Dynamics of nascent and active zone ultrastructure as synapses enlarge during long-term potentiation in mature hippocampus

Journal of Comparative Neurology

Volumn 522, Issue 17, 2014, Pages 3861-3884

  Bell, Maria Elizabeth ^a   Bourne, Jennifer N ^a,b   Chirillo, Michael A ^a,c   Mendenhall, John M ^a   Kuwajima, Masaaki ^a   Harris, Kristen M ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Long term potentiation; Postsynaptic density; Reconstruction; RRID:AB_1769134; RRID:AB_2113447; RRID:nif 0000 23420; RRID:nif 0000 31686; Serial section electron microscopy; Synaptic plasticity; Synaptic vesicles

Indexed keywords

GLUTAMATE RECEPTOR; GLUTAMIC ACID; AMPA RECEPTOR; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 1;

ACTIVE ZONE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CELL VACUOLE; CONTROLLED STUDY; DENDRITIC SPINE; ELECTRON MICROSCOPY; ELECTRON TOMOGRAPHY; HIPPOCAMPUS; HIPPOCAMPUS THETA RHYTHM; IMMUNOGOLD LABELING; IN VIVO STUDY; LONG TERM POTENTIATION; MALE; NASCENT ZONE; NONHUMAN; POSTSYNAPTIC DENSITY; PRESYNAPTIC NERVE; PRESYNAPTIC VESICLE; PRIORITY JOURNAL; PROTEIN TRANSPORT; RAT; STOCHASTIC MODEL; SYNAPSE; TISSUE FIXATION; ANALYSIS OF VARIANCE; ANIMAL; BIOPHYSICS; CYTOLOGY; DENDRITE; ELECTROSTIMULATION; IN VITRO STUDY; METABOLISM; NEWBORN; PHYSIOLOGY; SECRETORY VESICLE; SYNAPTOSOME; THREE DIMENSIONAL IMAGING; TIME; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BIOPHYSICS; DENDRITES; ELECTRIC STIMULATION; HIPPOCAMPUS; IMAGING, THREE-DIMENSIONAL; IN VITRO TECHNIQUES; LONG-TERM POTENTIATION; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; PRESYNAPTIC TERMINALS; RATS; RECEPTORS, AMPA; SECRETORY VESICLES; SYNAPSES; TIME FACTORS;

EID: 84908469595     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23646     Document Type: Article

References (150)

1. Ahmari SE, Smith SJ. 2002. Knowing a nascent synapse when you see it. Neuron 34:333-336.
2. Ahmari SE, Buchanan J, Smith SJ. 2000. Assembly of presynaptic active zones from cytoplasmic transport packets. Nat Neurosci 3:445-451.
3. Akins MR, Biederer T. 2006. Cell-cell interactions in synaptogenesis. Curr Opin Neurobiol 16:83-89.
4. Allen C, Stevens CF. 1994. An evaluation of causes for unreliability of synaptic transmission. Proc Natl Acad Sci U S A 91:10380-10383.
5. Ashby MC, Maier SR, Nishimune A, Henley JM. 2006. Lateral diffusion drives constitutive exchange of AMPA receptors at dendritic spines and is regulated by spine morphology. J Neurosci 26:7046-7055.
6. Barrow SL, Constable JR, Clark E, El-Sabeawy F, McAllister AK, Washbourne P. 2009. Neuroligin1: a cell adhesion molecule that recruits PSD-95 and NMDA receptors by distinct mechanisms during synaptogenesis. Neural Dev 4:17.
7. Bassani S, Folci A, Zapata J, Passafaro M. 2013. AMPAR trafficking in synapse maturation and plasticity. Cell Mol Life Sci 288:33873-33883.
8. Bekkers JM, Stevens CF. 1995. Quantal analysis of EPSCs recorded from small numbers of synapses in hippocampal cultures. J Neurophysiol 73:1145-1156.
9. Bender VA, Pugh JR, Jahr CE. 2009. Presynaptically expressed long-term potentiation increases multivesicular release at parallel fiber synapses. J Neurosci 29:10974-10978.
10. Benson DL, Huntley GW. 2010. Building and remodeling synapses. Hippocampus 22:954-968.
11. Benson DL, Schnapp LM, Shapiro L, Huntley GW. 2000. Making memories stick: cell-adhesion molecules in synaptic plasticity. Trends Cell Biol 10:473-482.
