Antigenic compartmentation of the cerebellar cortex in the chicken (Gallus domesticus)

Journal of Comparative Neurology

Volumn 518, Issue 12, 2010, Pages 2221-2239

  Marzban, Hassan ^a   Chung, Seung Hyuk ^a   Pezhouh, Maryam Kherad ^a   Feirabend, Hans ^b   Watanabe, Masahiko ^c   Voogd, Jan ^d   Hawkes, Richard ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c HOKKAIDO UNIVERSITY   (Japan)

^d ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Pattern formation; Phospholipase c 4; Purkinje cell; Stripe; Whole mount immunohistochemistry; Zebrin ii

Indexed keywords

ALDOLASE C; ANTIGEN; PHOSPHOLIPASE C BETA4; UNCLASSIFIED DRUG; ZEBRIN 2;

ADULT ANIMAL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; BRAIN DEVELOPMENT; CEREBELLUM CORTEX; CEREBELLUM VERMIS; CHICKEN; CONTROLLED STUDY; HEMISPHERE; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; WESTERN BLOTTING;

AGING; ANIMALS; ANTIGENS; AVIAN PROTEINS; BLOTTING, WESTERN; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CEREBELLAR CORTEX; CHICKENS; IMMUNOHISTOCHEMISTRY; NERVE TISSUE PROTEINS; PHOSPHOLIPASE C BETA; SPECIES SPECIFICITY;

EID: 77952119187     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22328     Document Type: Article

References (123)

1. AhnAH,DziennisS,HawkesR,HerrupK.1994. ThecloningofzebrinIIrevealsitsidentitywithaldolaseC.Development120:2081-2090. (Pubitemid24232276)
2. Akaogi K-I, Sato Y, lkarashi K, Kawasaki T. 1994. Mossy fiber projections from the brain stem to the nodulus in the cat. An experimental study comparing the nodulus, the uvula and the flocculus. Brain Res 638: 12-20.
3. Akintunde A, Eisenman LM. 1994. External cuneocerebellar projections and Purkinje cell zebrin II stripes: a direct comparison of parasagittal striping in the mouse cerebellum. J Chem Neuroanat 7: 75-86. (Pubitemid 24271596)
4. Apps R, Garwicz M. 2005. Anatomical and physiological foundations of cerebellar information processing. Nat Rev Neurosci 6: 297-311. (Pubitemid 40469984)
5. Apps R, Hawkes R. 2009. Cerebellar cortical organization: a one-map hypothesis. Nature Rev Neurosci 10: 670-681.
6. Arends J, Voogd J. 1989. Topographic aspects of the olivocerebellar system in the pigeon. Exp Brain Res 17(suppl): 52-57.
7. Arends JJ, Zeigler HP. 1991. Organization of the cerebellum in the pigeon (Columba livia): I. Corticonuclear and corticovestibular connections. J Comp Neurol 306: 221-244.
8. Armstrong C, Hawkes R. 2000. Pattern formation in the cerebellar cortex. Biochem Cell Biol 78: 551-562.
9. Armstrong C, Hawkes R. 2001. Selective failure of Purkinje cell dispersion in the cerebellum of the weaver mouse. J Comp Neurol 439: 151-161. (Pubitemid 32906019)
10. Armstrong CL, Krueger-Naug AM, Currie WC, Hawkes R. 2000. Constitutive expression of the 25 kDa heat shock protein HSP25 reveals novel parasagittal stripes of Purkinje cells in the adult mouse cerebellar cortex. J Comp Neurol 416: 383-397. (Pubitemid 30027135)
11. Arndt K, Redies C. 1998. Development of cadherin-defined parasagittal subdivisions in the embryonic chick cerebellum. J Comp Neurol 401: 367-381. (Pubitemid 28489522)
12. Baimbridge KG, Miller JJ. 1982. Immunohistochemical localization of calcium-binding protein in the cerebellum, hippocampal formation and olfactory bulb of the rat Brain Res 245: 223-229.
13. Beierbach E, Park C, Ackerman SL, Goldowitz D, Hawkes R. 2001. Abnormal dispersion of a Purkinje cell subset in the mouse mutant cerebellar deficient folia (cdf). J Comp Neurol 436: 42-51.
