Heterogeneity of parvalbumin expression in the avian cerebellar cortex and comparisons with zebrin II

Neuroscience

Volumn 185, Issue , 2011, Pages 73-84

  Wylie, D R ^a   Gutierrez Ibanez, C ^a   Graham, D J ^a   Kreuzer, M B ^a   Pakan, J M P ^a   Iwaniuk, A N ^b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF LETHBRIDGE   (Canada)

Author keywords

Aldolase c; Calcium binding proteins; Cerebellum; Parvalbumin; Purkinje cells; Zebrin

Indexed keywords

CELL PROTEIN; PARVALBUMIN; UNCLASSIFIED DRUG; ZEBRIN II;

ANIMAL TISSUE; ARTICLE; CEREBELLUM CORTEX; CONTROLLED STUDY; FINCH; FOWL; HUMMINGBIRD; IMMUNOREACTIVITY; NERVE CELL PLASTICITY; NONHUMAN; PIGEON; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PURKINJE CELL; SPECIES DIFFERENCE;

ANIMALS; CEREBELLAR CORTEX; COLUMBIDAE; NERVE TISSUE PROTEINS; PARVALBUMINS; SONGBIRDS; SPECIES SPECIFICITY;

EID: 79956281976     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.04.014     Document Type: Article

References (95)

