Cerebellar regulation mechanisms learned from studies on GluRδ2

Molecular Neurobiology

Volumn 33, Issue 1, 2006, Pages 1-15

  Hirano, Tomoo ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Cerebellum; Glutamate receptor; Learning; Memory; Motor control; Purkinje cell; Synapse formation; Synaptic plasticity

Indexed keywords

GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR DELTA2; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; BRAIN FUNCTION; CEREBELLUM; COMPARATIVE STUDY; GENE EXPRESSION; LEARNING; LONG TERM DEPRESSION; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SYNAPTIC TRANSMISSION;

EID: 29844454269     PISSN: 08937648     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1440-1789.2006.00647.x     Document Type: Review

References (121)

1. Hollmann M. and Heinemann S. (1994) Cloned glutamate receptors. Annu. Rev. Neurosci. 17, 31-108.
2. Conn P. J. and Pin J. P. (1997) Pharmacology and functions of metabotropic glutamate receptors. Annu. Rev. Pharmacol. 37, 205-237.
3. Araki K., Meguro H., Kushiya E., Takayama C., Inoue Y., and Mishina M. (1993) Selective expression of the glutamate receptor channel δ2 subunit in cerebellar Purkinje cells. Biochem. Biophys. Res. Commun. 197, 1267-1276.
4. Lomeli H., Sprengel R., Laurie D. J., et al. (1993) The rat delta-1 and delta-2 subunits extend the excitatory amino acid receptor family. FEBS Lett. 315, 318-322.
5. Rossi F. and Borsello T. (1993) Ectopic Purkinje cells in the adult rat: olivary innervation and different capabilities of migration and development after grafting. J. Comp. Neurol. 337, 70-82.
6. Takayama C., Nakagawa S., Watanabe M., Mishina M., and Inoue Y. (1995) Light- and electron-microscopic localization of the glutamate receptor channel δ2 subunit in the mouse Purkinje cell. Neurosci. Lett. 188, 89-92.
7. Petralia R. S., Sans N., Wang Y. X., et al. (2004) Loss of GluR2 alpha-amino-3-hydroxy- 5-methyl-4-isoxazoleproprionic acid receptor subunit differentially affects remaining synaptic glutamate receptors in cerebellum and cochlear nuclei. Eur. J. Neurosci. 19, 2017-2029.
8. Hirano T., Kasono K., Araki K., Shinozuka K., and Mishina M. (1994) Involvement of the glutamate receptor δ2 subunit in the long-term depression of glutamate responsiveness in cultured rat Purkinje cells. Neurosci. Lett. 182, 172-176.
9. Jeromin A., Huganir R. L., and Linden D. J. (1996) Suppression of the glutamate receptor δ2 subunit produces a specific impairment in cerebellar long-term depression. J. Neurophysiol. 76, 3578-3583.
10. Kashiwabuchi N., Ikeda K., Araki K., et al. (1995) Impairment of motor coordination, Purkinje cell synapse formation, and cerebellar long-term depression in GluR δ2 mutant mice. Cell 81, 245-252.
11. Funabiki K., Mishina M., and Hirano T, (1995) Retarded vestibular compensation in mutant mice deficient in δ2 glutamate receptor subunit. Neuroreport 7, 189-192.
12. Kishimoto Y., Kawahara S., Suzuki M., Mori H., Mishina M., and Kirino Y. (2001) Classical eyeblink conditioning in glutamate receptor subunit δ2 mutant mice is impaired in the delay paradigm but not in the trace paradigm. Eur. J. Neurosci. 13, 1249-1253.
13. Yoshida T., Katoh A., Ohtsuki G., Mishina M., and Hirano T. (2004) Oscillating Purkinje neuron activity causing involuntary eye movement in a mutant mouse deficient in the glutamate receptor δ2 subunit. J. Neurosci. 24, 2440-2448.
14. Ohtsuki G., Kawaguchi S., Mishina M., and Hirano T. (2004) Enhanced inhibitory synaptic transmission in the cerebellar molecular layer of the GluRδ2 knock-out mouse. J. Neurosci. 24, 10,900-10,907.
15. Sacchetti B., Scelfo B., Tempia F., and Starata P. (2004) Long-term synaptic changes induced in the cerebellar cortex by fear conditioning. Neuron 42, 973-982.
16. Yuzaki M. (2003) The δ2 glutamate receptor: 10 years later. Neurosci. Res. 46, 11-22.
17. Yuzaki M. (2004) The δ2 glutamate receptor: a key molecule controlling synaptic plasticity and structure in Purkinje cells. Cerebellum 3, 89-93.