12. Bliss TV, Collingridge GL. 1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
13. Bourne JN, Harris KM. 2008. Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 31:47-67.
14. Bourne JN, Harris KM. 2011. Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP. Hippocampus 21:354-373.
15. Bourne JN, Harris KM. 2012a. Changes in the complexity and volume of smooth endoplasmic reticulum are coupled with synaptic enlargement along mature hippocampal dendrites during LTP. Soc Neuroscience Abstr 145.05.
16. Bourne JN, Harris KM. 2012b. Nanoscale analysis of structural synaptic plasticity. Curr Opin Neurobiol 22:372-382.
17. Bourne JN, Kirov SA, Sorra KE, Harris KM. 2007. Warmer preparation of hippocampal slices prevents synapse proliferation that might obscure LTP-related structural plasticity. Neuropharmacology 52:55-59.
18. Bourne JN, Chirillo MA, Harris KM. 2013. Presynaptic ultrastructural plasticity along CA3→CA1 axons during LTP in mature hippocampus. J Comp Neurol doi: 10 1002/cne23384.
19. Bozdagi O, Shan W, Tanaka H, Benson DL, Huntley GW. 2000. Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation. Neuron 28:245-259.
20. Bozdagi O, Wang XB, Nikitczuk JS, Anderson TR, Bloss EB, Radice GL, Zhou Q, Benson DL, Huntley GW. 2010. Persistence of coordinated long-term potentiation and dendritic spine enlargement at mature hippocampal CA1 synapses requires N-cadherin. J Neurosci 30:9984-9989.
21. Bredt DS, Nicoll RA. 2003. AMPA receptor trafficking at excitatory synapses. Neuron 40:361-379.
22. Buchanan J, Sun YA, Poo MM. 1989. Studies of nerve-muscle interactions in Xenopus cell culture: fine structure of early functional contacts. J Neurosci 9:1540-1554.
23. Cao G, Harris KM. 2012. Developmental regulation of the late phase of long-term potentiation (L-LTP) and metaplasticity in hippocampal area CA1 of the rat. J Neurophysiol 107:902-912.
24. Chen X, Winters C, Azzam R, Li X, Galbraith JA, Leapman RD, Reese TS. 2008. Organization of the core structure of the postsynaptic density. Proc Natl Acad Sci U S A 105:4453-4458.
25. Choquet D, Triller A. 2013. The dynamic synapse. Neuron 80:691-703.
26. Christie JM, Jahr CE. 2006. Multivesicular release at Schaffer collateral-CA1 hippocampal synapses. J Neurosci 26:210-216.
27. Collingridge GL, Isaac JT, Wang YT. 2004. Receptor trafficking and synaptic plasticity. Nat Rev Neurosci 5:952-962.
28. Dani A, Huang B, Bergan J, Dulac C, Zhuang X. 2010. Superresolution imaging of chemical synapses in the brain. Neuron 68:843-856.
29. Dean C, Scholl FG, Choih J, DeMaria S, Berger J, Isacoff E, Scheiffele P. 2003. Neurexin mediates the assembly of presynaptic terminals. Nat Neurosci 6:708-716.
30. + exchanger NHE6 into Dendritic spines of hippocampal pyramidal neurons during NMDA receptor-dependent long-term potentiation. J Neurosci 33:595-610.
31. Derkach VA, Oh MC, Guire ES, Soderling TR. 2007. Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat Rev Neurosci 8:101-113.
32. deWit J., Sylwestrak E, O'Sullivan ML, Otto S, Tiglio K, Savas JN, Yates JR III, Comoletti D, Taylor P, Ghosh A. 2009. LRRTM2 interacts with neurexin1 and regulates excitatory synapse formation. Neuron 64:799-806.
33. Dresbach T, Torres V, Wittenmayer N, Altrock WD, Zamorano P, Zuschratter W, Nawrotzki R, Ziv NE, Garner CC, Gundelfinger ED. 2006. Assembly of active zone precursor vesicles: obligatory trafficking of presynaptic cytomatrix proteins Bassoon and Piccolo via a trans-Golgi compartment. J Biol Chem 281:6038-6047.
34. Durand GM, Kovalchuk Y, Konnerth A. 1996. Long-term potentiation and functional synapse induction in developing hippocampus. Nature 381:71-75.
