Antigenic compartmentation of the cerebellar cortex in an Australian marsupial, the tammar wallaby macropus eugenii

Brain, Behavior and Evolution

Volumn 80, Issue 3, 2012, Pages 196-209

  Marzban, Hassan ^a,b   Hoy, Nathan ^a   Marotte, Lauren R ^c   Hawkes, Richard ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

^c AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Immunohistochemistry; Purkinje cell; Stripes; Zebrin II

Indexed keywords

ANTIGEN; NERVE PROTEIN; ZEBRIN II;

ANIMAL; ARTICLE; CEREBELLUM CORTEX; CHEMISTRY; CLASSIFICATION; COMPARATIVE STUDY; FEMALE; HISTOLOGY; IMMUNOLOGY; KANGAROO; MALE; MAMMAL; MORPHOGENESIS; MOUSE; PURKINJE CELL; SPECIES DIFFERENCE;

ANIMALS; ANTIGENS; BODY PATTERNING; CEREBELLAR CORTEX; FEMALE; MACROPODIDAE; MALE; MAMMALS; MICE; NERVE TISSUE PROTEINS; PURKINJE CELLS; SPECIES SPECIFICITY;

AVES; MACROPUS EUGENII; MAMMALIA; METATHERIA;

EID: 84867982457     PISSN: 00068977     EISSN: None     Source Type: Journal    
DOI: 10.1159/000340069     Document Type: Article

References (75)

