Skip to main content

Deciphering Cerebellar Neural Circuitry Involved in Higher Order Functions Using the Zebrafish Model

  • Chapter
  • First Online:
New Principles in Developmental Processes

Abstract

The central nervous system (CNS) in vertebrate species is one of the most complex structures in the animal body, containing enormous numbers of neurons that connect to each other through their axons and dendrites to carry out complex tasks. Recent comparative anatomical and functional studies of neural circuits in different vertebrate CNS reveal that, although the structure of the CNS is simpler in lower vertebrates (such as teleosts) than that in mammals, the basic organization of neural circuitry in the CNS is conserved and the formation of neural circuits is controlled by similar or identical mechanisms. In this chapter, we focus on the cerebellum, which is derived from the dorsal part of the most anterior hindbrain and is involved in motor control and higher cognitive/emotional functions. We describe the structure and development processes of the cerebellar neurons and neural circuits in zebrafish and compared them with those in mammals. A variety of techniques and resources is available for zebrafish research on neural development and function, including classical reverse genetics, transgenics, and optogenetics. We discuss how studies on neural circuitry in zebrafish provide us with a general scheme of the formation and function of cerebellar neural circuitry in vertebrate species.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Acampora D, Avantaggiato V, Tuorto F, Simeone A (1997) Genetic control of brain morphogenesis through Otx gene dosage requirement. Development (Camb) 124(18):3639–3650

    CAS  Google Scholar 

  • 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):35–41. doi:10.1016/j.modgep.2004.06.009, pii: S1567-133X(04)00093-6

    CAS  PubMed  Google Scholar 

  • Ahrens MB, Li JM, Orger MB, Robson DN, Schier AF, Engert F, Portugues R (2012) Brain-wide neuronal dynamics during motor adaptation in zebrafish. Nature (Lond) 485(7399):471–477. doi:10.1038/nature11057

    CAS  Google Scholar 

  • Ahrens MB, Orger MB, Robson DN, Li JM, Keller PJ (2013) Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat Methods 10(5):413–420. doi:10.1038/nmeth.2434

    CAS  PubMed  Google Scholar 

  • Aizenberg M, Schuman EM (2011) Cerebellar-dependent learning in larval zebrafish. J Neurosci 31(24):8708–8712. doi:10.1523/JNEUROSCI.6565-10.2011

    CAS  PubMed  Google Scholar 

  • Alder J, Cho NK, Hatten ME (1996) Embryonic precursor cells from the rhombic lip are specified to a cerebellar granule neuron identity. Neuron 17(3):389–399, pii: S0896-6273(00)80172-5

    CAS  PubMed  Google Scholar 

  • Alonso JR, Arevalo R, Brinon JG, Lara J, Weruaga E, Aijon J (1992) Parvalbumin immunoreactive neurons and fibres in the teleost cerebellum. Anat Embryol (Berl) 185(4):355–361

    CAS  Google Scholar 

  • Altman J, Bayer SA (1997) Development of the cerebellar system in relation to its evolution, structure, and function. CRC, Boca Raton

    Google Scholar 

  • Apps R, Hawkes R (2009) Cerebellar cortical organization: a one-map hypothesis. Nat Rev Neurosci 10(9):670–681. doi:10.1038/nrn2698

    CAS  PubMed  Google Scholar 

  • Arrenberg AB, Del Bene F, Baier H (2009) Optical control of zebrafish behavior with halorhodopsin. Proc Natl Acad Sci USA 106(42):17968–17973. doi:10.1073/pnas.0906252106

    CAS  PubMed Central  PubMed  Google Scholar 

  • Asakawa K, Suster ML, Mizusawa K, Nagayoshi S, Kotani T, Urasaki A, Kishimoto Y, Hibi M, Kawakami K (2008) Genetic dissection of neural circuits by Tol2 transposon-mediated Gal4 gene and enhancer trapping in zebrafish. Proc Natl Acad Sci USA 105(4):1255–1260. doi:10.1073/pnas.0704963105

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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):406–426. doi:10.1016/j.ydbio.2009.04.013, pii: S0012-1606(09)00245-0

    CAS  PubMed  Google Scholar 

  • Bally-Cuif L, Wassef M (1994) Ectopic induction and reorganization of Wnt-1 expression in quail/chick chimeras. Development (Camb) 120(12):3379–3394

    CAS  Google Scholar 

  • Beck JC, Gilland E, Tank DW, Baker R (2004) Quantifying the ontogeny of optokinetic and vestibuloocular behaviors in zebrafish, medaka, and goldfish. J Neurophysiol 92(6):3546–3561. doi:10.1152/jn.00311.2004

