Advertisement

The Development of the Cerebellum: From the Beginnings

  • Jan VoogdEmail author
Chapter
Part of the Contemporary Clinical Neuroscience book series (CCNE)

Abstract

Sotelo stated in his introduction for a consensus paper on cerebellar development (Leto et al., Cerebellum 15:789–828, 2015) that “The work done in the late nineteenth century until the late 1970s provided substantial and significant information; however, it was only descriptive and barely addressed the mechanisms involved.” Observations and their description, the nomenclature that evolved from these studies, and the ideas they fostered, indeed, formed the basis for our understanding of the mechanisms that underlie the complex development of the cerebellum, to be reviewed in this volume. This chapter will highlight some of these early contributions to the origin of the cerebellum, its histogenesis, the migration of its neurons, the development of the longitudinal Purkinje cell zones, their target nuclei and their connections, and the folial pattern of the cerebellum.

References

  1. 1.
    Ahn AH, Dziennis S, Hawkes R, Herrup K. The cloning of zebrin II reveals its identity with aldolase C. Development. 1994;120:2081–90.PubMedGoogle Scholar
  2. 2.
    Altman J. Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and of the molecular layer. J Comp Neurol. 1972;145:399–462.PubMedCrossRefGoogle Scholar
  3. 3.
    Altman J. Morphological development of the rat cerebellum and some of its mechanisms. Exp Brain Res Suppl. 1982;6:8–49.CrossRefGoogle Scholar
  4. 4.
    Altman J, Bayer SA. Embryonic development of the rat cerebellum. III. Regional differences in the time of origin, migration and settling of Purkinje cells. J Comp Neurol. 1985a;231:42–65.PubMedCrossRefGoogle Scholar
  5. 5.
    Altman J, Bayer SA. Embryonic development of the rat crebellum. II. Transformation and regional distribution of the deep neurons. J Comp Neurol. 1985b;231:27–41.PubMedCrossRefGoogle Scholar
  6. 6.
    Altman J, Bayer SA. Embryonic development of the rat cerebellum. I Delineation of the cerebellar primordium and early cell movements. J Comp Neurol. 1985c;231:1–26.PubMedCrossRefGoogle Scholar
  7. 7.
    Armstrong CL, Krueger-Naug AM, Currie RW, Hawkes R. Expresion of heat-shock protein Hsp25 in mouse Purkinje cells during development reveals novel features of cerebellar compartmentation. J Comp Neurol. 2001;429:7–21.PubMedCrossRefGoogle Scholar
  8. 8.
    Arndt K, Redies C. Development of cadherin-defined parasagittal subdivisions in the embryonic chicken cerebellum. J Comp Neurol. 1998;401:367–81.PubMedCrossRefGoogle Scholar
  9. 9.
    Arsénio Nunes ML, Sotelo C. The development of the spinocerebellar system in the postnatal rat. J Comp Neurol. 1985;237:291–306.PubMedCrossRefGoogle Scholar
  10. 10.
    Athias M. L’histogenése de l’ écorce du cervelet. J Anat Physiol Norm Pathol. 1897;33:372–404.Google Scholar
  11. 11.
    Bechterew WV. Zur Anatomie der Schenkel des Kleinhirns insb. der Brückenarme. Neurol Centralbl. 1885;4:121–5.Google Scholar
  12. 12.
    Bechterew WV. Die Leitungsbahnen im Gehirn und Rückenmark. Leipzig: Arthur Georgi; 1899.CrossRefGoogle Scholar
  13. 13.
    Bergmann KGLC. Motiz über einige Strukturverhältnisse des Cerebellum und Rückenmarks. Z Ration Med. 1857;8:360–3.Google Scholar
  14. 14.
    Bergqvist H, Källén B. Studies on the topography of the migration areas in the vertebrate brain. Acata Anat. 1953;17:353–69.CrossRefGoogle Scholar
  15. 15.
