Structural components of synaptic plasticity and memory consolidation

Cold Spring Harbor Perspectives in Biology

Volumn 7, Issue 7, 2015, Pages 1-29

  Bailey, Craig H ^a,b,c   Kandel, Eric R ^a,b,c,d   Harris, Kristen M ^e  

^a New York Presbyterian Columbia University Medical Center   (United States)

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^c Kavli Institute for Brain Science   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^e UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APLYSIA; INVERTEBRATA; MAMMALIA;

EID: 84936765191     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a021758     Document Type: Article

References (294)

1. AbrahamWC, Bear MF. 1996. Metaplasticity: The plasticity of synaptic plasticity. Trends Neurosci 19: 126-130.
2. Abraham WC, Huggett A. 1997. Induction and reversal of long-term potentiation by repeated high-frequency stimulation in rat hippocampal slices. Hippocampus 7: 137-145.
3. Abraham WC, Tate WP. 1997. Metaplasticity: A new vista across the field of synaptic plasticity. Prog Neurobiol 52: 303-323.
4. AbrahamWC, Mason-Parker SE, Bear MF,Webb S, TateWP. 2001. Heterosynaptic metaplasticity in the hippocampus in vivo: A BCM-like modifiable threshold for LTP. Proc Natl Acad Sci 98: 10924-10929.
5. Abraham WC, Logan B, Greenwood JM, Dragunow M. 2002. Induction and experience-dependent consolidation of stable long-term potentiation lasting months in the hippocampus. J Neurosci 22: 9626-9634.
6. Ahmari SE, Smith SJ. 2002. Knowing a nascent synapse when you see it. Neuron 34: 333-336.
7. Ahmari SE, Buchanan J, Smith SJ. 2000. Assembly of presynaptic active zones fromcytoplasmic transport packets. Nat Neurosci 3: 445-451.
8. Akins MR, Biederer T. 2006. Cell-cell interactions in synaptogenesis. Curr Opin Neurobiol 16: 83-89.
9. Alberini CM, Kandel ER. 2014. The regulation of transcription in memory consolidation. Cold Spring Harb Perspect Biol doi: 110.1101/cshperspect.a021741.
10. Alberini CM, Ghirardi M,Metz R, Kandel ER. 1994. C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia. Cell 76: 1099-1114.
11. Alvarez VA, Sabatini BL. 2007. Anatomical and physiological plasticity of dendritic spines. Annu Rev Neurosci 30: 79- 97.
12. Alvarez VA, Ridenour DA, Sabatini BL. 2007. Distinct structural and ionotropic roles ofNMDA receptors in controlling spine and synapse stability. J Neurosci 27: 7365- 7376.
13. Bacskai BJ, Hochner B,Mahaut-Smith M, Adams SR, Kaang BK, Kandel ER, Tsien RY. 1993. Spatially resolved dynamics of cAMP and protein kinase A subunits in Aplysia sensory neurons. Science 260: 222-226.
14. Bailey CH. 1991. Morphological basis of short- and longterm memory in Aplysia. In Perspectives on cognitive neuroscience (ed. Weingartner H, Lister R), pp. 76-92. Oxford University Press, New York.
15. Bailey CH, Chen M. 1983. Morphological basis of long-term habituation and sensitization in Aplysia. Science 220: 91-93.
16. Bailey CH, Chen M. 1988a. Long-term memory in Aplysia modulates the total number of varicosities of single identified sensory neurons. ProcNatl Acad Sci 85: 2373-2377.
17. Bailey CH, Chen M. 1988b. Long-term sensitization in Aplysia increases the number of presynaptic contacts onto the identified gill motor neuron L7. Proc Natl Acad Sci 85: 9356-9359.
18. Bailey CH, Chen M. 1989. Time course of structural changes at identified sensory neuron synapses during long-term sensitization in Aplysia. J Neurosci 9: 1774-1780.
19. Bailey CH, Chen M. 1990. Morphological alterations at identified sensory neuron synapses during long-term sensitization in Aplysia. In The biology of memory, Vol. 23. Symposium Medicum Hoechst (ed. Squire L, Lindenlaub E), pp. 135-153. Schattauer, Stuttgart, Germany.
20. Bailey CH, Kandel ER. 1985. Molecular approaches to the study of short-term and long-term memory. In Functions of the brain (ed. Coen CW), pp. 98-129. Clarendon, Oxford.
21. Bailey CH, Kandel ER. 1993. Structural changes accompanying memory storage. Annu Rev Physiol 55: 397-426.
22. Bailey CH, Kandel ER. 2004. Synaptic growth and the persistence of long-term memory: A molecular perspective. In The new cognitive neurosciences (ed. Gazzaniga MS), Vol. III, pp. 647-664. MIT Press, Cambridge, MA.
23. Bailey CH,Kandel ER. 2008a. Synaptic remodeling, synaptic growth and the storage of long-term memory in Aplysia. In The essence of memory, progress in brain research (ed. Sossin W, et al.), pp. 179-198. Elsevier, Amsterdam.
24. Bailey CH, Kandel ER. 2008b. Activity-dependent remodeling of presynaptic boutons. In New encyclopedia of neuroscience (ed. Squire L), pp. 67-74. Elsevier, Amsterdam.
25. Bailey CH, Kandel ER. 2009. Synaptic and cellular basis of learning. In Handbook of neuroscience for behavioral sciences (ed. Cacioppo JT, Berntson GG), Vol. 1, Chap. 27, pp. 528-551. Wiley, New York.
26. Bailey CH, Thompson EB, Castellucci VF, Kandel ER. 1979. Ultrastructure of the synapses of sensory neurons that mediate the gill-withdrawal reflex in Aplysia. J Neurocytol 8: 415-444.
27. Bailey CH, Chen M, Keller F, Kandel ER. 1992a. Serotoninmediated endocytosis of apCAM: An early step of learning- related synaptic growth in Aplysia. Science 25: 645- 649.
28. Bailey CH,Montarolo PG, Chen M, Kandel ER, Schacher S. 1992b. Inhibitors of protein and RNA synthesis block the structural changes that accompany long-term heterosynaptic plasticity in the sensory neurons of Aplysia.Neuron 9: 749-758.
29. Bailey CH, Bartsch D, Kandel ER. 1996. Toward a molecular definition of long-term memory storage. Proc Natl Acad Sci 93: 13445-13452.
