Biochemical Computation for Spine Structural Plasticity

Neuron

Volumn 87, Issue 1, 2015, Pages 63-75

  Nishiyama, Jun ^a   Yasuda, Ryohei ^a  

^a MAX PLANCK FLORIDA INSTITUTE FOR NEUROSCIENCE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM ION; CALMODULIN;

ACTIN FILAMENT; CALCIUM SIGNALING; CELL NUCLEUS; DENDRITIC SPINE; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC DENSITY; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REGULATORY MECHANISM; REVIEW; DENDRITE; HUMAN; LEARNING; PHYSIOLOGY; SIGNAL TRANSDUCTION;

DENDRITES; DENDRITIC SPINES; HUMANS; LEARNING; LONG-TERM POTENTIATION; NEURONAL PLASTICITY; SIGNAL TRANSDUCTION;

EID: 84937405392     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.05.043     Document Type: Review

References (153)

1. Aakalu G., Smith W.B., Nguyen N., Jiang C., Schuman E.M. Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron 2001, 30:489-502.
2. Abraham W.C. Metaplasticity: tuning synapses and networks for plasticity. Nat. Rev. Neurosci. 2008, 9:387.
3. Abraham W.C., Christie B.R., Logan B., Lawlor P., Dragunow M. Immediate early gene expression associated with the persistence of heterosynaptic long-term depression in the hippocampus. Proc. Natl. Acad. Sci. USA 1994, 91:10049-10053.
4. Adams J.P., Dudek S.M. Late-phase long-term potentiation: getting to the nucleus. Nat. Rev. Neurosci. 2005, 6:737-743.
5. Alberini C.M. Transcription factors in long-term memory and synaptic plasticity. Physiol. Rev. 2009, 89:121-145.
6. Araki Y., Zeng M., Zhang M., Huganir R.L. Rapid dispersion of SynGAP from synaptic spines triggers AMPA receptor insertion and spine enlargement during LTP. Neuron 2015, 85:173-189.
7. Araya R., Jiang J., Eisenthal K.B., Yuste R. The spine neck filters membrane potentials. Proc. Natl. Acad. Sci. USA 2006, 103:17961-17966.
8. Araya R., Vogels T.P., Yuste R. Activity-dependent dendritic spine neck changes are correlated with synaptic strength. Proc. Natl. Acad. Sci. USA 2014, 111:E2895-E2904.
9. Barbosa A.C., Kim M.S., Ertunc M., Adachi M., Nelson E.D., McAnally J., Richardson J.A., Kavalali E.T., Monteggia L.M., Bassel-Duby R., Olson E.N. MEF2C, a transcription factor that facilitates learning and memory by negative regulation of synapse numbers and function. Proc. Natl. Acad. Sci. USA 2008, 105:9391-9396.
10. Barral Y., Mermall V., Mooseker M.S., Snyder M. Compartmentalization of the cell cortex by septins is required for maintenance of cell polarity in yeast. Mol. Cell 2000, 5:841-851.
11. Bastrikova N., Gardner G.A., Reece J.M., Jeromin A., Dudek S.M. Synapse elimination accompanies functional plasticity in hippocampal neurons. Proc. Natl. Acad. Sci. USA 2008, 105:3123-3127.
12. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361:31-39.
13. Bliss T.V., Collingridge G.L. Expression of NMDA receptor-dependent LTP in the hippocampus: bridging the divide. Mol. Brain 2013, 6:5.
14. Bloodgood B.L., Sabatini B.L. Neuronal activity regulates diffusion across the neck of dendritic spines. Science 2005, 310:866-869.
15. Bloodgood B.L., Giessel A.J., Sabatini B.L. Biphasic synaptic Ca influx arising from compartmentalized electrical signals in dendritic spines. PLoS Biol. 2009, 7:e1000190.
16. Borgdorff A.J., Choquet D. Regulation of AMPA receptor lateral movements. Nature 2002, 417:649-653.
17. Bosch M., Castro J., Saneyoshi T., Matsuno H., Sur M., Hayashi Y. Structural and molecular remodeling of dendritic spine substructures during long-term potentiation. Neuron 2014, 82:444-459.
