Synapse elimination in the developing cerebellum

Cellular and Molecular Life Sciences

Volumn 70, Issue 24, 2013, Pages 4667-4680

  Hashimoto, Kouichi ^a,b   Kano, Masanobu ^c  

^a HIROSHIMA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

Cerebellum; Climbing fiber; Dendrite; Inferior olive; Parallel fiber; Postnatal development; Purkinje cell; Synapse

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; GLUTAMATE DECARBOXYLASE 67; METABOTROPIC RECEPTOR 1; SOMATOMEDIN C; VESICULAR GLUTAMATE TRANSPORTER 2;

BRAIN DEVELOPMENT; CALCIUM TRANSPORT; CELL EXPANSION; CELL MATURATION; CEREBELLUM; CLIMBING FIBER; GABAERGIC SYSTEM; INNERVATION; MOLECULAR DYNAMICS; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NERVE CONDUCTION; NERVOUS SYSTEM FUNCTION; NONHUMAN; PERINATAL PERIOD; PROTEIN EXPRESSION; PROTEIN FUNCTION; PURKINJE CELL; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE ELIMINATION; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS;

ANIMALS; ANIMALS, NEWBORN; CEREBELLUM; DENDRITES; MICE; MODELS, NEUROLOGICAL; NERVE FIBERS; NEUROGENESIS; PURKINJE CELLS; SYNAPSES;

ANIMALIA;

EID: 84889888396     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-013-1405-2     Document Type: Review

References (123)

1. Hensch TK (2004) Critical period regulation. Annu Rev Neurosci 27:549-579. doi: 10.1146/annurev.neuro.27.070203.144327
2. Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274(5290):1133-1138
3. Lichtman JW, Colman H (2000) Synapse elimination and indelible memory. Neuron 25(2):269-278
4. Luo L, O'Leary DD (2005) Axon retraction and degeneration in development and disease. Annu Rev Neurosci 28:127-156. doi: 10.1146/annurev.neuro.28.061604. 135632
5. Purves D, Lichtman JW (1980) Elimination of synapses in the developing nervous system. Science 210(4466):153-157
6. Eccles JC, Llinas R, Sasaki K (1966) The excitatory synaptic action of climbing fibres on the purinje cells of the cerebellum. J Physiol 182(2):268-296
7. Palay SL, Chan-Palay V (1974) Cerebellar Cortex. Springer, New York
8. Miyakawa H, Lev-Ram V, Lasser-Ross N, Ross WN (1992) Calcium transients evoked by climbing fiber and parallel fiber synaptic inputs in guinea pig cerebellar Purkinje neurons. J Neurophysiol 68(4):1178-1189
9. Crepel F (1982) Regression of functional synapses in the immature mammalian cerebellunm. Trends Neurosci 5:266-269
10. Crepel F, Mariani J, Delhaye-Bouchaud N (1976) Evidence for a multiple innervation of Purkinje cells by climbing fibers in the immature rat cerebellum. J Neurobiol 7(6):567-578
11. Lohof AM, Delhaye-Bouchaud N, Mariani J (1996) Synapse elimination in the central nervous system: functional significance and cellular mechanisms. Rev Neurosci 7(2):85-101
12. Hashimoto K, Kano M (2005) Postnatal development and synapse elimination of climbing fiber to Purkinje cell projection in the cerebellum. Neurosci Res 53(3):221-228 Epub 2005 Sep 2001
13. Hashimoto K, Yoshida T, Sakimura K, Mishina M, Watanabe M, Kano M (2009) Influence of parallel fiber-Purkinje cell synapse formation on postnatal development of climbing fiber-Purkinje cell synapses in the cerebellum. Neuroscience 162(3):601-611 Epub 2008 Dec 2031
14. Kano M, Hashimoto K (2009) Synapse elimination in the central nervous system. Curr Opin Neurobiol 19(2):154-161. doi: 10.1016/j.conb.2009.05.002
15. Kano M, Hashimoto K (2012) Activity-dependent maturation of climbing fiber to Purkinje cell synapses during postnatal cerebellar development. Cerebellum 11(2):449-450. doi: 10.1007/s12311-011-0337-3