18. Hirai H., Kirsch J., Laube B., Betz H., and Kuhse J. (1996) The glycine binding site of the N-methyl-D-aspartate receptor subunit NR1: identification of novel determinants of co-agonist potentiation in the extracellular M3-M4 loop region. Proc. Natl. Acad. Sci. USA 93, 6031-6036.
19. Laube B., Hirai H., Sturgess M., Betz H., and Kuhse J. (1997) Molecular determinants of agonist discrimination by NMDA receptor subunits: analysis of the glutamate binding site on the NR2B subunit. Neuron 18, 493-503.
20. Armstrong N., Sun Y., Chen G. Q., and Gouaux E. (1998) Structure of a glutamate-receptor ligand-binding core in complex with kainate. Nature 395, 913-917.
21. Mayat E., Petralia R. S., Wang Y. X., and Wenthold R. J. (1995) Immunoprecipitation, immunoblotting, and immunocytochemstry studies suggest that glutamate receptor δ subunits form novel postsynaptic receptor complexes. J. Neurosci. 15, 2533-2546.
22. Burnashev N. (1996) Calcium permeability of glutamate-gated channels in the central nervous system. Curr. Opin. Neurobiol. 6, 311-317.
23. Panchenko V. A., Glasser C. R., Partin K. M., and Mayer M. L. (1999) Amino acid substitutions in the pore of rat glutamate receptors at sites influencing block by polyamines. J. Physiol. 520, 337-357.
24. Zuo J., De Jager, P. L., Takahashi K. A., Jiang W., Linden D. J., and Heintz N. (1997) Neurodegeneration in Lurcher mice caused by mutation in δ2 glutamate receptor gene. Nature 388, 769-773.
25. Kohda K., Wang Y., and Yuzaki M. (2000) Mutation of a glutamate receptor motif reveals its role in gating and δ2 receptor channel properties. Nat. Neurosci. 3, 315-322.
26. Taverna F., Xiong Z. G., Brandes L., Roder J. C., Slater M. W., and MacDonald J. F. (2000) The lurcher mutation of an alpha-amino-3-hydroxy-5- methyl-4-isoxazolepropionic acid receptor subunit enhances potency of glutamate and converts an antagonist to an agonist. J. Biol. Chem. 275, 8475-8479.
27. 2+. J. Neurosci. 20, 5973-5980.
28. 2+ permeability and PKC modification of the GluRδ channels. Neurosci. Res. 41, 193-200.
29. Yue Z., Horton A., Bravin M., Dejager P. L., Selimi F., and Heinz N. (2002) A novel protein complex linking the δ2 glutamate receptor and autophagy: implications for neurodegeneration in lurcher mice. Neuron 35, 921-933.
30. Hirai H. and Matsuda S. (1999) Interaction of the C-terminal domain of δ glutamate receptor with spectrin in the dendritic spines of cultured Purkinje cells. Neurosci. Res. 34, 281-287.
31. Roche K. W., Ly C. D., Petralia R. S., et al. (1999) Postsynaptic density-93 interacts with the δ2 glutamate receptor subunit at parallel fiber synapses. J. Neurosci. 19, 3926-3934.
32. Hironaka K., Umemori H., Tezuka T., Mishina M., and Yamamoto T. (2000) The protein-tyrosine phosphatase PTPMEG interacts with glutamate receptor δ2 and ε subunits. J. Biol. Chem. 275, 16,167-16,173.
33. Miyagi Y., Yamashita T., Fukaya M., et al. (2002). Delphilin: a novel PDZ and forming homology domain-containing protein that synaptically colocalizes and interacts with glutamate receptor δ2 subunit. J. Neurosci. 22, 803-814.
34. Uemura T., Mori H., and Mishina M. (2004) Direct interaction of GluRδ2 with Shank scaffold proteins in cerebellar Purkinje cells. Mol. Cell. Neurosci. 26, 330-341.
35. Yap C. C., Murate M., Kishigami S., et al. (2003) Adaptor protein complex-4 (AP-4) is expressed in the central nervous system neurons and interacts with glutamate receptor δ2. Mol. Cell. Neurosci. 24, 283-295.
36. Ly C. D., Roche K. W., Lee H., and Wenthold R. J. (2002) Identification of rat EMAP, a δ-glutamate receptor binding protein. Biochem. Biophys. Res. Commun. 291, 85-90.