18. Branco T., Häusser M. The single dendritic branch as a fundamental functional unit in the nervous system. Curr. Opin. Neurobiol. 2010, 20:494-502.
19. Bredt D.S., Nicoll R.A. AMPA receptor trafficking at excitatory synapses. Neuron 2003, 40:361-379.
20. Butko M.T., Yang J., Geng Y., Kim H.J., Jeon N.L., Shu X., Mackey M.R., Ellisman M.H., Tsien R.Y., Lin M.Z. Fluorescent and photo-oxidizing TimeSTAMP tags track protein fates in light and electron microscopy. Nat. Neurosci. 2012, 15:1742-1751.
21. Buxbaum A.R., Wu B., Singer R.H. Single β-actin mRNA detection in neurons reveals a mechanism for regulating its translatability. Science 2014, 343:419-422.
22. Bywalez W.G., Patirniche D., Rupprecht V., Stemmler M., Herz A.V., Pálfi D., Rózsa B., Egger V. Local postsynaptic voltage-gated sodium channel activation in dendritic spines of olfactory bulb granule cells. Neuron 2015, 85:590-601.
23. Ch'ng T.H., Martin K.C. Synapse-to-nucleus signaling. Curr. Opin. Neurobiol. 2011, 21:345-352.
24. Ch'ng T.H., Uzgil B., Lin P., Avliyakulov N.K., O'Dell T.J., Martin K.C. Activity-dependent transport of the transcriptional coactivator CRTC1 from synapse to nucleus. Cell 2012, 150:207-221.
25. Chazeau A., Mehidi A., Nair D., Gautier J.J., Leduc C., Chamma I., Kage F., Kechkar A., Thoumine O., Rottner K., et al. Nanoscale segregation of actin nucleation and elongation factors determines dendritic spine protrusion. EMBO J. 2014, 33:2745-2764.
26. Cheng D., Hoogenraad C.C., Rush J., Ramm E., Schlager M.A., Duong D.M., Xu P., Wijayawardana S.R., Hanfelt J., Nakagawa T., et al. Relative and absolute quantification of postsynaptic density proteome isolated from rat forebrain and cerebellum. Mol. Cell. Proteomics 2006, 5:1158-1170.
27. Chowdhury S., Shepherd J.D., Okuno H., Lyford G., Petralia R.S., Plath N., Kuhl D., Huganir R.L., Worley P.F. Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron 2006, 52:445-459.
28. Cole C.J., Mercaldo V., Restivo L., Yiu A.P., Sekeres M.J., Han J.H., Vetere G., Pekar T., Ross P.J., Neve R.L., et al. MEF2 negatively regulates learning-induced structural plasticity and memory formation. Nat. Neurosci. 2012, 15:1255-1264.
29. Costa-Mattioli M., Sossin W.S., Klann E., Sonenberg N. Translational control of long-lasting synaptic plasticity and memory. Neuron 2009, 61:10-26.
30. Cracco J.B., Serrano P., Moskowitz S.I., Bergold P.J., Sacktor T.C. Protein synthesis-dependent LTP in isolated dendrites of CA1 pyramidal cells. Hippocampus 2005, 15:551-556.
31. Desmond N.L., Levy W.B. Synaptic correlates of associative potentiation/depression: an ultrastructural study in the hippocampus. Brain Res. 1983, 265:21-30.
32. Doyère V., Srebro B., Laroche S. Heterosynaptic LTD and depotentiation in the medial perforant path of the dentate gyrus in the freely moving rat. J. Neurophysiol. 1997, 77:571-578.
33. Engert F., Bonhoeffer T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 1999, 399:66-70.
34. Enoki R., Hu Y.L., Hamilton D., Fine A. Expression of long-term plasticity at individual synapses in hippocampus is graded, bidirectional, and mainly presynaptic: optical quantal analysis. Neuron 2009, 62:242-253.
35. Ewers H., Tada T., Petersen J.D., Racz B., Sheng M., Choquet D. A Septin-Dependent Diffusion Barrier at Dendritic Spine Necks. PLoS ONE 2014, 9:e113916.
36. Flavell S.W., Cowan C.W., Kim T.K., Greer P.L., Lin Y., Paradis S., Griffith E.C., Hu L.S., Chen C., Greenberg M.E. Activity-dependent regulation of MEF2 transcription factors suppresses excitatory synapse number. Science 2006, 311:1008-1012.