16. Watanabe M, Kano M (2011) Climbing fiber synapse elimination in cerebellar Purkinje cells. Eur J Neurosci 34(10):1697-1710. doi: 10.1111/j.1460-9568.2011.07894.x
17. Apps R, Hawkes R (2009) Cerebellar cortical organization: a one-map hypothesis. Nat Rev Neurosci 10(9):670-681. doi: 10.1038/nrn2698
18. 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(4):538-552. doi: 10.1002/cne.902910405
19. Sarna 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(3):303-313. doi: 10.1002/cne.20912
20. Buisseret-Delmas C, Angaut P (1993) The cerebellar olivo-corticonuclear connections in the rat. Prog Neurobiol 40(1):63-87
21. Sugihara I, Quy PN (2007) Identification of aldolase C compartments in the mouse cerebellar cortex by olivocerebellar labeling. J Comp Neurol 500(6):1076-1092. doi: 10.1002/cne.21219
22. 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(40):8771-8785. doi: 10.1523/JNEUROSCI. 1961-04.2004
23. Lang EJ, Sugihara I, Welsh JP, Llinas R (1999) Patterns of spontaneous Purkinje cell complex spike activity in the awake rat. J Neurosci 19(7):2728-2739
24. Llinas R, Sasaki K (1989) The functional organization of the olivo-cerebellar system as examined by multiple Purkinje cell recordings. Eur J Neurosci 1(6):587-602
25. Mukamel EA, Nimmerjahn A, Schnitzer MJ (2009) Automated analysis of cellular signals from large-scale calcium imaging data. Neuron 63(6):747-760. doi: 10.1016/j.neuron.2009.08.009
26. Schultz SR, Kitamura K, Post-Uiterweer A, Krupic J, Hausser M (2009) Spatial pattern coding of sensory information by climbing fiber-evoked calcium signals in networks of neighboring cerebellar Purkinje cells. J Neurosci 29(25):8005-8015. doi: 10.1523/JNEUROSCI.4919-08.2009
27. Sugihara I (2006) Organization and remodeling of the olivocerebellar climbing fiber projection. Cerebellum 5(1):15-22. doi: 10.1080/14734220500527385
28. Sugihara I, Wu HS, Shinoda Y (2001) The entire trajectories of single olivocerebellar axons in the cerebellar cortex and their contribution to Cerebellar compartmentalization. J Neurosci 21(19):7715-7723
29. Morara S, van der Want JJ, de Weerd H, Provini L, Rosina A (2001) Ultrastructural analysis of climbing fiber-Purkinje cell synaptogenesis in the rat cerebellum. Neuroscience 108(4):655-671
30. Wassef M, Chedotal A, Cholley B, Thomasset M, Heizmann CW, Sotelo C (1992) Development of the olivocerebellar projection in the rat: I. Transient biochemical compartmentation of the inferior olive. J Comp Neurol 323(4):519-536. doi: 10.1002/cne.903230405
31. Chedotal A, Sotelo C (1992) Early development of olivocerebellar projections in the fetal rat Using CGRP immunocytochemistry. Eur J Neurosci 4(11):1159-1179
32. Sugihara I (2005) Microzonal projection and climbing fiber remodeling in single olivocerebellar axons of newborn rats at postnatal days 4-7. J Comp Neurol 487(1):93-106. doi: 10.1002/cne.20531
33. Chedotal A, Sotelo C (1993) The 'creeper stage' in cerebellar climbing fiber synaptogenesis precedes the 'pericellular nest'-ultrastructural evidence with parvalbumin immunocytochemistry. Brain Res Dev Brain Res 76(2):207-220
34. Armengol JA, Sotelo C (1991) Early dendritic development of Purkinje cells in the rat cerebellum. A light and electron microscopic study using axonal tracing in 'in vitro' slices. Brain Res Dev Brain Res 64(1-2):95-114
35. Mason CA (1986) Axon development in mouse cerebellum: embryonic axon forms and expression of synapsin I. Neuroscience 19(4):1319-1333
36. West MJ, del Cerro M (1976) Early formation of synapses in the molecular layer of the fetal rat cerebellum. J Comp Neurol 165(2):137-153. doi: 10.1002/cne.901650203