    Bolk L. Over de ontwikkeling van het cerebellum bij den mensch (About the development of the human cerebelklum). Versl Kon Acad Amsterdam. 1905:635–41.Google Scholar
  16. 16.
    Bolk L. Das Cerebellum der Säugetiere. Haarlem: Fischer; 1906.Google Scholar
  17. 17.
    Bourrat F, Sotelo C. Neuronal migration and dendritic maturation of medial cerebellar nucleus in rat embryos: an HRP in vitro study using cerebellar slabs. Brain Res. 1986;378:69–85.PubMedCrossRefGoogle Scholar
  18. 18.
    Bradley OC. On the development and homology of the mammalian cerebellar fissures. J Anat Physiol. 1903;37:112–30. 221–240PubMedPubMedCentralGoogle Scholar
  19. 19.
    Bradley OC. The mammalian cerebellum: its lobes and fissures. J Anat Physiol. 1904;38:448–75.PubMedPubMedCentralGoogle Scholar
  20. 20.
    Braun K, Schachner M, Schleich H, Heizmann CW. Cellular localization of the Ca2+−binding protein parvalbumin in the developing avian cerebellum. Cell Tissue Res. 1986;243:69–78.CrossRefGoogle Scholar
  21. 21.
    Brochu G, Maler L, Hawkes R. Zebrin II: a polypeptide antigen expressed selectively by Purkinje cells reveals compartments in rat and fish cerebellum. J Comp Neurol. 1990;291:538–52.PubMedCrossRefGoogle Scholar
  22. 22.
    Cajal RY. A propos de certains élements bipolaires du cervelet avec quelques détails nouveaux sur l’évolution ds fibres nerveuses. Int Monatschrifr Anat Physiol. 1890a;7:47–468.Google Scholar
  23. 23.
    Cajal RY. Sur les fibres nerveuses de la couche granulaire du cervelet et sur l’évolution des élements cérébelleux. Int Monatschrift Anatomie Physiol. 1890b;7:12–29.Google Scholar
  24. 24.
    Cajal SRY. A propos de certains éléments bipolaires du cervelet et quelques détails nouveaux sur l’évolution des fibres cérébelleuses. Int Monatschrift Anatomie Physiol. 1890c;8:447–68.Google Scholar
  25. 25.
    Cajal SRY. Histologie du système nerveux de l’homme et des vertebrés. Paris: Maloine; 1909–1911.Google Scholar
  26. 26.
    Chédotal A, Sotelo C. Early development of olivocerebellar projections in the fetal rat using CGRP immunohistochemistry. Eur J Neurosci. 1992;4:1159–79.PubMedCrossRefGoogle Scholar
  27. 27.
    Chédotal A, Bloch-Gallego E, Sotelo C. The embryonic cerebellum contains topographic clues that guide developing inferior olivary axons. Development. 1997;124:861–70.PubMedGoogle Scholar
  28. 28.
    Chédotal A, Pourquié O, Ezan F, San Clemente H, Sotelo C. BEN as a presumptive target recognition molecule during the development of the olivocerebellar system. J Neurosci. 1996;16:3296–310.PubMedCrossRefGoogle Scholar
  29. 29.
    Cholley B, Wassef M, Arsénio-Nunes L, Sotelo C. Proxinal trajectory of the brachium conjunctivum in rat fetuses and its early association with the parabrachial nucleus. A study combining in vitro HRP anterograde tracing and immunochemistry. Brain Res Dev Brain Res. 1989;45:185–202.PubMedCrossRefGoogle Scholar
  30. 30.
    Corrales JD, Rocco GL, Blaess S, Guo O, Joyner AL. Spatial pattern of sonic hedgehog signaling through the Gli gens during cerebellar development. Development. 2004;131:5581–90.PubMedCrossRefGoogle Scholar
  31. 31.
    Darkschewitsch L, Freud S. Ueber die Beziehung des Strickkörpers zum Hinterstrang und Hinterstrangskern nebst Bemerkungen ueber zwei Felden der Onblongata. Neurol Zentralbl. 1886;5:121–9.Google Scholar
  32. 32.