1. Ahn A.H., Dziennis S., Hawkes R., Herrup K. The cloning of zebrin II reveals its identity with aldolase C. Development 1994, 120:2081-2090.
2. Andersson G., Oscarsson O. Climbing fiber microzones in cerebellar vermis and their projection to different groups of cells in the lateral vestibular nucleus. Exp Brain Res 1978, 32:565-579.
3. Apps R., Garwicz M. Anatomical and physiological foundations of cerebellar information processing. Nat Rev Neurosci 2005, 6:297-311.
4. Akintunde A., Eisenman L.M. External cuneocerebellar projection and Purkinje cell zebrin II bands: a direct comparison of parasagittal banding in the mouse cerebellum. J Chem Neuroanat 1994, 7:75-86.
5. Apps R., Hawkes R. Cerebellar cortical organization: a one-map hypothesis. Nat Rev Neurosci 2009, 10:670-681.
6. Armstrong C.L., Hawkes R. Pattern formation in the cerebellar cortex. Biochem Cell Biol 2000, 78:551-562.
7. Armstrong C.L., Krueger-Naug A.M., Currie R.W., Hawkes R. Constitutive expression of the 25-kDa heat shock protein Hsp25 reveals novel parasagittal bands of Purkinje cells in the adult mouse cerebellar cortex. J Comp Neurol 2000, 416:383-397.
8. Baimbridge K.G., Celio M.R., Rogers J.H. Calcium-binding proteins in the nervous system. Trends Neurosci 1992, 15:303-308.
9. Barmack N.H., Yakhnitsa V. Topsy turvy: functions of climbing and mossy fibers in the vestibulo-cerebellum. Neuroscientist 2011, 17:221-236.
10. Barmack N.H., Yakhnitsa V. Distribution of granule cells projecting to focal Purkinje cells in mouse uvula-nodulus. Neuroscience 2008, 156:216-221.
11. Barmack N.H., Yakhnitsa V. Cerebellar climbing fibers modulate simple spikes in Purkinje cells. J Neurosci 2003, 23:7904-7916.
12. Bastianelli E. Distribution of calcium-binding proteins in the cerebellum. Cerebellum 2003, 2:242-262.
13. Bishop G.A., Seelandt C.M., King J.S. Cellular localization of corticotropin releasing factor receptors in the adult mouse cerebellum. Neuroscience 2000, 101:1083-1092.
14. Braun K., Schachner M., Scheich M., Claus C.W. Cellular localization of the Ca2+-binding protein parvalbumin in the developing avian cerebellum. Cell Tissue Res 1986, 243:69-78.
15. Brecha N., Karten H.J., Hunt S.P. Projections of the nucleus of the basal optic root in the pigeon: an autoradiographic and horseradish peroxidase study. J Comp Neurol 1980, 189:615-670.
16. 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, 291:538-552.
17. Celio M.R. Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 1990, 35:375-475.
18. Chan-Palay V., Nilaver G., Palay S.L., Beinfeld M.C., Zimmerman E.A., Wu J.Y., O'Donohue T.L. Chemical heterogeneity in cerebellar Purkinje cells: existence and coexistence of glutamic acid decarboxylase-like and motilin-like immunoreactivities. Proc Natl Acad Sci 1981, 78:7787-7791.
19. Chockkan V., Hawkes R. Functional and antigenic maps in the rat cerebellum: zebrin compartmentation and vibrissal receptive fields in lobule IXa. J Comp Neurol 1994, 345:33-45.
20. Clarke P.G. Some visual and other connections to the cerebellum of the pigeon. J Comp Neurol 1977, 174:535-552.
21. Crowder N.A., Winship I.R., Wylie D.R. Topographic organization of inferior olive cells projecting to translational zones in the vestibulocerebellum of pigeons. J Comp Neurol 2000, 419:87-95.
22. Cummings S.L. Distribution of corticotropin-releasing factor in the cerebellum and precerebellar nuclei of the cat. J Comp Neurol 1989, 289:657-675.
23. Cummings S.L., Young W.S., Bishop G.A., De Souza E.B., King J.S. Distribution of corticotropin-releasing factor in the cerebellum and precerebellar nuclei of the opossum: a study utilizing immunohistochemistry, in situ hybridization histochemistry, and receptor autoradiography. J Comp Neurol 1989, 280:501-521.
24. Dehnes Y., Chaudhry F.A., Ullensvang K., Lehre K.P., Storm-Mathisen J., Danbolt N.C. The glutamate transporter EAAT4 in rat cerebellar Purkinje cells: a glutamate-gated chloride channel concentrated near the synapse in parts of the dendritic membrane facing astroglia. J Neurosci 1998, 18:3606-3619.
25. Eisenman L.M., Hawkes R. Antigenic compartmentation in the mouse cerebellar cortex: zebrin and HNK-1 reveal a complex, overlapping molecular topography. J Comp Neurol 1993, 335:586-605.
