[{"file_date_updated":"2024-10-11T10:04:23Z","contributor":[{"id":"3F8ABDDA-F248-11E8-B48F-1D18A9856A87","contributor_type":"researcher","last_name":"Kim","first_name":"Olena"},{"orcid":"0000-0003-0408-6094","first_name":"Yuji","last_name":"Okamoto","contributor_type":"researcher","id":"3337E116-F248-11E8-B48F-1D18A9856A87"},{"last_name":"Kaufmann","orcid":"0000-0001-9735-5315","first_name":"Walter","id":"3F99E422-F248-11E8-B48F-1D18A9856A87","contributor_type":"researcher"},{"last_name":"Brose","first_name":"Nils ","contributor_type":"researcher"},{"last_name":"Shigemoto","first_name":"Ryuichi","orcid":"0000-0001-8761-9444","id":"499F3ABC-F248-11E8-B48F-1D18A9856A87","contributor_type":"researcher"},{"id":"353C1B58-F248-11E8-B48F-1D18A9856A87","contributor_type":"supervisor","last_name":"Jonas","orcid":"0000-0001-5001-4804","first_name":"Peter M"}],"year":"2024","month":"10","related_material":{"record":[{"id":"18603","status":"public","relation":"used_in_publication"}]},"author":[{"full_name":"Kim, Olena","id":"3F8ABDDA-F248-11E8-B48F-1D18A9856A87","last_name":"Kim","orcid":"0000-0003-2344-1039","first_name":"Olena"}],"date_updated":"2026-04-16T12:20:33Z","ddc":["570"],"project":[{"grant_number":"692692","name":"Biophysics and circuit function of a giant cortical glutamatergic synapse","call_identifier":"H2020","_id":"25B7EB9E-B435-11E9-9278-68D0E5697425"}],"abstract":[{"text":"It is widely believed that information storage in neuronal circuits involves nanoscopic structural changes at synapses, resulting in the formation of synaptic engrams. However, direct evidence for this hypothesis is lacking. To test this conjecture, we combined chemical potentiation, functional analysis by paired pre-postsynaptic recordings, and structural analysis by electron microscopy (EM) and freeze-fracture replica labeling (FRL) at the murine hippocampal mossy fiber synapse, a key synapse in the trisynaptic circuit of the hippocampus. Biophysical analysis of synaptic transmission revealed that forskolin-induced chemical potentiation increased the readily releasable vesicle pool size and vesicular release probability by 146% and 49%, respectively. Structural analysis of mossy fiber synapses by EM and FRL demonstrated an increase in the number of vesicles close to the plasma membrane and the number of clusters of the priming protein Munc13-1, indicating an increase in the number of both docked and primed vesicles. Furthermore, FRL analysis revealed a significant reduction of the distance between Munc13-1 and CaV2.1 Ca2+ channels, suggesting reconfiguration of the channel-vesicle coupling nanotopography. Our results indicate that presynaptic plasticity is associated with structural reorganization of active zones. We propose that changes in potential nanoscopic organization at synaptic vesicle release sites may be correlates of learning and memory at a plastic central synapse.","lang":"eng"}],"status":"public","has_accepted_license":"1","oa_version":"Submitted Version","date_created":"2024-10-11T10:12:17Z","type":"research_data","corr_author":"1","citation":{"chicago":"Kim, Olena. “Presynaptic CAMP-PKA-Mediated Potentiation Induces Reconfiguration of Synaptic Vesicle Pools and Channel-Vesicle Coupling at Hippocampal Mossy Fiber Boutons.” Institute of Science and Technology Austria, 2024. <a href=\"https://doi.org/10.15479/AT:ISTA:18296\">https://doi.org/10.15479/AT:ISTA:18296</a>.","ama":"Kim O. Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons. 2024. doi:<a href=\"https://doi.org/10.15479/AT:ISTA:18296\">10.15479/AT:ISTA:18296</a>","ista":"Kim O. 2024. Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons, Institute of Science and Technology Austria, <a href=\"https://doi.org/10.15479/AT:ISTA:18296\">10.15479/AT:ISTA:18296</a>.","ieee":"O. Kim, “Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons.” Institute of Science and Technology Austria, 2024.","apa":"Kim, O. (2024). Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons. Institute of Science and Technology Austria. <a href=\"https://doi.org/10.15479/AT:ISTA:18296\">https://doi.org/10.15479/AT:ISTA:18296</a>","short":"O. Kim, (2024).","mla":"Kim, Olena. <i>Presynaptic CAMP-PKA-Mediated Potentiation Induces Reconfiguration of Synaptic Vesicle Pools and Channel-Vesicle Coupling at Hippocampal Mossy Fiber Boutons</i>. Institute of Science and Technology Austria, 2024, doi:<a href=\"https://doi.org/10.15479/AT:ISTA:18296\">10.15479/AT:ISTA:18296</a>."},"ec_funded":1,"oa":1,"title":"Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons","user_id":"68b8ca59-c5b3-11ee-8790-cd641c68093d","department":[{"_id":"PeJo"},{"_id":"RySh"},{"_id":"EM-Fac"}],"keyword":["Hippocampal mossy fiber synapses","short-term potentiation","long-term potentiation","presynaptic plasticity","electron microscopy","freeze-fracture replica labeling","paired recordings","forskolin","cyclic adenosine monophosphate (cAMP)","protein kinase A (PKA)","neuromodulation","synaptic vesicle pools","presynaptic Ca2+ channels","Munc13","docking","priming","active zone"],"day":"11","tmp":{"short":"CC BY (4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)"},"article_processing_charge":"No","publisher":"Institute of Science and Technology Austria","doi":"10.15479/AT:ISTA:18296","file":[{"file_id":"18297","file_name":"Kim_et_al_2024_PlosBio_Source_data.zip","date_updated":"2024-10-11T10:04:19Z","checksum":"0a977e7df54c418251b10dfd3f8a015c","success":1,"file_size":164382,"date_created":"2024-10-11T10:04:19Z","content_type":"application/zip","access_level":"open_access","creator":"okim","relation":"main_file"},{"access_level":"open_access","relation":"main_file","creator":"okim","content_type":"text/plain","date_created":"2024-10-11T10:04:23Z","file_size":654,"date_updated":"2024-10-11T10:04:23Z","file_name":"info.txt","file_id":"18298","success":1,"checksum":"5b9343d6b2035ac3185e390fad4d3830"}],"date_published":"2024-10-11T00:00:00Z","_id":"18296"},{"date_updated":"2026-07-28T08:33:51Z","OA_place":"repository","doi":"10.1101/2024.05.02.592169","project":[{"name":"Synaptic computations of the hippocampal CA3 circuitry","_id":"fc2be41b-9c52-11eb-aca3-faa90aa144e9","call_identifier":"H2020","grant_number":"101026635"},{"_id":"26AA4EF2-B435-11E9-9278-68D0E5697425","name":"Molecular Drug Targets","call_identifier":"FWF","grant_number":"W1232-B24"},{"grant_number":"26137","name":"Studying Organelle Structure and Function at Nanoscale Resolution with Expansion Microscopy","_id":"6285a163-2b32-11ec-9570-8e204ca2dba5"}],"acknowledgement":"We thank Florian Marr for excellent technical assistance, Christina Altmutter and Julia Flor for technical support, Alois Schlögl for programming, Todor Asenov for development of the transportation box for human brain tissue, Tim Vogels for guidance on simulations, Marcus Huber for mathematical advice, and Eleftheria Kralli-Beller for manuscript editing. This research was supported by the Scientific Services Units (SSUs) of ISTA, and we are particularly grateful for assistance from Christoph Sommer and the Imaging and Optics Facility, Preclinical Facility, Life Science Facility, Miba Machine Shop, and Scientific Computing. We also acknowledge the excellent support of the Medical University of Vienna Department of Neurosurgery staff, Romana Hoeftberger and the Division of Neuropathology and Neurochemistry, and Gregor Kasprian and the Division of Neuroradiology and Musculoskeletal Radiology. The project received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (Marie Skłodowska-Curie Actions Individual Fellowship no. 101026635 to J.F.W.), the Austrian Science Fund (FWF; grant PAT 4178023 to P.J.; grant DK W1232 to M.R.T. and J.G.D.) and the Austrian Academy of Sciences (DOC fellowship 26137 to M.R.T.).","status":"public","abstract":[{"lang":"eng","text":"The human brain has remarkable computational power. It generates sophisticated behavioral sequences, stores engrams over an individual’s lifetime, and produces higher cognitive functions up to the level of consciousness. However, so little of our neuroscience knowledge covers the human brain, and it remains unknown whether this organ is truly unique, or is a scaled version of the extensively studied rodent brain. To address this fundamental question, we determined the cellular, synaptic, and connectivity rules of the hippocampal CA3 recurrent circuit using multicellular patch clamp-recording. This circuit is the largest autoassociative network in the brain, and plays a key role in memory and higher-order computations such as pattern separation and pattern completion. We demonstrate that human hippocampal CA3 employs sparse connectivity, in stark contrast to neocortical recurrent networks. Connectivity sparsifies from rodents to humans, providing a circuit architecture that maximizes associational power. Unitary synaptic events at human CA3–CA3 synapses showed both distinct species-specific and circuit-dependent properties, with high reliability, unique amplitude precision, and long integration times. We also identify differential scaling rules between hippocampal pathways from rodents to humans, with a moderate increase in the convergence of CA3 inputs per cell, but a marked increase in human mossy fiber innervation. Anatomically guided full-scale modeling suggests that the human brain’s sparse connectivity, expanded neuronal number, and reliable synaptic signaling combine to enhance the associative memory storage capacity of CA3. Together, our results reveal unique rules of connectivity and synaptic signaling in the human hippocampus, demonstrating the absolute necessity of human brain research and beginning to unravel the remarkable performance of our autoassociative memory circuits."}],"type":"preprint","corr_author":"1","main_file_link":[{"open_access":"1","url":"https://doi.org/10.1101/2024.05.02.592169"}],"oa_version":"Preprint","publication":"bioRxiv","date_created":"2024-12-19T11:35:08Z","language":[{"iso":"eng"}],"ec_funded":1,"citation":{"mla":"Watson, Jake F., et al. “Human Hippocampal CA3 Uses Specific Functional Connectivity Rules for Efficient Associative Memory.” <i>BioRxiv</i>, doi:<a href=\"https://doi.org/10.1101/2024.05.02.592169\">10.1101/2024.05.02.592169</a>.","short":"J.F. Watson, V. Vargas-Barroso, R.J. Morse-Mora, A. Navas-Olive, M. Tavakoli, J.G. Danzl, M. Tomschik, K. Rössler, P.M. Jonas, BioRxiv (n.d.).","apa":"Watson, J. F., Vargas-Barroso, V., Morse-Mora, R. J., Navas-Olive, A., Tavakoli, M., Danzl, J. G., … Jonas, P. M. (n.d.). Human hippocampal CA3 uses specific functional connectivity rules for efficient associative memory. <i>bioRxiv</i>. <a href=\"https://doi.org/10.1101/2024.05.02.592169\">https://doi.org/10.1101/2024.05.02.592169</a>","ama":"Watson JF, Vargas-Barroso V, Morse-Mora RJ, et al. Human hippocampal CA3 uses specific functional connectivity rules for efficient associative memory. <i>bioRxiv</i>. doi:<a href=\"https://doi.org/10.1101/2024.05.02.592169\">10.1101/2024.05.02.592169</a>","ista":"Watson JF, Vargas-Barroso V, Morse-Mora RJ, Navas-Olive A, Tavakoli M, Danzl JG, Tomschik M, Rössler K, Jonas PM. Human hippocampal CA3 uses specific functional connectivity rules for efficient associative memory. bioRxiv, <a href=\"https://doi.org/10.1101/2024.05.02.592169\">10.1101/2024.05.02.592169</a>.","ieee":"J. F. Watson <i>et al.</i>, “Human hippocampal CA3 uses specific functional connectivity rules for efficient associative memory,” <i>bioRxiv</i>. .","chicago":"Watson, Jake F., Victor Vargas-Barroso, Rebecca J. Morse-Mora, Andrea Navas-Olive, Mojtaba Tavakoli, Johann G Danzl, Matthias Tomschik, Karl Rössler, and Peter M Jonas. “Human Hippocampal CA3 Uses Specific Functional Connectivity Rules for Efficient Associative Memory.” <i>BioRxiv</i>, n.d. <a href=\"https://doi.org/10.1101/2024.05.02.592169\">https://doi.org/10.1101/2024.05.02.592169</a>."},"_id":"18688","date_published":"2024-05-02T00:00:00Z","title":"Human hippocampal CA3 uses specific functional connectivity rules for efficient associative memory","publication_status":"draft","oa":1,"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","year":"2024","department":[{"_id":"JoDa"},{"_id":"PeJo"}],"month":"05","related_material":{"record":[{"relation":"later_version","status":"public","id":"18879"},{"relation":"dissertation_contains","status":"public","id":"18681"}]},"day":"02","author":[{"full_name":"Watson, Jake F.","first_name":"Jake F.","last_name":"Watson"},{"full_name":"Vargas-Barroso, Victor","last_name":"Vargas-Barroso","first_name":"Victor"},{"full_name":"Morse-Mora, Rebecca J.","first_name":"Rebecca J.","last_name":"Morse-Mora"},{"full_name":"Navas-Olive, Andrea","last_name":"Navas-Olive","first_name":"Andrea"},{"last_name":"Tavakoli","orcid":"0000-0002-7667-6854","first_name":"Mojtaba","full_name":"Tavakoli, Mojtaba","id":"3A0A06F4-F248-11E8-B48F-1D18A9856A87"},{"last_name":"Danzl","orcid":"0000-0001-8559-3973","first_name":"Johann G","full_name":"Danzl, Johann G","id":"42EFD3B6-F248-11E8-B48F-1D18A9856A87"},{"last_name":"Tomschik","first_name":"Matthias","full_name":"Tomschik, Matthias"},{"first_name":"Karl","last_name":"Rössler","full_name":"Rössler, Karl"},{"id":"353C1B58-F248-11E8-B48F-1D18A9856A87","full_name":"Jonas, Peter M","first_name":"Peter M","orcid":"0000-0001-5001-4804","last_name":"Jonas"}],"acknowledged_ssus":[{"_id":"Bio"},{"_id":"LifeSc"},{"_id":"M-Shop"},{"_id":"PreCl"},{"_id":"ScienComp"}],"article_processing_charge":"No"},{"_id":"14843","quality_controlled":"1","date_published":"2024-03-06T00:00:00Z","file":[{"file_size":8192355,"success":1,"checksum":"30098b4f0209556ddfb3540a23d07ca5","file_id":"19614","file_name":"2024_Neuron_Chen.pdf","date_updated":"2025-04-23T14:02:08Z","creator":"dernst","relation":"main_file","access_level":"open_access","content_type":"application/pdf","date_created":"2025-04-23T14:02:08Z"}],"acknowledgement":"We thank Drs. David DiGregorio and Erwin Neher for critically reading an earlier version of the manuscript, Ralf Schneggenburger for helpful discussions, Benjamin Suter and Katharina Lichter for support with image analysis, Chris Wojtan for advice on numerical solution of partial differential equations, Maria Reva for help with Ripley analysis, Alois Schlögl for programming, and Akari Hagiwara and Toshihisa Ohtsuka for anti-ELKS antibody. We are grateful to Florian Marr, Christina Altmutter, and Vanessa Zheden for excellent technical assistance and to Eleftheria Kralli-Beller for manuscript editing. This research was supported by the Scientific Services Units (SSUs) of ISTA (Electron Microscopy Facility, Preclinical Facility, and Machine Shop). The project received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement no. 692692), the Fonds zur Förderung der Wissenschaftlichen Forschung (Z 312-B27, Wittgenstein award; P 36232-B), all to P.J., and a DOC fellowship of the Austrian Academy of Sciences to J.-J.C.","isi":1,"doi":"10.1016/j.neuron.2023.12.002","publisher":"Elsevier","article_processing_charge":"Yes (via OA deal)","PlanS_conform":"1","publication_identifier":{"eissn":["1097-4199"],"issn":["0896-6273"]},"tmp":{"short":"CC BY (4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)"},"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","oa":1,"title":"Developmental transformation of Ca2+ channel-vesicle nanotopography at a central GABAergic synapse","day":"06","department":[{"_id":"PeJo"},{"_id":"EM-Fac"},{"_id":"RySh"}],"date_created":"2024-01-21T23:00:56Z","oa_version":"Published Version","scopus_import":"1","publication":"Neuron","type":"journal_article","corr_author":"1","abstract":[{"text":"The coupling between Ca2+ channels and release sensors is a key factor defining the signaling properties of a synapse. However, the coupling nanotopography at many synapses remains unknown, and it is unclear how it changes during development. To address these questions, we examined coupling at the cerebellar inhibitory basket cell (BC)-Purkinje cell (PC) synapse. Biophysical analysis of transmission by paired recording and intracellular pipette perfusion revealed that the effects of exogenous Ca2+ chelators decreased during development, despite constant reliance of release on P/Q-type Ca2+ channels. Structural analysis by freeze-fracture replica labeling (FRL) and transmission electron microscopy (EM) indicated that presynaptic P/Q-type Ca2+ channels formed nanoclusters throughout development, whereas docked vesicles were only clustered at later developmental stages. Modeling suggested a developmental transformation from a more random to a more clustered coupling nanotopography. Thus, presynaptic signaling developmentally approaches a point-to-point configuration, optimizing speed, reliability, and energy efficiency of synaptic transmission.","lang":"eng"}],"status":"public","has_accepted_license":"1","external_id":{"pmid":["38215739"],"isi":["001202925700001"]},"ec_funded":1,"article_type":"original","citation":{"chicago":"Chen, JingJing, Walter Kaufmann, Chong Chen, itaru Arai, Olena Kim, Ryuichi Shigemoto, and Peter M Jonas. “Developmental Transformation of Ca2+ Channel-Vesicle Nanotopography at a Central GABAergic Synapse.” <i>Neuron</i>. Elsevier, 2024. <a href=\"https://doi.org/10.1016/j.neuron.2023.12.002\">https://doi.org/10.1016/j.neuron.2023.12.002</a>.","ama":"Chen J, Kaufmann W, Chen C, et al. Developmental transformation of Ca2+ channel-vesicle nanotopography at a central GABAergic synapse. <i>Neuron</i>. 