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Developmental Axonal Pruning and Synaptic Plasticity

  • Bibiana Scelfo
  • Mario Rosario BuffelliEmail author
Chapter
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Abstract

The functioning of the nervous system depends upon the underlying specific and highly ordered patterns of neuronal connections. The embryonic pattern of neuronal connectivity is essentially established by specific molecular cues and is refined by synapse elimination and axonal pruning of exuberant or inaccurate connections during later developmental stages. In this chapter we provide a general description of the phenomena of synapse elimination, axonal pruning, and synaptic plasticity in the central and the peripheral nervous system. Also, we briefly describe the role of the adhesion molecules in these processes.

Keywords

Synapse elimination Polyneuronal innervation Axonal pruning Neuronal connectivity Synaptic plasticity 

Notes

Acknowledgments

We thank Telethon-Italy for the Grant No. GGP030164, MIUR-Italy for the Grant PRIN-2006, Fondazione Cariverona, University of Verona, the National Institute of Neuroscience-Italy and the Regione Piemonte, grant for Ricerca Sanitaria Finalizzata 2006.

References

  1. Abbott LF and Nelson SB (2000) Synaptic plasticity: taming the beast. Nat Neurosci 3 Suppl:1178–1183PubMedCrossRefGoogle Scholar
  2. Abbott LF and Regehr WG (2004) Synaptic computation. Nature 431:796–803PubMedCrossRefGoogle Scholar
  3. Akaaboune M, Culican SM, Turney SG et al. (1999) Rapid and reversible effects of activity on acetylcholine receptor density at the neuromuscular junction in vivo [see comments]. Science 286:503–507PubMedCrossRefGoogle Scholar
  4. Alger BE and Teyler TJ (1976) Long-term and short-term plasticity in the CA1, CA3, and dentate regions of the rat hippocampal slice. Brain Res 110:463–480PubMedCrossRefGoogle Scholar
  5. 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 145:399–463PubMedCrossRefGoogle Scholar
  6. Amaral DG and Dent JA (1981) Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions. J Comp Neurol 195:51–86PubMedCrossRefGoogle Scholar
  7. Andjus PR, Zhu L, Cesa R et al. (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 121:563–572PubMedCrossRefGoogle Scholar
  8. Aoto J and Chen L (2007) Bidirectional ephrin/Eph signaling in synaptic functions. Brain Res 1184:72–80PubMedCrossRefGoogle Scholar
  9. Araç D, Boucard AA, Ozkan E et al. (2007) Structures of neuroligin-1 and the neuroligin-1/neurexin-1 beta complex reveal specific protein-protein and protein-Ca2+ interactions. Neuron 56:992–1003PubMedCrossRefGoogle Scholar
  10. Bagri A, Cheng HJ, Yaron A et al. (2003) Stereotyped pruning of long hippocampal axon branches triggered by retraction inducers of the semaphorin family. Cell 113:285–299PubMedCrossRefGoogle Scholar
  11. Balice-Gordon RJ and Lichtman JW (1994) Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature 372:519–524PubMedCrossRefGoogle Scholar
  12. Baranes D, Lederfein D, Huang YY et al. (1998) Tissue plasminogen activator contributes to the late phase of LTP and to synaptic growth in the hippocampal mossy fiber pathway. Neuron 21:813–825PubMedCrossRefGoogle Scholar
  13. Barria A, Muller D, Derkach V et al. (1997) Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science 276:2042–2045PubMedCrossRefGoogle Scholar
  14. Beattie EC, Stellwagen D, Morishita W et al. (2002) Control of synaptic strength by glial TNFalpha. Science 295:2282–2285PubMedCrossRefGoogle Scholar
  15. Berardi N, Pizzorusso T and Maffei L (2004) Extracellular matrix and visual cortical plasticity: freeing the synapse. Neuron 44:905–908PubMedGoogle Scholar
  16. Bernstein M and Lichtman JW (1999) Axonal atrophy: the retraction reaction. Curr Opin Neurobiol 9:364–370PubMedCrossRefGoogle Scholar
  17. Betz WJ, Caldwell JH and Ribchester RR (1980) Sprouting of active nerve terminals in partially inactive muscles of the rat. J Physiol 303:281–297PubMedGoogle Scholar
  18. Bidoia C, Misgeld T, Weinzierl E et al. (2004) Comment on “Reelin promotes peripheral synapse elimination and maturation”. Science 303:1977; author reply 1977PubMedCrossRefGoogle Scholar
  19. Bishop DL, Misgeld T, Walsh MK et al. (2004) Axon branch removal at developing synapses by axosome shedding. Neuron 44:651–661PubMedCrossRefGoogle Scholar
  20. Bliss TV and Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232:331–356PubMedGoogle Scholar
  21. Bonhoeffer T and Yuste R (2002) Spine motility. Phenomenology, mechanisms, and function. Neuron 35:1019–1027PubMedCrossRefGoogle Scholar
  22. Bosman LW, Takechi H, Hartmann J et al. (2008) Homosynaptic long-term synaptic potentiation of the “winner” climbing fiber synapse in developing Purkinje cells. J Neurosci 28:798–807PubMedCrossRefGoogle Scholar
  23. Boulanger LM and Shatz CJ (2004) Immune signalling in neural development, synaptic plasticity and disease. Nat Rev Neurosci 5:521–531PubMedCrossRefGoogle Scholar
  24. Bravin M, Rossi F and Strata P (1995) Different climbing fibres innervate separate dendritic regions of the same Purkinje cell in hypogranular cerebellum. J Comp Neurol 357:395–407PubMedCrossRefGoogle Scholar
  25. Brown MC, Jansen JKS and Essen DV (1976) Polyneuronal innervation of skeletal muscle in new-born rats and its elimination during maturation. J Physiol 261:387–424PubMedGoogle Scholar