14. Brandis F. 1894. Untersuchungen über das Gehirn der Vögel. II Tiel: Das Kleinhirn. Arch Mikr Anat 43: 787-813.
15. BrechaN,KartenHJ,HuntSP.1980. Projectionsofthenucleusofthebasalopticrootinthepigeon: anautoradiographicandhorseradishperoxidasestudy.JCompNeurol189:615-670. (Pubitemid10105676)
16. BrochuG,MalerL,HawkesR.1990.ZebrinII: apolypeptideantigenexpressedselectivelybyPurkinjecellsrevealscompartmentsinrata ndfishcerebellum.JCompNeurol291:538-552.(Pubitemid20047467)
17. Brodai A, Kristiansen K, Jansen J. 1950. Experimental demonstration of a pontine homolog in birds. J Comp Neurol 92: 23-69.
18. Chockkan V, Hawkes R. 1994. Functional and antigenic maps in the rat cerebellum: zebrin compartmentation and vibrissal receptive fields in lobule IXa. J Comp Neurol 345: 33-45. (Pubitemid 24179416)
19. Chung SH, Marzban H, Croci L, Consalez GG, Hawkes R. 2008. Purkinje cell subtype specification in the cerebellar cortex: EBF2 acts to repress the zebrin II-negative Purkinje cell phenotype. Neuroscience 153: 721-732.
20. Chung SH, Marzban H, Watanabe M, Hawkes R. 2009. Phospholipase Cβ4 identifies a novel subset of unipolar brush cells in the adult mouse cerebellum. Cerebellum 8: 267-276.
21. Clarke PG. 1976. Proceedings: The visual input to the pigeon cerebellum. J Physiol 258: 61P-62P.
22. Clarke PG. 1977. Some visual and other connections to the cerebellum of the pigeon. J Comp Neurol 174: 535-552.
23. Comolli A. 1911. Per una nueva divisione del cerveletto. Arch Ital Anat Embryol 9: 247-273.
24. Croci L, Chung S-H, Masserdotti G, Gianola S, Motti E, Tonini R, Braida D, Bizzoca A, Gennarini G, Corradi A, Sala M, Rossi F, Hawkes R, Consalez GG. 2006. A key role for the HLH transcription factor EBF2 (COE2, O/E-3) in Purkinje neuron migration and cerebellar cortical topography. Development 133: 2719-2729. (Pubitemid 44177892)
25. Crowder NA, Winship IR, Wylie DR. 2000. Topographic organization of inferior olive cells projecting to translational zones in the vestibulocerebellum of pigeons. J Comp Neurol 419: 87-95.
26. Davis CA. 1993. Whole-mount immunohistochemistry. Methods Enzymol 225: 502-516.
27. De Camilli P, Miller PE, Levitt P, Walter U, Greengard P. 1984. Anatomy of cerebellar Purkinje cells in the rat determined by a specific immunohistochemical marker. Neuroscience 11: 761-817. (Pubitemid 14111172)
28. DentJA,PoisonAG,KlymkowskyMW.1989.Awhole- mountimmunocytochemicalanalysisoftheexpressionoftheintermediatefilamentprotein vimentininXenopus.Development105:61-74.(Pubitemid19046650)
29. Doré L, Jacobson C, Hawkes R. 1990. Organization and postnatal development of zebrin II antigenic compartmentation in the cerebellar vermis of the grey opossum, Monodelphis domestica. J Comp Neurol 291: 431-449. (Pubitemid 20028781)
30. Edinger L. 1910. Ueber die Eintheilung des Zerebellums. Anat Anz 35: 319-323.
31. EisenmanLM,HawkesR.1993. Antigeniccompartmentationinthemousecerebellarcortex:zebrinIIandHNK- 1revealacomplex,overlappingmoleculartopography.JCompNeurol335:586-605. (Pubitemid23254255)
32. Fabrici G. 1612. De formatione ovi et pulli. Patavii, (Padua).
33. Feirabend HKP. 1983. Anatomy and development of longitudinal patterns in the architecture of the cerebellum of the white leghorn (Gallus domesticus). Thesis, University of Leiden.