37. Crepel F (1971) Maturation of climbing fiber responses in the rat. Brain Res 35(1):272-276
38. Woodward DJ, Hoffer BJ, Siggins GR, Bloom FE (1971) The ontogenetic development of synaptic junctions, synaptic activation and responsiveness to neurotransmitter substances in rat cerebellar purkinje cells. Brain Res 34(1):73-97
39. Sotelo C (2004) Cellular and genetic regulation of the development of the cerebellar system. Prog Neurobiol 72(5):295-339. doi: 10.1016/j.pneurobio.2004. 03.004
40. Mariani J, Crepel F, Mikoshiba K, Changeux JP, Sotelo C (1977) Anatomical, physiological and biochemical studies of the cerebellum from Reeler mutant mouse. Philos Trans R Soc Lond B 281(978):1-28
41. Crepel F, Mariani J (1976) Multiple innervation of Purkinje cells by climbing fibers in the cerebellum of the Weaver Mutant Mouse. J Neurobiol 7(6):579-582
42. Puro DG, Woodward DJ (1977) The climbing fiber system in the Weaver mutant. Brain Res 129(1):141-146
43. Crepel F, Delhaye-Bouchaud N, Guastavino JM, Sampaio I (1980) Multiple innervation of cerebellar Purkinje cells by climbing fibres in staggerer mutant mouse. Nature 283(5746):483-484
44. Mariani J, Changeux JP (1980) Multiple innervation of Purkinje cells by climbing fibers in the cerebellum of the adult staggerer mutant mouse. J Neurobiol 11(1):41-50
45. Benoit P, Mariani J, Delhaye-Bouchaud N, Chappuis G (1987) Evidence for a multiple innervation of cerebellar Purkinje cells by climbing fibers in adult ferrets infected at birth by a mink enteritis virus. Brain Res 431(1):51-57
46. Crepel F, Delhaye-Bouchaud N, Dupont JL (1981) Fate of the multiple innervation of cerebellar Purkinje cells by climbing fibers in immature control, X-irradiated and hypothyroid rats. Brain Res 227(1):59-71
47. Woodward DJ, Hoffer BJ, Altman J (1974) Physiological and pharmacological properties of Purkinje cells in rat cerebellum degranulated by postnatal x-irradiation. J Neurobiol 5(4):283-304
48. Bosman LW, Takechi H, Hartmann J, Eilers J, Konnerth A (2008) Homosynaptic long-term synaptic potentiation of the "winner" climbing fiber synapse in developing Purkinje cells. J Neurosci 28(4):798-807. doi: 10.1523/JNEUROSCI.4074-07.2008
49. Hashimoto K, Kano M (2003) Functional differentiation of multiple climbing fiber inputs during synapse elimination in the developing cerebellum. Neuron 38(5):785-796
50. Ohtsuki G, Hirano T (2008) Bidirectional plasticity at developing climbing fiber-Purkinje neuron synapses. Eur J Neurosci 28(12):2393-2400. doi: 10.1111/j.1460-9568.2008.06539.x
51. Scelfo B, Strata P (2005) Correlation between multiple climbing fibre regression and parallel fibre response development in the postnatal mouse cerebellum. Eur J Neurosci 21(4):971-978
52. Hashimoto K, Ichikawa R, Kitamura K, Watanabe M, Kano M (2009) Translocation of a "winner" climbing fiber to the Purkinje cell dendrite and subsequent elimination of "losers" from the soma in developing cerebellum. Neuron 63(1):106-118. doi: 10.1016/j.neuron.2009.06.008
53. Wadiche JI, Jahr CE (2001) Multivesicular release at climbing fiber-Purkinje cell synapses. Neuron 32(2):301-313
54. 2+ channel in Purkinje cell mediates synaptic competition and elimination in developing cerebellum. Proc Natl Acad Sci USA 108(24):9987-9992. doi: 10.1073/pnas.1101488108
55. Nakayama H, Miyazaki T, Kitamura K, Hashimoto K, Yanagawa Y, Obata K, Sakimura K, Watanabe M, Kano M (2012) GABAergic inhibition regulates developmental synapse elimination in the cerebellum. Neuron 74(2):384-396. doi: 10.1016/j.neuron.2012.02.032