37. Frey U., Morris R.G. Synaptic tagging and long-term potentiation. Nature 1997, 385:533-536.
38. Frost N.A., Shroff H., Kong H., Betzig E., Blanpied T.A. Single-molecule discrimination of discrete perisynaptic and distributed sites of actin filament assembly within dendritic spines. Neuron 2010, 67:86-99.
39. Fu M., Yu X., Lu J., Zuo Y. Repetitive motor learning induces coordinated formation of clustered dendritic spines in vivo. Nature 2012, 483:92-95.
40. Fujii H., Inoue M., Okuno H., Sano Y., Takemoto-Kimura S., Kitamura K., Kano M., Bito H. Nonlinear decoding and asymmetric representation of neuronal input information by CaMKIIα and calcineurin. Cell Rep. 2013, 3:978-987.
41. Goldfarb D.S., Corbett A.H., Mason D.A., Harreman M.T., Adam S.A. Importin alpha: a multipurpose nuclear-transport receptor. Trends Cell Biol. 2004, 14:505-514.
42. Govindarajan A., Kelleher R.J., Tonegawa S. A clustered plasticity model of long-term memory engrams. Nat. Rev. Neurosci. 2006, 7:575-583.
43. 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.
44. Grunditz A., Holbro N., Tian L., Zuo Y., Oertner T.G. Spine neck plasticity controls postsynaptic calcium signals through electrical compartmentalization. J. Neurosci. 2008, 28:13457-13466.
45. Gu J., Lee C.W., Fan Y., Komlos D., Tang X., Sun C., Yu K., Hartzell H.C., Chen G., Bamburg J.R., Zheng J.Q. ADF/cofilin-mediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity. Nat. Neurosci. 2010, 13:1208-1215.
46. Guzowski J.F., Lyford G.L., Stevenson G.D., Houston F.P., McGaugh J.L., Worley P.F., Barnes C.A. Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J. Neurosci. 2000, 20:3993-4001.
47. Harnett M.T., Makara J.K., Spruston N., Kath W.L., Magee J.C. Synaptic amplification by dendritic spines enhances input cooperativity. Nature 2012, 491:599-602.
48. 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.
49. Harvey C.D., Svoboda K. Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature 2007, 450:1195-1200.
50. 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.
51. Hayama T., Noguchi J., Watanabe S., Takahashi N., Hayashi-Takagi A., Ellis-Davies G.C., Matsuzaki M., Kasai H. GABA promotes the competitive selection of dendritic spines by controlling local Ca2+ signaling. Nat. Neurosci. 2013, 16:1409-1416.
52. Hill T.C., Zito K. LTP-induced long-term stabilization of individual nascent dendritic spines. J. Neurosci. 2013, 33:678-686.
53. Holtmaat A., Wilbrecht L., Knott G.W., Welker E., Svoboda K. Experience-dependent and cell-type-specific spine growth in the neocortex. Nature 2006, 441:979-983.
54. 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.
55. Huber K.M., Kayser M.S., Bear M.F. Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 2000, 288:1254-1257.
56. Huganir R.L., Nicoll R.A. AMPARs and synaptic plasticity: the last 25 years. Neuron 2013, 80:704-717.
57. Jeffrey R.A., Ch'ng T.H., O'Dell T.J., Martin K.C. Activity-dependent anchoring of importin alpha at the synapse involves regulated binding to the cytoplasmic tail of the NR1-1a subunit of the NMDA receptor. J. Neurosci. 2009, 29:15613-15620.
58. Jordan B.A., Kreutz M.R. Nucleocytoplasmic protein shuttling: the direct route in synapse-to-nucleus signaling. Trends Neurosci. 2009, 32:392-401.
59. Kang H., Schuman E.M. A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 1996, 273:1402-1406.
60. Karpova A., Mikhaylova M., Bera S., Bär J., Reddy P.P., Behnisch T., Rankovic V., Spilker C., Bethge P., Sahin J., et al. Encoding and transducing the synaptic or extrasynaptic origin of NMDA receptor signals to the nucleus. Cell 2013, 152:1119-1133.