30. Bailey CH, Kaang BK, Chen M, Marin C, Lim A, Kandel ER. 1997. Mutation in the phosphorylation sites of MAP kinase blocks learning-related internalization of apCAM in Aplysia sensory neurons. Neuron 18: 913-924.
31. Bailey CH, Kandel ER, Si K. 2004. The persistence of longterm memory: A molecular approach to self-sustaining changes in learning-induced synaptic growth. Neuron 44: 49-57.
32. Bailey CH, Kandel ER, Si K, Choi YB. 2005. Toward a molecular biology of learning-related synaptic growth in Aplysia. Cell Sci Rev 2: 27-57.
33. Bailey CH, Barco A, Hawkins RD, Kandel ER. 2008. Molecular studies of learning and memory in Aplysia and the hippocampus: A comparative analysis of implicit and explicit memory storage. In Learning and memory: Comprehensive reference, Vol 4. Molecular mechanisms of memory (ed. Byrne JH), pp. 11-29. Elsevier, Amsterdam.
34. Bailey ME,Wang AC, Hao J, JanssenWG, Hara Y, Dumitriu D, Hof PR, Morrison JH. 2011. Interactive effects of age and estrogen on cortical neurons: Implications for cognitive aging. Neuroscience 191: 148-158.
35. Barnes CA, JungMW,McNaughton BL, Korol DL, Andreasson K,Worley PF. 1994. LTP saturation and spatial learning disruption: Effects of task variables and saturation levels. J Neurosci 14: 5793-5806.
36. 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.
37. Bell ME, Bourne JN, Chirillo MA, Harris KM. 2014. Conversion of nascent to active zones as synapses enlarge during long-term potentiation in mature hippocampus. J Comp Neurol 522: 3861-3884.
38. Bender RA, Kirschstein T, Kretz O, Brewster AL, Richichi C, Ruschenschmidt C, Shigemoto R, Beck H, Frotscher M, Baram TZ. 2007. Localization of HCN1 channels to presynaptic compartments: Novel plasticity that may contribute to hippocampal maturation. J Neurosci 27: 4697- 4706.
39. Benson DL, Huntley GW. 2010. Building and remodeling synapses. Hippocampus 22: 954-968.
40. Benson DL, Schnapp LM, Shapiro L, Huntley GW. 2000. Making memories stick: Cell-adhesion molecules in synaptic plasticity. Trends Cell Biol 10: 473-482.
41. Bliss TV, Collingridge GL, Morris RG. 2013. Synaptic plasticity in health and disease: Introduction and overview. Philos Trans R Soc Lond B Biol Sci 369: 20130129.
42. Bock DD, Lee WC, Kerlin AM, Andermann ML, Hood G, Wetzel AW, Yurgenson S, Soucy ER, Kim HS, Reid RC. 2011. Network anatomy and in vivo physiology of visual cortical neurons. Nature 471: 177-182.
43. Bonhoeffer T, Yuste R. 2002. Spine motility. Phenomenology, mechanisms, and function. Neuron 35: 1019-1027.
44. Bourne J, Harris KM. 2007. Do thin spines learn to be mushroom spines that remember? Curr Opin Neurobiol 17: 381-386.
45. Bourne JN, Harris KM. 2008. Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 31: 47-67.
46. 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.
47. Bourne JN, Harris KM. 2012. Nanoscale analysis of structural synaptic plasticity. Curr Opin Neurobiol 22: 372- 382.
48. Bourne JN, Sorra KE, Hurlburt J, Harris KM. 2007. Polyribosomes are increased in spines of CA1 dendrites 2 h after the induction of LTP in mature rat hippocampal slices. Hippocampus 17: 1-4.
49. Bourne JN, Chirillo MA, Harris KM. 2013. Presynaptic ultrastructural plasticity along CA3 → CA1 axons during LTP in mature hippocampus. J Comp Neurol 521: 3898- 3912.
50. Bowden JB, Abraham WC, Harris KM. 2012. Differential effects of strain, circadian cycle, and stimulation pattern on LTP and concurrent LTD in the dentate gyrus of freely moving rats. Hippocampus 22: 1363-1370.
51. 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.
52. 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.
53. 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.
54. Budnik V, Salinas PC. 2011. Wnt signaling during synaptic development and plasticity. Curr Opin Neurobiol 21: 151-159.
55. Buzsaki G. 2002. θ Oscillations in the hippocampus. Neuron 33: 325-340.
56. Buzsaki G, Haas HL, Anderson EG. 1987. Long-term potentiation induced by physiologically relevant stimulus patterns. Brain Res 435: 331-333.
57. 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.
58. Cardona A. 2013. Towards semi-automatic reconstruction of neural circuits. Neuroinformatics 11: 31-33.
59. Cardona A, Saalfeld S, Preibisch S, Schmid B, Cheng A, Pulokas J, Tomancak P, Hartenstein V. 2010. An integrated micro- and macroarchitectural analysis of the Drosophila brain by computer-assisted serial section electron microscopy. PLoS Biol 8: e1000502.
60. Casadio A, Martin KC, Giustetto M, Zhu H, Chen M, Bartsch D, Bailey CH, Kandel ER. 1999. A transient, neuron- wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell 99: 221-237.
61. Castellucci V, Pinsker H, Kupfermann I, Kandel ER. 1970. Neuronal mechanisms of habituation and dishabituation of the gill-withdrawal reflex in Aplysia. Science 167: 1745-1748.
62. Castellucci VF, Blumenfeld H, Goelet P, Kandel ER. 1989. Inhibitor of protein synthesis blocks long-term behavioral sensitization in the isolated gill-withdrawal reflex of Aplysia. Science 220: 91-93.
63. Chen YC, Bourne J, Pieribone VA, Fitzsimonds RM. 2004. The role of actin in the regulation of dendritic spine morphology and bidirectional synaptic plasticity. Neuro- Report 15: 829-832.
64. Chen S, Cai D, Pearce K, Sun PYW, Roberts AC, Glanzman DL. 2014. Reinstatement of long-term memory following erasure of its behavioral and synaptic expression in Aplysia. eLife 3: e03896.
65. Choi Y-B, Li H-L, Kassabov SR, Jin I, Puthanveettil SV, Karl KA, Lu Y, Kim J-H, Bailey CH, Kandel ER. 2011. Neurexin-Neuroligin transsynaptic interaction mediates learning-related synaptic remodeling and long-term facilitation in Aplysia. Neuron 70: 1-14.