56. Altman J, Bayer SA (1997) Development of the cerebellar system: in relation to its evolution, structure, and functions. CRC, Boca Raton
57. Ramon Y, Cajal S (1911) Histologie du systeme nerveux de l'homme et des vertebres. vol II. Maloine, Paris
58. Mason CA, Christakos S, Catalano SM (1990) Early climbing fiber interactions with Purkinje cells in the postnatal mouse cerebellum. J Comp Neurol 297(1):77-90
59. Ichikawa R, Yamasaki M, Miyazaki T, Konno K, Hashimoto K, Tatsumi H, Inoue Y, Kano M, Watanabe M (2011) Developmental switching of perisomatic innervation from climbing fibers to basket cell fibers in cerebellar Purkinje cells. J Neurosci 31(47):16916-16927. doi: 10.1523/JNEUROSCI.2396-11.2011
60. Sotelo C (2008) Development of "Pinceaux" formations and dendritic translocation of climbing fibers during the acquisition of the balance between glutamatergic and γ-aminobutyric acidergic inputs in developing Purkinje cells. J Comp Neurol 506(2):240-262. doi: 10.1002/cne.21501
61. Altman J (1972) Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and of the molecular layer. J Comp Neurol 145(4):399-463. doi: 10.1002/cne.901450402
62. Watanabe M (2008) Molecular mechanisms governing competitive synaptic wiring in cerebellar Purkinje cells. Tohoku J Exp Med 214(3):175-190
63. Maejima T, Hashimoto K, Yoshida T, Aiba A, Kano M (2001) Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron 31(3):463-475
64. Carrillo J, Nishiyama N, Nishiyama H (2013) Dendritic translocation establishes the winner in cerebellar climbing fiber synapse elimination. J Neurosci 33(18):7641-7653. doi: 10.1523/JNEUROSCI.4561-12.2013
65. Faust PL (2003) Abnormal cerebellar histogenesis in PEX2 Zellweger mice reflects multiple neuronal defects induced by peroxisome deficiency. J Comp Neurol 461(3):394-413. doi: 10.1002/cne.10699
66. Watanabe F, Miyazaki T, Takeuchi T, Fukaya M, Nomura T, Noguchi S, Mori H, Sakimura K, Watanabe M, Mishina M (2008) Effects of FAK ablation on cerebellar foliation, Bergmann glia positioning and climbing fiber territory on Purkinje cells. Eur J Neurosci 27(4):836-854. doi: 10.1111/j.1460-9568.2008. 06069.x
67. Takagishi Y, Hashimoto K, Kayahara T, Watanabe M, Otsuka H, Mizoguchi A, Kano M, Murata Y (2007) Diminished climbing fiber innervation of Purkinje cells in the cerebellum of myosin Va mutant mice and rats. Develop Neurobiol 67(7):909-923. doi: 10.1002/dneu.20375
68. 2+ channel α1A regulates synaptic competition on developing cerebellar Purkinje cells. J Neurosci 24(7):1734-1743
69. Miyazaki T, Yamasaki M, Hashimoto K, Yamazaki M, Abe M, Usui H, Kano M, Sakimura K, Watanabe M (2012) Cav2.1 in cerebellar Purkinje cells regulates competitive excitatory synaptic wiring, cell survival, and cerebellar biochemical compartmentalization. J Neurosci 32(4):1311-1328. doi: 10.1523/JNEUROSCI.2755-11.2012
70. Lorenzetto E, Caselli L, Feng G, Yuan W, Nerbonne JM, Sanes JR, Buffelli M (2009) Genetic perturbation of postsynaptic activity regulates synapse elimination in developing cerebellum. Proc Natl Acad Sci USA 106(38):16475-16480. doi: 10.1073/pnas.0907298106
71. Duvick L, Barnes J, Ebner B, Agrawal S, Andresen M, Lim J, Giesler GJ, Zoghbi HY, Orr HT (2010) SCA1-like disease in mice expressing wild-type ataxin-1 with a serine to aspartic acid replacement at residue 776. Neuron 67(6):929-935. doi: 10.1016/j.neuron.2010.08.022
72. Bravin M, Morando L, Vercelli A, Rossi F, Strata P (1999) Control of spine formation by electrical activity in the adult rat cerebellum. Proc Natl Acad Sci USA 96(4):1704-1709