    PubMed  Google Scholar 

  • Bell CC (2002) Evolution of cerebellum-like structures. Brain Behav Evol 59(5–6):312–326

    PubMed  Google Scholar 

  • Bell CC, Han V, Sawtell NB (2008) Cerebellum-like structures and their implications for cerebellar function. Annu Rev Neurosci 31:1–24. doi:10.1146/annurev.neuro.30.051606.094225

    CAS  PubMed  Google Scholar 

  • 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 (Camb) 128(21):4165–4176

    CAS  Google Scholar 

  • 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 (Lond) 390(6656):169–172. doi:10.1038/36579

    CAS  Google Scholar 

  • Boyden ES, Katoh A, Raymond JL (2004) Cerebellum-dependent learning: the role of multiple plasticity mechanisms. Annu Rev Neurosci 27:581–609. doi:10.1146/annurev.neuro.27.070203.144238

    CAS  PubMed  Google Scholar 

  • Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8(9):1263–1268. doi:10.1038/nn1525

    CAS  PubMed  Google Scholar 

  • 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 (Camb) 123:179–190

    CAS  Google Scholar 

  • Broccoli V, Boncinelli E, Wurst W (1999) The caudal limit of Otx2 expression positions the isthmic organizer. Nature (Lond) 401(6749):164–168. doi:10.1038/43670

    CAS  Google Scholar 

  • Brockerhoff SE, Hurley JB, Janssen-Bienhold U, Neuhauss SC, Driever W, Dowling JE (1995) A behavioral screen for isolating zebrafish mutants with visual system defects. Proc Natl Acad Sci USA 92(23):10545–10549

    CAS  PubMed Central  PubMed  Google Scholar 

  • Buckles GR, Thorpe CJ, Ramel MC, Lekven AC (2004) Combinatorial Wnt control of zebrafish midbrain-hindbrain boundary formation. Mech Dev 121(5):437–447. doi:10.1016/j.mod.2004.03.026, pii: S0925477304000747

    CAS  PubMed  Google Scholar 

  • 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 (Camb) 129(4):905–916

    CAS  Google Scholar 

  • Butler AB, Hodos H (1996) Comparative vertebrate neuroanatomy: evolution and adaptation. Wiley-Liss, New York

    Google Scholar 

  • 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):3048–3057. doi:10.1523/JNEUROSCI.6201-09.2010

    CAS  PubMed Central  PubMed  Google Scholar 

  • Crossley PH, Martinez S, Martin GR (1996) Midbrain development induced by FGF8 in the chick embryo. Nature (Lond) 380(6569):66–68. doi:10.1038/380066a0

    CAS  Google Scholar 

  • Curado S, Anderson RM, Jungblut B, Mumm J, Schroeter E, Stainier DY (2007) Conditional targeted cell ablation in zebrafish: a new tool for regeneration studies. Dev Dyn 236(4):1025–1035. doi:10.1002/dvdy.21100

    CAS  PubMed  Google Scholar 

  • Dahlem TJ, Hoshijima K, Jurynec MJ, Gunther D, Starker CG, Locke AS, Weis AM, Voytas DF, Grunwald DJ (2012) Simple methods for generating and detecting locus-specific mutations induced with TALENs in the zebrafish genome. PLoS Genet 8(8):e1002861. doi:10.1371/journal.pgen.1002861

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dahmane N, Ruiz i Altaba A (1999) Sonic hedgehog regulates the growth and patterning of the cerebellum. Development (Camb) 126(14):3089–3100

    Google Scholar 

  • Dickinson ME, Krumlauf R, McMahon AP (1994) Evidence for a mitogenic effect of Wnt-1 in the developing mammalian central nervous system. Development (Camb) 120(6):1453–1471

    CAS  Google Scholar 

  • Distel M, Hocking JC, Volkmann K, Koster RW (2010) The centrosome neither persistently leads migration nor determines the site of axonogenesis in migrating neurons in vivo. J Cell Biol 191(4):875–890. doi:10.1083/jcb.201004154

    CAS  PubMed Central  PubMed  Google Scholar 

  • Distel M, Jennifer CH, Koster RW (2011) In vivo cell biology using Gal4-mediated multicolor subcellular labeling in zebrafish. Commun Integr Biol 4(3):336–339. doi:10.4151/cib.4.3.15037

    PubMed Central  PubMed  Google Scholar 

  • Douglass AD, Kraves S, Deisseroth K, Schier AF, Engert F (2008) Escape behavior elicited by single, channelrhodopsin-2-evoked spikes in zebrafish somatosensory neurons. Curr Biol 18(15):1133–1137. doi:10.1016/j.cub.2008.06.077, pii: S0960-9822(08)00959-7