1. Ahn AH, Dziennis S, Hawkes R, Herrup K (1994): The cloning of zebrin II reveals its identity with aldolase C. Development 120: 2081-2090. (Pubitemid 24232276)
2. Akintunde A, Eisenman LM (1994): External cuneocerebellar projections and Purkinje cell zebrin II bands: a direct comparison of parasagittal banding in the mouse cerebellum. J Chem Neuroanat 7: 75-86. (Pubitemid 24271596)
3. Apps R, Hawkes R (2009): Cerebellar cortical organization: a one-map hypothesis. Nature Rev Neurosci 10: 670-681.
4. Armstrong C, Chung S-H, Armstrong J, Hochgeschwender U, Jeong Y-G, Hawkes R (2009): A novel somatostatin-immunoreactive mossy fiber pathway associated with HSP25-immunoreactive Purkinje cell stripes in the mouse cerebellum. J Comp Neurol 517: 524-538.
5. Armstrong CL, Krueger-Naug AM, Currie WC, Hawkes R (2000): Constitutive expression of the 25 kDa heat shock protein HSP25 reveals novel parasagittal bands of Purkinje in the adult mouse cerebellar cortex. J Comp Neurol 416: 383-397. (Pubitemid 30027135)
6. Armstrong CL, Krueger-Naug AM, Currie WC, Hawkes R (2001): Constitutive expression of heat shock protein HSP25 in the central nervous system of the developing and adult mouse. J Comp Neurol 434: 262-274. (Pubitemid 32402134)
7. Ashwell KWS (2010): Cerebellum, vestibular and precerebellar nuclei; in Ashwell K (ed): The Neurobiology of Australian Marsupials. Cambridge, Cambridge University Press, pp 82-94.
8. Ashwell KW, Paxinos G, Watson CR (2007): Cyto-and chemoarchitecture of the cerebellum of the short-beaked echidna (Tachyglossus aculeatus) . Brain Behav Evol 70: 71-89. (Pubitemid 47236962)
9. Baimbridge KG, Miller JJ, Parkes CO (1982): Calcium-binding protein distribution in the rat brain. Brain Res 239: 519-525. (Pubitemid 12116500)
10. Bishop GA, Ho RH, King JS (1985): Localization of serotonin immunoreactivity in the opossum cerebellum. J Comp Neurol 235: 301-321. (Pubitemid 15041615)
11. Brochu G, Maler L, Hawkes R (1990): Zebrin II: a polypeptide antigen expressed selectively by Purkinje cells reveals compartments in rat and fish cerebellum. J Comp Neurol 291: 538-552. (Pubitemid 20047467)
12. Caffe AR, Von Schantz M, Szel A, Voogd J, Van Veen T (1994): Distribution of Purkinje cellspecific zebrin II/aldolase C immunoreactivity in the mouse, rat, rabbit, and human retina. J Comp Neurol 348: 291-297. (Pubitemid 24293606)
13. Chen G, Hanson CL, Ebner TJ (1996): Functional parasagittal compartments in the rat cerebellar cortex: an in vivo optical imaging study using neutral red. J Neurophysiol 76: 4169-4174. (Pubitemid 27009714)
14. 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)
15. Cummings SL, Young WS, King JS (1994): Early development of cerebellar afferent systems that contain corticotropin-releasing factor. J Comp Neurol 350: 534-549. (Pubitemid 24372033)
16. 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)
17. Dore 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)
18. Eisenman LM, Hawkes R (1993): Antigenic compartmentation in the mouse cerebellar cortex: zebrin and HNK-1 reveal a complex, overlapping molecular topography. J Comp Neurol 335: 586-605. (Pubitemid 23254255)
19. Fujita H, Oh-Nishi A, Obayashi S, Sugihara I (2010): Organization of the marmoset cerebellum in three-dimensional space: lobulation, aldolase C compartmentalization and axonal projection. J Comp Neurol 518: 1764-1791.
20. Furutama D, Morita N, Takano R, Sekine Y, Sadakata T, Shinoda Y, Hayashi K, Mishima Y, Mikoshiba K, Hawkes R, Furuichi T (2010): Expression of the IP3R1 promoter-driven nls-LacZ transgene in Purkinje cell parasagittal arrays of developing mouse cerebellum. J Neurosci Res 88: 2810-2825.
21. Gravel C, Eisenman LE, Sasseville R, Hawkes R (1987): Parasagittal organization of the rat cerebellar cortex: a direct correlation between antigenic Purkinje cell bands revealed by mabQ113 and the organization of the olivocerebellar projection. J Comp Neurol 263:294-310. (Pubitemid 17160251)
22. Hallem JS, Thompson JH, Gundappa-Sulur G, Hawkes R, Bjaalie 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. sNeuroscience 93: 1083-1094. (Pubitemid 29341655)