73. Kakizawa S, Miyazaki T, Yanagihara D, Iino M, Watanabe M, Kano M (2005) Maintenance of presynaptic function by AMPA receptor-mediated excitatory postsynaptic activity in adult brain. Proc Natl Acad Sci USA 102(52):19180-19185. doi: 10.1073/pnas.0504359103
74. Andjus PR, Zhu L, Cesa R, Carulli D, Strata P (2003) A change in the pattern of activity affects the developmental regression of the Purkinje cell polyinnervation by climbing fibers in the rat cerebellum. Neuroscience 121(3):563-572
75. Kakizawa S, Yamada K, Iino M, Watanabe M, Kano M (2003) Effects of insulin-like growth factor I on climbing fibre synapse elimination during cerebellar development. Eur J Neurosci 17(3):545-554
76. Altman J, Anderson WJ (1972) Experimental reorganization of the cerebellar cortex. I. Morphological effects of elimination of all microneurons with prolonged X-irradiation started at birth. J Comp Neurol 146(3):355-406
77. Landis DM, Sidman RL (1978) Electron microscopic analysis of postnatal histogenesis in the cerebellar cortex of staggerer mutant mice. J Comp Neurol 179(4):831-863
78. Rakic P, Sidman RL (1973) Organization of cerebellar cortex secondary to deficit of granule cells in weaver mutant mice. J Comp Neurol 152(2):133-161
79. Sotelo C (1975) Anatomical, physiological and biochemical studies of the cerebellum from mutant mice. II. Morphological study of cerebellar cortical neurons and circuits in the weaver mouse. Brain Res 94(1):19-44
80. Hashimoto K, Ichikawa R, Takechi H, Inoue Y, Aiba A, Sakimura K, Mishina M, Hashikawa T, Konnerth A, Watanabe M, Kano M (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(24):9701-9712
81. Ichikawa R, Miyazaki T, Kano M, Hashikawa T, Tatsumi H, Sakimura K, Mishina M, Inoue Y, Watanabe M (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(19):8487-8503
82. Kashiwabuchi N, Ikeda K, Araki K, Hirano T, Shibuki K, Takayama C, Inoue Y, Kutsuwada T, Yagi T, Kang Y et al (1995) Impairment of motor coordination, Purkinje cell synapse formation, and cerebellar long-term depression in GluR δ2 mutant mice. Cell 81(2):245-252
83. Kurihara H, Hashimoto K, Kano M, Takayama C, Sakimura K, Mishina M, Inoue Y, Watanabe M (1997) Impaired parallel fiber - > Purkinje cell synapse stabilization during cerebellar development of mutant mice lacking the glutamate receptor δ2 subunit. J Neurosci 17(24):9613-9623
84. Nishiyama H, Fukaya M, Watanabe M, Linden DJ (2007) Axonal motility and its modulation by activity are branch-type specific in the intact adult cerebellum. Neuron 56(3):472-487. doi: 10.1016/j.neuron.2007.09.010
85. Hirai H, Pang Z, Bao D, Miyazaki T, Li L, Miura E, Parris J, Rong Y, Watanabe M, Yuzaki M, Morgan JI (2005) Cbln1 is essential for synaptic integrity and plasticity in the cerebellum. Natl Neurosci 8(11):1534-1541. doi: 10.1038/nn1576
86. Matsuda K, Miura E, Miyazaki T, Kakegawa W, Emi K, Narumi S, Fukazawa Y, Ito-Ishida A, Kondo T, Shigemoto R, Watanabe M, Yuzaki M (2010) Cbln1 is a ligand for an orphan glutamate receptor δ2, a bidirectional synapse organizer. Science 328(5976):363-368. doi: 10.1126/science.1185152
87. Uemura T, Lee SJ, Yasumura M, Takeuchi T, Yoshida T, Ra M, Taguchi R, Sakimura K, Mishina M (2010) Trans-synaptic interaction of GluRδ2 and Neurexin through Cbln1 mediates synapse formation in the cerebellum. Cell 141(6):1068-1079. doi: 10.1016/j.cell.2010.04.035
