CoChat
Sign Up
Cited by 352Neuroscience and Neuropharmacology ResearchCellular transport and secretionNeuroinflammation and Neurodegeneration Mechanisms

Transcellular Nanoalignment of Synaptic Function

Open access
Biederer, Thomas, Kaeser, Pascal S., Blanpied, Thomas A.·2017·Neuron
DOI 10.1016/j.neuron.2017.10.006PMC PMC5777221
Open this paper in CoChat — free accountOpen PDF

Abstract

At each of the brain's vast number of synapses, the presynaptic nerve terminal, synaptic cleft, and postsynaptic specialization form a transcellular unit to enable efficient transmission of information between neurons. While we know much about the molecular machinery within each compartment, we are only beginning to understand how these compartments are structurally registered and functionally integrated with one another. This review will describe the organization of each compartment and then discuss their alignment across pre- and postsynaptic cells at a nanometer scale. We propose that this architecture may allow for precise synaptic information exchange and may be modulated to contribute to the remarkable plasticity of brain function.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.neuron.2017.10.006

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • When the CTD of neuroligin 1 is included, it partitions with AMPAR/TARPs but not with NMDARs, reminiscent of nanocolumns in the PSD.

    “Remarkably, when the CTD of neuroligin 1 is included, it partitions with the AMPAR/TARPs but not with the NMDARs, reminiscent of nanocolumns in the PSD (251–253)”

    From Synaptic memory and CaMKII (2023) · cites this paper as [252]

    In “Lateral patterning of cytosolic PSD components” (page unavailable), the paper reports that AMPARs and NMDARs occupy separate synaptic zones in EM tomography and that TARPs associate with AMPAR scaffolds. But it does not report that the CTD of neuroligin-1 partitions with AMPAR/TARPs rather than NMDARs; its “Candidate mechanisms of trans-synaptic alignment” section instead describes neuroligin-1 as broadly distributed over the PSD. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

  • AMPAR clusters are juxtaposed across from the presynaptic release site.

    “Of particular interest is the finding that these clusters are juxtaposed across from presynaptic release site (251, 252, 260).”

    From Synaptic memory and CaMKII (2023) · cites this paper as [252]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

No citation lists for this paper

No citation lists for this paper yet — checked again daily.