    CAS  PubMed Central  PubMed  Google Scholar 

  • du Lac S, Raymond JL, Sejnowski TJ, Lisberger SG (1995) Learning and memory in the vestibulo-ocular reflex. Annu Rev Neurosci 18:409–441. doi:10.1146/annurev.ne.18.030195.002205

    PubMed  Google Scholar 

  • Easter SS Jr, Nicola GN (1996) The development of vision in the zebrafish (Danio rerio). Dev Biol 180(2):646–663

    CAS  PubMed  Google Scholar 

  • Fatemi SH, Halt AR, Realmuto G, Earle J, Kist DA, Thuras P, Merz A (2002) Purkinje cell size is reduced in cerebellum of patients with autism. Cell Mol Neurobiol 22(2):171–175

    PubMed  Google Scholar 

  • 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 (Camb) 133(10):1891–1900. doi:10.1242/dev.02352

    CAS  Google Scholar 

  • Fujishima K, Horie R, Mochizuki A, Kengaku M (2012) Principles of branch dynamics governing shape characteristics of cerebellar Purkinje cell dendrites. Development (Camb) 139(18):3442–3455. doi:10.1242/dev.081315

    CAS  Google Scholar 

  • Furuichi T, Shiraishi-Yamaguchi Y, Sato A, Sadakata T, Huang J, Shinoda Y, Hayashi K, Mishima Y, Tomomura M, Nishibe H, Yoshikawa F (2011) Systematizing and cloning of genes involved in the cerebellar cortex circuit development. Neurochem Res 36(7):1241–1252. doi:10.1007/s11064-011-0398-1

    CAS  PubMed  Google Scholar 

  • Gaj T, Gersbach CA, Barbas CF 3rd (2013) ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31(7):397–405. doi:10.1016/j.tibtech.2013.04.004

    CAS  PubMed  Google Scholar 

  • Gomez A, Duran E, Salas C, Rodriguez F (2010) Cerebellum lesion impairs eyeblink-like classical conditioning in goldfish. Neuroscience 166(1):49–60. doi:10.1016/j.neuroscience.2009.12.018, pii: S0306-4522(09)02051-X

    CAS  PubMed  Google Scholar 

  • Hashimoto M, Hibi M (2012) Development and evolution of cerebellar neural circuits. Dev Growth Differ 54(3):373–389. doi:10.1111/j.1440-169X.2012.01348.x

    CAS  PubMed  Google Scholar 

  • Heap LA, Goh CC, Kassahn KS, Scott EK (2013) Cerebellar output in zebrafish: an analysis of spatial patterns and topography in eurydendroid cell projections. Front Neural Circuits 7:53. doi:10.3389/fncir.2013.00053

    PubMed Central  PubMed  Google Scholar 

  • Hibi M, Shimizu T (2012) Development of the cerebellum and cerebellar neural circuits. Dev Neurobiol 72(3):282–301. doi:10.1002/dneu.20875

    PubMed  Google Scholar 

  • Hidalgo-Sanchez M, Millet S, Simeone A, Alvarado-Mallart RM (1999) Comparative analysis of Otx2, Gbx2, Pax2, Fgf8 and Wnt1 gene expressions during the formation of the chick midbrain/hindbrain domain. Mech Dev 81(1–2):175–178

    CAS  PubMed  Google Scholar 

  • Hoshino M (2006) Molecular machinery governing GABAergic neuron specification in the cerebellum. Cerebellum 5(3):193–198. doi:10.1080/14734220600589202, pii: U0771321MJN0N232

    CAS  PubMed  Google Scholar 

  • 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. doi:10.1016/j.neuron.2005.06.007, pii: S0896-6273(05)00485-X

    CAS  PubMed  Google Scholar 

  • Huang P, Xiao A, Zhou M, Zhu Z, Lin S, Zhang B (2011) Heritable gene targeting in zebrafish using customized TALENs. Nat Biotechnol 29(8):699–700. doi:10.1038/nbt.1939

    PubMed  Google Scholar 

  • Hwang WY, Fu Y, Reyon D, Maeder ML, Tsai SQ, Sander JD, Peterson RT, Yeh JR, Joung JK (2013) Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol 31(3):227–229. doi:10.1038/nbt.2501

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ikenaga T, Yoshida M, Uematsu K (2005) Morphology and immunohistochemistry of efferent neurons of the goldfish corpus cerebelli. J Comp Neurol 487(3):300–311. doi:10.1002/cne.20553

    CAS  PubMed  Google Scholar 

  • Ikenaga T, Yoshida M, Uematsu K (2006) Cerebellar efferent neurons in teleost fish. Cerebellum 5(4):268–274. doi:10.1080/14734220600930588, pii: H82731V07J781700