61. Kelleher R.J., Govindarajan A., Jung H.Y., Kang H., Tonegawa S. Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 2004, 116:467-479.
62. Kennedy M.J., Hughes R.M., Peteya L.A., Schwartz J.W., Ehlers M.D., Tucker C.L. Rapid blue-light-mediated induction of protein interactions in living cells. Nat. Methods 2010, 7:973-975.
63. Kim C.H., Lisman J.E. A role of actin filament in synaptic transmission and long-term potentiation. J. Neurosci. 1999, 19:4314-4324.
64. Kim I.H., Racz B., Wang H., Burianek L., Weinberg R., Yasuda R., Wetsel W.C., Soderling S.H. Disruption of Arp2/3 results in asymmetric structural plasticity of dendritic spines and progressive synaptic and behavioral abnormalities. J. Neurosci. 2013, 33:6081-6092.
65. Kim I.H., Wang H., Soderling S.H., Yasuda R. Loss of Cdc42 leads to defects in synaptic plasticity and remote memory recall. eLife 2014, 3:3.
66. Kleindienst T., Winnubst J., Roth-Alpermann C., Bonhoeffer T., Lohmann C. Activity-dependent clustering of functional synaptic inputs on developing hippocampal dendrites. Neuron 2011, 72:1012-1024.
67. 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.
68. Korobova F., Svitkina T. Molecular architecture of synaptic actin cytoskeleton in hippocampal neurons reveals a mechanism of dendritic spine morphogenesis. Mol. Biol. Cell 2010, 21:165-176.
69. Kovács K.A., Steullet P., Steinmann M., Do K.Q., Magistretti P.J., Halfon O., Cardinaux J.R. TORC1 is a calcium- and cAMP-sensitive coincidence detector involved in hippocampal long-term synaptic plasticity. Proc. Natl. Acad. Sci. USA 2007, 104:4700-4705.
70. Kovalchuk Y., Eilers J., Lisman J., Konnerth A. NMDA receptor-mediated subthreshold Ca(2+) signals in spines of hippocampal neurons. J. Neurosci. 2000, 20:1791-1799.
71. 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.
72. Kuroda S., Schweighofer N., Kawato M. Exploration of signal transduction pathways in cerebellar long-term depression by kinetic simulation. J. Neurosci. 2001, 21:5693-5702.
73. Kwon H.B., Sabatini B.L. Glutamate induces de novo growth of functional spines in developing cortex. Nature 2011, 474:100-104.
74. Lai C.S., Franke T.F., Gan W.B. Opposite effects of fear conditioning and extinction on dendritic spine remodelling. Nature 2012, 483:87-91.
75. Lang C., Barco A., Zablow L., Kandel E.R., Siegelbaum S.A., Zakharenko S.S. Transient expansion of synaptically connected dendritic spines upon induction of hippocampal long-term potentiation. Proc. Natl. Acad. Sci. USA 2004, 101:16665-16670.
76. Larkum M.E., Nevian T. Synaptic clustering by dendritic signalling mechanisms. Curr. Opin. Neurobiol. 2008, 18:321-331.
77. Lee S.J., Escobedo-Lozoya Y., Szatmari E.M., Yasuda R. Activation of CaMKII in single dendritic spines during long-term potentiation. Nature 2009, 458:299-304.
78. Lee S., Park H., Kyung T., Kim N.Y., Kim S., Kim J., Heo W.D. Reversible protein inactivation by optogenetic trapping in cells. Nat. Methods 2014, 11:633-636.
79. Levskaya A., Weiner O.D., Lim W.A., Voigt C.A. Spatiotemporal control of cell signalling using a light-switchable protein interaction. Nature 2009, 461:997-1001.
80. Lin M.Z., Glenn J.S., Tsien R.Y. A drug-controllable tag for visualizing newly synthesized proteins in cells and whole animals. Proc. Natl. Acad. Sci. USA 2008, 105:7744-7749.
81. Lisman J., Yasuda R., Raghavachari S. Mechanisms of CaMKII action in long-term potentiation. Nat. Rev. Neurosci. 2012, 13:169-182.
82. Mainen Z.F., Malinow R., Svoboda K. Synaptic calcium transients in single spines indicate that NMDA receptors are not saturated. Nature 1999, 399:151-155.