References 242 · Cited by 352

Research works printed but not linked: 203

  1. Acuna C Liu X Gonzalez A Südhof TC 2015 RIM-BPs Mediate Tight Coupling of Action Potentials to Ca<sup>2+</sup>-Triggered Neurotransmitter Release Neuron 87 1234 1247 26402606
  2. Ahmad-Annuar A Ciani L Simeonidis I Herreros J Fredj NB Rosso SB Hall A Brickley S Salinas PC 2006 Signaling across the synapse: a role for Wnt and Dishevelled in presynaptic assembly and neurotransmitter release J Cell Biol 174 127 139 16818724 PMC2064170
  3. Anderson GR Aoto J Tabuchi K Foldy C Covy J Yee AX Wu D Lee SJ Chen L Malenka RC Sudhof TC 2015 beta-Neurexins Control Neural Circuits by Regulating Synaptic Endocannabinoid Signaling Cell 162 593 606 26213384 PMC4709013
  4. Andrews-Zwilling YS Kawabe H Reim K Varoqueaux F Brose N 2006 Binding to Rab3A-interacting molecule RIM regulates the presynaptic recruitment of Munc13-1 and ubMunc13-2 The Journal of biological chemistry 281 19720 19731 16704978
  5. Aoto J Martinelli DC Malenka RC Tabuchi K Sudhof TC 2013 Presynaptic neurexin-3 alternative splicing trans-synaptically controls postsynaptic AMPA receptor trafficking Cell 154 75 88 23827676 PMC3756801
  6. Arons MH Thynne CJ Grabrucker AM Li D Schoen M Cheyne JE Boeckers TM Montgomery JM Garner CC 2012 Autism-associated mutations in ProSAP2/Shank3 impair synaptic transmission and neurexin-neuroligin-mediated transsynaptic signaling J Neurosci 32 14966 14978 23100419 PMC3752148
  7. Augustin I Rosenmund C Sudhof TC Brose N 1999 Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles Nature 400 457 461 10440375
  8. Bats C Groc L Choquet D 2007 The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking Neuron 53 719 734 17329211
  9. Beaubien F Raja R Kennedy TE Fournier AE Cloutier JF 2016 Slitrk1 is localized to excitatory synapses and promotes their development Sci Rep 6 27343 27273464 PMC4895136
  10. Biederer T Sara Y Mozhayeva M Atasoy D Liu X Kavalali ET Südhof TC 2002 SynCAM, a synaptic adhesion molecule that drives synapse assembly Science 297 1525 1531 12202822
  11. Bloom FE Aghajanian GK 1966 Cytochemistry of synapses: selective staining for electron microscopy Science 154 1575 1577 5924927
  12. Borst JG Sakmann B 1996 Calcium influx and transmitter release in a fast CNS synapse Nature 383 431 434 8837774
  13. Boyken J Grønborg M Riedel D Urlaub H Jahn R Chua JJ 2013 Molecular Profiling of Synaptic Vesicle Docking Sites Reveals Novel Proteins but Few Differences between Glutamatergic and GABAergic Synapses Neuron 78 285 297 23622064
  14. Broadhead MJ Horrocks MH Zhu F Muresan L Benavides-Piccione R DeFelipe J Fricker D Kopanitsa MV Duncan RR Klenerman D Komiyama NH Lee SF Grant SG 2016 PSD95 nanoclusters are postsynaptic building blocks in hippocampus circuits Sci Rep 6 24626 27109929 PMC4842999
  15. Bucurenciu I Kulik A Schwaller B Frotscher M Jonas P 2008 Nanodomain coupling between Ca2+ channels and Ca2+ sensors promotes fast and efficient transmitter release at a cortical GABAergic synapse Neuron 57 536 545 18304483
  16. Budreck EC Kwon OB Jung JH Baudouin S Thommen A Kim HS Fukazawa Y Harada H Tabuchi K Shigemoto R Scheiffele P Kim JH 2013 Neuroligin-1 controls synaptic abundance of NMDA-type glutamate receptors through extracellular coupling Proc Natl Acad Sci U S A 110 725 730 23269831 PMC3545745
  17. Burette AC Lesperance T Crum J Martone M Volkmann N Ellisman MH Weinberg RJ 2012 Electron tomographic analysis of synaptic ultrastructure J Comp Neurol 520 2697 2711 22684938 PMC3856703
  18. Burger PM Mehl E Cameron PL Maycox PR Baumert M Lottspeich F De Camilli P Jahn R 1989 Synaptic vesicles immunoisolated from rat cerebral cortex contain high levels of glutamate Neuron 3 715 720 2577130
  19. Calakos N Schoch S Sudhof TC Malenka RC 2004 Multiple roles for the active zone protein RIM1alpha in late stages of neurotransmitter release Neuron 42 889 896 15207234
  20. Chamma I Letellier M Butler C Tessier B Lim KH Gauthereau I Choquet D Sibarita JB Park S Sainlos M Thoumine O 2016 Mapping the dynamics and nanoscale organization of synaptic adhesion proteins using monomeric streptavidin Nat Commun 7 10773 26979420 PMC4799371
  21. Chanda S Hale WD Zhang B Wernig M Sudhof TC 2017 Unique versus Redundant Functions of Neuroligin Genes in Shaping Excitatory and Inhibitory Synapse Properties J Neurosci 37 6816 6836 28607166 PMC5518416
  22. Cheadle L Biederer T 2012 The novel synaptogenic protein Farp1 links postsynaptic cytoskeletal dynamics and transsynaptic organization J Cell Biol 199 985 1001 23209303 PMC3518221
  23. Chen J Billings SE Nishimune H 2011 Calcium channels link the muscle-derived synapse organizer laminin beta2 to Bassoon and CAST/Erc2 to organize presynaptic active zones The Journal of neuroscience: the official journal of the Society for NeuroScience 31 512 525 21228161 PMC3723116
  24. Chen LY Jiang M Zhang B Gokce O Sudhof TC 2017 Conditional Deletion of All Neurexins Defines Diversity of Essential Synaptic Organizer Functions for Neurexins Neuron 94 611 625 e614 28472659 PMC5501922
  25. Chen X Nelson CD Li X Winters CA Azzam R Sousa AA Leapman RD Gainer H Sheng M Reese TS 2011 PSD-95 Is Required to Sustain the Molecular Organization of the Postsynaptic Density J Neurosci 31 6329 6338 21525273 PMC3099547
  26. 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 18326622 PMC2393784
  27. Chih B Engelman H Scheiffele P 2005 Control of excitatory and inhibitory synapse formation by neuroligins Science 307 1324 1328 15681343
  28. Choi Y Nam J Whitcomb DJ Song YS Kim D Jeon S Um JW Lee SG Woo J Kwon SK Li Y Mah W Kim HM Ko J Cho K Kim E 2016 SALM5 trans-synaptically interacts with LAR-RPTPs in a splicing-dependent manner to regulate synapse development Sci Rep 6 26676 27225731 PMC4881023
  29. Choquet D Triller A 2013 The dynamic synapse Neuron 80 691 703 24183020
  30. Christie JM Jahr CE 2006 Multivesicular release at Schaffer collateral-CA1 hippocampal synapses J Neurosci 26 210 216 16399689 PMC2670931
  31. Chubykin AA Atasoy D Etherton MR Brose N Kavalali ET Gibson JR Südhof TC 2007 Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2 Neuron 54 919 931 17582332 PMC3738748
  32. Constals A Penn AC Compans B Toulme E Phillipat A Marais S Retailleau N Hafner AS Coussen F Hosy E Choquet D 2015 Glutamate-induced AMPA receptor desensitization increases their mobility and modulates short-term plasticity through unbinding from Stargazin Neuron 85 787 803 25661182
