[{"_id":"21502","author":[{"full_name":"Akther, Sonam","first_name":"Sonam","last_name":"Akther"},{"first_name":"Ashley Bomin","last_name":"Lee","full_name":"Lee, Ashley Bomin"},{"full_name":"Konno, Ayumu","first_name":"Ayumu","last_name":"Konno"},{"first_name":"Antonis","last_name":"Asiminas","full_name":"Asiminas, Antonis"},{"full_name":"Vittani, Marta","first_name":"Marta","last_name":"Vittani"},{"full_name":"Mishima, Tsuneko","last_name":"Mishima","first_name":"Tsuneko"},{"first_name":"Hirokazu","last_name":"Hirai","full_name":"Hirai, Hirokazu"},{"last_name":"Meehan","first_name":"Claire Francesca","full_name":"Meehan, Claire Francesca"},{"full_name":"Duran, Jordi","last_name":"Duran","first_name":"Jordi"},{"full_name":"Guinovart, Joan","last_name":"Guinovart","first_name":"Joan"},{"first_name":"Hitoshi","last_name":"Ashida","full_name":"Ashida, Hitoshi"},{"last_name":"Morita","first_name":"Tsuyoshi","full_name":"Morita, Tsuyoshi"},{"last_name":"Baba","first_name":"Otto","full_name":"Baba, Otto"},{"full_name":"Shigemoto, Ryuichi","id":"499F3ABC-F248-11E8-B48F-1D18A9856A87","last_name":"Shigemoto","orcid":"0000-0001-8761-9444","first_name":"Ryuichi"},{"last_name":"Nedergaard","first_name":"Maiken","full_name":"Nedergaard, Maiken"},{"full_name":"Hirase, Hajime","first_name":"Hajime","last_name":"Hirase"}],"article_number":"115192","scopus_import":"1","quality_controlled":"1","citation":{"apa":"Akther, S., Lee, A. B., Konno, A., Asiminas, A., Vittani, M., Mishima, T., … Hirase, H. (2026). Distribution and functional significance of rodent cerebellar glycogen. <i>IScience</i>. Elsevier. <a href=\"https://doi.org/10.1016/j.isci.2026.115192\">https://doi.org/10.1016/j.isci.2026.115192</a>","short":"S. Akther, A.B. Lee, A. Konno, A. Asiminas, M. Vittani, T. Mishima, H. Hirai, C.F. Meehan, J. Duran, J. Guinovart, H. Ashida, T. Morita, O. Baba, R. Shigemoto, M. Nedergaard, H. Hirase, IScience 29 (2026).","chicago":"Akther, Sonam, Ashley Bomin Lee, Ayumu Konno, Antonis Asiminas, Marta Vittani, Tsuneko Mishima, Hirokazu Hirai, et al. “Distribution and Functional Significance of Rodent Cerebellar Glycogen.” <i>IScience</i>. Elsevier, 2026. <a href=\"https://doi.org/10.1016/j.isci.2026.115192\">https://doi.org/10.1016/j.isci.2026.115192</a>.","mla":"Akther, Sonam, et al. “Distribution and Functional Significance of Rodent Cerebellar Glycogen.” <i>IScience</i>, vol. 29, no. 4, 115192, Elsevier, 2026, doi:<a href=\"https://doi.org/10.1016/j.isci.2026.115192\">10.1016/j.isci.2026.115192</a>.","ieee":"S. Akther <i>et al.</i>, “Distribution and functional significance of rodent cerebellar glycogen,” <i>iScience</i>, vol. 29, no. 4. Elsevier, 2026.","ista":"Akther S, Lee AB, Konno A, Asiminas A, Vittani M, Mishima T, Hirai H, Meehan CF, Duran J, Guinovart J, Ashida H, Morita T, Baba O, Shigemoto R, Nedergaard M, Hirase H. 2026. Distribution and functional significance of rodent cerebellar glycogen. iScience. 29(4), 115192.","ama":"Akther S, Lee AB, Konno A, et al. Distribution and functional significance of rodent cerebellar glycogen. <i>iScience</i>. 2026;29(4). doi:<a href=\"https://doi.org/10.1016/j.isci.2026.115192\">10.1016/j.isci.2026.115192</a>"},"DOAJ_listed":"1","type":"journal_article","intvolume":"        29","publisher":"Elsevier","volume":29,"article_type":"original","title":"Distribution and functional significance of rodent cerebellar glycogen","external_id":{"pmid":["41890976"]},"publication":"iScience","year":"2026","OA_place":"publisher","department":[{"_id":"RySh"}],"article_processing_charge":"Yes","date_created":"2026-03-29T22:07:07Z","acknowledgement":"This work was supported by the Novo Nordisk Foundation (NNFOC0058058, H. Hirase), the Danmarks Frie Forskningsfond (0134-00107B and 5283-00069A, H.Hirase), the Lundbeck Foundation, Japan Society for the Promotion of Science Grants-in-Aid for Scientific Research (KAKENHI) program (22K06454/24H01221, A.K.; 23K27482, H.Hirai), the Japan Agency for Medical Research and Development (AMED) Brain Mapping by Integrated Neurotechnologies for Disease Studies (Brain/MINDS) (JP21dm0207111, H. Hirai), AMED Brain/MINDS 2.0 (JP23wm0625001 and JP24wm0625103, H. Hirai), and grants from the Spanish Ministerio de Ciencia e Innovación (MCIU/FEDER/AEI) (PID2020-118699 GB-100, J.D.) and the Fundación Ramón Areces (J.D.). Sonam Akther has been supported by the RIKEN IPA fellowship. We are thankful to Dr. Yuki Oe for his support in the initial stage of this study and to Dan Xue for his help with the graphical abstract. We thank Dr. Pia Weikop for providing CTN research infrastructure. The authors declare no competing financial interests.","publication_identifier":{"eissn":["2589-0042"]},"language":[{"iso":"eng"}],"oa":1,"date_updated":"2026-03-30T06:20:06Z","oa_version":"Published Version","issue":"4","day":"17","date_published":"2026-03-17T00:00:00Z","status":"public","publication_status":"epub_ahead","abstract":[{"text":"The mammalian brain stores glucose, the main circulating energy substrate, as glycogen. In rodents, the cerebellum contains relatively high glycogen levels, yet its cellular and subcellular distribution remains poorly defined. Using monoclonal antibodies against glycogen, we examined its distribution in the mouse cerebellar cortex. Glycogen was predominantly localized to Bergmann glia (BG) processes in the molecular layer and was also detected in Purkinje cells (PCs), the principal cerebellar neurons. To assess the functional significance of cerebellar glycogen, we analyzed behavior in mice lacking glycogen synthase 1 (Gys1) in BG or PCs using a floxed Gys1 line. Gys1 deficiency in either PCs or GFAP-positive cells reduced anxiety-like behavior, whereas combined deletion caused PC degeneration and ataxia. These findings reveal a critical role for glycogen metabolism in both astrocytes and neurons in cerebellar function.","lang":"eng"}],"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","doi":"10.1016/j.isci.2026.115192","pmid":1,"OA_type":"gold","month":"03","main_file_link":[{"open_access":"1","url":"https://doi.org/10.1016/j.isci.2026.115192"}]},{"status":"public","date_published":"2025-12-01T00:00:00Z","publication_status":"published","abstract":[{"lang":"eng","text":"Metabotropic GABA (GABAB) receptors have modulatory functions on neuronal excitability and\r\nneurotransmitter release. To fulfil these functions, GABAB receptors form macromolecular signaling complexes with G proteins, effectors, and other associated proteins. Here we investigated the postnatal development of GABAB receptors (GABAB1 and GABAB2 subunits) in mouse brain, focusing on potential similarities in the spatial and temporal expression pattern\r\nof their associated proteins CaV2.1, Gαo, Gβ5, and RGS7, using histoblots, immunofluorescence, and immunoelectron microscopic techniques. At all ages analyzed, histoblot showed that the six proteins were widely expressed in the brain, with mostly an\r\noverlapping pattern throughout postnatal development. In the hippocampus, immunoelectron microscopy and quantitative analysis of immunoparticles for GABAB1, GABAB2, Gαo, Gβ5, and RGS7 revealed their progressive enrichment around excitatory synapses on dendritic spines of CA1 pyramidal cells toward P15. At presynaptic sites, GABAB receptors colocalize with\r\nCaV2.1, Gαo, Gβ5, and RGS7 in the active zone and extrasynaptic membranes of axon terminals, establishing synapses on dendritic spines of CA1 pyramidal cells. In the cerebellum, double immunofluorescence at P7 and P10 revealed the colocalization of GABAB1 and CaV2.1\r\nin the whole dendritic tree of developing Purkinje cells. Immunoelectron microscopy at P15 showed that GABAB1, GABAB2, CaV2.1, Gαo, Gβ5, and RGS7 are distributed along the dendritic surface of Purkinje cells, enriched close to excitatory synapses in spines.