66. Clarke LE, Barres BA. 2013. Emerging roles of astrocytes in neural circuit development. Nat Rev Neurosci 14: 311- 321.
67. Coggan JS, Bartol TM, Esquenazi E, Stiles JR, Lamont S, Martone ME, Berg DK, Ellisman MH, Sejnowski TJ. 2005. Evidence for ectopic neurotransmission at a neuronal synapse. Science 309: 446-451.
68. Cooney JR, Hurlburt JL, Selig DK, Harris KM, Fiala JC. 2002. Endosomal compartments serve multiple hippocampal dendritic spines from a widespread rather than a local store of recycling membrane. J Neurosci 22: 2215- 2224.
69. Cui-Wang T, Hanus C, Cui T, Helton T, Bourne J,Watson D, Harris KM, EhlersMD. 2012. Local zones of endoplasmic reticulum complexity confine cargo in neuronal dendrites. Cell 148: 309-321.
70. 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.
71. Denk W, Horstmann H. 2004. Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol 2: e329.
72. De Paola V, Holtmaat A, Knott G, Song S, Wilbrecht L, Caroni P, Svoboda K. 2006. Cell type-specific structural plasticity of axonal branches and boutons in the adult neocortex. Neuron 49: 861-875.
73. 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.
74. Diana G, Domenici MR, Loizzo A, Scotti de Carolis A, Sagratella S. 1994. Age and strain differences in rat place learning and hippocampal dentate gyrus frequency-potentiation. Neurosci Lett 171: 113-116.
75. Dudai Y. 2012. The restless engram: Consolidations never end. Annu Rev Neurosci 35: 227-247.
76. Durand GM, Kovalchuk Y, Konnerth A. 1996. Long-term potentiation and functional synapse induction in developing hippocampus. Nature 381: 71-75.
77. Ebbinghaus H. 1885. Über das gedächnis: Untersuchungen zur experimentellen psychologie [Memory: A contribution to experimental psychology]. Veit, Leipzig, Germany.
78. Edwards F. 1991. Neurobiology. LTP is a long-term problem. Nature 350: 271-272.
79. Elste AM, Benson DL. 2006. Structural basis for developmentally regulated changes in cadherin function at synapses. J Comp Neurol 495: 324-335.
80. Engert F, Bonhoeffer T. 1999. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399: 66-70.
81. 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.
82. Fiala JC, Feinberg M, Popov V, Harris KM. 1998. Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J Neurosci 18: 8900-8911.
83. Fields RD. 2005. Making memories stick. Sci Am 292: 75- 81.
84. Fiete IR, Senn W, Wang CZ, Hahnloser RH. 2010. Spiketime- dependent plasticity and heterosynaptic competition organize networks to produce long scale-free sequences of neural activity. Neuron 65: 563-576.
85. Foy MR, Baudry M, Akopian GK, Thompson RF. 2010. Regulation of hippocampal synaptic plasticity by estrogen and progesterone. Vitam Horm 82: 219-239.
86. Franks KM, Bartol TM Jr, Sejnowski TJ. 2002. A Monte Carlo model reveals independent signaling at central glutamatergic synapses. Biophys J 83: 2333-2348.
87. Franks KM, Stevens CF, Sejnowski TJ. 2003. Independent sources of quantal variability at single glutamatergic synapses. J Neurosci 23: 3186-3195.
88. Frey U, Morris RG. 1997. Synaptic tagging and long-term potentiation. Nature 385: 533-536.
89. Frey U, Schollmeier K, Reymann KG, Seidenbecher T. 1995. Asymptotic hippocampal long-term potentiation in rats does not preclude additional potentiation at later phases. Neuroscience 67: 799-807.
90. 2+ signals by small oblique dendrites of CA1 pyramidal neurons. J Neurosci 23: 3243-3250.
91. Frost WN, Castellucci VF, Hawkins RD, Kandel ER. 1985. Monosynaptic connections made by the sensory neurons of the gill- and siphon-withdrawal reflex in Aplysia participates in the storage of long-term memory for sensitization. Proc Natl Acad Sci 82: 8266-8269.
92. 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.
93. Gasparini S, Losonczy A, Chen X, Johnston D, Magee JC. 2007. Associative pairing enhances action potential backpropagation in radial oblique branches of CA1 pyramidal neurons. J Physiol 580: 787-800.
94. Geinisman Y, Berry RW, Disterhoft JF, Power JM, van der Zee EA. 2001. Associative learning elicits the formation of multiple-synapse boutons. J Neurosci 21: 5568-5573.
95. Ghirardi M, Montarolo PG, Kandel ER. 1995. A novel intermediate stage in the transition between short- and long-term facilitation in the sensory to motor neuron synapse of Aplysia. Neuron 14: 413-420.
96. Giannone G, Mondin M, Grillo-Bosch D, Tessier B, Saint-Michel E, Czondor K, Sainlos M, Choquet D, Thoumine O. 2013. Neurexin-1β binding to neuroligin-1 triggers the preferential recruitment of PSD-95 versus gephyrin through tyrosine phosphorylation of neuroligin-1. Cell Rep 3: 1996-2007.
97. Glanzman DL, Kandel ER, Schacher S. 1990. Target-dependent structural changes accompanying long-term synaptic facilitation in Aplysia neurons. Science 249: 779-802.
98. Govindarajan A, Kelleher RJ, Tonegawa S. 2006. A clustered plasticity model of long-term memory engrams. Nat Rev Neurosci 7: 575-583.
99. Govindarajan A, Israely I, Huang SY, Tonegawa S. 2011. The dendritic branch is the preferred integrative unit for protein synthesis-dependent LTP. Neuron 69: 132-146.
100. 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.
101. Greenough WT, Bailey CH. 1988. The anatomy of a memory: Convergence of results across a diversity of tests. Trends Neurosci 11: 142-147.
102. Groc L, Gustafsson B, Hanse E. 2006. AMPA signalling in nascent glutamatergic synapses: There and not there! Trends Neurosci 29: 132-139.
103. Grutzendler J, Kasthuri N, Gan WB. 2002. Long-term dendritic spine stability in the adult cortex.Nature 420: 812- 816.