2024;112(5):755-771.e9. doi:<a href=\"https://doi.org/10.1016/j.neuron.2023.12.002\">10.1016/j.neuron.2023.12.002</a>","ieee":"J. Chen <i>et al.</i>, “Developmental transformation of Ca2+ channel-vesicle nanotopography at a central GABAergic synapse,” <i>Neuron</i>, vol. 112, no. 5. Elsevier, p. 755–771.e9, 2024.","ista":"Chen J, Kaufmann W, Chen C, Arai  itaru, Kim O, Shigemoto R, Jonas PM. 2024. Developmental transformation of Ca2+ channel-vesicle nanotopography at a central GABAergic synapse. Neuron. 112(5), 755–771.e9.","apa":"Chen, J., Kaufmann, W., Chen, C., Arai,  itaru, Kim, O., Shigemoto, R., &#38; Jonas, P. M. (2024). Developmental transformation of Ca2+ channel-vesicle nanotopography at a central GABAergic synapse. <i>Neuron</i>. Elsevier. <a href=\"https://doi.org/10.1016/j.neuron.2023.12.002\">https://doi.org/10.1016/j.neuron.2023.12.002</a>","short":"J. Chen, W. Kaufmann, C. Chen,  itaru Arai, O. Kim, R. Shigemoto, P.M. Jonas, Neuron 112 (2024) 755–771.e9.","mla":"Chen, JingJing, et al. “Developmental Transformation of Ca2+ Channel-Vesicle Nanotopography at a Central GABAergic Synapse.” <i>Neuron</i>, vol. 112, no. 5, Elsevier, 2024, p. 755–771.e9, doi:<a href=\"https://doi.org/10.1016/j.neuron.2023.12.002\">10.1016/j.neuron.2023.12.002</a>."},"language":[{"iso":"eng"}],"OA_place":"publisher","intvolume":"       112","date_updated":"2026-09-03T22:30:34Z","ddc":["570"],"OA_type":"hybrid","project":[{"name":"Biophysics and circuit function of a giant cortical glutamatergic synapse","call_identifier":"H2020","_id":"25B7EB9E-B435-11E9-9278-68D0E5697425","grant_number":"692692"},{"name":"Synaptic communication in neuronal microcircuits","_id":"25C5A090-B435-11E9-9278-68D0E5697425","call_identifier":"FWF","grant_number":"Z00312"},{"_id":"bd88be38-d553-11ed-ba76-81d5a70a6ef5","name":"Mechanisms of GABA release in hippocampal circuits","grant_number":"P36232"},{"grant_number":"25383","name":"Development of nanodomain coupling between Ca2+ channels and release sensors at a central inhibitory synapse","_id":"26B66A3E-B435-11E9-9278-68D0E5697425"}],"acknowledged_ssus":[{"_id":"EM-Fac"},{"_id":"PreCl"},{"_id":"M-Shop"}],"author":[{"full_name":"Chen, JingJing","id":"2C4E65C8-F248-11E8-B48F-1D18A9856A87","last_name":"Chen","first_name":"JingJing"},{"first_name":"Walter","orcid":"0000-0001-9735-5315","last_name":"Kaufmann","id":"3F99E422-F248-11E8-B48F-1D18A9856A87","full_name":"Kaufmann, Walter"},{"id":"3DFD581A-F248-11E8-B48F-1D18A9856A87","full_name":"Chen, Chong","first_name":"Chong","last_name":"Chen"},{"first_name":"Itaru","last_name":"Arai","full_name":"Arai, Itaru","id":"32A73F6C-F248-11E8-B48F-1D18A9856A87"},{"id":"3F8ABDDA-F248-11E8-B48F-1D18A9856A87","full_name":"Kim, Olena","first_name":"Olena","orcid":"0000-0003-2344-1039","last_name":"Kim"},{"id":"499F3ABC-F248-11E8-B48F-1D18A9856A87","full_name":"Shigemoto, Ryuichi","first_name":"Ryuichi","orcid":"0000-0001-8761-9444","last_name":"Shigemoto"},{"first_name":"Peter M","orcid":"0000-0001-5001-4804","last_name":"Jonas","id":"353C1B58-F248-11E8-B48F-1D18A9856A87","full_name":"Jonas, Peter M"}],"pmid":1,"page":"755-771.e9","year":"2024","publication_status":"published","file_date_updated":"2025-04-23T14:02:08Z","related_material":{"record":[{"status":"public","id":"15101","relation":"dissertation_contains"}],"link":[{"url":"https://ista.ac.at/en/news/synapses-brought-to-the-point/","relation":"press_release","description":"News on ISTA Website"}]},"issue":"5","volume":112,"month":"03"},{"OA_place":"publisher","date_updated":"2026-04-07T13:24:22Z","ddc":["570"],"project":[{"call_identifier":"H2020","_id":"25B7EB9E-B435-11E9-9278-68D0E5697425","name":"Biophysics and circuit function of a giant cortical glutamatergic synapse","grant_number":"692692"},{"grant_number":"Z00312","name":"Synaptic communication in neuronal microcircuits","_id":"25C5A090-B435-11E9-9278-68D0E5697425","call_identifier":"FWF"},{"grant_number":"P36232","_id":"bd88be38-d553-11ed-ba76-81d5a70a6ef5","name":"Mechanisms of GABA release in hippocampal circuits"},{"name":"Development of nanodomain coupling between Ca2+ channels and release sensors at a central inhibitory synapse","_id":"26B66A3E-B435-11E9-9278-68D0E5697425","grant_number":"25383"}],"oa_version":"Published Version","date_created":"2024-03-11T10:09:54Z","corr_author":"1","type":"dissertation","abstract":[{"lang":"eng","text":"The coupling between presynaptic Ca2+ channels and release sensors is a key factor that\r\ndetermines speed and efficacy of synapse transmission. At some excitatory synapses,\r\nchannel–sensor coupling becomes tighter during development, and tightening is often\r\nassociated with a switch in the reliance on different Ca2+ channel subtypes. However, the\r\ncoupling topography at many synapses remains unknown, and it is unclear how it changes\r\nduring development. To address this question, we analyzed the coupling configuration at the\r\ncerebellar basket cell (BC) to Purkinje cell (PC) synapse at different developmental stages,\r\ncombining biophysical analysis, structural analysis, and modeling.\r\nQuantal analysis of BC–PC indicated that release probability decreased, while the\r\nnumber of functional sites increased during development. Although transmitter release\r\npersistently relied on P/Q-type Ca2+ channels in the time period postnatal day 7–23, effects\r\nof the Ca2+ chelator EGTA and BAPTA applied by intracellular pipette perfusion decreased\r\nduring development, indicative of tightening of source-sensor coupling. Furthermore,\r\npresynaptic action potentials became shorter during development, suggesting reduced\r\nefficacy of Ca2+ channel activation.\r\nStructural analysis by freeze-fracture replica labeling (FRL) and transmission electron\r\nmicroscopy (EM) indicated that presynaptic P/Q-type Ca2+ channels formed nanoclusters\r\nthroughout development, whereas docked vesicles were only clustered at later\r\ndevelopmental stages. The number of functional release sites correlated better with the AZ\r\nnumber early in development, but match better with the Ca2+ channel cluster number at later\r\nstages.\r\nModeling suggested a developmental transformation from a more random to a more\r\nclustered coupling nanotopography. Thus, presynaptic signaling developmentally approaches\r\na point-to-point configuration, optimizing speed, reliability, and energy efficiency of synaptic\r\ntransmission."}],"has_accepted_license":"1","status":"public","citation":{"chicago":"Chen, JingJing. “Developmental Transformation of Nanodomain Coupling between Ca2+ Channels and Release Sensors at a Central GABAergic Synapse.” Institute of Science and Technology Austria, 2024. <a href=\"https://doi.org/10.15479/at:ista:15101\">https://doi.org/10.15479/at:ista:15101</a>.","short":"J. Chen, Developmental Transformation of Nanodomain Coupling between Ca2+ Channels and Release Sensors at a Central GABAergic Synapse, Institute of Science and Technology Austria, 2024.","mla":"Chen, JingJing. <i>Developmental Transformation of Nanodomain Coupling between Ca2+ Channels and Release Sensors at a Central GABAergic Synapse</i>. Institute of Science and Technology Austria, 2024, doi:<a href=\"https://doi.org/10.15479/at:ista:15101\">10.15479/at:ista:15101</a>.","ama":"Chen J. Developmental transformation of nanodomain coupling between Ca2+ channels and release sensors at a central GABAergic synapse. 2024. doi:<a href=\"https://doi.org/10.15479/at:ista:15101\">10.15479/at:ista:15101</a>","ieee":"J. Chen, “Developmental transformation of nanodomain coupling between Ca2+ channels and release sensors at a central GABAergic synapse,” Institute of Science and Technology Austria, 2024.","ista":"Chen J. 2024. Developmental transformation of nanodomain coupling between Ca2+ channels and release sensors at a central GABAergic synapse. Institute of Science and Technology Austria.","apa":"Chen, J. (2024). <i>Developmental transformation of nanodomain coupling between Ca2+ channels and release sensors at a central GABAergic synapse</i>. Institute of Science and Technology Austria. <a href=\"https://doi.org/10.15479/at:ista:15101\">https://doi.org/10.15479/at:ista:15101</a>"},"ec_funded":1,"language":[{"iso":"eng"}],"year":"2024","publication_status":"published","file_date_updated":"2024-04-02T22:30:03Z","related_material":{"record":[{"status":"public","id":"14843","relation":"part_of_dissertation"}]},"month":"03","alternative_title":["ISTA Thesis"],"acknowledged_ssus":[{"_id":"EM-Fac"}],"author":[{"full_name":"Chen, JingJing","id":"2C4E65C8-F248-11E8-B48F-1D18A9856A87","first_name":"JingJing","last_name":"Chen"}],"page":"84","doi":"10.15479/at:ista:15101","file":[{"creator":"jchen","relation":"source_file","access_level":"closed","date_created":"2024-03-11T14:10:58Z","content_type":"application/vnd.openxmlformats-officedocument.wordprocessingml.document","file_size":11271363,"embargo_to":"open_access","checksum":"db4947474ffa271e66c254b6fe876a55","file_name":"Thesis_Jingjing CHEN.docx","file_id":"15104","date_updated":"2024-04-02T22:30:03Z"},{"date_created":"2024-03-11T14:11:06Z","content_type":"application/pdf","access_level":"open_access","relation":"main_file","creator":"jchen","date_updated":"2024-04-02T22:30:03Z","embargo":"2024-04-01","file_name":"Thesis_Jingjing CHEN_merged.pdf","file_id":"15105","checksum":"a5eeae8b5702cd540f5d03469bc33dde","file_size":16627311}],"degree_awarded":"PhD","publisher":"Institute of Science and Technology Austria","supervisor":[{"first_name":"Peter M","orcid":"0000-0001-5001-4804","last_name":"Jonas","id":"353C1B58-F248-11E8-B48F-1D18A9856A87","full_name":"Jonas, Peter M"}],"date_published":"2024-03-11T00:00:00Z","_id":"15101","user_id":"ba8df636-2132-11f1-aed0-ed93e2281fdd","oa":1,"title":"Developmental transformation of nanodomain coupling between Ca2+ channels and release sensors at a central GABAergic synapse","day":"11","department":[{"_id":"GradSch"},{"_id":"PeJo"}],"article_processing_charge":"No","publication_identifier":{"issn":["2663-337X"]},"tmp":{"short":"CC BY (4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)"}},{"doi":"10.1073/pnas.2301449121","acknowledgement":"We thank Erwin Neher and Ipe Ninan for critical comments on the manuscript. This project has received funding from the European Research Council (ERC) and European Commission, under the European Union’s Horizon 2020 research and innovation program (ERC grant agreement no. 694539 to R.S. and the Marie Skłodowska-Curie grant agreement no. 665385 to C.Ö.). This study was supported by the Cooperative Study Program of Center for Animal Resources and Collaborative Study of NINS. We thank Kohgaku Eguchi for statistical analysis, Yu Kasugai for additional EM imaging, Robert Beattie for the design of the slice recovery chamber for Flash and Freeze experiments, Todor Asenov from the ISTA machine shop for custom part preparations for high-pressure freezing, the ISTA preclinical facility for animal caretaking, and the ISTA EM facilities for technical support.","file":[{"file_size":13648221,"file_name":"2024_PNAS_Koppensteiner.pdf","file_id":"15110","date_updated":"2024-03-12T13:42:42Z","success":1,"checksum":"b25b2a057c266ff317a48b0d54d6fc8a","access_level":"open_access","creator":"dernst","relation":"main_file","content_type":"application/pdf","date_created":"2024-03-12T13:42:42Z"}],"isi":1,"publisher":"National Academy of Sciences","date_published":"2024-02-20T00:00:00Z","_id":"15084","quality_controlled":"1","article_number":"e2301449121","day":"20","department":[{"_id":"RySh"},{"_id":"PeJo"}],"license":"https://creativecommons.org/licenses/by-nc-nd/4.0/","user_id":"317138e5-6ab7-11ef-aa6d-ffef3953e345","oa":1,"title":"GABAB receptors induce phasic release from medial habenula terminals through activity-dependent recruitment of release-ready vesicles","article_processing_charge":"Yes (in subscription journal)","APC_amount":"5887,8 EUR","publication_identifier":{"issn":["0027-8424"],"eissn":["1091-6490"]},"tmp":{"short":"CC BY-NC-ND (4.0)","legal_code_url":"https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode","name":"Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0)","image":"/images/cc_by_nc_nd.png"},"OA_type":"hybrid","project":[{"_id":"25CA28EA-B435-11E9-9278-68D0E5697425","name":"In situ analysis of single channel subunit composition in neurons: physiological implication in synaptic plasticity and behaviour","call_identifier":"H2020","grant_number":"694539"},{"_id":"2564DBCA-B435-11E9-9278-68D0E5697425","name":"International IST Doctoral Program","call_identifier":"H2020","grant_number":"665385"}],"intvolume":"       121","OA_place":"publisher","date_updated":"2026-09-03T22:30:38Z","ddc":["570"],"ec_funded":1,"article_type":"original","citation":{"mla":"Koppensteiner, Peter, et al. “GABAB Receptors Induce Phasic Release from Medial Habenula Terminals through Activity-Dependent Recruitment of Release-Ready Vesicles.” <i>Proceedings of the National Academy of Sciences of the United States of America</i>, vol. 121, no. 8, e2301449121, National Academy of Sciences, 2024, doi:<a href=\"https://doi.org/10.1073/pnas.2301449121\">10.1073/pnas.2301449121</a>.","short":"P. Koppensteiner, P. Bhandari, C. Önal, C. Borges Merjane, E. Le Monnier, U. Roy, Y. Nakamura, T. Sadakata, M. Sanbo, M. Hirabayashi, J. Rhee, N. Brose, P.M. Jonas, R. Shigemoto, Proceedings of the National Academy of Sciences of the United States of America 121 (2024).","apa":"Koppensteiner, P., Bhandari, P., Önal, C., Borges Merjane, C., Le Monnier, E., Roy, U., … Shigemoto, R. (2024). GABAB receptors induce phasic release from medial habenula terminals through activity-dependent recruitment of release-ready vesicles. <i>Proceedings of the National Academy of Sciences of the United States of America</i>. National Academy of Sciences. <a href=\"https://doi.org/10.1073/pnas.2301449121\">https://doi.org/10.1073/pnas.2301449121</a>","ista":"Koppensteiner P, Bhandari P, Önal C, Borges Merjane C, Le Monnier E, Roy U, Nakamura Y, Sadakata T, Sanbo M, Hirabayashi M, Rhee J, Brose N, Jonas PM, Shigemoto R. 2024. GABAB receptors induce phasic release from medial habenula terminals through activity-dependent recruitment of release-ready vesicles. Proceedings of the National Academy of Sciences of the United States of America. 121(8), e2301449121.","ama":"Koppensteiner P, Bhandari P, Önal C, et al. GABAB receptors induce phasic release from medial habenula terminals through activity-dependent recruitment of release-ready vesicles. <i>Proceedings of the National Academy of Sciences of the United States of America</i>. 2024;121(8). doi:<a href=\"https://doi.org/10.1073/pnas.2301449121\">10.1073/pnas.2301449121</a>","ieee":"P. Koppensteiner <i>et al.</i>, “GABAB receptors induce phasic release from medial habenula terminals through activity-dependent recruitment of release-ready vesicles,” <i>Proceedings of the National Academy of Sciences of the United States of America</i>, vol. 121, no. 8. National Academy of Sciences, 2024.","chicago":"Koppensteiner, Peter, Pradeep Bhandari, Cihan Önal, Carolina Borges Merjane, Elodie Le Monnier, Utsa Roy, Yukihiro Nakamura, et al. “GABAB Receptors Induce Phasic Release from Medial Habenula Terminals through Activity-Dependent Recruitment of Release-Ready Vesicles.” <i>Proceedings of the National Academy of Sciences of the United States of America</i>. National Academy of Sciences, 2024. <a href=\"https://doi.org/10.1073/pnas.2301449121\">https://doi.org/10.1073/pnas.2301449121</a>."},"language":[{"iso":"eng"}],"date_created":"2024-03-05T09:23:55Z","publication":"Proceedings of the National Academy of Sciences of the United States of America","scopus_import":"1","oa_version":"Published Version","type":"journal_article","corr_author":"1","abstract":[{"lang":"eng","text":"GABAB receptor (GBR) activation inhibits neurotransmitter release in axon terminals in the brain, except in medial habenula (MHb) terminals, which show robust potentiation. However, mechanisms underlying this enigmatic potentiation remain elusive. Here, we report that GBR activation on MHb terminals induces an activity-dependent transition from a facilitating, tonic to a depressing, phasic neurotransmitter release mode. This transition is accompanied by a 4.1-fold increase in readily releasable vesicle pool (RRP) size and a 3.5-fold increase of docked synaptic vesicles (SVs) at the presynaptic active zone (AZ). Strikingly, the depressing phasic release exhibits looser coupling distance than the tonic release. Furthermore, the tonic and phasic release are selectively affected by deletion of synaptoporin (SPO) and Ca\r\n            <jats:sup>2+</jats:sup>\r\n            -dependent activator protein for secretion 2 (CAPS2), respectively. SPO modulates augmentation, the short-term plasticity associated with tonic release, and CAPS2 retains the increased RRP for initial responses in phasic response trains. The cytosolic protein CAPS2 showed a SV-associated distribution similar to the vesicular transmembrane protein SPO, and they were colocalized in the same terminals. We developed the “Flash and Freeze-fracture” method, and revealed the release of SPO-associated vesicles in both tonic and phasic modes and activity-dependent recruitment of CAPS2 to the AZ during phasic release, which lasted several minutes. Overall, these results indicate that GBR activation translocates CAPS2 to the AZ along with the fusion of CAPS2-associated SVs, contributing to persistency of the RRP increase. Thus, we identified structural and molecular mechanisms underlying tonic and phasic neurotransmitter release and their transition by GBR activation in MHb terminals."