\r\nAltogether, these data suggest that macromolecular complexes composed of GABAB1 /GABAB2/CaV2.1/ Gαo/Gβ5/RGS7 are pre-assembled during key stages of postnatal development in hippocampal and cerebellar neurons."}],"ddc":["570"],"doi":"10.14670/HH-18-970","pmid":1,"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","tmp":{"short":"CC BY (4.0)","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode"},"month":"12","OA_type":"gold","language":[{"iso":"eng"}],"oa":1,"issue":"12","date_updated":"2025-11-24T10:24:35Z","oa_version":"Published Version","file":[{"content_type":"application/pdf","relation":"main_file","date_updated":"2025-11-24T10:23:39Z","creator":"dernst","access_level":"open_access","success":1,"file_name":"2025_HistologyHistopathology_Aguado.pdf","file_size":18093266,"date_created":"2025-11-24T10:23:39Z","file_id":"20677","checksum":"779d67434400c0f94af42c35ba21c672"}],"day":"01","year":"2025","publication":"Histology and Histopathology","external_id":{"pmid":["40704638"]},"title":"Developmental regulation of GABAB receptors and downstream molecules in the mouse brain","article_type":"original","volume":40,"page":"1967-1984","OA_place":"publisher","department":[{"_id":"RySh"}],"publication_identifier":{"eissn":["1699-5848"]},"date_created":"2025-11-23T23:01:37Z","acknowledgement":"We thank Ms. Diane Latawiec for the English revision of the manuscript. Funding sources were the Spanish Ministerio de Economía y Competitividad, and Junta de Comunidades de CastillaLa Mancha (Spain). Grants PID2021-125875OB-I00 funded by MCIN/AEI/ 10.13039/501100011033 and “ERDF A way of making Europe” to RL. This work was also supported by Castilla-La Mancha Regional Government and the European Regional Development Fund (SBPLY/21/180501/000064) and the Universidad de Castilla-La Mancha (2023-GRIN-34187) to RL.","article_processing_charge":"Yes","author":[{"last_name":"Aguado","first_name":"Carolina","full_name":"Aguado, Carolina"},{"last_name":"Alfaro-Ruiz","first_name":"Rocío","full_name":"Alfaro-Ruiz, Rocío"},{"full_name":"Martínez-Poyato, María Llanos","first_name":"María Llanos","last_name":"Martínez-Poyato"},{"first_name":"Ana Esther","last_name":"Moreno-Martínez","full_name":"Moreno-Martínez, Ana Esther"},{"first_name":"Sebastián","last_name":"García-Madrona","full_name":"García-Madrona, Sebastián"},{"first_name":"Alberto","last_name":"Roldán-Sastre","full_name":"Roldán-Sastre, Alberto"},{"last_name":"Alonso-Gómez","first_name":"Pablo","full_name":"Alonso-Gómez, Pablo"},{"full_name":"Fernández, Miriam","first_name":"Miriam","last_name":"Fernández"},{"first_name":"Ricardo","last_name":"Puertas-Avendaño","full_name":"Puertas-Avendaño, Ricardo"},{"last_name":"Shigemoto","id":"499F3ABC-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0001-8761-9444","first_name":"Ryuichi","full_name":"Shigemoto, Ryuichi"},{"first_name":"Kirill A.","last_name":"Martemyanov","full_name":"Martemyanov, Kirill A."},{"first_name":"Rafael","last_name":"Luján","full_name":"Luján, Rafael"}],"file_date_updated":"2025-11-24T10:23:39Z","_id":"20659","citation":{"chicago":"Aguado, Carolina, Rocío Alfaro-Ruiz, María Llanos Martínez-Poyato, Ana Esther Moreno-Martínez, Sebastián García-Madrona, Alberto Roldán-Sastre, Pablo Alonso-Gómez, et al. “Developmental Regulation of GABAB Receptors and Downstream Molecules in the Mouse Brain.” <i>Histology and Histopathology</i>. Sercrisma International, 2025. <a href=\"https://doi.org/10.14670/HH-18-970\">https://doi.org/10.14670/HH-18-970</a>.","apa":"Aguado, C., Alfaro-Ruiz, R., Martínez-Poyato, M. L., Moreno-Martínez, A. E., García-Madrona, S., Roldán-Sastre, A., … Luján, R. (2025). Developmental regulation of GABAB receptors and downstream molecules in the mouse brain. <i>Histology and Histopathology</i>. Sercrisma International. <a href=\"https://doi.org/10.14670/HH-18-970\">https://doi.org/10.14670/HH-18-970</a>","short":"C. Aguado, R. Alfaro-Ruiz, M.L. Martínez-Poyato, A.E. Moreno-Martínez, S. García-Madrona, A. Roldán-Sastre, P. Alonso-Gómez, M. Fernández, R. Puertas-Avendaño, R. Shigemoto, K.A. Martemyanov, R. Luján, Histology and Histopathology 40 (2025) 1967–1984.","ama":"Aguado C, Alfaro-Ruiz R, Martínez-Poyato ML, et al. Developmental regulation of GABAB receptors and downstream molecules in the mouse brain. <i>Histology and Histopathology</i>. 2025;40(12):1967-1984. doi:<a href=\"https://doi.org/10.14670/HH-18-970\">10.14670/HH-18-970</a>","ieee":"C. Aguado <i>et al.</i>, “Developmental regulation of GABAB receptors and downstream molecules in the mouse brain,” <i>Histology and Histopathology</i>, vol. 40, no. 12. Sercrisma International, pp. 1967–1984, 2025.","ista":"Aguado C, Alfaro-Ruiz R, Martínez-Poyato ML, Moreno-Martínez AE, García-Madrona S, Roldán-Sastre A, Alonso-Gómez P, Fernández M, Puertas-Avendaño R, Shigemoto R, Martemyanov KA, Luján R. 2025. Developmental regulation of GABAB receptors and downstream molecules in the mouse brain. Histology and Histopathology. 40(12), 1967–1984.","mla":"Aguado, Carolina, et al. “Developmental Regulation of GABAB Receptors and Downstream Molecules in the Mouse Brain.” <i>Histology and Histopathology</i>, vol. 40, no. 12, Sercrisma International, 2025, pp. 1967–84, doi:<a href=\"https://doi.org/10.14670/HH-18-970\">10.14670/HH-18-970</a>."},"has_accepted_license":"1","scopus_import":"1","quality_controlled":"1","type":"journal_article","PlanS_conform":"1","publisher":"Sercrisma International","intvolume":"        40"},{"citation":{"ama":"Martín‐Belmonte A, Aguado C, Alfaro‐Ruiz R, et al. Nanoarchitecture of CaV&#62;2.1 channels and GABAB receptors in the mouse hippocampus: Impact of APP/PS1 pathology. <i>Brain Pathology</i>. 2025;35(2). doi:<a href=\"https://doi.org/10.1111/bpa.13279\">10.1111/bpa.13279</a>","ista":"Martín‐Belmonte A, Aguado C, Alfaro‐Ruiz R, Kulik A, de la Ossa L, Moreno‐Martínez AE, Alberquilla S, García‐Carracedo L, Fernández M, Fajardo‐Serrano A, Aso E, Shigemoto R, Martín ED, Fukazawa Y, Ciruela F, Luján R. 2025. Nanoarchitecture of CaV&#62;2.1 channels and GABAB receptors in the mouse hippocampus: Impact of APP/PS1 pathology. Brain Pathology. 35(2), e13279.","mla":"Martín‐Belmonte, Alejandro, et al. “Nanoarchitecture of CaV&#62;2.1 Channels and GABAB Receptors in the Mouse Hippocampus: Impact of APP/PS1 Pathology.” <i>Brain Pathology</i>, vol. 35, no. 2, e13279, Wiley, 2025, doi:<a href=\"https://doi.org/10.1111/bpa.13279\">10.1111/bpa.13279</a>.","ieee":"A. Martín‐Belmonte <i>et al.