    CAS  PubMed  Google Scholar 

  • Ito M (1982) Cerebellar control of the vestibulo-ocular reflex–around the flocculus hypothesis. Annu Rev Neurosci 5:275–296. doi:10.1146/annurev.ne.05.030182.001423

    CAS  PubMed  Google Scholar 

  • Ito M (2002a) Historical review of the significance of the cerebellum and the role of Purkinje cells in motor learning. Ann N Y Acad Sci 978:273–288

    PubMed  Google Scholar 

  • Ito M (2002b) The molecular organization of cerebellar long-term depression. Nat Rev Neurosci 3(11):896–902. doi:10.1038/nrn962

    CAS  PubMed  Google Scholar 

  • Ito M (2005) Bases and implications of learning in the cerebellum: adaptive control and internal model mechanism. Prog Brain Res 148:95–109. doi:10.1016/S0079-6123(04)48009-1, pii: S0079612304480091

    PubMed  Google Scholar 

  • Ito M (2006) Cerebellar circuitry as a neuronal machine. Prog Neurobiol 78(3–5):272–303. doi:10.1016/j.pneurobio.2006.02.006, pii: S0301-0082(06)00023-2

    PubMed  Google Scholar 

  • Ito M (2008) Control of mental activities by internal models in the cerebellum. Nat Rev Neurosci 9(4):304–313. doi:10.1038/nrn2332

    CAS  PubMed  Google Scholar 

  • Ito M (2013) Error detection and representation in the olivo-cerebellar system. Front Neural Circuits 7:1. doi:10.3389/fncir.2013.00001

    PubMed Central  PubMed  Google Scholar 

  • Jorntell H, Hansel C (2006) Synaptic memories upside down: bidirectional plasticity at cerebellar parallel fiber–Purkinje cell synapses. Neuron 52(2):227–238. doi:10.1016/j.neuron.2006.09.032, pii: S0896-6273(06)00770-7

    PubMed  Google Scholar 

  • Joyner AL, Liu A, Millet S (2000) Otx2, Gbx2 and Fgf8 interact to position and maintain a mid-hindbrain organizer. Curr Opin Cell Biol 12(6):736–741, pii: S0955-0674(00)00161-7

    CAS  PubMed  Google Scholar 

  • Kaneko M, Yamaguchi K, Eiraku M, Sato M, Takata N, Kiyohara Y, Mishina M, Hirase H, Hashikawa T, Kengaku M (2011) Remodeling of monoplanar Purkinje cell dendrites during cerebellar circuit formation. PLoS One 6(5):e20108. doi:10.1371/journal.pone.0020108

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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):1–17. doi:10.1016/j.ydbio.2010.03.024, pii: S0012-1606(10)00207-1

    CAS  PubMed  Google Scholar 

  • 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. doi:10.1523/JNEUROSCI.0072-09.2009

    CAS  PubMed  Google Scholar 

  • 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(1):9. doi:10.1186/1749-8104-8-9

    PubMed Central  PubMed  Google Scholar 

  • Kim JJ, Thompson RF (1997) Cerebellar circuits and synaptic mechanisms involved in classical eyeblink conditioning. Trends Neurosci 20(4):177–181, pii: S0166223696100813

    CAS  PubMed  Google Scholar 

  • Kimura Y, Satou C, Fujioka S, Shoji W, Umeda K, Ishizuka T, Yawo H, Higashijima S (2013) Hindbrain V2a neurons in the excitation of spinal locomotor circuits during zebrafish swimming. Curr Biol 23(10):843–849. doi:10.1016/j.cub.2013.03.066

    CAS  PubMed  Google Scholar 

  • Koeppen AH (2005) The pathogenesis of spinocerebellar ataxia. Cerebellum 4(1):62–73

    CAS  PubMed  Google Scholar 

  • Koster RW, Fraser SE (2001) Direct imaging of in vivo neuronal migration in the developing cerebellum. Curr Biol 11(23):1858–1863, pii: S0960-9822(01)00585-1

    CAS  PubMed  Google Scholar 

  • Laine J, Axelrad H (1994) The candelabrum cell: a new interneuron in the cerebellar cortex. J Comp Neurol 339(2):159–173. doi:10.1002/cne.903390202

    CAS  PubMed  Google Scholar 

  • 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(6):933–947. doi:10.1016/j.neuron.2005.11.031, pii: S0896-6273(05)01043-3

    CAS  PubMed  Google Scholar 

  • Linden DJ, Connor JA (1993) Cellular mechanisms of long-term depression in the cerebellum. Curr Opin Neurobiol 3(3):401–406

