posterior axis during gastrulation in Xenopus. Mech Dev 112(1–2):141–151PubMedCrossRefPubMedCentralGoogle Scholar
  99. Toyama R, Gomez DM, Mana MD, Dawid IB (2004) Sequence relationships and expression patterns of zebrafish zic2 and zic5 genes. Gene Expr Patterns 4(3):345–350PubMedCrossRefPubMedCentralGoogle Scholar
  100. Volkmann K, Rieger S, Babaryka A, Koster RW (2008) The zebrafish cerebellar rhombic lip is spatially patterned in producing granule cell populations of different functional compartments. Dev Biol 313(1):167–180PubMedCrossRefPubMedCentralGoogle Scholar
  101. Volkmann K, Chen YY, Harris MP, Wullimann MF, Koster RW (2010) The zebrafish cerebellar upper rhombic lip generates tegmental hindbrain nuclei by long-distance migration in an evolutionary conserved manner. J Comp Neurol 518(14):2794–2817PubMedPubMedCentralGoogle Scholar
  102. Wang VY, Zoghbi HY (2001) Genetic regulation of cerebellar development. Nat Rev Neurosci 2(7):484–491PubMedCrossRefPubMedCentralGoogle Scholar
  103. 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(1):31–43PubMedCrossRefPubMedCentralGoogle Scholar
  104. Wechsler-Reya RJ, Scott MP (1999) Control of neuronal precursor proliferation in the cerebellum by sonic hedgehog. Neuron 22(1):103–114PubMedCrossRefPubMedCentralGoogle Scholar
  105. Wingate RJ (2001) The rhombic lip and early cerebellar development. Curr Opin Neurobiol 11(1):82–88PubMedCrossRefPubMedCentralGoogle Scholar
  106. Wingate RJ, Hatten ME (1999) The role of the rhombic lip in avian cerebellum development. Development 126(20):4395–4404PubMedPubMedCentralGoogle Scholar
  107. Wullimann MF (1997) The central nervous system. In: Evans DH, Claiborne JB (eds) In physiology of fishes, vol II. CRC Press, Boca RatonGoogle Scholar
  108. Wullimann MF, Northcutt RG (1988) Connections of the corpus cerebelli in the green sunfish and the common goldfish: a comparison of perciform and cypriniform teleosts. Brain Behav Evol 32(5):293–316PubMedCrossRefPubMedCentralGoogle Scholar
  109. Wullimann MF, Northcutt RG (1989) Afferent connections of the valvula cerebelli in two teleosts, the common goldfish and the green sunfish. J Comp Neurol 289(4):554–567PubMedCrossRefPubMedCentralGoogle Scholar
  110. Wurst W, Bally-Cuif L (2001) Neural plate patterning: upstream and downstream of the isthmic organizer. Nat Rev Neurosci 2(2):99–108PubMedCrossRefPubMedCentralGoogle Scholar
  111. Xue HG, Yang CY, Yamamoto N (2008) Afferent sources to the inferior olive and distribution of the olivocerebellar climbing fibers in cyprinids. J Comp Neurol 507(3):1409–1427PubMedPubMedCentralCrossRefGoogle Scholar
  112. Zecchin E, Mavropoulos A, Devos N, Filippi A, Tiso N, Meyer D, Peers B, Bortolussi M, Argenton F (2004) Evolutionary conserved role of ptf1a in the specification of exocrine pancreatic fates. Dev Biol 268(1):174–184PubMedCrossRefPubMedCentralGoogle Scholar

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© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.ARMI- Australian Regenerative Medicine InstituteMonash UniversityMelbourneAustralia
  2. 2.CRTD - Center for Regenerative Therapies TU DresdenTU DresdenDresdenGermany

Section editors and affiliations

  • Noriyuki Koibuchi
    • 1
  1. 1.Department of Integrative PhysiologyGunma University Graduate School of MedicineMaebashiJapan

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