Calbindin in cerebellar Purkinje cells is a critical determinant of the precision of motor coordination

Journal of Neuroscience

Volumn 23, Issue 8, 2003, Pages 3469-3477

  Barski, Jaroslaw J ^a,b   Hartmann, Jana ^c   Rose, Christine R ^c   Hoebeek, Freek ^d   Mörl, Karin ^a   Noll Hussong, Michael ^c   De Zeeuw, Chris I ^d   Konnerth, Arthur ^c   Meyer, Michael ^a,b  

^a MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF MUNICH   (Germany)

^d ERASMUS UNIVERSITY ROTTERDAM   (Netherlands)

Author keywords

Calbindin D 28k; Conditional null mutant; Long term depression; Motor coordination; Purkinje cell; Synaptically evoked calcium transients

Indexed keywords

CALBINDIN; CALCIUM ION; GLUTAMATE RECEPTOR; INOSITOL TRISPHOSPHATE; METABOTROPIC RECEPTOR;

AMPLITUDE MODULATION; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN FUNCTION; CALCIUM TRANSPORT; CEREBELLUM; CONTROLLED STUDY; DENDRITE; DEPRESSION; DISEASE SEVERITY; GENE MUTATION; MOTOR CONTROL; MOTOR COORDINATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; SENSORY DYSFUNCTION; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TIME;

EID: 0038333642     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-08-03469.2003     Document Type: Article

References (48)

