{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,21]],"date-time":"2026-10-21T21:52:44Z","timestamp":1792619564501,"version":"4.5.0"},"reference-count":58,"publisher":"Association for Research in Vision and Ophthalmology (ARVO)","issue":"6","license":[{"start":{"date-parts":[[2026,6,1]],"date-time":"2026-06-01T00:00:00Z","timestamp":1780272000000},"content-version":"unspecified","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Invest. Ophthalmol. Vis. Sci."],"published-print":{"date-parts":[[2026,6,1]]},"DOI":"10.1167\/iovs.67.6.1","type":"journal-article","created":{"date-parts":[[2026,6,1]],"date-time":"2026-06-01T13:00:59Z","timestamp":1780318859000},"page":"1","source":"Crossref","is-referenced-by-count":1,"title":["Revisiting the Molecular Architecture of Photoreceptor Ribbon Synapses Using Ultrastructure Expansion Microscopy"],"prefix":"10.1167","volume":"67","author":[{"given":"Kei","family":"Takahashi","sequence":"first","affiliation":[{"name":"Division of Experimental Retinal Therapies, Department of Clinical Sciences & Advanced Medicine, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Natalia","family":"Dolgova","sequence":"additional","affiliation":[{"name":"Division of Experimental Retinal Therapies, Department of Clinical Sciences & Advanced Medicine, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Raghavi","family":"Sudharsan","sequence":"additional","affiliation":[{"name":"Division of Experimental Retinal Therapies, Department of Clinical Sciences & Advanced Medicine, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"William A.","family":"Beltran","sequence":"additional","affiliation":[{"name":"Division of Experimental Retinal Therapies, Department of Clinical Sciences & Advanced Medicine, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, United States"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"27","reference":[{"key":"bib1","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1152\/physrev.00026.2018","article-title":"Sensory processing at ribbon synapses in the retina and the cochlea","volume":"100","author":"Moser","year":"2020","journal-title":"Physiol Rev"},{"key":"bib2","doi-asserted-by":"publisher","first-page":"812","DOI":"10.1038\/nrn2924","article-title":"The diverse roles of ribbon synapses in sensory neurotransmission","volume":"11","author":"Matthews","year":"2010","journal-title":"Nat Rev Neurosci"},{"key":"bib3","doi-asserted-by":"publisher","first-page":"20","DOI":"10.1016\/j.tins.2004.11.009","article-title":"Structure and function of ribbon synapses","volume":"28","author":"Sterling","year":"2005","journal-title":"Trends Neurosci"},{"key":"bib4","doi-asserted-by":"publisher","first-page":"80","DOI":"10.1098\/rspb.1966.0086","article-title":"Organization of the primate retina: electron microscopy","volume":"166","author":"Dowling","year":"1966","journal-title":"Proc R Soc Lond B Biol Sci"},{"key":"bib5","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1016\/j.pbiomolbio.2020.05.010","article-title":"Towards high-throughput in situ structural biology using electron cryotomography","volume":"160","author":"B\u00f6hning","year":"2021","journal-title":"Prog Biophys Mol Biol"},{"key":"bib6","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1167\/iovs.63.8.11","article-title":"Multiple invagination patterns and synaptic efficacy in primate and mouse rod synaptic terminals","volume":"63","author":"Tsukamoto","year":"2022","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"bib7","doi-asserted-by":"publisher","first-page":"5468","DOI":"10.1523\/JNEUROSCI.2267-22.2023","article-title":"Three-dimensional ultrastructure of the normal rod photoreceptor synapse and degenerative changes induced by retinal detachment","volume":"43","author":"Torten","year":"2023","journal-title":"J