37. Yap C. C., Muto Y., Kishida H., Hashikawa T., and Yano R. (2003) PKC regulates the δ2 glutamate receptor interaction with S-SCAM/ MAGI-2 protein. Biochem. Biophys. Res. Commun. 301, 1122-1128.
38. Hung A. Y. and Sheng M. (2002) PDZ domains: structural modules for protein complex assembly. J. Biol. Chem. 277, 5699-5702.
39. Takayama C., Nakagawa S., Watanabe M., Mishina M., and Inoue Y. (1996) Developmental changes in expression and distribution of the glutamate receptor channel δ2 subunit according to the Purkinje cell maturation. Brain Res. Dev. Brain Res. 92, 147-155.
40. Landsend A. S., Amiry-Moghaddam M., Matsubara A., et al. (1997) Differential localization of δ glutamate receptors in the rat cerebellum: coexpression with AMPA receptors in parallel fiber-spine synapses and absence from climbing fiber synapses. J. Neurosci. 17, 834-842.
41. Zhao H. M., Wenthold R. J., Wang Y. X., and Petralia R.S. (1997) δ-glutamate receptors are differentially distributed at parallel and climbing fiber synapses on Purkinje cells. J. Neurochem. 68, 1041-1052.
42. Matsuda I. and Mishina M. (2000) Identification of a juxtamembrane segment of the glutamate receptor δ2 subunit required for the plasma membrane localization. Biochem. Biophys. Res. Commun. 275, 565-571.
43. Matsuda S., Hannen R., Matsuda K., Yamada N., Tubbs T., and Yuzaki M. (2004) The C-terminal juxtamembrane region of the δ2 glutamate receptor controls its export from the endoplasmic reticulum. Eur. J. Neurosci. 19, 1683-1690.
44. Ito M., Sakurai M., and Tongroach P. (1982) Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells. J. Physiol. 324, 113-134.
45. Sakurai M. (1987) Synaptic modification of parallel fibre-Purkinje cell transmission in in vitro guinea-pig cerebellar slices. J. Physiol. 394, 463-480.
46. Hirano T. (1990) Depression and potentiation of the synaptic transmission between a granule cell and a Purkinje cell in rat cerebellar culture. Neurosci. Lett. 119, 141-144.
47. Ito M. (1989) Long-term depression. Annu. Rev. Neurosci. 12, 85-102.
48. Hansel C., Linden D. J., and D'Angelo E. (2001) Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum. Nat. Neurosci. 4, 467-475.
49. Ito M. (2001) Cerebellar long-term depression: characterization, signal transduction, and functional roles. Physiol. Rev. 81, 1143-1195.
50. Hirano, T. (1990) Effects of postsynaptic depolarization in the induction of synaptic depression between a granule cell and a Purkinje cell in rat cerebellar culture. Neurosci. Lett. 119, 145-147.
51. Linden D. J., Dickinson M. H., Smeyne M., and Connor J. A. (1991) A long-term depression of AMPA currents in cultured cerebellar Purkinje neurons. Neuron 7, 81-89.
52. Linden D. J. (1995) Long-term synaptic depression. Annu. Rev. Neurosci. 18, 319-357.
53. Shigemoto R., Abe T., Nomura S., Nakanishi S., and Hirano T. (1994) Antibodies inactivating mGluR1 metabotropic glutamate receptor block long-term depression in cultured Purkinje cells. Neuron 12, 1245-1255.
54. Matsuda S., Launey T., Mikawa S., and Hirai H. (2000) Disruption of AMPA receptor GluR2 clusters following long-term depression induction in cerebellar Purkinje neurons. EMBO J. 19, 2765-2774.
55. Xia J., Chung H. J., Wihler C., Huganir R. L., and Linden D. J. (2000) Cerebellar long-term depression requires PKC-regulated interactions between GluR2/3 and PDZ domain-containing proteins. Neuron 28, 499-510.
56. Hirano T., Kasono K., Araki K., and Mishina M. (1995) Suppression of LTD in cultured Purkinje cells deficient in the glutamate receptor δ2 subunit. NeuroReport 6, 524-526.
57. Hirai H., Launey T., Mikawa S., et al. (2003) New role of δ2-glutamate receptors in AMPA receptor trafficking and cerebellar function. Nat. Neurosci. 6, 869-876.
58. Hirai, H., Miyazaki T., Kakegawa W., et al. (2005) Rescue of abnormal phentypes of the δ2 glutamate receptor-null mice by mutant δ2 transgenes. EMBO Rep. 6, 90-95.