}],"has_accepted_license":"1","status":"public","external_id":{"isi":["001208567300006"],"pmid":["38346189"]},"issue":"8","related_material":{"link":[{"url":"https://ista.ac.at/en/news/neuronal-insights-flash-and-freeze-fracture/","relation":"press_release","description":"News on ISTA Website"}],"record":[{"relation":"research_data","status":"public","id":"13173"},{"id":"19271","status":"public","relation":"dissertation_contains"}]},"volume":121,"month":"02","year":"2024","file_date_updated":"2024-03-12T13:42:42Z","publication_status":"published","pmid":1,"acknowledged_ssus":[{"_id":"M-Shop"},{"_id":"PreCl"},{"_id":"EM-Fac"}],"author":[{"full_name":"Koppensteiner, Peter","id":"3B8B25A8-F248-11E8-B48F-1D18A9856A87","last_name":"Koppensteiner","orcid":"0000-0002-3509-1948","first_name":"Peter"},{"orcid":"0000-0003-0863-4481","first_name":"Pradeep","last_name":"Bhandari","full_name":"Bhandari, Pradeep","id":"45EDD1BC-F248-11E8-B48F-1D18A9856A87"},{"first_name":"Hüseyin C","orcid":"0000-0002-2771-2011","last_name":"Önal","id":"4659D740-F248-11E8-B48F-1D18A9856A87","full_name":"Önal, Hüseyin C"},{"id":"4305C450-F248-11E8-B48F-1D18A9856A87","full_name":"Borges Merjane, Carolina","first_name":"Carolina","orcid":"0000-0003-0005-401X","last_name":"Borges Merjane"},{"last_name":"Le Monnier","first_name":"Elodie","id":"3B59276A-F248-11E8-B48F-1D18A9856A87","full_name":"Le Monnier, Elodie"},{"last_name":"Roy","first_name":"Utsa","id":"4d26cf11-5355-11ee-ae5a-eb05e255b9b2","full_name":"Roy, Utsa"},{"full_name":"Nakamura, Yukihiro","last_name":"Nakamura","first_name":"Yukihiro"},{"last_name":"Sadakata","first_name":"Tetsushi","full_name":"Sadakata, Tetsushi"},{"full_name":"Sanbo, Makoto","last_name":"Sanbo","first_name":"Makoto"},{"first_name":"Masumi","last_name":"Hirabayashi","full_name":"Hirabayashi, Masumi"},{"full_name":"Rhee, JeongSeop","last_name":"Rhee","first_name":"JeongSeop"},{"full_name":"Brose, Nils","last_name":"Brose","first_name":"Nils"},{"first_name":"Peter M","orcid":"0000-0001-5001-4804","last_name":"Jonas","id":"353C1B58-F248-11E8-B48F-1D18A9856A87","full_name":"Jonas, Peter M"},{"full_name":"Shigemoto, Ryuichi","id":"499F3ABC-F248-11E8-B48F-1D18A9856A87","last_name":"Shigemoto","orcid":"0000-0001-8761-9444","first_name":"Ryuichi"}]},{"author":[{"last_name":"Ortiz-Leal","first_name":"Irene","full_name":"Ortiz-Leal, Irene"},{"full_name":"Torres, Mateo V.","first_name":"Mateo V.","last_name":"Torres"},{"full_name":"Vargas Barroso, Victor M","id":"2F55A9DE-F248-11E8-B48F-1D18A9856A87","last_name":"Vargas Barroso","first_name":"Victor M"},{"first_name":"Luis Eusebio","last_name":"Fidalgo","full_name":"Fidalgo, Luis Eusebio"},{"full_name":"López-Beceiro, Ana María","first_name":"Ana María","last_name":"López-Beceiro"},{"full_name":"Larriva-Sahd, Jorge A.","first_name":"Jorge A.","last_name":"Larriva-Sahd"},{"first_name":"Pablo","last_name":"Sánchez-Quinteiro","full_name":"Sánchez-Quinteiro, Pablo"}],"pmid":1,"year":"2023","file_date_updated":"2023-02-06T07:56:14Z","publication_status":"published","volume":16,"month":"01","date_created":"2023-02-05T23:01:00Z","publication":"Frontiers in Neuroanatomy","scopus_import":"1","oa_version":"Published Version","type":"journal_article","abstract":[{"text":"Introduction: The olfactory system in most mammals is divided into several subsystems based on the anatomical locations of the neuroreceptor cells involved and the receptor families that are expressed. In addition to the main olfactory system and the vomeronasal system, a range of olfactory subsystems converge onto the transition zone located between the main olfactory bulb (MOB) and the accessory olfactory bulb (AOB), which has been termed the olfactory limbus (OL). The OL contains specialized glomeruli that receive noncanonical sensory afferences and which interact with the MOB and AOB. Little is known regarding the olfactory subsystems of mammals other than laboratory rodents.\r\nMethods: We have focused on characterizing the OL in the red fox by performing general and specific histological stainings on serial sections, using both single and double immunohistochemical and lectin-histochemical labeling techniques.\r\nResults: As a result, we have been able to determine that the OL of the red fox (Vulpes vulpes) displays an uncommonly high degree of development and complexity.\r\nDiscussion: This makes this species a novel mammalian model, the study of which could improve our understanding of the noncanonical pathways involved in the processing of chemosensory cues.","lang":"eng"}],"has_accepted_license":"1","status":"public","external_id":{"isi":["000919786900001"],"pmid":["36704406"]},"article_type":"original","citation":{"apa":"Ortiz-Leal, I., Torres, M. V., Vargas Barroso, V. M., Fidalgo, L. E., López-Beceiro, A. M., Larriva-Sahd, J. A., &#38; Sánchez-Quinteiro, P. (2023). The olfactory limbus of the red fox (Vulpes vulpes). New insights regarding a noncanonical olfactory bulb pathway. <i>Frontiers in Neuroanatomy</i>. Frontiers. <a href=\"https://doi.org/10.3389/fnana.2022.1097467\">https://doi.org/10.3389/fnana.2022.1097467</a>","ama":"Ortiz-Leal I, Torres MV, Vargas Barroso VM, et al. The olfactory limbus of the red fox (Vulpes vulpes). New insights regarding a noncanonical olfactory bulb pathway. <i>Frontiers in Neuroanatomy</i>. 2023;16. doi:<a href=\"https://doi.org/10.3389/fnana.2022.1097467\">10.3389/fnana.2022.1097467</a>","ieee":"I. Ortiz-Leal <i>et al.</i>, “The olfactory limbus of the red fox (Vulpes vulpes). New insights regarding a noncanonical olfactory bulb pathway,” <i>Frontiers in Neuroanatomy</i>, vol. 16. Frontiers, 2023.","ista":"Ortiz-Leal I, Torres MV, Vargas Barroso VM, Fidalgo LE, López-Beceiro AM, Larriva-Sahd JA, Sánchez-Quinteiro P. 2023. The olfactory limbus of the red fox (Vulpes vulpes). New insights regarding a noncanonical olfactory bulb pathway. Frontiers in Neuroanatomy. 16, 1097467.","mla":"Ortiz-Leal, Irene, et al. “The Olfactory Limbus of the Red Fox (Vulpes Vulpes). New Insights Regarding a Noncanonical Olfactory Bulb Pathway.” <i>Frontiers in Neuroanatomy</i>, vol. 16, 1097467, Frontiers, 2023, doi:<a href=\"https://doi.org/10.3389/fnana.2022.1097467\">10.3389/fnana.2022.1097467</a>.","short":"I. Ortiz-Leal, M.V. Torres, V.M. Vargas Barroso, L.E. Fidalgo, A.M. López-Beceiro, J.A. Larriva-Sahd, P. Sánchez-Quinteiro, Frontiers in Neuroanatomy 16 (2023).","chicago":"Ortiz-Leal, Irene, Mateo V. Torres, Victor M Vargas Barroso, Luis Eusebio Fidalgo, Ana María López-Beceiro, Jorge A. Larriva-Sahd, and Pablo Sánchez-Quinteiro. “The Olfactory Limbus of the Red Fox (Vulpes Vulpes). New Insights Regarding a Noncanonical Olfactory Bulb Pathway.” <i>Frontiers in Neuroanatomy</i>. Frontiers, 2023. <a href=\"https://doi.org/10.3389/fnana.2022.1097467\">https://doi.org/10.3389/fnana.2022.1097467</a>."},"language":[{"iso":"eng"}],"intvolume":"        16","date_updated":"2023-08-16T11:37:52Z","ddc":["570"],"article_processing_charge":"No","publication_identifier":{"eissn":["1662-5129"]},"tmp":{"short":"CC BY (4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)"},"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","oa":1,"title":"The olfactory limbus of the red fox (Vulpes vulpes). New insights regarding a noncanonical olfactory bulb pathway","day":"10","department":[{"_id":"PeJo"}],"_id":"12515","date_published":"2023-01-10T00:00:00Z","quality_controlled":"1","article_number":"1097467","isi":1,"acknowledgement":"This work was partially supported by a grant from “Consello Social Universidade de Santiago de Compostela” 2022-PU004.We would like to show special gratitude to Prof. Ludwig Wagner (Medical University, Vienna) for kindly providing us with the secretagogin antibody. We thank the Wildlife Recovery Centres of Galicia, Dirección Xeral de Patrimonio Natural (Xunta de Galicia, Spain), and Federación Galega de Caza for providing the red foxes used in this study.","doi":"10.3389/fnana.2022.1097467","file":[{"content_type":"application/pdf","date_created":"2023-02-06T07:56:14Z","creator":"dernst","relation":"main_file","access_level":"open_access","checksum":"49cd40f3bda6f267079427042e7d15e3","success":1,"file_id":"12518","file_name":"2022_FrontiersNeuroanatomy_OrtizLeal.pdf","date_updated":"2023-02-06T07:56:14Z","file_size":21943473}],"publisher":"Frontiers"},{"publication_identifier":{"eissn":["1422-0067"]},"tmp":{"short":"CC BY (4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)"},"article_processing_charge":"No","department":[{"_id":"PeJo"}],"day":"21","oa":1,"title":"Single-molecule localization microscopy of presynaptic active zones in Drosophila melanogaster after rapid cryofixation","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","article_number":"2128","quality_controlled":"1","_id":"12567","date_published":"2023-01-21T00:00:00Z","publisher":"MDPI","isi":1,"file":[{"file_id":"12569","file_name":"2023_IJMS_Mrestani.pdf","date_updated":"2023-02-20T07:09:27Z","success":1,"checksum":"69a35dcd3e0249f902ab881b06ee2e58","file_size":2823025,"date_created":"2023-02-20T07:09:27Z","content_type":"application/pdf","access_level":"open_access","creator":"dernst","relation":"main_file"}],"acknowledgement":"This work has been supported by funding of the German Research Foundation (Deutsche Forschungsgemeinschaft [DFG], CRC 166, Project B06 to M.H. and A.-L.S., FOR 3004 SYNABS P1 to M.H.) and by the Interdisciplinary Clinical Research Center (IZKF) Würzburg (Z-3/69 to M.M.P., N-229 to M.H. and A.-L.S.). A.M. is funded by the University of Leipzig Clinician Scientist Program.","doi":"10.3390/ijms24032128","pmid":1,"author":[{"last_name":"Mrestani","first_name":"Achmed","full_name":"Mrestani, Achmed"},{"full_name":"Lichter, Katharina","id":"39302e62-fcfc-11ec-8196-8b01447dbd3d","orcid":"0000-0002-1485-0351","first_name":"Katharina","last_name":"Lichter"},{"full_name":"Sirén, Anna Leena","first_name":"Anna Leena","last_name":"Sirén"},{"full_name":"Heckmann, Manfred","first_name":"Manfred","last_name":"Heckmann"},{"last_name":"Paul","first_name":"Mila M.","full_name":"Paul, Mila M."},{"last_name":"Pauli","first_name":"Martin","full_name":"Pauli, Martin"}],"month":"01","issue":"3","volume":24,"publication_status":"published","file_date_updated":"2023-02-20T07:09:27Z","year":"2023","article_type":"original","citation":{"mla":"Mrestani, Achmed, et al. “Single-Molecule Localization Microscopy of Presynaptic Active Zones in Drosophila Melanogaster after Rapid Cryofixation.” <i>International Journal of Molecular Sciences</i>, vol. 24, no. 3, 2128, MDPI, 2023, doi:<a href=\"https://doi.org/10.3390/ijms24032128\">10.3390/ijms24032128</a>.","short":"A. Mrestani, K. Lichter, A.L. Sirén, M. Heckmann, M.M. Paul, M. Pauli, International Journal of Molecular Sciences 24 (2023).","apa":"Mrestani, A., Lichter, K., Sirén, A. L., Heckmann, M., Paul, M. M., &#38; Pauli, M. (2023). Single-molecule localization microscopy of presynaptic active zones in Drosophila melanogaster after rapid cryofixation. <i>International Journal of Molecular Sciences</i>. MDPI. <a href=\"https://doi.org/10.3390/ijms24032128\">https://doi.org/10.3390/ijms24032128</a>","ista":"Mrestani A, Lichter K, Sirén AL, Heckmann M, Paul MM, Pauli M. 2023. Single-molecule localization microscopy of presynaptic active zones in Drosophila melanogaster after rapid cryofixation. International Journal of Molecular Sciences. 24(3), 2128.","ama":"Mrestani A, Lichter K, Sirén AL, Heckmann M, Paul MM, Pauli M. Single-molecule localization microscopy of presynaptic active zones in Drosophila melanogaster after rapid cryofixation. <i>International Journal of Molecular Sciences</i>. 2023;24(3). doi:<a href=\"https://doi.org/10.3390/ijms24032128\">10.3390/ijms24032128</a>","ieee":"A. Mrestani, K. Lichter, A. L. Sirén, M. Heckmann, M. M. Paul, and M. Pauli, “Single-molecule localization microscopy of presynaptic active zones in Drosophila melanogaster after rapid cryofixation,” <i>International Journal of Molecular Sciences</i>, vol. 24, no. 3. MDPI, 2023.","chicago":"Mrestani, Achmed, Katharina Lichter, Anna Leena Sirén, Manfred Heckmann, Mila M. Paul, and Martin Pauli. “Single-Molecule Localization Microscopy of Presynaptic Active Zones in Drosophila Melanogaster after Rapid Cryofixation.” <i>International Journal of Molecular Sciences</i>. MDPI, 2023. <a href=\"https://doi.org/10.3390/ijms24032128\">https://doi.org/10.3390/ijms24032128</a>."},"language":[{"iso":"eng"}],"abstract":[{"text":"Single-molecule localization microscopy (SMLM) greatly advances structural studies of diverse biological tissues. For example, presynaptic active zone (AZ) nanotopology is resolved in increasing detail. Immunofluorescence imaging of AZ proteins usually relies on epitope preservation using aldehyde-based immunocompetent fixation. Cryofixation techniques, such as high-pressure freezing (HPF) and freeze substitution (FS), are widely used for ultrastructural studies of presynaptic architecture in electron microscopy (EM). HPF/FS demonstrated nearer-to-native preservation of AZ ultrastructure, e.g., by facilitating single filamentous structures. Here, we present a protocol combining the advantages of HPF/FS and direct stochastic optical reconstruction microscopy (dSTORM) to quantify nanotopology of the AZ scaffold protein Bruchpilot (Brp) at neuromuscular junctions (NMJs) of Drosophila melanogaster. Using this standardized model, we tested for preservation of Brp clusters in different FS protocols compared to classical aldehyde fixation. In HPF/FS samples, presynaptic boutons were structurally well preserved with ~22% smaller Brp clusters that allowed quantification of subcluster topology. In summary, we established a standardized near-to-native preparation and immunohistochemistry protocol for SMLM analyses of AZ protein clusters in a defined model synapse. Our protocol could be adapted to study protein arrangements at single-molecule resolution in other intact tissue preparations.","lang":"eng"}],"has_accepted_license":"1","external_id":{"isi":["000930324700001"],"pmid":["36768451"]},"status":"public","scopus_import":"1","date_created":"2023-02-19T23:00:56Z","publication":"International Journal of Molecular Sciences","oa_version":"Published Version","type":"journal_article","date_updated":"2025-04-23T08:48:27Z","ddc":["570"],"intvolume":"        24"},{"date_updated":"2025-06-25T05:56:45Z","intvolume":"      2633","OA_place":"repository","OA_type":"green","abstract":[{"lang":"eng","text":"Here we describe the in vivo DNA assembly approach, where molecular cloning procedures are performed using an E. coli recA-independent recombination pathway, which assembles linear fragments of DNA with short homologous termini. This pathway is present in all standard laboratory E. coli strains and, by bypassing the need for in vitro DNA assembly, allows simplified molecular cloning to be performed without the plasmid instability issues associated with specialized recombination-cloning bacterial strains. The methodology requires specific primer design and can perform all standard plasmid modifications (insertions, deletions, mutagenesis, and sub-cloning) in a rapid, simple, and cost-efficient manner, as it does not require commercial kits or specialized bacterial strains. Additionally, this approach can be used to perform complex procedures such as multiple modifications to a plasmid, as up to 6 linear fragments can be assembled in vivo by this recombination pathway. Procedures generally require less than 3 h, involving PCR amplification, DpnI digestion of template DNA, and transformation, upon which circular plasmids are assembled. In this chapter we describe the requirements, procedure, and potential pitfalls when using this technique, as well as protocol variations to overcome the most common issues."}],"external_id":{"pmid":["36853454"]},"status":"public","date_created":"2023-03-12T23:01:02Z","scopus_import":"1","oa_version":"Submitted Version","publication":"DNA Manipulation and Analysis","type":"book_chapter","main_file_link":[{"open_access":"1","url":"https://zaguan.unizar.es/record/125930/files/texto_completo.pdf"}],"citation":{"chicago":"Arroyo-Urea, Sandra, Jake Watson, and Javier García-Nafría. “Molecular Cloning Using In Vivo DNA Assembly.” In <i>DNA Manipulation and Analysis</i>, edited by Garry Scarlett, 2633:33–44. MIMB. New York, NY, United States: Springer Nature, 2023. <a href=\"https://doi.org/10.1007/978-1-0716-3004-4_3\">https://doi.org/10.1007/978-1-0716-3004-4_3</a>.","ieee":"S. Arroyo-Urea, J. Watson, and J. García-Nafría, “Molecular Cloning Using In Vivo DNA Assembly,” in <i>DNA Manipulation and Analysis</i>, vol. 2633, G. Scarlett, Ed. New York, NY, United States: Springer Nature, 2023, pp. 33–44.","ista":"Arroyo-Urea S, Watson J, García-Nafría J. 2023.Molecular Cloning Using In Vivo DNA Assembly. In: DNA Manipulation and Analysis. Methods in Molecular Biology, vol. 2633, 33–44.","ama":"Arroyo-Urea S, Watson J, García-Nafría J. Molecular Cloning Using In Vivo DNA Assembly. In: Scarlett G, ed. <i>DNA Manipulation and Analysis</i>. Vol 2633. MIMB. New York, NY, United States: Springer Nature; 2023:33-44. doi:<a href=\"https://doi.org/10.1007/978-1-0716-3004-4_3\">10.1007/978-1-0716-3004-4_3</a>","apa":"Arroyo-Urea, S., Watson, J., &#38; García-Nafría, J. (2023). Molecular Cloning Using In Vivo DNA Assembly. In G. Scarlett (Ed.), <i>DNA Manipulation and Analysis</i> (Vol. 2633, pp. 33–44). New York, NY, United States: Springer Nature. <a href=\"https://doi.org/10.1007/978-1-0716-3004-4_3\">https://doi.org/10.1007/978-1-0716-3004-4_3</a>","short":"S. Arroyo-Urea, J. Watson, J. García-Nafría, in:, G. Scarlett (Ed.), DNA Manipulation and Analysis, Springer Nature, New York, NY, United States, 2023, pp. 33–44.","mla":"Arroyo-Urea, Sandra, et al. “Molecular Cloning Using In Vivo DNA Assembly.” <i>DNA Manipulation and Analysis</i>, edited by Garry Scarlett, vol. 2633, Springer Nature, 2023, pp. 33–44, doi:<a href=\"https://doi.org/10.1007/978-1-0716-3004-4_3\">10.1007/978-1-0716-3004-4_3</a>."