    De Sanctis S. Untersuchungen über den Bau der Markscheidenentwicklung des menschlichen Kleinhirns. Monatsch Psychiatr Neurol. 1898;4:237–46.CrossRefGoogle Scholar
  33. 33.
    Distel H, Holländer H. Autoradiographic tracing of developing subcortical projections of the occipital region in fetal rabbits. J Comp Neurol. 1980;192:505–18.PubMedCrossRefGoogle Scholar
  34. 34.
    Ekerot C-F. The dorsal spino-olivary system in the cat. II. Somatotopical organization. Exp Brain Res. 1979;36:219–32.PubMedCrossRefGoogle Scholar
  35. 35.
    Englund C, Kowallzyk T, Daza RAM, Dagan A, Lau C, Rose MF, Hetner RF. Unipolar brush cells of the cerebellum are produced in the rhombic lip and migrate through developing white matter. J Neurosci. 2006;26:9184–95.PubMedCrossRefGoogle Scholar
  36. 36.
    Feirabend HKP. Anatomy and development of longitudinal patterns in the architecture of the cerebellum of the white leghorn (Gallus domesticus), Thesis Leiden; 1983.Google Scholar
  37. 37.
    Feirabend HKP, van Lusemburg EA, van Denderen-van Dorp H, Voogd J. A 3H thymidine autoradiographic study of the development of the cerebellum of the white leghorn (Gallus domesticus): evidence for longitudinal neuroblast generation patterns. Acta Morph Neerl Scand. 1985;23:115–26.Google Scholar
  38. 38.
    Flechsig P. Die Leitungsbahnen im Gehirn und Rückenmark auf Grund Entwicklungsgeschictlicher Untersuchungen dargestellt. Leipzig; 1876.Google Scholar
  39. 39.
    Fujita H, Morita N, Furuichi T, Sugihara I. Clustered fine compartmentalization of the mouse cerebellar cortex and its rearrangement into the postnatal striped configuration. J Neurosci. 2012;32:15688–703.PubMedCrossRefGoogle Scholar
  40. 40.
    Goldowitz D, Hamre K. The cells and molecules that make a cerebellum. TINS. 1998;21:375–82.PubMedGoogle Scholar
  41. 41.
    Goodlett CR, Hamre KM, West JR. Regional differences in the timing of dendritic outgrowth of Purkinje cells in the vermal cerebellum demonstrated by MAP2 immunocytochemistry. Dev Brain Res. 1990;53:131–4.CrossRefGoogle Scholar
  42. 42.
    Gould BB, Rakic P. The total number, time of origin and kinetics of proliferation of neurons comprising the deep cerebellar nuclei in the Rhesus monkey. Exp Brain Res. 1981;44:195–206.PubMedCrossRefGoogle Scholar
  43. 43.
    Grishkat HL, Eisenman LM. Development of the spinocerebellar projection in the prenatal mouse. J Comp Neurol. 1995;363:93–108.PubMedCrossRefGoogle Scholar
  44. 44.
    Groenewegen HJ, Voogd J. The parasagittal zonation of the olivocerebellar projection. I. Climbing fiber distribution in the vermis of cat cerebellum. J Comp Neurol. 1977;174:417–88.PubMedCrossRefGoogle Scholar
  45. 45.
    Hallonet MR, Teillet M-A, Le Douarin NM. A new approach to the development of the cerebellum provided by the quailchick marker system. Development. 1990;108:19–31.PubMedGoogle Scholar
  46. 46.
    Hashimoto K, Kano M. Postnatal development and synapse elimination of climbing fiber to Purkinje cell projection in the cerebellum. Neurosci Res. 2005;53:221–8.PubMedCrossRefGoogle Scholar
  47. 47.
    Hashimoto M, Mikishiba K. Mediolateral compartmentation of the cerebellum is determined on the “birth date” of Purkinje cells. J Neurosci. 2003;23:11342–51.PubMedCrossRefGoogle Scholar
  48. 48.