34. Feirabend HKP. 1990. Development of longitudinal patterns in the cerebellum of the chicken (Gallus domesticus): a cytoarchitectural study on the genesis of cerebellar modules. Eur J Morphol 28: 169-223.
35. Feirabend HKP, Voogd J. 1986. Myeloarchitecture of the cerebellum of the chicken (Gallus domesticus): an atlas of the compartmental subdivision of the cerebellar white matter. J Comp Neurol 251: 44-66.
36. Feirabend HKP, Choufoer H, Voogd J. 1996. White matter of the cerebellum of the chicken (Gallus domesticus): a quantitative light and electron microscopic analysis of myelinated fibers and fiber eompartmenta J Comp Neural 369: 236-251.
37. Freedman SL, Feirabend HKP, Vielvoye GJ, Voogd J. 1975. Reexamination of the ponto-cerebellar projection in the adult white leghorn (Gallus domesticus). Acta Morphoi Neerl Scand 13: 236-238.
38. Gallagher E, Howell BW, Soriano P, Cooper JA, Hawkes R. 1998. Cerebellar abnormalities in the disabled (mdabl-1) mouse. J Comp Neurol 402: 238-251.
39. Gamlin PD, Cohen DH. 1988. Projections of the retinorecipient pretectal nuclei in the pigeon (Columba livia). J Comp Neurol 269: 18-46.
40. Gravel C, Hawkes R. 1990. Parasagittal organization of the rat cerebellar cortex: direct comparison of Purkinje cell compartments and the organization of the spinocerebellar projection. J Comp Neurol 291: 79-102. (Pubitemid 20035900)
41. Gravel C, Eisenman LE, Sasseville R, Hawkes R. 1987. Parasagittal organization of the rat cerebellar cortex: a direct correlation between antigenic Purkinje cell stripes revealed by mabQ113 and the organization of the olivocerebellar projection. J Comp Neurol 263: 294-310. (Pubitemid 17160251)
42. Hallem JS, Thompson JH, Gundappa-Sulur G, Hawkes R, BjaaHe JG, Bower JM. 1999. Spatial correspondence between tactile projection patterns and the distribution of the antigenic Purkinje cell markers anti-zebrin I and anti-zebrin II in the cerebellar folium crus IIA of the rat. Neuroscience 93: 1083-1094. (Pubitemid 29341655)
43. Hawkes R. 1997. An anatomical model of cerebellar modules. Prog Brain Res 114: 39-52.
44. HawkesR,EisenmanLM.1997.Stripesandzones: theoriginsofregionalizationoftheadultcerebellum.PerspectDevNeurobiol5:95-104. (Pubitemid28140966)
45. Hawkes R, Gravel C. 1991. The modular cerebellum. Prog Neurobiol 36: 309-327.
46. Hawkes R, Herrup K. 1996. Aldolase C/zebrin II and the regionalization of the cerebellum. J Mol Neurobiol 6: 147-158.
47. Hawkes R, Brochu G, Doré L, Gravel C, Lecierc N. 1992. Zebrins: molecular markers of compartmentation in the cerebellum. In: Llinás R, Sotelo C, editors. The cerebellum revisited. New York: Springer-Verlag, p 22-55.
48. Herrup K, Kuemerle, B. 1997. The compartmentalization of the cerebellum. Annu Rev Neurosci 20: 61-90.
49. Hirai N. 1981. Vestibular afferent inputs to lobules I and II of the cerebellar anterior lobe in the cat Brain Res 277: 145-149.
50. Hirai N, Hongo T, Sasaki S, Yoshida K. 1979. The neck and labyrinthine influences on cervical spinocerebellar tract neurones of the central cervical nucleus in the cat. Prog Brain Res 30: 529-536.
51. HiraiN,HongoT,SasakiS.1984.Aphysiologicalstudyofidentification, axonalcourseandcerebellarprojectionofspinocerebellartractcellsinthecentralcervi calnucleusofthecat.BrainRes55:272-285.(Pubitemid14075492)
52. Huber GC, Crosby EC. 1929. The nuclei and fiber paths of the avian diencephalon, with consideration of telencephalic and certain mesencephalic centers and connections. J Comp Neuroi 48: 1-225.