Neurosci"},{"key":"bib8","doi-asserted-by":"publisher","first-page":"100253","DOI":"10.1016\/j.crmeth.2022.100253","article-title":"Rapid 3D-STORM imaging of diverse molecular targets in tissue","volume":"2","author":"Albrecht","year":"2022","journal-title":"Cell Rep Methods"},{"key":"bib9","doi-asserted-by":"publisher","first-page":"eabl7560","DOI":"10.1126\/sciadv.abl7560","article-title":"Resolving the molecular architecture of the photoreceptor active zone with 3D-MINFLUX","volume":"8","author":"Grabner","year":"2022","journal-title":"Sci Adv"},{"key":"bib10","doi-asserted-by":"publisher","first-page":"dmm052256","DOI":"10.1242\/dmm.052256","article-title":"P23H rhodopsin accumulation causes transient disruptions to synaptic protein levels in rod photoreceptors in a model of retinitis pigmentosa","volume":"18","author":"Thompson","year":"2025","journal-title":"Dis Model Mech"},{"key":"bib11","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1016\/j.preteyeres.2015.04.001","article-title":"Fixation strategies for retinal immunohistochemistry","volume":"48","author":"Stradleigh","year":"2015","journal-title":"Prog Retin Eye Res"},{"key":"bib12","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1016\/j.preteyeres.2015.04.004","article-title":"The pros and cons of vertebrate animal models for functional and therapeutic research on inherited retinal dystrophies","volume":"48","author":"Slijkerman","year":"2015","journal-title":"Prog Retin Eye Res"},{"key":"bib13","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1038\/s41592-018-0238-1","article-title":"Imaging cellular ultrastructures using expansion microscopy (U-ExM)","volume":"16","author":"Gambarotto","year":"2019","journal-title":"Nat Methods"},{"key":"bib14","doi-asserted-by":"publisher","first-page":"543","DOI":"10.1126\/science.1260088","article-title":"Optical imaging. Expansion microscopy","volume":"347","author":"Chen","year":"2015","journal-title":"Science"},{"key":"bib15","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1167\/iovs.66.2.1","article-title":"Mapping protein distribution in the canine photoreceptor sensory cilium and calyceal processes by ultrastructure expansion microscopy","volume":"66","author":"Takahashi","year":"2025","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"bib16","doi-asserted-by":"publisher","first-page":"618","DOI":"10.1002\/cm.21870","article-title":"Ultrastructure expansion microscopy (U-ExM) of mouse and human kidneys for analysis of subcellular structures","volume":"81","author":"Langner","year":"2024","journal-title":"Cytoskeleton (Hoboken)"},{"key":"bib17","doi-asserted-by":"publisher","first-page":"e3001649","DOI":"10.1371\/journal.pbio.3001649","article-title":"The connecting cilium inner scaffold provides a structural foundation that protects against retinal degeneration","volume":"20","author":"Mercey","year":"2022","journal-title":"PLoS Biol"},{"key":"bib18","doi-asserted-by":"publisher","first-page":"e90390","DOI":"10.1371\/journal.pone.0090390","article-title":"Canine retina has a primate fovea-like bouquet of cone photoreceptors which is affected by inherited macular degenerations","volume":"9","author":"Beltran","year":"2014","journal-title":"PLoS One"},{"key":"bib19","doi-asserted-by":"publisher","first-page":"109989","DOI":"10.1016\/j.exer.2024.109989","article-title":"An optimized workflow for transcriptomic analysis from archival paraformaldehyde-fixed retinal tissues collected by laser capture microdissection","volume":"246","author":"Takahashi","year":"2024","journal-title":"Exp Eye Res"},{"key":"bib20","doi-asserted-by":"publisher","first-page":"20","DOI":"10.1167\/iovs.67.2.20","article-title":"Crosstalk between R-loops, RNA\/DNA modifications, and cell death dynamics in canine models of retinitis