59. Crepel F. (1998) Nitric oxide and long-term depression in the cerebellum. Trends. Neurosci. 21, 63,64.
60. Feil R., Hartmann J., Luo C., et al. (2003) Impairment of LTD and cerebellar learning by Purkinje cell-specific ablation of cGMP-dependent protein kinase I. J. Cell Biol. 163, 295-302.
61. Kawasaki H., Fujii H., Gotoh Y., et al. (1999) Requirement for mitogen-activated protein kinase in cerebellar long term depression. J. Biol. Chem. 274, 13,498-13,502.
62. Boxall A. R., Lancaster B., and Garthwaite J. (1996) Tyrosine kinase is required for long-term depression in the cerebellum. Neuron 16, 805-813.
63. Launey T., Endo S., Sakai R., Harano J., and Ito M. (2004) Protein phosphatase 2A inhibition induces cerebellar long-term depression and declustering of synaptic AMPA receptor. Proc. Natl. Acad. Sci. USA 13, 676-681.
64. Miyata M., Okada D., Hashimoto K., Kano M., and Ito M. (1999) Corticotropin-releasing factor plays a permissive role in cerebellar long-term depression. Neuron 22, 763-765.
65. Kurihara H., Hashimoto K., Kano M., et al. (1997) Impaired parallel fiber->Purkinje cell synapse stabilization during cerebellar development of mutant mice lacking the glutamate receptor δ2 subunit. J. Neurosci. 17, 9613-9623.
66. Lalouette A., Lohof A., Sotelo C., Guenet J., and Mariani J. (2001) Neurobiological effects of a null mutation depend on genetic context: comparison between two hotfoot alleles of the delta-2 ionotropic glutamate receptor. Neuroscience 105, 443-455.
67. Takeuchi T., Miyazaki T., Watanabe M., Mori H., Sakimura K., and Mishina M. (2005) Control of synaptic connection by glutamate receptor δ2 in the adult cerebellum. J. Neurosci. 25, 2146-2156.
68. Hashimoto K. and Kano M. (2003) Functional differentiation of multiple climbing fiber inputs during synapse elimination in the developing cerebellum. Neuron 38, 785-796.
69. Hashimoto K., Ichikawa R., Takechi H., et al. (2001) Roles of glutamate receptor δ2 subunit (GluRδ2) and metabotropic glutamate receptor subtype 1 (mGluR1) in climbing fiber synapse elimination during postnatal cerebellar development. J. Neurosci. 21, 9701-9712.
70. Ichikawa R., Miyazaki,T., Kano M., et al. (2002) Distal extension of climbing fiber territory and multiple innervation caused by aberrant wiring to adjacent spiny branchlets in cerebellar Purkinje cells lacking glutamate receptor δ2. J. Neurosci. 22, 8487-8503.
71. Kano M., Hashimoto K., Kurihara H., et al. (1997) Persistent multiple climbing fiber innervation of cerebellar Purkinje cells in mice lacking mGluR1. Neuron 18, 71-79.
72. Ichise T., Kano M., Hashimoto K., et al. (2000) mGluR1 in cerebellar Purkinje cells essential for long-term depression, synapse elimination, and motor coordination. Science 288, 1832-1835.
73. Offermans S., Hashimoto K., Watanabe M., et al. (1997) Impaired motor coordination and persistent multiple climbing fiber innervation of cerebellar Purkinje cells in mice lacking Gαq. Proc. Natl. Acad. Sci. USA 94, 14,089-14,094.
74. Kano M., Hashimoto K., Watanabe M., et al. (1998) Phospholipase Cβ4 is specifically involved in climbing fiber synapse elimination in the developing cerebellum. Proc. Natl. Acad. Sci. USA 95, 15,724-15,729.
75. Kano M., Hashimoto K., Chen C., et al. (1995) Impaired synapse elimination during cerebellar development in PKCγ mutant mice. Cell 83, 1223-1231.
76. Morando L., Cesa R., Rasetti R., Harvey R., and Strata P. (2001) Role of glutamate δ2 receptors in activity-dependent competition between heterologous afferent fibers. Proc. Natl. Acad. Sci. USA 98, 9954-9959.
77. Cesa R., Morando L., and Strata P. (2003) Glutamate receptor δ2 subunit in activity-dependent heterologous synaptic competition. J. Neurosci. 23, 2363-2370.
78. 2+-dependent regulation of synaptic δ2 glutamate receptor density in cultured rat Purkinje neurons. Eur. J. Neurosci. 14, 73-82.