  33. Couteaux R Pecot-Dechavassine M 1970 [Synaptic vesicles and pouches at the level of “active zones” of the neuromuscular junction] C R Acad Sci Hebd Seances Acad Sci D 271 2346 2349 4995202
  34. Dalva MB Takasu MA Lin MZ Shamah SM Hu L Gale NW Greenberg ME 2000 EphB receptors interact with NMDA receptors and regulate excitatory synapse formation Cell 103 945 956 11136979
  35. Dani A Huang B Bergan J Dulac C Zhuang X 2010 Superresolution imaging of chemical synapses in the brain Neuron 68 843 856 21144999 PMC3057101
  36. Davydova D Marini C King C Klueva J Bischof F Romorini S Montenegro-Venegas C Heine M Schneider R Schroder MS Altrock WD Henneberger C Rusakov DA Gundelfinger ED Fejtova A 2014 Bassoon specifically controls presynaptic P/Q-type Ca(2+) channels via RIM-binding protein Neuron 82 181 194 24698275
  37. de Wit J Ghosh A 2016 Specification of synaptic connectivity by cell surface interactions Nat Rev Neurosci 17 22 35 26656254
  38. de Wit J Sylwestrak E O’Sullivan ML Otto S Tiglio K Savas JN Yates JR 3rd Comoletti D Taylor P Ghosh A 2009 LRRTM2 interacts with Neurexin1 and regulates excitatory synapse formation Neuron 64 799 806 20064388 PMC2829666
  39. Dean C Scholl FG Choih J DeMaria S Berger J Isacoff E Scheiffele P 2003 Neurexin mediates the assembly of presynaptic terminals Nature NeuroScience 6 708 716 12796785 PMC1646425
  40. DeGiorgis J Galbraith J Dosemeci A Chen X Reese T 2008 Distribution of the scaffolding proteins PSD-95, PSD-93, and SAP97 in isolated PSDs Brain Cell Biology 18392731
  41. Eggermann E Bucurenciu I Goswami SP Jonas P 2011 Nanodomain coupling between Ca2+ channels and sensors of exocytosis at fast mammalian synapses Nature Reviews NeuroScience 13 7 21 22183436 PMC3617475
  42. 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 17481397 PMC1993808
  43. 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 17360496 PMC1820728
  44. Elegheert J Cvetkovska V Clayton AJ Heroven C Vennekens KM Smukowski SN Regan MC Jia W Smith AC Furukawa H Savas JN de Wit J Begbie J Craig AM Aricescu AR 2017 Structural Mechanism for Modulation of Synaptic Neuroligin-Neurexin Signaling by MDGA Proteins Neuron 95 896 913 e810 28817804 PMC5563082
  45. Elegheert J Kakegawa W Clay JE Shanks NF Behiels E Matsuda K Kohda K Miura E Rossmann M Mitakidis N Motohashi J Chang VT Siebold C Greger IH Nakagawa T Yuzaki M Aricescu AR 2016 Structural basis for integration of GluD receptors within synaptic organizer complexes Science 353 295 299 27418511 PMC5291321
  46. Elias GM Funke L Stein V Grant SG Bredt DS Nicoll RA 2006 Synapse-specific and developmentally regulated targeting of AMPA receptors by a family of MAGUK scaffolding proteins Neuron 52 307 320 17046693
  47. Elste AM Benson DL 2006 Structural basis for developmentally regulated changes in cadherin function at synapses J Comp Neurol 495 324 335 16440298
  48. Erreger K Dravid SM Banke TG Wyllie DJ Traynelis SF 2005 Subunit-specific gating controls rat NR1/NR2A and NR1/NR2B NMDA channel kinetics and synaptic signalling profiles J Physiol 563 345 358 15649985 PMC1665591
  49. Fedchyshyn MJ Wang L-Y 2005 Developmental transformation of the release modality at the calyx of Held synapse The Journal of neuroScience 25 4131 4140 15843616 PMC6724960
  50. Fell B Eckrich S Blum K Eckrich T Hecker D Obermair GJ Munkner S Flockerzi V Schick B Engel J 2016 alpha2delta2 Controls the Function and Trans-Synaptic Coupling of Cav1.3 Channels in Mouse Inner Hair Cells and Is Essential for Normal Hearing J Neurosci 36 11024 11036 27798183 PMC6705655
  51. Fogel AI Stagi M Perez de Arce K Biederer T 2011 Lateral assembly of the immunoglobulin protein SynCAM 1 controls its adhesive function and instructs synapse formation EMBO J 30 4728 4738 21926970 PMC3243608
  52. Foster KA Crowley JJ Regehr WG 2005 The influence of multivesicular release and postsynaptic receptor saturation on transmission at granule cell to Purkinje cell synapses J Neurosci 25 11655 11665 16354924 PMC6726039
  53. Frank RA Grant SG 2017 Supramolecular organization of NMDA receptors and the postsynaptic density Curr Opin Neurobiol 45 139 147 28577431 PMC5557338
  54. Franks KM Bartol TMJ Sejnowski TJ 2002 A Monte Carlo model reveals independent signaling at central glutamatergic synapses Biophys J 83 2333 2348 12414671 PMC1302323
  55. Freche D Pannasch U Rouach N Holcman D 2011 Synapse geometry and receptor dynamics modulate synaptic strength PLoS One 6 e25122 21984900 PMC3184958
  56. Fukata M Fukata Y Adesnik H Nicoll RA Bredt DS 2004 Identification of PSD-95 Palmitoylating Enzymes Neuron 44 987 996 15603741
  57. 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 17237775 PMC4755312
  58. Gangwar SP Zhong X Seshadrinathan S Chen H Machius M Rudenko G 2017 Molecular Mechanism of MDGA1: Regulation of Neuroligin 2:Neurexin Trans-synaptic Bridges Neuron 94 1132 1141 e1134 28641112 PMC5745067
  59. Garcia EP McPherson PS Chilcote TJ Takei K De Camilli P 1995 rbSec1A and B colocalize with syntaxin 1 and SNAP-25 throughout the axon, but are not in a stable complex with syntaxin J Cell Biol 129 105 120 7698978 PMC2120371
  60. Glebov OO Cox S Humphreys L Burrone J 2016 Neuronal activity controls transsynaptic geometry Sci Rep 6 22703 26951792 PMC4782104
  61. Graf ER Zhang X Jin S-X Linhoff MW Craig AM 2004 Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins Cell 119 1013 1026 15620359 PMC2826211
  62. Gray EG 1959 Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study J Anat 93 420 433 13829103 PMC1244535
  63. Gray EG 1975 Synaptic fine structure and nuclear, cytoplasmic and extracellular networks: The stereoframework concept J Neurocytol 4 315 339 1133591
  64. Greger IH Watson JF Cull-Candy SG 2017 Structural and Functional Architecture of AMPA-Type Glutamate Receptors and Their Auxiliary Proteins Neuron 94 713 730 28521126
  65. Grunwald IC Korte M Wolfer D Wilkinson GA Unsicker K Lipp HP Bonhoeffer T Klein R 2001 Kinase-independent requirement of EphB2 receptors in hippocampal synaptic plasticity Neuron 32 1027 1040 11754835
  66. Han Y Babai N Kaeser P Südhof TC Schneggenburger R 2015 RIM1 and RIM2 redundantly determine Ca2+ channel density and readily releasable pool size at a large hindbrain synapse Journal of Neurophysiology 113 255 263 25343783 PMC4380487