53. Ingvar S. 1918. Zur Phylo- und Ontogenese des Kleinhirns. Folia Neurobiol 11: 205-495.
54. Iwaniuk AN, Marzban H, Pakan JP, Watanabe M, Hawkes R, Wylie DR. 2009. Compartmentation of the cerebellar cortex of hummingbirds (Aves: Trochilidae) revealed by the expression of zebrin II and phospholipase Cβ4. J Chem Neuroanat 37: 55-63.
55. JandeSS,TolnaiS,LawsonDE.1981.ImmunohistochemicallocalizationofvitaminD- dependentcalcium-bindingproteininduodenum,kidney,uterusandcerebellumofchickens. Histochemistry71:99-116.(Pubitemid11079383)
56. Ji Z, Hawkes R. 1994. 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 61: 935-954. (Pubitemid 24291933)
57. Kano M, Hashimoto K, Watanabe M, Kurihara H, Offermanns S, Jiang H, Wu Y, Jun K, Shin HS, lnoue Y, Simon Ml, Wu D. 1998. Phospholipase Cβ4 is specifically involved in climbing fiber synapse elimination in the developing cerebellum. Proc Natl Acad Sci U S A 95: 15724-15729.
58. Kim, JY, Marzban H, Chung SH, Watanabe M, Eisenman LM, Hawkes R. 2009. Purkinje cell compartmentation of the cerebellum of microchiropteran bats. J Comp Neurol 517: 193-219.
59. Larouche M, Diep C, Sillitoe RV, Hawkes R. 2003. The topographical anatomy of the cerebellum in the guinea pig, Cavia porcellus. Brain Res 965: 159-169. (Pubitemid 36183698)
60. Larouche M, Beffert U, Herz J, Hawkes R. 2008. The Reelin receptors Apoer2 and VIdIr coordinate the patterning of Purkinje cell topography in the developing mouse cerebellum. PLoSONE 3:e1653. (Pubitemid 351865655)
61. Larsell O. 1948. The development and subdivisions of the cerebellum of birds. J Comp Neurol 89: 123-182.
62. Larsell O. 1967. The cerebellum: from myxinoids through birds (Jansen J, editor). Minneapolis, MN: The University of Minnesota Press.
63. Liu A, Joyner AL. 2001 Early anterior/posterior patterning of the midbrain and cerebellum. Annu Rev Neurosci 24: 869-896. (Pubitemid 32695247)
64. Logan C, Millar C, Bharadia V, Rouleau K. 2002. Onset of TIx3 expression in the chick cerebellar cortex correlates with the morphological development of fissures and delineates a posterior transverse boundary. J Comp Neurol 448: 138-149. (Pubitemid 34538764)
65. Marzban H, Khanzada U, Shabir S, Hawkes R, Langnaese K, Smalla K-H, Bockers TM, Gundelfinger ED, Gordon-Weeks PR, Beesley PW. 2003a. Expression of the immunoglobulin superfamily neuroplastin adhesion molecules in adult and developing mouse cerebellum and their localization to parasagittal stripes. J Comp Neurol 462: 286-301. (Pubitemid 36736712)
66. Marzban H, Zahedi S, Sanchez M, Hawkes R. 2003b. Antigenic compartmentation of the cerebellar cortex of the Syrian hamster, Mesocricetus auratus. Brain Res 974: 176-183. (Pubitemid 36644164)
67. Marzban H, Sillitoe RV, Hoy M, Chung SH, Rafuse VF, Hawkes R. 2004. Abnormal HNK-1 expression in the cerebellum of an N-CAM null mouse. J Neurocytol 33: 117-130. (Pubitemid 38860223)
68. Marzban H, Chung S, Watanabe M, Hawkes R. 2007. Phospholipase Cβ4 expression reveals the continuity of cerebellar topography during development. J Comp Neurol 502: 857-871. (Pubitemid 46732501)
69. Marzban H, Kim C-T, Doom D, Chung S-H, Hawkes R. 2008. A novel transverse expression domain in the mouse cerebellum revealed by a neurofilament- assoeiated antigen. Neuroscience 153: 1190-1201.