},"language":[{"iso":"eng"}],"publication_status":"published","year":"2023","series_title":"MIMB","month":"03","volume":2633,"author":[{"full_name":"Arroyo-Urea, Sandra","first_name":"Sandra","last_name":"Arroyo-Urea"},{"full_name":"Watson, Jake","id":"63836096-4690-11EA-BD4E-32803DDC885E","orcid":"0000-0002-8698-3823","first_name":"Jake","last_name":"Watson"},{"full_name":"García-Nafría, Javier","first_name":"Javier","last_name":"García-Nafría"}],"alternative_title":["Methods in Molecular Biology"],"page":"33-44","pmid":1,"publisher":"Springer Nature","place":"New York, NY, United States","doi":"10.1007/978-1-0716-3004-4_3","quality_controlled":"1","_id":"12720","date_published":"2023-03-01T00:00:00Z","oa":1,"title":"Molecular Cloning Using In Vivo DNA Assembly","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","department":[{"_id":"PeJo"}],"day":"01","editor":[{"last_name":"Scarlett","first_name":"Garry","full_name":"Scarlett, Garry"}],"publication_identifier":{"issn":["1064-3745"],"eisbn":["978-1-0716-3004-4"],"eissn":["1940-6029"],"isbn":["978-1-0716-3003-7"]},"article_processing_charge":"No"},{"year":"2023","file_date_updated":"2023-03-27T06:51:09Z","publication_status":"published","volume":18,"issue":"3 March","month":"03","author":[{"full_name":"Rothman, Jason Seth","last_name":"Rothman","first_name":"Jason Seth"},{"id":"4305C450-F248-11E8-B48F-1D18A9856A87","full_name":"Borges Merjane, Carolina","last_name":"Borges Merjane","first_name":"Carolina","orcid":"0000-0003-0005-401X"},{"full_name":"Holderith, Noemi","last_name":"Holderith","first_name":"Noemi"},{"full_name":"Jonas, Peter M","id":"353C1B58-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0001-5001-4804","first_name":"Peter M","last_name":"Jonas"},{"last_name":"Angus Silver","first_name":"R.","full_name":"Angus Silver, R."}],"acknowledged_ssus":[{"_id":"EM-Fac"}],"pmid":1,"intvolume":"        18","ddc":["570"],"date_updated":"2025-04-23T08:50:50Z","project":[{"call_identifier":"H2020","name":"Biophysics and circuit function of a giant cortical glutamatergic synapse","_id":"25B7EB9E-B435-11E9-9278-68D0E5697425","grant_number":"692692"},{"grant_number":"Z00312","_id":"25C5A090-B435-11E9-9278-68D0E5697425","name":"Synaptic communication in neuronal microcircuits","call_identifier":"FWF"},{"grant_number":"V00739","call_identifier":"FWF","_id":"2696E7FE-B435-11E9-9278-68D0E5697425","name":"Structural plasticity at mossy fiber-CA3 synapses"}],"type":"journal_article","scopus_import":"1","oa_version":"Published Version","publication":"PLoS ONE","date_created":"2023-03-26T22:01:07Z","external_id":{"isi":["001024737400001"],"pmid":["36930689"]},"has_accepted_license":"1","status":"public","abstract":[{"text":"Stereological methods for estimating the 3D particle size and density from 2D projections are essential to many research fields. These methods are, however, prone to errors arising from undetected particle profiles due to sectioning and limited resolution, known as ‘lost caps’. A potential solution developed by Keiding, Jensen, and Ranek in 1972, which we refer to as the Keiding model, accounts for lost caps by quantifying the smallest detectable profile in terms of its limiting ‘cap angle’ (ϕ), a size-independent measure of a particle’s distance from the section surface. However, this simple solution has not been widely adopted nor tested. Rather, model-independent design-based stereological methods, which do not explicitly account for lost caps, have come to the fore. Here, we provide the first experimental validation of the Keiding model by comparing the size and density of particles estimated from 2D projections with direct measurement from 3D EM reconstructions of the same tissue. We applied the Keiding model to estimate the size and density of somata, nuclei and vesicles in the cerebellum of mice and rats, where high packing density can be problematic for design-based methods. Our analysis reveals a Gaussian distribution for ϕ rather than a single value. Nevertheless, curve fits of the Keiding model to the 2D diameter distribution accurately estimate the mean ϕ and 3D diameter distribution. While systematic testing using simulations revealed an upper limit to determining ϕ, our analysis shows that estimated ϕ can be used to determine the 3D particle density from the 2D density under a wide range of conditions, and this method is potentially more accurate than minimum-size-based lost-cap corrections and disector methods. Our results show the Keiding model provides an efficient means of accurately estimating the size and density of particles from 2D projections even under conditions of a high density.","lang":"eng"}],"language":[{"iso":"eng"}],"citation":{"short":"J.S. Rothman, C. Borges Merjane, N. Holderith, P.M. Jonas, R. Angus Silver, PLoS ONE 18 (2023).","mla":"Rothman, Jason Seth, et al. “Validation of a Stereological Method for Estimating Particle Size and Density from 2D Projections with High Accuracy.” <i>PLoS ONE</i>, vol. 18, no. 3 March, e0277148, Public Library of Science, 2023, doi:<a href=\"https://doi.org/10.1371/journal.pone.0277148\">10.1371/journal.pone.0277148</a>.","ama":"Rothman JS, Borges Merjane C, Holderith N, Jonas PM, Angus Silver R. Validation of a stereological method for estimating particle size and density from 2D projections with high accuracy. <i>PLoS ONE</i>. 2023;18(3 March). doi:<a href=\"https://doi.org/10.1371/journal.pone.0277148\">10.1371/journal.pone.0277148</a>","ieee":"J. S. Rothman, C. Borges Merjane, N. Holderith, P. M. Jonas, and R. Angus Silver, “Validation of a stereological method for estimating particle size and density from 2D projections with high accuracy,” <i>PLoS ONE</i>, vol. 18, no. 3 March. Public Library of Science, 2023.","ista":"Rothman JS, Borges Merjane C, Holderith N, Jonas PM, Angus Silver R. 2023. Validation of a stereological method for estimating particle size and density from 2D projections with high accuracy. PLoS ONE. 18(3 March), e0277148.","apa":"Rothman, J. S., Borges Merjane, C., Holderith, N., Jonas, P. M., &#38; Angus Silver, R. (2023). Validation of a stereological method for estimating particle size and density from 2D projections with high accuracy. <i>PLoS ONE</i>. Public Library of Science. <a href=\"https://doi.org/10.1371/journal.pone.0277148\">https://doi.org/10.1371/journal.pone.0277148</a>","chicago":"Rothman, Jason Seth, Carolina Borges Merjane, Noemi Holderith, Peter M Jonas, and R. Angus Silver. “Validation of a Stereological Method for Estimating Particle Size and Density from 2D Projections with High Accuracy.” <i>PLoS ONE</i>. Public Library of Science, 2023. <a href=\"https://doi.org/10.1371/journal.pone.0277148\">https://doi.org/10.1371/journal.pone.0277148</a>."},"ec_funded":1,"article_type":"original","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","title":"Validation of a stereological method for estimating particle size and density from 2D projections with high accuracy","oa":1,"day":"17","department":[{"_id":"PeJo"}],"article_processing_charge":"No","tmp":{"short":"CC BY (4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)"},"publication_identifier":{"eissn":["1932-6203"]},"doi":"10.1371/journal.pone.0277148","isi":1,"file":[{"creator":"dernst","relation":"main_file","access_level":"open_access","date_created":"2023-03-27T06:51:09Z","content_type":"application/pdf","file_size":7290413,"checksum":"2380331ec27cc87808826fc64419ac1c","success":1,"file_name":"2023_PLoSOne_Rothman.pdf","file_id":"12770","date_updated":"2023-03-27T06:51:09Z"}],"acknowledgement":"We thank the IST Austria Electron Microscopy Facility for technical support, and Diccon Coyle, Andrea Lőrincz and Zoltan Nusser for their helpful comments and discussions.\r\nFunding for JSR and RAS was from the Wellcome Trust (203048; 224499; https://\r\nwellcome.org/). RAS is in receipt of a Wellcome Trust Principal Research Fellowship (224499).\r\nFunding for CBM and PJ was from Fond zur Förderung der Wissenschaftlichen Forschung (V\r\n739-B27 Elise-Richter Programme to CBM, Z 312-B27 Wittgenstein Award to PJ; \r\nhttps://www.fwf.ac.at). PJ received funding from the European Research Council (ERC; https://erc.europa.eu) under the European Union’s Horizon 2020 research and innovation programme (grant agreement no. 692692). NH was supported by a European\r\nResearch Council Advanced Grant (ERC-AG787157).","publisher":"Public Library of Science","_id":"12759","date_published":"2023-03-17T00:00:00Z","quality_controlled":"1","article_number":"e0277148"},{"type":"journal_article","date_created":"2023-04-02T22:01:09Z","oa_version":"Published Version","scopus_import":"1","publication":"Nature Communications","external_id":{"isi":["001066658700003"]},"status":"public","has_accepted_license":"1","abstract":[{"text":"AMPA glutamate receptors (AMPARs) mediate excitatory neurotransmission throughout the brain. Their signalling is uniquely diversified by brain region-specific auxiliary subunits, providing an opportunity for the development of selective therapeutics. AMPARs associated with TARP γ8 are enriched in the hippocampus, and are targets of emerging anti-epileptic drugs. To understand their therapeutic activity, we determined cryo-EM structures of the GluA1/2-γ8 receptor associated with three potent, chemically diverse ligands. We find that despite sharing a lipid-exposed and water-accessible binding pocket, drug action is differentially affected by binding-site mutants. Together with patch-clamp recordings and MD simulations we also demonstrate that ligand-triggered reorganisation of the AMPAR-TARP interface contributes to modulation. Unexpectedly, one ligand (JNJ-61432059) acts bifunctionally, negatively affecting GluA1 but exerting positive modulatory action on GluA2-containing AMPARs, in a TARP stoichiometry-dependent manner. These results further illuminate the action of TARPs, demonstrate the sensitive balance between positive and negative modulatory action, and provide a mechanistic platform for development of both positive and negative selective AMPAR modulators.","lang":"eng"}],"language":[{"iso":"eng"}],"citation":{"chicago":"Zhang, Danyang, Remigijus Lape, Saher A. Shaikh, Bianka K. Kohegyi, Jake Watson, Ondrej Cais, Terunaga Nakagawa, and Ingo H. Greger. “Modulatory Mechanisms of TARP Γ8-Selective AMPA Receptor Therapeutics.” <i>Nature Communications</i>. Springer Nature, 2023. <a href=\"https://doi.org/10.1038/s41467-023-37259-5\">https://doi.org/10.1038/s41467-023-37259-5</a>.","ama":"Zhang D, Lape R, Shaikh SA, et al. Modulatory mechanisms of TARP γ8-selective AMPA receptor therapeutics. <i>Nature Communications</i>. 2023;14. doi:<a href=\"https://doi.org/10.1038/s41467-023-37259-5\">10.1038/s41467-023-37259-5</a>","ista":"Zhang D, Lape R, Shaikh SA, Kohegyi BK, Watson J, Cais O, Nakagawa T, Greger IH. 2023. Modulatory mechanisms of TARP γ8-selective AMPA receptor therapeutics. Nature Communications. 14, 1659.","ieee":"D. Zhang <i>et al.</i>, “Modulatory mechanisms of TARP γ8-selective AMPA receptor therapeutics,” <i>Nature Communications</i>, vol. 14. Springer Nature, 2023.","apa":"Zhang, D., Lape, R., Shaikh, S. A., Kohegyi, B. K., Watson, J., Cais, O., … Greger, I. H. (2023). Modulatory mechanisms of TARP γ8-selective AMPA receptor therapeutics. <i>Nature Communications</i>. Springer Nature. <a href=\"https://doi.org/10.1038/s41467-023-37259-5\">https://doi.org/10.1038/s41467-023-37259-5</a>","short":"D. Zhang, R. Lape, S.A. Shaikh, B.K. Kohegyi, J. Watson, O. Cais, T. Nakagawa, I.H. Greger, Nature Communications 14 (2023).","mla":"Zhang, Danyang, et al. “Modulatory Mechanisms of TARP Γ8-Selective AMPA Receptor Therapeutics.” <i>Nature Communications</i>, vol. 14, 1659, Springer Nature, 2023, doi:<a href=\"https://doi.org/10.1038/s41467-023-37259-5\">10.1038/s41467-023-37259-5</a>."},"article_type":"original","intvolume":"        14","ddc":["570"],"date_updated":"2023-12-13T11:15:58Z","author":[{"first_name":"Danyang","last_name":"Zhang","full_name":"Zhang, Danyang"},{"first_name":"Remigijus","last_name":"Lape","full_name":"Lape, Remigijus"},{"first_name":"Saher A.","last_name":"Shaikh","full_name":"Shaikh, Saher A."},{"full_name":"Kohegyi, Bianka K.","first_name":"Bianka K.","last_name":"Kohegyi"},{"full_name":"Watson, Jake","id":"63836096-4690-11EA-BD4E-32803DDC885E","last_name":"Watson","orcid":"0000-0002-8698-3823","first_name":"Jake"},{"full_name":"Cais, Ondrej","first_name":"Ondrej","last_name":"Cais"},{"last_name":"Nakagawa","first_name":"Terunaga","full_name":"Nakagawa, Terunaga"},{"first_name":"Ingo H.","last_name":"Greger","full_name":"Greger, Ingo H."}],"year":"2023","file_date_updated":"2023-04-03T06:38:56Z","publication_status":"published","volume":14,"month":"03","_id":"12786","date_published":"2023-03-25T00:00:00Z","quality_controlled":"1","article_number":"1659","file":[{"date_created":"2023-04-03T06:38:56Z","content_type":"application/pdf","relation":"main_file","creator":"dernst","access_level":"open_access","checksum":"0a97b31191432dae5853bbb5ccb7698d","success":1,"date_updated":"2023-04-03T06:38:56Z","file_name":"2023_NatureComm_Zhang.pdf","file_id":"12797","file_size":2613996}],"acknowledgement":"We thank James Krieger for generating the ‘proDy’ interaction maps in Fig. 5B and S7C, and Jan-Niklas Dohrke for critically reading the manuscript. We thank members of the Greger lab for insightful comments during this study. We acknowledge Trevor Rutherford for confirming ligand integrity by NMR. We are also grateful to LMB scientific computing and the EM facility for their support. This research was funded in part by the Wellcome Trust (223194/Z/21/Z) to I.H.G. For the purpose of Open Access, the MRC Laboratory of Molecular Biology has applied a CC BY public copyright licence to any Author Accepted Manuscript (AAM) version arising from this submission. Further funding came from the Medical Research Council (MRU105174197) to I.H.G, and NIH grant (R56/R01MH123474) to T.N.","doi":"10.1038/s41467-023-37259-5","isi":1,"publisher":"Springer Nature","article_processing_charge":"No","tmp":{"short":"CC BY (4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)"},"publication_identifier":{"eissn":["2041-1723"]},"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","title":"Modulatory mechanisms of TARP γ8-selective AMPA receptor therapeutics","oa":1,"day":"25","department":[{"_id":"PeJo"}]},{"publisher":"Institute of Science and Technology 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thank Jakob Vorlaufer, Nathalie Agudelo-Dueñas, Wiebke Jahr, Andreas Wartak for microscope maintenance and troubleshooting, Caroline Kreuzinger, Anna Freeman, and Irene Erber for technical assistance and Matthias Tomschik for support with obtaining human samples. We gratefully acknowledge Eder Miguel for setting up webKnossos and Marek Šuplata for computational support and hardware control. We are grateful to Ryuichi Shigemoto and Bernd Bickel for generous support, and Michael Sixt and Scott Boyd (Stanford University) for discussions and critical reading of the manuscript. PSD95-HaloTag mice were kindly provided by Seth Grant (University of Edinburgh). We acknowledge expert support by IST Austria’s scientific computing, imaging and optics, preclinical, and lab support facilities, and by the Library and Miba machine shop.