  26. Brownlee H, Gao PP, Frisen J et al. (2000) Multiple ephrins regulate hippocampal neurite outgrowth. J Comp Neurol 425:315–322PubMedCrossRefGoogle Scholar
  27. Buffelli M, Burgess RW, Feng G et al. (2003) Genetic evidence that relative synaptic efficacy biases the outcome of synaptic competition. Nature 424:430–434PubMedCrossRefGoogle Scholar
  28. Buffelli M, Busetto G, Bidoia C et al. (2004) Activity-dependent synaptic competition at mammalian neuromuscular junctions. News Physiol Sci 19:85–91PubMedGoogle Scholar
  29. Buffelli M, Busetto G, Cangiano L et al. (2002) Perinatal switch from synchronous to asynchronous activity of motoneurons: link with synapse elimination. Proc Natl Acad Sci USA 99:13200–13205PubMedCrossRefGoogle Scholar
  30. Busetto G, Buffelli M, Tognana E et al. (2000) Hebbian mechanisms revealed by electrical stimulation at developing rat neuromuscular junctions. J Neurosci 20:685–695PubMedGoogle Scholar
  31. Cabelli RJ, Shelton DL, Segal RA et al. (1997) Blockade of endogenous ligands of trkB inhibits formation of ocular dominance columns. Neuron 19:63–76PubMedCrossRefGoogle Scholar
  32. Cang J, Kaneko M, Yamada J et al. (2005) Ephrin-as guide the formation of functional maps in the visual cortex. Neuron 48:577–589PubMedCrossRefGoogle Scholar
  33. Cash S, Dan Y, Poo MM et al. (1996) Postsynaptic elevation of calcium induces persistent depression of developing neuromuscular synapses. Neuron 16:745–754PubMedCrossRefGoogle Scholar
  34. Celio MR, Spreafico R, De Biasi S et al. (1998) Perineuronal nets: past and present. Trends Neurosci 21:510–515PubMedCrossRefGoogle Scholar
  35. Chen C, Kano M, Abeliovich A et al. (1995) Impaired motor coordination correlates with persistent multiple climbing fiber innervation in PKC gamma mutant mice. Cell 83:1233–1242PubMedCrossRefGoogle Scholar
  36. Chen H, Bagri A, Zupicich JA et al. (2000) Neuropilin-2 regulates the development of selective cranial and sensory nerves and hippocampal mossy fiber projections. Neuron 25:43–56PubMedCrossRefGoogle Scholar
  37. Cheng HJ, Bagri A, Yaron A et al. (2001) Plexin-A3 mediates semaphorin signaling and regulates the development of hippocampal axonal projections. Neuron 32:249–263PubMedCrossRefGoogle Scholar
  38. Cheng HJ, Nakamoto M, Bergemann AD et al. (1995) Complementary gradients in expression and binding of ELF-1 and Mek4 in development of the topographic retinotectal projection map. Cell 82:371–381PubMedCrossRefGoogle Scholar
  39. Chih B and Scheiffele P (2003) Is reelin the answer to synapse elimination at the neuromuscular junction? Sci STKE 2003:pe45CrossRefGoogle Scholar
  40. Colbran RJ and Brown AM (2004) Calcium/calmodulin-dependent protein kinase II and synaptic plasticity. Curr Opin Neurobiol 14:318–327PubMedCrossRefGoogle Scholar
  41. Colman H, Nabekura J and Lichtman JW (1997) Alterations in synaptic strength preceding axon withdrawal [see comments]. Science 275:356–361PubMedCrossRefGoogle Scholar
  42. Comery TA, Harris JB, Willems PJ et al. (1997) Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proc Natl Acad Sci USA 94:5401–5404PubMedCrossRefGoogle Scholar
  43. Connold AL, Evers JV and Vrbova G (1986) Effect of low calcium and protease inhibitors on synapse elimination during postnatal development in the rat soleus muscle. Brain Res 393:99–107PubMedGoogle Scholar
  44. Conquet F, Bashir ZI, Davies CH et al. (1994) Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1. Nature 372:237–243PubMedCrossRefGoogle Scholar
  45. Corriveau RA, Huh GS and Shatz CJ (1998) Regulation of class I MHC gene expression in the developing and mature CNS by neural activity. Neuron 21:505–520PubMedCrossRefGoogle Scholar
  46. Costanzo EM, Barry JA and Ribchester RR (2000) Competition at silent synapses in reinnervated skeletal muscle. Nat Neurosci 3:694–700PubMedCrossRefGoogle Scholar
  47. Crepel F, Dhanjal SS and Garthwaite J (1981) Morphological and electrophysiological characteristics of rat cerebellar slices maintained in vitro. J Physiol 316:127–138PubMedGoogle Scholar
  48. Crowley JC and Katz LC (2002) Ocular dominance development revisited. Curr Opin Neurobiol 12:104–109PubMedCrossRefGoogle Scholar
  49. Crusio WE and Schwegler H (1987) Hippocampal mossy fiber distribution covaries with open-field habituation in the mouse. Behav Brain Res 26:153–158PubMedCrossRefGoogle Scholar
  50. Davis GW (2006) Homeostatic control of neural activity: from phenomenology to molecular design. Annu Rev Neurosci 29:307–323PubMedCrossRefGoogle Scholar
  51. Davis GW and Bezprozvanny I (2001) Maintaining the stability of neural function: a homeostatic hypothesis. Annu Rev Physiol 63:847–869PubMedCrossRefGoogle Scholar
  52. Davis GW and Goodman CS (1998) Genetic analysis of synaptic development and plasticity: homeostatic regulation of synaptic efficacy. Curr Opin Neurobiol 8:149–156PubMedCrossRefGoogle Scholar
  53. Davis S, Gale NW, Aldrich TH et al. (1994) Ligands for EPH-related receptor tyrosine kinases that require membrane attachment or clustering for activity. Science 266:816–819PubMedCrossRefGoogle Scholar
  54. Deppmann CD, Mihalas S, Sharma N et al. (2008) A model for neuronal competition during development. Science 320:369–373PubMedCrossRefGoogle Scholar
  55. Desai NS, Rutherford LC and Turrigiano GG (1999) BDNF regulates the intrinsic excitability of cortical neurons. Learn Mem 6:284–291PubMedGoogle Scholar