1. Aiba A, Kano M, Chen C, Stanton ME, Fox GD, Herrup K, Zwingman TA, Tonegawa S (1994) Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell 79:377-388.
2. Airaksinen MS, Eilers J, Garaschuk O, Thoenen H, Konnerth A, Meyer M (1997) Ataxia and altered dendritic calcium signaling in mice carrying a targeted null mutation of the calbindin D28k gene. Proc Natl Acad Sci USA 94:1488-1493.
3. Barski JJ, Dethleffsen K, Meyer M (2000) Cre recombinase expression in cerebellar Purkinje cells. Genesis 28:93-98.
4. Barski JJ, Morl K, Meyer M (2002) Conditional inactivation of the calbindin D-28k (Calb1) gene by Cre/loxP-mediated recombination. Genesis 32:165-168.
5. Caillard O, Moreno H, Schwaller B, Llano I, Celio MR, Marty A (2000) Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity. Proc Natl Acad Sci USA 97:13372-13377.
6. Callewaert G, Eilers J, Konnerth A (1996) Axonal calcium entry during fast 'sodium' action potentials in rat cerebellar Purkinje neurones. J Physiol (Lond) 495:641-647.
7. Celio MR (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35:375-475.
8. Chard PS, Jordan J, Marcuccilli CJ, Miller RJ, Leiden JM, Roos RP, Ghadge GD (1995) Regulation of excitatory transmission at hippocampal synapses by calbindin D28k. Proc Natl Acad Sci USA 92:5144-5148.
9. Conquet F, Bashir ZI, Davies CH, Daniel H, Ferraguti F, Bordi F, Franz-Bacon K, Reggiani A, Matarese V, Conde F (1994) Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1. Nature 372:237-243.
10. Daniel H, Levenes C, Crepel F (1998) Cellular mechanisms of cerebellar LTD. Trends Neurosci 21:401-407.
11. De Zeeuw CI, van Alphen AM, Koekkoek SK, Buharin E, Coesmans MP, Morpurgo MM, van den BJ (1998a) Recording eye movements in mice: a new approach to investigate the molecular basis of cerebellar control of motor learning and motor timing. Otolaryngol Head Neck Surg 119:193-203.
12. De Zeeuw CI, Hansel C, Bian F, Koekkoek SK, van Alphen AM, Linden DJ, Oberdick J (1998b) Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar LTD and adaptation of the vestibulo-ocular reflex. Neuron 20:495-508.
13. 2+ signalling in fine dendrites and spines of cerebellar Purkinje neurons. Nature 373:155-158.
14. Fierro L, Llano I (1996) High endogenous calcium buffering in Purkinje cells from rat cerebellar slices. J Physiol (Lond) 496:617-625.
15. Finch EA, Augustine GJ (1998) Local calcium signalling by inositol-1,4,5-trisphosphate in Purkinje cell dendrites. Nature 396:753-756.
16. Goossens J, Daniel H, Rancillac A, van der SJ, Oberdick J, Crepel F, De Zeeuw CI, Frens MA (2001) Expression of protein kinase C inhibitor blocks cerebellar long-term depression without affecting Purkinje cell excitability in alert mice. J Neurosci 21:5813-5823.
17. Gorcs TJ, Penke B, Boti Z, Katarova Z, Hamori J (1993) Immunohistochemical visualization of a metabotropic glutamate receptor. NeuroReport 4:283-286.
18. Ichise T, Kano M, Hashimoto K, Yanagihara D, Nakao K, Shigemoto R, Katsuki M, Aiba A (2000) mGluR1 in cerebellar Purkinje cells essential for long-term depression, synapse elimination, and motor coordination. Science 288:1832-1835.
19. Inoue T, Kato K, Kohda K, Mikoshiba K (1998) Type 1 inositol 1,4,5-trisphosphate receptor is required for induction of long-term depression in cerebellar Purkinje neurons. J Neurosci 18:5366-5373.
20. Ito M (1986) Long-term depression as a memory process in the cerebellum. Neurosci Res 3:531-539.
21. Ito M (2001) Cerebellar long-term depression: characterization, signal transduction, and functional roles. Physiol Rev 81:1143-1195.
22. Kano M, Hashimoto K, Watanabe M, Kurihara H, Offermanns S, Jiang H, Wu Y, Jun K, Shin HS, Inoue Y, Simon MI, Wu D (1998) Phospholipase cbeta4 is specifically involved in climbing fiber synapse elimination in the developing cerebellum. Proc Natl Acad Sci USA 95:15724-15729.
23. Kashiwabuchi N, Ikeda K, Araki K, Hirano T, Shibuki K, Takayama C, Inoue Y, Kutsuwada T, Yagi T, Kang Y (1995) Impairment of motor coordination, Purkinje cell synapse formation, and cerebellar long-term depression in GluR delta 2 mutant mice. Cell 81:245-252.
24. Klapstein GJ, Vietla S, Lieberman DN, Gray PA, Airaksinen MS, Thoenen H, Meyer M, Mody I (1998) Calbindin-D28k fails to protect hippocampal neurons against ischemia in spite of its cytoplasmic calcium buffering properties: evidence from calbindin-D28k knockout mice. Neuroscience 85:361-373.
25. Koekkoek SK, Alphen AM, vd BJ, Grosveld F, Galjart N, De Zeeuw CI (1997) Gain adaptation and phase dynamics of compensatory eye movements in mice. Genes Funct 1:175-190.
26. Konnerth A, Llano I, Armstrong CM (1990) Synaptic currents in cerebellar Purkinje cells. Proc Natl Acad Sci USA 87:2662-2665.
27. Konnerth A, Dreessen J, Augustine GJ (1992) Brief dendritic calcium signals initiate long-lasting synaptic depression in cerebellar Purkinje cells. Proc Natl Acad Sci USA 89:7051-7055.
28. Lev-Ram V, Wong ST, Storm DR, Tsien RY (2002) A new form of cerebellar long-term potentiation is postsynaptic and depends on nitric oxide but not cAMP. Proc Natl Acad Sci USA 99:8389-8393.
29. Llinas R, Sugimori M (1980a) Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol (Lond) 305:171-195.
30. Llinas R, Sugimori M (1980b) Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol (Lond) 305:197-213.
31. 2+ buffering in Purkinje neurons. Neuron 24:989-1002.
32. Martin LJ, Blackstone CD, Huganir RL, Price DL (1992) Cellular localization of a metabotropic glutamate receptor in rat brain. Neuron 9:259-270.
33. Matsumoto M, Nakagawa T, Inoue T, Nagata E, Tanaka K, Takano H, Minowa O, Kuno I, Sakakibara S, Yamada M, Yoneshima H, Miyawaki A, Fukuuchi Y, Furuichi T, Okano H, Mikoshiba K, Noda T (1996) Ataxia and epileptic seizures in mice lacking type 1 inositol 1,4,5-trisphosphate receptor. Nature 379:168-171.
34. Mikoshiba K, Furuichi T, Miyawaki A (1994) Structure and function of IP3 receptors. Semin Cell Biol 5:273-281.
35. Miyata M, Finch EA, Khiroug L, Hashimoto K, Hayasaka S, Oda SI, Inouye M, Takagishi Y, Augustine GJ, Kano M (2000) Local calcium release in dendritic spines required for long-term synaptic depression. Neuron 28:233-244.
36. Mushiake H, Strick PL (1993) Preferential activity of dentate neurons during limb movements guided by vision. J Neurophysiol 70:2660-2664.
37. Offermanns S, Hashimoto K, Watanabe M, Sun W, Kurihara H, Thompson RF, Inoue Y, Kano M, Simon MI (1997) Impaired motor coordination and persistent multiple climbing fiber innervation of cerebellar Purkinje cells in mice lacking Gaq. Proc Natl Acad Sci USA 94:14089-14094.
38. Passingham RE, Myers C, Rawlins N, Lightfoot V, Fearn S (1988) Premotor cortex in the rat. Behav Neurosci 102:101-109.
39. Pochet R, Pasteels B, Seto-Ohshima A, Bastianelli E, Kitajima S, Van Eldik LJ (1991) Calmodulin and calbindin localization in retina from six vertebrate species. J Comp Neurol 314:750-762.
40. Roberts WM (1993) Spatial calcium buffering in saccular hair cells. Nature 363:74-76.
41. Rose CR, Konnerth A (2001) Stores not just for storage. Intracellular calcium release and synaptic plasticity. Neuron 31:519-522.
42. Ryo Y, Miyawaki A, Furuichi T, Mikoshiba K (1993) Expression of the metabotropic glutamate receptor mGluR1 alpha and the ionotropic glutamate receptor GluR1 in the brain during the postnatal development of normal mouse and in the cerebellum from mutant mice. J Neurosci Res 36:19-32.
43. Sakurai M (1990) Calcium is an intracellular mediator of the climbing fiber in induction of cerebellar long-term depression. Proc Natl Acad Sci USA 87:3383-3385.
44. Scotti AL (1995) Calbindin D28k in the olivocerebellar projection. A light and electron microscopic study. J Anat 187:649-659.
45. Takechi H, Eilers J, Konnerth A (1998) A new class of synaptic response involving calcium release in dendritic spines, Nature 396:757-760.
46. van Alphen AM, De Zeeuw CI (2002) Cerebellar LTD facilitates but is not essential for long-term adaptation of the vestibulo-ocular reflex. Eur J Neurosci 16:486-490.
47. Wagner J, Keizer J (1994) Effects of rapid buffers on Ca2+ diffusion and Ca2+ oscillations. Biophys J 67:447-456.
48. Wang SS, Denk W, Hausser M (2000) Coincidence detection in single dendritic spines mediated by calcium release. Nat Neurosci 3:1266-1273.