\r\nWe gratefully acknowledge funding by the following sources: \r\nAustrian Science Fund (FWF) grant I3600-B27 (JGD)\r\nAustrian Science Fund (FWF) grant DK W1232 (JGD, JMM)\r\nAustrian Science Fund (FWF) grant Z 312-B27, Wittgenstein award (PJ)\r\nAustrian Science Funds (FWF) projects I4685-B, I6565-B (SYNABS) and DOC 33-B27 (RH)\r\nGesellschaft für Forschungsförderung NÖ (NFB) grant LSC18-022 (JGD)\r\nEuropean Union’s Horizon 2020 research and innovation programme, European Research Council (ERC) grant 715508 – REVERSEAUTISM (GN)\r\nEuropean Union’s Horizon 2020 research and innovation programme, European Research Council (ERC) grant 692692 – GIANTSYN (PJ)\r\nMarie Skłodowska-Curie Actions Fellowship GA no. 665385 under the EU Horizon 2020 program (JMM, JL)\r\nMarie Skłodowska-Curie Actions Individual Fellowship 101026635 under the EU Horizon 2020 program (JFW)","doi":"10.15479/AT:ISTA:13126","date_published":"2023-08-04T00:00:00Z","_id":"13126","department":[{"_id":"JoDa"},{"_id":"SaSi"},{"_id":"GaNo"},{"_id":"PeJo"},{"_id":"Bio"},{"_id":"RySh"}],"day":"04","title":"Research data for the publication \"Imaging brain tissue architecture across millimeter to nanometer scales\"","oa":1,"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","license":"https://creativecommons.org/licenses/by-nc-sa/4.0/","tmp":{"short":"CC BY-NC-SA (4.0)","legal_code_url":"https://creativecommons.org/licenses/by-nc-sa/4.0/legalcode","image":"/images/cc_by_nc_sa.png","name":"Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)"},"article_processing_charge":"No","project":[{"grant_number":"I03600","call_identifier":"FWF","_id":"265CB4D0-B435-11E9-9278-68D0E5697425","name":"Optical control of synaptic function via adhesion molecules"},{"call_identifier":"FWF","_id":"26AA4EF2-B435-11E9-9278-68D0E5697425","name":"Molecular Drug Targets","grant_number":"W1232-B24"},{"name":"Synaptic communication in neuronal microcircuits","_id":"25C5A090-B435-11E9-9278-68D0E5697425","call_identifier":"FWF","grant_number":"Z00312"},{"grant_number":"LS18-022","name":"High content imaging to decode human immune cell interactions in health and allergic disease","_id":"23889792-32DE-11EA-91FC-C7463DDC885E"},{"call_identifier":"H2020","_id":"25444568-B435-11E9-9278-68D0E5697425","name":"Probing the Reversibility of Autism Spectrum Disorders by Employing in vivo and in vitro Models","grant_number":"715508"},{"name":"Biophysics and circuit function of a giant cortical glutamatergic synapse","call_identifier":"H2020","_id":"25B7EB9E-B435-11E9-9278-68D0E5697425","grant_number":"692692"},{"grant_number":"665385","_id":"2564DBCA-B435-11E9-9278-68D0E5697425","call_identifier":"H2020","name":"International IST Doctoral Program"},{"grant_number":"101026635","_id":"fc2be41b-9c52-11eb-aca3-faa90aa144e9","name":"Synaptic computations of the hippocampal CA3 circuitry","call_identifier":"H2020"}],"ddc":["610"],"date_updated":"2026-04-14T08:34:35Z","citation":{"chicago":"Danzl, Johann G. “Research Data for the Publication ‘Imaging Brain Tissue Architecture across Millimeter to Nanometer Scales.’” Institute of Science and Technology Austria, 2023. <a href=\"https://doi.org/10.15479/AT:ISTA:13126\">https://doi.org/10.15479/AT:ISTA:13126</a>.","mla":"Danzl, Johann G. <i>Research Data for the Publication “Imaging Brain Tissue Architecture across Millimeter to Nanometer Scales.”</i> Institute of Science and Technology Austria, 2023, doi:<a href=\"https://doi.org/10.15479/AT:ISTA:13126\">10.15479/AT:ISTA:13126</a>.","short":"J.G. Danzl, (2023).","apa":"Danzl, J. G. (2023). Research data for the publication “Imaging brain tissue architecture across millimeter to nanometer scales.” Institute of Science and Technology Austria. <a href=\"https://doi.org/10.15479/AT:ISTA:13126\">https://doi.org/10.15479/AT:ISTA:13126</a>","ama":"Danzl JG. Research data for the publication “Imaging brain tissue architecture across millimeter to nanometer scales.” 2023. doi:<a href=\"https://doi.org/10.15479/AT:ISTA:13126\">10.15479/AT:ISTA:13126</a>","ista":"Danzl JG. 2023. Research data for the publication ‘Imaging brain tissue architecture across millimeter to nanometer scales’, Institute of Science and Technology Austria, <a href=\"https://doi.org/10.15479/AT:ISTA:13126\">10.15479/AT:ISTA:13126</a>.","ieee":"J. G. Danzl, “Research data for the publication ‘Imaging brain tissue architecture across millimeter to nanometer scales.’” Institute of Science and Technology Austria, 2023."},"ec_funded":1,"status":"public","has_accepted_license":"1","abstract":[{"text":"Mapping the complex and dense arrangement of cells and their connectivity in brain tissue demands nanoscale spatial resolution imaging. Super-resolution optical microscopy excels at visualizing specific molecules and individual cells but fails to provide tissue context. Here, we developed Comprehensive Analysis of Tissues across Scales (CATS), a technology to densely map brain tissue architecture from millimeter regional to nanometer synaptic scales in diverse chemically fixed brain preparations, including rodent and human. CATS uses fixation-compatible extracellular labeling and optical imaging, including stimulated emission depletion or expansion microscopy, to comprehensively delineate cellular structures. It enables three-dimensional reconstruction of single synapses and mapping of synaptic connectivity by identification and analysis of putative synaptic cleft regions. Applying CATS to the mouse hippocampal mossy fiber circuitry, we reconstructed and quantified the synaptic input and output structure of identified neurons. We furthermore demonstrate applicability to clinically derived human tissue samples, including formalin-fixed paraffin-embedded routine diagnostic specimens, for visualizing the cellular architecture of brain tissue in health and disease.","lang":"eng"}],"corr_author":"1","type":"research_data","date_created":"2023-06-07T07:15:12Z","oa_version":"Published Version","month":"08","related_material":{"link":[{"relation":"research_data","description":"Original data for Fig. 5d, Fig. 5d (N2V) and Fig. 5f-i, provided via an external link due to the large size (>10GB) of the datasets. ","url":"https://pub.ista.ac.at/group_danzl/data/CATS/"}],"record":[{"id":"14257","status":"public","relation":"used_in_publication"}]},"contributor":[{"id":"443DB6DE-F248-11E8-B48F-1D18A9856A87","last_name":"Michalska","first_name":"Julia M"},{"id":"46E28B80-F248-11E8-B48F-1D18A9856A87","last_name":"Lyudchik","first_name":"Julia"},{"last_name":"Velicky","orcid":"0000-0002-2340-7431","first_name":"Philipp","id":"39BDC62C-F248-11E8-B48F-1D18A9856A87"},{"last_name":"Stefanickova","first_name":"Hana","id":"ee3cb6ca-ec98-11ea-ae11-ff703e2254ed"},{"last_name":"Watson","first_name":"Jake","orcid":"0000-0002-8698-3823","id":"63836096-4690-11EA-BD4E-32803DDC885E"},{"last_name":"Cenameri","first_name":"Alban","id":"9ac8f577-2357-11eb-997a-e566c5550886"},{"last_name":"Sommer","first_name":"Christoph M","orcid":"0000-0003-1216-9105","id":"4DF26D8C-F248-11E8-B48F-1D18A9856A87"},{"last_name":"Amberg","first_name":"Nicole","orcid":"0000-0002-3183-8207","id":"4CD6AAC6-F248-11E8-B48F-1D18A9856A87"},{"last_name":"Venturino","orcid":"0000-0003-2356-9403","first_name":"Alessandro","id":"41CB84B2-F248-11E8-B48F-1D18A9856A87"},{"first_name":"Karl","last_name":"Roessler"},{"last_name":"Czech","first_name":"Thomas"},{"last_name":"Höftberger","first_name":"Romana"},{"last_name":"Siegert","orcid":"0000-0001-8635-0877","first_name":"Sandra","id":"36ACD32E-F248-11E8-B48F-1D18A9856A87"},{"id":"3E57A680-F248-11E8-B48F-1D18A9856A87","first_name":"Gaia","orcid":"0000-0002-7673-7178","last_name":"Novarino"},{"last_name":"Jonas","first_name":"Peter M","orcid":"0000-0001-5001-4804","id":"353C1B58-F248-11E8-B48F-1D18A9856A87"}],"file_date_updated":"2023-08-04T13:19:47Z","year":"2023","author":[{"id":"42EFD3B6-F248-11E8-B48F-1D18A9856A87","full_name":"Danzl, Johann G","first_name":"Johann G","orcid":"0000-0001-8559-3973","last_name":"Danzl"}],"acknowledged_ssus":[{"_id":"ScienComp"},{"_id":"Bio"},{"_id":"PreCl"},{"_id":"LifeSc"},{"_id":"M-Shop"},{"_id":"E-Lib"}]},{"department":[{"_id":"PeJo"},{"_id":"GaNo"},{"_id":"BeBi"},{"_id":"JoDa"},{"_id":"Bio"}],"day":"01","oa":1,"title":"Dense 4D nanoscale reconstruction of living brain tissue","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","publication_identifier":{"issn":["1548-7091"],"eissn":["1548-7105"]},"tmp":{"short":"CC BY (4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)"},"article_processing_charge":"Yes (in subscription journal)","publisher":"Springer Nature","isi":1,"doi":"10.1038/s41592-023-01936-6","file":[{"file_id":"19088","file_name":"2023_NatureMethods_Velicky.pdf","date_updated":"2025-02-26T08:01:57Z","success":1,"checksum":"a68e845780a82ea36d0d4d3212a87c10","file_size":14103039,"content_type":"application/pdf","date_created":"2025-02-26T08:01:57Z","access_level":"open_access","creator":"dernst","relation":"main_file"}],"acknowledgement":"We thank J. Vorlaufer, N. Agudelo and A. Wartak for microscope maintenance and troubleshooting, C. Kreuzinger and A. Freeman for technical assistance, M. Šuplata for hardware control support and M. Cunha dos Santos for initial exploration of software. We\r\nthank P. Henderson for advice on deep-learning training and M. Sixt, S. Boyd and T. Weiss for discussions and critical reading of the manuscript. L. Lavis (Janelia Research Campus) generously provided the JF585-HaloTag ligand. We acknowledge expert support by IST\r\nAustria’s scientific computing, imaging and optics, preclinical, library and laboratory support facilities and by the Miba machine shop. We gratefully acknowledge funding by the following sources: Austrian Science Fund (F.W.F.) grant no. I3600-B27 (J.G.D.), grant no. DK W1232\r\n(J.G.D. and J.M.M.) and grant no. Z 312-B27, Wittgenstein award (P.J.); the Gesellschaft für Forschungsförderung NÖ grant no. LSC18-022 (J.G.D.); an ISTA Interdisciplinary project grant (J.G.D. and B.B.); the European Union’s Horizon 2020 research and innovation programme,\r\nMarie-Skłodowska Curie grant 665385 (J.M.M. and J.L.); the European Union’s Horizon 2020 research and innovation programme, European Research Council grant no. 715767, MATERIALIZABLE (B.B.); grant no. 715508, REVERSEAUTISM (G.N.); grant no. 695568, SYNNOVATE (S.G.N.G.); and grant no. 692692, GIANTSYN (P.J.); the Simons\r\nFoundation Autism Research Initiative grant no. 529085 (S.G.N.G.); the Wellcome Trust Technology Development grant no. 202932 (S.G.N.G.); the Marie Skłodowska-Curie Actions Individual Fellowship no. 101026635 under the EU Horizon 2020 program (J.F.W.);\r\nthe Human Frontier Science Program postdoctoral fellowship LT000557/2018 (W.J.); and the National Science Foundation grant no. IIS-1835231 (H.P.) and NCS-FO-2124179 (H.P.).","_id":"13267","date_published":"2023-08-01T00:00:00Z","quality_controlled":"1","month":"08","related_material":{"record":[{"id":"12817","status":"public","relation":"research_data"},{"id":"14770","status":"public","relation":"shorter_version"},{"id":"18674","status":"public","relation":"dissertation_contains"},{"relation":"earlier_version","id":"11943","status":"public"}],"link":[{"url":"https://github.com/danzllab/LIONESS","relation":"software"}]},"volume":20,"publication_status":"published","file_date_updated":"2025-02-26T08:01:57Z","year":"2023","page":"1256-1265","pmid":1,"acknowledged_ssus":[{"_id":"ScienComp"},{"_id":"Bio"},{"_id":"PreCl"},{"_id":"E-Lib"},{"_id":"LifeSc"},{"_id":"M-Shop"}],"author":[{"full_name":"Velicky, Philipp","id":"39BDC62C-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0002-2340-7431","first_name":"Philipp","last_name":"Velicky"},{"id":"3FB91342-F248-11E8-B48F-1D18A9856A87","full_name":"Miguel Villalba, Eder","last_name":"Miguel Villalba","first_name":"Eder","orcid":"0000-0001-5665-0430"},{"last_name":"Michalska","first_name":"Julia M","orcid":"0000-0003-3862-1235","id":"443DB6DE-F248-11E8-B48F-1D18A9856A87","full_name":"Michalska, Julia M"},{"last_name":"Lyudchik","first_name":"Julia","id":"46E28B80-F248-11E8-B48F-1D18A9856A87","full_name":"Lyudchik, Julia"},{"full_name":"Wei, Donglai","last_name":"Wei","first_name":"Donglai"},{"full_name":"Lin, Zudi","last_name":"Lin","first_name":"Zudi"},{"id":"63836096-4690-11EA-BD4E-32803DDC885E","full_name":"Watson, Jake","last_name":"Watson","first_name":"Jake","orcid":"0000-0002-8698-3823"},{"full_name":"Troidl, Jakob","first_name":"Jakob","last_name":"Troidl"},{"last_name":"Beyer","first_name":"Johanna","full_name":"Beyer, Johanna"},{"first_name":"Yoav","last_name":"Ben Simon","full_name":"Ben Simon, Yoav","id":"43DF3136-F248-11E8-B48F-1D18A9856A87"},{"id":"4DF26D8C-F248-11E8-B48F-1D18A9856A87","full_name":"Sommer, Christoph M","last_name":"Sommer","first_name":"Christoph M","orcid":"0000-0003-1216-9105"},{"orcid":"0000-0003-0201-2315","first_name":"Wiebke","last_name":"Jahr","full_name":"Jahr, Wiebke","id":"425C1CE8-F248-11E8-B48F-1D18A9856A87"},{"id":"9ac8f577-2357-11eb-997a-e566c5550886","full_name":"Cenameri, Alban","first_name":"Alban","last_name":"Cenameri"},{"full_name":"Broichhagen, Johannes","last_name":"Broichhagen","first_name":"Johannes"},{"last_name":"Grant","first_name":"Seth G.N.","full_name":"Grant, Seth G.N."},{"last_name":"Jonas","orcid":"0000-0001-5001-4804","first_name":"Peter M","full_name":"Jonas, Peter M","id":"353C1B58-F248-11E8-B48F-1D18A9856A87"},{"orcid":"0000-0002-7673-7178","first_name":"Gaia","last_name":"Novarino","full_name":"Novarino, Gaia","id":"3E57A680-F248-11E8-B48F-1D18A9856A87"},{"full_name":"Pfister, Hanspeter","last_name":"Pfister","first_name":"Hanspeter"},{"orcid":"0000-0001-6511-9385","first_name":"Bernd","last_name":"Bickel","full_name":"Bickel, Bernd","id":"49876194-F248-11E8-B48F-1D18A9856A87"},{"first_name":"Johann G","orcid":"0000-0001-8559-3973","last_name":"Danzl","id":"42EFD3B6-F248-11E8-B48F-1D18A9856A87","full_name":"Danzl, Johann G"}],"project":[{"grant_number":"I03600","name":"Optical control of synaptic function via adhesion molecules","_id":"265CB4D0-B435-11E9-9278-68D0E5697425","call_identifier":"FWF"},{"_id":"2548AE96-B435-11E9-9278-68D0E5697425","call_identifier":"FWF","name":"Molecular Drug Targets","grant_number":"W1232"},{"grant_number":"Z00312","call_identifier":"FWF","name":"Synaptic communication in neuronal microcircuits","_id":"25C5A090-B435-11E9-9278-68D0E5697425"},{"_id":"23889792-32DE-11EA-91FC-C7463DDC885E","name":"High content imaging to decode human immune cell interactions in health and allergic disease","grant_number":"LS18-022"},{"grant_number":"665385","name":"International IST Doctoral Program","call_identifier":"H2020","_id":"2564DBCA-B435-11E9-9278-68D0E5697425"},{"grant_number":"715767","name":"MATERIALIZABLE: Intelligent fabrication-oriented Computational Design and Modeling","call_identifier":"H2020","_id":"24F9549A-B435-11E9-9278-68D0E5697425"},{"_id":"25444568-B435-11E9-9278-68D0E5697425","call_identifier":"H2020","name":"Probing the Reversibility of Autism Spectrum Disorders by Employing in vivo and in vitro Models","grant_number":"715508"},{"grant_number":"692692","_id":"25B7EB9E-B435-11E9-9278-68D0E5697425","name":"Biophysics and circuit function of a giant cortical glutamatergic synapse","call_identifier":"H2020"},{"call_identifier":"H2020","name":"Synaptic computations of the hippocampal CA3 circuitry","_id":"fc2be41b-9c52-11eb-aca3-faa90aa144e9","grant_number":"101026635"},{"_id":"2668BFA0-B435-11E9-9278-68D0E5697425","name":"High-speed 3D-nanoscopy to study the role of adhesion during 3D cell migration","grant_number":"LT00057"}],"OA_type":"hybrid","date_updated":"2026-07-06T12:49:46Z","ddc":["570"],"intvolume":"        20","OA_place":"publisher","article_type":"original","ec_funded":1,"citation":{"chicago":"Velicky, Philipp, Eder Miguel Villalba, Julia M Michalska, Julia Lyudchik, Donglai Wei, Zudi Lin, Jake Watson, et al. “Dense 4D Nanoscale Reconstruction of Living Brain Tissue.” <i>Nature Methods</i>. Springer Nature, 2023. <a href=\"https://doi.org/10.1038/s41592-023-01936-6\">https://doi.org/10.1038/s41592-023-01936-6</a>.","apa":"Velicky, P., Miguel Villalba, E., Michalska, J. M., Lyudchik, J., Wei, D., Lin, Z., … Danzl, J. G. (2023). Dense 4D nanoscale reconstruction of living brain tissue. <i>Nature Methods</i>. Springer Nature. <a href=\"https://doi.org/10.1038/s41592-023-01936-6\">https://doi.org/10.1038/s41592-023-01936-6</a>","ama":"Velicky P, Miguel Villalba E, Michalska JM, et al. Dense 4D nanoscale reconstruction of living brain tissue. <i>Nature Methods</i>. 2023;20:1256-1265. doi:<a href=\"https://doi.org/10.1038/s41592-023-01936-6\">10.1038/s41592-023-01936-6</a>","ista":"Velicky P, Miguel Villalba E, Michalska JM, Lyudchik J, Wei D, Lin Z, Watson J, Troidl J, Beyer J, Ben Simon Y, Sommer CM, Jahr W, Cenameri A, Broichhagen J, Grant SGN, Jonas PM, Novarino G, Pfister H, Bickel B, Danzl JG. 2023. Dense 4D nanoscale reconstruction of living brain tissue. Nature Methods. 20, 1256–1265.","ieee":"P. Velicky <i>et al.</i>, “Dense 4D nanoscale reconstruction of living brain tissue,” <i>Nature Methods</i>, vol. 20. Springer Nature, pp. 1256–1265, 2023.","mla":"Velicky, Philipp, et al. “Dense 4D Nanoscale Reconstruction of Living Brain Tissue.” <i>Nature Methods</i>, vol. 20, Springer Nature, 2023, pp. 1256–65, doi:<a href=\"https://doi.org/10.1038/s41592-023-01936-6\">10.1038/s41592-023-01936-6</a>.","short":"P. Velicky, E. Miguel Villalba, J.M. Michalska, J. Lyudchik, D. Wei, Z. Lin, J. Watson, J. Troidl, J. Beyer, Y. Ben Simon, C.M. Sommer, W. Jahr, A. Cenameri, J. Broichhagen, S.G.N. Grant, P.M. Jonas, G. Novarino, H. Pfister, B. Bickel, J.G. Danzl, Nature Methods 20 (2023) 1256–1265."},"language":[{"iso":"eng"}],"abstract":[{"lang":"eng","text":"Three-dimensional (3D) reconstruction of living brain tissue down to an individual synapse level would create opportunities for decoding the dynamics and structure–function relationships of the brain’s complex and dense information processing network; however, this has been hindered by insufficient 3D resolution, inadequate signal-to-noise ratio and prohibitive light burden in optical imaging, whereas electron microscopy is inherently static. Here we solved these challenges by developing an integrated optical/machine-learning technology, LIONESS (live information-optimized nanoscopy enabling saturated segmentation). This leverages optical modifications to stimulated emission depletion microscopy in comprehensively, extracellularly labeled tissue and previous information on sample structure via machine learning to simultaneously achieve isotropic super-resolution, high signal-to-noise ratio and compatibility with living tissue. This allows dense deep-learning-based instance segmentation and 3D reconstruction at a synapse level, incorporating molecular, activity and morphodynamic information. LIONESS opens up avenues for studying the dynamic functional (nano-)architecture of living brain tissue."