    CAS  PubMed  Google Scholar 

  • Liu A, Losos K, Joyner AL (1999) FGF8 can activate Gbx2 and transform regions of the rostral mouse brain into a hindbrain fate. Development (Camb) 126(21):4827–4838

    CAS  Google Scholar 

  • Livet J, Weissman TA, Kang H, Draft RW, Lu J, Bennis RA, Sanes JR, Lichtman JW (2007) Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system. Nature (Lond) 450(7166):56–62. doi:10.1038/nature06293

    CAS  Google Scholar 

  • 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 (Camb) 125(16):3049–3062

    CAS  Google Scholar 

  • Machold R, Fishell G (2005) Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron 48(1):17–24. doi:10.1016/j.neuron.2005.08.028, pii: S0896-6273(05)00703-8

    CAS  PubMed  Google Scholar 

  • Marsh E, Baker R (1997) Normal and adapted visuooculomotor reflexes in goldfish. J Neurophysiol 77(3):1099–1118

    CAS  PubMed  Google Scholar 

  • Martinez S, Crossley PH, Cobos I, Rubenstein JL, Martin GR (1999) FGF8 induces formation of an ectopic isthmic organizer and isthmocerebellar development via a repressive effect on Otx2 expression. Development (Camb) 126(6):1189–1200

    CAS  Google Scholar 

  • 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):162–171. doi:10.1016/j.ydbio.2008.03.016, pii: S0012-1606(08)00227-3

    CAS  PubMed Central  PubMed  Google Scholar 

  • Medina JF, Garcia KS, Nores WL, Taylor NM, Mauk MD (2000) Timing mechanisms in the cerebellum: testing predictions of a large-scale computer simulation. J Neurosci 20(14):5516–5525

    CAS  PubMed  Google Scholar 

  • Meek J (1992) Comparative aspects of cerebellar organization. From mormyrids to mammals. Eur J Morphol 30(1):37–51

    CAS  PubMed  Google Scholar 

  • Mikami Y, Yoshida T, Matsuda N, Mishina M (2004) Expression of zebrafish glutamate receptor delta2 in neurons with cerebellum-like wiring. Biochem Biophys Res Commun 322(1):168–176. doi:10.1016/j.bbrc.2004.07.095, pii: S0006-291X(04)01588-8

    CAS  PubMed  Google Scholar 

  • 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 (Lond) 401(6749):161–164. doi:10.1038/43664

    CAS  Google Scholar 

  • Mo W, Chen F, Nechiporuk A, Nicolson T (2010) Quantification of vestibular-induced eye movements in zebrafish larvae. BMC Neurosci 11:110. doi:10.1186/1471-2202-11-110

    PubMed Central  PubMed  Google Scholar 

  • Mueller T, Wullimann MF (2002) Expression domains of neuroD (nrd) in the early postembryonic zebrafish brain. Brain Res Bull 57(3–4):377–379, pii: S0361923001006943

    CAS  PubMed  Google Scholar 

  • 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):607–623. doi:10.1002/cne.902560413

    CAS  PubMed  Google Scholar 

  • Muto A, Ohkura M, Kotani T, Higashijima S, Nakai J, Kawakami K (2011) Genetic visualization with an improved GCaMP calcium indicator reveals spatiotemporal activation of the spinal motor neurons in zebrafish. Proc Natl Acad Sci USA 108(13):5425–5430. doi:10.1073/pnas.1000887108

    CAS  PubMed Central  PubMed  Google Scholar 

  • Muto A, Ohkura M, Abe G, Nakai J, Kawakami K (2013) Real-time visualization of neuronal activity during perception. Curr Biol 23(4):307–311. doi:10.1016/j.cub.2012.12.040

    CAS  PubMed  Google Scholar 

  • Nakai J, Ohkura M, Imoto K (2001) A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein. Nat Biotechnol 19(2):137–141. doi:10.1038/84397

    CAS  PubMed  Google Scholar 

  • Nishida K, Flanagan JG, Nakamoto M (2002) Domain-specific olivocerebellar projection regulated by the EphA-ephrin-A interaction. Development (Camb) 129(24):5647–5658

    CAS  Google Scholar 

  • Ogura E, Okuda Y, Kondoh H, Kamachi Y (2009) Adaptation of GAL4 activators for GAL4 enhancer trapping in zebrafish. Dev Dyn 238(3):641–655. doi:10.1002/dvdy.21863

    CAS  PubMed  Google Scholar 

  • Pan YA, Freundlich T, Weissman TA, Schoppik D, Wang XC, Zimmerman S, Ciruna B, Sanes JR, Lichtman JW, Schier AF (2013) Zebrabow: multispectral cell labeling for cell tracing and lineage analysis in zebrafish. Development (Camb) 140(13):2835–2846. doi:10.1242/dev.094631