79. Kohda K., Kamiya Y., Matsuda S., Kato K., Umemori H., and Yuzaki M. (2003) Heteromer formation of δ2 glutamate receptors with AMPA or kainate receptors. Brain Res. Mol. Brain Res. 110, 27-37.
80. Takai Y., Shimizu K., and Ohtsuka T. (2003) The roles of cadherins and nectins in interneuronal synapse formation. Curr. Opin. Neurobiol. 13, 520-526.
81. Yamagata M., Sanes J. R., and Weiner J. A. (2003) Synaptic adhesion molecules. Curr. Opin. Cell Biol. 15, 621-632.
82. Washbourne P., Dityatev A., Scheiffele P., et al. (2004) Cell adhesion molecules in synapse formation. J. Neurosci. 24, 9244-9249.
83. Clegg D. O., Wingerd K. L., Hikita S. T., and Tolhurst E. C. (2003) Integrins in the development, function and dysfunction of the nervous system. Front. Biosci. 8, 723-750.
84. Huang E. J. and Reichardt L. F. (2003) Trk receptors: roles in neuronal signal transduction. Annu. Rev. Biochem. 72, 609-642.
85. Gaiano N. and Fishell G. (2002) The role of notch in promoting glial and neural stem cell fates. Annu. Rev. Neurosci. 25, 471-490.
86. Hayashi T., Umemori H., Mishina M., and Yamamoto T. (1999) The AMPA receptor interacts with and signals through the protein tyrosine kinase Lyn. Nature 397, 72-76.
87. Passafaro M., Nakagawa T., Sala C., and Sheng M. (2003) Induction of dendritic spines by an extracellular domain of AMPA receptor subunit GluR2. Nature 424, 677-681.
88. Bergersen L., Waerhaug O., Helm J., et al. (2001) A novel postsynaptic density protein: the monocarboxylate transporter MCT2 is colocalized with δ-glutamate receptors in postsynaptic densities of parallel fiber-Purkinje cell synapses. Exp. Brain Res. 136, 523-534.
89. Robinson D. A. (1981) Control of eye movement. In: Brooks V., ed., Handbook of Physiology, Sect. 1, Bethesda, MD: Williams and Wilkins, pp. 1275-1320..
90. Raymond J. L., Lisberger S. G., and Mauk M. D. (1996) The cerebellum: a neuronal learning machine? Science 272, 1126-1131.
91. Llinas R. and Volkind R. A. (1973) The olivocerebellar system: functional properties as revealed by harmaline-induced tremor. Exp. Brain Res. 18, 69-87.
92. Llinas R. and Yarom Y. (1986) Oscillatory properties of guinea-pig inferior olivary neurones and their pharmacological modulation: an in vitro study. J. Physiol. 376, 163-182.
93. Katoh A., Yoshida T., Himeshima Y., Mishina M., and Hirano T. (2005) Defective control and adaptation of reflex eye movements in mutant mice deficient in either the glutamate receptor δ2 subunit or Purkinje cells. Eur. J. Neurosci. 21, 1315-1326.
94. Darlington C. L., Dutia M. B., and Smith P. F. (2002) The contribution of the intrinsic excitability of vestibular nucleus neurons to recovery from vestibular damage. Eur. J. Neurosci. 15, 1719-1727.
95. Murai N., Tsuji J., Ito J., Mishina M., and Hirano T. (2004) Vestibular compensation in glutamate receptor δ-2 subunit knockout mice: dynamic property of vestibulo-ocular reflex. Eur. Arch. Otorhinolaryngol. 261, 82-86.
96. Kitahara T., Takeda N., Uno A., Kubo T., Mishina M., and Kiyama H. (1998) Unilateral labyrinthectomy downregulates glutamate receptor δ-2 expression in the rat vestibulocerebellum. Mol. Brain Res. 61, 170-178.
97. Thompson R. F. (2005) In search of memory traces. Annu. Rev. Psychol. 56, 1-23.
98. Takatsuki K., Kawahara S., Kotani S., et al. (2003) The hippocampus plays an important role in eyeblink conditioning with a short trace interval in glutamate receptor subunit δ2 mutant mice. J. Neurosci. 23, 17-22.
99. Ito M. (1982) Cerebellar control of the vestibulo-ocular reflex - around the flocculus hypothesis. Annu. Rev. Neurosci. 5, 275-296.
100. du Lac S., Raymond J. L., Sejnowski T. J., and Lisberger S. G. (1995) Learning and memory in the vestibulo-ocular reflex. Annu. Rev. Neurosci, 18, 409-441.