88. Miyazaki T, Yamasaki M, Takeuchi T, Sakimura K, Mishina M, Watanabe M (2010) Ablation of glutamate receptor GluRδ2 in adult Purkinje cells causes multiple innervation of climbing fibers by inducing aberrant invasion to parallel fiber innervation territory. J Neurosci 30(45):15196-15209. doi: 10.1523/JNEUROSCI.0934-10.2010
89. Kano M, Hashimoto K, Chen C, Abeliovich A, Aiba A, Kurihara H, Watanabe M, Inoue Y, Tonegawa S (1995) Impaired synapse elimination during cerebellar development in PKC γ mutant mice. Cell 83(7):1223-1231
90. Kano M, Hashimoto K, Kurihara H, Watanabe M, Inoue Y, Aiba A, Tonegawa S (1997) Persistent multiple climbing fiber innervation of cerebellar Purkinje cells in mice lacking mGluR1. Neuron 18(1):71-79
91. 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 cβ4 is specifically involved in climbing fiber synapse elimination in the developing cerebellum. Proc Natl Acad Sci USA 95(26):15724-15729
92. 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 Gαq. Proc Natl Acad Sci USA 94(25):14089-14094
93. Kano M, Hashimoto K, Tabata T (2008) Type-1 metabotropic glutamate receptor in cerebellar Purkinje cells: a key molecule responsible for long-term depression, endocannabinoid signalling and synapse elimination. Philos Trans R Soc Lond B 363(1500):2173-2186
94. 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(5472):1832-1835
95. De Zeeuw CI, Hansel C, Bian F, Koekkoek SK, van Alphen AM, Linden DJ, Oberdick J (1998) Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar LTD and adaptation of the vestibulo-ocular reflex. Neuron 20(3):495-508
96. Hashimoto K, Watanabe M, Kurihara H, Offermanns S, Jiang H, Wu Y, Jun K, Shin HS, Inoue Y, Wu D, Simon MI, Kano M (2000) Climbing fiber synapse elimination during postnatal cerebellar development requires signal transduction involving Gαq and phospholipase Cβ4. Prog Brain Res 124:31-48
97. Batchelor AM, Garthwaite J (1997) Frequency detection and temporally dispersed synaptic signal association through a metabotropic glutamate receptor pathway. Nature 385(6611):74-77. doi: 10.1038/385074a0
98. Finch EA, Augustine GJ (1998) Local calcium signalling by inositol-1,4,5-trisphosphate in Purkinje cell dendrites. Nature 396(6713):753-756
99. Takechi H, Eilers J, Konnerth A (1998) A new class of synaptic response involving calcium release in dendritic spines. Nature 396(6713):757-760
100. Dzubay JA, Otis TS (2002) Climbing fiber activation of metabotropic glutamate receptors on cerebellar purkinje neurons. Neuron 36(6):1159-1167
101. Rabacchi S, Bailly Y, Delhaye-Bouchaud N, Mariani J (1992) Involvement of the N-methyl d-aspartate (NMDA) receptor in synapse elimination during cerebellar development. Science 256(5065):1823-1825
102. Kakizawa S, Yamasaki M, Watanabe M, Kano M (2000) Critical period for activity-dependent synapse elimination in developing cerebellum. J Neurosci 20(13):4954-4961
103. Lachamp P, Balland B, Tell F, Baude A, Strube C, Crest M, Kessler JP (2005) Early expression of AMPA receptors and lack of NMDA receptors in developing rat climbing fibre synapses. J Physiol 564(Pt 3):751-763. doi: 10.1113/jphysiol.2005.084517
104. Piochon C, Irinopoulou T, Brusciano D, Bailly Y, Mariani J, Levenes C (2007) NMDA receptor contribution to the climbing fiber response in the adult mouse Purkinje cell. J Neurosci 27(40):10797-10809. doi: 10.1523/JNEUROSCI.2422- 07.2007
105. Kano M, Nakayama H, Hashimoto K, Kitamura K, Sakimura K, Watanabe M (2013) Calcium-dependent regulation of climbing fiber synapse elimination during postnatal cerebellar development. J Physiol. doi: 10.1113/jphysiol.2012.248252
