Advertisement

Animal Models: An Overview

  • Noriyuki KoibuchiEmail author
Living reference work entry
  • 4 Downloads

Abstract

Animal studies are indispensable for studying the organization, structure, and function of specific organs and their integrative functions including those of the cerebellum. Animal studies are classified into several categories. First, they are used to clarify the mechanisms that induce specific anatomical, physiological, or behavioral phenotypes (phenotype-oriented). Second, they can be designed to analyze the roles of specific endogenous molecules/genes/proteins in cellular, organ, and behavioral functions (molecule-oriented). Third, they are used to examine the effects of exogenous chemicals (xenobiotics), such as pharmaceuticals, cosmetics, and industrial and environmental chemicals. Lastly, animal models that mimic human diseases can be used to better understand the pathophysiology of these diseases. Recent developments in molecular biology have enabled to generate a large number of gene-modified animals for such purposes. Such animal models have contributed greatly to increase knowledge of gene–phenotype and gene–disease interactions. However, it is clear that multiple genes are often involved in morphological, physiological, and behavioral phenotypes; as such, many neurological disorders are caused by polygenic abnormalities. Thus, studying naturally occurring mutant animals, and injury- or drug-induced animal models, remains very important. Owing to the large numbers that have been reported, it is beyond the scope of this chapter to discuss all the existing animal models for cerebellar research. Thus, this chapter primarily discusses representative naturally occurring mutant animal models that are used to study cerebellar functions and diseases. Before providing detailed descriptions of each animal model, general concepts, and classifications of animal models used for cerebellar research are introduced.

Keywords

C. Elegans Drosophila Fish Amphibian Reptile Chick Rat Mouse Rabbit Cat Primate 

References

  1. Akita K, Arai S (2009) The ataxic Syrian hamster: an animal model homologous to the pcd mutant mouse? Cerebellum 8:202–210PubMedCrossRefPubMedCentralGoogle Scholar
  2. Altman J (1987) Morphological and behavioral markers of environmentally induced retardation of brain development: an animal model. Environ Health Perspect 74:153–168PubMedPubMedCentralCrossRefGoogle Scholar
  3. Alusi SH, Worthigton J, Glickman S et al (2001) A study of tremor in multiple sclerosis. Brain 124:720–730PubMedCrossRefPubMedCentralGoogle Scholar
  4. Ariel M, Ward KC, Tolbert DL (2009) Topography of Purkinje cells and other calbindin-immunoreactive cells within adult and hatching turtle cerebellum. Cerebellum 8:463–476PubMedCrossRefPubMedCentralGoogle Scholar
  5. Armbrust KR, Wang X, Hathorn TJ et al (2014) Mutant β-III spectrin causes mGluR1α mislocalization and functional deficits in a mouse model of spinocerebellar ataxia type 5. J Neurosci 34:9891–9904PubMedPubMedCentralCrossRefGoogle Scholar
  6. Barmack NH, Baughman RW, Eckenstein FP (1992) Cholinergic innervation of the cerebellum or rat, rabbit, cat, and monkey as revealed by choline acetyltranferase activity and immunohistochemistry. J Comp Neurol 317:233–249PubMedCrossRefPubMedCentralGoogle Scholar
  7. Becker EB (2014) The moonwalker mouse: new insights into TRPC3 function, cerebellar development, and ataxia. Cerebellum 13:628–636PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bellen HJ, Tong C, Tsuda H (2010) 100 years of Drosophila research and its impact on vertebrate neuroscience: a history lesson for the future. Nat Rev Neurosci 11:514–522PubMedPubMedCentralCrossRefGoogle Scholar