    CAS  Google Scholar 

  • Pastor AM, de la Cruz RR, Baker R (1994) Cerebellar role in adaptation of the goldfish vestibuloocular reflex. J Neurophysiol 72(3):1383–1394

    CAS  PubMed  Google Scholar 

  • Pastor AM, De la Cruz RR, Baker R (1997) Characterization of Purkinje cells in the goldfish cerebellum during eye movement and adaptive modification of the vestibulo-ocular reflex. Prog Brain Res 114:359–381

    CAS  PubMed  Google Scholar 

  • Pfeffer PL, Gerster T, Lun K, Brand M, Busslinger M (1998) Characterization of three novel members of the zebrafish Pax2/5/8 family: dependency of Pax5 and Pax8 expression on the Pax2.1 (noi) function. Development (Camb) 125(16):3063–3074

    CAS  Google Scholar 

  • 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 (Camb) 126(13):2967–2978

    CAS  Google Scholar 

  • Pisharath H, Rhee JM, Swanson MA, Leach SD, Parsons MJ (2007) Targeted ablation of beta cells in the embryonic zebrafish pancreas using E. coli nitroreductase. Mech Dev 124(3):218–229. doi:10.1016/j.mod.2006.11.005, pii: S0925-4773(06)00215-2

    CAS  PubMed Central  PubMed  Google Scholar 

  • Portugues R, Engert F (2009) The neural basis of visual behaviors in the larval zebrafish. Curr Opin Neurobiol 19(6):644–647. doi:10.1016/j.conb.2009.10.007

    CAS  PubMed  Google Scholar 

  • 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 (Camb) 125(13):2381–2395

    CAS  Google Scholar 

  • Reifers F, Adams J, Mason IJ, Schulte-Merker S, Brand M (2000) Overlapping and distinct functions provided by fgf17, a new zebrafish member of the Fgf8/17/18 subgroup of Fgfs. Mech Dev 99(1–2):39–49, pii: S0925477300004755

    CAS  PubMed  Google Scholar 

  • Reim G, Brand M (2002) Spiel-ohne-grenzen/pou2 mediates regional competence to respond to Fgf8 during zebrafish early neural development. Development (Camb) 129(4):917–933

    CAS  Google Scholar 

  • 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 4:12. doi:10.1186/1749-8104-4-12

    PubMed Central  PubMed  Google Scholar 

  • Rodriguez CI, Dymecki SM (2000) Origin of the precerebellar system. Neuron 27(3):475–486, pii: S0896-6273(00)00059-3

    CAS  PubMed  Google Scholar 

  • Rodriguez F, Duran E, Gomez A, Ocana FM, Alvarez E, Jimenez-Moya F, Broglio C, Salas C (2005) Cognitive and emotional functions of the teleost fish cerebellum. Brain Res Bull 66(4–6):365–370. doi:10.1016/j.brainresbull.2004.11.026, pii: S0361-9230(05)00038-9

    CAS  PubMed  Google Scholar 

  • Sander JD, Cade L, Khayter C, Reyon D, Peterson RT, Joung JK, Yeh JR (2011) Targeted gene disruption in somatic zebrafish cells using engineered TALENs. Nat Biotechnol 29(8):697–698. doi:10.1038/nbt.1934

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schier AF, Neuhauss SC, Harvey M, Malicki J, Solnica-Krezel L, Stainier DY, Zwartkruis F, Abdelilah S, Stemple DL, Rangini Z, Yang H, Driever W (1996) Mutations affecting the development of the embryonic zebrafish brain. Development (Camb) 123:165–178

    CAS  Google Scholar 

  • Scott EK, Baier H (2009) The cellular architecture of the larval zebrafish tectum, as revealed by gal4 enhancer trap lines. Front Neural Circuits 3:13. doi:10.3389/neuro.04.013.2009

    PubMed Central  PubMed  Google Scholar 

  • Scott EK, Mason L, Arrenberg AB, Ziv L, Gosse NJ, Xiao T, Chi NC, Asakawa K, Kawakami K, Baier H (2007) Targeting neural circuitry in zebrafish using GAL4 enhancer trapping. Nat Methods 4(4):323–326. doi:10.1038/nmeth1033

    CAS  PubMed  Google Scholar 

  • Sillitoe RV, Joyner AL (2007) Morphology, molecular codes, and circuitry produce the three-dimensional complexity of the cerebellum. Annu Rev Cell Dev Biol 23:549–577. doi:10.1146/annurev.cellbio.23.090506.123237