</i>, “Nanoarchitecture of CaV&#62;2.1 channels and GABAB receptors in the mouse hippocampus: Impact of APP/PS1 pathology,” <i>Brain Pathology</i>, vol. 35, no. 2. Wiley, 2025.","chicago":"Martín‐Belmonte, Alejandro, Carolina Aguado, Rocío Alfaro‐Ruiz, Akos Kulik, Luis de la Ossa, Ana Esther Moreno‐Martínez, Samuel Alberquilla, et al. “Nanoarchitecture of CaV&#62;2.1 Channels and GABAB Receptors in the Mouse Hippocampus: Impact of APP/PS1 Pathology.” <i>Brain Pathology</i>. Wiley, 2025. <a href=\"https://doi.org/10.1111/bpa.13279\">https://doi.org/10.1111/bpa.13279</a>.","short":"A. Martín‐Belmonte, C. Aguado, R. Alfaro‐Ruiz, A. Kulik, L. de la Ossa, A.E. Moreno‐Martínez, S. Alberquilla, L. García‐Carracedo, M. Fernández, A. Fajardo‐Serrano, E. Aso, R. Shigemoto, E.D. Martín, Y. Fukazawa, F. Ciruela, R. Luján, Brain Pathology 35 (2025).","apa":"Martín‐Belmonte, A., Aguado, C., Alfaro‐Ruiz, R., Kulik, A., de la Ossa, L., Moreno‐Martínez, A. E., … Luján, R. (2025). Nanoarchitecture of CaV&#62;2.1 channels and GABAB receptors in the mouse hippocampus: Impact of APP/PS1 pathology. <i>Brain Pathology</i>. Wiley. <a href=\"https://doi.org/10.1111/bpa.13279\">https://doi.org/10.1111/bpa.13279</a>"},"has_accepted_license":"1","article_number":"e13279","quality_controlled":"1","scopus_import":"1","author":[{"last_name":"Martín‐Belmonte","first_name":"Alejandro","full_name":"Martín‐Belmonte, Alejandro"},{"full_name":"Aguado, Carolina","first_name":"Carolina","last_name":"Aguado"},{"first_name":"Rocío","last_name":"Alfaro‐Ruiz","full_name":"Alfaro‐Ruiz, Rocío"},{"first_name":"Akos","last_name":"Kulik","full_name":"Kulik, Akos"},{"first_name":"Luis","last_name":"de la Ossa","full_name":"de la Ossa, Luis"},{"full_name":"Moreno‐Martínez, Ana Esther","last_name":"Moreno‐Martínez","first_name":"Ana Esther"},{"full_name":"Alberquilla, Samuel","first_name":"Samuel","last_name":"Alberquilla"},{"full_name":"García‐Carracedo, Lucía","last_name":"García‐Carracedo","first_name":"Lucía"},{"first_name":"Miriam","last_name":"Fernández","full_name":"Fernández, Miriam"},{"first_name":"Ana","last_name":"Fajardo‐Serrano","full_name":"Fajardo‐Serrano, Ana"},{"full_name":"Aso, Ester","first_name":"Ester","last_name":"Aso"},{"full_name":"Shigemoto, Ryuichi","id":"499F3ABC-F248-11E8-B48F-1D18A9856A87","last_name":"Shigemoto","orcid":"0000-0001-8761-9444","first_name":"Ryuichi"},{"full_name":"Martín, Eduardo D.","first_name":"Eduardo D.","last_name":"Martín"},{"last_name":"Fukazawa","first_name":"Yugo","full_name":"Fukazawa, Yugo"},{"last_name":"Ciruela","first_name":"Francisco","full_name":"Ciruela, Francisco"},{"full_name":"Luján, Rafael","first_name":"Rafael","last_name":"Luján"}],"file_date_updated":"2025-04-16T09:56:08Z","_id":"17293","publisher":"Wiley","intvolume":"        35","type":"journal_article","DOAJ_listed":"1","isi":1,"OA_place":"publisher","year":"2025","publication":"Brain Pathology","external_id":{"isi":["001250034200001"],"pmid":["38887180"]},"article_type":"original","title":"Nanoarchitecture of CaV>2.1 channels and GABAB receptors in the mouse hippocampus: Impact of APP/PS1 pathology","volume":35,"publication_identifier":{"issn":["1015-6305"],"eissn":["1750-3639"]},"date_created":"2024-07-22T07:48:20Z","acknowledgement":"Funding sources were Spanish Ministerio de Economía y Competitividad, Junta de Comunidades de Castilla-La Mancha (Spain), Life Science Innovation Center at University of Fukui and German Research Foundation.\r\nGrants RTI2018-095812-B-I00 and PID2021-125875OB-I00 funded by MCIN/AEI/10.13039/501100011033 and by “ERDF A way of making Europe” to Rafael Luján. This study was also supported by a grant from Junta de Comunidades de Castilla-La Mancha (SBPLY/17/180501/000229 and SBPLY/21/180501/000064) and Universidad de Castilla-La Mancha (2023-GRIN-34187) to Rafael Luján, and Life Science Innovation Center (Research and Education Program for Life Science) at University of Fukui and JSPS KAKENHI Grant Numbers 16H04662, 17K19446, 18H05120 to Yugo Fukazawa and Margarita Salas fellowship from Ministerio de Universidades and Universidad de Castilla-La Mancha to Alejandro Martín-Belmonte. German Research Foundation (DFG FOR 2143) and BIOSS-2 to Akos Kulik.","article_processing_charge":"Yes","department":[{"_id":"RySh"}],"issue":"2","oa_version":"Published Version","date_updated":"2025-05-19T13:58:12Z","oa":1,"language":[{"iso":"eng"}],"day":"01","file":[{"checksum":"75a172800ab2e949abb66fba97cf70f0","date_created":"2025-04-16T09:56:08Z","file_id":"19582","success":1,"file_name":"2025_BrainPathology_MartinBelmonte.pdf","file_size":8767863,"creator":"dernst","access_level":"open_access","date_updated":"2025-04-16T09:56:08Z","content_type":"application/pdf","relation":"main_file"}],"license":"https://creativecommons.org/licenses/by-nc-nd/4.0/","publication_status":"published","abstract":[{"text":"Voltage-gated CaV2.1 (P/Q-type) Ca2+ channels play a crucial role in regulating neurotransmitter release, thus contributing to synaptic plasticity and to processes such as learning and memory. Despite their recognized importance in neural function, there is limited information on their potential involvement in neurodegenerative conditions such as Alzheimer's disease (AD). Here, we aimed to explore the impact of AD pathology on the density and nanoscale compartmentalization of CaV2.1 channels in the hippocampus in association with GABAB receptors. Histoblotting experiments showed that the density of CaV2.1 channel was significantly reduced in the hippocampus of APP/PS1 mice in a laminar-dependent manner. CaV2.1 channel was enriched in the active zone of the axon terminals and was present at a very low density over the surface of dendritic tree of the CA1 pyramidal cells, as shown by quantitative SDS-digested freeze-fracture replica labelling (SDS-FRL). In APP/PS1 mice, the density of CaV2.1 channel in the active zone was significantly reduced in the strata radiatum and lacunosum-moleculare, while it remained unaltered in the stratum oriens. The decline in Cav2.1 channel density was found to be associated with a corresponding impairment in the GABAergic synaptic function, as evidenced by electrophysiological experiments carried out in the hippocampus of APP/PS1 mice. Remarkably, double SDS-FRL showed a co-clustering of CaV2.1 channel and GABAB1 receptor in nanodomains (~40–50 nm) in wild type mice, while in APP/PS1 mice this nanoarchitecture was absent. Together, these findings suggest that the AD pathology-induced reduction in CaV2.1 channel density and CaV2.1-GABAB1 de-clustering may play a role in the synaptic transmission alterations shown in the AD hippocampus. Therefore, uncovering these layer-dependent changes in P/Q calcium currents associated with AD pathology can benefit the development of future strategies for AD management.","lang":"eng"}],"ddc":["570"],"status":"public","date_published":"2025-03-01T00:00:00Z","tmp":{"name":"Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0)","legal_code_url":"https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode","short":"CC BY-NC-ND (4.0)","image":"/images/cc_by_nc_nd.png"},"OA_type":"gold","month":"03","pmid":1,"doi":"10.1111/bpa.13279","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87"},{"degree_awarded":"PhD","OA_place":"publisher","related_material":{"record":[{"relation":"part_of_dissertation","id":"9437","status":"public"},{"relation":"part_of_dissertation","status":"public","id":"15084"}]},"title":"Asymmetrical modulation of fear expression via GABAB receptors in the mouse medial habenula","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"},{"call_identifier":"H2020","grant_number":"665385","name":"International IST Doctoral Program","_id":"2564DBCA-B435-11E9-9278-68D0E5697425"}],"year":"2025","article_processing_charge":"No","acknowledgement":"I would like to thank the European Research Council and European Commission, under the European Union’s Horizon 2020 research and innovation program (ERC grant agreement no. 694539 to Ryuichi Shigemoto and the Marie Skłodowska-Curie grant agreement no. 665385 to Cihan Önal), and the Austrian Neuroscience Association for providing financial support and opportunities, which were important in allowing me to present my work. I also wish to thank the\r\nPreclinical Facility, especially Michael Schunn, for