  56. Donoghue MJ and Rakic P (1999a) Molecular evidence for the early specification of presumptive functional domains in the embryonic primate cerebral cortex. J Neurosci 19:5967–5979PubMedGoogle Scholar
  57. Donoghue MJ and Rakic P (1999b) Molecular gradients and compartments in the embryonic primate cerebral cortex. Cereb Cortex 9:586–600PubMedCrossRefGoogle Scholar
  58. Duxson MJ (1982) The effect of postsynaptic block on development of the neuromuscular junction in postnatal rats. J Neurocytol 11:395–408PubMedCrossRefGoogle Scholar
  59. Eccles JC, Llinas R and Sasaki K (1966) The excitatory synaptic action of climbing fibres on the Purkinje cells of the cerebellum. J Physiol 182:268–296PubMedGoogle Scholar
  60. Eckenhoff MF and Pysh JJ (1979) Double-walled coated vesicle formation: evidence for massive and transient conjugate internalization of plasma membranes during cerebellar development. J Neurocytol 8:623–638PubMedCrossRefGoogle Scholar
  61. English AW and Schwartz G (1995) Both basic fibroblast growth factor and ciliary neurotrophic factor promote the retention of polyneuronal innervation of developing skeletal muscle fibers. Dev Biol 169:57–64PubMedCrossRefGoogle Scholar
  62. Evers MR, Salmen B, Bukalo O et al. (2002) Impairment of L-type Ca2+ channel-dependent forms of hippocampal synaptic plasticity in mice deficient in the extracellular matrix glycoprotein tenascin-C. J Neurosci 22:7177–7194PubMedGoogle Scholar
  63. Fagiolini M and Hensch TK (2000) Inhibitory threshold for critical-period activation in primary visual cortex. Nature 404:183–186PubMedCrossRefGoogle Scholar
  64. Faulkner RL, Low LK and Cheng HJ (2007) Axon pruning in the developing vertebrate hippocampus. Dev Neurosci 29:6–13PubMedCrossRefGoogle Scholar
  65. Favero M, Lorenzetto E, Bidoia C et al. (2007) Synapse formation and elimination: role of activity studied in different models of adult muscle reinnervation. J Neurosci Res 85:2610–2619PubMedCrossRefGoogle Scholar
  66. Feldman DE (2000) Inhibition and plasticity. Nat Neurosci 3:303–304PubMedCrossRefGoogle Scholar
  67. Fitzsimonds RM and Poo MM (1998) Retrograde signaling in the development and modification of synapses. Physiol Rev 78:143–170PubMedGoogle Scholar
  68. Fladby T (1987) Postnatal loss of synaptic terminals in the normal mouse soleus muscle. Acta Physiol Scand 129:229–238PubMedCrossRefGoogle Scholar
  69. Flourens P (1824) Recherches expérimentales sur les propriétés et les fonctions du système nerveux dans les animaux vertébrés. In: Clarke EaOM, C. (eds) The Human Brain and Spinal Cord. University of California Press, Berkeley and Los AngelesGoogle Scholar
  70. Gale NW, Holland SJ, Valenzuela DM et al. (1996) Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis. Neuron 17:9–19PubMedCrossRefGoogle Scholar
  71. Gan WB, Bishop DL, Turney SG et al. (1999) Vital imaging and ultrastructural analysis of individual axon terminals labeled by iontophoretic application of lipophilic dye. J Neurosci Methods 93:13–20PubMedCrossRefGoogle Scholar
  72. Gan WB and Lichtman JW (1998) Synaptic segregation at the developing neuromuscular junction. Science 282:1508–1511PubMedCrossRefGoogle Scholar
  73. Gao PP, Zhang JH, Yokoyama M et al. (1996) Regulation of topographic projection in the brain: Elf-1 in the hippocamposeptal system. Proc Natl Acad Sci USA 93:11161–11166PubMedCrossRefGoogle Scholar
  74. Geuze E, Vermetten E and Bremner JD (2005a) MR-based in vivo hippocampal volumetrics: 1. Review of methodologies currently employed. Mol Psychiatry 10:147–159PubMedCrossRefGoogle Scholar
  75. Geuze E, Vermetten E and Bremner JD (2005b) MR-based in vivo hippocampal volumetrics: 2. Findings in neuropsychiatric disorders. Mol Psychiatry 10:160–184PubMedCrossRefGoogle Scholar
  76. Gonzalez-Islas C and Wenner P (2006) Spontaneous network activity in the embryonic spinal cord regulates AMPAergic and GABAergic synaptic strength. Neuron 49:563–575PubMedCrossRefGoogle Scholar
  77. Goodman CS and Shatz CJ (1993) Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72 Suppl:77–98PubMedCrossRefGoogle Scholar
  78. Greenough WT, Hwang HM and Gorman C (1985) Evidence for active synapse formation or altered postsynaptic metabolism in visual cortex of rats reared in complex environments. Proc Natl Acad Sci USA 82:4549–4552PubMedCrossRefGoogle Scholar
  79. Gualandris A, Jones TE, Strickland S et al. (1996) Membrane depolarization induces calcium-dependent secretion of tissue plasminogen activator. J Neurosci 16:2220–2225PubMedGoogle Scholar
  80. Guimaraes A, Zaremba S and Hockfield S (1990) Molecular and morphological changes in the cat lateral geniculate nucleus and visual cortex induced by visual deprivation are revealed by monoclonal antibodies Cat-304 and Cat-301. J Neurosci 10:3014–3024PubMedGoogle Scholar
  81. Haas JS, Nowotny T and Abarbanel HD (2006) Spike-timing-dependent plasticity of inhibitory synapses in the entorhinal cortex. J Neurophysiol 96:3305–3313PubMedCrossRefGoogle Scholar
  82. Hashimoto K, Ichikawa R, Takechi H et al. (2001a) Roles of glutamate receptor delta 2 subunit (GluRdelta 2) and metabotropic glutamate receptor subtype 1 (mGluR1) in climbing fiber synapse elimination during postnatal cerebellar development. J Neurosci 21:9701–9712PubMedGoogle Scholar
  83. Hashimoto K, Miyata M, Watanabe M et al. (2001b) Roles of phospholipase Cbeta4 in synapse elimination and plasticity in developing and mature cerebellum. Mol Neurobiol 23:69–82PubMedCrossRefGoogle Scholar