  67. Han Y Kaeser PS Südhof TC Schneggenburger R 2011 RIM Determines Ca(2+) Channel Density and Vesicle Docking at the Presynaptic Active Zone Neuron 69 304 316 21262468 PMC3259453
  68. Hansen KB Ogden KK Yuan H Traynelis SF 2014 Distinct functional and pharmacological properties of Triheteromeric GluN1/GluN2A/GluN2B NMDA receptors Neuron 81 1084 1096 24607230 PMC3957490
  69. 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 11206537
  70. Harris KM Weinberg RJ 2012 Ultrastructure of synapses in the mammalian brain Cold Spring Harb Perspect Biol 4 PMC3331701 22357909
  71. Heine M Groc L Frischknecht R Beique JC Lounis B Rumbaugh G Huganir RL Cognet L Choquet D 2008 Surface mobility of postsynaptic AMPARs tunes synaptic transmission Science 320 201 205 18403705 PMC2715948
  72. Held RG Liu C Kaeser PS 2016 ELKS controls the pool of readily releasable vesicles at excitatory synapses through its N-terminal coiled-coil domains eLife 5 PMC4935463 27253063
  73. Hibino H Pironkova R Onwumere O Vologodskaia M Hudspeth AJ Lesage F 2002 RIM binding proteins (RBPs) couple Rab3-interacting molecules (RIMs) to voltage-gated Ca(2+) channels Neuron 34 411 423 11988172 PMC2151925
  74. High B Cole AA Chen X Reese TS 2015 Electron microscopic tomography reveals discrete transcleft elements at excitatory and inhibitory synapses Front Synaptic Neurosci 7 9 26113817 PMC4461817
  75. Holmes WR 1995 Modeling the effect of glutamate diffusion and uptake on NMDA and non-NMDA receptor saturation Biophys J 69 1734 1747 8580317 PMC1236407
  76. Honigmann A van den Bogaart G Iraheta E Risselada HJ Milovanovic D Mueller V Mullar S Diederichsen U Fasshauer D Grubmuller H Hell SW Eggeling C Kuhnel K Jahn R 2013 Phosphatidylinositol 4,5-bisphosphate clusters act as molecular beacons for vesicle recruitment Nat Struct Mol Biol 20 679 686 23665582 PMC3676452
  77. Hoppa MB Lana B Margas W Dolphin AC Ryan TA 2012 alpha2delta expression sets presynaptic calcium channel abundance and release probability Nature 486 122 125 22678293 PMC3376018
  78. Ichimura T Hashimoto PH 1988 Structural components in the synaptic cleft captured by freeze-substitution and deep etching of directly frozen cerebellar cortex J Neurocytol 17 3 12 3047323
  79. Ishikawa T Sahara Y Takahashi T 2002 A single packet of transmitter does not saturate postsynaptic glutamate receptors Neuron 34 613 621 12062044
  80. Jahn R Fasshauer D 2012 Molecular machines governing exocytosis of synaptic vesicles Nature 490 201 207 23060190 PMC4461657
  81. Jedlicka P Vnencak M Krueger DD Jungenitz T Brose N Schwarzacher SW 2015 Neuroligin-1 regulates excitatory synaptic transmission, LTP and EPSP-spike coupling in the dentate gyrus in vivo Brain Struct Funct 220 47 58 25713840
  82. Jeyifous O Lin EI Chen X Antinone SE Mastro R Drisdel R Reese TS Green WN 2016 Palmitoylation regulates glutamate receptor distributions in postsynaptic densities through control of PSD95 conformation and orientation Proc Natl Acad Sci U S A 113 E8482 E8491 27956638 PMC5206547
  83. Kaeser PS Deng L Chavez AE Liu X Castillo PE Sudhof TC 2009 ELKS2alpha/CAST deletion selectively increases neurotransmitter release at inhibitory synapses Neuron 64 227 239 19874790 PMC2785857
  84. Kaeser PS Deng L Wang Y Dulubova I Liu X Rizo J Südhof TC 2011 RIM proteins tether Ca2+ channels to presynaptic active zones via a direct PDZ-domain interaction Cell 144 282 295 21241895 PMC3063406
  85. Kaeser PS Regehr WG 2017 The readily releasable pool of synaptic vesicles Current Opinion in Neurobiology 43 63 70 28103533 PMC5447466
  86. Kaufmann N DeProto J Ranjan R Wan H Van Vactor D 2002 Drosophila liprin-alpha and the receptor phosphatase Dlar control synapse morphogenesis Neuron 34 27 38 11931739
  87. Kawabe H Mitkovski M Kaeser PS Hirrlinger J Opazo F Nestvogel D Kalla S Fejtova A Verrier SE Bungers SR Cooper BH Varoqueaux F Wang Y Nehring RB Gundelfinger ED Rosenmund C Rizzoli SO Sudhof TC Rhee J-S Brose N 2017 ELKS1 localizes the synaptic vesicle priming protein bMunc13-2 to a specific subset of active zones The Journal of cell biology 216 1143 1161 28264913 PMC5379939
  88. Keller D Babai N Kochubey O Han Y Markram H Schürmann F Schneggenburger R 2015 An Exclusion Zone for Ca<sup>2+</sup> Channels around Docked Vesicles Explains Release Control by Multiple Channels at a CNS Synapse PLoS Computational Biology 11 PMC4423980 25951120
  89. Kerr JM Blanpied TA 2012 Subsynaptic AMPA receptor distribution is acutely regulated by actin-driven reorganization of the postsynaptic density J Neurosci 32 658 673 22238102 PMC3596168
  90. Kharazia VN Weinberg RJ 1997 Tangential synaptic distribution of NMDA and AMPA receptors in rat neocortex Neurosci Lett 238 41 44 9464650
  91. Kim JA Kim D Won SY Han KA Park D Cho E Yun N An HJ Um JW Kim E Lee JO Ko J Kim HM 2017 Structural Insights into Modulation of Neurexin-Neuroligin Trans-synaptic Adhesion by MDGA1/Neuroligin-2 Complex Neuron 94 1121 1131 e1126 28641111
  92. Kittel RJRJ Wichmann C Rasse TM Fouquet W Schmidt M Schmid A Wagh DA Pawlu C Kellner RR Willig KI Hell SW Buchner E Heckmann M Sigrist SJ 2006 Bruchpilot promotes active zone assembly, Ca2+ channel clustering, and vesicle release Science … 312 1051 1054 16614170
  93. Kiyonaka S Wakamori M Miki T Uriu Y Nonaka M Bito H Beedle AM Mori E Hara Y De Waard M Kanagawa M Itakura M Takahashi M Campbell KP Mori Y 2007 RIM1 confers sustained activity and neurotransmitter vesicle anchoring to presynaptic Ca2+ channels Nature neuroScience 10 691 701 17496890 PMC2687938
  94. Korber N Stein V 2016 In vivo imaging demonstrates dendritic spine stabilization by SynCAM 1 Sci Rep 6 24241 27053173 PMC4823656
  95. Krueger-Burg D Papadopoulos T Brose N 2017 Organizers of inhibitory synapses come of age Curr Opin Neurobiol 45 66 77 28460365
  96. Kullmann DM Asztely F 1998 Extrasynaptic glutamate spillover in the hippocampus: evidence and implications Trends Neurosci 21 8 14 9464678
  97. Kurshan PT Oztan A Schwarz TL 2009 Presynaptic alpha2delta-3 is required for synaptic morphogenesis independent of its Ca2+-channel functions Nat Neurosci 12 1415 1423 19820706 PMC2996863
  98. Kwon HB Sabatini BL 2011 Glutamate induces de novo growth of functional spines in developing cortex Nature 474 100 104 21552280 PMC3107907
  99. Li TP Blanpied TA 2016 Control of Transmembrane Protein Diffusion within the Postsynaptic Density Assessed by Simultaneous Single-Molecule Tracking and Localization Microscopy Front Synaptic Neurosci 8 19 27499742 PMC4956670
  100. Li TP Song Y MacGillavry HD Blanpied TA Raghavachari S 2016 Protein Crowding within the Postsynaptic Density Can Impede the Escape of Membrane Proteins J Neurosci 36 4276 4295 27076425 PMC4829651
  101. Li Y Zhang P Choi TY Park SK Park H Lee EJ Lee D Roh JD Mah W Kim R Kim Y Kwon H Bae YC Choi SY Craig AM Kim E 2015 Splicing-Dependent Trans-synaptic SALM3-LAR-RPTP Interactions Regulate Excitatory Synapse Development and Locomotion Cell Rep 12 1618 1630 26321637 PMC4578660
  102. Li YX Xu Y Ju D Lester HA Davidson N Schuman EM 1998 Expression of a dominant negative TrkB receptor, T1, reveals a requirement for presynaptic signaling in BDNF-induced synaptic potentiation in cultured hippocampal neurons Proc Natl Acad Sci U S A 95 10884 10889 9724799 PMC27990
  103. Lisman J Raghavachari S 2006 A Unified Model of the Presynaptic and Postsynaptic Changes During LTP at CA1 Synapses. Sci STKE 2006 re11- 17033044
  104. Liu C Bickford LS Held RG Nyitrai H Sudhof TC Kaeser PS 2014 The Active Zone Protein Family ELKS Supports Ca2+ Influx at Nerve Terminals of Inhibitory Hippocampal Neurons The Journal of neuroscience: the official journal of the Society for NeuroScience 34 12289 12303 25209271 PMC4160768
  105. 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 10069344
  106. Lucic V Yang T Schweikert G Forster F Baumeister W 2005 Morphological characterization of molecular complexes present in the synaptic cleft Structure 13 423 434 15766544
  107. Lujan R Nusser Z Roberts JD Shigemoto R Somogyi P 1996 Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus Eur J Neurosci 8 1488 1500 8758956
  108. MacGillavry HD Kerr JM Blanpied TA 2011 Lateral organization of the postsynaptic density Mol Cell Neurosci 48 321 331 21920440 PMC3216044
  109. MacGillavry HD Song Y Raghavachari S Blanpied TA 2013 Nanoscale scaffolding domains within the postsynaptic density concentrate synaptic AMPA receptors Neuron 78 615 622 23719161 PMC3668352
  110. Maschi D Klyachko VA 2017 Spatiotemporal Regulation of Synaptic Vesicle Fusion Sites in Central Synapses Neuron 94 65 73 e63 28343869
  111. Masugi-Tokita M Tarusawa E Watanabe M Molnar E Fujimoto K Shigemoto R 2007 Number and density of AMPA receptors in individual synapses in the rat cerebellum as revealed by SDS-digested freeze-fracture replica labeling J Neurosci 27 2135 2144 17314308 PMC6673557
  112. McAllister AK Stevens CF 2000 Nonsaturation of AMPA and NMDA receptors at hippocampal synapses PNAS 97 6173 6178 10811899 PMC18577
  113. Melom JE Akbergenova Y Gavornik JP Littleton JT 2013 Spontaneous and evoked release are independently regulated at individual active zones J Neurosci 33 17253 17263 24174659 PMC3812501
  114. Miki T Kaufmann WA Malagon G Gomez L Tabuchi K Watanabe M Shigemoto R Marty A 2017 Numbers of presynaptic Ca2+ channel clusters match those of functionally defined vesicular docking sites in single central synapses Proc Natl Acad Sci U S A 114 E5246 E5255 28607047 PMC5495264
  115. Miki T Malagon G Pulido C Llano I Neher E Marty A 2016 Actin- and Myosin-Dependent Vesicle Loading of Presynaptic Docking Sites Prior to Exocytosis Neuron 91 808 823 27537485
  116. Missler M Südhof TC Biederer T 2012 Synaptic cell adhesion Synapses Südhof TC Sheng M Sabatini B Cold Spring Harbor Laboratory Press 31 48 PMC3312681 22278667
  117. Missler M Zhang WQ Rohlmann A Kattenstroth G Hammer RE Gottmann K Südhof TC 2003 alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis Nature 423 939 948 12827191
  118. 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 21940442 PMC6623291
  119. Muller CS Haupt A Bildl W Schindler J Knaus HG Meissner M Rammner B Striessnig J Flockerzi V Fakler B Schulte U 2010 Quantitative proteomics of the Cav2 channel nano-environments in the mammalian brain Proceedings of the National Academy of Sciences of the United States of America 107 14950 14957 20668236 PMC2930569
  120. Müller M Liu KSY Sigrist SJ Davis GW 2012 RIM controls homeostatic plasticity through modulation of the readily-releasable vesicle pool The Journal of neuroscience: the official journal of the Society for NeuroScience 32 16574 16585 23175813 PMC3523185
  121. Nagwaney S Harlow ML Jung JH Szule JA Ress D Xu J Marshall RM McMahan UJ 2009 Macromolecular connections of active zone material to docked synaptic vesicles and presynaptic membrane at neuromuscular junctions of mouse The Journal of comparative neurology 513 457 468 19226520 PMC4288958
  122. 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 23926273 PMC6619720
  123. Nicoll RA 2017 A Brief History of Long-Term Potentiation Neuron 93 281 290 28103477
  124. Nimchinsky EA Yasuda R Oertner TG Svoboda K 2004 The Number of Glutamate Receptors Opened by Synaptic Stimulation in Single Hippocampal Spines J. Neurosci 24 2054 2064 14985448 PMC6730404
  125. Noritake J Fukata Y Iwanaga T Hosomi N Tsutsumi R Matsuda N Tani H Iwanari H Mochizuki Y Kodama T Matsuura Y Bredt DS Hamakubo T Fukata M 2009 Mobile DHHC palmitoylating enzyme mediates activity-sensitive synaptic targeting of PSD-95 J Cell Biol 186 147 160 19596852 PMC2712995
  126. Nusser Z Lujan R Laube G Roberts JDB Molnar E Somogyi P 1998 Cell Type and Pathway Dependence of Synaptic AMPA Receptor Number and Variability in the Hippocampus Neuron 21 545 9768841
  127. O’Brien RJ Xu D Petralia RS Steward O Huganir RL Worley P 1999 Synaptic clustering of AMPA receptors by the extracellular immediate-early gene product Narp Neuron 23 309 323 10399937
  128. Oertner TG Sabatini BL Nimchinsky EA Svoboda K 2002 Facilitation at single synapses probed with optical quantal analysis Nat Neurosci 5 657 664 12055631
  129. Park H Li Y Tsien RW 2012 Influence of synaptic vesicle position on release probability and exocytotic fusion mode Science 335 1362 1366 22345401 PMC3776413
  130. Park KA Ribic A Laage Gaupp FM Coman D Huang Y Dulla CG Hyder F Biederer T 2016 Excitatory synaptic drive and feedforward inhibition in the hippocampal CA3 circuit are regulated by SynCAM 1 J Neurosci 36 7464 7475 27413156 PMC4945666
  131. Peixoto RT Kunz PA Kwon H Mabb AM Sabatini BL Philpot BD Ehlers MD 2012 Transsynaptic signaling by activity-dependent cleavage of neuroligin-1 Neuron 76 396 409 23083741 PMC3783515
  132. Perez de Arce K Schrod N Metzbower SW Allgeyer E Kong GK Tang AH Krupp AJ Stein V Liu X Bewersdorf J Blanpied TA Lucic V Biederer T 2015 Topographic Mapping of the Synaptic Cleft into Adhesive Nanodomains Neuron 88 1165 1172 26687224 PMC4687029
  133. Perez-Otano I Lujan R Tavalin SJ Plomann M Modregger J Liu XB Jones EG Heinemann SF Lo DC Ehlers MD 2006 Endocytosis and synaptic removal of NR3A-containing NMDA receptors by PACSIN1/syndapin1 Nat Neurosci 9 611 621 16617342 PMC1892311
  134. Pertsinidis A Mukherjee K Sharma M Pang ZP Park SR Zhang Y Brunger AT Südhof TC Chu S 2013 Ultrahigh-resolution imaging reveals formation of neuronal SNARE/Munc18 complexes in situ Proceedings of the National Academy of Sciences of the United States of America 110 E2812 2820 23821748 PMC3725074
  135. Petzoldt AG Lee YH Khorramshahi O Reynolds E Plested AJ Herzel H Sigrist SJ 2014 Gating characteristics control glutamate receptor distribution and trafficking in vivo Curr Biol 24 2059 2065 25131677
  136. Pfenninger K Sandri C Akert K Eugster CH 1969 Contribution to the problem of structural organization of the presynaptic area Brain research 12 10 18 4184686
  137. Prokop A 1999 Integrating bits and pieces: synapse structure and formation in Drosophila embryos Cell Tissue Res 297 169 186 10470487
  138. Regalado MP Terry-Lorenzo RT Waites CL Garner CC Malenka RC 2006 Transsynaptic signaling by postsynaptic synapse-associated protein 97 J Neurosci 26 2343 2357 16495462 PMC6674804
  139. Renner ML Cognet L Lounis B Triller A Choquet D 2009 The excitatory postsynaptic density is a size exclusion diffusion environment Neuropharmacology 56 30 36 18694768
  140. Ripley B Otto S Tiglio K Williams ME Ghosh A 2011 Regulation of synaptic stability by AMPA receptor reverse signaling Proc Natl Acad Sci U S A 108 367 372 21173224 PMC3017209
  141. Robbins EM Krupp AJ Perez de Arce K Ghosh AK Fogel AI Boucard A Südhof TC Stein V Biederer T 2010 SynCAM 1 adhesion dynamically regulates synapse number and impacts plasticity and learning Neuron 68 894 906 21145003 PMC3026433
  142. Sabatini BL Regehr WG 1999 Timing of synaptic transmission Annual review of physiology 61 521 542 10099700
  143. 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 17481398
  144. Sainlos M Tigaret C Poujol C Olivier NB Bard L Breillat C Thiolon K Choquet D Imperiali B 2011 Biomimetic divalent ligands for the acute disruption of synaptic AMPAR stabilization Nat Chem Biol 7 81 91 21186349
  145. Santamaria F Gonzalez J Augustine GJ Raghavachari S 2010 Quantifying the effects of elastic collisions and non-covalent binding on glutamate receptor trafficking in the post-synaptic density PLoS Comput Biol 6 e1000780 20485563 PMC2869312
  146. Santucci DM Raghavachari S 2008 The effects of NR2 subunit-dependent NMDA receptor kinetics on synaptic transmission and CaMKII activation PLoS Comput Biol 4 e1000208 18974824 PMC2563690
  147. Sara Y Bal M Adachi M Monteggia LM Kavalali ET 2011 Use-dependent AMPA receptor block reveals segregation of spontaneous and evoked glutamatergic neurotransmission J Neurosci 31 5378 5382 21471372 PMC3086544
  148. Savtchenko LP Rusakov DA 2014 Moderate AMPA receptor clustering on the nanoscale can efficiently potentiate synaptic current Philos Trans R Soc Lond B Biol Sci 369 20130167 24298165 PMC3843895
  149. 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 10892652
  150. Schluter OM Xu W Malenka RC 2006 Alternative N-terminal domains of PSD-95 and SAP97 govern activity-dependent regulation of synaptic AMPA receptor function Neuron 51 99 111 16815335
  151. Schneider R Hosy E Kohl J Klueva J Choquet D Thomas U Voigt A Heine M 2015 Mobility of calcium channels in the presynaptic membrane Neuron 86 672 679 25892305
  152. Schnell E Sizemore M Karimzadegan S Chen L Bredt DS Nicoll RA 2002 Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number Proc Natl Acad Sci U S A 99 13902 13907 12359873 PMC129795
  153. Schoch S Castillo PE Jo T Mukherjee K Geppert M Wang Y Schmitz F Malenka RC Südhof TC 2002 RIM1alpha forms a protein scaffold for regulating neurotransmitter release at the active zone Nature 415 321 326 11797009
  154. Schoch S Gundelfinger ED 2006 Molecular organization of the presynaptic active zone Cell and tissue research 326 379 391 16865347
  155. Schwenk J Harmel N Brechet A Zolles G Berkefeld H Muller CS Bildl W Baehrens D Huber B Kulik A Klocker N Schulte U Fakler B 2012 High-resolution proteomics unravel architecture and molecular diversity of native AMPA receptor complexes Neuron 74 621 633 22632720
  156. Serra-Pages C Medley QG Tang M Hart A Streuli M 1998 Liprins, a family of LAR transmembrane protein-tyrosine phosphatase-interacting proteins J Biol Chem 273 15611 15620 9624153
  157. Sheng J He L Zheng H Xue L Luo F Shin W Sun T Kuner T Yue DT Wu LG 2012 Calcium-channel number critically influences synaptic strength and plasticity at the active zone Nat Neurosci 15 998 1006 22683682 PMC4891200
  158. Shinoe T Goda Y 2015 Tuning synapses by proteolytic remodeling of the adhesive surface Curr Opin Neurobiol 35 148 155 26318535
  159. 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 23129658 PMC3511127
  160. Siddiqui TJ Tari PK Connor SA Zhang P Dobie FA She K Kawabe H Wang YT Brose N Craig AM 2013 An LRRTM4-HSPG complex mediates excitatory synapse development on dentate gyrus granule cells Neuron 79 680 695 23911104
  161. Siksou L Rostaing P Lechaire JP Boudier T Ohtsuka T Fejtova A Kao HT Greengard P Gundelfinger ED Triller A Marty S 2007 Three-dimensional architecture of presynaptic terminal cytomatrix J Neurosci 27 6868 6877 17596435 PMC6672225
  162. Siksou L Varoqueaux F Pascual O Triller A Brose N Marty S 2009 A common molecular basis for membrane docking and functional priming of synaptic vesicles The European journal of neuroScience 30 49 56 19558619
  163. Silver RA Lubke J Sakmann B Feldmeyer D 2003 High-Probability Uniquantal Transmission at Excitatory Synapses in Barrel Cortex Science 302 1981 1984 14671309
  164. Singh SK Stogsdill JA Pulimood NS Dingsdale H Kim YH Pilaz LJ Kim IH Manhaes AC Rodrigues WS Jr Pamukcu A Enustun E Ertuz Z Scheiffele P Soderling SH Silver DL Ji RR Medina AE Eroglu C 2016 Astrocytes Assemble Thalamocortical Synapses by Bridging NRX1alpha and NL1 via Hevin Cell 164 183 196 26771491 PMC4715262
  165. Sinnen BL Bowen AB Forte JS Hiester BG Crosby KC Gibson ES Dell’Acqua ML Kennedy MJ 2017 Optogenetic Control of Synaptic Composition and Function Neuron 93 646 660 e645 28132827 PMC5300939
  166. 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 23931994 PMC3741667
  167. Soler-Llavina GJ Fuccillo MV Ko J Sudhof TC Malenka RC 2011 The neurexin ligands, neuroligins and leucine-rich repeat transmembrane proteins, perform convergent and divergent synaptic functions in vivo Proc Natl Acad Sci U S A 108 16502 16509 21953696 PMC3189075
  168. Stanley EF 1993 Single calcium channels and acetylcholine release at a presynaptic nerve terminal Neuron 11 1007 1011 8274272
  169. Stevens CF Wang Y 1995 Facilitation and depression at single central synapses Neuron 14 795 802 7718241
  170. Sudhof TC 2013 Neurotransmitter release: the last millisecond in the life of a synaptic vesicle Neuron 80 675 690 24183019 PMC3866025
  171. Swulius MT Kubota Y Forest A Waxham MN 2010 Structure and composition of the postsynaptic density during development J Comp Neurol 518 4243 4260 20878786 PMC2948241
  172. Takumi Y Ramirez-Leon V Laake P Rinvik E Ottersen OP 1999 Different modes of expression of AMPA and NMDA receptors in hippocampal synapses Nat Neurosci 2 618 624 10409387
  173. Tarr TB Dittrich M Meriney SD 2013 Are unreliable release mechanisms conserved from NMJ to CNS? Trends Neurosci 36 14 22 23102681 PMC4076818
  174. Tarusawa E Matsui K Budisantoso T Molnar E Watanabe M Matsui M Fukazawa Y Shigemoto R 2009 Input-specific intrasynaptic arrangements of ionotropic glutamate receptors and their impact on postsynaptic responses J Neurosci 29 12896 12908 19828804 PMC6665298
  175. Tomita S Fukata M Nicoll RA Bredt DS 2004 Dynamic interaction of stargazin-like TARPs with cycling AMPA receptors at synapses Science 303 1508 1511 15001777
  176. Tong G Jahr CE 1994 Multivesicular release from excitatory synapses of cultured hippocampal neurons Neuron 12 51 59 7507341
  177. Tong XJ Lopez-Soto EJ Li L Liu H Nedelcu D Lipscombe D Hu Z Kaplan JM 2017 Retrograde Synaptic Inhibition Is Mediated by alpha-Neurexin Binding to the alpha2delta Subunits of N-Type Calcium Channels Neuron 95 326 340 e325 28669545 PMC5548138
  178. 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 8909549 PMC2121068
  179. Um JW Kim KH Park BS Choi Y Kim D Kim CY Kim SJ Kim M Ko JS Lee SG Choii G Nam J Heo WD Kim E Lee JO Ko J Kim HM 2014 Structural basis for LAR-RPTP/Slitrk complex-mediated synaptic adhesion Nat Commun 5 5423 25394468
  180. Um JW Ko J 2013 LAR-RPTPs: Synaptic adhesion molecules that shape synapse development Trends in Cell Biology 23 465 475 23916315
  181. Uteshev VV Pennefather PS 1996 A mathematical description of miniature postsynaptic current generation at central nervous system synapses Biophys J 71 1256 1266 8874000 PMC1233593
  182. Valtschanoff JG Weinberg RJ 2001 Laminar organization of the NMDA receptor complex within the postsynaptic density J Neurosci 21 1211 1217 11160391 PMC6762240
  183. van den Bogaart G Meyenberg K Risselada HJ Amin H Willig KI Hubrich BE Dier M Hell SW Grubmuller H Diederichsen U Jahn R 2011 Membrane protein sequestering by ionic protein-lipid interactions Nature 479 552 555 22020284 PMC3409895
  184. Vardar G Chang S Arancillo M Wu Y-J Trimbuch T Rosenmund C 2016 Distinct Functions of Syntaxin-1 in Neuronal Maintenance, Synaptic Vesicle Docking, and Fusion in Mouse Neurons Journal of NeuroScience 36 7911 7924 27466336 PMC6601879
  185. Varoqueaux F Aramuni G Rawson RL Mohrmann R Missler M Gottmann K Zhang W Südhof TC Brose N 2006 Neuroligins determine synapse maturation and function Neuron 51 741 754 16982420
  186. Varoqueaux F Sigler A Rhee JS Brose N Enk C Reim K Rosenmund C 2002 Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming Proceedings of the National Academy of Sciences of the United States of America 99 9037 9042 12070347 PMC124419
  187. Vitureira N Letellier M White IJ Goda Y 2011 Differential control of presynaptic efficacy by postsynaptic N-cadherin and beta-catenin Nat Neurosci 15 81 89 22138644 PMC3245860
  188. Wahl LM Pouzat C Stratford KJ 1996 Monte Carlo simulation of fast excitatory synaptic transmission at a hippocampal synapse J Neurophysiol 75 597 608 8714637
  189. Wang Y Fehlhaber KE Sarria I Cao Y Ingram NT Guerrero-Given D Throesch B Baldwin K Kamasawa N Ohtsuka T Sampath AP Martemyanov KA 2017 The Auxiliary Calcium Channel Subunit alpha2delta4 Is Required for Axonal Elaboration, Synaptic Transmission, and Wiring of Rod Photoreceptors Neuron 93 1359 1374 e1356 28262416 PMC5364038
  190. Wang Y Okamoto M Schmitz F Hofmann K Sudhof TC 1997 Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion Nature 388 593 598 9252191
  191. Wilhelm BG Mandad S Truckenbrodt S Kröhnert K Schäfer C Rammner B Koo SJ Claβen GA Krauss M Haucke V Urlaub H Rizzoli SO 2014 Composition of isolated synaptic boutons reveals the amounts of vesicle trafficking proteins Science 344 1023 1028 24876496
  192. 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 19628693 PMC2726414
  193. Woo J Kwon SK Choi S Kim S Lee JR Dunah AW Sheng M Kim E 2009 Trans-synaptic adhesion between NGL-3 and LAR regulates the formation of excitatory synapses Nat Neurosci 12 428 437 19252495
  194. Xie X Liaw J-S Baudry M Berger TW 1997 Novel expression mechanism for synaptic potentiation: Alignment of presynaptic release site and postsynaptic receptor PNAS 94 6983 6988 9192678 PMC21271
  195. Xu-Friedman MA Regehr WG 2004 Structural contributions to short-term synaptic plasticity Physiol Rev 84 69 85 14715911
  196. Yamagata M Herman JP Sanes JR 1995 Lamina-specific expression of adhesion molecules in developing chick optic tectum J Neurosci 15 4556 4571 7790923 PMC6577700
  197. Yim YS Kwon Y Nam J Yoon HI Lee K Kim DG Kim E Kim CH Ko J 2013 Slitrks control excitatory and inhibitory synapse formation with LAR receptor protein tyrosine phosphatases Proc Natl Acad Sci U S A 110 4057 4062 23345436 PMC3593915
  198. Yuzaki M 2017 The C1q complement family of synaptic organizers: not just complementary Curr Opin Neurobiol 45 9 15 28219683
  199. Zenisek D Steyer JA Almers W 2000 Transport, capture and exocytosis of single synaptic vesicles at active zones Nature 406 849 854 10972279
  200. Zhan H Bruckner J Zhang Z O’Connor-Giles K 2016 Three-dimensional imaging of Drosophila motor synapses reveals ultrastructural organizational patterns J Neurogenet 30 237 246 27981875 PMC5281062

200 of 203 shown

Authors
Biederer, T., Kaeser, P. S., & Blanpied, T. A.
Affiliations
  • Tufts University (US)
  • Harvard University (US)
  • University of Maryland, Baltimore (US)
Corresponding author
  • Biederer, Thomas
  • Kaeser, Pascal S.
  • Blanpied, Thomas A.
ORCID
Venue
Neuron
Publisher
Elsevier BV
Published
2017-11
Volume
96
Issue
3
Pages
680-696
ISSN
0896-6273 (ISSN-L)
DOI
10.1016/j.neuron.2017.10.006
PMC
PMC5777221
OpenAlex
W2765327979
Cited by
352
References
242
Citations by year
2026: 32 · 2025: 42 · 2024: 40 · 2023: 27 · 2022: 46 · 2021: 60 · 2020: 38 · 2019: 37 · 2018: 29 · 2012: 1
FWCI
3.51
Type
journal article
Language
en
Open access
Licence
Locations
  • Neuron (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
NIH (R01NS083898, R01MH113349, R01NS103484, R01DA018928, R01MH080046, R01MH111527)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords
synaptic function, presynaptic terminals, synaptic cleft, postsynaptic specialization, synaptic plasticity, synaptic transmission
MeSH terms
Animals, Cell Communication, Exocytosis, Humans, Synaptic Transmission, Neuronal Plasticity, Synapses, Synaptic Vesicles, Presynaptic Terminals

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review