Balance and stability of synaptic structures during synaptic plasticity

Neuron

Volumn 82, Issue 2, 2014, Pages 430-443

  Meyer, Daniel ^a   Bonhoeffer, Tobias ^a   Scheuss, Volker ^a  

^a MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; ANIMALS, NEWBORN; CA1 REGION, HIPPOCAMPAL; CARRIER PROTEINS; DENDRITIC SPINES; GLUTAMIC ACID; GREEN FLUORESCENT PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; NEURONAL PLASTICITY; NEURONS; ORGAN CULTURE TECHNIQUES; PLANT LECTINS; POST-SYNAPTIC DENSITY; RATS; RATS, WISTAR; SYNAPSES; TIME FACTORS; TRANSDUCTION, GENETIC;

EID: 84898685224     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.02.031     Document Type: Article

References (72)

1. Abraham W.C., Williams J.M. Properties and mechanisms of LTP maintenance. Neuroscientist 2003, 9:463-474.
2. Arellano J.I., Benavides-Piccione R., Defelipe J., Yuste R. Ultrastructure of dendritic spines: correlation between synaptic and spine morphologies. Front. Neurosci. 2007, 1:131-143.
3. Becker N., Wierenga C.J., Fonseca R., Bonhoeffer T., Nägerl U.V. LTD induction causes morphological changes of presynaptic boutons and reduces their contacts with spines. Neuron 2008, 60:590-597.
4. Benson D.L., Huntley G.W. Synapse adhesion: a dynamic equilibrium conferring stability and flexibility. Curr. Opin. Neurobiol. 2012, 22:397-404.
5. Blanpied T.A., Kerr J.M., Ehlers M.D. Structural plasticity with preserved topology in the postsynaptic protein network. Proc. Natl. Acad. Sci. USA 2008, 105:12587-12592.
6. Bozdagi O., Shan W., Tanaka H., Benson D.L., Huntley G.W. Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation. Neuron 2000, 28:245-259.
7. Bozdagi O., Wang X.B., Nikitczuk J.S., Anderson T.R., Bloss E.B., Radice G.L., Zhou Q., Benson D.L., Huntley G.W. Persistence of coordinated long-term potentiation and dendritic spine enlargement at mature hippocampal CA1 synapses requires N-cadherin. J.Neurosci. 2010, 30:9984-9989.
8. Chen X., Winters C., Azzam R., Li X., Galbraith J.A., Leapman R.D., Reese T.S. Organization of the core structure of the postsynaptic density. Proc. Natl. Acad. Sci. USA 2008, 105:4453-4458.
9. Dalva M.B., McClelland A.C., Kayser M.S. Cell adhesion molecules: signalling functions at the synapse. Nat. Rev. Neurosci. 2007, 8:206-220.
10. Desmond N.L., Levy W.B. Synaptic correlates of associative potentiation/depression: an ultrastructural study in the hippocampus. Brain Res. 1983, 265:21-30.
11. Desmond N.L., Levy W.B. Changes in the postsynaptic density with long-term potentiation in the dentate gyrus. J.Comp. Neurol. 1986, 253:476-482.
12. Desmond N.L., Levy W.B. Synaptic interface surface area increases with long-term potentiation in the hippocampal dentate gyrus. Brain Res. 1988, 453:308-314.
13. Ehrlich I., Klein M., Rumpel S., Malinow R. PSD-95 is required for activity-driven synapse stabilization. Proc. Natl. Acad. Sci. USA 2007, 104:4176-4181.
14. Engert F., Bonhoeffer T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 1999, 399:66-70.
15. Fonseca R., Nägerl U.V., Morris R.G., Bonhoeffer T. Competing for memory: hippocampal LTP under regimes of reduced protein synthesis. Neuron 2004, 44:1011-1020.
16. Futai K., Kim M.J., Hashikawa T., Scheiffele P., Sheng M., Hayashi Y. Retrograde modulation of presynaptic release probability through signaling mediated by PSD-95-neuroligin. Nat. Neurosci. 2007, 10:186-195.
17. Govindarajan A., Israely I., Huang S.Y., Tonegawa S. The dendritic branch is the preferred integrative unit for protein synthesis-dependent LTP. Neuron 2011, 69:132-146.
18. Grunwald I.C., Korte M., Adelmann G., Plueck A., Kullander K., Adams R.H., Frotscher M., Bonhoeffer T., Klein R. Hippocampal plasticity requires postsynaptic ephrinBs. Nat. Neurosci. 2004, 7:33-40.
19. Gundelfinger E.D., Fejtova A. Molecular organization and plasticity of the cytomatrix at the active zone. Curr. Opin. Neurobiol. 2012, 22:423-430.
20. Harris K.M., Stevens J.K. Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J.Neurosci. 1989, 9:2982-2997.
21. Harvey C.D., Svoboda K. Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature 2007, 450:1195-1200.
22. Harvey C.D., Yasuda R., Zhong H., Svoboda K. The spread of Ras activity triggered by activation of a single dendritic spine. Science 2008, 321:136-140.