104. Habib D, Tsui CK, Rosen LG, Dringenberg HC. 2013. Occlusion of low-frequency-induced, heterosynaptic longterm potentiation in the rat hippocampus in vivo following spatial training. Cereb Cortex 24: 3090-3096.
105. Han JH, Lim YS, Kandel ER, Kaang BK. 2004. Role of Aplysia cell adhesion molecules during 5-HT-induced longterm functional and structural changes. Learn Mem 11: 421-435.
106. 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.
107. 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.
108. Harris KM, Kater SB. 1994. Dendritic spines: Cellular specializations imparting both stability and flexibility to synaptic function. Annu Rev Neurosci 17: 341-371.
109. Harris KM, Stevens JK. 1987. Study of dendritic spines by serial electron microscopy and three-dimensional reconstructions. Neurol Neurobiol 37: 179-199.
110. 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.
111. 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.
112. Harris KM, Teyler TJ. 1983. Age differences in a circadian influence on hippocampal LTP. Brain Res 261: 69-73.
113. Harris KM,Weinberg RJ. 2012. Ultrastructure of synapses in the mammalian brain. Cold Spring Harb Perspect Biol 4: a005587.
114. 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.
115. 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.
116. Hatada Y, Wu F, Sun ZY, Schacher S, Goldberg DJ. 2000. Presynaptic morphological changes associated with long-term synaptic facilitation are triggered by actin polymerization at preexisting varicosities. J Neurosci 20: RC82.
117. Hawkins RD, Kandel ER, Bailey CH. 2006. Molecular mechanisms of memory storage in Aplysia. Biol Bull 210: 174- 191.
118. Hawkins RD, Kandel ER, Jin I. 2012. Possible roles of spontaneous transmitter release in homeostasis and growth related plasticity at Aplysia sensory-motor neuron synapses. In Molluscan neuroscience in the genomic era: From gastropods to cephalopods, Abstract 294.06. Scripps Research Institute, Jupiter, FL.
119. Heine M, Thoumine O, Mondin M, Tessier B, Giannone G, Choquet D. 2008. Activity-independent and subunitspecific recruitment of functional AMPA receptors at neurexin/neuroligin contacts. Proc Natl Acad Sci 105: 20947-20952.
120. Helmstaedter M, Briggman KL, Denk W. 2011. High-accuracy neurite reconstruction for high-throughput neuroanatomy. Nat Neurosci 14: 1081-1088.
121. 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.
122. Holtmaat A, Svoboda K. 2009. Experience-dependent structural synaptic plasticity in the mammalian brain. Nat Rev Neurosci 10: 647-658.
123. Holtmaat AJ, Trachtenberg JT, Wilbrecht L, Shepherd GM, Zhang X, Knott GW, Svoboda K. 2005. Transient and persistent dendritic spines in the neocortex in vivo. Neuron 45: 279-291.
124. Horton AC, Racz B, Monson EE, Lin AL, Weinberg RJ, Ehlers MD. 2005. Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 48: 757-771.
125. Hsia AY, Malenka RC, Nicoll RA. 1998. Development of excitatory circuitry in the hippocampus. J Neurophysiol 79: 2013-2024.
126. Huang YY, Kandel ER. 1994. Recruitment of long-lasting and protein kinase A-dependent long-term potentiation in the CA1 region of hippampus requires repeated tetanization. Learn Mem 1: 74-82.
127. Huang YY, Colino A, Selig DK, Malenka RC. 1992. The influence of prior synaptic activity on the induction of long-term potentiation. Science 255: 730-733.
128. Hübener M, Bonhoeffer T. 2010. Searching for engrams. Neuron 67: 363-371.
129. Hyman JM, Wyble BP, Goyal V, Rossi CA, Hasselmo ME. 2003. Stimulation in hippocampal region CA1 in behaving rats yields long-term potentiation when delivered to the peak of θ and long-term depression when delivered to the trough. J Neurosci 23: 11725-11731.
130. Ichtchenko K, Hata Y, Nguyen T, Ullrich B, Missler M,Moomaw C, Sudhof TC. 1995. Neuroligin 1: A splice sitespecific ligand for β-neurexins. Cell 81: 435-443.
131. 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.
132. Isaac JT, Nicoll RA, Malenka RC. 1995. Evidence for silent synapses: Implications for the expression of LTP. Neuron 15: 427-434.
133. Jessell TM, Kandel ER. 1993. Synaptic transmission: A bidirectional and self-modifiable form of cell-cell communication. Cell 72 (Suppl): 1-30.
134. Jin I, Puthanveettil S, Udo H, Karl K, Kandel ER, Hawkins RD. 2012a. Spontaneous transmitter release is critical for the induction of long-term and intermediate-term facilitation in Aplysia. Proc Natl Acad Sci 109: 9131-9136.
135. Jin I, Udo H, Rayman JB, Puthanveettil S, Kandel ER, Hawkins RD. 2012b. Spontaneous transmitter release recruits postsynaptic mechanisms of long-term and intermediate- term facilitation in Aplysia. Proc Natl Acad Sci 109: 9137-9142.
136. Kandel ER. 2001. The molecular biology of memory storage: A dialogue between genes and synapses. Science 294: 1030-1038.
137. Kandel ER. 2009. The biology of memory: A forty-year perspective. J Neurosci 29: 12748-12756.
138. Kang J,Huguenard JR, PrinceDA. 1996. Development of BK channels in neocortical pyramidal neurons. J Neurophysiol 76: 188-198.
139. Kasai H, Fukuda M, Watanabe S, Hayashi-Takagi A, Noguchi J. 2010. Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci 33: 121-129.
140. Kassabov SR, Choi YB, Karl KA, VishwasraoHD, Bailey CH, Kandel ER. 2013. A single Aplysia neurotrophin mediates synaptic facilitation via differentially processed isoforms secreted as mature or precursor forms. Cell Rep 3: 1-15.
141. Kayser MS, McClelland AC, Hughes EG, Dalva MB. 2006. Intracellular and transsynaptic regulation of glutamatergic synaptogenesis by EphB receptors. J Neurosci 26: 12152-12164.
142. Kelleher RJ, Govindarajan A, Tonegawa S. 2004. Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron 44: 59-73.
143. Kennedy MB. 2000. Signal-processing machines at the postsynaptic density. Science 290: 750-754.
144. 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.