83. Makino H., Malinow R. Compartmentalized versus global synaptic plasticity on dendrites controlled by experience. Neuron 2011, 72:1001-1011.
84. Maletic-Savatic M., Malinow R., Svoboda K. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 1999, 283:1923-1927.
85. 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.
86. Matsuzaki M., Honkura N., Ellis-Davies G.C., Kasai H. Structural basis of long-term potentiation in single dendritic spines. Nature 2004, 429:761-766.
87. Meyer D., Bonhoeffer T., Scheuss V. Balance and stability of synaptic structures during synaptic plasticity. Neuron 2014, 82:430-443.
88. Moczulska K.E., Tinter-Thiede J., Peter M., Ushakova L., Wernle T., Bathellier B., Rumpel S. Dynamics of dendritic spines in the mouse auditory cortex during memory formation and memory recall. Proc. Natl. Acad. Sci. USA 2013, 110:18315-18320.
89. Murakoshi H., Wang H., Yasuda R. Local, persistent activation of Rho GTPases during plasticity of single dendritic spines. Nature 2011, 472:100-104.
90. Nägerl U.V., Eberhorn N., Cambridge S.B., Bonhoeffer T. Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron 2004, 44:759-767.
91. Nagerl U.V., Kostinger G., Anderson J.C., Martin K.A., Bonhoeffer T. Protracted synaptogenesis after activity-dependent spinogenesis in hippocampal neurons. J. Neurosci. 2007, 27:8149-8156.
92. Noguchi J., Matsuzaki M., Ellis-Davies G.C., Kasai H. Spine-neck geometry determines NMDA receptor-dependent Ca2+ signaling in dendrites. Neuron 2005, 46:609-622.
93. Nonaka M., Kim R., Fukushima H., Sasaki K., Suzuki K., Okamura M., Ishii Y., Kawashima T., Kamijo S., Takemoto-Kimura S., et al. Region-specific activation of CRTC1-CREB signaling mediates long-term fear memory. Neuron 2014, 84:92-106.
94. Oh W.C., Hill T.C., Zito K. Synapse-specific and size-dependent mechanisms of spine structural plasticity accompanying synaptic weakening. Proc. Natl. Acad. Sci. USA 2013, 110:E305-E312.
95. Oh W.C., Parajuli L.K., Zito K. Heterosynaptic structural plasticity on local dendritic segments of hippocampal CA1 neurons. Cell Rep. 2015, 10:162-169.
96. Okada D., Ozawa F., Inokuchi K. Input-specific spine entry of soma-derived Vesl-1S protein conforms to synaptic tagging. Science 2009, 324:904-909.
97. 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.
98. Okamoto K., Bosch M., Hayashi Y. The roles of CaMKII and F-actin in the structural plasticity of dendritic spines: a potential molecular identity of a synaptic tag?. Physiology (Bethesda) 2009, 24:357-366.
99. Okuno H., Akashi K., Ishii Y., Yagishita-Kyo N., Suzuki K., Nonaka M., Kawashima T., Fujii H., Takemoto-Kimura S., Abe M., et al. Inverse synaptic tagging of inactive synapses via dynamic interaction of Arc/Arg3.1 with CaMKIIβ. Cell 2012, 149:886-898.
100. Oliveira A.F., Yasuda R. Neurofibromin is the major ras inactivator in dendritic spines. J. Neurosci. 2014, 34:776-783.
101. Ostroff L.E., Fiala J.C., Allwardt B., Harris K.M. Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices. Neuron 2002, 35:535-545.
102. Park M., Salgado J.M., Ostroff L., Helton T.D., Robinson C.G., Harris K.M., Ehlers M.D. Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes. Neuron 2006, 52:817-830.
103. Patterson M.A., Szatmari E.M., Yasuda R. AMPA receptors are exocytosed in stimulated spines and adjacent dendrites in a Ras-ERK-dependent manner during long-term potentiation. Proc. Natl. Acad. Sci. USA 2010, 107:15951-15956.
104. Plath N., Ohana O., Dammermann B., Errington M.L., Schmitz D., Gross C., Mao X., Engelsberg A., Mahlke C., Welzl H., et al. Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 2006, 52:437-444.