23. Hayashi M.K., Tang C., Verpelli C., Narayanan R., Stearns M.H., Xu R.M., Li H., Sala C., Hayashi Y. The postsynaptic density proteins Homer and Shank form a polymeric network structure. Cell 2009, 137:159-171.
24. Hering H., Sheng M. Dendritic spines: structure, dynamics and regulation. Nat. Rev. Neurosci. 2001, 2:880-888.
25. Honkura N., Matsuzaki M., Noguchi J., Ellis-Davies G.C., Kasai H. The subspine organization of actin fibers regulates the structure and plasticity of dendritic spines. Neuron 2008, 57:719-729.
26. Hosokawa T., Rusakov D.A., Bliss T.V., Fine A. Repeated confocal imaging of individual dendritic spines in the living hippocampal slice: evidence for changes in length and orientation associated with chemically induced LTP. J.Neurosci. 1995, 15:5560-5573.
27. Inoue Y., Udo H., Inokuchi K., Sugiyama H. Homer1a regulates the activity-induced remodeling of synaptic structures in cultured hippocampal neurons. Neuroscience 2007, 150:841-852.
28. Kasai H., Hayama T., Ishikawa M., Watanabe S., Yagishita S., Noguchi J. Learning rules and persistence of dendritic spines. Eur. J. Neurosci. 2010, 32:241-249.
29. Kopec C.D., Real E., Kessels H.W., Malinow R. GluR1 links structural and functional plasticity at excitatory synapses. J.Neurosci. 2007, 27:13706-13718.
30. Kramár E.A., Lin B., Rex C.S., Gall C.M., Lynch G. Integrin-driven actin polymerization consolidates long-term potentiation. Proc. Natl. Acad. Sci. USA 2006, 103:5579-5584.
31. Krucker T., Siggins G.R., Halpain S. Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus. Proc. Natl. Acad. Sci. USA 2000, 97:6856-6861.
32. Kuriu T., Inoue A., Bito H., Sobue K., Okabe S. Differential control of postsynaptic density scaffolds via actin-dependent and -independent mechanisms. J.Neurosci. 2006, 26:7693-7706.
33. Lisman J., Raghavachari S. A unified model of the presynaptic and postsynaptic changes during LTP at CA1 synapses. Sci. STKE 2006, 2006:re11.
34. Malenka R.C., Bear M.F. LTP and LTD: an embarrassment of riches. Neuron 2004, 44:5-21.
35. Maletic-Savatic M., Malinow R., Svoboda K. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 1999, 283:1923-1927.
36. Malinow R., Malenka R.C. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 2002, 25:103-126.
37. Marrone D.F., Petit T.L. The role of synaptic morphology in neural plasticity: structural interactions underlying synaptic power. Brain Res. Brain Res. Rev. 2002, 38:291-308.
38. Matsuzaki M., Ellis-Davies G.C., Nemoto T., Miyashita Y., Iino M., Kasai H. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 2001, 4:1086-1092.
39. Matsuzaki M., Honkura N., Ellis-Davies G.C.R., Kasai H. Structural basis of long-term potentiation in single dendritic spines. Nature 2004, 429:761-766.
40. Mendez P., De Roo M., Poglia L., Klauser P., Muller D. N-cadherin mediates plasticity-induced long-term spine stabilization. J.Cell Biol. 2010, 189:589-600.
41. Murakoshi H., Yasuda R. Postsynaptic signaling during plasticity of dendritic spines. Trends Neurosci. 2012, 35:135-143.
42. Murthy V.N., Schikorski T., Stevens C.F., Zhu Y. Inactivity produces increases in neurotransmitter release and synapse size. Neuron 2001, 32:673-682.
43. Nikonenko I., Boda B., Steen S., Knott G., Welker E., Muller D. PSD-95 promotes synaptogenesis and multiinnervated spine formation through nitric oxide signaling. J.Cell Biol. 2008, 183:1115-1127.
44. Nusser Z., Lujan R., Laube G., Roberts J.D., Molnar E., Somogyi P. Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 1998, 21:545-559.
45. Okabe S. Molecular dynamics of the excitatory synapse. Synaptic Plasticity 2012, 131-152. Springer, Vienna. M.R. Kreutz, C. Sala (Eds.).
46. Okabe S., Miwa A., Okado H. Spine formation and correlated assembly of presynaptic and postsynaptic molecules. J.Neurosci. 2001, 21:6105-6114.
47. Okamoto K., Nagai T., Miyawaki A., Hayashi Y. Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat. Neurosci. 2004, 7:1104-1112.
48. Opazo P., Sainlos M., Choquet D. Regulation of AMPA receptor surface diffusion by PSD-95 slots. Curr. Opin. Neurobiol. 2012, 22:453-460.
49. Petralia R.S., Sans N., Wang Y.X., Wenthold R.J. Ontogeny of postsynaptic density proteins at glutamatergic synapses. Mol. Cell. Neurosci. 2005, 29:436-452.