35. Easley-Neal C, Fierro J, Jr., Buchanan J, Washbourne P. 2013. Late recruitment of synapsin to nascent synapses is regulated by Cdk5. Cell Rep 3:1199-1212.
36. Ebbinghaus H. 1885. Über das Gedächnis: Untersuchungen zur experimentellen Psychologie. Leipzig: Veit & Co.
37. Edwards F. 1991. Neurobiology. LTP is a long term problem. Nature 350:271-272.
38. Ehlers MD, Heine M, Groc L, Lee MC, Choquet D. 2007. Diffusional trapping of GluR1 AMPA receptors by input-specific synaptic activity. Neuron 54:447-460.
39. Ehrlich I, Klein M, Rumpel S, Malinow R. 2007. PSD-95 is required for activity-driven synapse stabilization. Proc Natl Acad Sci U S A 104:4176-4181.
40. Elste AM, Benson DL. 2006. Structural basis for developmentally regulated changes in cadherin function at synapses. J Comp Neurol 495:324-335.
41. Enoki R, Hu YL, Hamilton D, Fine A. 2009. Expression of long-term plasticity at individual synapses in hippocampus is graded, bidirectional, and mainly presynaptic: optical quantal analysis. Neuron 62:242-253.
42. Fannon AM, Colman DR. 1996. A model for central synaptic junctional complex formation based on the differential adhesive specificities of the cadherins. Neuron 17:423-434.
43. Fiala JC. 2005. Reconstruct: a free editor for serial section microscopy. J Microsc 218:52-61.
44. Fiala JC, Harris KM. 2001a. Cylindrical diameters method for calibrating section thickness in serial electron microscopy. J Microsc 202:468-472.
45. Fiala JC, Harris KM. 2001b. Extending unbiased stereology of brain ultrastructure to three-dimensional volumes. J Am Med Inform Assoc 8:1-16.
46. Fiala JC, Feinberg M, Popov V, Harris KM. 1998. Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J Neurosci 18:8900-8911.
47. Fiala JC, Kirov SA, Feinberg MD, Petrak LJ, George P, Goddard CA, Harris KM. 2003. Timing of neuronal and glial ultrastructure disruption during brain slice preparation and recovery in vitro. J Comp Neurol 465:90-103.
48. Fifkova E, Anderson CL. 1981. Stimulation-induced changes in dimensions of stalks of dendritic spines in the dentate molecular layer. Exp Neurol 74:621-627.
49. Fifkova E, Van Harreveld A. 1977. Long-lasting morphological changes in dendritic spines of dentate granular cells following stimulation of the entorhinal area. J Neurocytol 6:211-230.
50. Franks KM, Bartol TM Jr, Sejnowski TJ. 2002. A Monte Carlo model reveals independent signaling at central glutamatergic synapses. Biophys J 83:2333-2348.
51. Franks KM, Stevens CF, Sejnowski TJ. 2003. Independent sources of quantal variability at single glutamatergic synapses. J Neurosci 23:3186-3195.
52. Futai K, Kim MJ, Hashikawa T, Scheiffele P, Sheng M, Hayashi Y. 2007. Retrograde modulation of presynaptic release probability through signaling mediated by PSD-95-neuroligin. Nat Neurosci 10:186-195.
53. Geinisman Y, de Toledo-Morrell L, Morrell F, Heller RE, Rossi M, Parshall RF. 1993. Structural synaptic correlate of long-term potentiation: formation of axospinous synapses with multiple, completely partitioned transmission zones. Hippocampus 3:435-445.
54. Giannone G, Mondin M, Grillo-Bosch D, Tessier B, Saint-Michel E, Czondor K, Sainlos M, Choquet D, Thoumine O. 2013. Neurexin-1beta binding to neuroligin-1 triggers the preferential recruitment of PSD-95 versus gephyrin through tyrosine phosphorylation of neuroligin-1. Cell Rep 3:1996-2007.
55. Graf ER, Zhang X, Jin SX, Linhoff MW, Craig AM. 2004. Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119:1013-1026.
56. Groc L, Gustafsson B, Hanse E. 2006. AMPA signalling in nascent glutamatergic synapses: there and not there! Trends Neurosci 29:132-139.
57. Hanse E, Taira T, Lauri S, Groc L. 2009. Glutamate synapse in developing brain: an integrative perspective beyond the silent state. Trends Neurosci 32:532-537.