  84. Hata Y, Butz S and Südhof TC (1996) CASK: a novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. J Neurosci 16:2488–2494PubMedGoogle Scholar
  85. Hebb D (1949) The Organization of Behavior. Wiley, New YorkGoogle Scholar
  86. Hensch TK, Fagiolini M, Mataga N et al. (1998) Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282:1504–1508PubMedCrossRefGoogle Scholar
  87. Hinton VJ, Brown WT, Wisniewski K et al. (1991) Analysis of neocortex in three males with the fragile X syndrome. Am J Med Genet 41:289–294PubMedCrossRefGoogle Scholar
  88. Hirai H (2001) Modification of AMPA receptor clustering regulates cerebellar synaptic plasticity. Neurosci Res 39:261–267PubMedCrossRefGoogle Scholar
  89. Hua JY and Smith SJ (2004) Neural activity and the dynamics of central nervous system development. Nat Neurosci 7:327–332PubMedCrossRefGoogle Scholar
  90. Huang ZJ, Kirkwood A, Pizzorusso T et al. (1999) BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98:739–755PubMedCrossRefGoogle Scholar
  91. Hubel DH and Wiesel TN (1963) Receptive Fields of Cells in Striate Cortex of Very Young, Visually Inexperienced Kittens. J Neurophysiol 26:994–1002PubMedGoogle Scholar
  92. Hubel DH and Wiesel TN (1970) The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J Physiol 206:419–436PubMedGoogle Scholar
  93. Hubel DH, Wiesel TN and LeVay S (1977) Plasticity of ocular dominance columns in monkey striate cortex. Philos Trans R Soc Lond B Biol Sci 278:377–409PubMedCrossRefGoogle Scholar
  94. Huber AB, Kolodkin AL, Ginty DD et al. (2003) Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Annu Rev Neurosci 26:509–563PubMedCrossRefGoogle Scholar
  95. Huh GS, Boulanger LM, Du H et al. (2000) Functional requirement for class I MHC in CNS development and plasticity. Science 290:2155–2159PubMedCrossRefGoogle Scholar
  96. Hume RI and Purves D (1981) Geometry of neonatal neurones and the regulation of synapse elimination. Nature 293:469–471PubMedCrossRefGoogle Scholar
  97. Hunt CA, Schenker LJ and Kennedy MB (1996) PSD-95 is associated with the postsynaptic density and not with the presynaptic membrane at forebrain synapses. J Neurosci 16:1380–1388Google Scholar
  98. Ichtchenko K, Nguyen T and Südhof TC (1996) Structures, alternative splicing, and neurexin binding of multiple neuroligins. J Biol Chem 271:2676–2682PubMedCrossRefGoogle Scholar
  99. Ito M (1984) The Cerebellum and Neural Control. Raven Press, New YorkGoogle Scholar
  100. Ito M (1989) Long-term depression. Annu Rev Neurosci 12:85–102PubMedCrossRefGoogle Scholar
  101. Ito M (2001) Cerebellar long-term depression: characterization, signal transduction, and functional roles. Physiol Rev 81:1143–1195PubMedGoogle Scholar
  102. Ito M and Kano M (1982) Long-lasting depression of parallel fiber-Purkinje cell transmission induced by conjunctive stimulation of parallel fibers and climbing fibers in the cerebellar cortex. Neurosci Lett 33:253–258PubMedCrossRefGoogle Scholar
  103. Ivanco TL and Greenough WT (2002) Altered mossy fiber distributions in adult Fmr1 (FVB) knockout mice. Hippocampus 12:47–54PubMedCrossRefGoogle Scholar
  104. Jansen JK and Fladby T (1990) The perinatal reorganization of the innervation of skeletal muscle in mammals. Prog Neurobiol 34:39–90PubMedCrossRefGoogle Scholar
  105. Jennings C (1994) Developmental neurobiology. Death of a synapse. Nature 372:498–499PubMedCrossRefGoogle Scholar
  106. Kano M, Hashimoto K, Chen C et al. (1995) Impaired synapse elimination during cerebellar development in PKC gamma mutant mice. Cell 83:1223–1231PubMedCrossRefGoogle Scholar
  107. Kantor DB and Kolodkin AL (2003) Curbing the excesses of youth: molecular insights into axonal pruning. Neuron 38:849–852PubMedCrossRefGoogle Scholar
  108. Kasthuri N and Lichtman JW (2003) The role of neuronal identity in synaptic competition. Nature 424:426–430PubMedCrossRefGoogle Scholar
  109. Katz LC and Crowley JC (2002) Development of cortical circuits: lessons from ocular dominance columns. Nat Rev Neurosci 3:34–42PubMedCrossRefGoogle Scholar
  110. Katz LC and Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133–1138PubMedCrossRefGoogle Scholar
  111. Keller-Peck CR, Walsh MK, Gan WB et al. (2001) Asynchronous synapse elimination in neonatal motor units: studies using GFP transgenic mice. Neuron 31:381–394.PubMedCrossRefGoogle Scholar
  112. Kirov SA, Sorra KE and Harris KM (1999) Slices have more synapses than perfusion-fixed hippocampus from both young and mature rats. J Neurosci 19:2876–2886PubMedGoogle Scholar
  113. Knight R (1996) Contribution of human hippocampal region to novelty detection. Nature 383:256–259PubMedCrossRefGoogle Scholar
  114. Kolodkin AL (1998) Semaphorin-mediated neuronal growth cone guidance. Prog Brain Res 117:115–132PubMedCrossRefGoogle Scholar
  115. Kornau HC and Seeburg PH (1997) Partner selection by PDZ domains. Nat Biotechnol 15:319PubMedCrossRefGoogle Scholar
  116. Kreitzer AC and Regehr WG (2001) Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29:717–727PubMedCrossRefGoogle Scholar
  117. Krueger S and Fitzsimonds RM (2006) Remodeling the plasticity debate: the presynaptic locus revisited. Physiology (Bethesda) 21:346–351Google Scholar