105. Ploski J.E., Pierre V.J., Smucny J., Park K., Monsey M.S., Overeem K.A., Schafe G.E. The activity-regulated cytoskeletal-associated protein (Arc/Arg3.1) is required for memory consolidation of pavlovian fear conditioning in the lateral amygdala. J. Neurosci. 2008, 28:12383-12395.
106. Pulipparacharuvil S., Renthal W., Hale C.F., Taniguchi M., Xiao G., Kumar A., Russo S.J., Sikder D., Dewey C.M., Davis M.M., et al. Cocaine regulates MEF2 to control synaptic and behavioral plasticity. Neuron 2008, 59:621-633.
107. Racz B., Weinberg R.J. Organization of the Arp2/3 complex in hippocampal spines. The J. Neurosci. 2008, 28:5654-5659.
108. Ramachandran B., Frey J.U. Interfering with the actin network and its effect on long-term potentiation and synaptic tagging in hippocampal CA1 neurons in slices in vitro. J. Neurosci. 2009, 29:12167-12173.
109. Redondo R.L., Morris R.G. Making memories last: the synaptic tagging and capture hypothesis. Nat. Rev. Neurosci. 2011, 12:17-30.
110. Sabatini B.L., Oertner T.G., Svoboda K. The life cycle of Ca(2+) ions in dendritic spines. Neuron 2002, 33:439-452.
111. Schikorski T., Stevens C.F. Quantitative ultrastructural analysis of hippocampal excitatory synapses. J. Neurosci. 1997, 17:5858-5867.
112. Sdrulla A.D., Linden D.J. Double dissociation between long-term depression and dendritic spine morphology in cerebellar Purkinje cells. Nat. Neurosci. 2007, 10:546-548.
113. Segev I., Rall W. Computational study of an excitable dendritic spine. J. Neurophysiol. 1988, 60:499-523.
114. Smith K.R., Kopeikina K.J., Fawcett-Patel J.M., Leaderbrand K., Gao R., Schürmann B., Myczek K., Radulovic J., Swanson G.T., Penzes P. Psychiatric risk factor ANK3/ankyrin-G nanodomains regulate the structure and function of glutamatergic synapses. Neuron 2014, 84:399-415.
115. Sobczyk A., Svoboda K. Activity-dependent plasticity of the NMDA-receptor fractional Ca2+ current. Neuron 2007, 53:17-24.
116. 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.
117. 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.
118. Steward O., Levy W.B. Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus. J. Neurosci. 1982, 2:284-291.
119. Sutton M.A., Schuman E.M. Dendritic protein synthesis, synaptic plasticity, and memory. Cell 2006, 127:49-58.
120. Svoboda K., Tank D.W., Denk W. Direct measurement of coupling between dendritic spines and shafts. Science 1996, 272:716-719.
121. Tada T., Simonetta A., Batterton M., Kinoshita M., Edbauer D., Sheng M. Role of Septin cytoskeleton in spine morphogenesis and dendrite development in neurons. Curr. Biol. 2007, 17:1752-1758.
122. Takahashi N., Kitamura K., Matsuo N., Mayford M., Kano M., Matsuki N., Ikegaya Y. Locally synchronized synaptic inputs. Science 2012, 335:353-356.
123. 2+ /calmodulin-dependent protein kinase II activity in living neurons. J. Neurosci. 2005, 25:3107-3112.
124. Takizawa P.A., DeRisi J.L., Wilhelm J.E., Vale R.D. Plasma membrane compartmentalization in yeast by messenger RNA transport and a septin diffusion barrier. Science 2000, 290:341-344.
125. 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.
126. Tanaka K., Augustine G.J. A positive feedback signal transduction loop determines timing of cerebellar long-term depression. Neuron 2008, 59:608-620.
127. 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.
128. Thompson K.R., Otis K.O., Chen D.Y., Zhao Y., O'Dell T.J., Martin K.C. Synapse to nucleus signaling during long-term synaptic plasticity; a role for the classical active nuclear import pathway. Neuron 2004, 44:997-1009.
129. Toni N., Buchs P.A., Nikonenko I., Bron C.R., Muller D. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 1999, 402:421-425.
130. Tønnesen J., Katona G., Rózsa B., Nägerl U.V. Spine neck plasticity regulates compartmentalization of synapses. Nat. Neurosci. 2014, 17:678-685.