58. Harlow ML, Ress D, Stoschek A, Marshall RM, McMahan UJ. 2001. The architecture of active zone material at the frog's neuromuscular junction. Nature 409:479-484.
59. Harris KM, Stevens JK. 1989. Dendritic spines of CA1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J Neurosci 9:2982-2997.
60. Harris KM, Sultan P. 1995. Variation in the number, location and size of synaptic vesicles provides an anatomical basis for the nonuniform probability of release at hippocampal CA1 synapses. Neuropharmacology 34:1387-1395.
61. Harris KM, Jensen FE, Tsao B. 1992. Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J Neurosci 12:2685-2705.
62. Harris KM, Perry E, Bourne J, Feinberg M, Ostroff L, Hurlburt J. 2006. Uniform serial sectioning for transmission electron microscopy. J Neurosci 26:12101-12103.
63. Harvey CD, Yasuda R, Zhong H, Svoboda K. 2008. The spread of Ras activity triggered by activation of a single dendritic spine. Science 321:136-140.
64. Heine M, Thoumine O, Mondin M, Tessier B, Giannone G, Choquet D. 2008. Activity-independent and subunit-specific recruitment of functional AMPA receptors at neurexin/neuroligin contacts. Proc Natl Acad Sci U S A 105:20947-20952.
65. Henkemeyer M, Itkis OS, Ngo M, Hickmott PW, Ethell IM. 2003. Multiple EphB receptor tyrosine kinases shape dendritic spines in the hippocampus. J Cell Biol 163:1313-1326.
66. Hering H, Sheng M. 2001. Dendritic spines: structure, dynamics and regulation. Nat Rev Neurosci 2:880-888.
67. Ichtchenko K, Hata Y, Nguyen T, Ullrich B, Missler M, Moomaw C, Sudhof TC. 1995. Neuroligin 1: a splice site-specific ligand for beta-neurexins. Cell 81:435-443.
68. Irie M, Hata Y, Takeuchi M, Ichtchenko K, Toyoda A, Hirao K, Takai Y, Rosahl TW, Sudhof TC. 1997. Binding of neuroligins to PSD-95. Science 277:1511-1515.
69. Isaac JT, Nicoll RA, Malenka RC. 1995. Evidence for silent synapses: implications for the expression of LTP. Neuron 15:427-434.
70. Jensen FE, Harris KM. 1989. Preservation of neuronal ultrastructure in hippocampal slices using rapid microwave-enhanced fixation. J Neurosci Methods 29:217-230.
71. Kayser MS, McClelland AC, Hughes EG, Dalva MB. 2006. Intracellular and trans-synaptic regulation of glutamatergic synaptogenesis by EphB receptors. J Neurosci 26:12152-12164.
72. Kerchner GA, Nicoll RA. 2008. Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat Rev Neurosci 9:813-825.
73. Kim JH, Udo H, Li HL, Youn TY, Chen M, Kandel ER, Bailey CH. 2003. Presynaptic activation of silent synapses and growth of new synapses contribute to intermediate and long-term facilitation in Aplysia. Neuron 40:151-165.
74. Kinney JP, Spacek J, Bartol TM, Bajaj CL, Harris KM, Sejnowski TJ. 2013. Extracellular sheets and tunnels modulate glutamate diffusion in hippocampal neuropil. J Comp Neurol 521:448-464.
75. Kirov SA, Harris KM. 1999. Dendrites are more spiny on mature hippocampal neurons when synapses are inactivated. Nat Neurosci 2:878-883.
76. Klein R. 2009. Bidirectional modulation of synaptic functions by Eph/ephrin signaling. Nat Neurosci 12:15-20.
77. Kramar EA, Babayan AH, Gavin CF, Cox CD, Jafari M, Gall CM, Rumbaugh G, Lynch G. 2012. Synaptic evidence for the efficacy of spaced learning. Proc Natl Acad Sci U S A 109:5121-5126.
78. Lai KO, Ip NY. 2009. Synapse development and plasticity: roles of ephrin/Eph receptor signaling. Curr Opin Neurobiol 19:275-283.
79. Lang C, Barco A, Zablow L, Kandel ER, Siegelbaum SA, Zakharenko SS. 2004. Transient expansion of synaptically connected dendritic spines upon induction of hippocampal long-term potentiation. Proc Natl Acad Sci U S A 101:16665-16670.