  118. Kuffler D, Thompson W and Jansen J (1977) The elimination of synapses in multiply-innervated skeletal muscle fibres of the rat: dependence on the distance between end-plates. Brain Res 138:353–358PubMedCrossRefGoogle Scholar
  119. Kullander K and Klein R (2002) Mechanisms and functions of Eph and ephrin signalling. Nat Rev Mol Cell Biol 3:475–486PubMedCrossRefGoogle Scholar
  120. Kwon YW, Abbondanzo SJ, Stewart CL et al. (1995) Leukemia inhibitory factor influences the timing of programmed synapses withdrawal from neonatal muscles. J Neurobiol 28:35–50PubMedCrossRefGoogle Scholar
  121. Kwon YW and Gurney ME (1996) Brain-derived neurotrophic factor transiently stabilizes silent synapses on developing neuromuscular junctions. J Neurobiol 29:503–516PubMedCrossRefGoogle Scholar
  122. Lauder JM and Mugnaini E (1980) Infrapyramidal mossy fibers in the hippocampus of the hyperthyroid rat. A light and electron microscopic study. Dev Neurosci 3:248–265PubMedCrossRefGoogle Scholar
  123. Lauri SE, Kaukinen S, Kinnunen T et al. (1999) Regulatory role and molecular interactions of a cell-surface heparan sulfate proteoglycan (N-syndecan) in hippocampal long-term potentiation. J Neurosci 19:1226–1235PubMedGoogle Scholar
  124. Lauri SE, Palmer M, Segerstrale M et al. (2007) Presynaptic mechanisms involved in the expression of STP and LTP at CA1 synapses in the hippocampus. Neuropharmacology 52:1–11PubMedCrossRefGoogle Scholar
  125. LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184PubMedCrossRefGoogle Scholar
  126. Lein ES and Shatz CJ (2000) Rapid regulation of brain-derived neurotrophic factor mRNA within eye-specific circuits during ocular dominance column formation. J Neurosci 20:1470–1483PubMedGoogle Scholar
  127. Leslie KR, Nelson SB and Turrigiano GG (2001) Postsynaptic depolarization scales quantal amplitude in cortical pyramidal neurons. J Neurosci 21:RC170PubMedGoogle Scholar
  128. LeVay S, Stryker MP and Shatz CJ (1978) Ocular dominance columns and their development in layer IV of the cat’s visual cortex: a quantitative study. J Comp Neurol 179:223–244PubMedCrossRefGoogle Scholar
  129. Lissin DV, Gomperts SN, Carroll RC et al. (1998) Activity differentially regulates the surface expression of synaptic AMPA and NMDA glutamate receptors. Proc Natl Acad Sci USA 95:7097–7102PubMedCrossRefGoogle Scholar
  130. Liu XB, Low LK, Jones EG et al. (2005) Stereotyped axon pruning via plexin signaling is associated with synaptic complex elimination in the hippocampus. J Neurosci 25:9124–9134PubMedCrossRefGoogle Scholar
  131. Liu Y, Fields RD, Fitzgerald S et al. (1994) Proteolytic activity, synapse elimination, and the Hebb synapse. J Neurobiol 25:325–335PubMedCrossRefGoogle Scholar
  132. Lo YJ and Poo MM (1991) Activity-dependent synaptic competition in vitro: heterosynaptic suppression of developing synapses. Science 254:1019–1022PubMedCrossRefGoogle Scholar
  133. Lohof AM, Delhaye-Bouchaud N and Mariani J (1996) Synapse elimination in the central nervous system: functional significance and cellular mechanisms. Rev Neurosci 7:85–101PubMedGoogle Scholar
  134. Lowel S and Singer W (1992) Selection of intrinsic horizontal connections in the visual cortex by correlated neuronal activity. Science 255:209–212PubMedCrossRefGoogle Scholar
  135. Luo L and O’Leary DD (2005) Axon retraction and degeneration in development and disease. Annu Rev Neurosci 28:127–156PubMedCrossRefGoogle Scholar
  136. Luthl A, Laurent JP, Figurov A et al. (1994) Hippocampal long-term potentiation and neural cell adhesion molecules L1 and NCAM. Nature 372:777–779PubMedCrossRefGoogle Scholar
  137. Mackarehtschian K, Lau CK, Caras I et al. (1999) Regional differences in the developing cerebral cortex revealed by ephrin-A5 expression. Cereb Cortex 9:601–610PubMedCrossRefGoogle Scholar
  138. Maffei A, Nelson SB and Turrigiano GG (2004) Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. Nat Neurosci 7:1353–1359PubMedCrossRefGoogle Scholar
  139. Maguire EA, Burgess N and O’Keefe J (1999) Human spatial navigation: cognitive maps, sexual dimorphism, and neural substrates. Curr Opin Neurobiol 9:171–177PubMedCrossRefGoogle Scholar
  140. Maguire EA, Frith CD, Burgess N et al. (1998) Knowing where things are parahippocampal involvement in encoding object locations in virtual large-scale space. J Cogn Neurosci 10:61–76PubMedCrossRefGoogle Scholar
  141. Mainen ZF, Maletic-Savatic M, Shi SH et al. (1999) Two-photon imaging in living brain slices. Methods 18:231–239, 181PubMedCrossRefGoogle Scholar
  142. Majewska AK and Sur M (2006) Plasticity and specificity of cortical processing networks. Trends Neurosci 29:323–329PubMedCrossRefGoogle Scholar
  143. Marder E and Prinz AA (2003) Current compensation in neuronal homeostasis. Neuron 37:2–4PubMedCrossRefGoogle Scholar
  144. Maren S (2001) Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 24:897–931PubMedCrossRefGoogle Scholar
  145. Mariani J and Changeux JP (1980) Multiple innervation of Purkinje cells by climbing fibers in the cerebellum of the adult staggerer mutant mouse. J Neurobiol 11:41–50PubMedCrossRefGoogle Scholar
  146. Martinez A, Otal R, Sieber BA et al. (2005) Disruption of ephrin-A/EphA binding alters synaptogenesis and neural connectivity in the hippocampus. Neuroscience 135:451–461PubMedCrossRefGoogle Scholar
  147. Mason CA, Christakos S and Catalano SM (1990) Early climbing fiber interactions with Purkinje cells in the postnatal mouse cerebellum. J Comp Neurol 297:77–90PubMedCrossRefGoogle Scholar