50. Petrini E.M., Lu J., Cognet L., Lounis B., Ehlers M.D., Choquet D. Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation. Neuron 2009, 63:92-105.
51. Redondo R.L., Morris R.G. Making memories last: the synaptic tagging and capture hypothesis. Nat. Rev. Neurosci. 2011, 12:17-30.
52. Regalado M.P., Terry-Lorenzo R.T., Waites C.L., Garner C.C., Malenka R.C. Transsynaptic signaling by postsynaptic synapse-associated protein 97. J.Neurosci. 2006, 26:2343-2357.
53. Sala C., Piëch V., Wilson N.R., Passafaro M., Liu G., Sheng M. Regulation of dendritic spine morphology and synaptic function by Shank and Homer. Neuron 2001, 31:115-130.
54. Schikorski T., Stevens C.F. Quantitative fine-structural analysis of olfactory cortical synapses. Proc. Natl. Acad. Sci. USA 1999, 96:4107-4112.
55. Shapira M., Zhai R.G., Dresbach T., Bresler T., Torres V.I., Gundelfinger E.D., Ziv N.E., Garner C.C. Unitary assembly of presynaptic active zones from Piccolo-Bassoon transport vesicles. Neuron 2003, 38:237-252.
56. Sheng M., Hoogenraad C.C. The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu. Rev. Biochem. 2007, 76:823-847.
57. Shepherd G.M., Harris K.M. Three-dimensional structure and composition of CA3->CA1 axons in rat hippocampal slices: implications for presynaptic connectivity and compartmentalization. J.Neurosci. 1998, 18:8300-8310.
58. Sorra K.E., Harris K.M. Stability in synapse number and size at 2hr after long-term potentiation in hippocampal area CA1. J.Neurosci. 1998, 18:658-671.
59. Star E.N., Kwiatkowski D.J., Murthy V.N. Rapid turnover of actin in dendritic spines and its regulation by activity. Nat. Neurosci. 2002, 5:239-246.
60. Steiner P., Higley M.J., Xu W., Czervionke B.L., Malenka R.C., Sabatini B.L. Destabilization of the postsynaptic density by PSD-95 serine 73 phosphorylation inhibits spine growth and synaptic plasticity. Neuron 2008, 60:788-802.
61. Stewart M.G., Medvedev N.I., Popov V.I., Schoepfer R., Davies H.A., Murphy K., Dallérac G.M., Kraev I.V., Rodríguez J.J. Chemically induced long-term potentiation increases the number of perforated and complex postsynaptic densities but does not alter dendritic spine volume in CA1 of adult mouse hippocampal slices. Eur. J. Neurosci. 2005, 21:3368-3378.
62. Sturgill J.F., Steiner P., Czervionke B.L., Sabatini B.L. Distinct domains within PSD-95 mediate synaptic incorporation, stabilization, and activity-dependent trafficking. J.Neurosci. 2009, 29:12845-12854.
63. Takumi Y., Ramírez-León V., Laake P., Rinvik E., Ottersen O.P. Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat. Neurosci. 1999, 2:618-624.
64. Tanaka J., Horiike Y., Matsuzaki M., Miyazaki T., Ellis-Davies G.C., Kasai H. Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines. Science 2008, 319:1683-1687.
65. Valtschanoff J.G., Weinberg R.J. Laminar organization of the NMDA receptor complex within the postsynaptic density. J.Neurosci. 2001, 21:1211-1217.
66. Van Harreveld A., Fifkova E. Swelling of dendritic spines in the fascia dentata after stimulation of the perforant fibers as a mechanism of post-tetanic potentiation. Exp. Neurol. 1975, 49:736-749.
67. Watt A.J., Sjöström P.J., Häusser M., Nelson S.B., Turrigiano G.G. A proportional but slower NMDA potentiation follows AMPA potentiation in LTP. Nat. Neurosci. 2004, 7:518-524.
68. Weed S.A., Karginov A.V., Schafer D.A., Weaver A.M., Kinley A.W., Cooper J.A., Parsons J.T. Cortactin localization to sites of actin assembly in lamellipodia requires interactions with F-actin and the Arp2/3 complex. J.Cell Biol. 2000, 151:29-40.
69. Xie Z., Srivastava D.P., Photowala H., Kai L., Cahill M.E., Woolfrey K.M., Shum C.Y., Surmeier D.J., Penzes P. Kalirin-7 controls activity-dependent structural and functional plasticity of dendritic spines. Neuron 2007, 56:640-656.
70. Yoshihara Y., De Roo M., Muller D. Dendritic spine formation and stabilization. Curr. Opin. Neurobiol. 2009, 19:146-153.
71. Yuste R., Bonhoeffer T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu. Rev. Neurosci. 2001, 24:1071-1089.
72. Zhang P., Lisman J.E. Activity-dependent regulation of synaptic strength by PSD-95 in CA1 neurons. J.Neurophysiol. 2012, 107:1058-1066.