    Hawkes R, Leclerc N. Antigenic map of the rat cerebellar cortex: the distribution of parasagittal bands as revealed by monoclonal anti-Purkinje cell antibody mapQ113. J Comp Neurol. 1987;256:29–41.PubMedCrossRefGoogle Scholar
  49. 49.
    Herrick CL. Contributions to the comparative morphology of the central nervous system. I. Illustrations of the architectonic of the cerebellum. J Comp Neurol. 1891;1:2–37.Google Scholar
  50. 50.
    Hess N. De cerebelli gyrorum r textura disquisitiones microscopicae Dopat Schünmann. 1858.Google Scholar
  51. 51.
    Hillman DE, Chen S, Ackman J. Perinatal methylazoxymethanol acetate uncouples coincidence of orientation of cerebellar folia and parallel fibers. Neuroscience. 1988;24:99–110.PubMedCrossRefGoogle Scholar
  52. 52.
    His W. Zur Geschichte des Gehirns sowie der centralen und peripherischen Nervenbahnen beim menschlichen Embryo. Abhandlungen der mathematisch-physichen Classe der Königl. Sachsichen Ges Wiss. 1888;VII:341–92.Google Scholar
  53. 53.
    His W. Die Entwicklug des menschlichen Rautenhirns vom Ende des ersten bis am Beginn des dritten Monats. Abandlungen der mathematischen-physischen Classe der Königl. Sachsichen Ges Wiss. 1891;17:1–74.Google Scholar
  54. 54.
    Hochstetter F. Beträg zur entwicklungsgeschichte des menschlichen Gehirns. Wien/Leipzig: Deuticke; 1929.Google Scholar
  55. 55.
    Ji Z, Hawkes R. Topography of Purkinje cell compartments and mossy fiber terminal fields in lobules II and III of the rat cerebellar cortex: spinocerebellar and cuneocerebellar projections. Neuroscience. 1994;61:935–54.PubMedCrossRefGoogle Scholar
  56. 56.
    Ji Z, Hawkes R. Partial ablation of the neonatal external granular layer disrupts mossy fiber topography in the adult rat cerebellum. J Comp Neurol. 1996;371:578–88.PubMedCrossRefGoogle Scholar
  57. 57.
    Kanemitsu A, Kobayashi Y. Time of origin of Purkinje cells and neurons of the deep cerebellar nuclei of the chick embryo examined with 3H-thymidine autoradiography. Anat Anz. 1988;165:67–75.Google Scholar
  58. 58.
    Kappel RM. The development of the cerebellum in Macaca mulatta. A study of regional differences during corticogenesis. Thesis Leiden; 1981.Google Scholar
  59. 59.
    Karam SD, Burrows RC, Logan C, Koblar S, Pasquale EB, Bothwell M. Eph receptors and ephrins in the developing chick cerebellum: relationship to sagittal patterning and granule cell migration. J Neurosci. 2000;20:6488–500.PubMedCrossRefGoogle Scholar
  60. 60.
    Karam SD, Kim YS, Rothwell M. Granule cells migrate within raphes in the developing cerebellum: an evolutionarily conserved event. J Comp Neurol. 2001;440:127–35.PubMedCrossRefGoogle Scholar
  61. 61.
    Korneliusen HK. Cerebellar corticogenesis in cetacea, with special reference to regional variations. J Hirnforsch. 1967;9:151–85.Google Scholar
  62. 62.
    Korneliusen HK. On the ontogenetic development of the cerebellum (nuclei, fissures and cortex) of the rat, with special reference to regional variations in corticogenesis. J Hirnforsch. 1968;10:379–412.Google Scholar
  63. 63.
    Korneliusen HK, Jansen J. On the early development and homology of the central cerebellar nuclei in cetacea. J Hirnforsch. 1965;8:47–56.Google Scholar
  64. 64.