145. Klein R. 2009. Bidirectional modulation of synaptic functions by Eph/ephrin signaling. Nat Neurosci 12: 15-20.
146. Knott GW, Holtmaat A, Wilbrecht L, Welker E, Svoboda K. 2006. Spine growth precedes synapse formation in the adult neocortex in vivo. Nat Neurosci 9: 1117-1124.
147. Kopec CD, Li B, Wei W, Boehm J, Malinow R. 2006. Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. J Neurosci 26: 2000-2009.
148. Kozorovitskiy Y, Gross CG,Kopil C, Battaglia L,McBreen M, Stranahan AM, Gould E. 2005. Experience induces structural and biochemical changes in the adult primate brain. Proc Natl Acad Sci 102: 17478-17482.
149. 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 109: 5121-5126.
150. Lai KO, Ip NY. 2009. Synapse development and plasticity: Roles of ephrin/Eph receptor signaling. Curr Opin Neurobiol 19: 275-283.
151. Lai CS, Franke TF, Gan WB. 2012. Opposite effects of fear conditioning and extinction on dendritic spine remodelling. Nature 483: 87-91.
152. 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 101: 16665-16670.
153. Lee SH, Lim CS, Park H, Lee JA, Han JH, Kim H, Cheang YH, Lee SH, Lee YS, Ko HG, et al. 2007. Nuclear translocation of CAM-associated protein activates transcription for long-term facilitation in Aplysia. Cell 129: 801- 812.
154. Lee WC, Chen JL, Huang H, Leslie JH, Amitai Y, So PT, Nedivi E. 2008. A dynamic zone defines interneuron remodeling in the adult neocortex. Proc Natl Acad Sci 105: 19968-19973.
155. Lee SH, Shim J, Choi SL, Lee N, Lee CH, Bailey CH, Kandel ER, Jang DJ, Kaang BK. 2012. Learning-related synaptic growth mediated by internalization of Aplysia cell adhesion molecule is controlled by membrane phosphatidylinositol 4,5-bisphosphate synthetic pathway. J Neuroscience 32: 16296-16305.
156. Leinekugel X, Khazipov R, Cannon R, Hirase H, Ben-Ari Y, Buzsaki G. 2002. Correlated bursts of activity in the neonatal hippocampus in vivo. Science 296: 2049-2052.
157. Li Z, Sheng M. 2003. Some assembly required: The development of neuronal synapses. Nat Rev Mol Cell Biol 4: 833-841.
158. Li H-L, Huang BS, Vishwasrao H, Sutedja N, ChenW, Jin I, Hawkins RD, Bailey CH, Kandel ER. 2009. Dscam mediates remodeling of glutamate receptors in Aplysia during de novo and learning-related synapse formation. Neuron 61: 527-540.
159. 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.
160. Lichtman JW, Sanes JR. 2008. Ome sweet ome:What can the genome tell us about the connectome? Curr Opin Neurobiol 18: 346-353.
161. Lim BK, Matsuda N, Poo MM. 2008. Ephrin-B reverse signaling promotes structural and functional synaptic maturation in vivo. Nat Neurosci 11: 160-169.
162. LinhoffMW, 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.
163. Lisman J, Harris KM. 1993. Quantal analysis and synaptic anatomy-Integrating two views of hippocampal plasticity. Trends Neurosci 16: 141-147.
164. Loebrich S, Nedivi E. 2009. The function of activity-regulated genes in the nervous system. Physiol Rev 89: 1079- 1103.
165. Losonczy A, Magee JC. 2006. Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. Neuron 50: 291-307.
166. LuW, Bushong EA, Shih TP, Ellisman MH, Nicoll RA. 2013. The cell-autonomous role of excitatory synaptic transmission in the regulation of neuronal structure and function. Neuron 78: 433-439.
167. Lynch G, Gall CM. 2013. Mechanism based approaches for rescuing and enhancing cognition. Front Neurosci 7: 143.
168. 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.
169. Macdougall MJ, Fine A. 2014. The expression of long-term potentiation: Reconciling the priests and the positivists. Philos Trans R Soc Lond B Biol Sci 369: 20130135.
170. Magee J, HoffmanD, Colbert C, JohnstonD. 1998. Electrical and calcium signaling in dendrites of hippocampal pyramidal neurons. Annu Rev Physiol 60: 327-346.
171. Majewska AK, Newton JR, Sur M. 2006. Remodeling of synaptic structure in sensory cortical areas in vivo. J Neurosci 26: 3021-3029.
172. + channel polypeptides in rat hippocampal neurons developing in situ and in vitro. J Neurosci 15: 3840-3851.
173. Maletic-Savatic M, Malinow R, Svoboda K. 1999. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283: 1923-1927.
174. Malinow R, Malenka RC. 2002. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25: 103-126.
175. Malinow R, Mainen ZF, Hayashi Y. 2000. LTP mechanisms: From silence to four-lane traffic. Curr Opin Neurobiol 10: 352-357.
176. Manahan-VaughanD, Schwegler H. 2011. Strain-dependent variations in spatial learning and in hippocampal synaptic plasticity in the dentate gyrus of freely behaving rats. Front Behav Neurosci 5: 7.
177. Marinesco S, Carew TJ. 2002. Serotonin release evoked by tail nerve stimulation in the CNS of Aplysia: Characterization and relationship to heterosynaptic plasticity. J Neurosci 22: 2299-2312.
178. Marrone DF. 2005. The morphology of bi-directional experience- dependent cortical plasticity: A meta-analysis. Brain Res Brain Res Rev 50: 100-113.
179. Martin KC. 2004. Local protein synthesis during axon guidance and synaptic plasticity. Curr Opin Neurobiol 14: 305-310.
180. Martin EC, Casadio A, Zhu H, Yaping E, Rose J, Chen M, Bailey CH,Kandel ER. 1997a. Synapse-specific long-term facilitation of Aplysia sensory somatic synapses: A function for local protein synthesis memory storage. Cell 91: 927-938.
181. Martin KC, Michael D, Rose JC, Barad M, Casadio A, Zhu H, Kandel ER. 1997b. MAP kinase translocates into the nucleus of the presynaptic cell and is required for longterm facilitation in Aplysia. Neuron 18: 899-912.
182. Matsuo N, Reijmers L, Mayford M. 2008. Spine-type-specific recruitment of newly synthesized AMPA receptors with learning. Science 319: 1104-1107.
183. 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.
184. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H. 2004. Structural basis of long-term potentiation in single dendritic spines. Nature 429: 761-766.