23. Hassiotis M, Paxinos G, Ashwell KWS (2004): Cyto-and chemoarchitecture of the cerebral cortex of the Australian echidna ( Tachyglossus aculeatus ). I. Areal organisation. J Comp Neurol 475: 493-517. (Pubitemid 38859362)
24. Hawkes R (1997): An anatomical model of cerebellar modules. Prog Brain Res 114: 39-52.
25. Hawkes R, Brochu G, Dore, L, Gravel C, Leclerc N (1992): Zebrins: molecular markers of compartmentation in the cerebellum; in Llinas R, Sotelo C (eds): The Cerebellum Revisited. New York, Springer, pp 22-55.
26. Hawkes R, Gravel C (1991): The modular cerebellum. Prog Neurobiol 36: 309-327.
27. Hazlett JC, Martin GF, Dom R (1971): Spinocerebellar fibers of the opossum Didelphis marsupialis virginiana . Brain Res 33: 257-271.
28. Holst MC (1986): The olivocerebellar projection in a marsupial and a monotreme; thesis, The University of New South Wales.
29. Iwaniuk AN, Hurd PL, Wylie DR (2007): Comparative morphology of the avian cerebellum. II. Size of folia. Brain Behav Evol 69: 196-219. (Pubitemid 46377212)
30. Iwaniuk AN, Marzban H, Pakan JM, Watanabe M, Hawkes R, Wong-Wylie DR (2009): Compartmentation of the cerebellar cortex of hummingbirds (Aves: Trochilidae) revealed by the expression of zebrin II and phospholipase C4. J Chem Neuroanat 37: 55-63.
31. 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)
32. Karlen SJ, Krubitzer L (2007): The functional and anatomical organization of marsupial neocortex: evidence for parallel evolution across mammals. Prog Neurobiol 82: 122-141. (Pubitemid 46829605)
33. 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.
34. Larouche M, Diep C, Sillitoe R, Hawkes R (2003): The topographical anatomy of the cerebellum in the guinea pig, Cavia porcellus . Brain Res 965: 159-169. (Pubitemid 36183698)
35. Larsell O (1970): The Comparative Anatomy and Histology of the Cerebellum from Monotremes through Apes. Minneapolis, University of Minnesota Press, p 269.
36. Linauts M, Martin GF (1978): The organization of olivo-cerebellar projections in the opossum, Didelphis virginiana , as revealed by the retrograde transport of horseradish peroxidase. J Comp Neurol 179: 355-381. (Pubitemid 8373136)
37. Martin GF, Dom R, King JS, Robards M, Watson CRR (1975): The inferior olivary nucleus of the opossum (Didelphis marsupialis virginiana) , its organisation and connections. J Comp Neurol 160: 507-534.
38. Marzban H, Chung S-H, Pezhouh MK, Feirabend H, Watanabe M, Voogd J, Hawkes R (2010): Antigenic compartmentation of the cerebellar cortex in the chicken (Gallus domesticu s ) . J Comp Neurol 518: 2221-2239.
39. Marzban H, Hawkes R (2011): On the architecture of the posterior zone of the cerebellum. Cerebellum 3: 422-34.
40. Marzban H, Hoy N, Aavani T, Sarko DK, Catania KC, Hawkes R (2011): Compartmentation of the cerebellar cortex in the naked mole-rat (Heterocephalus glaber) . Cerebellum 3: 435-48.
41. Marzban H, Kim C-T, Doorn D, Chung S-H, Hawkes R (2008): A novel transverse expression domain in the mouse cerebellum revealed by a neurofilament-associated antigen. Neuroscience 153: 1190-1201.
42. Marzban H, Zahedi S, Sanchez M, Hawkes R (2003): Antigenic compartmentation of the cerebellar cortex in the Syrian hamster Mesocricetus auratus . Brain Res 974: 176-183. (Pubitemid 36549231)
43. Meek J, Hafmans TGM, Maler L, Hawkes R (1992): The distribution of zebrin II in the gigantocerebellum of the mormyrid fish Gnathonemus petersii compared with other teleosts. J Comp Neurol 316: 17-31.
44. Mikkelsen TS, Wakefield MJ, Aken B, et al (2007): Genome of the marsupial Monodelphis domestica reveals innovation in noncoding sequences. Nature 447: 167-177. (Pubitemid 46763085)
45. Murphy WJ, Pevzner PA, O'Brien SJ (2004): Mammalian phylogenomics comes of age. Trends Genet 20: 631-639. (Pubitemid 39441282)
46. 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)
47. 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)