pigmentosa","volume":"67","author":"Appelbaum","year":"2026","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"bib21","doi-asserted-by":"publisher","first-page":"1226603","DOI":"10.3389\/fncel.2023.1226603","article-title":"Molecular characterization of MAP9 in the photoreceptor sensory cilia as a modifier in canine RPGRIP1-associated cone-rod dystrophy","volume":"17","author":"Takahashi","year":"2023","journal-title":"Front Cell Neurosci"},{"key":"bib22","doi-asserted-by":"publisher","first-page":"825","DOI":"10.1083\/jcb.200408157","article-title":"Molecular dissection of the photoreceptor ribbon synapse: physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex","volume":"168","author":"tom Dieck","year":"2005","journal-title":"J Cell Biol"},{"key":"bib23","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1016\/j.mcn.2014.08.004","article-title":"Differential synaptic distribution of the scaffold proteins Cask and Caskin1 in the bovine retina","volume":"62","author":"Anjum","year":"2014","journal-title":"Mol Cell Neurosci"},{"key":"bib24","doi-asserted-by":"publisher","first-page":"218","DOI":"10.1016\/j.ydbio.2021.04.001","article-title":"Development and maintenance of vision's first synapse","volume":"476","author":"Burger","year":"2021","journal-title":"Dev Biol"},{"key":"bib25","doi-asserted-by":"publisher","first-page":"6126","DOI":"10.1523\/JNEUROSCI.0322-12.2012","article-title":"Presynaptic dystroglycan-pikachurin complex regulates the proper synaptic connection between retinal photoreceptor and bipolar cells","volume":"32","author":"Omori","year":"2012","journal-title":"J Neurosci"},{"key":"bib26","doi-asserted-by":"publisher","first-page":"3107","DOI":"10.1016\/j.celrep.2019.05.056","article-title":"Presynaptic expression of LRIT3 transsynaptically organizes the postsynaptic glutamate signaling complex containing TRPM1","volume":"27","author":"Hasan","year":"2019","journal-title":"Cell Rep"},{"key":"bib27","doi-asserted-by":"publisher","first-page":"249","DOI":"10.1016\/S0896-6273(00)80531-0","article-title":"Compartmentalization of calcium extrusion mechanisms in the outer and inner segments of photoreceptors","volume":"21","author":"Krizaj","year":"1998","journal-title":"Neuron"},{"key":"bib28","doi-asserted-by":"publisher","first-page":"10136","DOI":"10.1523\/JNEUROSCI.18-23-10136.1998","article-title":"Immunocytochemical localization of the postsynaptic density protein PSD-95 in the mammalian retina","volume":"18","author":"Koulen","year":"1998","journal-title":"J Neurosci"},{"key":"bib29","doi-asserted-by":"publisher","first-page":"685","DOI":"10.1146\/annurev-biochem-060815-014352","article-title":"Mitochondrial machineries for protein import and assembly","volume":"86","author":"Wiedemann","year":"2017","journal-title":"Annu Rev Biochem"},{"key":"bib30","doi-asserted-by":"publisher","first-page":"923","DOI":"10.1038\/nn.2160","article-title":"Pikachurin, a dystroglycan ligand, is essential for photoreceptor ribbon synapse formation","volume":"11","author":"Sato","year":"2008","journal-title":"Nat Neurosci"},{"key":"bib31","doi-asserted-by":"publisher","first-page":"433","DOI":"10.1002\/cne.903010308","article-title":"Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity","volume":"301","author":"Greferath","year":"1990","journal-title":"J Comp Neurol"},{"key":"bib32","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1002\/(SICI)1096-9861(19980525)395:1&lt;43::AID-CNE4&gt;3.0.CO;2-H","article-title":"Alpha subunit of Go localizes in the dendritic tips of ON bipolar cells","volume":"395","author":"Vardi","year":"1998","journal-title":"J Comp Neurol"},{"key":"bib33","doi-asserted-by":"publisher","first-page":"711","DOI":"10.1083\/jcb.201202123","article-title":"GPR158\/179 regulate G protein signaling by controlling localization and activity of the RGS7 complexes","volume":"197","author":"Orlandi","year":"2012","journal-title":"J Cell