80. Lavenex P, Lavenex PB, Bennett JL, Amaral DG. 2009. Postmortem changes in the neuroanatomical characteristics of the primate brain: hippocampal formation. J Comp Neurol 512:27-51.
81. Li Z, Sheng M. 2003. Some assembly required: the development of neuronal synapses. Nat Rev Mol Cell Biol 4:833-841.
82. Liao D, Hessler NA, Malinow R. 1995. Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375:400-404.
83. Lim BK, Matsuda N, Poo MM. 2008. Ephrin-B reverse signaling promotes structural and functional synaptic maturation in vivo. Nat Neurosci 11:160-169.
84. Linhoff MW, Lauren J, Cassidy RM, Dobie FA, Takahashi H, Nygaard HB, Airaksinen MS, Strittmatter SM, Craig AM. 2009. An unbiased expression screen for synaptogenic proteins identifies the LRRTM protein family as synaptic organizers. Neuron 61:734-749.
85. Lisman J, Harris KM. 1993. Quantal analysis and synaptic anatomy-integrating two views of hippocampal plasticity. Trends Neurosci 16:141-147.
86. Lisman J, Raghavachari S. 2006. A unified model of the presynaptic and postsynaptic changes during LTP at CA1 synapses. Sci STKE 2006(356):re11.
87. Liu G, Choi S, Tsien RW. 1999. Variability of neurotransmitter concentration and nonsaturation of postsynaptic AMPA receptors at synapses in hippocampal cultures and slices. Neuron 22:395-409.
88. Luscher C, Nicoll RA, Malenka RC, Muller D. 2000. Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nat Neurosci 3:545-550.
89. Lynch G, Gall CM. 2013. Mechanism based approaches for rescuing and enhancing cognition. Front Neurosci 7:143.
90. Lynch G, Kramar EA, Babayan AH, Rumbaugh G, Gall CM. 2013. Differences between synaptic plasticity thresholds result in new timing rules for maximizing long-term potentiation. Neuropharmacology 64:27-36.
91. Maas C, Torres VI, Altrock WD, Leal-Ortiz S, Wagh D, Terry-Lorenzo RT, Fejtova A, Gundelfinger ED, Ziv NE, Garner CC. 2012. Formation of Golgi-derived active zone precursor vesicles. J Neurosci 32:11095-11108.
92. Macdougall MJ, Fine A. 2014. The expression of long-term potentiation: reconciling the preists and the postivists. Philos Trans R Soc Lond B Biol Sci 369:20130135.
93. MacGillavry HD, Song Y, Raghavachari S, Blanpied TA. 2013. Nanoscale scaffolding domains within the postsynaptic density concentrate synaptic AMPA receptors. Neuron 78:615-622.
94. Makino H, Malinow R. 2009. AMPA receptor incorporation into synapses during LTP: the role of lateral movement and exocytosis. Neuron 64:381-390.
95. Malinow R, Malenka RC. 2002. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
96. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, Iino M, Kasai H. 2001. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci 4:1086-1092.
97. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H. 2004. Structural basis of long-term potentiation in single dendritic spines. Nature 429:761-766.
98. McAllister AK, Stevens CF. 2000. Nonsaturation of AMPA and NMDA receptors at hippocampal synapses. Proc Natl Acad Sci U S A 97:6173-6178.
99. McGeachie AB, Cingolani LA, Goda Y. 2011. Stabilising influence: integrins in regulation of synaptic plasticity. Neurosci Res 70:24-29.
100. Mendez P, De RM, Poglia L, Klauser P, Muller D. 2010. N-cadherin mediates plasticity-induced long-term spine stabilization. J Cell Biol 189:589-600.
101. Miller DC. 1998. Use of perfusion fixation for improved neuropathologic examination. Arch Pathol Lab Med 122:949.
102. Mishchenko Y, Hu T, Spacek J, Mendenhall J, Harris KM, Chklovskii DB. 2010. Ultrastructural analysis of hippocampal neuropil from the connectomics perspective. Neuron 67:1009-1020.
103. Mondin M, Labrousse V, Hosy E, Heine M, Tessier B, Levet F, Poujol C, Blanchet C, Choquet D, Thoumine O. 2011. Neurexin-neuroligin adhesions capture surface-diffusing AMPA receptors through PSD-95 scaffolds. J Neurosci 31:13500-13515.
104. Murata Y, Constantine-Paton M. 2013. Postsynaptic density scaffold SAP102 regulates cortical synapse development through EphB and PAK signaling pathway. J Neurosci 33:5040-5052.