48. Pearce AR, Marotte LR (2003): The first thalamocortical synapses are made in the cortical plate in the developing visual cortex of the wallaby (Macropus eugenii) . J Comp Neurol 461: 205-216. (Pubitemid 36583463)
49. Renfree MB, Holt AB, Green SW, Carr JP, Cheek DB (1982): Ontogeny of the brain in a marsupial (Macropus eugenii) throughout pouch life. I. Brain growth. Brain Behav Evol 20: 57-71. (Pubitemid 13228021)
50. Renfree MB, Papenfuss AT, Deakin JE, et al (2011): Genome sequence of an Australian kangaroo, Macropus eugenii , provides insight into the evolution of mammalian reproduction and development. Genome Biol 12:R81.
51. Riley HA (1929): The mammalian cerebellum. A comparative study of the arbor vitae and folial patterns. Res Publ Assoc Nerv Ment Dis 6: 37-192.
52. 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. (Pubitemid 34121021)
53. Sarna J, Hawkes R (2003): Patterned Purkinje cell death in the cerebellum. Prog Neurobiol 70: 473-507. (Pubitemid 37249428)
54. Sarna JR, Marzban H, Watanabe M, Hawkes R (2006): Complementary bands of phospholipase Cβ3 and Cβ4 expression by Purkinje cell subsets in the mouse cerebellum. J Comp Neurol 496: 303-313.
55. Sarna J, Miranda SRP, Schuchman EH, Hawkes R (2001): Patterned cerebellar Purkinje cell death in a transgenic model of Niemann-Pick type A/B disease. Europ J Neurosci 13: 1873-1880. (Pubitemid 32537213)
56. 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.
57. Sillitoe RV, Hawkes R (2002): Whole-mount immunohistochemistry: a high-throughput screen for patterning defects in the mouse cerebellum. J Histochem Cytochem 50: 235-244. (Pubitemid 34106762)
58. Sillitoe RV, Hulliger M, Dyck R, Hawkes R (2003a): Antigenic compartmentation of the cat cerebellar cortex. Brain Res 977: 1-15. (Pubitemid 36644164)
59. Sillitoe RV, Kunzle 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)
60. Sillitoe RV, Malz CR, Rockland K, Hawkes R (2004): Antigenic compartmentation of the primate and tree shrew cerebellum: a common topography of zebrin II in Macaca mulatta and Tupaia belangeri . J Anat 204: 257-269. (Pubitemid 38515143)
61. 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)
62. Smith GE (1903a): Notes on the morphology of the mammalian cerebellum. J Anat 37: 329-332.
63. Smith GE (1903b): Further observations of the natural mode of subdivision of the mammalian cerebellum. Anat Anzeig 23: 368-384.
64. Sugihara I (2006): Organization and remodeling of the olivocerebellar climbing fiber projection. Cerebellum 5: 15-22. (Pubitemid 44113386)
65. Terman JR, Wang XM, Martin GF (1998): Origin, course, and laterality of spinocerebellar axons in the North American opossum, Didelphis virginiana . Anat Rec 4:528-547. (Pubitemid 28366725)
66. Tyndale-Biscoe H (2005): Life of marsupials. Collingwood, CSIRO Publishing, pp 27.
67. Voogd J (1967): Comparative aspects of the structure and fiber connections of the mammalian cerebellum. Prog Brain Res 25: 94-134.
68. Voogd J (1969): The importance of fiber connections in the comparative anatomy of the mammalian cerebellum; in Llinas R (ed): Neurobiology of Cerebellar Evolution and Development. Chicago: Am Med Assoc, pp 493-514.
69. Voogd J (2004): The human cerebellum. J Chem Neuroanat 4:243-252. (Pubitemid 38077148)
70. Voogd J, Jaarsma D, Marani E (1996): The cerebellum: chemoarchitecture and anatomy; in Swanson LW, Bjorkland A, Hokfelt T (eds): Handbook of Chemical Neuroanatomy, Integrated Systems of the CNS III, ed 12. Amsterdam, Elsevier, pp 1-369.
71. Voogd J, Ruigrok TJH (1997): Transverse and longitudinal patterns in the mammalian cerebellum. Prog Brain Res 114: 21-37.
72. 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 USA 95:2615-2620. (Pubitemid 28145991)
73. Watson CR, Broomhead A, Holst MC (1976): Spinocerebellar tracts in the brush-tailed possum, Trichosurus vulpecula . Brain Behav Evol 13: 142-153.
74. Watson CR, Herron P (1977): The inferior olivary complex of marsupials. J Comp Neurol 176: 527-537. (Pubitemid 8227776)
75. Ziehen T (1897): Das Centralnervensystem der Monotremen und Marsupialier. I. Makroskopische Anatomie. Jena Denkschrift 6: 168-187.