}],"has_accepted_license":"1","external_id":{"pmid":["37429995"],"isi":["001025621500001"]},"status":"public","oa_version":"Published Version","scopus_import":"1","date_created":"2023-07-23T22:01:13Z","publication":"Nature Methods","corr_author":"1","type":"journal_article"},{"doi":"10.1038/s41467-022-32559-8","isi":1,"file":[{"file_name":"2022_NatureCommunications_BenSimon.pdf","file_id":"11990","date_updated":"2022-08-26T11:51:40Z","success":1,"checksum":"405936d9e4d33625d80c093c9713a91f","file_size":5910357,"content_type":"application/pdf","date_created":"2022-08-26T11:51:40Z","access_level":"open_access","creator":"dernst","relation":"main_file"}],"acknowledgement":"We thank F. Marr and A. Schlögl for technical assistance, E. Kralli-Beller for manuscript editing, as well as C. Sommer and the Imaging and Optics Facility of the Institute of Science and Technology Austria (ISTA) for image analysis scripts and microscopy support. We extend our gratitude to J. Wallenschus and D. Rangel Guerrero for technical assistance acquiring single-unit data and I. Gridchyn for help with single-unit clustering. Finally, we also thank B. Suter for discussions, A. Saunders, M. Jösch, and H. Monyer for critically reading earlier versions of the manuscript, C. Petersen for sharing clearing protocols, and the Scientific Service Units of ISTA for efficient support. This project was funded by the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (ERC advanced grant No 692692 to P.J.) and the Fond zur Förderung der Wissenschaftlichen Forschung (Z 312-B27, Wittgenstein award for P.J. and I3600-B27 for J.G.D. and P.V.).","publisher":"Springer Nature","date_published":"2022-08-16T00:00:00Z","_id":"11951","quality_controlled":"1","article_number":"4826","day":"16","keyword":["General Physics and Astronomy","General Biochemistry","Genetics and Molecular Biology","General Chemistry","Multidisciplinary"],"department":[{"_id":"JoCs"},{"_id":"PeJo"},{"_id":"JoDa"}],"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","oa":1,"title":"A direct excitatory projection from entorhinal layer 6b neurons to the hippocampus contributes to spatial coding and memory","article_processing_charge":"No","publication_identifier":{"issn":["2041-1723"]},"tmp":{"short":"CC BY (4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)"},"project":[{"grant_number":"692692","_id":"25B7EB9E-B435-11E9-9278-68D0E5697425","call_identifier":"H2020","name":"Biophysics and circuit function of a giant cortical glutamatergic synapse"},{"_id":"265CB4D0-B435-11E9-9278-68D0E5697425","call_identifier":"FWF","name":"Optical control of synaptic function via adhesion molecules","grant_number":"I03600"},{"_id":"25C5A090-B435-11E9-9278-68D0E5697425","call_identifier":"FWF","name":"Synaptic communication in neuronal microcircuits","grant_number":"Z00312"}],"intvolume":"        13","date_updated":"2025-06-12T06:10:44Z","ddc":["570"],"citation":{"short":"Y. Ben Simon, K. Käfer, P. Velicky, J.L. Csicsvari, J.G. Danzl, P.M. Jonas, Nature Communications 13 (2022).","mla":"Ben Simon, Yoav, et al. “A Direct Excitatory Projection from Entorhinal Layer 6b Neurons to the Hippocampus Contributes to Spatial Coding and Memory.” <i>Nature Communications</i>, vol. 13, 4826, Springer Nature, 2022, doi:<a href=\"https://doi.org/10.1038/s41467-022-32559-8\">10.1038/s41467-022-32559-8</a>.","ista":"Ben Simon Y, Käfer K, Velicky P, Csicsvari JL, Danzl JG, Jonas PM. 2022. A direct excitatory projection from entorhinal layer 6b neurons to the hippocampus contributes to spatial coding and memory. Nature Communications. 13, 4826.","ama":"Ben Simon Y, Käfer K, Velicky P, Csicsvari JL, Danzl JG, Jonas PM. A direct excitatory projection from entorhinal layer 6b neurons to the hippocampus contributes to spatial coding and memory. <i>Nature Communications</i>. 2022;13. doi:<a href=\"https://doi.org/10.1038/s41467-022-32559-8\">10.1038/s41467-022-32559-8</a>","ieee":"Y. Ben Simon, K. Käfer, P. Velicky, J. L. Csicsvari, J. G. Danzl, and P. M. Jonas, “A direct excitatory projection from entorhinal layer 6b neurons to the hippocampus contributes to spatial coding and memory,” <i>Nature Communications</i>, vol. 13. Springer Nature, 2022.","apa":"Ben Simon, Y., Käfer, K., Velicky, P., Csicsvari, J. L., Danzl, J. G., &#38; Jonas, P. M. (2022). A direct excitatory projection from entorhinal layer 6b neurons to the hippocampus contributes to spatial coding and memory. <i>Nature Communications</i>. Springer Nature. <a href=\"https://doi.org/10.1038/s41467-022-32559-8\">https://doi.org/10.1038/s41467-022-32559-8</a>","chicago":"Ben Simon, Yoav, Karola Käfer, Philipp Velicky, Jozsef L Csicsvari, Johann G Danzl, and Peter M Jonas. “A Direct Excitatory Projection from Entorhinal Layer 6b Neurons to the Hippocampus Contributes to Spatial Coding and Memory.” <i>Nature Communications</i>. Springer Nature, 2022. <a href=\"https://doi.org/10.1038/s41467-022-32559-8\">https://doi.org/10.1038/s41467-022-32559-8</a>."},"article_type":"original","ec_funded":1,"language":[{"iso":"eng"}],"scopus_import":"1","date_created":"2022-08-24T08:25:50Z","publication":"Nature Communications","oa_version":"Published Version","type":"journal_article","corr_author":"1","abstract":[{"lang":"eng","text":"The mammalian hippocampal formation (HF) plays a key role in several higher brain functions, such as spatial coding, learning and memory. Its simple circuit architecture is often viewed as a trisynaptic loop, processing input originating from the superficial layers of the entorhinal cortex (EC) and sending it back to its deeper layers. Here, we show that excitatory neurons in layer 6b of the mouse EC project to all sub-regions comprising the HF and receive input from the CA1, thalamus and claustrum. Furthermore, their output is characterized by unique slow-decaying excitatory postsynaptic currents capable of driving plateau-like potentials in their postsynaptic targets. Optogenetic inhibition of the EC-6b pathway affects spatial coding in CA1 pyramidal neurons, while cell ablation impairs not only acquisition of new spatial memories, but also degradation of previously acquired ones. Our results provide evidence of a functional role for cortical layer 6b neurons in the adult brain."}],"has_accepted_license":"1","external_id":{"pmid":["35974109"],"isi":["000841396400008"]},"status":"public","volume":13,"month":"08","year":"2022","file_date_updated":"2022-08-26T11:51:40Z","publication_status":"published","pmid":1,"acknowledged_ssus":[{"_id":"Bio"},{"_id":"SSU"}],"author":[{"first_name":"Yoav","last_name":"Ben Simon","full_name":"Ben Simon, Yoav","id":"43DF3136-F248-11E8-B48F-1D18A9856A87"},{"last_name":"Käfer","first_name":"Karola","id":"2DAA49AA-F248-11E8-B48F-1D18A9856A87","full_name":"Käfer, Karola"},{"full_name":"Velicky, Philipp","id":"39BDC62C-F248-11E8-B48F-1D18A9856A87","last_name":"Velicky","orcid":"0000-0002-2340-7431","first_name":"Philipp"},{"id":"3FA14672-F248-11E8-B48F-1D18A9856A87","full_name":"Csicsvari, Jozsef L","last_name":"Csicsvari","first_name":"Jozsef L","orcid":"0000-0002-5193-4036"},{"first_name":"Johann G","orcid":"0000-0001-8559-3973","last_name":"Danzl","id":"42EFD3B6-F248-11E8-B48F-1D18A9856A87","full_name":"Danzl, Johann G"},{"id":"353C1B58-F248-11E8-B48F-1D18A9856A87","full_name":"Jonas, Peter M","last_name":"Jonas","first_name":"Peter M","orcid":"0000-0001-5001-4804"}]},{"publisher":"eLife Sciences Publications","doi":"10.7554/elife.79848","acknowledgement":"We thank F Marr for technical assistance, A Murray for RVdG-CVS-N2c viruses and Neuro2A packaging cell-lines and J Watson for reading the manuscript. This research was supported by the Scientific Service Units (SSU) of IST-Austria through resources provided by the Imaging and Optics Facility (IOF) and the Preclinical Facility (PCF). This project was funded by the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (ERC advanced grant No 692692, PJ, ERC starting grant No 756502, MJ), the Fond zur Förderung der Wissenschaftlichen Forschung (Z 312-B27, Wittgenstein award, PJ), the Human Frontier Science Program (LT000256/2018-L, AS) and EMBO (ALTF 1098-2017, AS).","isi":1,"file":[{"date_created":"2023-01-30T11:50:53Z","content_type":"application/pdf","relation":"main_file","creator":"dernst","access_level":"open_access","checksum":"5a2a65e3e7225090c3d8199f3bbd7b7b","success":1,"date_updated":"2023-01-30T11:50:53Z","file_name":"2022_eLife_Sumser.pdf","file_id":"12463","file_size":8506811}],"article_number":"79848","_id":"12288","date_published":"2022-09-15T00:00:00Z","quality_controlled":"1","oa":1,"title":"Fast, high-throughput production of improved rabies viral vectors for specific, efficient and versatile transsynaptic retrograde labeling","user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","department":[{"_id":"MaJö"},{"_id":"PeJo"}],"keyword":["General Immunology and Microbiology","General Biochemistry","Genetics and Molecular Biology","General Medicine","General Neuroscience"],"day":"15","publication_identifier":{"eissn":["2050-084X"]},"tmp":{"short":"CC BY (4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)"},"article_processing_charge":"No","date_updated":"2025-04-15T08:29:05Z","ddc":["570"],"intvolume":"        11","project":[{"_id":"25B7EB9E-B435-11E9-9278-68D0E5697425","call_identifier":"H2020","name":"Biophysics and circuit function of a giant cortical glutamatergic synapse","grant_number":"692692"},{"grant_number":"756502","call_identifier":"H2020","_id":"2634E9D2-B435-11E9-9278-68D0E5697425","name":"Circuits of Visual Attention"},{"grant_number":"Z00312","call_identifier":"FWF","_id":"25C5A090-B435-11E9-9278-68D0E5697425","name":"Synaptic communication in neuronal microcircuits"},{"name":"Neuronal networks of salience and spatial detection in the murine superior colliculus","_id":"266D407A-B435-11E9-9278-68D0E5697425","grant_number":"LT000256"},{"grant_number":"ALTF 1098-2017","_id":"264FEA02-B435-11E9-9278-68D0E5697425","name":"Connecting sensory with motor processing in the superior colliculus"}],"abstract":[{"lang":"eng","text":"To understand the function of neuronal circuits, it is crucial to disentangle the connectivity patterns within the network. However, most tools currently used to explore connectivity have low throughput, low selectivity, or limited accessibility. Here, we report the development of an improved packaging system for the production of the highly neurotropic RVdGenvA-CVS-N2c rabies viral vectors, yielding titers orders of magnitude higher with no background contamination, at a fraction of the production time, while preserving the efficiency of transsynaptic labeling. Along with the production pipeline, we developed suites of ‘starter’ AAV and bicistronic RVdG-CVS-N2c vectors, enabling retrograde labeling from a wide range of neuronal populations, tailored for diverse experimental requirements. We demonstrate the power and flexibility of the new system by uncovering hidden local and distal inhibitory connections in the mouse hippocampal formation and by imaging the functional properties of a cortical microcircuit across weeks. Our novel production pipeline provides a convenient approach to generate new rabies vectors, while our toolkit flexibly and efficiently expands the current capacity to label, manipulate and image the neuronal activity of interconnected neuronal circuits in vitro and in vivo."}],"external_id":{"isi":["000892204300001"],"pmid":["36040301"]},"has_accepted_license":"1","status":"public","publication":"eLife","date_created":"2023-01-16T10:04:15Z","scopus_import":"1","oa_version":"Published Version","corr_author":"1","type":"journal_article","ec_funded":1,"article_type":"original","citation":{"chicago":"Sumser, Anton L, Maximilian A Jösch, Peter M Jonas, and Yoav Ben Simon. “Fast, High-Throughput Production of Improved Rabies Viral Vectors for Specific, Efficient and Versatile Transsynaptic Retrograde Labeling.” <i>ELife</i>. eLife Sciences Publications, 2022. <a href=\"https://doi.org/10.7554/elife.79848\">https://doi.org/10.7554/elife.79848</a>.","short":"A.L. Sumser, M.A. Jösch, P.M. Jonas, Y. Ben Simon, ELife 11 (2022).","mla":"Sumser, Anton L., et al. “Fast, High-Throughput Production of Improved Rabies Viral Vectors for Specific, Efficient and Versatile Transsynaptic Retrograde Labeling.” <i>ELife</i>, vol. 11, 79848, eLife Sciences Publications, 2022, doi:<a href=\"https://doi.org/10.7554/elife.79848\">10.7554/elife.79848</a>.","ista":"Sumser AL, Jösch MA, Jonas PM, Ben Simon Y. 2022. Fast, high-throughput production of improved rabies viral vectors for specific, efficient and versatile transsynaptic retrograde labeling. eLife. 11, 79848.","ieee":"A. L. Sumser, M. A. Jösch, P. M. Jonas, and Y. Ben Simon, “Fast, high-throughput production of improved rabies viral vectors for specific, efficient and versatile transsynaptic retrograde labeling,” <i>eLife</i>, vol. 11. eLife Sciences Publications, 2022.","ama":"Sumser AL, Jösch MA, Jonas PM, Ben Simon Y. Fast, high-throughput production of improved rabies viral vectors for specific, efficient and versatile transsynaptic retrograde labeling. <i>eLife</i>. 2022;11. doi:<a href=\"https://doi.org/10.7554/elife.79848\">10.7554/elife.79848</a>","apa":"Sumser, A. L., Jösch, M. A., Jonas, P. M., &#38; Ben Simon, Y. (2022). Fast, high-throughput production of improved rabies viral vectors for specific, efficient and versatile transsynaptic retrograde labeling. <i>ELife</i>. eLife Sciences Publications. <a href=\"https://doi.org/10.7554/elife.79848\">https://doi.org/10.7554/elife.79848</a>"},"language":[{"iso":"eng"}],"file_date_updated":"2023-01-30T11:50:53Z","publication_status":"published","year":"2022","month":"09","volume":11,"acknowledged_ssus":[{"_id":"Bio"},{"_id":"PreCl"}],"author":[{"last_name":"Sumser","orcid":"0000-0002-4792-1881","first_name":"Anton L","full_name":"Sumser, Anton L","id":"3320A096-F248-11E8-B48F-1D18A9856A87"},{"id":"2BD278E6-F248-11E8-B48F-1D18A9856A87","full_name":"Jösch, Maximilian A","last_name":"Jösch","first_name":"Maximilian A","orcid":"0000-0002-3937-1330"},{"full_name":"Jonas, Peter M","id":"353C1B58-F248-11E8-B48F-1D18A9856A87","last_name":"Jonas","orcid":"0000-0001-5001-4804","first_name":"Peter M"},{"last_name":"Ben Simon","first_name":"Yoav","id":"43DF3136-F248-11E8-B48F-1D18A9856A87","full_name":"Ben Simon, Yoav"}],"pmid":1},{"publisher":"Springer Nature","file":[{"creator":"dernst","relation":"main_file","access_level":"open_access","date_created":"2022-02-21T07:59:32Z","content_type":"application/pdf","file_size":2625540,"checksum":"d86ee8eabe8b794730729ffbb1a8832e","success":1,"file_id":"10778","file_name":"2022_NatureCommunications_Herguedas.pdf","date_updated":"2022-02-21T07:59:32Z"}],"isi":1,"acknowledgement":"We thank Ondrej Cais for critical reading of the manuscript. We are grateful to LMB\r\nscientific computing and the EM facility for support, Paul Emsley for help with model\r\nbuilding and Takanori Nakane for helpful comments with Relion 3.1. This work was\r\nsupported by grants from the Medical Research Council (MC_U105174197) and BBSRC\r\n(BB/N002113/1) to I.H.G, and grants from the MCIN/AEI/ 10.13039/501100011033 and\r\n“ESF Investing in your future” to B.H (PID2019-106284GA-I00 and RYC2018-025720-I).","doi":"10.1038/s41467-022-28404-7","article_number":"734","_id":"10763","date_published":"2022-02-08T00:00:00Z","quality_controlled":"1","department":[{"_id":"PeJo"}],"day":"08","title":"Mechanisms underlying TARP modulation of the GluA1/2-γ8 AMPA receptor","oa":1,"user_id":"ba8df636-2132-11f1-aed0-ed93e2281fdd","tmp":{"short":"CC BY (4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)"},"publication_identifier":{"eissn":["2041-1723"]},"article_processing_charge":"No","ddc":["570"],"date_updated":"2026-04-02T12:14:43Z","intvolume":"        13","language":[{"iso":"eng"}],"citation":{"chicago":"Herguedas, Beatriz, Bianka K. Kohegyi, Jan Niklas Dohrke, Jake Watson, Danyang Zhang, Hinze Ho, Saher A. Shaikh, Remigijus Lape, James M. Krieger, and Ingo H. Greger. “Mechanisms Underlying TARP Modulation of the GluA1/2-Γ8 AMPA Receptor.” <i>Nature Communications</i>. Springer Nature, 2022. <a href=\"https://doi.org/10.1038/s41467-022-28404-7\">https://doi.org/10.1038/s41467-022-28404-7</a>.","mla":"Herguedas, Beatriz, et al. “Mechanisms Underlying TARP Modulation of the GluA1/2-Γ8 AMPA Receptor.” <i>Nature Communications</i>, vol. 13, 734, Springer Nature, 2022, doi:<a href=\"https://doi.org/10.1038/s41467-022-28404-7\">10.1038/s41467-022-28404-7</a>.","short":"B. Herguedas, B.K. Kohegyi, J.N. Dohrke, J. Watson, D. Zhang, H. Ho, S.A. Shaikh, R. Lape, J.M. Krieger, I.H. Greger, Nature Communications 13 (2022).","apa":"Herguedas, B., Kohegyi, B. K., Dohrke, J. N., Watson, J., Zhang, D., Ho, H., … Greger, I. H. (2022). Mechanisms underlying TARP modulation of the GluA1/2-γ8 AMPA receptor. <i>Nature Communications</i>. Springer Nature. <a href=\"https://doi.org/10.1038/s41467-022-28404-7\">https://doi.org/10.1038/s41467-022-28404-7</a>","ieee":"B. Herguedas <i>et al.</i>, “Mechanisms underlying TARP modulation of the GluA1/2-γ8 AMPA receptor,” <i>Nature Communications</i>, vol. 13. Springer Nature, 2022.","ista":"Herguedas B, Kohegyi BK, Dohrke JN, Watson J, Zhang D, Ho H, Shaikh SA, Lape R, Krieger JM, Greger IH. 2022. Mechanisms underlying TARP modulation of the GluA1/2-γ8 AMPA receptor. Nature Communications. 