105. Nagerl UV, Eberhorn N, Cambridge SB, Bonhoeffer T. 2004. Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron 44:759-767.
106. Nair D, Hosy E, Petersen JD, Constals A, Giannone G, Choquet D, Sibarita JB. 2013. Super-resolution imaging reveals that AMPA receptors inside synapses are dynamically organized in nanodomains regulated by PSD95. J Neurosci 33:13204-13224.
107. Nolt MJ, Lin Y, Hruska M, Murphy J, Sheffler-Colins SI, Kayser MS, Passer J, Bennett MV, Zukin RS, Dalva MB. 2011. EphB controls NMDA receptor function and synaptic targeting in a subunit-specific manner. J Neurosci 31:5353-5364.
108. Nuriya M, Huganir RL. 2006. Regulation of AMPA receptor trafficking by N-cadherin. J Neurochem 97:652-661.
109. Opazo P, Choquet D. 2011. A three-step model for the synaptic recruitment of AMPA receptors. Mol Cell Neurosci 46:1-8.
110. Opazo P, Labrecque S, Tigaret CM, Frouin A, Wiseman PW, De KP, Choquet D. 2010. CaMKII triggers the diffusional trapping of surface AMPARs through phosphorylation of stargazin. Neuron 67:239-252.
111. Ostroff LE, Fiala JC, Allwardt B, Harris KM. 2002. Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices. Neuron 35:535-545.
112. Owald D, Sigrist SJ. 2009. Assembling the presynaptic active zone. Curr Opin Neurobiol 19:311-318.
113. Petralia RS, Esteban JA, Wang YX, Partridge JG, Zhao HM, Wenthold RJ, Malinow R. 1999. Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses. Nat Neurosci 2:31-36.
114. Raghavachari S, Lisman JE. 2004. Properties of quantal transmission at CA1 synapses. J Neurophysiol 92:2456-2467.
115. Ratnayaka A, Marra V, Bush D, Burden JJ, Branco T, Staras K. 2012. Recruitment of resting vesicles into recycling pools supports NMDA receptor-dependent synaptic potentiation in cultured hippocampal neurons. J Physiol 590:1585-1597.
116. Roberts JC, McCrossan MV, Jones HB. 1990. The case for perfusion fixation of large tissue samples for ultrastructural pathology. Ultrastruct Pathol 14:177-191.
117. Ruger HA, Bussenius CE. 1913. Memory: A contribution to experimental psychology, Hermann Ebbinghaus (1885). New York: Teachers College, Columbia University.
118. Sabo SL, Gomes RA, McAllister AK. 2006. Formation of presynaptic terminals at predefined sites along axons. J Neurosci 26:10813-10825.
119. Saglietti L, Dequidt C, Kamieniarz K, Rousset MC, Valnegri P, Thoumine O, Beretta F, Fagni L, Choquet D, Sala C, Sheng M, Passafaro M. 2007. Extracellular interactions between GluR2 and N-cadherin in spine regulation. Neuron 54:461-477.
120. Scheiffele P. 2003. Cell-cell signaling during synapse formation in the CNS. Annu Rev Neurosci 26:485-508.
121. Scheiffele P, Fan J, Choih J, Fetter R, Serafini T. 2000. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101:657-669.
122. Schikorski T, Stevens CF. 1997. Quantitative ultrastructural analysis of hippocampal excitatory synapses. J Neurosci 17:5858-5867.
123. Shapira M, Zhai RG, Dresbach T, Bresler T, Torres VI, Gundelfinger ED, Ziv NE, Garner CC. 2003. Unitary assembly of presynaptic active zones from Piccolo-Bassoon transport vesicles. Neuron 38:237-252.
124. Sheng M, Kim MJ. 2002. Postsynaptic signaling and plasticity mechanisms. Science 298:776-780.
125. Shepherd JD, Huganir RL. 2007. The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu Rev Cell Dev Biol 23:613-643.
126. Shi SH, Hayashi Y, Petralia RS, Zaman SH, Wenthold RJ, Svoboda K, Malinow R. 1999. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284:1811-1816.
127. Shipman SL, Nicoll RA. 2012. Dimerization of postsynaptic neuroligin drives synaptic assembly via transsynaptic clustering of neurexin. Proc Natl Acad Sci U S A 109:19432-19437.