always welcoming me from my earliest days as an intern. My gratitude goes as well to the Miba Machine Shop, in particular Todor Asenov, Astrit Arslani, and Thomas Menner, whose technical expertise often saved the day.","date_created":"2025-02-28T14:15:53Z","acknowledged_ssus":[{"_id":"PreCl"},{"_id":"M-Shop"}],"publication_identifier":{"eissn":["2663-337X"]},"department":[{"_id":"GradSch"},{"_id":"RySh"}],"has_accepted_license":"1","citation":{"short":"C. Önal, Asymmetrical Modulation of Fear Expression via GABAB Receptors in the Mouse Medial Habenula, Institute of Science and Technology Austria, 2025.","apa":"Önal, C. (2025). <i>Asymmetrical modulation of fear expression via GABAB receptors in the mouse medial habenula</i>. Institute of Science and Technology Austria. <a href=\"https://doi.org/10.15479/AT-ISTA-19271\">https://doi.org/10.15479/AT-ISTA-19271</a>","chicago":"Önal, Cihan. “Asymmetrical Modulation of Fear Expression via GABAB Receptors in the Mouse Medial Habenula.” Institute of Science and Technology Austria, 2025. <a href=\"https://doi.org/10.15479/AT-ISTA-19271\">https://doi.org/10.15479/AT-ISTA-19271</a>.","mla":"Önal, Cihan. <i>Asymmetrical Modulation of Fear Expression via GABAB Receptors in the Mouse Medial Habenula</i>. Institute of Science and Technology Austria, 2025, doi:<a href=\"https://doi.org/10.15479/AT-ISTA-19271\">10.15479/AT-ISTA-19271</a>.","ieee":"C. Önal, “Asymmetrical modulation of fear expression via GABAB receptors in the mouse medial habenula,” Institute of Science and Technology Austria, 2025.","ista":"Önal C. 2025. Asymmetrical modulation of fear expression via GABAB receptors in the mouse medial habenula. Institute of Science and Technology Austria.","ama":"Önal C. Asymmetrical modulation of fear expression via GABAB receptors in the mouse medial habenula. 2025. doi:<a href=\"https://doi.org/10.15479/AT-ISTA-19271\">10.15479/AT-ISTA-19271</a>"},"file_date_updated":"2026-02-01T23:30:02Z","_id":"19271","author":[{"full_name":"Önal, Hüseyin C","last_name":"Önal","id":"4659D740-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0002-2771-2011","first_name":"Hüseyin C"}],"publisher":"Institute of Science and Technology Austria","type":"dissertation","ddc":["570","571","573","599"],"publication_status":"published","abstract":[{"lang":"eng","text":"The medial habenula (MHb) is implicated in regulating emotional responses\r\nto aversive events. Studies in zebrafish have identified a remarkable morphological\r\nleft-right asymmetry in the dorsal habenula (zebrafish equivalent of mammalian\r\nMHb)-to-interpeduncular nucleus (IPN) pathway and its left-side specific role in\r\nmodulating fear responses. However, there is little evidence for structural or\r\nfunctional lateralization in the mammalian MHb-IPN pathway.\r\nHere, I investigated the synaptic properties of the left and right MHb\r\nafferents to the IPN in mice and addressed whether these synaptic connections\r\nselectively influence the expression of conditioned fear in mice. My findings reveal\r\nthat each individual IPN neuron receives inputs from both left and right MHb.\r\nElectrophysiological recordings from the same postsynaptic IPN neurons\r\ndemonstrate that the left MHb-originating synapses exhibit lower release\r\nprobability and higher 𝛾-aminobutyric acid type B receptor (GABABR)-mediated\r\npotentiation compared to the right MHb-originating synapses. Interestingly,\r\nchemogenetic inhibition of cholinergic neurons in the left but not the right MHb\r\nsignificantly attenuated cue-dependent fear recall. Furthermore, conditional\r\ndeletion of GABABR in the left MHb interfered with the recall of cued fear memory,\r\nwhereas that in the right MHb neurons spared fear memory expression.\r\nCollectively, I demonstrate a functional asymmetry of the MHb in mice,\r\nrevealing a predominant role for GABABR-mediated signaling in the left MHb-IPN\r\npathway in the modulation of fear memories. These findings suggest that\r\nlateralized pathways could represent a fundamental principle in the neural\r\nregulation of emotion across species."}],"date_published":"2025-03-04T00:00:00Z","status":"public","month":"03","tmp":{"name":"Creative Commons Attribution-NonCommercial 4.0 International (CC BY-NC 4.0)","legal_code_url":"https://creativecommons.org/licenses/by-nc/4.0/legalcode","short":"CC BY-NC (4.0)","image":"/images/cc_by_nc.png"},"user_id":"ba8df636-2132-11f1-aed0-ed93e2281fdd","doi":"10.15479/AT-ISTA-19271","supervisor":[{"full_name":"Shigemoto, Ryuichi","first_name":"Ryuichi","last_name":"Shigemoto","id":"499F3ABC-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0001-8761-9444"}],"alternative_title":["ISTA Thesis"],"date_updated":"2026-04-07T12:40:42Z","oa_version":"Published Version","language":[{"iso":"eng"}],"ec_funded":1,"oa":1,"day":"04","corr_author":"1","license":"https://creativecommons.org/licenses/by-nc/4.0/","file":[{"date_updated":"2026-02-01T23:30:02Z","access_level":"closed","creator":"hoenal","relation":"source_file","embargo_to":"open_access","content_type":"application/vnd.openxmlformats-officedocument.wordprocessingml.document","file_id":"19272","date_created":"2025-02-28T13:57:01Z","checksum":"c1a4d75a7471de9f954697b06cd18d28","file_size":25869143,"file_name":"Cihan_Onal_Thesis_Final.docx"},{"date_updated":"2026-02-01T23:30:02Z","embargo":"2026-02-01","access_level":"open_access","creator":"hoenal","relation":"main_file","content_type":"application/pdf","file_id":"19273","date_created":"2025-02-28T13:57:04Z","checksum":"de4e62147ab9f04098dc8cd898c630da","file_name":"Cihan_Onal_Thesis_Final_pdfa.pdf","file_size":12077596}]},{"_id":"18052","author":[{"id":"42E121A4-F248-11E8-B48F-1D18A9856A87","last_name":"Kleindienst","first_name":"David","full_name":"Kleindienst, David"},{"id":"D93824F4-D9BA-11E9-BB12-F207E6697425","last_name":"Costanzo","orcid":"0000-0001-9732-3815","first_name":"Tommaso","full_name":"Costanzo, Tommaso"},{"last_name":"Shigemoto","id":"499F3ABC-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0001-8761-9444","first_name":"Ryuichi","full_name":"Shigemoto, Ryuichi"}],"scopus_import":"1","quality_controlled":"1","citation":{"ista":"Kleindienst D, Costanzo T, Shigemoto R. 2024.Automated Imaging and Analysis of Synapses in Freeze-Fracture Replica Samples with Deep Learning. In: New Aspects in Analyzing the Synaptic Organization of the Brain. Neuromethods, , 123–137.","ieee":"D. Kleindienst, T. Costanzo, and R. Shigemoto, “Automated Imaging and Analysis of Synapses in Freeze-Fracture Replica Samples with Deep Learning,” in <i>New Aspects in Analyzing the Synaptic Organization of the Brain</i>, 1st ed., J. H. R. Lübke and A. Rollenhagen, Eds. New York: Springer Nature, 2024, pp. 123–137.","mla":"Kleindienst, David, et al. “Automated Imaging and Analysis of Synapses in Freeze-Fracture Replica Samples with Deep Learning.” <i>New Aspects in Analyzing the Synaptic Organization of the Brain</i>, edited by Joachim H.R.  Lübke and Astrid Rollenhagen, 1st ed., Springer Nature, 2024, pp. 123–37, doi:<a href=\"https://doi.org/10.1007/978-1-0716-4019-7_8\">10.1007/978-1-0716-4019-7_8</a>.","ama":"Kleindienst D, Costanzo T, Shigemoto R. Automated Imaging and Analysis of Synapses in Freeze-Fracture Replica Samples with Deep Learning. In: Lübke JHR, Rollenhagen A, eds. <i>New Aspects in Analyzing the Synaptic Organization of the Brain</i>. 