106. Bosman LWJ, Hartmann J, Barski JJ, Lepier A, Noll-Hussong M, Reichardt LF, Konnerth A (2006) Requirement of TrkB for synapse elimination in developing cerebellar Purkinje cells. Brain Cell Biol 35:87-101
107. Johnson EM, Craig ET, Yeh HH (2007) TrkB is necessary for pruning at the climbing fibre-Purkinje cell synapse in the developing murine cerebellum. J Physiol 582(Pt 2):629-646
108. Sherrard RM, Bower AJ (2002) Climbing fiber development: do neurotrophins have a part to play? Cerebellum 1(4):265-275. doi: 10.1080/147342202320883579
109. Sherrard RM, Dixon KJ, Bakouche J, Rodger J, Lemaigre-Dubreuil Y, Mariani J (2009) Differential expression of TrkB isoforms switches climbing fiber-Purkinje cell synaptogenesis to selective synapse elimination. Develop Neurobiol 69(10):647-662. doi: 10.1002/dneu.20730
110. Rico B, Xu B, Reichardt LF (2002) TrkB receptor signaling is required for establishment of GABAergic synapses in the cerebellum. Nat Neurosci 5(3):225-233. doi: 10.1038/nn808
111. Drake-Baumann R (2006) Activity-dependent modulation of inhibition in Purkinje cells by TrkB ligands. Cerebellum 5(3):220-226. doi: 10.1080/14734220600621344
112. Seil FJ (2003) TrkB receptor signaling and activity-dependent inhibitory synaptogenesis. Histol Histopathol 18(2):635-646
113. Song JW, Misgeld T, Kang H, Knecht S, Lu J, Cao Y, Cotman SL, Bishop DL, Lichtman JW (2008) Lysosomal activity associated with developmental axon pruning. J Neurosci 28(36):8993-9001. doi: 10.1523/JNEUROSCI.0720-08.2008
114. Bishop DL, Misgeld T, Walsh MK, Gan WB, Lichtman JW (2004) Axon branch removal at developing synapses by axosome shedding. Neuron 44(4):651-661. doi: 10.1016/j.neuron.2004.10.026
115. Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, Ransohoff RM, Greenberg ME, Barres BA, Stevens B (2012) Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74(4):691-705. doi: 10.1016/j.neuron.2012.03.026
116. Stevens B, Allen NJ, Vazquez LE, Howell GR, Christopherson KS, Nouri N, Micheva KD, Mehalow AK, Huberman AD, Stafford B, Sher A, Litke AM, Lambris JD, Smith SJ, John SW, Barres BA (2007) The classical complement cascade mediates CNS synapse elimination. Cell 131(6):1164-1178. doi: 10.1016/j.cell.2007.10.036
117. Stephan AH, Barres BA, Stevens B (2012) The complement system: an unexpected role in synaptic pruning during development and disease. Annu Rev Neurosci 35:369-389. doi: 10.1146/annurev-neuro-061010-113810
118. 2+/calmodulin kinase IV-deficient mice. J Neurosci 20(22):RC107
119. Hansel C, de Jeu M, Belmeguenai A, Houtman SH, Buitendijk GH, Andreev D, De Zeeuw CI, Elgersma Y (2006) αCaMKII Is essential for cerebellar LTD and motor learning. Neuron 51(6):835-843. doi: 10.1016/j.neuron.2006.08.013
120. Letellier M, Wehrle R, Mariani J, Lohof AM (2009) Synapse elimination in olivo-cerebellar explants occurs during a critical period and leaves an indelible trace in Purkinje cells. Proc Natl Acad Sci USA 106(33):14102-14107. doi: 10.1073/pnas.0902820106
121. Ohno T, Sakurai M (2005) Critical period for activity-dependent elimination of corticospinal synapses in vitro. Neuroscience 132(4):917-922. doi: 10.1016/j.neuroscience.2005.01.056
122. Uesaka N, Mikuni T, Hashimoto K, Hirai H, Sakimura K, Kano M (2012) Organotypic coculture preparation for the study of developmental synapse elimination in mammalian brain. J Neurosci 32(34):11657-11670. doi: 10.1523/JNEUROSCI.1097-12.2012
123. Mikuni T, Uesaka N, Okuno H, Hirai H, Deisseroth K, Bito H, Kano M (2013) Arc/Arg3.1 is a postsynaptic mediator of activity-dependent synapse elimination in the developing cerebellum. Neuron 78(6):1024-1035. doi: 10.1016/j.neuron. 2013.04.036