Biol"},{"key":"bib34","doi-asserted-by":"publisher","first-page":"402","DOI":"10.1002\/1096-9861(20000731)423:3&lt;402::AID-CNE4&gt;3.0.CO;2-E","article-title":"Localization of mGluR6 to dendrites of ON bipolar cells in primate retina","volume":"423","author":"Vardi","year":"2000","journal-title":"J Comp Neurol"},{"key":"bib35","doi-asserted-by":"publisher","first-page":"3023","DOI":"10.1152\/jn.00608.2007","article-title":"Nyctalopin expression in retinal bipolar cells restores visual function in a mouse model of complete X-linked congenital stationary night blindness","volume":"98","author":"Gregg","year":"2007","journal-title":"J Neurophysiol"},{"key":"bib36","doi-asserted-by":"publisher","first-page":"332","DOI":"10.1073\/pnas.0912730107","article-title":"TRPM1 is a component of the retinal ON bipolar cell transduction channel in the mGluR6 cascade","volume":"107","author":"Koike","year":"2010","journal-title":"Proc Natl Acad Sci USA"},{"key":"bib37","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1016\/S0896-6273(00)00011-8","article-title":"The cone pedicle, a complex synapse in the retina","volume":"27","author":"Haverkamp","year":"2000","journal-title":"Neuron"},{"key":"bib38","doi-asserted-by":"publisher","first-page":"2488","DOI":"10.1523\/JNEUROSCI.21-07-02488.2001","article-title":"The synaptic architecture of AMPA receptors at the cone pedicle of the primate retina","volume":"21","author":"Haverkamp","year":"2001","journal-title":"J Neurosci"},{"key":"bib39","doi-asserted-by":"publisher","first-page":"471","DOI":"10.1002\/cne.1081","article-title":"Localization of kainate receptors at the cone pedicles of the primate retina","volume":"436","author":"Haverkamp","year":"2001","journal-title":"J Comp Neurol"},{"key":"bib40","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1002\/cne.903020217","article-title":"Localization of two calcium binding proteins, calbindin (28 kD) and parvalbumin (12 kD), in the vertebrate retina","volume":"302","author":"Hamano","year":"1990","journal-title":"J Comp Neurol"},{"key":"bib41","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1016\/S0168-0102(98)00070-4","article-title":"Immunocytochemical localization of calretinin containing neurons in retina from rabbit, cat, and dog","volume":"32","author":"Jeon","year":"1998","journal-title":"Neurosci Res"},{"key":"bib42","doi-asserted-by":"publisher","first-page":"850","DOI":"10.1002\/cne.24101","article-title":"Membrane-associated guanylate kinase scaffolds organize a horizontal cell synaptic complex restricted to invaginating contacts with photoreceptors","volume":"525","author":"Vila","year":"2017","journal-title":"J Comp Neurol"},{"key":"bib43","doi-asserted-by":"publisher","first-page":"561","DOI":"10.1016\/0896-6273(95)90312-7","article-title":"Mammalian rod terminal: architecture of a binary synapse","volume":"14","author":"Rao-Mirotznik","year":"1995","journal-title":"Neuron"},{"key":"bib44","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1146\/annurev-vision-082114-035709","article-title":"Ribbon synapses and visual processing in the retina","volume":"1","author":"Lagnado","year":"2015","journal-title":"Annu Rev Vis Sci"},{"key":"bib45","doi-asserted-by":"publisher","first-page":"156","DOI":"10.1016\/j.mcn.2009.02.003","article-title":"PSD95\u00df regulates plasma membrane Ca2+ pump localization at the photoreceptor synapse","volume":"41","author":"Aartsen","year":"2009","journal-title":"Mol Cell Neurosci"},{"key":"bib46","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1038\/nrn2540","article-title":"Organization and dynamics of PDZ-domain-related supramodules in the postsynaptic density","volume":"10","author":"Feng","year":"2009","journal-title":"Nat Rev Neurosci"},{"key":"bib47","doi-asserted-by":"publisher","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":"bib48","first-page":"19","article-title":"Role