70. Matsushita M, Tanami T. 1987. Spinocerebellar projections from the central cervical nucleus in the cat, as studied by anterograde transport of wheat germ agglutinin-horseradish peroxidase. J Comp Neurol 266: 376-397. (Pubitemid 18003971)
71. Nakamura M, Sato K, Fukaya M, Araishi K, Aiba A, Kano M, Watanabe M. 2004. Signaling complex formation of phospholipase Cβ4 with metabotropic glutamate receptor type 1 alpha and 1,4,5-triphosphate receptor at the perisynapse and endoplasmic reticulum in the mouse brain. Eur J Neurosci 20: 2929-2944. (Pubitemid 40007287)
72. Nakamura H, Sato T, Suzuki-Hirano A. 2008. Isthmus organizer for mesencephalon and metencephalon. Dev Growth Differ 50 (suppl 1): 113-118.
73. Narboux-Nême N, Louvi A, Alexandre P, Wassef M. 2005. Regionalization of the isthmic and cerebellar primordial. Prog Brain Res 148: 29-36.
74. Necker R. 2001. Spinocerebellar projections in the pigeon with special reference to the neck region of the body. J Comp Neurol 429: 403-418. (Pubitemid 32010047)
75. Neudert F, Redies C. 2008. Neural circuits revealed by axon tracing and mapping Cadherin expression in the embryonic chicken cerebellum. J Comp Neurol. 509: 283-301.
76. Neudert F, Nuernberger KK, Redies C. 2008. Comparative analysis of Cadherin expression and connectivity patterns in the cerebellar system of ferret and mouse. J Comp Neurol 511: 736-752.
77. Oberdick J, Schilling K, Smeyne RJ, Corbin RJ, Bocchiaro C, Morgan JI. 1993. Control of segment-like patterns of gene expression in the mouse cerebellum. Neuron 10: 1007-1018. (Pubitemid 23194392)
78. Oberdick J, Baader SL, Schilling K. 1998. From zebra stripes to postal zones: deciphering patterns of gene expression in the cerebellum. Trends Neurosci 21: 383-390. (Pubitemid 28384555)
79. Okado N, Ito R, Homma S. 1987. The terminal distribution pattern of spinocerebellar fibers. An anterograde labelling study in the posthatching chick. Anat Embryol (Berl) 176: 175-182.
80. Ozol K, Hayden JM, Oberdick J, Hawkes R. 1999. Transverse zones in the vermis of the mouse cerebellum. J Comp Neurol 412: 95-111. (Pubitemid 29380327)
81. Pakan JMP, Wylie DR. 2006. Two optic flow pathways from the pretectal nucleus lentiformis mesencephali to the cerebellum, in pigeons (Columba lima). J Comp Neurol 499: 732-744.
82. Pakan JMP, Wylie DR. 2008. Congruence of zebrin II expression and functional zones defined by climbing fiber topography in the flocculus. Neuroscience 157: 57-69.
83. Pakan JMP, Iwaniuk AN, Wong Wylie DR, Hawkes R, Marzban H. 2007. Purkinje cell compartmentation as revealed by zebrin II expression in the cerebellar cortex of pigeons (Columba livia). J Comp Neurol 501: 619-630. (Pubitemid 46622499)
84. Pakan JM, Graham DJ, Iwaniuk AN, Wylie DR. 2008. Differential projections from the vestibular nuclei to the flocculus and uvula-nodulus in pigeons (Columba tivia). J Comp Neurol 508: 402-417.
85. Pijpers A, Apps R, Pardoe J, Voogd J, Ruigrok TJ. 2006. Precise spatial relationships between mossy fibers and climbing fibers in rat cerebellar cortical zones. J Neurosci 26: 12067-12080. (Pubitemid 44772117)
86. Sanchez M, Sillitoe RV, Attwell PJ, Ivarsson M, Rahman S, Yeo CH, Hawkes R. 2002. Compartmentation of the rabbit cerebellar cortex. J Comp Neurol 444: 159-173.