26. Fortin M., Marchand R., Parent A. Calcium-binding proteins in primate cerebellum. Neurosci Res 1998, 30:155-168.
27. Fujita H., Oh-Nishi A., Obayashi S., Sugihara I. Organization of the marmoset cerebellum in three-dimensional space: lobulation, aldolase C compartmentalization and axonal projection. J Comp Neurol 2010, 518:1764-1791.
28. Graf W., Simpson J.I., Leonard C.S. Spatial organization of visual messages of the rabbit's cerebellar flocculus. II. Complex and simple spike responses of Purkinje cells. J Neurophysiol 1988, 60:2091-2121.
29. Hawkes R., Gravel C. The modular cerebellum. Prog Neurobiol 1991, 36:309-327.
30. Hawkes R., Herrup K. Aldolase C/zebrin II and the regionalization of the cerebellum. J Mol Neurosci 1995, 6:147-158.
31. Herrup K., Kuemerle B. The compartmentalization of the cerebellum. Annu Rev Neurosci 1997, 20:61-90.
32. Iwaniuk A.N., Hurd P.L., Wylie D.R.W. Comparative morphology of the avian cerebellum: I. Degree of foliation. Brain Behav Evol 2006, 68:45-62.
33. Iwaniuk A.N., Hurd P.I., Wylie D.R. The comparative morphology of the cerebellum in caprimulgiform birds: evolutionary and functional implications. Brain Behav Evol 2006, 67:53-68.
34. Iwaniuk A.N., Hurd P.L., Wylie D.R. Comparative morphology of the avian cerebellum: II. Relative size of folia. Brain Behav Evol 2007, 69:196-219.
35. Iwaniuk A.N., Lefevbre L., Wylie D.R. The comparative approach and brain-behaviour relationships: a tool for understanding tool use. Can J Exp Psych 2009, 63:150-159.
36. Iwaniuk A.N., Marzban H., Pakan J.M.P., Watanabe M., Hawkes R., Wylie D.R.W. Compartmentation of the cerebellar cortex of hummingbirds (Aves: Trochilidae) revealed by the expression of zebrin II and phospholipase Câ4. J Chem Neuroanat 2009, 37:55-63.
37. Jaarsma D., Levey A.I., Frostholm A., Rotter A., Voogd J. Light-microscopic distribution and parasagittal organisation of muscarinic receptors in rabbit cerebellar cortex. J Chem Neuroanat 1995, 9:241-259.
38. King J.S., Madtes P., Bishop G.A., Overbeck T.L. The distribution of corticotropin-releasing factor (CRF), CRF binding sites and CRF1 receptor mRNA in the mouse cerebellum. Prog Brain Res 1997, 114:55-66.
39. Kohr G., Lambert C.E., Mody I. Calbindin-D28K (CaBP) levels and calcium currents in acutely dissociated epileptic neurons. Exp Brain Res 1991, 85:543-551.
40. Larsell O. The cerebellum: from myxinoids through birds 1967, The University of Minnesota Press, Minnesota.
41. Lau K.L., Glover R.G., Linkenhoker B., Wylie D.R. Topographical organization of inferior olive cells projecting to translation and rotation zones in the vestibulocerebellum of pigeons. Neuroscience 1998, 85:605-614.
42. Llinas R., Sasaki K. The functional organization of the olivo-cerebellar system as examined by multiple Purkinje cell recordings. Eur J Neurosci 1989, 1:587-602.
43. Marzban H., Chung S.H., Pezhouh M.K., Feirabend H., Watanabe M., Voogd J., Hawkes R. Antigenic compartmentation of the cerebellar cortex in the chicken (Gallus domesticus). J Comp Neurol 2010, 518:2221-2239.
44. Marzban H., Chung S., Watanabe M., Hawkes R. Phospholipase Cbeta4 expression reveals the continuity of cerebellar topography through development. J Comp Neurol 2007, 502:857-871.
45. Marzban H., Sillitoe R.V., Hoy M., Chung S.H., Rafuse V.F., Hawkes R. Abnormal HNK-1 expression in the cerebellum of an N-CAM null mouse. J Neurocytol 2004, 33:117-130.
46. Miles F.A., Lisberger S.G. Plasticity in the vestibulo-ocular reflex: a new hypothesis. Annu Rev Neurosci 1981, 4:273-299.
47. Nagao S., Kwak S., Kanazawa I. EAAT4, a glutamate transporter with properties of a chloride channel, is predominantly localized in Purkinje cell dendrites, and forms parasagittal compartments in rat cerebellum. Neuroscience 1997, 78:929-933.
48. Pakan J.M.P., Graham D.J., Gutiérrez-Ibáñez C., Wylie D.R. Organization of the cerebellum: correlating zebrin immunochemistry with optic flow zones in the pigeon flocculus. Vis Neurosci 2011, 28:163-174.
49. Pakan J.M., Graham D.J., Wylie D.R. Organization of visual mossy fiber projections and zebrin expression in the pigeon vestibulocerebellum. J Comp Neurol 2010, 518:175-198.
50. Pakan J.M., Iwaniuk A.N., Wylie D.R., Hawkes R., Marzban H. Purkinje cell compartmentation as revealed by zebrin II expression in the cerebellar cortex of pigeons (Columba livia). J Comp Neurol 2007, 501:619-630.