  148. Mataga N, Mizuguchi Y and Hensch TK (2004) Experience-dependent pruning of dendritic spines in visual cortex by tissue plasminogen activator. Neuron 44:1031–1041PubMedCrossRefGoogle Scholar
  149. Mataga N, Nagai N and Hensch TK (2002) Permissive proteolytic activity for visual cortical plasticity. Proc Natl Acad Sci USA 99:7717–7721PubMedCrossRefGoogle Scholar
  150. Maya Vetencourt JF, Sale A, Viegi A et al. (2008) The antidepressant fluoxetine restores plasticity in the adult visual cortex. Science 320:385–388PubMedCrossRefGoogle Scholar
  151. McLaughlin T, Hindges R and O’Leary DD (2003) Regulation of axial patterning of the retina and its topographic mapping in the brain. Curr Opin Neurobiol 13:57–69PubMedCrossRefGoogle Scholar
  152. Midtgaard J (1995) Spatial synaptic integration in Purkinje cell dendrites. J Physiol Paris 89:23–32PubMedCrossRefGoogle Scholar
  153. Mineur YS, Sluyter F, de Wit S et al. (2002) Behavioral and neuroanatomical characterization of the Fmr1 knockout mouse. Hippocampus 12:39–46PubMedCrossRefGoogle Scholar
  154. Miyata M, Kim HT, Hashimoto K et al. (2001) Deficient long-term synaptic depression in the rostral cerebellum correlated with impaired motor learning in phospholipase C beta4 mutant mice. Eur J Neurosci 13:1945–1954PubMedCrossRefGoogle Scholar
  155. Miyazaki T, Hashimoto K, Shin HS et al. (2004) P/Q-type Ca2+ channel alpha1A regulates synaptic competition on developing cerebellar Purkinje cells. J Neurosci 24:1734–1743PubMedCrossRefGoogle Scholar
  156. Mizumori SJ, Ragozzino KE, Cooper BG et al. (1999) Hippocampal representational organization and spatial context. Hippocampus 9:444–451PubMedCrossRefGoogle Scholar
  157. Mori T, Wanaka A, Taguchi A et al. (1995) Differential expressions of the eph family of receptor tyrosine kinase genes (sek, elk, eck) in the developing nervous system of the mouse. Brain Res Mol Brain Res 29:325–335PubMedCrossRefGoogle Scholar
  158. Murthy VN, Schikorski T, Stevens CF et al. (2001) Inactivity produces increases in neurotransmitter release and synapse size. Neuron 32:673–682PubMedCrossRefGoogle Scholar
  159. Nakamoto M, Cheng HJ, Friedman GC et al. (1996) Topographically specific effects of ELF-1 on retinal axon guidance in vitro and retinal axon mapping in vivo. Cell 86:755–766PubMedCrossRefGoogle Scholar
  160. Napper RM and Harvey RJ (1988) Number of parallel fiber synapses on an individual Purkinje cell in the cerebellum of the rat. J Comp Neurol 274:168–177PubMedCrossRefGoogle Scholar
  161. Nguyen QT and Lichtman JW (1996) Mechanism of synapse disassembly at the developing neuromuscular junction. Curr Opin Neurobiol 6:104–112PubMedCrossRefGoogle Scholar
  162. Nguyen QT, Parsadanian AS, Snider WD et al. (1998) Hyperinnervation of neuromuscular junctions caused by GDNF overexpression in muscle. Science 279:1725–1729PubMedCrossRefGoogle Scholar
  163. Nicoll RA and Malenka RC (1999) Expression mechanisms underlying NMDA receptor-dependent long-term potentiation. Ann N Y Acad Sci 868:515–525PubMedCrossRefGoogle Scholar
  164. O’Brien RA, Ostberg AJ and Vrbova G (1980) The effect of acetylcholine on the function and structure of the developing mammalian neuromuscular junction. Neuroscience 5:1367–1379PubMedCrossRefGoogle Scholar
  165. O’Brien RJ, Lau LF and Huganir RL (1998) Molecular mechanisms of glutamate receptor clustering at excitatory synapses. Curr Opin Neurobiol 8:364–369PubMedCrossRefGoogle Scholar
  166. O’Brien RJ, Xu D, Petralia RS et al. (1999) Synaptic clustering of AMPA receptors by the extracellular immediate-early gene product Narp. Neuron 23:309–323PubMedCrossRefGoogle Scholar
  167. O’Leary DD and Koester SE (1993) Development of projection neuron types, axon pathways, and patterned connections of the mammalian cortex. Neuron 10:991–1006PubMedCrossRefGoogle Scholar
  168. Oray S, Majewska A and Sur M (2004) Dendritic spine dynamics are regulated by monocular deprivation and extracellular matrix degradation. Neuron 44:1021–1030PubMedCrossRefGoogle Scholar
  169. Palay SL, Billings-Gagliardi S and Chan-Palay V (1974) Neuronal perikarya with dispersed, single ribosomes in the visual cortex of Macaca mulatta. J Cell Biol 63:1074–1089PubMedCrossRefGoogle Scholar
  170. Paradis S, Sweeney ST and Davis GW (2001) Homeostatic control of presynaptic release is triggered by postsynaptic membrane depolarization. Neuron 30:737–749PubMedCrossRefGoogle Scholar
  171. Patrizi A, Scelfo B, Viltono L et al. (2008) Synapse formation and clustering of neuroligin-2 in the absence of GABAA receptors. Proc Natl Acad Sci USA 105:13151–13156PubMedCrossRefGoogle Scholar
  172. Penn AA, Riquelme PA, Feller MB et al. (1998) Competition in retinogeniculate patterning driven by spontaneous activity. Science 279:2108–2112PubMedCrossRefGoogle Scholar
  173. Perrier JF, Alaburda A and Hounsgaard J (2002) Spinal plasticity mediated by postsynaptic L-type Ca2+ channels. Brain Res Brain Res Rev 40:223–229PubMedCrossRefGoogle Scholar
  174. Pizzorusso T, Medini P, Berardi N et al. (2002) Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298:1248–1251PubMedCrossRefGoogle Scholar
  175. Pulver SR, Bucher D, Simon DJ et al. (2005) Constant amplitude of postsynaptic responses for single presynaptic action potentials but not bursting input during growth of an identified neuromuscular junction in the lobster, Homarus americanus. J Neurobiol 62:47–61PubMedCrossRefGoogle Scholar