  9. Boukhtouche F, Doulazmi M, Frederic F et al (2006) RORα, a pivotal nuclear receptor for Purkinje neuron survival and differentiation: from development to ageing. Cerebellum 5:97–104PubMedCrossRefGoogle Scholar
  10. Bracha V, Zbarska S, Parker K et al (2009) The cerebellum and eye-blink conditioning: learning versus network performance hypothesis. Neuroscience 162:787–796PubMedCrossRefPubMedCentralGoogle Scholar
  11. Brown ME, Martin JR, Rosenbluth J et al (2011) A novel path for rapid transverse communication of vestibular signals in turtle cerebellum. J Neurophysiol 105:1071–1088PubMedCrossRefPubMedCentralGoogle Scholar
  12. Burright EN, Clark HB, Servadio A et al (1995) SCA1 transgenic mice: a model for neurodegeneration caused by an expanded CAG trinucleotide repeat. Cell 82:937–948PubMedCrossRefGoogle Scholar
  13. Burt DW (2004) Chicken genomics charts a path to the genome sequence. Brief Funct Genomic Proteomic 3:60–67PubMedCrossRefPubMedCentralGoogle Scholar
  14. Butts T, Chaplin N, Wingate JT (2011) Can clues from evolution unlock the molecular development of the cerebellum? Mol Neurobiol 43:67–76PubMedCrossRefPubMedCentralGoogle Scholar
  15. Campbell DB (1996) Extrapolation from animals to man. The integration of pharmacokinetics and pharmacodynamics. Ann N Y Acad Sci 801:116–135PubMedCrossRefPubMedCentralGoogle Scholar
  16. Carvalho MC, Nazari EM, Farina M et al (2008) Behavioral, morphological and biochemical changes after in ovo exposure to methylmercury in chicks. Toxicol Sci 106:180–185PubMedCrossRefPubMedCentralGoogle Scholar
  17. Cemal CK, Carroll CJ, Lawrence L et al (2002) YAC transgenic mice carrying pathological alleles of the MJD1 locus exhibit a mild and slowly progressive cerebellar deficit. Hum Mol Genet 11:1075–1094PubMedCrossRefPubMedCentralGoogle Scholar
  18. Chen JC, Chesler M (1991) Extracellular alkalinization evoked by GABA and its relationship to activity-dependent pH shifts in turtle cerebellum. J Physiol 442:431–446PubMedPubMedCentralCrossRefGoogle Scholar
  19. Clark GA, McCormick DA, Lavond DG et al (1984) Effects of lesions of cerebellar nuclei on conditioned behavioral and hippocampal neuronal responses. Brain Res 291:125–136PubMedCrossRefPubMedCentralGoogle Scholar
  20. Clayton NS, Dickinson A (1998) Episodic-like memory during cache recovery by scrub jays. Nature 6699:272–274CrossRefGoogle Scholar
  21. Cohen RW, Fisher RS, Duong T et al (1991) Altered excitatory amino acid function and morphology of the cerebellum of the spastic Han-Wistar rat. Mol Brain Res 11:27–36PubMedCrossRefPubMedCentralGoogle Scholar
  22. De Goef B, Grommen SVH, Darras VM (2008) The chicken embryo as a model for developmental endocrinology: development of the thyrotropic, corticotropic, and somatotropic axes. Mol Cell Endocrinol 293:17–24CrossRefGoogle Scholar
  23. Descan N (1987) The use of xenopus oocytes for the study of ion channels. CRC Crit Rev Biochem 22:317–318CrossRefGoogle Scholar
  24. Dietrich H, Straka H (2016) Prolonged vestibular stimulation induces homeostatic plasticity of the vestibulo-ocular reflex in larval Xenopus laevis. Eur J Neurosci 44:1787–1796PubMedCrossRefPubMedCentralGoogle Scholar
  25. Driever W, Solnica-Krezel L, Schier AF et al (1996) A genetic screen for mutation s affecting embryogenesis in zebrafish. Development 123:37–46PubMedPubMedCentralGoogle Scholar
  26. Durr A (2010) Autosomal dominant cerebellar ataxias: polyglutamine expansions and beyond. Lancet Neurol 9:885–894PubMedCrossRefPubMedCentralGoogle Scholar
  27. Dusart I, Guenet JL, Sotelo C (2006) Purkinje cell death: differences between developmental cell death and neurodegenerative death in mutant mice. Cerebellum 5:163–173PubMedCrossRefPubMedCentralGoogle Scholar
  28. Fernandez-Gonzalez A, La Spada AR, Treadaway J et al (2002) Purkinje cell degeneration (pcd) phenotypes caused by mutations in the axotomy-induced gene, Nna1. Science 295:1904–1906PubMedCrossRefPubMedCentralGoogle Scholar
  29. Fletcher CF, Lutz CM, O’Sullivan TN et al (1996) Absence epilepsy in tottering mutant mice is associated with calcium channel defects. Cell 87:607–617PubMedCrossRefPubMedCentralGoogle Scholar
  30. Friedman MJ, Shah AG, Fand Z-H et al (2007) Polyglutamine domain modulates the TBP-TFIIB interaction: implications for its normal function and neurodegeneration. Nat Neurosci 10:1519–1528PubMedCrossRefPubMedCentralGoogle Scholar
  31. Fu Y-H, Ptacek LJ (2002) Spinocerebellar ataxia type 4. In: Manto MU, Pandolfo M (eds) The cerebellum and its disorders. Cambridge University Press, CambridgeGoogle Scholar
  32. Fujita H, Oh-Nishi A, Obayashi S et al (2010) Organization of the marmoset cerebellum in three dimensional space: lobulation, aldolase C compartmentalization and axonal projection. J Comp Neurol 518:1764–1791PubMedCrossRefPubMedCentralGoogle Scholar
  33. Furutani-Seki M, Sasado T, Morinaga C et al (2004) A systematic genome-wide screen for mutations affecting organogenesis in Medaka, Oryzias latipes. Mech Dev 121:647–658CrossRefGoogle Scholar
  34. Gatewood BK, Cottingham RW (2000) Mouse-human comparative map resources on the web. Brief Bioinform 1:60–75PubMedCrossRefPubMedCentralGoogle Scholar
  35. Goti D, Katzen SM, Mez J et al (2004) A mutant ataxin-3 putative-cleavage fragment in brains of Machado-Joseph disease patients and transgenic mice is cytotoxic above a critical concentration. J Neurosci 24:10266–10279PubMedPubMedCentralCrossRefGoogle Scholar
  36. Grillner S (1975) Locomotion in vertebrates: central mechanisms and reflex interaction. Physiol Rev 55:247–304PubMedCrossRefPubMedCentralGoogle Scholar
  37. Haffter P, Granato M, Brand M et al (1996) The identification of genes with unique and essential functions in the development of zebrafish, Danio rerio. Development 123:1–36PubMedPubMedCentralGoogle Scholar
  38. Han VZ, Meek J, Campbell HR et al (2006) Cell morphology and circuitry in the cerebellar lobes of the mormyrid cerebellum. J Comp Neurol 497:309–325PubMedCrossRefPubMedCentralGoogle Scholar
  39. Harkins AB, Fox AP (2002) Cell death in weaver mouse cerebellum. Cerebellum 1:201–206PubMedCrossRefPubMedCentralGoogle Scholar
  40. Hashiguchi S, Doi H, Kunii M et al (2019) Ataxic phenotype with altered CaV3.1 channel property in a mouse model for spinocerebellar ataxia 42. Neurobiol Dis 130:104516PubMedCrossRefPubMedCentralGoogle Scholar
  41. Hirai H (2012) Basic research on cerebellar gene therapy using lentiviral vectors. Cerebellum 11:443–445PubMedCrossRefPubMedCentralGoogle Scholar
  42. Howe K, Clark MD, Torroja CF et al (2013) The zebrafish reference genome sequence and its relationship to the human genome. Nature 496:498–503PubMedPubMedCentralCrossRefGoogle Scholar
  43. Hoxha E, Gabriele RMC, Balbo I et al (2017) Motor deficits and cerebellar atrophy in Elovl5 knock out mice. Front Cell Neurosci 11:343PubMedPubMedCentralCrossRefGoogle Scholar
  44. Huynh DP, Figueroa K, Hoang N et al (2000) Nuclear localization or inclusion body formation of ataxin-2 are not necessary for SCA2 pathogenesis in mouse or human. Nat Genet 26:44–50PubMedCrossRefPubMedCentralGoogle Scholar
  45. Hyun B-H, Kim M-S, Choi Y-K et al (2001) Mapping of the pogo gene, a new ataxic mutant from Korean wild mince, on central mouse chromosome 8. Mamm Genome 12:250–252PubMedCrossRefPubMedCentralGoogle Scholar
  46. Ikenaga T, Yoshida M, Uematsu K (2006) Cerebellar efferent neurons in teleost fish. Cerebellum 5:268–274PubMedCrossRefPubMedCentralGoogle Scholar
  47. Ishikawa Y, Yamamoto N, Yasuda T et al (2010) Morphogenesis of the medaka cerebellum, with special reference to the mesencephalic sheet, a structure homologous to the rostrolateral part of mammalian anterior medullary velum. Brain Behav Evol 75:88–103PubMedCrossRefPubMedCentralGoogle Scholar
  48. Joven A, Morona R, González A, Moreno N et al (2013) Expression patterns of Pax6 and Pax7 in the adult brain of a urodele amphibian, Pleurodeles waltl. J Comp Neurol 2521:2088–2124PubMedCrossRefGoogle Scholar
  49. Katsuyama Y, Terashima T (2009) Developmental anatomy of reeler mutant mouse. Develop Growth Differ 51:271–286CrossRefGoogle Scholar
  50. Ke MC, Guo CC, Raymond JL (2009) Elimination of climbing fiber instructive signals during motor learning. Nat Neurosci 12:1171–1179PubMedCrossRefPubMedCentralGoogle Scholar
  51. Kiehl TR, Shibata H, Pulst SM (2000) The ortholog of human ataxin-2 is essential for early embryonic patterning in C. elegans. J Mol Neurosci 15:231–241PubMedCrossRefPubMedCentralGoogle Scholar
  52. Klockgether T (2007) Ataxias. Parkinsonism Relat Disord 13(Supple 3):S391–S394PubMedCrossRefGoogle Scholar
  53. Koibuchi N (2009) Animal models to study thyroid hormone action in cerebellum. Cerebellum 8:89–97PubMedCrossRefGoogle Scholar
  54. Koibuchi N, Jingu H, Iwasaki T et al (2003) Current perspectives on the role of thyroid hormone in growth and development of cerebellum. Cerebellum 2:279–289PubMedCrossRefGoogle Scholar
  55. La Spada AR, Fu Y-H, Sopher BL et al (2001) Polyglutamine-expanded ataxin-7 antagonizes CRX function and induces cone-rod dystrophy in a mouse model of SCA7. Neuron 31:913–927PubMedCrossRefPubMedCentralGoogle Scholar
  56. Luo J, Redies C (2004) Overexpression of genes in Purkinje cells in the embryonic chicken cerebellum by in vivo electroporation. J Neurosci Methods 139:241–245PubMedCrossRefPubMedCentralGoogle Scholar
  57. Ma L, Zhao Y, Chen Y et al (2018) Caenorhabditis elegans as a model system for target identification and drug screening against neurodegenerative diseases. Eur J Pharmacol 819:169–180PubMedCrossRefPubMedCentralGoogle Scholar
  58. MacKenzie-Graham A, Tiwari-Woodruff SK, Sharma G et al (2009) Purkinje cell loss in experimental autoimmune encephalomyelitis. NeuroImage 48:637–651PubMedPubMedCentralCrossRefGoogle Scholar
  59. Mancini C, Hoxha E, Iommarini L et al (2019) Mice harboring a SCA28 patient mutation in AFG3L2 develop late-onset ataxia associated with enhanced mitochondrial proteotoxicity. Neurobiol Dis 124:14–28PubMedCrossRefPubMedCentralGoogle Scholar
  60. Manto M, Marmolino D (2009) Animal models of human cerebellar ataxias: a cornerstone for the therapies of the twenty-first century. Cerebellum 8:137–154PubMedCrossRefPubMedCentralGoogle Scholar
  61. Margolis RL (2002) The spinocerebellar ataxias: order emerges from chaos. Curr Neurol Neurosci Rep 2:447–456PubMedCrossRefPubMedCentralGoogle Scholar
  62. Matsui T, Koyano KW, Tamura K et al (2012) FMRI activity in the macaque cerebellum evoked by intracortical microstimulation of the primary somatosensory cortex: evidence for polysynaptic propagation. PLoS One 7:e47515PubMedPubMedCentralCrossRefGoogle Scholar
  63. McGurk L, Berson A, Bonini NM (2015) Drosophila as an in vivo model for human neurodegenerative disease. Genetics 201:377–402PubMedPubMedCentralCrossRefGoogle Scholar
  64. Mori S (1997) Carp experiment in space microgravity –a visual-vestibular sensory conflict model. Biol Sci Space 11:327–333PubMedCrossRefGoogle Scholar
  65. Mori S, Matsui T, Kuze B et al (1998) Cerebellar-induced locomotion: reticulospinal control of spinal rhythm generating mechanisms in cats. Ann N Y Acad Sci 860:94–105PubMedCrossRefGoogle Scholar
  66. Morona R, González A (2009) Immunohistochemical localization of calbindin-D28k and calretinin in the brainstem of anuran and urodele amphibians. J Comp Neurol 515:503–537PubMedCrossRefGoogle Scholar
  67. Moseley ML, Zu T, Ikeda Y et al (2006) Bidirectional expression of CUG and CAG expansion transcripts and intranuclear polyglutamine inclusions in spinocebellar ataxia type 8. Nat Genet 38:758–769PubMedCrossRefGoogle Scholar
  68. Murphy MJ, Clark NB (1990) The avian embryo as a model for early developmental endocrinology. J Exp Zool 4(Suppl):177–180CrossRefGoogle Scholar
  69. Nabulsi N, Huang Y, Weinzimmer D et al (2010) High-resolution imaging of brain 5-HT1B receptors in the rhesus monkey using [11C]P943. Nucl Med Biol 37:205–214PubMedCrossRefGoogle Scholar
  70. Ngwenya A, Patzke N, Herculano-Houzel S et al (2018) Potential adult neurogenesis in the telencephalon and cerebellar cortex of the Nile crocodile revealed with doublecortin immunohistochemistry. Anat Rec (Hoboken) 301:659–672CrossRefGoogle Scholar
  71. Nieuwenhuys R (1976) Aspects of the structural organization of the cerebellum of mormyrid fishes. Exp Brain Res 1(suppl):90–95Google Scholar
  72. Nigon VM, Félix M-A (2017) History of research on C. elegans and other free-living nematodes as model organisms. WormBook 2017:1–84PubMedPubMedCentralGoogle Scholar
  73. Okamoto H, Hirate Y, Ando H (2004) Systematic identification of factors in zebrafish regulating the early midbrain and cerebellar development by ordered differentia display and caged mRNA technology. Front Biosci 9:93–99PubMedCrossRefPubMedCentralGoogle Scholar
  74. Orlovsky GN (1970) Influence of the cerebellum on the reticulo-spinal neurons during locomotion. Biophysics 15:928–936Google Scholar
  75. Pidoux L, Le Blanc P, Levenes C et al (2018) A subcortical circuit linking the cerebellum to the basal ganglia engaged in vocal learning. elife 7. pii: e32167Google Scholar
  76. Postlethwait JH, Yan YL, Gates MA et al (1998) Vertebrate genome evolution and the zebrafish gene map. Nat Genet 18:345–349CrossRefGoogle Scholar
  77. Reiter LT, Potocki L, Chien S et al (2001) A systematic analysis of human disease-associated gene sequences in Drosophila melanogaster. Genome Res 11:1114–1125PubMedPubMedCentralCrossRefGoogle Scholar
  78. Rodríguez F, Durán A, Gómez FM et al (2005) Cognitive and emotional functions of the teleost fish cerebellum. Brain Res Bull 66:365–370PubMedCrossRefGoogle Scholar
  79. Sarna JR, Hawkes R (2003) Patterned Purkinje cell death in cerebellum. Prog Neurobiol 70:473–507PubMedCrossRefGoogle Scholar
  80. Sasado T, Tanaka M, Kobayashi K et al (2010) The National BioResource Project Medaka (NBRP Medaka): an integrated bioresource for biological and biomedical sciences. Exp Anim 59:13–23PubMedCrossRefGoogle Scholar
  81. Sasaki E, Suemizu H, Shimada A et al (2009) Generation of transgenic non-human primates with germline transmission. Nature 459:523–527PubMedCrossRefGoogle Scholar
  82. Sato T, Oyake M, Nakamura K et al (1999) Transgenic mouse harboring a full-length human mutant DRPLA gene exhibit age-dependent intergenerational and somatic instabilities of CAG repeats comparable with those in DRPLA patients. Hum Mol Genet 8:99–106PubMedCrossRefPubMedCentralGoogle Scholar
  83. Sato T, Miura M, Yamada M et al (2009) Severe neurological phenotypes of Q129 DRPLA transgenic mice serendipitously created by en masse expansion of CAG repeats in Q76 DRPLA mice. Hum Mol Genet 18:723–736PubMedCrossRefPubMedCentralGoogle Scholar
  84. Sawtell NB, Bell CC (2008) Adaptive processing in electrosensory systems: Linkis to cerebellar plasticity and learning. J Physiol Paris 102:223–232PubMedCrossRefPubMedCentralGoogle Scholar
  85. Schmahmann JD (2004) Disorders of the cerebellum: ataxia dysmetria of thought and cerebellar cognitive affective syndrome. J Neuropsychiatry Clin Neurosci 16:367–378PubMedCrossRefPubMedCentralGoogle Scholar
  86. Schmahmann JD, Weilburg JB, Shcerman JC (2007) The neuropsychiatry of the cerebellum – insights from the clinic. Cerebellum 6:254–267PubMedCrossRefPubMedCentralGoogle Scholar
  87. Schmidt T, Schmidt J, Hübener J (2015) Model systems for spinocerebellar ataxias: lessons learned about the pathogenesis. In: McGrath I (ed) Spinocerebellar Ataxia. Foster Academics, Jersey City, pp 1–26Google Scholar
  88. Seki T, Sato M, Kibe Y et al (2018) Lysosomal dysfunction and early glial activation are involved in the pathogenesis of spinocerebellar ataxia type 21 caused by mutant transmembrane protein 240. Neurobiol Dis 120:34–50PubMedCrossRefPubMedCentralGoogle Scholar
  89. Somogyi P, Takagi H, Reichards JG et al (1989) Subcellular localization of benzodiazepine/GABAA receptors in the cerebellum of rat, cat, and monkey using monoclonal antibodies. J Neurosci 9:2197–2209PubMedPubMedCentralCrossRefGoogle Scholar
  90. Stern CD (2005) The chick: a great model system becomes even greater. Dev Cell 8:9–17PubMedPubMedCentralGoogle Scholar
  91. Strick PL, Dum RP, Fiez JA (2009) Cerebellum and nonmotor function. Ann Rev Neurosci 32:413–434PubMedCrossRefPubMedCentralGoogle Scholar
  92. Sugahara F, Murakami Y, Pascual-Anaya J et al (2017) Reconstructing the ancestral vertebrate brain. Develop Growth Differ 59:163–174CrossRefGoogle Scholar
  93. Sultan F, Glickstein M (2007) The cerebellum: comparative and animal studies. Cerebellum 6:168–176PubMedCrossRefPubMedCentralGoogle Scholar
  94. Takeuchi M, Yamaguchi S, Sakakibara Y et al (2017) Gene expression profiling of granule cells and Purkinje cells in the zebrafish cerebellum. J Comp Neurol 525:1558–1585PubMedCrossRefPubMedCentralGoogle Scholar
  95. Teixeira-Castro A, Ailion M, Jalles A et al (2011) Neuron-specific proteotoxicity of mutant ataxin-3 in C. elegans: rescue by the DAF-16 and HSF-1 pathways. Hum Mol Genet 20:2996–3009PubMedPubMedCentralCrossRefGoogle Scholar
  96. Thompson RF (1986) The neurobiology of learning and memory. Science 233:941–947PubMedCrossRefPubMedCentralGoogle Scholar
  97. Tokuda S, Kuramoto T, Tanaka K et al (2007) The ataxic groggy rat has a missense mutation in the P/Q-type voltage-gated Ca2+ channel α1A subunit gene and exhibits absence seizures. Brain Res 1133:168–177PubMedCrossRefPubMedCentralGoogle Scholar
  98. Tolbert DL, Conoyer B, Ariel M (2004) Quantitative analysis of granule cell axons and climbing fiber afferents in the turtle cerebellar cortex. Anat Embryol 209:49–58PubMedPubMedCentralCrossRefGoogle Scholar
  99. Tomioka I, Ishibashi H, Minakawa EN et al (2017) Transgenic monkey model of the polyglutamine diseases recapitulating progressive neurological symptoms. eNeuro 4. pii: ENEURO.0250-16.2017Google Scholar
  100. van de Leemput J, Chandran J, Knight MA et al (2007) Deletion at ITPR1 underlies ataxia in mice and spinocerebellar ataxia 15 in humans. PLoS Genet 3:e108PubMedPubMedCentralCrossRefGoogle Scholar
  101. Warrick JM, Paulson HL, Gray-Board GL et al (1998) Expanded polyglutamine protein forms nuclear inclusions and causes neural degeneration in Drosophila. Cell 93:939–949PubMedCrossRefPubMedCentralGoogle Scholar
  102. Watase K, Weeber E, XU B et al (2002) A long CAG repeat in the mouse sca1 locus replicates SCA1 features and reveals the impact of protein solubility on selective neurodegeneration. Neuron 34:905–919PubMedCrossRefPubMedCentralGoogle Scholar
  103. Watase K, Barrett CF, Miyazaki T et al (2008) Spinocerebellar ataxia type 6 knockin mice develop a progressive neuronal dysfunction with age-dependent accumulation of mutant Cav2.1 channels. Proc Natl Acad Sci USA 105:11987–11992PubMedCrossRefPubMedCentralGoogle Scholar
  104. Whishaw IQ, Kolb B (eds) (2005) The behavior of the laboratory rat. A handbook with tests. Oxford University Press, LondonGoogle Scholar
  105. White MC, Gao R, Xu W et al (2010) Inactivation of hnRNP K by expanded intronic AUUCA repeat induces apoptosis via translocation of PKCδ to mitochondria in spinocerebellar ataxia 10. PLoS Genet 6:e1000984PubMedPubMedCentralCrossRefGoogle Scholar
  106. Wingate RJT, Hatten ME (1999) The role of the rhombic lip in avian cerebellum development. Development 126:4395–4404PubMedPubMedCentralGoogle Scholar
  107. Wylie DR, Hoops D, Aspden JW et al (2016) Zebrin II is expressed in sagittal stripes in the cerebellum of dragon lizards (Ctenophorus sp.). Brain Behav Evol 88:177–186PubMedCrossRefPubMedCentralGoogle Scholar
  108. Xu Z, Tito AJ, Rui YN et al (2015) Studying polyglutamine diseases in Drosophila. Exp Neurol 274:25–41PubMedPubMedCentralCrossRefGoogle Scholar
  109. Xue H-G, Yang C-Y, Yamamoto N (2008) Afferent source to the inferior olive and distribution of the olivocerebellar climbing fibers in cyprinids. J Comp Neurol 507:1409–1427PubMedCrossRefPubMedCentralGoogle Scholar
  110. Yoo S-Y, Pennesi ME, Weeber EJ et al (2003) SCA7 knockin mice model human SCA7 and reveal gradual accumulation of mutant ataxin-7 in neurons and abnormalities in short-term plasticity. Neuron 37:913–927CrossRefGoogle Scholar
  111. Yvert G, Liderberg KS, Picaud S et al (2000) Expanded polyglutamines induce neurodegeneration and trans-neuronal alterations in cerebellum and retia of SCA7 transgenic mice. Hum Mol Genet 9:2491–2506PubMedCrossRefPubMedCentralGoogle Scholar
  112. Zhang Y, Snider A, Willard L et al (2009) Loss of Purkinje cells in the PKCγH101Y transgenic mouse. Biochem Biophys Res Commun 378:524–528PubMedCrossRefPubMedCentralGoogle Scholar
  113. Zhang Y, Magnus G, Han VZ (2010) Electrophysiological characteristics of cells in the anterior caudal lobe of the mormyrid cerebellum. Neuroscience 171:79–91PubMedCrossRefGoogle Scholar
  114. Zu T, Duvick LA, Kaytor MD et al (2004) Recovery from polyglutamine-induced neurodegeneration in conditional SCA1 transgenic mice. J Neurosci 24:8853–8861PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Department of Integrative PhysiologyGunma University Graduate School of MedicineMaebashiJapan

Section editors and affiliations

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

Personalised recommendations