13, 734.","ama":"Herguedas B, Kohegyi BK, Dohrke JN, et al. Mechanisms underlying TARP modulation of the GluA1/2-γ8 AMPA receptor. <i>Nature Communications</i>. 2022;13. doi:<a href=\"https://doi.org/10.1038/s41467-022-28404-7\">10.1038/s41467-022-28404-7</a>"},"article_type":"original","external_id":{"pmid":["35136046"],"isi":["000757297200008"]},"has_accepted_license":"1","status":"public","abstract":[{"lang":"eng","text":"AMPA-type glutamate receptors (AMPARs) mediate rapid signal transmission at excitatory\r\nsynapses in the brain. Glutamate binding to the receptor’s ligand-binding domains (LBDs)\r\nleads to ion channel activation and desensitization. Gating kinetics shape synaptic transmission\r\nand are strongly modulated by transmembrane AMPAR regulatory proteins (TARPs)\r\nthrough currently incompletely resolved mechanisms. Here, electron cryo-microscopy\r\nstructures of the GluA1/2 TARP-γ8 complex, in both open and desensitized states\r\n(at 3.5 Å), reveal state-selective engagement of the LBDs by the large TARP-γ8 loop (‘β1’),\r\nelucidating how this TARP stabilizes specific gating states. We further show how TARPs alter\r\nchannel rectification, by interacting with the pore helix of the selectivity filter. Lastly, we\r\nreveal that the Q/R-editing site couples the channel constriction at the filter entrance to the\r\ngate, and forms the major cation binding site in the conduction path. Our results provide a\r\nmechanistic framework of how TARPs modulate AMPAR gating and conductance."}],"type":"journal_article","scopus_import":"1","oa_version":"Published Version","date_created":"2022-02-20T23:01:30Z","publication":"Nature Communications","month":"02","volume":13,"file_date_updated":"2022-02-21T07:59:32Z","publication_status":"published","year":"2022","pmid":1,"author":[{"last_name":"Herguedas","first_name":"Beatriz","full_name":"Herguedas, Beatriz"},{"first_name":"Bianka K.","last_name":"Kohegyi","full_name":"Kohegyi, Bianka K."},{"last_name":"Dohrke","first_name":"Jan Niklas","full_name":"Dohrke, Jan Niklas"},{"orcid":"0000-0002-8698-3823","first_name":"Jake","last_name":"Watson","full_name":"Watson, Jake","id":"63836096-4690-11EA-BD4E-32803DDC885E"},{"first_name":"Danyang","last_name":"Zhang","full_name":"Zhang, Danyang"},{"first_name":"Hinze","last_name":"Ho","full_name":"Ho, Hinze"},{"first_name":"Saher A.","last_name":"Shaikh","full_name":"Shaikh, Saher A."},{"full_name":"Lape, Remigijus","last_name":"Lape","first_name":"Remigijus"},{"full_name":"Krieger, James M.","first_name":"James M.","last_name":"Krieger"},{"full_name":"Greger, Ingo H.","first_name":"Ingo H.","last_name":"Greger"}]},{"file_date_updated":"2023-04-20T22:30:03Z","publication_status":"published","year":"2022","month":"04","related_material":{"record":[{"id":"7473","status":"public","relation":"part_of_dissertation"},{"id":"11222","status":"public","relation":"part_of_dissertation"}]},"acknowledged_ssus":[{"_id":"EM-Fac"},{"_id":"PreCl"}],"author":[{"last_name":"Kim","orcid":"0000-0003-2344-1039","first_name":"Olena","full_name":"Kim, Olena","id":"3F8ABDDA-F248-11E8-B48F-1D18A9856A87"}],"alternative_title":["ISTA Thesis"],"page":"132","date_updated":"2026-06-18T10:49:27Z","ddc":["570"],"OA_place":"publisher","project":[{"grant_number":"708497","name":"Presynaptic calcium channels distribution and impact on coupling at the hippocampal mossy fiber synapse","call_identifier":"H2020","_id":"25BAF7B2-B435-11E9-9278-68D0E5697425"},{"grant_number":"692692","name":"Biophysics and circuit function of a giant cortical glutamatergic synapse","_id":"25B7EB9E-B435-11E9-9278-68D0E5697425","call_identifier":"H2020"},{"name":"Zellkommunikation in Gesundheit und Krankheit","call_identifier":"FWF","_id":"25C3DBB6-B435-11E9-9278-68D0E5697425","grant_number":"W01205"},{"grant_number":"Z00312","_id":"25C5A090-B435-11E9-9278-68D0E5697425","name":"Synaptic communication in neuronal microcircuits","call_identifier":"FWF"}],"abstract":[{"lang":"eng","text":"One of the fundamental questions in Neuroscience is how the structure of synapses and their physiological properties are related. While synaptic transmission remains a dynamic process, electron microscopy provides images with comparably low temporal resolution (Studer et al., 2014). The current work overcomes this challenge and describes an improved “Flash and Freeze” technique (Watanabe et al., 2013a; Watanabe et al., 2013b) to study synaptic transmission at the hippocampal mossy fiber-CA3 pyramidal neuron synapses, using mouse acute brain slices and organotypic slices culture. The improved method allowed for selective stimulation of presynaptic mossy fiber boutons and the observation of synaptic vesicle pool dynamics at the active zones. Our results uncovered several intriguing morphological features of mossy fiber boutons. First, the docked vesicle pool was largely depleted (more than 70%) after stimulation, implying that the docked synaptic vesicles pool and readily releasable pool are vastly overlapping in mossy fiber boutons. Second, the synaptic vesicles are skewed towards larger diameters, displaying a wide range of sizes. An increase in the mean diameter of synaptic vesicles, after single and repetitive stimulation, suggests that smaller vesicles have a higher release probability. Third, we observed putative endocytotic structures after moderate light stimulation, matching the timing of previously described ultrafast endocytosis (Watanabe et al., 2013a; Delvendahl et al., 2016). \r\n\tIn addition, synaptic transmission depends on a sophisticated system of protein machinery and calcium channels (Südhof, 2013b), which amplifies the challenge in studying synaptic communication as these interactions can be potentially modified during synaptic plasticity. And although recent study elucidated the potential correlation between physiological and morphological properties of synapses during synaptic plasticity (Vandael et al., 2020), the molecular underpinning of it remains unknown. Thus, the presented work tries to overcome this challenge and aims to pinpoint changes in the molecular architecture at hippocampal mossy fiber bouton synapses during short- and long-term potentiation (STP and LTP), we combined chemical potentiation, with the application of a cyclic adenosine monophosphate agonist (i.e. forskolin) and freeze-fracture replica immunolabelling. This method allowed the localization of membrane-bound proteins with nanometer precision within the active zone, in particular, P/Q-type calcium channels and synaptic vesicle priming proteins Munc13-1/2. First, we found that the number of clusters of Munc13-1 in the mossy fiber bouton active zone increased significantly during STP, but decreased to lower than the control value during LTP. Secondly, although the distance between the calcium channels and Munc13-1s did not change after induction of STP, it shortened during the LTP phase. Additionally, forskolin did not affect Munc13-2 distribution during STP and LTP. These results indicate the existence of two distinct mechanisms that govern STP and LTP at mossy fiber bouton synapses: an increase in the readily realizable pool in the case of STP and a potential increase in release probability during LTP. “Flash and freeze” and functional electron microscopy, are versatile methods that can be successfully applied to intact brain circuits to study synaptic transmission even at the molecular level.\r\n"}],"has_accepted_license":"1","status":"public","oa_version":"Published Version","date_created":"2022-04-20T09:47:12Z","type":"dissertation","corr_author":"1","citation":{"apa":"Kim, O. (2022). <i>Nanoarchitecture of hippocampal mossy fiber-CA3 pyramidal neuron synapses</i>. Institute of Science and Technology Austria. <a href=\"https://doi.org/10.15479/at:ista:11196\">https://doi.org/10.15479/at:ista:11196</a>","ama":"Kim O. Nanoarchitecture of hippocampal mossy fiber-CA3 pyramidal neuron synapses. 2022. doi:<a href=\"https://doi.org/10.15479/at:ista:11196\">10.15479/at:ista:11196</a>","ieee":"O. Kim, “Nanoarchitecture of hippocampal mossy fiber-CA3 pyramidal neuron synapses,” Institute of Science and Technology Austria, 2022.","ista":"Kim O. 2022. Nanoarchitecture of hippocampal mossy fiber-CA3 pyramidal neuron synapses. Institute of Science and Technology Austria.","mla":"Kim, Olena. <i>Nanoarchitecture of Hippocampal Mossy Fiber-CA3 Pyramidal Neuron Synapses</i>. Institute of Science and Technology Austria, 2022, doi:<a href=\"https://doi.org/10.15479/at:ista:11196\">10.15479/at:ista:11196</a>.","short":"O. Kim, Nanoarchitecture of Hippocampal Mossy Fiber-CA3 Pyramidal Neuron Synapses, Institute of Science and Technology Austria, 2022.","chicago":"Kim, Olena. “Nanoarchitecture of Hippocampal Mossy Fiber-CA3 Pyramidal Neuron Synapses.” Institute of Science and Technology Austria, 2022. <a href=\"https://doi.org/10.15479/at:ista:11196\">https://doi.org/10.15479/at:ista:11196</a>."},"ec_funded":1,"language":[{"iso":"eng"}],"oa":1,"title":"Nanoarchitecture of hippocampal mossy fiber-CA3 pyramidal neuron synapses","user_id":"ba8df636-2132-11f1-aed0-ed93e2281fdd","department":[{"_id":"PeJo"},{"_id":"GradSch"}],"day":"20","publication_identifier":{"issn":["2663-337X"]},"tmp":{"short":"CC BY-NC-ND (4.0)","legal_code_url":"https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode","name":"Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0)","image":"/images/cc_by_nc_nd.png"},"article_processing_charge":"No","degree_awarded":"PhD","publisher":"Institute of Science and Technology Austria","doi":"10.15479/at:ista:11196","file":[{"date_created":"2022-04-20T14:21:56Z","content_type":"application/pdf","relation":"main_file","creator":"okim","access_level":"open_access","checksum":"1616a8bf6f13a57c892dac873dcd0936","date_updated":"2023-04-20T22:30:03Z","embargo":"2023-04-19","file_name":"Olena_KIM_thesis_final.pdf","file_id":"11220","file_size":21273537},{"date_updated":"2023-04-20T22:30:03Z","file_id":"11221","file_name":"KIM_thesis_final.zip","checksum":"1acb433f98dc42abb0b4b0cbb0c4b918","embargo_to":"open_access","file_size":59248569,"content_type":"application/x-zip-compressed","date_created":"2022-04-20T14:22:56Z","access_level":"closed","relation":"source_file","creator":"okim"}],"supervisor":[{"first_name":"Peter M","orcid":"0000-0001-5001-4804","last_name":"Jonas","id":"353C1B58-F248-11E8-B48F-1D18A9856A87","full_name":"Jonas, Peter M"}],"date_published":"2022-04-20T00:00:00Z","_id":"11196"},{"author":[{"first_name":"Philipp","orcid":"0000-0002-2340-7431","last_name":"Velicky","id":"39BDC62C-F248-11E8-B48F-1D18A9856A87","full_name":"Velicky, Philipp"},{"first_name":"Eder","orcid":"0000-0001-5665-0430","last_name":"Miguel Villalba","id":"3FB91342-F248-11E8-B48F-1D18A9856A87","full_name":"Miguel Villalba, Eder"},{"id":"443DB6DE-F248-11E8-B48F-1D18A9856A87","full_name":"Michalska, Julia M","first_name":"Julia M","orcid":"0000-0003-3862-1235","last_name":"Michalska"},{"full_name":"Wei, Donglai","first_name":"Donglai","last_name":"Wei"},{"full_name":"Lin, Zudi","last_name":"Lin","first_name":"Zudi"},{"id":"63836096-4690-11EA-BD4E-32803DDC885E","full_name":"Watson, Jake","last_name":"Watson","first_name":"Jake","orcid":"0000-0002-8698-3823"},{"full_name":"Troidl, Jakob","last_name":"Troidl","first_name":"Jakob"},{"first_name":"Johanna","last_name":"Beyer","full_name":"Beyer, Johanna"},{"last_name":"Ben Simon","first_name":"Yoav","full_name":"Ben Simon, Yoav","id":"43DF3136-F248-11E8-B48F-1D18A9856A87"},{"full_name":"Sommer, Christoph M","id":"4DF26D8C-F248-11E8-B48F-1D18A9856A87","last_name":"Sommer","orcid":"0000-0003-1216-9105","first_name":"Christoph M"},{"first_name":"Wiebke","orcid":"0000-0003-0201-2315","last_name":"Jahr","id":"425C1CE8-F248-11E8-B48F-1D18A9856A87","full_name":"Jahr, Wiebke"},{"full_name":"Cenameri, Alban","id":"9ac8f577-2357-11eb-997a-e566c5550886","last_name":"Cenameri","first_name":"Alban"},{"full_name":"Broichhagen, Johannes","last_name":"Broichhagen","first_name":"Johannes"},{"full_name":"Grant, Seth G. N.","last_name":"Grant","first_name":"Seth G. N."},{"last_name":"Jonas","first_name":"Peter M","orcid":"0000-0001-5001-4804","id":"353C1B58-F248-11E8-B48F-1D18A9856A87","full_name":"Jonas, Peter M"},{"full_name":"Novarino, Gaia","id":"3E57A680-F248-11E8-B48F-1D18A9856A87","last_name":"Novarino","orcid":"0000-0002-7673-7178","first_name":"Gaia"},{"first_name":"Hanspeter","last_name":"Pfister","full_name":"Pfister, Hanspeter"},{"id":"49876194-F248-11E8-B48F-1D18A9856A87","full_name":"Bickel, Bernd","first_name":"Bernd","orcid":"0000-0001-6511-9385","last_name":"Bickel"},{"last_name":"Danzl","first_name":"Johann G","orcid":"0000-0001-8559-3973","id":"42EFD3B6-F248-11E8-B48F-1D18A9856A87","full_name":"Danzl, Johann G"}],"article_processing_charge":"No","oa":1,"publication_status":"draft","title":"Saturated reconstruction of living brain tissue","year":"2022","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","month":"05","department":[{"_id":"PeJo"},{"_id":"GaNo"},{"_id":"BeBi"},{"_id":"JoDa"}],"day":"09","related_material":{"record":[{"id":"13267","status":"public","relation":"later_version"},{"relation":"dissertation_contains","id":"12470","status":"public"}]},"abstract":[{"text":"Complex wiring between neurons underlies the information-processing network enabling all brain functions, including cognition and memory. For understanding how the network is structured, processes information, and changes over time, comprehensive visualization of the architecture of living brain tissue with its cellular and molecular components would open up major opportunities. However, electron microscopy (EM) provides nanometre-scale resolution required for full <jats:italic>in-silico</jats:italic> reconstruction<jats:sup>1–5</jats:sup>, yet is limited to fixed specimens and static representations. Light microscopy allows live observation, with super-resolution approaches<jats:sup>6–12</jats:sup> facilitating nanoscale visualization, but comprehensive 3D-reconstruction of living brain tissue has been hindered by tissue photo-burden, photobleaching, insufficient 3D-resolution, and inadequate signal-to-noise ratio (SNR). Here we demonstrate saturated reconstruction of living brain tissue. We developed an integrated imaging and analysis technology, adapting stimulated emission depletion (STED) microscopy<jats:sup>6,13</jats:sup> in extracellularly labelled tissue<jats:sup>14</jats:sup> for high SNR and near-isotropic resolution. Centrally, a two-stage deep-learning approach leveraged previously obtained information on sample structure to drastically reduce photo-burden and enable automated volumetric reconstruction down to single synapse level. Live reconstruction provides unbiased analysis of tissue architecture across time in relation to functional activity and targeted activation, and contextual understanding of molecular labelling. This adoptable technology will facilitate novel insights into the dynamic functional architecture of living brain tissue.","lang":"eng"}],"das_tickbox":"1","status":"public","oa_version":"Preprint","date_created":"2022-08-23T11:07:59Z","publication":"bioRxiv","corr_author":"1","main_file_link":[{"open_access":"1","url":"https://doi.org/10.1101/2022.03.16.484431"}],"type":"preprint","citation":{"chicago":"Velicky, Philipp, Eder Miguel Villalba, Julia M Michalska, Donglai Wei, Zudi Lin, Jake Watson, Jakob Troidl, et al. “Saturated Reconstruction of Living Brain Tissue.” <i>BioRxiv</i>, n.d. <a href=\"https://doi.org/10.1101/2022.03.16.484431\">https://doi.org/10.1101/2022.03.16.484431</a>.","apa":"Velicky, P., Miguel Villalba, E., Michalska, J. M., Wei, D., Lin, Z., Watson, J., … Danzl, J. G. (n.d.). Saturated reconstruction of living brain tissue. <i>bioRxiv</i>. <a href=\"https://doi.org/10.1101/2022.03.16.484431\">https://doi.org/10.1101/2022.03.16.484431</a>","ieee":"P. Velicky <i>et al.</i>, “Saturated reconstruction of living brain tissue,” <i>bioRxiv</i>. .","ama":"Velicky P, Miguel Villalba E, Michalska JM, et al. Saturated reconstruction of living brain tissue. <i>bioRxiv</i>. doi:<a href=\"https://doi.org/10.1101/2022.03.16.484431\">10.1101/2022.03.16.484431</a>","ista":"Velicky P, Miguel Villalba E, Michalska JM, Wei D, Lin Z, Watson J, Troidl J, Beyer J, Ben Simon Y, Sommer CM, Jahr W, Cenameri A, Broichhagen J, Grant SGN, Jonas PM, Novarino G, Pfister H, Bickel B, Danzl JG. Saturated reconstruction of living brain tissue. bioRxiv, <a href=\"https://doi.org/10.1101/2022.03.16.484431\">10.1101/2022.03.16.484431</a>.","mla":"Velicky, Philipp, et al. “Saturated Reconstruction of Living Brain Tissue.” <i>BioRxiv</i>, doi:<a href=\"https://doi.org/10.1101/2022.03.16.484431\">10.1101/2022.03.16.484431</a>.","short":"P. Velicky, E. Miguel Villalba, J.M. Michalska, D. Wei, Z. Lin, J. Watson, J. Troidl, J. Beyer, Y. Ben Simon, C.M. Sommer, W. Jahr, A. Cenameri, J. Broichhagen, S.G.N. Grant, P.M. Jonas, G. Novarino, H. Pfister, B. Bickel, J.G. Danzl, BioRxiv (n.d.)."