131. Tyszkiewicz A.B., Muir T.W. Activation of protein splicing with light in yeast. Nat. Methods 2008, 5:303-305.
132. 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.
133. Wang X.B., Yang Y., Zhou Q. Independent expression of synaptic and morphological plasticity associated with long-term depression. J. Neurosci. 2007, 27:12419-12429.
134. Wiegert J.S., Oertner T.G. Long-term depression triggers the selective elimination of weakly integrated synapses. Proc. Natl. Acad. Sci. USA 2013, 110:E4510-E4519.
135. Wu Y.I., Frey D., Lungu O.I., Jaehrig A., Schlichting I., Kuhlman B., Hahn K.M. A genetically encoded photoactivatable Rac controls the motility of living cells. Nature 2009, 461:104-108.
136. Xie Y., Vessey J.P., Konecna A., Dahm R., Macchi P., Kiebler M.A. The GTP-binding protein Septin 7 is critical for dendrite branching and dendritic-spine morphology. Curr. Biol. 2007, 17:1746-1751.
137. Xu T., Yu X., Perlik A.J., Tobin W.F., Zweig J.A., Tennant K., Jones T., Zuo Y. Rapid formation and selective stabilization of synapses for enduring motor memories. Nature 2009, 462:915-919.
138. Yang G., Pan F., Gan W.B. Stably maintained dendritic spines are associated with lifelong memories. Nature 2009, 462:920-924.
139. Yasuda R. Imaging spatiotemporal dynamics of neuronal signaling using fluorescence resonance energy transfer and fluorescence lifetime imaging microscopy. Curr. Opin. Neurobiol. 2006, 16:551-561.
140. Yasuda R. Studying signal transduction in single dendritic spines. Cold Spring Harb. Perspect. Biol. 2012, 4:4.
141. Yasuda R., Murakoshi H. The mechanisms underlying the spatial spreading of signaling activity. Curr. Opin. Neurobiol. 2011, 21:313-321.
142. Yasuda R., Harvey C.D., Zhong H., Sobczyk A., van Aelst L., Svoboda K. Supersensitive Ras activation in dendrites and spines revealed by two-photon fluorescence lifetime imaging. Nat. Neurosci. 2006, 9:283-291.
143. Yazawa M., Sadaghiani A.M., Hsueh B., Dolmetsch R.E. Induction of protein-protein interactions in live cells using light. Nat. Biotechnol. 2009, 27:941-945.
144. Yuste R. Dendritic spines and distributed circuits. Neuron 2011, 71:772-781.
145. Yuste R. Electrical compartmentalization in dendritic spines. Annu. Rev. Neurosci. 2013, 36:429-449.
146. Yuste R., Denk W. Dendritic spines as basic functional units of neuronal integration. Nature 1995, 375:682-684.
147. Zakharenko S.S., Zablow L., Siegelbaum S.A. Visualization of changes in presynaptic function during long-term synaptic plasticity. Nat. Neurosci. 2001, 4:711-717.
148. Zhai S., Ark E.D., Parra-Bueno P., Yasuda R. Long-distance integration of nuclear ERK signaling triggered by activation of a few dendritic spines. Science 2013, 342:1107-1111.
149. Zhang Y., Cudmore R.H., Lin D.T., Linden D.J., Huganir R.L. Visualization of NMDA receptor-dependent AMPA receptor synaptic plasticity in vivo. Nat. Neurosci. 2015, 18:402-407.
150. Zhou Q., Homma K.J., Poo M.M. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 2004, 44:749-757.
151. Zhou Y., Wu H., Li S., Chen Q., Cheng X.W., Zheng J., Takemori H., Xiong Z.Q. Requirement of TORC1 for late-phase long-term potentiation in the hippocampus. PLoS ONE 2006, 1:e16.
152. Zhou X.X., Chung H.K., Lam A.J., Lin M.Z. Optical control of protein activity by fluorescent protein domains. Science 2012, 338:810-814.
153. Zhu J.J., Qin Y., Zhao M., Van Aelst L., Malinow R. Ras and Rap control AMPA receptor trafficking during synaptic plasticity. Cell 2002, 110:443-455.