51. Pakan J.M., Todd K.G., Nguyen A.P., Winship I.R., Hurd P.L., Jantzie L.L., Wylie D.R. Inferior olivary neurons innervate multiple zones of the flocculus in pigeons (Columba livia). J Comp Neurol 2005, 486:159-168.
52. Pakan J.M., Wylie D.R. Congruence of zebrin II expression and functional zones defined by climbing fiber topography in the flocculus. Neuroscience 2008, 157:57-69.
53. Paukert M., Huang Y.H., Tanaka K., Rothstein J.D., Bergles D.E. Zones of enhanced glutamate release from climbing fibers in the mammalian cerebellum. J Neurosci 2010, 30:7290-7299.
54. Pfeiffer C.P., Britto L.R. Distribution of calcium-binding proteins in the chick visual system. Braz J Med Biol Res 1997, 30:1315-1318.
55. Pritz M.B., Siadati A. Calcium binding protein immunoreactivity in nucleus rotundus in a reptile, Caiman crocodilus. Brain Behav Evol 1999, 53:277-287.
56. Resibois A., Rogers J.H. Calretinin in rat brain: an immunohistochemical study. Neuroscience 1992, 46:101-134.
57. Rogers J.H. Immunoreactivity for calretinin and other calcium-binding proteins in cerebellum. Neuroscience 1989, 31:711-721.
58. Ruigrok T.J. Collateralization of climbing and mossy fibers projecting to the nodulus and flocculus of the rat cerebellum. J Comp Neurol 2003, 466:278-298.
59. Sarna J.R., Marzban H., Watanabe M., Hawkes R. Complementary stripes of phospholipase Cbeta3 and Cbeta4 expression by Purkinje cell subsets in the mouse cerebellum. J Comp Neurol 2006, 496:303-313.
60. Sawada K., Fukui Y., Hawkes R. Spatial distribution of corticotropin-releasing factor immunopositive climbing fibers in the mouse cerebellum: analysis by whole mount immunohistochemistry. Brain Res 2008, 1222:106-117.
61. Sawada K., Sakata-Haga H., Fukui Y. Alternating array of tyrosine hydroxylase and heat shock protein 25 immunopositive Purkinje cell stripes in zebrin II-defined transverse zone of the cerebellum of rolling mouse Nagoya. Brain Res 2010, 1343:46-53.
62. Schwaller B. The continuing disappearance of "pure" Ca2+ buffers. Cell Mol Life Sci 2009, 66:275-300.
63. Schwaller B. Emerging functions of the "Ca2+ buffers" parvalbumin, calbindin D-28k and calretinin in the brain. Handbook of neurochemistry and molecular neurobiology. Neural protein metabolism and function 2007, Vol. 7:197-222. Springer, New York. A. Lajtha, N. Banik (Eds.).
64. Schwaller B., Meyer M., Schiffmann S. 'New' functions for 'old' proteins: the role of the calcium-binding proteins calbindin D-28k, calretinin and parvalbumin, in cerebellar physiology. Studies with knockout mice. Cerebellum 2002, 1:241-258.
65. Servais L., Bearzatto B., Schwaller B., Dumont M., De Saedeleer C., Dan B., Barski J.J., Schiffmann S.N., Cheron G. Mono- and dual-frequency fast cerebellar oscillation in mice lacking parvalbumin and/or calbindin D-28k. Eur J Neurosci 2005, 22:861-870.
66. Sillitoe R.V., Hawkes R. Whole-mount immunohistochemistry: a high throughput screen for patterning defects in the mouse cerebellum. J Histochem Cytochem 2002, 50:235-244.
67. Sillitoe R.V., Marzban H., Larouche M., Zahedi S., Affanni J., Hawkes R. Conservation of the architecture of the anterior lobe vermis of the cerebellum across mammalian species. Prog Brain Res 2005, 148:283-297.
68. Sillitoe R.V., Vogel M.W., Joyner A.L. Engrailed homeobox genes regulate establishment of the cerebellar afferent circuit map. J Neurosci 2010, 30:10015-10024.
69. Simpson J., Graf W., Leonard C. The coordinate system of visual climbing fibres to the flocculus. Progress in oculomotor research 1981, 475-485. Elsevier, Oxford. A.F. Fuchs, K.A. Becker (Eds.).
70. Sotelo C., Wassef M. Cerebellar development: afferent organization and Purkinje cell heterogeneity. Philos Trans R Soc Lond B Biol Sci 1991, 331:307-313.
71. Sugihara I., Ebata S., Shinoda Y. Functional compartmentalization in the flocculus and the ventral dentate and dorsal group y nuclei; an analysis of single olivocerebellar axonal morphology. J Comp Neurol 2004, 470:113-133.
72. Sugihara I., Quy P.N. Identification of aldolase C compartments in the mouse cerebellar cortex by olivocerebellar labeling. J Comp Neurol 2007, 500:1076-1092.
73. Sugihara I., Shinoda Y. Molecular, topographic, and functional organization of the cerebellar nuclei: analysis by three-dimensional mapping of the olivonuclear projection and aldolase C labeling. J Neurosci 2007, 27(36):9696-9710.