128. Soler-Llavina GJ, Arstikaitis P, Morishita W, Ahmad M, Sudhof TC, Malenka RC. 2013. Leucine-rich repeat transmembrane proteins are essential for maintenance of long-term potentiation. Neuron 79:439-446.
129. Song JY, Ichtchenko K, Sudhof TC, Brose N. 1999. Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc Natl Acad Sci U S A 96:1100-1105.
130. Sorra KE, Harris KM. 1998. Stability in synapse number and size at 2 hr after long-term potentiation in hippocampal area CA1. J Neurosci 18:658-671.
131. Sorra KE, Mishra A, Kirov SA, Harris KM. 2006. Dense core vesicles resemble active-zone transport vesicles and are diminished following synaptogenesis in mature hippocampal slices. Neurosci 141:2097-2106.
132. Spacek J, Harris KM. 1997. Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat. J Neurosci 17:190-203.
133. Spacek J, Harris KM. 1998. Three-dimensional organization of cell adhesion junctions at synapses and dendritic spines in area CA1 of the rat hippocampus. J Comp Neurol 393:58-68.
134. Stan A, Pielarski KN, Brigadski T, Wittenmayer N, Fedorchenko O, Gohla A, Lessmann V, Dresbach T, Gottmann K. 2010. Essential cooperation of N-cadherin and neuroligin-1 in the transsynaptic control of vesicle accumulation. Proc Natl Acad Sci U S A 107:11116-11121.
135. Sudhof TC. 2008. Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455:903-911.
136. Sytnyk V, Leshchyns'ka I, Delling M, Dityateva G, Dityatev A, Schachner M. 2002. Neural cell adhesion molecule promotes accumulation of TGN organelles at sites of neuron-to-neuron contacts. J Cell Biol 159:649-661.
137. Tang L, Hung CP, Schuman EM. 1998. A role for the cadherin family of cell adhesion molecules in hippocampal long-term potentiation. Neuron 20:1165-1175.
138. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, Yuan H, Myers SJ, Dingledine R. 2010. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62:405-496.
139. Uchida N, Honjo Y, Johnson KR, Wheelock MJ, Takeichi M. 1996. The catenin/cadherin adhesion system is localized in synaptic junctions bordering transmitter release zones. J Cell Biol 135:767-779.
140. Vaughn JE. 1989. Fine structure of synaptogenesis in the vertebrate central nervous system. Synapse 3:255-285.
141. Waites CL, Craig AM, Garner CC. 2005. Mechanisms of vertebrate synaptogenesis. Annu Rev Neurosci 28:251-274.
142. Weeks AC, Ivanco TL, LeBoutillier JC, Racine RJ, Petit TL. 2001. Sequential changes in the synaptic structural profile following long-term potentiation in the rat dentate gyrus: III. Long-term maintenance phase. Synapse 40:74-84.
143. Willig KI, Steffens H, Gregor C, Herholt A, Rossner MJ, Hell SW. 2014. Nanoscopy of filamentous actin in cortical dendrites of a living mouse. Biophys J 106:L01-L03.
144. Wittenmayer N, Korber C, Liu H, Kremer T, Varoqueaux F, Chapman ER, Brose N, Kuner T, Dresbach T. 2009. Postsynaptic neuroligin1 regulates presynaptic maturation. Proc Natl Acad Sci U S A 106:13564-13569.
145. Wu YE, Huo L, Maeder CI, Feng W, Shen K. 2013. The balance between capture and dissociation of presynaptic proteins controls the spatial distribution of synapses. Neuron 78:994-1011.
146. Yuste R, Bonhoeffer T. 2001. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 24:1071-1089.
147. Zhai RG, Vardinon-Friedman H, Cases-Langhoff C, Becker B, Gundelfinger ED, Ziv NE, Garner CC. 2001. Assembling the presynaptic active zone: a characterization of an active one precursor vesicle. Neuron 29:131-143.
148. Zhang P, Lisman JE. 2012. Activity-dependent regulation of synaptic strength by PSD-95 in CA1 neurons. J Neurophysiol 107:1058-1066.
149. Ziv NE, Garner CC. 2001. Principles of glutamatergic synapse formation: seeing the forest for the trees. Curr Opin Neurobiol 11:536-543.
150. Ziv NE, Garner CC. 2004. Cellular and molecular mechanisms of presynaptic assembly. Nat Rev Neurosci 5:385-399.