    CAS  PubMed  Google Scholar 

  • Simeone A (2000) Positioning the isthmic organizer where Otx2 and Gbx2meet. Trends Genet 16(6):237–240, pii: S0168-9525(00)02000-X

    CAS  PubMed  Google Scholar 

  • Simeone A, Acampora D, Gulisano M, Stornaiuolo A, Boncinelli E (1992) Nested expression domains of four homeobox genes in developing rostral brain. Nature (Lond) 358(6388):687–690. doi:10.1038/358687a0

    CAS  Google Scholar 

  • Sotelo C (2008) Viewing the cerebellum through the eyes of Ramon y Cajal. Cerebellum 7(4):517–522. doi:10.1007/s12311-008-0078-0

    PubMed  Google Scholar 

  • Su CY, Kemp HA, Moens CB (2013) Cerebellar development in the absence of Gbx function in zebrafish. Dev Biol doi: 10.1016/j.ydbio.2013.10.026, pii: S0012-1606(13)00581-2

    Google Scholar 

  • Suda Y, Matsuo I, Aizawa S (1997) Cooperation between Otx1 and Otx2 genes in developmental patterning of rostral brain. Mech Dev 69(1–2):125–141

    CAS  PubMed  Google Scholar 

  • Sugihara I (2006) Organization and remodeling of the olivocerebellar climbing fiber projection. Cerebellum 5(1):15–22. doi:10.1080/14734220500527385

    PubMed  Google Scholar 

  • Sugihara I, Quy PN (2007) Identification of aldolase C compartments in the mouse cerebellar cortex by olivocerebellar labeling. J Comp Neurol 500(6):1076–1092. doi:10.1002/cne.21219

    CAS  PubMed  Google Scholar 

  • Sugihara I, Shinoda Y (2004) Molecular, topographic, and functional organization of the cerebellar cortex: a study with combined aldolase C and olivocerebellar labeling. J Neurosci 24(40):8771–8785. doi:10.1523/JNEUROSCI.1961-04.2004

    CAS  PubMed  Google Scholar 

  • Sugihara I, Marshall SP, Lang EJ (2007) Relationship of complex spike synchrony bands and climbing fiber projection determined by reference to aldolase C compartments in crus IIa of the rat cerebellar cortex. J Comp Neurol 501(1):13–29. doi:10.1002/cne.21223

    CAS  PubMed  Google Scholar 

  • Tanabe K, Kani S, Shimizu T, Bae YK, Abe T, Hibi M (2010) Atypical protein kinase C regulates primary dendrite specification of cerebellar Purkinje cells by localizing Golgi apparatus. J Neurosci 30(50):16983–16992. doi:10.1523/JNEUROSCI.3352-10.2010

    CAS  PubMed  Google Scholar 

  • Tsai PT, Hull C, Chu Y, Greene-Colozzi E, Sadowski AR, Leech JM, Steinberg J, Crawley JN, Regehr WG, Sahin M (2012) Autistic-like behaviour and cerebellar dysfunction in Purkinje cell Tsc1 mutant mice. Nature (Lond) 488(7413):647–651. doi:10.1038/nature11310

    CAS  Google Scholar 

  • Umeda K, Shoji W, Sakai S, Muto A, Kawakami K, Ishizuka T, Yawo H (2013) Targeted expression of a chimeric channelrhodopsin in zebrafish under regulation of Gal4-UAS system. Neurosci Res 75(1):69–75. doi:10.1016/j.neures.2012.08.010

    CAS  PubMed  Google Scholar 

  • Valente A, Huang KH, Portugues R, Engert F (2012) Ontogeny of classical and operant learning behaviors in zebrafish. Learn Mem 19(4):170–177. doi:10.1101/lm.025668.112

    PubMed Central  PubMed  Google Scholar 

  • 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):167–180. doi:10.1016/j.ydbio.2007.10.024, pii: S0012-1606(07)01438-8

    CAS  PubMed  Google Scholar 

  • Voogd J, Glickstein M (1998) The anatomy of the cerebellum. Trends Neurosci 21(9):370–375, pii: S0166-2236(98)01318-6

    CAS  PubMed  Google Scholar 

  • Wallace VA (1999) Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr Biol 9(8):445–448, pii: S096098229980195X

    CAS  PubMed  Google Scholar 

  • 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):31–43. doi:10.1016/j.neuron.2005.08.024, pii: S0896-6273(05)00699-9

    CAS  PubMed  Google Scholar 

  • Wassarman KM, Lewandoski M, Campbell K, Joyner AL, Rubenstein JL, Martinez S, Martin GR (1997) Specification of the anterior hindbrain and establishment of a normal mid/hindbrain organizer is dependent on Gbx2 gene function. Development (Camb) 124(15):2923–2934