1st ed. New York: Springer Nature; 2024:123-137. doi:<a href=\"https://doi.org/10.1007/978-1-0716-4019-7_8\">10.1007/978-1-0716-4019-7_8</a>","short":"D. Kleindienst, T. Costanzo, R. Shigemoto, in:, J.H.R. Lübke, A. Rollenhagen (Eds.), New Aspects in Analyzing the Synaptic Organization of the Brain, 1st ed., Springer Nature, New York, 2024, pp. 123–137.","apa":"Kleindienst, D., Costanzo, T., &#38; Shigemoto, R. (2024). Automated Imaging and Analysis of Synapses in Freeze-Fracture Replica Samples with Deep Learning. In J. H. R. Lübke &#38; A. Rollenhagen (Eds.), <i>New Aspects in Analyzing the Synaptic Organization of the Brain</i> (1st ed., pp. 123–137). New York: Springer Nature. <a href=\"https://doi.org/10.1007/978-1-0716-4019-7_8\">https://doi.org/10.1007/978-1-0716-4019-7_8</a>","chicago":"Kleindienst, David, Tommaso Costanzo, and Ryuichi Shigemoto. “Automated Imaging and Analysis of Synapses in Freeze-Fracture Replica Samples with Deep Learning.” In <i>New Aspects in Analyzing the Synaptic Organization of the Brain</i>, edited by Joachim H.R.  Lübke and Astrid Rollenhagen, 1st ed., 123–37. New York: Springer Nature, 2024. <a href=\"https://doi.org/10.1007/978-1-0716-4019-7_8\">https://doi.org/10.1007/978-1-0716-4019-7_8</a>."},"type":"book_chapter","editor":[{"full_name":"Lübke, Joachim H.R. ","last_name":"Lübke","first_name":"Joachim H.R. "},{"last_name":"Rollenhagen","first_name":"Astrid","full_name":"Rollenhagen, Astrid"}],"publisher":"Springer Nature","title":"Automated Imaging and Analysis of Synapses in Freeze-Fracture Replica Samples with Deep Learning","project":[{"grant_number":"694539","call_identifier":"H2020","name":"In situ analysis of single channel subunit composition in neurons: physiological implication in synaptic plasticity and behaviour","_id":"25CA28EA-B435-11E9-9278-68D0E5697425"}],"publication":"New Aspects in Analyzing the Synaptic Organization of the Brain","year":"2024","place":"New York","page":"123-137","department":[{"_id":"EM-Fac"},{"_id":"RySh"}],"article_processing_charge":"No","acknowledgement":"This research was supported by the European Research Council Advanced Grant 694539 to RS and by the Scientific Service Units of IST Austria through resources provided by the Electron Microscopy Facility.","date_created":"2024-09-10T12:32:38Z","publication_identifier":{"eissn":["1940-6045"],"issn":["0893-2336"],"eisbn":["9781071640197"],"isbn":["9781071640180"]},"acknowledged_ssus":[{"_id":"EM-Fac"}],"language":[{"iso":"eng"}],"ec_funded":1,"alternative_title":["Neuromethods"],"date_updated":"2025-04-14T07:27:15Z","oa_version":"None","corr_author":"1","edition":"1","day":"27","date_published":"2024-08-27T00:00:00Z","status":"public","publication_status":"published","abstract":[{"text":"Sodium dodecyl sulfate-digested freeze-fracture replica labeling (SDS-FRL) is an electron microscope (EM) sample preparation technique which allows for high-resolution visualization of membrane proteins with high sensitivity. However, image acquisition of specific replica profiles such as synapses in a large field of EM view needs a valid experience and a long time for manual searching. Here, we describe how to utilize deep learning for automatizing image acquisition of specific profiles of interest in replica samples. This protocol facilitates the labor-intensive collection of EM images, in particular for rare profiles. We provide instructions for using SerialEM image acquisition software in conjunction with object detection by our newly developed deep learning software DarEM, to automatically acquire tilt series of all synapses in a selected region. We then show how to perform a mostly automated analysis of gold particle labeling in the acquired images by utilizing Darea software.","lang":"eng"}],"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","doi":"10.1007/978-1-0716-4019-7_8","month":"08"},{"day":"05","file":[{"creator":"dernst","access_level":"open_access","date_updated":"2024-10-21T12:15:38Z","content_type":"application/pdf","relation":"main_file","checksum":"03d6dd1b84efa24e9e9ede748d08764d","date_created":"2024-10-21T12:15:38Z","file_id":"18460","success":1,"file_size":7215329,"file_name":"2024_NatureComm_Zupancic.pdf"}],"oa_version":"Published Version","date_updated":"2025-09-08T14:25:06Z","language":[{"iso":"eng"}],"oa":1,"month":"10","OA_type":"gold","tmp":{"short":"CC BY (4.0)","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode"},"user_id":"317138e5-6ab7-11ef-aa6d-ffef3953e345","pmid":1,"doi":"10.1038/s41467-024-52762-z","ddc":["570"],"abstract":[{"lang":"eng","text":"Acquisition of specialized cellular features is controlled by the ordered expression of transcription factors (TFs) along differentiation trajectories. Here, we find a member of the Onecut TF family, ONECUT3, expressed in postmitotic neurons that leave their Ascl1+/Onecut1/2+ proliferative domain in the vertebrate hypothalamus to instruct neuronal differentiation. We combined single-cell RNA-seq and gain-of-function experiments for gene network reconstruction to show that ONECUT3 affects the polarization and morphogenesis of both hypothalamic GABA-derived dopamine and thyrotropin-releasing hormone (TRH)+ glutamate neurons through neuron navigator-2 (NAV2). In vivo, siRNA-mediated knockdown of ONECUT3 in neonatal mice reduced NAV2 mRNA, as well as neurite complexity in Onecut3-containing neurons, while genetic deletion of Onecut3/ceh-48 in C. elegans impaired neurocircuit wiring, and sensory discrimination-based behaviors. Thus, ONECUT3, conserved across neuronal subtypes and many species, underpins the polarization and morphological plasticity of phenotypically distinct neurons that descend from a common pool of Ascl1+ progenitors in the hypothalamus."}],"publication_status":"published","status":"public","date_published":"2024-10-05T00:00:00Z","PlanS_conform":"1","publisher":"Springer Nature","intvolume":"        15","isi":1,"DOAJ_listed":"1","type":"journal_article","citation":{"chicago":"Zupančič, Maja, Erik Keimpema, Evgenii O. Tretiakov, Stephanie J. Eder, Itamar Lev, Lukas Englmaier, Pradeep Bhandari, et al. “Concerted Transcriptional Regulation of the Morphogenesis of Hypothalamic Neurons by ONECUT3.” <i>Nature Communications</i>. Springer Nature, 2024. <a href=\"https://doi.org/10.1038/s41467-024-52762-z\">https://doi.org/10.1038/s41467-024-52762-z</a>.","short":"M. Zupančič, E. Keimpema, E.O. Tretiakov, S.J. Eder, I. Lev, L. Englmaier, P. Bhandari, S.A. Fietz, W. Härtig, E. Renaux, A. Villunger, T. Hökfelt, M. Zimmer, F. Clotman, T. Harkany, Nature Communications 15 (2024).","apa":"Zupančič, M., Keimpema, E., Tretiakov, E. O., Eder, S. J., Lev, I., Englmaier, L., … Harkany, T. (2024). Concerted transcriptional regulation of the morphogenesis of hypothalamic neurons by ONECUT3. <i>Nature Communications</i>. Springer Nature. <a href=\"https://doi.org/10.1038/s41467-024-52762-z\">https://doi.org/10.1038/s41467-024-52762-z</a>","ama":"Zupančič M, Keimpema E, Tretiakov EO, et al. Concerted transcriptional regulation of the morphogenesis of hypothalamic neurons by ONECUT3. <i>Nature Communications</i>. 2024;15. doi:<a href=\"https://doi.org/10.1038/s41467-024-52762-z\">10.1038/s41467-024-52762-z</a>","mla":"Zupančič, Maja, et al. “Concerted Transcriptional Regulation of the Morphogenesis of Hypothalamic Neurons by ONECUT3.” <i>Nature Communications</i>, vol. 15, 8631, Springer Nature, 2024, doi:<a href=\"https://doi.org/10.1038/s41467-024-52762-z\">10.1038/s41467-024-52762-z</a>.","ista":"Zupančič M, Keimpema E, Tretiakov EO, Eder SJ, Lev I, Englmaier L, Bhandari P, Fietz SA, Härtig W, Renaux E, Villunger A, Hökfelt T, Zimmer M, Clotman F, Harkany T. 2024. Concerted transcriptional regulation of the morphogenesis of hypothalamic neurons by ONECUT3. Nature Communications. 