74. Thompson R.F., Steinmetz J.E. The role of the cerebellum in classical conditioning of discrete behavioral responses. Neuroscience 2009, 162:732-755.
75. Van Brederode J.F., Mulligan K.A., Hendrickson A.E. Calcium-binding proteins as markers for subpopulations of GABAergic neurons in monkey striate cortex. J Comp Neurol 1990, 298:1-22.
76. van den Dungen H.M., Groenewegen H.J., Tilders F.J., Schoemaker J. Immunoreactive corticotropin releasing factor in adult and developing rat cerebellum: its presence in climbing and mossy fibres. J Chem Neuroanat 1988, 1:339-349.
77. Voogd J., Bigaré F. Topographical distribution of olivary and cortico nuclear fibers in the cerebellum: a review. The inferior olivary nucleus: anatomy and physiology 1980, 207-234. Raven, New York. J. Courville, C. de Montigny, Y. Lamarre (Eds.).
78. Voogd J., Broere G., van Rossum J. The medio-lateral distribution of the spinocerebellar projection in the anterior lobe and the simple lobule in the cat and a comparison with some other afferent fibre systems. Psychiatr Neurol Neurochir 1969, 72:137-151.
79. Voogd J., Glickstein M. The anatomy of the cerebellum. Trends Neurosci 1998, 21:370-375.
80. Voogd J., Ruigrok T.J. 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.
81. Voogd J., Wylie D.R. Functional and anatomical organization of floccular zones: a preserved feature in vertebrates. J Comp Neurol 2004, 470:107-112.
82. Wadiche J.I., Jahr C.E. Patterned expression of Purkinje cell glutamate transporters controls synaptic plasticity. Nat Neurosci 2005, 8:1329-1334.
83. Waespe W., Henn V. Gaze stabilization in the primate. The interaction of the vestibulo-ocular reflex, optokinetic nystagmus, and smooth pursuit. Rev Physiol Biochem Pharmacol 1987, 106:37-125.
84. Winship I.R., Wylie D.R. Zonal organization of the vestibulocerebellum in pigeons (Columba livia): I. Climbing fibre input to the flocculus. J Comp Neurol 2003, 456:127-139.
85. Wu H.S., Sugihara I., Shinoda Y. Projection patterns of single mossy fibers originating from the lateral reticular nucleus in the rat cerebellar cortex and nuclei. J Comp Neurol 1999, 411:97-118.
86. Wylie D.R., Bischof W.F., Frost B.J. Common reference frame for neural coding of translational and rotational optic flow. Nature 1998, 392:278-282.
87. Wylie D.R., Brown M.R., Barkley R.R., Winship I.R., Crowder N.A., Todd K.G. Zonal organization of the vestibulocerebellum in pigeons (Columba livia): II. Projections of the rotation zones of the flocculus. J Comp Neurol 2003, 456:140-153.
88. Wylie D.R., Brown M.R., Winship I.R., Crowder N.A., Todd K.G. Zonal organization of the vestibulocerebellum in pigeons (Columba livia): III. Projections of the translation zones of the ventral uvula and nodulus. J Comp Neurol 2003, 465:179-194.
89. Wylie D.R., Frost B.J. Purkinje cells in the vestibulocerebellum of the pigeon respond best to either translational or rotational wholefield visual motion. Exp Brain Res 1991, 86:229-232.
90. Wylie D.R., Frost B.J. Responses of pigeon vestibulocerebellar neurons to optokinetic stimulation. II. The 3-dimensional reference frame of rotation neurons in the flocculus. J Neurophysiol 1993, 70:2647-2659.
91. Wylie D.R., Frost B.J. Complex spike activity of Purkinje cells in the ventral uvula and nodulus of pigeons in response to translational optic flow. J Neurophysiol 1999, 81:256-266.
92. Wylie D.R., Kripalani T., Frost B.J. Responses of pigeon vestibulocerebellar neurons to optokinetic stimulation. I. Functional organization of neurons discriminating between translational and rotational visual flow. J Neurophysiol 1993, 70:2632-2646.
93. Wylie D.R., Lau K.L., Lu X., Glover R.G., Valsangkar-Smyth M. Projections of Purkinje cells in the translation and rotation zones of the vestibulocerebellum in pigeon (Columba livia). J Comp Neurol 1999, 413:480-493.
94. Yamaguchi T., Winsky L., Jacobowitz D.M. Calretinin, a neuronal calcium binding protein, inhibits phosphorylation of a 39 kDa synaptic membrane protein from rat brain cerebral cortex. Neurosci Lett 1991, 131:79-82.
95. Zheng N., Raman I.M. Synaptic inhibition, excitation, and plasticity in neurons of the cerebellar nuclei. Cerebellum 2010, 9:56-66.