},"language":[{"iso":"eng"}],"_id":"11943","date_published":"2022-05-09T00:00:00Z","date_updated":"2026-09-03T22:31:06Z","OA_place":"repository","doi":"10.1101/2022.03.16.484431"},{"date_updated":"2026-09-03T22:31:06Z","doi":"10.1101/2022.08.17.504272","abstract":[{"text":"Mapping the complex and dense arrangement of cells and their connectivity in brain tissue demands nanoscale spatial resolution imaging. Super-resolution optical microscopy excels at visualizing specific molecules and individual cells but fails to provide tissue context. Here we developed Comprehensive Analysis of Tissues across Scales (CATS), a technology to densely map brain tissue architecture from millimeter regional to nanoscopic synaptic scales in diverse chemically fixed brain preparations, including rodent and human. CATS leverages fixation-compatible extracellular labeling and advanced optical readout, in particular stimulated-emission depletion and expansion microscopy, to comprehensively delineate cellular structures. It enables 3D-reconstructing single synapses and mapping synaptic connectivity by identification and tailored analysis of putative synaptic cleft regions. Applying CATS to the hippocampal mossy fiber circuitry, we demonstrate its power to reveal the system’s molecularly informed ultrastructure across spatial scales and assess local connectivity by reconstructing and quantifying the synaptic input and output structure of identified neurons.","lang":"eng"}],"status":"public","das_tickbox":"1","publication":"bioRxiv","date_created":"2022-08-24T08:24:52Z","oa_version":"Preprint","corr_author":"1","type":"preprint","main_file_link":[{"url":"https://doi.org/10.1101/2022.08.17.504272","open_access":"1"}],"citation":{"mla":"Michalska, Julia M., et al. “Uncovering Brain Tissue Architecture across Scales with Super-Resolution Light Microscopy.” <i>BioRxiv</i>, doi:<a href=\"https://doi.org/10.1101/2022.08.17.504272\">10.1101/2022.08.17.504272</a>.","short":"J.M. Michalska, J. Lyudchik, P. Velicky, H. Korinkova, J. Watson, A. Cenameri, C.M. Sommer, A. Venturino, K. Roessler, T. Czech, S. Siegert, G. Novarino, P.M. Jonas, J.G. Danzl, BioRxiv (n.d.).","apa":"Michalska, J. M., Lyudchik, J., Velicky, P., Korinkova, H., Watson, J., Cenameri, A., … Danzl, J. G. (n.d.). Uncovering brain tissue architecture across scales with super-resolution light microscopy. <i>bioRxiv</i>. <a href=\"https://doi.org/10.1101/2022.08.17.504272\">https://doi.org/10.1101/2022.08.17.504272</a>","ista":"Michalska JM, Lyudchik J, Velicky P, Korinkova H, Watson J, Cenameri A, Sommer CM, Venturino A, Roessler K, Czech T, Siegert S, Novarino G, Jonas PM, Danzl JG. Uncovering brain tissue architecture across scales with super-resolution light microscopy. bioRxiv, <a href=\"https://doi.org/10.1101/2022.08.17.504272\">10.1101/2022.08.17.504272</a>.","ama":"Michalska JM, Lyudchik J, Velicky P, et al. Uncovering brain tissue architecture across scales with super-resolution light microscopy. <i>bioRxiv</i>. doi:<a href=\"https://doi.org/10.1101/2022.08.17.504272\">10.1101/2022.08.17.504272</a>","ieee":"J. M. Michalska <i>et al.</i>, “Uncovering brain tissue architecture across scales with super-resolution light microscopy,” <i>bioRxiv</i>. .","chicago":"Michalska, Julia M, Julia Lyudchik, Philipp Velicky, Hana Korinkova, Jake Watson, Alban Cenameri, Christoph M Sommer, et al. “Uncovering Brain Tissue Architecture across Scales with Super-Resolution Light Microscopy.” <i>BioRxiv</i>, n.d. <a href=\"https://doi.org/10.1101/2022.08.17.504272\">https://doi.org/10.1101/2022.08.17.504272</a>."},"language":[{"iso":"eng"}],"_id":"11950","date_published":"2022-08-18T00:00:00Z","oa":1,"publication_status":"draft","title":"Uncovering brain tissue architecture across scales with super-resolution light microscopy","year":"2022","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","department":[{"_id":"SaSi"},{"_id":"GaNo"},{"_id":"PeJo"},{"_id":"JoDa"}],"month":"08","day":"18","related_material":{"record":[{"status":"public","id":"12470","relation":"dissertation_contains"}]},"author":[{"full_name":"Michalska, Julia M","id":"443DB6DE-F248-11E8-B48F-1D18A9856A87","last_name":"Michalska","orcid":"0000-0003-3862-1235","first_name":"Julia M"},{"full_name":"Lyudchik, Julia","id":"46E28B80-F248-11E8-B48F-1D18A9856A87","first_name":"Julia","last_name":"Lyudchik"},{"full_name":"Velicky, Philipp","id":"39BDC62C-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0002-2340-7431","first_name":"Philipp","last_name":"Velicky"},{"first_name":"Hana","last_name":"Korinkova","full_name":"Korinkova, Hana","id":"ee3cb6ca-ec98-11ea-ae11-ff703e2254ed"},{"id":"63836096-4690-11EA-BD4E-32803DDC885E","full_name":"Watson, Jake","last_name":"Watson","first_name":"Jake","orcid":"0000-0002-8698-3823"},{"id":"9ac8f577-2357-11eb-997a-e566c5550886","full_name":"Cenameri, Alban","first_name":"Alban","last_name":"Cenameri"},{"full_name":"Sommer, Christoph M","id":"4DF26D8C-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0003-1216-9105","first_name":"Christoph M","last_name":"Sommer"},{"id":"41CB84B2-F248-11E8-B48F-1D18A9856A87","full_name":"Venturino, Alessandro","last_name":"Venturino","first_name":"Alessandro","orcid":"0000-0003-2356-9403"},{"full_name":"Roessler, Karl","last_name":"Roessler","first_name":"Karl"},{"full_name":"Czech, Thomas","first_name":"Thomas","last_name":"Czech"},{"orcid":"0000-0001-8635-0877","first_name":"Sandra","last_name":"Siegert","full_name":"Siegert, Sandra","id":"36ACD32E-F248-11E8-B48F-1D18A9856A87"},{"last_name":"Novarino","first_name":"Gaia","orcid":"0000-0002-7673-7178","id":"3E57A680-F248-11E8-B48F-1D18A9856A87","full_name":"Novarino, Gaia"},{"last_name":"Jonas","first_name":"Peter M","orcid":"0000-0001-5001-4804","id":"353C1B58-F248-11E8-B48F-1D18A9856A87","full_name":"Jonas, Peter M"},{"full_name":"Danzl, Johann G","id":"42EFD3B6-F248-11E8-B48F-1D18A9856A87","last_name":"Danzl","orcid":"0000-0001-8559-3973","first_name":"Johann G"}],"article_processing_charge":"No"},{"pmid":1,"author":[{"last_name":"Balmer","first_name":"Timothy S","full_name":"Balmer, Timothy S"},{"id":"4305C450-F248-11E8-B48F-1D18A9856A87","full_name":"Borges Merjane, Carolina","first_name":"Carolina","orcid":"0000-0003-0005-401X","last_name":"Borges Merjane"},{"full_name":"Trussell, Laurence O","last_name":"Trussell","first_name":"Laurence O"}],"volume":10,"month":"02","year":"2021","file_date_updated":"2024-04-09T11:13:07Z","publication_status":"published","language":[{"iso":"eng"}],"article_type":"original","citation":{"short":"T.S. Balmer, C. Borges Merjane, L.O. Trussell, ELife 10 (2021).","mla":"Balmer, Timothy S., et al. “Incomplete Removal of Extracellular Glutamate Controls Synaptic Transmission and Integration at a Cerebellar Synapse.” <i>ELife</i>, vol. 10, e63819, eLife Sciences Publications, 2021, doi:<a href=\"https://doi.org/10.7554/elife.63819\">10.7554/elife.63819</a>.","ista":"Balmer TS, Borges Merjane C, Trussell LO. 2021. Incomplete removal of extracellular glutamate controls synaptic transmission and integration at a cerebellar synapse. eLife. 10, e63819.","ieee":"T. S. Balmer, C. Borges Merjane, and L. O. Trussell, “Incomplete removal of extracellular glutamate controls synaptic transmission and integration at a cerebellar synapse,” <i>eLife</i>, vol. 10. eLife Sciences Publications, 2021.","ama":"Balmer TS, Borges Merjane C, Trussell LO. Incomplete removal of extracellular glutamate controls synaptic transmission and integration at a cerebellar synapse. <i>eLife</i>. 2021;10. doi:<a href=\"https://doi.org/10.7554/elife.63819\">10.7554/elife.63819</a>","apa":"Balmer, T. S., Borges Merjane, C., &#38; Trussell, L. O. (2021). Incomplete removal of extracellular glutamate controls synaptic transmission and integration at a cerebellar synapse. <i>ELife</i>. eLife Sciences Publications. <a href=\"https://doi.org/10.7554/elife.63819\">https://doi.org/10.7554/elife.63819</a>","chicago":"Balmer, Timothy S, Carolina Borges Merjane, and Laurence O Trussell. “Incomplete Removal of Extracellular Glutamate Controls Synaptic Transmission and Integration at a Cerebellar Synapse.” <i>ELife</i>. eLife Sciences Publications, 2021. <a href=\"https://doi.org/10.7554/elife.63819\">https://doi.org/10.7554/elife.63819</a>."},"type":"journal_article","oa_version":"Published Version","date_created":"2024-04-03T07:58:11Z","publication":"eLife","status":"public","external_id":{"pmid":["33616036"]},"has_accepted_license":"1","abstract":[{"text":"Synapses of glutamatergic mossy fibers (MFs) onto cerebellar unipolar brush cells (UBCs) generate slow excitatory (ON) or inhibitory (OFF) postsynaptic responses dependent on the complement of glutamate receptors expressed on the UBC’s large dendritic brush. Using mouse brain slice recording and computational modeling of synaptic transmission, we found that substantial glutamate is maintained in the UBC synaptic cleft, sufficient to modify spontaneous firing in OFF UBCs and tonically desensitize AMPARs of ON UBCs. The source of this ambient glutamate was spontaneous, spike-independent exocytosis from the MF terminal, and its level was dependent on activity of glutamate transporters EAAT1–2. Increasing levels of ambient glutamate shifted the polarity of evoked synaptic responses in ON UBCs and altered the phase of responses to in vivo-like synaptic activity. Unlike classical fast synapses, receptors at the UBC synapse are virtually always exposed to a significant level of glutamate, which varies in a graded manner during transmission.","lang":"eng"}],"intvolume":"        10","ddc":["570"],"date_updated":"2024-04-09T11:15:01Z","article_processing_charge":"Yes","tmp":{"short":"CC BY (4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)"},"publication_identifier":{"issn":["2050-084X"]},"day":"22","keyword":["General Immunology and Microbiology","General Biochemistry","Genetics and Molecular Biology","General Medicine","General Neuroscience"],"department":[{"_id":"PeJo"}],"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","title":"Incomplete removal of extracellular glutamate controls synaptic transmission and integration at a cerebellar synapse","oa":1,"quality_controlled":"1","_id":"15273","date_published":"2021-02-22T00:00:00Z","article_number":"e63819","doi":"10.7554/elife.63819","file":[{"success":1,"checksum":"bbd4de2e54b7fbc11fba14f59e87fe3f","date_updated":"2024-04-09T11:13:07Z","file_id":"15307","file_name":"2021_eLife_Balmer.pdf","file_size":6997954,"date_created":"2024-04-09T11:13:07Z","content_type":"application/pdf","relation":"main_file","creator":"dernst","access_level":"open_access"}],"publisher":"eLife Sciences Publications"},{"tmp":{"short":"CC BY-NC-ND (4.0)","legal_code_url":"https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode","name":"Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0)","image":"/images/cc_by_nc_nd.png"},"publication_identifier":{"issn":["0165-0270"],"eissn":["1872-678X"]},"article_processing_charge":"Yes (via OA deal)","title":"MOD: A novel machine-learning optimal-filtering method for accurate and efficient detection of subthreshold synaptic events in vivo","oa":1,"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","department":[{"_id":"PeJo"},{"_id":"ScienComp"}],"day":"09","article_number":"109125","quality_controlled":"1","_id":"9329","date_published":"2021-03-09T00:00:00Z","publisher":"Elsevier","acknowledgement":"This project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement number 692692 to P.J.) and the Fond zur Förderung der Wissenschaftlichen Forschung (Z 312-B27, Wittgenstein award to P.J.). We thank Drs. Jozsef Csicsvari, Christoph Lampert, and Federico Stella for critically reading previous manuscript versions. We are also grateful to Drs. Josh Merel and Ben Shababo for their help with applying the Bayesian detection method to our data. We also thank Florian Marr for technical assistance, Eleftheria Kralli-Beller for manuscript editing, and the Scientific Service Units of IST Austria for efficient support.","file":[{"success":1,"checksum":"2a5800d91b96d08b525e17319dcd5e44","file_name":"2021_JourNeuroscienceMeth_Zhang.pdf","file_id":"9339","date_updated":"2021-04-19T08:30:22Z","file_size":6924738,"content_type":"application/pdf","date_created":"2021-04-19T08:30:22Z","creator":"dernst","relation":"main_file","access_level":"open_access"}],"doi":"10.1016/j.jneumeth.2021.109125","isi":1,"author":[{"full_name":"Zhang, Xiaomin","id":"423EC9C2-F248-11E8-B48F-1D18A9856A87","last_name":"Zhang","first_name":"Xiaomin"},{"last_name":"Schlögl","orcid":"0000-0002-5621-8100","first_name":"Alois","full_name":"Schlögl, Alois","id":"45BF87EE-F248-11E8-B48F-1D18A9856A87"},{"full_name":"Vandael, David H","id":"3AE48E0A-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0001-7577-1676","first_name":"David H","last_name":"Vandael"},{"last_name":"Jonas","orcid":"0000-0001-5001-4804","first_name":"Peter M","full_name":"Jonas, Peter M","id":"353C1B58-F248-11E8-B48F-1D18A9856A87"}],"acknowledged_ssus":[{"_id":"SSU"}],"pmid":1,"publication_status":"published","file_date_updated":"2021-04-19T08:30:22Z","year":"2021","month":"03","volume":357,"issue":"6","has_accepted_license":"1","external_id":{"isi":["000661088500005"],"pmid":["33711356"]},"status":"public","abstract":[{"lang":"eng","text":"Background: To understand information coding in single neurons, it is necessary to analyze subthreshold synaptic events, action potentials (APs), and their interrelation in different behavioral states. However, detecting excitatory postsynaptic potentials (EPSPs) or currents (EPSCs) in behaving animals remains challenging, because of unfavorable signal-to-noise ratio, high frequency, fluctuating amplitude, and variable time course of synaptic events.\r\nNew method: We developed a method for synaptic event detection, termed MOD (Machine-learning Optimal-filtering Detection-procedure), which combines concepts of supervised machine learning and optimal Wiener filtering. Experts were asked to manually score short epochs of data. The algorithm was trained to obtain the optimal filter coefficients of a Wiener filter and the optimal detection threshold. Scored and unscored data were then processed with the optimal filter, and events were detected as peaks above threshold.\r\nResults: We challenged MOD with EPSP traces in vivo in mice during spatial navigation and EPSC traces in vitro in slices under conditions of enhanced transmitter release. The area under the curve (AUC) of the receiver operating characteristics (ROC) curve was, on average, 0.894 for in vivo and 0.969 for in vitro data sets, indicating high detection accuracy and efficiency.\r\nComparison with existing methods: When benchmarked using a (1 − AUC)−1 metric, MOD outperformed previous methods (template-fit, deconvolution, and Bayesian methods) by an average factor of 3.13 for in vivo data sets, but showed comparable (template-fit, deconvolution) or higher (Bayesian) computational efficacy.\r\nConclusions: MOD may become an important new tool for large-scale, real-time analysis of synaptic activity."}],"type":"journal_article","scopus_import":"1","oa_version":"Published Version","publication":"Journal of Neuroscience Methods","date_created":"2021-04-18T22:01:39Z","language":[{"iso":"eng"}],"citation":{"chicago":"Zhang, Xiaomin, Alois Schlögl, David H Vandael, and Peter M Jonas. “MOD: A Novel Machine-Learning Optimal-Filtering Method for Accurate and Efficient Detection of Subthreshold Synaptic Events in Vivo.” <i>Journal of Neuroscience Methods</i>. Elsevier, 2021. <a href=\"https://doi.org/10.1016/j.jneumeth.2021.109125\">https://doi.org/10.1016/j.jneumeth.2021.109125</a>.","short":"X. Zhang, A. Schlögl, D.H. Vandael, P.M. Jonas, Journal of Neuroscience Methods 357 (2021).","mla":"Zhang, Xiaomin, et al. “MOD: A Novel Machine-Learning Optimal-Filtering Method for Accurate and Efficient Detection of Subthreshold Synaptic Events in Vivo.” <i>Journal of Neuroscience Methods</i>, vol. 357, no. 6, 109125, Elsevier, 2021, doi:<a href=\"https://doi.org/10.1016/j.jneumeth.2021.109125\">10.1016/j.jneumeth.2021.109125</a>.","ista":"Zhang X, Schlögl A, Vandael DH, Jonas PM. 2021. MOD: A novel machine-learning optimal-filtering method for accurate and efficient detection of subthreshold synaptic events in vivo. Journal of Neuroscience Methods. 357(6), 109125.","ieee":"X. Zhang, A. Schlögl, D. H. Vandael, and P. M. Jonas, “MOD: A novel machine-learning optimal-filtering method for accurate and efficient detection of subthreshold synaptic events in vivo,” <i>Journal of Neuroscience Methods</i>, vol. 357, no. 6. Elsevier, 2021.","ama":"Zhang X, Schlögl A, Vandael DH, Jonas PM. MOD: A novel machine-learning optimal-filtering method for accurate and efficient detection of subthreshold synaptic events in vivo. <i>Journal of Neuroscience Methods</i>. 2021;357(6). doi:<a href=\"https://doi.org/10.1016/j.jneumeth.2021.109125\">10.1016/j.jneumeth.2021.109125</a>","apa":"Zhang, X., Schlögl, A., Vandael, D. H., &#38; Jonas, P. M. (2021). MOD: A novel machine-learning optimal-filtering method for accurate and efficient detection of subthreshold synaptic events in vivo. <i>Journal of Neuroscience Methods</i>. Elsevier. <a href=\"https://doi.org/10.1016/j.jneumeth.2021.109125\">https://doi.org/10.1016/j.jneumeth.2021.109125</a>"},"article_type":"original","ec_funded":1,"ddc":["570"],"date_updated":"2025-06-12T06:39:15Z","intvolume":"       357","project":[{"name":"Biophysics and circuit function of a giant cortical glutamatergic synapse","call_identifier":"H2020","_id":"25B7EB9E-B435-11E9-9278-68D0E5697425","grant_number":"692692"},{"_id":"25C5A090-B435-11E9-9278-68D0E5697425","call_identifier":"FWF","name":"Synaptic communication in neuronal microcircuits","grant_number":"Z00312"}]}]