15, 8631.","ieee":"M. Zupančič <i>et al.</i>, “Concerted transcriptional regulation of the morphogenesis of hypothalamic neurons by ONECUT3,” <i>Nature Communications</i>, vol. 15. Springer Nature, 2024."},"scopus_import":"1","quality_controlled":"1","article_number":"8631","has_accepted_license":"1","file_date_updated":"2024-10-21T12:15:38Z","_id":"18445","author":[{"full_name":"Zupančič, Maja","last_name":"Zupančič","first_name":"Maja"},{"first_name":"Erik","last_name":"Keimpema","full_name":"Keimpema, Erik"},{"first_name":"Evgenii O.","last_name":"Tretiakov","full_name":"Tretiakov, Evgenii O."},{"full_name":"Eder, Stephanie J.","last_name":"Eder","first_name":"Stephanie J."},{"full_name":"Lev, Itamar","first_name":"Itamar","last_name":"Lev"},{"full_name":"Englmaier, Lukas","last_name":"Englmaier","first_name":"Lukas"},{"last_name":"Bhandari","id":"45EDD1BC-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0003-0863-4481","first_name":"Pradeep","full_name":"Bhandari, Pradeep"},{"last_name":"Fietz","first_name":"Simone A.","full_name":"Fietz, Simone A."},{"full_name":"Härtig, Wolfgang","last_name":"Härtig","first_name":"Wolfgang"},{"full_name":"Renaux, Estelle","first_name":"Estelle","last_name":"Renaux"},{"full_name":"Villunger, Andreas","first_name":"Andreas","last_name":"Villunger"},{"last_name":"Hökfelt","first_name":"Tomas","full_name":"Hökfelt, Tomas"},{"full_name":"Zimmer, Manuel","last_name":"Zimmer","first_name":"Manuel"},{"last_name":"Clotman","first_name":"Frédéric","full_name":"Clotman, Frédéric"},{"last_name":"Harkany","first_name":"Tibor","full_name":"Harkany, Tibor"}],"publication_identifier":{"eissn":["2041-1723"]},"article_processing_charge":"Yes (via OA deal)","acknowledgement":"The authors thank Z. Máté, G. Szabó, and F. Erdélyi for the custom generation of transgenic mouse lines, C. Fekete for Trh transgenic tissues (all from the Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, Hungary), A. Goudmaeker for IVF recovery of a frozen mouse line (SSS animal facility, Université catholique de Louvain), and Y. Yanagawa (Department of Genetic and Behavioral Neuroscience, Gunma University Graduate School of Medicine, Maebashi, Japan) for providing GAD67gfp/+ mice. We also thank S. Cloer, D. Preininger, and A. Weissenbacher (Tiergarten Schönbrunn, Vienna, Austria) for providing naked mole rats, Seba’s fruit bats, and Indian flying foxes, as well as F. Aujard (CNRS, UMR 7179 ‘Adaptive mechanisms and evolution’, France) for Microcebus tissues. I. Milenkovic and G.G. Kovács (Clinical Institute of Neurology, Medical University of Vienna, Vienna, Austria) are acknowledged for providing post-mortem human brain samples. We are indebted to S. Rehman (Medical University of Vienna), M. Kalusa (University of Leipzig, Leipzig, Germany), and W. Reimann (Paul Flechsig Institute for Brain Research, Leipzig, Germany) for their technical assistance. C. elegans strains were provided by the National Bioresource Project for the nematode, Japan, and the CGC, with the latter being funded by the NIH Office of Research Infrastructure Programs (P40 OD010440). This work was supported by the Austrian Science Fund (FWF, P 34121-B; to E.K.), the Swedish Research Council (2023-03058, T.Ha; 2020-01688, T.Hö.), the Swedish Brain Foundation (Hjärnfonden, FO2022-0300, to T.Ha.), the Novo Nordisk Foundation (NNF23OC0084476, to T.Ha.), the European Research Council (FOODFORLIFE, ERC-2020-AdG-101021016; to T.Ha.), the Université Catholique de Louvain (‘Fonds spéciaux de recherche’-FSR, to F.C.), and Fonds de la Recherche Scientifique F.R.S.-FNRS (‘Project de recherche (PDR)’ #T.0039.21, to F.C.). S.J.E. is supported by the Simons Foundation #543069. I.L. is supported by a post-doctoral fellowship from the Human Frontiers Science Program (LT000335/2020-L). E.R. holds a PhD grant from the FRIA (F.R.S.-FNRS, Belgium). F.C. is a Research Director of the F.R.S.-FNRS (Belgium).\r\nOpen access funding provided by Karolinska Institute.","date_created":"2024-10-20T22:02:05Z","department":[{"_id":"RySh"}],"OA_place":"publisher","publication":"Nature Communications","year":"2024","volume":15,"title":"Concerted transcriptional regulation of the morphogenesis of hypothalamic neurons by ONECUT3","article_type":"original","external_id":{"isi":["001409493300014"],"pmid":["39366958"]}},{"status":"public","year":"2024","title":"Shared behavioural impairments in visual perception and place avoidance across different autism models are driven by periaqueductal grey hypoexcitability in Setd5 haploinsufficient mice","date_published":"2024-05-15T00:00:00Z","related_material":{"record":[{"relation":"used_in_publication","id":"17142","status":"public"}]},"abstract":[{"text":"Relevant information about the data can be found in the 'Readme_Data.txt' file. \r\nA previous version of the publication can be found on BioRxiv: https://www.biorxiv.org/content/10.1101/2022.10.11.511691v4\r\nand published in Plos Biology (2024)","lang":"eng"}],"ddc":["570"],"doi":"10.15479/AT:ISTA:15385","department":[{"_id":"MaJö"},{"_id":"PreCl"},{"_id":"SiHi"},{"_id":"RySh"},{"_id":"GaNo"}],"user_id":"68b8ca59-c5b3-11ee-8790-cd641c68093d","acknowledged_ssus":[{"_id":"PreCl"},{"_id":"M-Shop"},{"_id":"LifeSc"},{"_id":"Bio"}],"tmp":{"name":"Creative Commons Attribution-NonCommercial 4.0 International (CC BY-NC 4.0)","legal_code_url":"https://creativecommons.org/licenses/by-nc/4.0/legalcode","short":"CC BY-NC (4.0)","image":"/images/cc_by_nc.png"},"acknowledgement":"We thank Armel Nicolas, Bella Bruszel and Ewelina Dutkiewicz from the ISTA Mass Spectrometry Service (Lab Services Facilities) for all Proteomics work, including samples preparation, LC/MS data acquisition, searches and data evaluation. We thank Prof. Peter Jonas for his suggestion on the involvement of potassium channels and members of the Neuroethology group for their comments on the manuscript. Katalin Szigeti and Julie Murmann for experimental help. This research was supported by the Scientific Service Units of ISTA through resources provided by the Lab Support Facility, the Imaging and Optics Facility, the Machine Shop Unit and the Preclinical Facility, especially Freyja Langer and Michael Schunn. ","date_created":"2024-05-13T15:04:04Z","month":"05","article_processing_charge":"No","author":[{"full_name":"Burnett, Laura","orcid":"0000-0002-8937-410X","id":"3B717F68-F248-11E8-B48F-1D18A9856A87","last_name":"Burnett","first_name":"Laura"},{"full_name":"Koppensteiner, Peter","orcid":"0000-0002-3509-1948","id":"3B8B25A8-F248-11E8-B48F-1D18A9856A87","last_name":"Koppensteiner","first_name":"Peter"},{"orcid":"0000-0003-2012-9947","last_name":"Symonova","id":"3C0C7BC6-F248-11E8-B48F-1D18A9856A87","first_name":"Olga","full_name":"Symonova, Olga"},{"first_name":"Tomas","orcid":"0000-0002-2634-6283","last_name":"Masson","id":"93ac43e8-8599-11eb-9b86-f6efb0a4c207","full_name":"Masson, Tomas"},{"last_name":"Vega Zuniga","id":"2E7C4E78-F248-11E8-B48F-1D18A9856A87","first_name":"Tomas A","full_name":"Vega Zuniga, Tomas A"},{"full_name":"Contreras, Ximena","first_name":"Ximena","last_name":"Contreras","id":"475990FE-F248-11E8-B48F-1D18A9856A87"},{"last_name":"Rülicke","first_name":"Thomas","full_name":"Rülicke, Thomas"},{"first_name":"Ryuichi","id":"499F3ABC-F248-11E8-B48F-1D18A9856A87","last_name":"Shigemoto","orcid":"0000-0001-8761-9444","full_name":"Shigemoto, Ryuichi"},{"first_name":"Gaia","orcid":"0000-0002-7673-7178","id":"3E57A680-F248-11E8-B48F-1D18A9856A87","last_name":"Novarino","full_name":"Novarino, Gaia"},{"orcid":"0000-0002-3937-1330","last_name":"Jösch","id":"2BD278E6-F248-11E8-B48F-1D18A9856A87","first_name":"Maximilian