    CAS  Google Scholar 

  • Wechsler-Reya RJ, Scott MP (1999) Control of neuronal precursor proliferation in the cerebellum by Sonic hedgehog. Neuron 22(1):103–114, pii: S0896-6273(00)80682-0

    CAS  PubMed  Google Scholar 

  • Wilson LJ, Wingate RJ (2006) Temporal identity transition in the avian cerebellar rhombic lip. Dev Biol 297(2):508–521. doi:10.1016/j.ydbio.2006.05.028, pii: S0012-1606(06)00867-0

    CAS  PubMed  Google Scholar 

  • Wilson SW, Brand M, Eisen JS (2002) Patterning the zebrafish central nervous system. Results Probl Cell Differ 40:181–215

    CAS  PubMed  Google Scholar 

  • Wingate RJ (2001) The rhombic lip and early cerebellar development. Curr Opin Neurobiol 11(1):82–88, pii: S0959-4388(00)00177-X

    CAS  PubMed  Google Scholar 

  • Wingate R (2005) Math-Map(ic)s. Neuron 48(1):1–4. doi:10.1016/j.neuron.2005.09.012, pii: S0896-6273(05)00779-8

    CAS  PubMed  Google Scholar 

  • Wingate RJ, Hatten ME (1999) The role of the rhombic lip in avian cerebellum development. Development (Camb) 126(20):4395–4404

    CAS  Google Scholar 

  • Wullimann MF, Rupp B, Reichert H (1996) Neuroanatomy of the zebrafish brain: a topological atlas. Birkhäuser, Basel

    Google Scholar 

  • Wurst W, Bally-Cuif L (2001) Neural plate patterning: upstream and downstream of the isthmic organizer. Nat Rev Neurosci 2(2):99–108

    CAS  PubMed  Google Scholar 

  • Xiao A, Wang Z, Hu Y, Wu Y, Luo Z, Yang Z, Zu Y, Li W, Huang P, Tong X, Zhu Z, Lin S, Zhang B (2013) Chromosomal deletions and inversions mediated by TALENs and CRISPR/Cas in zebrafish. Nucleic Acids Res 41(14):e141. doi:10.1093/nar/gkt464

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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(41):10924–10934. doi:10.1523/JNEUROSCI.1423-07.2007

    CAS  PubMed  Google Scholar 

  • Yoshida M, Hirano R (2010) Effects of local anesthesia of the cerebellum on classical fear conditioning in goldfish. Behav Brain Funct 6:20. doi:10.1186/1744-9081-6-20

    PubMed Central  PubMed  Google Scholar 

  • Yoshida M, Kondo H (2012) Fear conditioning-related changes in cerebellar Purkinje cell activities in goldfish. Behav Brain Funct 8:52. doi:10.1186/1744-9081-8-52

    PubMed Central  PubMed  Google Scholar 

  • Yoshida M, Okamura I, Uematsu K (2004) Involvement of the cerebellum in classical fear conditioning in goldfish. Behav Brain Res 153(1):143–148. doi:10.1016/j.bbr.2003.11.008

    PubMed  Google Scholar 

  • Zervas M, Millet S, Ahn S, Joyner AL (2004) Cell behaviors and genetic lineages of the mesencephalon and rhombomere 1. Neuron 43(3):345–357. doi:10.1016/j.neuron.2004.07.010, pii: S0896627304004283

    CAS  PubMed  Google Scholar 

  • Zupanc GK, Hinsch K, Gage FH (2005) Proliferation, migration, neuronal differentiation, and long-term survival of new cells in the adult zebrafish brain. J Comp Neurol 488(3):290–319. doi:10.1002/cne.20571

    PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank past and current members of the Hibi Laboratory for their contribution to the works cited here. The studies conducted in the Hibi Laboratory have been supported by grants from the Uehara Memorial Foundation (M.H.), Takeda Science Foundation (M.H.), the Naito Foundation Natural Science Scholarship (M.H.), and Grants-in-Aid for Scientific Research from the Ministry of Education, Science, Sports and Technology (M.H., T.S.)

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Masahiko Hibi .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Japan

About this chapter

Cite this chapter

Hibi, M., Shimizu, T. (2014). Deciphering Cerebellar Neural Circuitry Involved in Higher Order Functions Using the Zebrafish Model. In: Kondoh, H., Kuroiwa, A. (eds) New Principles in Developmental Processes. Springer, Tokyo. https://doi.org/10.1007/978-4-431-54634-4_13

Download citation

Publish with us

Policies and ethics