  176. Purves D and Hume RI (1981) The relation of postsynaptic geometry to the number of presynaptic axons that innervate autonomic ganglion cells. J Neurosci 1:441–452PubMedGoogle Scholar
  177. Purves D and Lichtman JW (1980) Elimination of synapses in the developing nervous system. Science 210:153–157PubMedCrossRefGoogle Scholar
  178. Quattrocchi CC, Huang C, Niu S et al. (2003) Reelin promotes peripheral synapse elimination and maturation. Science 301:649–653PubMedCrossRefGoogle Scholar
  179. Rabacchi S, Bailly Y, Delhaye-Bouchaud N et al. (1992a) Involvement of the N-methyl D-aspartate (NMDA) receptor in synapse elimination during cerebellar development. Science 256:1823–1825PubMedCrossRefGoogle Scholar
  180. Rabacchi SA, Bailly Y, Delhaye-Bouchaud N et al. (1992b) Role of the target in synapse elimination: studies in cerebellum of developing lurcher mutants and adult chimeric mice. J Neurosci 12:4712–4720PubMedGoogle Scholar
  181. Ramon y Cajal S (1911) Histologie du Systeme Nerveux de I’Homme et des Vertebres. Maloine, ParisGoogle Scholar
  182. Raymond CR, Ireland DR and Abraham WC (2003) NMDA receptor regulation by amyloid-beta does not account for its inhibition of LTP in rat hippocampus. Brain Res 968:263–272PubMedCrossRefGoogle Scholar
  183. Riley DA (1981) Ultrastructural evidence for axon retraction during the spontaneous elimination of polyneuronal innervation of the rat soleus muscle. J Neurocytol 10:425–440PubMedCrossRefGoogle Scholar
  184. Rossi FM, Bozzi Y, Pizzorusso T et al. (1999) Monocular deprivation decreases brain-derived neurotrophic factor immunoreactivity in the rat visual cortex. Neuroscience 90:363–368PubMedCrossRefGoogle Scholar
  185. Sacchetti B, Scelfo B, Tempia F et al. (2004) Long-term synaptic changes induced in the cerebellar cortex by fear conditioning. Neuron 42:973–982PubMedCrossRefGoogle Scholar
  186. Saghatelyan AK, Gorissen S, Albert M et al. (2000) The extracellular matrix molecule tenascin-R and its HNK-1 carbohydrate modulate perisomatic inhibition and long-term potentiation in the CA1 region of the hippocampus. Eur J Neurosci 12:3331–3342PubMedCrossRefGoogle Scholar
  187. Sahay A, Kim CH, Sepkuty JP et al. (2005) Secreted semaphorins modulate synaptic transmission in the adult hippocampus. J Neurosci 25:3613–3620PubMedCrossRefGoogle Scholar
  188. Sanes JR and Lichtman JW (1999) Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22:389–442PubMedCrossRefGoogle Scholar
  189. Scelfo B, Sacchetti B and Strata P (2008) Learning-related long-term potentiation of inhibitory synapses in the cerebellar cortex. Proc Natl Acad Sci USA 105:769–774PubMedCrossRefGoogle Scholar
  190. Scelfo B and Strata P (2005) Correlation between multiple climbing fibre regression and parallel fibre response development in the postnatal mouse cerebellum. Eur J Neurosci 21:971–978PubMedCrossRefGoogle Scholar
  191. Scelfo B, Strata P and Knöpfel T (2003) Sodium imaging of climbing fiber innervation fields in developing mouse Purkinje cells. J Neurophysiol 89:2555–2563PubMedCrossRefGoogle Scholar
  192. Schopke R, Wolfer DP, Lipp HP et al. (1991) Swimming navigation and structural variations of the infrapyramidal mossy fibers in the hippocampus of the mouse. Hippocampus 1:315–328PubMedCrossRefGoogle Scholar
  193. Schwegler H, Crusio WE, Lipp HP et al. (1991) Early postnatal hyperthyroidism alters hippocampal circuitry and improves radial-maze learning in adult mice. J Neurosci 11:2102–2106PubMedGoogle Scholar
  194. Segal M and Andersen P (2000) Dendritic spines shaped by synaptic activity. Curr Opin Neurobiol 10:582–586PubMedCrossRefGoogle Scholar
  195. Shapiro L, Love J and Colman DR (2007) Adhesion molecules in the nervous system: structural insights into function and diversity. Annu Rev Neurosci 30:451–474PubMedCrossRefGoogle Scholar
  196. Shatz CJ (1990) Competitive interactions between retinal ganglion cells during prenatal development. J Neurobiol 21:197–211PubMedCrossRefGoogle Scholar
  197. Shepherd JD, Rumbaugh G, Wu J et al. (2006) Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors. Neuron 52:475–484PubMedCrossRefGoogle Scholar
  198. Shi S, Hayashi Y, Esteban JA et al. (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105:331–343PubMedCrossRefGoogle Scholar
  199. Singh KK and Miller FD (2005) Activity regulates positive and negative neurotrophin-derived signals to determine axon competition. Neuron 45:837–845PubMedCrossRefGoogle Scholar
  200. Singh KK, Park KJ, Hong EJ et al. (2008) Developmental axon pruning mediated by BDNF-p75NTR-dependent axon degeneration. Nat Neurosci 11:649–658PubMedCrossRefGoogle Scholar
  201. Snider WD and Lichtman JW (1996) Are neurotrophins synaptotrophins? Mol Cell Neurosci 7:433–442PubMedCrossRefGoogle Scholar
  202. Song JY, Ichtchenko K, Südhof TC et al. (1999) Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc Natl Acad Sci USA 96:1100–1105PubMedCrossRefGoogle Scholar
  203. Srihari T and Vrbova G (1978) The role of muscle activity in the differentiation of neuromuscular junctions in slow and fast chick muscles. J Neurocytol 7:529–540PubMedCrossRefGoogle Scholar
  204. Srinivasan J, Schachner M and Catterall WA (1998) Interaction of voltage-gated sodium channels with the extracellular matrix molecules tenascin-C and tenascin-R. Proc Natl Acad Sci USA 95:15753–15757PubMedCrossRefGoogle Scholar