A","full_name":"Jösch, Maximilian A"}],"_id":"15385","file_date_updated":"2024-05-16T09:08:20Z","oa":1,"citation":{"apa":"Burnett, L., Koppensteiner, P., Symonova, O., Masson, T., Vega Zuniga, T. A., Contreras, X., … Jösch, M. A. (2024). Shared behavioural impairments in visual perception and place avoidance across different autism models are driven by periaqueductal grey hypoexcitability in Setd5 haploinsufficient mice. Institute of Science and Technology Austria. <a href=\"https://doi.org/10.15479/AT:ISTA:15385\">https://doi.org/10.15479/AT:ISTA:15385</a>","short":"L. Burnett, P. Koppensteiner, O. Symonova, T. Masson, T.A. Vega Zuniga, X. Contreras, T. Rülicke, R. Shigemoto, G. Novarino, M.A. Jösch, (2024).","chicago":"Burnett, Laura, Peter Koppensteiner, Olga Symonova, Tomas Masson, Tomas A Vega Zuniga, Ximena Contreras, Thomas Rülicke, Ryuichi Shigemoto, Gaia Novarino, and Maximilian A Jösch. “Shared Behavioural Impairments in Visual Perception and Place Avoidance across Different Autism Models Are Driven by Periaqueductal Grey Hypoexcitability in Setd5 Haploinsufficient Mice.” Institute of Science and Technology Austria, 2024. <a href=\"https://doi.org/10.15479/AT:ISTA:15385\">https://doi.org/10.15479/AT:ISTA:15385</a>.","ista":"Burnett L, Koppensteiner P, Symonova O, Masson T, Vega Zuniga TA, Contreras X, Rülicke T, Shigemoto R, Novarino G, Jösch MA. 2024. Shared behavioural impairments in visual perception and place avoidance across different autism models are driven by periaqueductal grey hypoexcitability in Setd5 haploinsufficient mice, Institute of Science and Technology Austria, <a href=\"https://doi.org/10.15479/AT:ISTA:15385\">10.15479/AT:ISTA:15385</a>.","mla":"Burnett, Laura, et al. <i>Shared Behavioural Impairments in Visual Perception and Place Avoidance across Different Autism Models Are Driven by Periaqueductal Grey Hypoexcitability in Setd5 Haploinsufficient Mice</i>. Institute of Science and Technology Austria, 2024, doi:<a href=\"https://doi.org/10.15479/AT:ISTA:15385\">10.15479/AT:ISTA:15385</a>.","ieee":"L. Burnett <i>et al.</i>, “Shared behavioural impairments in visual perception and place avoidance across different autism models are driven by periaqueductal grey hypoexcitability in Setd5 haploinsufficient mice.” Institute of Science and Technology Austria, 2024.","ama":"Burnett L, Koppensteiner P, Symonova O, et al. Shared behavioural impairments in visual perception and place avoidance across different autism models are driven by periaqueductal grey hypoexcitability in Setd5 haploinsufficient mice. 2024. doi:<a href=\"https://doi.org/10.15479/AT:ISTA:15385\">10.15479/AT:ISTA:15385</a>"},"keyword":["ASD","periaqueductal gray","perception","behavior","potassium channels"],"has_accepted_license":"1","oa_version":"Published Version","date_updated":"2025-09-08T07:57:11Z","file":[{"success":1,"file_size":"1149617663","file_name":"PatchClamp.zip","checksum":"9205eb0876f0f08552dbad80d6884b4b","date_created":"2024-05-15T06:09:17Z","file_id":"15396","content_type":"application/zip","relation":"main_file","creator":"mjoesch","access_level":"open_access","date_updated":"2024-05-15T06:09:17Z"},{"success":1,"file_name":"SiliconProbe.zip","file_size":"564903112","date_created":"2024-05-15T06:09:12Z","file_id":"15397","content_type":"application/zip","relation":"main_file","date_updated":"2024-05-15T06:09:12Z","creator":"mjoesch","access_level":"open_access"},{"file_id":"15398","date_created":"2024-05-15T06:09:14Z","checksum":"49a807bbab06b5fada38f532e2176e2e","file_size":"11685703","file_name":"WesternBlot.zip","success":1,"date_updated":"2024-05-15T06:09:14Z","access_level":"open_access","creator":"mjoesch","relation":"main_file","content_type":"application/zip"},{"success":1,"file_name":"Behaviour.zip","file_size":"1335626779","checksum":"beeeeaa43770090f3b291209ed6b0623","date_created":"2024-05-15T06:09:38Z","file_id":"15399","content_type":"application/zip","relation":"main_file","creator":"mjoesch","access_level":"open_access","date_updated":"2024-05-15T06:09:38Z"},{"content_type":"text/plain","relation":"main_file","date_updated":"2024-05-16T09:08:20Z","creator":"mjoesch","access_level":"open_access","success":1,"file_name":"Readme_Data.txt","file_size":18841,"date_created":"2024-05-16T09:08:20Z","file_id":"15400","checksum":"8862ad7719388304d1d19f8e7db8bb00"}],"type":"research_data","corr_author":"1","publisher":"Institute of Science and Technology Austria","day":"15"},{"abstract":[{"lang":"eng","text":"Despite the diverse genetic origins of autism spectrum disorders (ASDs), affected individuals share strikingly similar and correlated behavioural traits that include perceptual and sensory processing challenges. Notably, the severity of these sensory symptoms is often predictive of the expression of other autistic traits. However, the origin of these perceptual deficits remains largely elusive. Here, we show a recurrent impairment in visual threat perception that is similarly impaired in 3 independent mouse models of ASD with different molecular aetiologies. Interestingly, this deficit is associated with reduced avoidance of threatening environments—a nonperceptual trait. Focusing on a common cause of ASDs, the Setd5 gene mutation, we define the molecular mechanism. We show that the perceptual impairment is caused by a potassium channel (Kv1)-mediated hypoexcitability in a subcortical node essential for the initiation of escape responses, the dorsal periaqueductal grey (dPAG). Targeted pharmacological Kv1 blockade rescued both perceptual and place avoidance deficits, causally linking seemingly unrelated trait deficits to the dPAG. Furthermore, we show that different molecular mechanisms converge on similar behavioural phenotypes by demonstrating that the autism models Cul3 and Ptchd1, despite having similar behavioural phenotypes, differ in their functional and molecular alteration. Our findings reveal a link between rapid perception controlled by subcortical pathways and appropriate learned interactions with the environment and define a nondevelopmental source of such deficits in ASD."}],"publication_status":"published","ddc":["570"],"date_published":"2024-06-10T00:00:00Z","status":"public","tmp":{"short":"CC BY (4.0)","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode"},"month":"06","OA_type":"gold","doi":"10.1371/journal.pbio.3002668","pmid":1,"user_id":"317138e5-6ab7-11ef-aa6d-ffef3953e345","oa_version":"Published Version","date_updated":"2025-09-08T07:57:11Z","language":[{"iso":"eng"}],"ec_funded":1,"oa":1,"APC_amount":"6081,83 EUR","day":"10","corr_author":"1","file":[{"file_size":4016568,"file_name":"2024_PloS_Burnett.pdf","success":1,"file_id":"18805","date_created":"2025-01-09T10:39:41Z","checksum":"496e1aa4fd5b92b7e4087ecc2c964133","relation":"main_file","content_type":"application/pdf","date_updated":"2025-01-09T10:39:41Z","access_level":"open_access","creator":"dernst"}],"OA_place":"publisher","related_material":{"link":[{"url":"https://doi.org/10.5281/zenodo.11130587","relation":"software"}],"record":[{"id":"15385","status":"public","relation":"research_data"}]},"article_type":"original","external_id":{"isi":["001246176800003"],"pmid":["38857283"]},"title":"Shared behavioural impairments in visual perception and place avoidance across different autism models are driven by periaqueductal grey hypoexcitability in Setd5 haploinsufficient mice","volume":22,"year":"2024","project":[{"grant_number":"756502","call_identifier":"H2020","name":"Circuits of Visual Attention","_id":"2634E9D2-B435-11E9-9278-68D0E5697425"}],"publication":"PLoS Biology","acknowledgement":"This work was supported by a European Research Council Starting Grant 756502 (MJ). ","date_created":"2024-06-16T22:01:05Z","article_processing_charge":"Yes","publication_identifier":{"eissn":["1545-7885"],"issn":["1544-9173"]},"department":[{"_id":"RySh"},{"_id":"GaNo"},{"_id":"MaJö"}],"has_accepted_license":"1","quality_controlled":"1","scopus_import":"1","article_number":"e3002668","citation":{"ama":"Burnett L, Koppensteiner P, Symonova O, et al. Shared behavioural impairments in visual perception and place avoidance across different autism models are driven by periaqueductal grey hypoexcitability in Setd5 haploinsufficient mice. <i>PLoS Biology</i>. 