87. Sama JR, Marzban H, Watanabe M, Hawkes R. 2006. Complementary stripes of phospholipase Cβ3 and Cβ4 expression by Purkinje cell subsets in the mouse cerebellum. J Comp Neurol 496: 303-313. (Pubitemid 41798082)
88. Sawada K, Fukui Y, Hawkes R. 2008. Spatial distribution of corticotropin-releasing factor immunopositive climbing fibers in the mouse cerebellum: analysis by whole mount immunocytochemistry. Brain Res 1222: 106-117.
89. Schwarz IE, Schwarz DW. 1983. The primary vestibular projection to the cerebellar cortex in the pigeon (Columba livia). J Comp Neurol 216: 438-444.
90. Seil FJ, Johnson ML, Hawkes R. 1995. Molecular compartmentation expressed in cerebellar cultures in the absence of neuronal activity and neuron-glial interactions. J Comp Neurol 356: 398-407.
91. Shimazono J. 1912. Das Kleinhirn der Vögel. Arch Mikr Anat 80: 397-449.
92. SillitoeRV,HawkesR.2002.Whole-mountimmunohistochemistry: ahigh-throughputscreenforpatterningdefectsinthemousecerebellum, JHistochemCytochem50:235-244.(Pubitemid34106762)
93. 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.
94. Sillitoe RV, Hulliger M, Dyck R, Hawkes, R. 2003a. Antigenic compartmentation of the cat cerebellar cortex. Brain Res 977: 1-15. (Pubitemid 36644164)
95. Sillitoe RV, Künzle H, Hawkes R. 2003b. Zebrin II compartmentation of the cerebellum in a basal insectivore, the Madagascan hedgehog tenrec Echinops telfairi. J Anat 203: 283-296. (Pubitemid 37160665)
96. Sillitoe RV, MaIz C, Rockland K, Hawkes R. 2004. Antigenic compartmentation of the primate and scandentid cerebellum: a common topography of zebrin II in Macaca mulatta and Tupaia belangerie. J Anat 204: 257-269. (Pubitemid 38515143)
97. Sillitoe RV, Marzban H, Larouche M, Zahedi S, Affanni J, Hawkes R. 2005. Conservation of the architecture of the anterior lobe vermis of the cerebellum across mammalian species. Prog Brain Res 148: 283-297. (Pubitemid 40127312)
98. 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: 8771-8785. (Pubitemid 39362972)
99. Sugiyama T, Hirono M, Suzuki K, Nakamura Y, Aiba A, Nakamura K, Nakao K, Katsuki M, Yoshioka T. 1999. Localization of phospholipase Cβ isozymes in the mouse cerebellum. Biochem Biophys Res Commun 265: 473-478.
100. TakacsJ,MarkovaL,BorostyankoiZ,GoresTJ,HamoriJ.1999. Metabotropicglutamatereceptortype1aexpressingunipolarbrushcellsinthecerebellarc ortexofdifferentspecies:acomparativequantitativestudy.JNeurosciRes55:733-748. (Pubitemid29173487)
101. Tano D, Napieralski JA, Eisenman LM, Messer A, Plummer, J, Hawkes R. 1992. Novel developmental boundary in the cerebellum revealed by zebrin expression in the lurcher (Lc/+) mutant mouse. J Comp Neurol 323: 128-136.
102. Vielvoye GJ. 1977. Spinocerebellar tracts in the white leghom (Gallus domesticus). Thesis, University of Leiden.
103. Vielvoye GJ, Voogd J. 1977. Time dependence of terminal degeneration in spino-cerebellar mossy fiber rosettes in the chicken and the application of terminal degeneration in successive degeneration experiments. J Comp Neurol 175: 233-242. (Pubitemid 8164478)
104. Voogd J. 1967. Comparative aspects of the structure and fibre connections of the mammalian cerebellum. Prog Brain Res 25: 94-134.