of Bassoon and Piccolo in assembly and molecular organization of the active zone","volume":"7","author":"Gundelfinger","year":"2015","journal-title":"Front Synaptic Neurosci"},{"key":"bib49","doi-asserted-by":"publisher","first-page":"1291","DOI":"10.1093\/hmg\/ddl047","article-title":"Mpp4 recruits Psd95 and Veli3 towards the photoreceptor synapse","volume":"15","author":"Aartsen","year":"2006","journal-title":"Hum Mol Genet"},{"key":"bib50","doi-asserted-by":"publisher","first-page":"e1715232024","DOI":"10.1523\/JNEUROSCI.1715-23.2024","article-title":"Distinct SAP102 and PSD-95 nano-organization defines multiple types of synaptic scaffold protein domains at single synapses","volume":"44","author":"Metzbower","year":"2024","journal-title":"J Neurosci"},{"key":"bib51","doi-asserted-by":"publisher","first-page":"1669","DOI":"10.1167\/iovs.05-0845","article-title":"A frameshift mutation in RPGR exon ORF15 causes photoreceptor degeneration and inner retina remodeling in a model of X-linked retinitis pigmentosa","volume":"47","author":"Beltran","year":"2006","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"bib52","doi-asserted-by":"publisher","first-page":"126","DOI":"10.1002\/cne.21284","article-title":"Connections of diffuse bipolar cells in primate retina are biased against S-cones","volume":"502","author":"Lee","year":"2007","journal-title":"J Comp Neurol"},{"key":"bib53","doi-asserted-by":"publisher","first-page":"225","DOI":"10.1186\/s12917-020-02390-8","article-title":"Changes in retinal layer thickness with maturation in the dog: an in vivo spectral domain\u2013optical coherence tomography imaging study","volume":"16","author":"Occelli","year":"2020","journal-title":"BMC Vet Res"},{"key":"bib54","doi-asserted-by":"publisher","first-page":"107926","DOI":"10.1016\/j.exer.2020.107926","article-title":"In-vivo longitudinal changes in thickness of the postnatal canine retina","volume":"192","author":"Dufour","year":"2020","journal-title":"Exp Eye Res"},{"key":"bib55","doi-asserted-by":"publisher","first-page":"667046","DOI":"10.3389\/fncel.2021.667046","article-title":"Synaptic scaffolds, ion channels and polyamines in mouse photoreceptor synapses: anatomy of a signaling complex","volume":"15","author":"Vila","year":"2021","journal-title":"Front Cell Neurosci"},{"key":"bib56","first-page":"2165","article-title":"Ultrastructural changes of photoreceptor synaptic ribbons in relation to time of day and illumination","volume":"40","author":"Adly","year":"1999","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"bib57","doi-asserted-by":"publisher","first-page":"611","DOI":"10.1177\/1073858409340253","article-title":"The making of synaptic ribbons: how they are built and what they do","volume":"15","author":"Schmitz","year":"2009","journal-title":"Neuroscientist"},{"key":"bib58","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1007\/BF01188430","article-title":"Ribbon synapses of the mammalian retina contain two types of synaptic bodies\u2014ribbons and spheres","volume":"18","author":"Vollrath","year":"1989","journal-title":"J Neurocytol"}],"container-title":["Investigative Ophthalmology &amp; Visual Science"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/iovs.arvojournals.org\/article.aspx?doi=10.1167\/iovs.67.6.1","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,10,13]],"date-time":"2026-10-13T21:32:13Z","timestamp":1791927133000},"score":1,"resource":{"primary":{"URL":"http:\/\/iovs.arvojournals.org\/article.aspx?doi=10.1167\/iovs.67.6.1"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,6,1]]},"references-count":58,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2026,6,1]]}},"URL":"https:\/\/doi.org\/10.1167\/iovs.67.6.1","relation":{},"ISSN":["1552-5783"],"issn-type":[{"value":"1552-5783","type":"print"}],"subject":[],"published":{"date-parts":[[2026,6,1]]}}}