    Korneliussen HK. Comments on the cerebellum and its division. Brain Res. 1968;8:229–36.PubMedCrossRefGoogle Scholar
  65. 65.
    Kuithan W. Die Entwicklung des Kleinhirns bei Säugetieren, Münchener medizinische Abhandlungen. 1895.Google Scholar
  66. 66.
    Lakke EA, Guldemond JM, Voogd J. The ontogeny of the spinocerebellar projection in the chicken. A study using WGA HRP as a tracer. Acta Histochem Suppl. 1986;27:47–51.Google Scholar
  67. 67.
    Langelaan JW. On the development of the external form of the human cerebellum. Brain. 1919;42:130–70.CrossRefGoogle Scholar
  68. 68.
    Larouche M, Che PM, Hawkes R. Neurogranin expression identifies a novel array of Purkinje cell parasagittal stripes during mouse cerebellar development. J Comp Neurol. 2006;494:215–27.PubMedCrossRefGoogle Scholar
  69. 69.
    Larramendi LMH. Analysis of synaptogenesis in the cerebellum of the mouse. In: Llinas R, editor. Neurobiology of cerebellar evolution and development. Chicago: AMA; 1969. p. 803–43.Google Scholar
  70. 70.
    Larsell O. Cerebellum and corpus pontobulbare of the bat (Myotis). J Comp Neurol. 1936;64:299–345.CrossRefGoogle Scholar
  71. 71.
    Larsell O. The development and subdivisions of the cerebellum of birds. J Comp Neurol. 1948;98:123–82.CrossRefGoogle Scholar
  72. 72.
    Larsell O. The morphogenesis and adult pattern of the lobules and tissues of the cerebellum of the white rat. J Comp Neurol. 1952;97:281–356.PubMedCrossRefGoogle Scholar
  73. 73.
    Leclerc N, Gravel C, Hawkes R. Development of parasagittal zonation in the rat cerebellar cortex: MabQ113 antigenic bands are created postnatally by the suppression of antigen expression in a subset of Purkinje cells. J Comp Neurol. 1988;273:399–420.PubMedCrossRefGoogle Scholar
  74. 74.
    Leto E, Arancillo M, Becker EBE, Busso A, Chiang C, Baodin J, Dubyns WB, Dusart I, Haldipur P, Hatten ME, Hoshino M, Joyner AL, Kano M, Kilpatrisck DL, Koibuchi N, Marino S, Martinez S, Muillen KJ, Millnner TO, Miyata T, Parmigiani E, Schilling S, Sekerková G, Sillitoe RV, Sotelo C, Uesaka N, Wefers A, Wingatae RJT, Hawkes R. Consensus paper: cerebellar deveopment. Cerebellum. 2015;15:789–828.PubMedCentralCrossRefPubMedGoogle Scholar
  75. 75.
    Lin JC, Cepko CL. Granule cell raphes and parasagittal domains of Purkinje cells: complementary patterns in developing chick cerebellum. J Neurosci. 1998;18:9342–53.PubMedCrossRefGoogle Scholar
  76. 76.
    Lugaro. Ueber die Histogenese der Körner der Kleinhirnrinde. Anat Anz. 1894;10:710–3.Google Scholar
  77. 77.
    Machold R, Fishell G. Math 1 is expressed in temporary discrete pools of cerebellar rhombic-lip neural progenitors. Neuron. 2005;48:17–24.PubMedCrossRefGoogle Scholar
  78. 78.
    Maklad A, Fritsch B. Partial separation of posterior crista and saccular fibers to the nodulus and uvula of the cerebellum in mice, and its development. Dev Brain Res. 2003;140:223–36.CrossRefGoogle Scholar
  79. 79.
    Marin F, Puelles L. Morphological fate of rhombomeres in quail/chick chimeras: a segmental analysis of hindbrain nuclei. Eur J Neurosci. 1995;7:1714–38.PubMedCrossRefGoogle Scholar
  80. 80.