105. Voogd J, Barmack NH. 2005. Oculomotor cerebellum. Prog Brain Res 151: 231-268.
106. VoogdJ,RuigrokTJ.1997. Transverseandlongitudinalpatternsinthemammaliancerebellum.ProgBrainRes114:21-37. (Pubitemid27244963)
107. Voogd J, Ruigrok TJ. 2004. 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 33: 5-21. (Pubitemid 38860216)
108. Voogd J, Wylie DR. 2004. Functional and anatomical organization of floccular zones: a preserved feature in vertebrates. J Comp Neurol 470: 107-112. (Pubitemid 38160686)
109. Voogd J, Gerrits NM, Ruigrok TJ. 1996a. Organization of the vestibulocerebellum. Ann NY Acad Sci 781: 553-579.
110. Voogd J, Jaarsma D, Marani E. 1996b. The cerebellum: ehemoarchitecture and anatomy. In: Swanson LW, Björklund A, Hökfelt T, editors. Integrated systems of the CNS, Part III: Cerebellum, basal ganglia, olfactory system. Handbook of chemical neuroanatomy. Amsterdam: Elsevier Science. 12: 1-369.
111. VoogdJ,PardoeJ,RuigrokTJ,AppsR.2003. Thedistributionofclimbingandmossyfibercollateralbranchesfromthecopulapyramidis andtheparamedianlobule: congruenceofclimbingfibercorticalzonesandthepatternofzebrinstripingwithintherat cerebellum.JNeurosci23:4645-4656.(Pubitemid36706193)
112. Walther E, Dichgans M, Maricich SM, Romito RR, Yang F, Dziennis S, Zackson S, Hawkes R, Herrup K. 1998. Genomic sequences of aldolase C (zebrin II) direct lacZ expression exclusively in non-neuronal cells of transgenic mice. Proc Natl Acad Sci U S A 95: 2615-2620. (Pubitemid 28145991)
113. WassefM,JoynerAL.1997.Earlymesencephalic/ metencephalicpatterninganddevelopmentofthecerebellum.PerspectDevNeurobiol5:3-16. (Pubitemid28140959)
114. WassefM,SoteloC,ThomassetM,GranholmAC,LedereN,RafrafiJ,HawkesR.1990. ExpressionofcompartmentationantigenzebrinIincerebellartransplants. JCompNeurol294:223-234.(Pubitemid20101599)
115. Winship IR, Wylie DR. 2003. Zonal organization of the vestibulocerebellum in pigeons (Columba livia): I. Climbing fiber input to the flocculus. J Comp Neurol 456: 127-139.
116. Whitlock DG. 1952. A neurohistological and neurophysiological study of afferent fiber tracts and receptive areas of the avian cerebellum. J Comp Neurol 97: 567-635.
117. Wold JE. 1981. The vestibular nuclei in the domestic hen (Gallus domesticus): VI. Afferents from the cerebellum. J Comp Neurol 20: 319-341.
118. Wylie DR. 2001. Projections from the nucleus of the basal optic root and nucleus lentiformis mesencephali to the inferior olive in pigeons (Columba livia). J Comp Neurol 429: 502-513. (Pubitemid 32010053)
119. Wylie DR, Frost BJ. 1999. Complex spike activity of Purkinje cells in the ventral uvula and nodulus of pigeons in response to translational optic flow. J Neurophysiol 81: 256-266.
120. Wylie DR, Linkenhoker B. 1996. Mossy fibres from the nucleus of the basal optic root project to the vesibular and cerebellar nuclei in pigeons. Neurosci Lett 219: 83-86. (Pubitemid 26396320)
121. Wylie DR, Lau KL, Lu X, Glover RG, Valsangkar-Smyth M. 1999. Projections of Purkinje cells in the translation and rotation zones of the vestibulocerebellum in pigeon (Columba livia). J Comp Neurol 413: 480-493. (Pubitemid 29445032)
122. Wylie DR, Brown MR, Barkley RR, Winship IR, Crowder NA, Todd KG. 2003a. Zonal organization of the vestibulocerebellum in pigeons (Columba livia): II. Projections of the rotation zones of the flocculus. J Comp Neurol 456: 140-153.
123. Wylie DR, Brown MR, Winship IR, Crowder NA, Todd KG. 2003b. Zonal organization of the vestibulocerebellum in pigeons (Columba livia): III. Projections of the translation zones of the ventral uvula and nodulus. J Comp Neurol 465: 179-194.