185. Mauelshagen J, Parker GR, Carew TJ. 1996. Dynamics of induction and expression of long-term synaptic facilitation in Aplysia. J Neurosci 16: 7099-7108.
186. Mayford M, Barzilai A, Keller F, Schacher S, Kandel ER. 1992. Modulation of an NCAM-related adhesion molecule with long-term synaptic plasticity in Aplysia. Science 256: 638-644.
187. Mayford M, Siegelbaum SA, Kandel ER. 2012. Synapses and memory storage. Cold Spring Harb Perspect Biol 4: a005751.
188. McAllister AM. 2007. Dynamic aspects of CNS synapse formation. Ann Rev Neurosci 30: 425-450.
189. Meinertzhagen IA, Takemura SY, Lu Z,Huang S, Gao S, Ting CY, Lee CH. 2009. From form to function: The ways to know a neuron. J Neurogenet 23: 68-77.
190. Mendez P, De Roo M, Poglia L, Klauser P, Muller D. 2010. N-cadherin mediates plasticity-induced long-term spine stabilization. J Cell Biol 189: 589-600.
191. Minerbi A, Kahana R, Goldfeld L, Kaufman M, Marom S, Ziv NE. 2009. Long-term relationships between synaptic tenacity, synaptic remodeling, and network activity. PLoS Biol 7: e1000136.
192. Miniaci MC, Kim J-H, Puthenveettil S, Si K, Zhu H, Kandel ER, Bailey CH. 2008. Sustained CPEB-dependent local protein synthesis is required to stabilize synaptic growth for persistence of long-term facilitation in Aplysia. Neuron 59: 1024-1036.
193. 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.
194. +- channel proteins in the rat brain. Brain Res 750: 251-263.
195. Moczulska KE, Tinter-Thiede J, Peter M, Ushakova L, Wernle T, Bathellier B, Rumpel S. 2013. Dynamics of dendritic spines in the mouse auditory cortex during memory formation and memory recall. Proc Natl Acad Sci 110: 18315-18320.
196. Mohns EJ, Blumberg MS. 2008. Synchronous bursts of neuronal activity in the developing hippocampus: Modulation by active sleep and association with emerging gamma and θ rhythms. J Neurosci 28: 10134-10144.
197. Molnar E, Pickard L, Duckworth JK. 2002. Developmental changes in ionotropic glutamate receptors: Lessons from hippocampal synapses. Neuroscientist 8: 143-153.
198. 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.
199. Montarolo PG, Goelet P, Castellucci VF, Morgan J, Kandel ER, Schacher S. 1986. A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science 234: 1249-1254.
200. Morgan SL, Teyler TJ. 2001. Electrical stimuli patterned after the θ-rhythm induce multiple forms of LTP. J Neurophysiol 86: 1289-1296.
201. Moser MB, Trommald M, Egeland T, Andersen P. 1997. Spatial training in a complex environment and isolation alter the spine distribution differently in rat CA1 pyramidal cells. J Comp Neurol 380: 373-381.
202. Moser EI, Krobert KA, Moser MB, Morris RG. 1998. Impaired spatial learning after saturation of long-term potentiation. Science 281: 2038-2042.
203. 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.
204. Nagerl UV, Eberhorn N, Cambridge SB, Bonhoeffer T. 2004. Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron 44: 759-767.
205. Nagerl UV, Kostinger G, Anderson JC, Martin KA, Bonhoeffer T. 2007. Protracted synaptogenesis after activitydependent spinogenesis in hippocampal neurons. J Neurosci 27: 8149-8156.
206. 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.
207. Nelson SB, Turrigiano GG. 2008. Strength through diversity. Neuron 60: 477-482.
208. Nguyen PV, Kandel ER. 1997. Brief θ-burst stimulation induces a transcription-dependent late phase of LTP requiring cAMP in area CA1 of the mouse hippocampus. Learn Mem 4: 230-243.
209. Nicholson DA, Trana R, Katz Y, Kath WL, Spruston N, Geinisman Y. 2006. Distance-dependent differences in synapse number and AMPA receptor expression in hippocampal CA1 pyramidal neurons. Neuron 50: 431-442.
210. 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.
211. Nuriya M, Huganir RL. 2006. Regulation of AMPA receptor trafficking by N-cadherin. J Neurochem 97: 652-661.
212. 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.
213. Ostroff LE, Cain CK, Bedont J, Monfils MH, Ledoux JE. 2010. Fear and safety learning differentially affect synapse size and dendritic translation in the lateral amygdala. Proc Natl Acad Sci 107: 9418-9423.
214. Ouyang Y, Wong M, Capani F, Rensing N, Lee CS, Liu Q, Neusch C, Martone ME, Wu JY, Yamada K, et al. 2005. Transient decrease in F-actin may be necessary for translocation of proteins into dendritic spines. Eur J Neurosci 22: 2995-3005.
215. Park M, Salgado JM, Ostroff L, Helton TD, Robinson CG, Harris KM, Ehlers MD. 2006. Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes. Neuron 52: 817-830.
216. Park MK, Choi YM, Kang YK, Petersen OH. 2008. The endoplasmic reticulum as an integrator of multiple dendritic events. Neuroscientist 14: 68-77.
217. Peters A, Palay SL,Webster D. 1976. The fine structure of the nervous system: The neurons and supporting cells. W.B. Saunders, Philadelphia.
218. 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.
219. Phillips LL, Pollack AE, Steward O. 1990. Protein synthesis in the neuropil of the rat dentate gyrus during synapse development. J Neurosci Res 26: 474-482.
220. Pierce JP, van Leyen K, McCarthy JB. 2000. Translocation machinery for synthesis of integral membrane and secretory proteins in dendritic spines. Nat Neurosci 3: 311- 313.
221. Poirazi P, Brannon T,Mel BW. 2003. Arithmetic of subthreshold synaptic summation in a model CA1 pyramidal cell. Neuron 37: 977-987.
222. Popov VI, Davies HA, Rogachevsky VV, Patrushev IV, Errington ML, Gabbott PL, Bliss TV, Stewart MG. 2004. Remodelling of synaptic morphology but unchanged synaptic density during late phase long-term potentiation (LTP): A serial section electron micrograph study in the dentate gyrus in the anaesthetised rat. Neurosci 128: 251-262.