2024;22. doi:<a href=\"https://doi.org/10.1371/journal.pbio.3002668\">10.1371/journal.pbio.3002668</a>","ista":"Burnett L, Koppensteiner P, Symonova O, Masson T, Vega Zuniga TA, Contreras X, Rülicke T, Shigemoto R, Novarino G, Jösch MA. 2024. Shared behavioural impairments in visual perception and place avoidance across different autism models are driven by periaqueductal grey hypoexcitability in Setd5 haploinsufficient mice. PLoS Biology. 22, e3002668.","mla":"Burnett, Laura, et al. “Shared Behavioural Impairments in Visual Perception and Place Avoidance across Different Autism Models Are Driven by Periaqueductal Grey Hypoexcitability in Setd5 Haploinsufficient Mice.” <i>PLoS Biology</i>, vol. 22, e3002668, Public Library of Science, 2024, doi:<a href=\"https://doi.org/10.1371/journal.pbio.3002668\">10.1371/journal.pbio.3002668</a>.","ieee":"L. Burnett <i>et al.</i>, “Shared behavioural impairments in visual perception and place avoidance across different autism models are driven by periaqueductal grey hypoexcitability in Setd5 haploinsufficient mice,” <i>PLoS Biology</i>, vol. 22. Public Library of Science, 2024.","chicago":"Burnett, Laura, Peter Koppensteiner, Olga Symonova, Tomas Masson, Tomas A Vega Zuniga, Ximena Contreras, Thomas Rülicke, Ryuichi Shigemoto, Gaia Novarino, and Maximilian A Jösch. “Shared Behavioural Impairments in Visual Perception and Place Avoidance across Different Autism Models Are Driven by Periaqueductal Grey Hypoexcitability in Setd5 Haploinsufficient Mice.” <i>PLoS Biology</i>. Public Library of Science, 2024. <a href=\"https://doi.org/10.1371/journal.pbio.3002668\">https://doi.org/10.1371/journal.pbio.3002668</a>.","short":"L. Burnett, P. Koppensteiner, O. Symonova, T. Masson, T.A. Vega Zuniga, X. Contreras, T. Rülicke, R. Shigemoto, G. Novarino, M.A. Jösch, PLoS Biology 22 (2024).","apa":"Burnett, L., Koppensteiner, P., Symonova, O., Masson, T., Vega Zuniga, T. A., Contreras, X., … Jösch, M. A. (2024). Shared behavioural impairments in visual perception and place avoidance across different autism models are driven by periaqueductal grey hypoexcitability in Setd5 haploinsufficient mice. <i>PLoS Biology</i>. Public Library of Science. <a href=\"https://doi.org/10.1371/journal.pbio.3002668\">https://doi.org/10.1371/journal.pbio.3002668</a>"},"author":[{"orcid":"0000-0002-8937-410X","id":"3B717F68-F248-11E8-B48F-1D18A9856A87","last_name":"Burnett","first_name":"Laura","full_name":"Burnett, Laura"},{"full_name":"Koppensteiner, Peter","last_name":"Koppensteiner","id":"3B8B25A8-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0002-3509-1948","first_name":"Peter"},{"first_name":"Olga","orcid":"0000-0003-2012-9947","id":"3C0C7BC6-F248-11E8-B48F-1D18A9856A87","last_name":"Symonova","full_name":"Symonova, Olga"},{"full_name":"Masson, Tomas","orcid":"0000-0002-2634-6283","last_name":"Masson","id":"93ac43e8-8599-11eb-9b86-f6efb0a4c207","first_name":"Tomas"},{"full_name":"Vega Zuniga, Tomas A","last_name":"Vega Zuniga","id":"2E7C4E78-F248-11E8-B48F-1D18A9856A87","first_name":"Tomas A"},{"id":"475990FE-F248-11E8-B48F-1D18A9856A87","last_name":"Contreras","first_name":"Ximena","full_name":"Contreras, Ximena"},{"last_name":"Rülicke","first_name":"Thomas","full_name":"Rülicke, Thomas"},{"first_name":"Ryuichi","id":"499F3ABC-F248-11E8-B48F-1D18A9856A87","last_name":"Shigemoto","orcid":"0000-0001-8761-9444","full_name":"Shigemoto, Ryuichi"},{"first_name":"Gaia","orcid":"0000-0002-7673-7178","id":"3E57A680-F248-11E8-B48F-1D18A9856A87","last_name":"Novarino","full_name":"Novarino, Gaia"},{"full_name":"Jösch, Maximilian A","first_name":"Maximilian A","last_name":"Jösch","id":"2BD278E6-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0002-3937-1330"}],"_id":"17142","file_date_updated":"2025-01-09T10:39:41Z","intvolume":"        22","publisher":"Public Library of Science","DOAJ_listed":"1","type":"journal_article","isi":1},{"DOAJ_listed":"1","type":"journal_article","isi":1,"publisher":"American Association for the Advancement of Science","intvolume":"        10","author":[{"full_name":"Früh, Simon","last_name":"Früh","first_name":"Simon"},{"full_name":"Boudkkazi, Sami","last_name":"Boudkkazi","first_name":"Sami"},{"orcid":"0000-0002-3509-1948","id":"3B8B25A8-F248-11E8-B48F-1D18A9856A87","last_name":"Koppensteiner","first_name":"Peter","full_name":"Koppensteiner, Peter"},{"full_name":"Sereikaite, Vita","first_name":"Vita","last_name":"Sereikaite"},{"first_name":"Li Yuan","last_name":"Chen","full_name":"Chen, Li Yuan"},{"full_name":"Fernandez-Fernandez, Diego","first_name":"Diego","last_name":"Fernandez-Fernandez"},{"full_name":"Rem, Pascal D.","last_name":"Rem","first_name":"Pascal D."},{"first_name":"Daniel","last_name":"Ulrich","full_name":"Ulrich, Daniel"},{"full_name":"Schwenk, Jochen","first_name":"Jochen","last_name":"Schwenk"},{"last_name":"Chen","first_name":"Ziyang","full_name":"Chen, Ziyang"},{"full_name":"Monnier, Elodie Le","first_name":"Elodie Le","last_name":"Monnier"},{"last_name":"Fritzius","first_name":"Thorsten","full_name":"Fritzius, Thorsten"},{"first_name":"Sabrina M.","last_name":"Innocenti","full_name":"Innocenti, Sabrina M."},{"last_name":"Besseyrias","first_name":"Valérie","full_name":"Besseyrias, Valérie"},{"full_name":"Trovò, Luca","last_name":"Trovò","first_name":"Luca"},{"full_name":"Stawarski, Michal","first_name":"Michal","last_name":"Stawarski"},{"first_name":"Emanuela","last_name":"Argilli","full_name":"Argilli, Emanuela"},{"full_name":"Sherr, Elliott H.","first_name":"Elliott H.","last_name":"Sherr"},{"first_name":"Bregje","last_name":"Van Bon","full_name":"Van Bon, Bregje"},{"last_name":"Kamsteeg","first_name":"Erik Jan","full_name":"Kamsteeg, Erik Jan"},{"full_name":"Iascone, Maria","last_name":"Iascone","first_name":"Maria"},{"last_name":"Pilotta","first_name":"Alba","full_name":"Pilotta, Alba"},{"first_name":"Maria R.","last_name":"Cutrì","full_name":"Cutrì, Maria R."},{"last_name":"Azamian","first_name":"Mahshid S.","full_name":"Azamian, Mahshid S."},{"first_name":"Andrés","last_name":"Hernández-García","full_name":"Hernández-García, Andrés"},{"last_name":"Lalani","first_name":"Seema R.","full_name":"Lalani, Seema R."},{"first_name":"Jill A.","last_name":"Rosenfeld","full_name":"Rosenfeld, Jill A."},{"last_name":"Zhao","first_name":"Xiaonan","full_name":"Zhao, Xiaonan"},{"last_name":"Vogel","first_name":"Tiphanie P.","full_name":"Vogel, Tiphanie P."},{"full_name":"Ona, Herda","last_name":"Ona","first_name":"Herda"},{"last_name":"Scott","first_name":"Daryl A.","full_name":"Scott, Daryl A."},{"first_name":"Peter","last_name":"Scheiffele","full_name":"Scheiffele, