{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T02:58:28Z","timestamp":1790737108546,"version":"4.1.0"},"reference-count":52,"publisher":"Elsevier BV","issue":"5","license":[{"start":{"date-parts":[[2018,5,1]],"date-time":"2018-05-01T00:00:00Z","timestamp":1525132800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2018,5,1]],"date-time":"2018-05-01T00:00:00Z","timestamp":1525132800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2018,3,30]],"date-time":"2018-03-30T00:00:00Z","timestamp":1522368000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["IOS1555933"],"award-info":[{"award-number":["IOS1555933"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01MH109690"],"award-info":[{"award-number":["R01MH109690"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["A06 SFB958"],"award-info":[{"award-number":["A06 SFB958"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["TP09 SFB740"],"award-info":[{"award-number":["TP09 SFB740"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002347","name":"Bundesministerium f\u00fcr Bildung und Forschung","doi-asserted-by":"publisher","award":["01ZX1614J"],"award-info":[{"award-number":["01ZX1614J"]}],"id":[{"id":"10.13039\/501100002347","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["cell.com","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Cell Reports"],"published-print":{"date-parts":[[2018,5]]},"DOI":"10.1016\/j.celrep.2018.03.126","type":"journal-article","created":{"date-parts":[[2018,5,2]],"date-time":"2018-05-02T04:09:51Z","timestamp":1525234191000},"page":"1259-1274","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":75,"title":["Active Zone Scaffold Protein Ratios Tune Functional Diversity across Brain Synapses"],"prefix":"10.1016","volume":"23","author":[{"given":"Andreas","family":"Fulterer","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Till F.M.","family":"Andlauer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anatoli","family":"Ender","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marta","family":"Maglione","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katherine","family":"Eyring","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jennifer","family":"Woitkuhn","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martin","family":"Lehmann","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tanja","family":"Matkovic-Rachid","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joerg R.P.","family":"Geiger","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexander M.","family":"Walter","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katherine I.","family":"Nagel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stephan J.","family":"Sigrist","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.celrep.2018.03.126_bib1","doi-asserted-by":"crossref","first-page":"792","DOI":"10.1016\/j.neuron.2016.07.042","article-title":"How to make an active zone: unexpected universal functional redundancy between RIMs and RIM-BPs","volume":"91","author":"Acuna","year":"2016","journal-title":"Neuron"},{"key":"10.1016\/j.celrep.2018.03.126_bib2","doi-asserted-by":"crossref","first-page":"e03895","DOI":"10.7554\/eLife.03895","article-title":"Drep-2 is a novel synaptic protein important for learning and memory","volume":"3","author":"Andlauer","year":"2014","journal-title":"eLife"},{"key":"10.1016\/j.celrep.2018.03.126_bib3","doi-asserted-by":"crossref","first-page":"2987","DOI":"10.1152\/jn.00283.2003","article-title":"Two dynamically distinct inhibitory networks in layer 4 of the neocortex","volume":"90","author":"Beierlein","year":"2003","journal-title":"J.\u00a0Neurophysiol."},{"key":"10.1016\/j.celrep.2018.03.126_bib4","doi-asserted-by":"crossref","first-page":"e14859","DOI":"10.7554\/eLife.14859","article-title":"The wiring diagram of a glomerular olfactory system","volume":"5","author":"Berck","year":"2016","journal-title":"eLife"},{"key":"10.1016\/j.celrep.2018.03.126_bib5","doi-asserted-by":"crossref","first-page":"1311","DOI":"10.1038\/nn.4364","article-title":"Active zone scaffolds differentially accumulate Unc13 isoforms to tune Ca(2+) channel-vesicle coupling","volume":"19","author":"B\u00f6hme","year":"2016","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.celrep.2018.03.126_bib6","doi-asserted-by":"crossref","first-page":"718","DOI":"10.1038\/nn.3974","article-title":"Synaptic diversity enables temporal coding of coincident multisensory inputs in single neurons","volume":"18","author":"Chabrol","year":"2015","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.celrep.2018.03.126_bib7","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1038\/nn.2489","article-title":"Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe","volume":"13","author":"Chou","year":"2010","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.celrep.2018.03.126_bib8","doi-asserted-by":"crossref","first-page":"9696","DOI":"10.1523\/JNEUROSCI.6542-10.2011","article-title":"Presynapses in Kenyon cell dendrites in the mushroom body calyx of Drosophila","volume":"31","author":"Christiansen","year":"2011","journal-title":"J.\u00a0Neurosci."},{"key":"10.1016\/j.celrep.2018.03.126_bib9","doi-asserted-by":"crossref","first-page":"1479","DOI":"10.1038\/nn1808","article-title":"SYD-2 Liprin-alpha organizes presynaptic active zone formation through ELKS","volume":"9","author":"Dai","year":"2006","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.celrep.2018.03.126_bib10","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1016\/j.neuron.2011.01.005","article-title":"RIM proteins activate vesicle priming by reversing autoinhibitory homodimerization of Munc13","volume":"69","author":"Deng","year":"2011","journal-title":"Neuron"},{"key":"10.1016\/j.celrep.2018.03.126_bib11","series-title":"Probability and Statistics for Engineering and the Sciences","author":"Devore","year":"2011"},{"key":"10.1016\/j.celrep.2018.03.126_bib12","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1038\/nrn3125","article-title":"Nanodomain coupling between Ca2+ channels and sensors of exocytosis at fast mammalian synapses","volume":"13","author":"Eggermann","year":"2011","journal-title":"Nat. Rev. Neurosci."},{"key":"10.1016\/j.celrep.2018.03.126_bib13","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1083\/jcb.200812150","article-title":"Maturation of active zone assembly by Drosophila Bruchpilot","volume":"186","author":"Fouquet","year":"2009","journal-title":"J.\u00a0Cell Biol."},{"key":"10.1016\/j.celrep.2018.03.126_bib14","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1016\/j.conb.2015.12.008","article-title":"Computational implications of biophysical diversity and multiple timescales in neurons and synapses for circuit performance","volume":"37","author":"Gjorgjieva","year":"2016","journal-title":"Curr. Opin. Neurobiol."},{"key":"10.1016\/j.celrep.2018.03.126_bib15","doi-asserted-by":"crossref","first-page":"1821","DOI":"10.1038\/nn.3547","article-title":"Integration of the olfactory code across dendritic claws of single mushroom body neurons","volume":"16","author":"Gruntman","year":"2013","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.celrep.2018.03.126_bib16","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1038\/nature10926","article-title":"Teneurins instruct synaptic partner matching in an olfactory map","volume":"484","author":"Hong","year":"2012","journal-title":"Nature"},{"key":"10.1016\/j.celrep.2018.03.126_bib17","doi-asserted-by":"crossref","first-page":"e00967","DOI":"10.7554\/eLife.00967","article-title":"UNC-13L, UNC-13S, and Tomosyn form a protein code for fast and slow neurotransmitter release in Caenorhabditis elegans","volume":"2","author":"Hu","year":"2013","journal-title":"eLife"},{"key":"10.1016\/j.celrep.2018.03.126_bib18","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1016\/j.neuron.2017.02.047","article-title":"The mechanisms and functions of synaptic facilitation","volume":"94","author":"Jackman","year":"2017","journal-title":"Neuron"},{"key":"10.1016\/j.celrep.2018.03.126_bib19","doi-asserted-by":"crossref","first-page":"1143","DOI":"10.1083\/jcb.201606086","article-title":"ELKS1 localizes the synaptic vesicle priming protein bMunc13-2 to a specific subset of active zones","volume":"216","author":"Kawabe","year":"2017","journal-title":"J.\u00a0Cell Biol."},{"key":"10.1016\/j.celrep.2018.03.126_bib20","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1016\/j.neuron.2008.02.030","article-title":"Homeostatic matching and nonlinear amplification at identified central synapses","volume":"58","author":"Kazama","year":"2008","journal-title":"Neuron"},{"key":"10.1016\/j.celrep.2018.03.126_bib21","doi-asserted-by":"crossref","first-page":"1136","DOI":"10.1038\/nn.2376","article-title":"Origins of correlated activity in an olfactory circuit","volume":"12","author":"Kazama","year":"2009","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.celrep.2018.03.126_bib22","doi-asserted-by":"crossref","first-page":"1051","DOI":"10.1126\/science.1126308","article-title":"Bruchpilot promotes active zone assembly, Ca2+ channel clustering, and vesicle release","volume":"312","author":"Kittel","year":"2006","journal-title":"Science"},{"key":"10.1016\/j.celrep.2018.03.126_bib23","doi-asserted-by":"crossref","first-page":"1938","DOI":"10.1016\/j.cub.2010.09.060","article-title":"Structural long-term changes at mushroom body input synapses","volume":"20","author":"Kremer","year":"2010","journal-title":"Curr. Biol."},{"key":"10.1016\/j.celrep.2018.03.126_bib24","doi-asserted-by":"crossref","first-page":"10294","DOI":"10.1073\/pnas.1220560110","article-title":"Glutamate is an inhibitory neurotransmitter in the Drosophila olfactory system","volume":"110","author":"Liu","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.celrep.2018.03.126_bib25","doi-asserted-by":"crossref","first-page":"e03726","DOI":"10.7554\/eLife.03726","article-title":"Synaptic organization of the Drosophila antennal lobe and its regulation by the Teneurins","volume":"3","author":"Mosca","year":"2014","journal-title":"eLife"},{"key":"10.1016\/j.celrep.2018.03.126_bib26","doi-asserted-by":"crossref","first-page":"e27347","DOI":"10.7554\/eLife.27347","article-title":"Presynaptic LRP4 promotes synapse number and function of excitatory CNS neurons","volume":"6","author":"Mosca","year":"2017","journal-title":"eLife"},{"key":"10.1016\/j.celrep.2018.03.126_bib27","doi-asserted-by":"crossref","first-page":"4325","DOI":"10.1523\/JNEUROSCI.3887-15.2016","article-title":"Mechanisms underlying population response dynamics in inhibitory interneurons of the Drosophila antennal lobe","volume":"36","author":"Nagel","year":"2016","journal-title":"J.\u00a0Neurosci."},{"key":"10.1016\/j.celrep.2018.03.126_bib28","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1038\/nn.3895","article-title":"Synaptic and circuit mechanisms promoting broadband transmission of olfactory stimulus dynamics","volume":"18","author":"Nagel","year":"2015","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.celrep.2018.03.126_bib29","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1016\/j.conb.2018.01.001","article-title":"Creating diverse synapses from the same molecules","volume":"51","author":"Nusser","year":"2018","journal-title":"Curr. Opin. Neurobiol."},{"key":"10.1016\/j.celrep.2018.03.126_bib30","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1038\/nrn3170","article-title":"Deep molecular diversity of mammalian synapses: why it matters and how to measure it","volume":"13","author":"O\u2019Rourke","year":"2012","journal-title":"Nat. Rev. Neurosci."},{"key":"10.1016\/j.celrep.2018.03.126_bib31","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1083\/jcb.200908055","article-title":"A Syd-1 homologue regulates pre- and postsynaptic maturation in Drosophila","volume":"188","author":"Owald","year":"2010","journal-title":"J.\u00a0Cell Biol."},{"key":"10.1016\/j.celrep.2018.03.126_bib32","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/j.conb.2016.04.009","article-title":"Mechanisms controlling assembly and plasticity of presynaptic active zone scaffolds","volume":"39","author":"Petzoldt","year":"2016","journal-title":"Curr. Opin. Neurobiol."},{"key":"10.1016\/j.celrep.2018.03.126_bib33","doi-asserted-by":"crossref","first-page":"1350","DOI":"10.1016\/j.neuron.2017.08.016","article-title":"Stable positioning of Unc13 restricts synaptic vesicle fusion to defined release sites to promote synchronous neurotransmission","volume":"95","author":"Reddy-Alla","year":"2017","journal-title":"Neuron"},{"key":"10.1016\/j.celrep.2018.03.126_bib34","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1038\/1092","article-title":"Target-cell-specific facilitation and depression in neocortical circuits","volume":"1","author":"Reyes","year":"1998","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.celrep.2018.03.126_bib35","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1016\/S0896-6273(02)00568-8","article-title":"Differential control of vesicle priming and short-term plasticity by Munc13 isoforms","volume":"33","author":"Rosenmund","year":"2002","journal-title":"Neuron"},{"key":"10.1016\/j.celrep.2018.03.126_bib36","doi-asserted-by":"crossref","first-page":"1920","DOI":"10.1002\/cne.23966","article-title":"Synaptic circuitry of identified neurons in the antennal lobe of Drosophila melanogaster","volume":"524","author":"Rybak","year":"2016","journal-title":"J.\u00a0Comp. Neurol."},{"key":"10.1016\/j.celrep.2018.03.126_bib37","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1038\/s41593-017-0041-9","article-title":"Synaptic weight set by Munc13-1 supramolecular assemblies","volume":"21","author":"Sakamoto","year":"2018","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.celrep.2018.03.126_bib38","doi-asserted-by":"crossref","first-page":"659","DOI":"10.1038\/nn.2122","article-title":"Activity-dependent site-specific changes of glutamate receptor composition in\u00a0vivo","volume":"11","author":"Schmid","year":"2008","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.celrep.2018.03.126_bib39","doi-asserted-by":"crossref","first-page":"6546","DOI":"10.1523\/JNEUROSCI.23-16-06546.2003","article-title":"Experience-dependent strengthening of Drosophila neuromuscular junctions","volume":"23","author":"Sigrist","year":"2003","journal-title":"J.\u00a0Neurosci."},{"key":"10.1016\/j.celrep.2018.03.126_bib40","doi-asserted-by":"crossref","first-page":"142","DOI":"10.3389\/fncel.2016.00142","article-title":"Super resolution imaging of genetically labeled synapses in Drosophila brain tissue","volume":"10","author":"Sp\u00fchler","year":"2016","journal-title":"Front. Cell. Neurosci."},{"key":"10.1016\/j.celrep.2018.03.126_bib41","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/j.tins.2016.01.005","article-title":"The nanophysiology of fast transmitter release","volume":"39","author":"Stanley","year":"2016","journal-title":"Trends Neurosci."},{"key":"10.1016\/j.celrep.2018.03.126_bib42","doi-asserted-by":"crossref","first-page":"452","DOI":"10.1016\/j.neuron.2010.06.029","article-title":"From dendrite to soma: dynamic routing of inhibition by complementary interneuron microcircuits in olfactory cortex","volume":"67","author":"Stokes","year":"2010","journal-title":"Neuron"},{"key":"10.1016\/j.celrep.2018.03.126_bib43","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.neuron.2012.06.012","article-title":"The presynaptic active zone","volume":"75","author":"S\u00fcdhof","year":"2012","journal-title":"Neuron"},{"key":"10.1016\/j.celrep.2018.03.126_bib44","doi-asserted-by":"crossref","first-page":"536","DOI":"10.1126\/science.1222482","article-title":"Elfn1 regulates target-specific release probability at CA1-interneuron synapses","volume":"338","author":"Sylwestrak","year":"2012","journal-title":"Science"},{"key":"10.1016\/j.celrep.2018.03.126_bib45","doi-asserted-by":"crossref","first-page":"e26975","DOI":"10.7554\/eLife.26975","article-title":"A connectome of a learning and memory center in the adult Drosophila brain","volume":"6","author":"Takemura","year":"2017","journal-title":"eLife"},{"key":"10.1016\/j.celrep.2018.03.126_bib46","doi-asserted-by":"crossref","first-page":"665","DOI":"10.1126\/science.1244811","article-title":"Loose coupling between Ca2+ channels and release sensors at a plastic hippocampal synapse","volume":"343","author":"Vyleta","year":"2014","journal-title":"Science"},{"key":"10.1016\/j.celrep.2018.03.126_bib47","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1016\/j.neuron.2007.01.021","article-title":"The coupling between synaptic vesicles and Ca2+ channels determines fast neurotransmitter release","volume":"53","author":"Wadel","year":"2007","journal-title":"Neuron"},{"key":"10.1016\/j.celrep.2018.03.126_bib48","doi-asserted-by":"crossref","first-page":"777","DOI":"10.1016\/j.neuron.2016.07.005","article-title":"Fusion competent synaptic vesicles persist upon active zone disruption and loss of vesicle docking","volume":"91","author":"Wang","year":"2016","journal-title":"Neuron"},{"key":"10.1016\/j.celrep.2018.03.126_bib49","doi-asserted-by":"crossref","first-page":"1012","DOI":"10.1016\/j.neuron.2013.05.010","article-title":"mSYD1A, a mammalian synapse-defective-1 protein, regulates synaptogenic signaling and vesicle docking","volume":"78","author":"Wentzel","year":"2013","journal-title":"Neuron"},{"key":"10.1016\/j.celrep.2018.03.126_bib50","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1146\/annurev-neuro-062111-150533","article-title":"Early olfactory processing in Drosophila: mechanisms and principles","volume":"36","author":"Wilson","year":"2013","journal-title":"Annu. Rev. Neurosci."},{"key":"10.1016\/j.celrep.2018.03.126_bib51","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1002\/cne.10155","article-title":"Synaptic organization of the mushroom body calyx in Drosophila melanogaster","volume":"445","author":"Yasuyama","year":"2002","journal-title":"J.\u00a0Comp. Neurol."},{"key":"10.1016\/j.celrep.2018.03.126_bib52","doi-asserted-by":"crossref","first-page":"e01180","DOI":"10.7554\/eLife.01180","article-title":"Position of UNC-13 in the active zone regulates synaptic vesicle release probability and release kinetics","volume":"2","author":"Zhou","year":"2013","journal-title":"eLife"}],"container-title":["Cell Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S221112471830514X?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S221112471830514X?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,10,31]],"date-time":"2025-10-31T10:19:46Z","timestamp":1761905986000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S221112471830514X"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,5]]},"references-count":52,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2018,5]]}},"alternative-id":["S221112471830514X"],"URL":"https:\/\/doi.org\/10.1016\/j.celrep.2018.03.126","relation":{},"ISSN":["2211-1247"],"issn-type":[{"value":"2211-1247","type":"print"}],"subject":[],"published":{"date-parts":[[2018,5]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Active Zone Scaffold Protein Ratios Tune Functional Diversity across Brain Synapses","name":"articletitle","label":"Article Title"},{"value":"Cell Reports","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.celrep.2018.03.126","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2018 The Author(s).","name":"copyright","label":"Copyright"}]}}