223. Puthanveettil SV,Monje FJ, Miniaci MC, Choi YB, Karl KA, Khandros E, Gawinowicz MA, Sheetz MP, Kandel ER. 2008. A new component in synaptic plasticity: Upregulation of kinesin in the neurons of the gill-withdrawal reflex. Cell 135: 960-973.
224. Rajasethupathy P, Fiumara F, Sheridan R, Betel D, Puthanveettil SV, James J, Russo JJ, Sander C, Tuschl T, Kandel ER. 2009. Characterization of small RNAs in Aplysia reveals a role for MIR-124 in constraining long-term synaptic plasticity through CREB. Neuron 66: 803-817.
225. Rajasethupathy P, Antonov I, Sheridan R, Frey S, Sander C, Tuschl T, Kandel ER. 2012. A role for neuronal piRNAs in the epigenetic control of memory-related synaptic plasticity. Cell 149: 693-707.
226. Ramón y Cajal S. 1894. Croonian lecture. La fine structure des centres nerveux. Proc R Soc London 55: 444-468
227. De Felipe J and Jones EG. 1988. Cajal on the cerebral cortex. An annotated translation of the complete writings, pp. 83-88. Oxford University Press, New York.
228. Raymond CR, Redman SJ. 2006. Spatial segregation of neuronal calcium signals encodes different forms of LTP in rat hippocampus. J Physiol 570: 97-111.
229. Restivo L, Vetere G, Bontempi B, Ammassari-Teule M. 2009. The formation of recent and remote memory is associated with time-dependent formation of dendritic spines in the hippocampus and anterior cingulate cortex. J Neurosci 29: 8206-8214.
230. Reymann KG, Frey JU. 2007. The late maintenance of hippocampal LTP: Requirements, phases, "synaptic tagging," "late-associativity" and implications. Neuropharmacology 52: 24-40.
231. Rogerson T, Cai DJ, Frank A, Sano Y, Shobe J, Lopez-Aranda MF, Silva AJ. 2014. Synaptic tagging during memory allocation. Nat Rev Neurosci 15: 157-169.
232. Rongo C, Kaplan JM. 1999. CaMKII regulates the density of central glutamatergic synapses in vivo. Nature 402: 195- 199.
233. Sabo SL, Gomes RA, McAllister AK. 2006. Formation of presynaptic terminals at predefined sites along axons. J Neurosci 26: 10813-10825.
234. Saglietti L, Dequidt C, Kamieniarz K, Rousset MC, Valnegri P, Thoumine O, Beretta F, Fagni L, Choquet D, Sala C, et al. 2007. Extracellular interactions between GluR2 and Ncadherin in spine regulation. Neuron 54: 461-477.
235. Sanders J, Cowansage K, Baumgärtel K, Mayford M. 2012. Elimination of dendritic spines with long-term memory is specific to active circuits. J Neurosci 32: 12570-12578.
236. Sans N, Petralia RS, Wang YX, Blahos J, Hell JW, Wenthold RJ. 2000. A developmental change in NMDA receptorassociated proteins at hippocampal synapses. J Neurosci 20: 1260-1271.
237. Schacher S, Hu JY. 2014. The less things change, the more they are different: Contributions of long-term synaptic plasticity and homeostasis to memory. Learn Mem 21: 128-134.
238. Scheiffele P. 2003. Cell-cell signaling during synapse formation in the CNS. Annu Rev Neurosci 26: 485-508.
239. 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.
240. Schwartz H, Castellucci VF, Kandel ER. 1971. Functions of identified neurons and synapses in abdominal ganglion of Aplysia in absence of protein synthesis. J Neurophysiol 34: 9639-9653.
241. Sebeo J, Hsiao K, Bozdagi O, Dumitriu D, Ge Y, Zhou Q, Benson DL. 2009. Requirement for protein synthesis at developing synapses. J Neurosci 29: 9778-9793.
242. Senkov O, Sun M,Weinhold B, Gerardy-Schahn R, Schachner M, Dityatev A. 2006. Polysialylated neural cell adhesion molecule is involved in induction of long-term potentiation and memory acquisition and consolidation in a fear-conditioning paradigm. J Neurosci 26: 10888- 109898.
243. Sfakianos MK, Eisman A, Gourley SL, Bradley WD, Scheetz AJ, Settleman J, Taylor JR, Greer CA, Williamson A, Koleske AJ. 2007. Inhibition of Rho via Arg and p190Rho- GAP in the postnatal mouse hippocampus regulates dendritic spine maturation, synapse and dendrite stability, and behavior. J Neurosci 27: 10982-10992.
244. 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.
245. Sheng M, Hoogenraad CC. 2007. The postsynaptic architecture of excitatory synapses: A more quantitative view. Annu Rev Biochem 76: 823-847.
246. Shepherd GM, Harris KM. 1998. Three-dimensional structure and composition of CA3 → CA1 axons in rat hippocampal slices: Implications for presynaptic connectivity and compartmentalization. JNeurosci 18: 8300-8310.
247. Sherrington CS. 1897. The central nervous system. In A textbook of physiology, 7th ed. (ed. Foster M), Vol. 3.Mac- Millan, London.
248. Shu X, Lev-Ram V, Deerinck TJ, Qi Y, Ramko EB, Davidson MW, Jin Y, Ellisman MH, Tsien RY. 2011. A genetically encoded tag for correlated light and electron microscopy of intact cells, tissues, and organisms. PLoS Biol 9: e1001041.
249. Si K. 2015. Long-term maintenance. Cold Spring Harb Perspect Biol doi: 10.1101/cshperspect.a021774.
250. Si K, Giustetto M, Etkin A, Hsu R, Janisiewicz AM, Miniaci MC, Kim JH, Zhu H, Kandel ER. 2003. A neuronal isoform of CPEB regulates local protein synthesis and stabilizes synapse-specific long-term facilitation in Aplysia. Cell 115: 893-904.
251. Soler-Llavina GJ, Arstikaitis P,MorishitaW, Ahmad M, Sudhof TC, Malenka RC. 2013. Leucine-rich repeat transmembrane proteins are essential for maintenance of long-term potentiation. Neuron 79: 439-446.
252. Song JY, Ichtchenko K, Sudhof TC, Brose N. 1999. Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc Natl Acad Sci 96: 1100-1105.
253. Sorra KE, Harris KM. 2000. Overview on the structure, composition, function, development, and plasticity of hippocampal dendritic spines. Hippocampus 10: 501- 511.
254. 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.
255. 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.
256. Spacek J, Harris KM. 1998. Three-dimensional organization of cell adhesion junctions at synapses and dendritic spines in areaCA1 of the rat hippocampus. J CompNeurol 393: 58-68.
257. Spacek J, Lieberman AR. 1974. Ultrastructure and threedimensional organization of synaptic glomeruli in rat somatosensory thalamus. J Anat 117: 487-516.
258. 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 107: 11116-11121.
259. Staubli U, Lynch G. 1987. Stable hippocampal long-term potentiation elicited by "θ" pattern stimulation. Brain Res 435: 227-234.
260. Steiner P, Higley MJ, Xu W, Czervionke BL, Malenka RC, Sabatini BL. 2008. Destabilization of the postsynaptic density by PSD-95 serine 73 phosphorylation inhibits spine growth and synaptic plasticity. Neuron 60: 788- 802.
261. Stettler DD, Yamahachi H, LiW, DenkW, Gilbert CD. 2006. Axons and synaptic boutons are highly dynamic in adult visual cortex. Neuron 49: 877-887.
262. StewardO, Schuman EM. 2001. Protein synthesis at synaptic sites on dendrites. Annu Rev Neurosci 24: 299-325.
263. Stewart MG, Medvedev NI, Popov VI, Schoepfer R, Davies HA, Murphy K, Dallerac GM, Kraev IV, Rodriguez JJ. 2005. 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 JNeurosci 21: 3368-3378.
264. Stuart G, Spruston N, Hausser M. 2008. Dendrites, 2nd ed. Oxford University Press, New York.
265. Sudhof TC. 2008. Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455: 903-911.
266. Sutton MA, Masters SE, Bagnall MW, Carew TJ. 2001. Molecular mechanisms underlying a unique intermediate phase of memory in Aplysia. Neuron 31: 143-154.
267. 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.
268. Takeuchi T, Duszkiewicz AJ, Morris RG. 2014. The synaptic plasticity and memory hypothesis: Encoding, storage and persistence. Philos Trans R Soc Lond B Biol Sci 369: 20130288.
269. Tanaka H, Shan W, Phillips GR, Arndt K, Bozdagi O, Shapiro L, HuntleyGW, Benson DL, Colman DR. 2000. Molecular modification of N-cadherin in response to synaptic activity. Neuron 25: 93-107.
270. Toni N, Teng EM, Bushong EA, Aimone JB, Zhao C, Consiglio A, van Praag H, Martone ME, Ellisman MH, Gage FH. 2007. Synapse formation on neurons born in the adult hippocampus. Nat Neurosci 10: 727-734.
271. Trommald M, Hulleberg G, Andersen P. 1996. Long-term potentiation is associated with new excitatory spine synapses on rat dentate granule cells. Learn Mem3: 218-228.
272. Turrigiano G. 2007. Homeostatic signaling: The positive side of negative feedback. Curr Opin Neurobiol 17: 318- 324.
273. Turrigiano GG, Nelson SB. 2004. Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5: 97- 107.
274. 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.
275. Udo H, Jin I, Kim J-H, Li H-L, Youn T, Hawkins RD, Kandel ER, Bailey CH. 2005. Serotonin-induced regulation of the actin network for learning-related synaptic growth requires CdC42, N-WASP and PAK in Aplysia sensory neurons. Neuron 45: 887-901.
276. Van Harreveld A, Fifkova E. 1975. Swelling of dendritic spines in the fascia dentata after stimulation of the perforant fibers as a mechanism of post-tetanic potentiation. Exp Neurol 49: 736-749.
277. Van Horn SC, Erisir A, Sherman SM. 2000. Relative distribution of synapses in the A-laminae of the lateral geniculate nucleus of the cat. J Comp Neurol 416: 509-520.
278. Vaughn JE. 1989. Fine structure of synaptogenesis in the vertebrate central nervous system. Synapse 3: 255-285.
279. Ventura R, Harris KM. 1999. Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 19: 6897-6906.
280. Wainwright ML, Zhang H, Byrne JH, Cleary LJ. 2002. Localized neuronal outgrowth induced by long-term sensitization training in Aplysia. J Neurosci 22: 4132-4141.
281. Waites CL, Craig AM, Garner CC. 2005. Mechanisms of vertebrate synaptogenesis. Annu Rev Neurosci 28: 251- 274.
282. Wang Y, Zhu G, Briz V, Hsu YT, Bi X, Baudry M. 2014. A molecular brake controls the magnitude of long-term potentiation. Nat Commun 5: 3051.
283. Wilke SA, Antonios JK, Bushong EA, Badkoobehi A, Malek E, Hwang M, Terada M, Ellisman MH, Ghosh A. 2013. Deconstructing complexity: Serial block-face electron microscopic analysis of the hippocampal mossy fiber synapse. J Neurosci 33: 507-522.
284. Witcher MR, Kirov SA, Harris KM. 2007. Plasticity of perisynaptic astroglia during synaptogenesis in the mature rat hippocampus. Glia 55: 13-23.
285. 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 106: 13564-13569.
286. Xu T, Yu X, Perlik AJ, Tobin WF, Zweig JA, Tennant K, Jones T, Zuo Y. 2009. Rapid formation and selective stabilization of synapses for enduring motor memories. Nature 462: 915-919.
287. Yang Y, Wang XB, Frerking M, Zhou Q. 2008. Spine expansion and stabilization associated with long-term potentiation. J Neurosci 28: 5740-5751.
288. Yang G, Pan F, Gan WB. 2009. Stably maintained dendritic spines are associated with lifelong memories.Nature 462: 920-924.
289. Young JZ, Nguyen PV. 2005. Homosynaptic and heterosynaptic inhibition of synaptic tagging and capture of long-term potentiation by previous synaptic activity. J Neurosci 25: 7221-7231.
290. Yuste R, Bonhoeffer T. 2001. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 24: 1071-1089.
291. 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.
292. Zhou Q, Homma KJ, Poo MM. 2004. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44: 749-757.
293. Zito K, Parnas D, Fetter RD, Isacoff EY, Goodman CS. 1999. Watching a synapse grow: Noninvasive confocal imaging of synaptic growth in Drosophila. Neuron 22: 719-729.
294. Ziv NE, Garner CC. 2004. Cellular mechanisms of presynaptic assembly. Nat Rev Neurosci 5: 385-399.