101. Boyden E. S., Katoh A., and Raymond J. L. (2004) Cerebellum-dependent learning: the role of multiple plasticity mechanisms. Annu. Rev. Neurosci. 27, 581-609.
102. Katoh A., Kitazawa H., Itohara S., and Nagao S. (2000) Inhibition of nitric oxide synthesis and gene knockout of neuronal nitric oxide synthase impaired adaptation of mouse optokinetic response eye movements. Learn. Mem. 7, 220-226.
103. Kano M., Rexhausen U., Dreessen J., and Konnerth A. (1992) Synaptic excitation produces a long-lasting rebound potentiation of inhibitory synaptic signals in cerebellar Purkinje cells. Nature 356, 601-604.
104. B receptors in a Purkinje neuron. Neuron 27, 339-347.
105. Lalouette A., Guenet J. L., and Vriz S. (1998) Hotfoot mouse mutations affect the δ2 glutamate receptor gene and are allelic to lurcher. Genomics 15, 9-13.
106. Wang Y., Matsuda S., Drews V., Torashima T., Meisler M. H., and Yuzaki M. (2003) A hot spot for hotfoot mutations in the gene encoding the δ2 glutamate receptor. Eur. J. Neurosci. 17, 1581-1590.
107. Matsuda S. and Yuzaki M. (2002) Mutation in hotfoot-4J mice results in retention of δ2 glutamate receptors in ER. Eur. J. Neurosci. 16, 1507-1516.
108. Aiba A., Kano M., Chen C., et al. (1994) Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell 7, 377-388.
109. Conquet F., Bashir Z. I., Davies C. H., et al. (1994) Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1. Nature 372, 237-243.
110. Hashimoto K., Watanabe M., Kurihara H., et al. (2000) Climbing fiber synapse elimination during postnatal cerebellar development requires signal transduction involving Gαq and phospholipase Cβ4. Prog. Brain Res. 124, 31-48.
111. Hartmann J., Blum R., Kovalchuk Y., et al. (2004) Distinct roles of Gαq and Gα11 for Purkinje cell signaling and motor behavior. J. Neurosci. 24, 5119-5130.
112. Miyata M., Kim H., Hashimoto K., et al. (2001) Deficient long-term synaptic depression in the rostral cerebellum correlated with impaired motor learning in phospholipase Cβ4 mutant mice. Eur. J. Neurosci. 13, 1945-1954.
113. Inoue T., Kato K., Kohda K., and Mikoshiba K. (1998) Type 1 inositol 1,4,5-trisphosphate receptor is required for long-term depression in cerebellar Purkinje neurons. J. Neurosci. 18, 5366-5373.
114. Matsumoto M. and Nagata E. (1999) Type 1 inositol 1,4,5-trisphosphate receptor knock-out mice: their phenotypes and their meaning in neuroscience and clinical practice. J. Mol. Med. 77, 406-411.
115. Lev-Ram V., Nebyelul Z., Ellisman M. H., Huang P. L., and Tsien R. Y. (1997) Absence of cerebellar long-term depression in mice lacking neuronal nitric oxide synthase. Learn. Mem. 4, 169-177.
116. Feil R., Hartmann J., Luo C., et al. (2003) Impairment of LTD and cerebellar learning by Purkinje-cell specific ablation of cGMP-dependent protein kinase I. J. Cell Biol. 163, 295-302.
117. Shibuki K., Gomi H., Chen L., et al. (1996) Deficient cerebellar long-term depression, impaired eyeblink conditioning, and normal motor coordination in GFAP mutant mice. Neuron 16, 587-599.
118. De Zeeuw C. I., Hansel C., Bian F., et al. (1998) Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar LTD and adaptation of the vestibulo-ocular reflex. Neuron 20, 495-508.
119. van Alphen A. M. and De Zeeuw C. I. (2002) Cerebellar LTD facilitates but is not essential for long-term adaptation of the vestibulo-ocular reflex. Eur. J. Neurosci. 16, 486-490.
120. Hu W., Zuo J., De Jager P. L., and Heintz N. (1998) The human glutamate receptor δ2 gene (GRID2) maps to chromosome 4q22. Genomics 47, 143-145.
121. Mikami Y., Yoshida T., Matsuda N., and Mishina M. (2004) Expression of zebrafish glutamate receptor δ2 in neurons with cerebellum-like wiring. Biochem. Biophys. Res. Commun. 322, 168-176.