  205. Stellwagen D and Shatz CJ (2002) An instructive role for retinal waves in the development of retinogeniculate connectivity. Neuron 33:357–367PubMedCrossRefGoogle Scholar
  206. Stevens B, Allen NJ, Vazquez LE et al. (2007) The classical complement cascade mediates CNS synapse elimination. Cell 131:1164–1178PubMedCrossRefGoogle Scholar
  207. Südhof TC (2008) Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455:903–911PubMedCrossRefGoogle Scholar
  208. Sur M and Leamey CA (2001) Development and plasticity of cortical areas and networks. Nat Rev Neurosci 2:251–262PubMedCrossRefGoogle Scholar
  209. Swanwick CC, Murthy NR and Kapur J (2006) Activity-dependent scaling of GABAergic synapse strength is regulated by brain-derived neurotrophic factor. Mol Cell Neurosci 31:481–492PubMedCrossRefGoogle Scholar
  210. Tang L, Hung CP and Schuman EM (1998) A role for the cadherin family of cell adhesion molecules in hippocampal long-term potentiation. Neuron 20:1165–1175PubMedCrossRefGoogle Scholar
  211. Tao HW and Poo M (2001) Retrograde signaling at central synapses. Proc Natl Acad Sci USA 98:11009–11015PubMedCrossRefGoogle Scholar
  212. Thach WT (2007) On the mechanism of cerebellar contributions to cognition. Cerebellum 6:163–167PubMedCrossRefGoogle Scholar
  213. Thiagarajan TC, Lindskog M and Tsien RW (2005) Adaptation to synaptic inactivity in hippocampal neurons. Neuron 47:725–737PubMedCrossRefGoogle Scholar
  214. Thompson RF (1990) Neural mechanisms of classical conditioning in mammals. Philos Trans R Soc Lond B Biol Sci 329:161–170PubMedCrossRefGoogle Scholar
  215. Thompson W and Jansen JK (1977) The extent of sprouting of remaining motor units in partly denervated immature and adult rat soleus muscle. Neuroscience 2:523–535PubMedCrossRefGoogle Scholar
  216. Thompson WJ (1983) Synapse elimination in neonatal rat muscle is sensitive to the pattern of muscle use. Nature 302:614–616PubMedCrossRefGoogle Scholar
  217. Thompson WJ, Kuffler DP and Jansen JKS (1979) The effect of prolonged reversible block of nerve impulses on the elimination of polyneuronal innervation of new-born rat skeletal muscle. Neuroscience 4:271–281PubMedCrossRefGoogle Scholar
  218. Turrigiano GG (1999) Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same. Trends Neurosci 22:221–227PubMedCrossRefGoogle Scholar
  219. Turrigiano GG, Leslie KR, Desai NS et al. (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391:892–896PubMedCrossRefGoogle Scholar
  220. Turrigiano GG and Nelson SB (2004) Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5:97–107PubMedCrossRefGoogle Scholar
  221. Walsh MK and Lichtman JW (2003) In vivo time-lapse imaging of synaptic takeover associated with naturally occurring synapse elimination. Neuron 37:67–73PubMedCrossRefGoogle Scholar
  222. Weimann JM, Zhang YA, Levin ME et al. (1999) Cortical neurons require Otx1 for the refinement of exuberant axonal projections to subcortical targets. Neuron 24:819–831PubMedCrossRefGoogle Scholar
  223. Wierenga CJ, Ibata K and Turrigiano GG (2005) Postsynaptic expression of homeostatic plasticity at neocortical synapses. J Neurosci 25:2895–2905PubMedCrossRefGoogle Scholar
  224. Wierenga CJ, Walsh MF and Turrigiano GG (2006) Temporal regulation of the expression locus of homeostatic plasticity. J Neurophysiol 96:2127–2133PubMedCrossRefGoogle Scholar
  225. Wiesel TN and Hubel DH (1963) Effects of Visual Deprivation on Morphology and Physiology of Cells in the Cats Lateral Geniculate Body. J Neurophysiol 26:978–993PubMedGoogle Scholar
  226. Windrem MS and Finlay BL (1991) Thalamic ablations and neocortical development: alterations of cortical cytoarchitecture and cell number. Cereb Cortex 1:230–240PubMedCrossRefGoogle Scholar
  227. Wong RO (1999) Retinal waves and visual system development. Annu Rev Neurosci 22:29–47PubMedCrossRefGoogle Scholar
  228. Xiao P, Bahr BA, Staubli U et al. (1991) Evidence that matrix recognition contributes to stabilization but not induction of LTP. Neuroreport 2:461–464PubMedCrossRefGoogle Scholar
  229. Xiao ZC, Ragsdale DS, Malhotra JD et al. (1999) Tenascin-R is a functional modulator of sodium channel beta subunits. J Biol Chem 274:26511–26517PubMedCrossRefGoogle Scholar
  230. Yates PA, Roskies AL, McLaughlin T et al. (2001) Topographic-specific axon branching controlled by ephrin-As is the critical event in retinotectal map development. J Neurosci 21:8548–8563PubMedGoogle Scholar
  231. Yue Y, Chen ZY, Gale NW et al. (2002) Mistargeting hippocampal axons by expression of a truncated Eph receptor. Proc Natl Acad Sci USA 99:10777–10782PubMedCrossRefGoogle Scholar
  232. Zakharenko SS, Zablow L and Siegelbaum SA (2001) Visualization of changes in presynaptic function during long-term synaptic plasticity. Nat Neurosci 4:711–717PubMedCrossRefGoogle Scholar
  233. Zhang W and Linden DJ (2003) The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat Rev Neurosci 4:885–900PubMedCrossRefGoogle Scholar
  234. Zucker RS (1989) Short-term synaptic plasticity. Annu Rev Neurosci 12:13–31PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Dipartimento di Neuroscienze – Sezione di FisiologiaIstituto Nazionale di Neuroscienze, Universita’ di TorinoTorinoItaly
  2. 2.Dipartimento di Scienze Neurologiche e della Visione, Sezione di FisiologiaUniversità di VeronaVeronaItalia

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