    Martinez S, Alvarado-Mallart R-M. Rostral cerebellum originates from the caudal portion of the so-called ‘mesencephalic’ vesicle: a study using chick/quail chimeras. J Neurosci. 1989;1:549–60.Google Scholar
  81. 81.
    Miale IL, Sidman RL. An autoradiographic analysis of histogenesis in the mouse cerebellum. Exp Neurol. 1961;4:77–295.CrossRefGoogle Scholar
  82. 82.
    Morara S, Van der Want JJL, De Weerd H, Provini L, Rosina A. Ultrastructural analysis of climbing fiber-Purkinje cell synaptogenesis in the rat cerebellum. Neuroscience. 2001;108:655–71.PubMedCrossRefGoogle Scholar
  83. 83.
    Morris RJ, Beech JN, Heizmann CW. Two distinct phases and mechanisms of axonal growth shown in primary vestibular fibers in the brain demonstrated by parvalbumin immunohistochemistry. Neuroscience. 1988;27:571–96.PubMedCrossRefPubMedCentralGoogle Scholar
  84. 84.
    Nagata I, Katsuhiko O, Wawana A, Kimura-Kuroda J. Aligned neurite bundles of granule cells regulate orientation of Purkinje cell dentrites by perpendicular contact guidance in two-dimensional and three-dimensional mouse cerebellar cultures. J Comp Neurol. 2006;499:274–89.PubMedCrossRefGoogle Scholar
  85. 85.
    Namba K, Sugihara I, Hashimoto M. Close correlation between the birth date of Purkinje cells and the longitudinal compartmentalization of the mouse adult cerebellum. J Comp Neurol. 2011;519:2594–614.PubMedCrossRefGoogle Scholar
  86. 86.
    Neudert F, Nuernberger KK, Redies C. Comparative analysis of cadherin expression and connectivity patterns in the cerebellar system of ferret and mouse. J Comp Neurol. 2008;511:736–52.PubMedCrossRefGoogle Scholar
  87. 87.
    Niewenhuys R, Puelles L. Toward a new neuromorphology. New York: Springer; 2016.CrossRefGoogle Scholar
  88. 88.
    Nieuwenhuys R, Voogd J, van Huijzen C. The human central nervous system. 4th ed. Heidelberg: Springer; 2008.CrossRefGoogle Scholar
  89. 89.
    Nishida K, Flanagan JG, Nakamoto M. Domain-specific olivocerebellar projection regulated by the EphA-ephrin-A interaction. Development. 2002;129:5647–58.PubMedCrossRefGoogle Scholar
  90. 90.
    Obersteiner H. Beiträge zur Kenntniss vom feineren Bau der Kleinhirnrinde mit besonderer Berücksichtigung der Entwicklung. Sitzungsberichte der kaiserlichen Akademie der Wissenschaften. Math Naturwisenschaftliche Klasse Abth II. 1869;60:101–14.Google Scholar
  91. 91.
    Okado N, Yoshimoto M, Furber SE. Pathway formation and the terminal distribution pattern of the spinocerebellar projection in the chick embryo. Anat Embryol (Berl). 1987;176:165–74.CrossRefGoogle Scholar
  92. 92.
    Paradies MA, Grishkat HL, Smeyne RJ, Oberdick J, Morgan JI, Eisenman LM. Correspondence between L7-LacZ-expressing Purkinje cells and labeled olivocerebellar fibers during late embryogenesis in the mouse. J Comp Neurol. 1996;374:451–66.PubMedCrossRefGoogle Scholar
  93. 93.
    Pierce ET. Histogenesis of the deep cerebellar nuclei in the mouse: an autoradiographic study. Brain Res. 1975;95:503–18.PubMedCrossRefGoogle Scholar
  94. 94.
    Pitman T, Tolbert DL. Organization of transient projections from the p[rimary] somatosensory cortex to the cerebellar nuclei in kittens. Anat Embryol (Berl). 1988;178:441–7.CrossRefGoogle Scholar
  95. 95.
    Popoff. Ueber die Histogenese der Kleinhirnrinde. Biol Centralblatt. 1897;17:485–512. 530–542, 605–620, 640–650, 664–687Google Scholar
  96. 96.
    Pourquié O, Hallonet MR, Le Douarin NM. Association of BEN glycoprotein expression with climbing fiber axogenesis in the avian cerebellum. J Neurosci. 1992;12:1548–57.PubMedCrossRefGoogle Scholar
  97. 97.
    Rakic P. Principles of neural cell migration. Experientia. 1990;46:882–91.PubMedCrossRefGoogle Scholar
  98. 98.
    Redies C, Luckner R, Arndt K. Granule cell raphes in the cerebellar cortex of chicken and mouse. Brain Res Bull. 2002;57:341.PubMedCrossRefGoogle Scholar
  99. 99.
    Redies C, Neudert F, Lin JC. Cadherins in cerebellar development: translation of embryonic patterning into mature functional compartmentalization. Cerebellum. 2011;10:393–408.PubMedCrossRefGoogle Scholar
  100. 100.
    Rüdeberg S-I. Morphogenetic studies on the cerebellar nuclei and their homologization in different vertebrates including man. Lund: Hakan Olssons; 1961.Google Scholar
  101. 101.
    Saetersdal TAS. On the ontogenesis of the avian cerebellum. Part III. Formation of fissures with a discussion of fissure homologies between the avian and mammalian cerebellum. Universitetet i Bergen Arbok Naturvitenskapelig Rekke. 1959b;3:5–44.Google Scholar
  102. 102.
    Schaper A. Die morphologische und histologsche Entwicklung des Kleinhirns der Teleostier. Anat Anz. 1894;9:489–501.Google Scholar
  103. 103.
    Sekerková G, Iljic E, Mugnaini E. Time of origin of unipolar brush cells in the rat cerebellum as observed by prenatal bromodeoxyuridine labeling. Neuroscience. 2004;127:845–58.PubMedCrossRefGoogle Scholar
  104. 104.
    Sgaier SK, Millet S, Villanueva MP, Berensteyn F, Song C, Joyner AL. Morphogenetic and cellular movements that shape the mouse cerebellum: insights from genetic fate mapping. Neuron. 2005;45:27–40.PubMedPubMedCentralGoogle Scholar
  105. 105.
    Smith GE. The primary subdivision of the mammalian cerebellum. J Anat Physiol. 1902;36:381–5.PubMedPubMedCentralGoogle Scholar
  106. 106.
    Stroud BB. The mammalian cerebellum. J Comp Neurol. 1895;5:71–118.CrossRefGoogle Scholar
  107. 107.
    Sugihara I, Shinoda Y. Molecular, topographic, and functional organization of the cerebellar cortex: a study with combined aldolase C and olivocerebellar labeling. J Neurosci. 2004;24:8771–85.PubMedCrossRefGoogle Scholar
  108. 108.
    Tello JF. Histogenése du cervelet et ses voies cehz la souris blanche. Trab Inst Cajal Invest Biol. 1940;32:1–72.Google Scholar
  109. 109.
    Tolbert DL. Somatotopically organized transient projections from the primary somatosensory cortex to the cerebellar cortex. Dev Brain Res. 1989;45:113–27.CrossRefGoogle Scholar
  110. 110.
    Tolbert DL, Panneton WM. Transient cerebrocerebellar projections in kittens: postnatal development and topography. J Comp Neurol. 1983;221:216–28.PubMedCrossRefGoogle Scholar
  111. 111.
    Vaage S. The segmentation of the primitive neural tube in chick embryos (Gallus domesticus). A morphological, histochemical and autoradiographical investigation. Adv Anat Embryol Cell Biol. 1969;41:1–81.Google Scholar
  112. 112.
    Vielvoye GJ. Spinocerebellar tracts in the white leghorn (Gallus domesticus), Thesis Leiden; 1977.Google Scholar
  113. 113.
    Voogd J. The cerebellum of the cat, thesis Leiden, Assen: van Gorcum; 1964.Google Scholar
  114. 114.
    Voogd J. The importance of fiber connections in the comparative anatomy of the mammalian cerebellum. In: Llinas R, editor. Neurobiology of cerebellar evolution and development. Chicago: AMA; 1969. p. 493–514.Google Scholar
  115. 115.
    Voogd J. Cerebellum and precerebellar nuclei. In: Paxinos G, Mai JK, editors. The human nervous system. Amsterdam: Elsevier; 2004. p. 321–92.CrossRefGoogle Scholar
  116. 116.
    Voogd J, van Baarsen K. The horseshoe-shaped commissure of Wernekinck or the decusation of the brachium conjunctivum. Methodological changes in the 1840s. Cerebellum. 2014;13:113–20.PubMedCrossRefGoogle Scholar
  117. 117.
    Voogd J, Ruigrok TJ. The organization of the corticonuclear and olivocerebellar climbing fiber projections to the rat cerebellar vermis: the congruence of projection zones and the zebrin pattern. J Neurocytol. 2004;33:5–21.PubMedCrossRefGoogle Scholar
  118. 118.
    Voogd J, Pardoe J, Ruigrok TJ, Apps R. The distribution of climbing and mossy fiber collateral branches from the copula pyramidis and the paramedian lobule: congruence of climbing fiber cortical zones and the pattern of zebrin banding within the rat cerebellum. J Neurosci. 2003;23:4645–56.PubMedCrossRefGoogle Scholar
  119. 119.
    Wang VY, Szoghbi HY. Math 1 expression redefines the rhombic lip derivates and reveals novel lineages within the brainstem and cerebellum. Neuron. 2005;48:31–43.PubMedCrossRefGoogle Scholar
  120. 120.
    Wassef M, Sotelo C. Asynchrony in the expression of guanosine 3′:5′-phosphate-dependent protein kinase by clusters of Purkinje cells during the perinatal development of rat cerebellum. Neuroscience. 1984;13:1217–41.PubMedCrossRefPubMedCentralGoogle Scholar
  121. 121.
    Wassef M, Chedotal A, Cholley B, Thomasset M, Heizmann CW, Sotelo C. Development of the olivocerebellar projection in the rat: I. Transient biochemical compartmentation of the inferior olive. J Comp Neurol. 1992a;323:519–36.PubMedCrossRefPubMedCentralGoogle Scholar
  122. 122.
    Wassef M, Cholley B, Heizmann CW, Sotelo C. Development of the olivocerebellar projection in the rat: II. Matching of the developmental compartments of the cerebellum and inferior olive through the projection map. J Comp Neurol. 1992b;323:537–50.PubMedCrossRefGoogle Scholar
  123. 123.
    Wassef M, Zanetta JP, Breher A, Sotelo C. Transient biochemical compartmentalization of Purkinje cells during early cerebellar development. Dev Biol. 1985;111:129–37.PubMedCrossRefGoogle Scholar
  124. 124.
    Widenreich F. Zur Anatomie dr zentralen Kleinhirnkerne der Sáuger. Z Morphol Antrhropol. 1899;1:259–312.Google Scholar
  125. 125.
    Yuasa S, Kawamura K, Ono K, Yamakuni T, Takahashi Y. Development and migration of Purkinje cells in the mouse cerebellar primordium. Anat Embryol. 1991;184:195–212.PubMedCrossRefGoogle Scholar
  126. 126.
    Zhang L, Goldman JE. Developmental fates and migratory pathways of dividing progenitors in the postnatal rat cerebellum. J Comp Neurol. 1996a;370:536–50.PubMedCrossRefGoogle Scholar
  127. 127.
    Zhang L, Goldman JE. Generation of cerebellar interneurons from dividing progenitors in white matter. Neuron. 1996b;16:47–54.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department NeuroscienceErasmus Medical CenterRotterdamThe Netherlands

Personalised recommendations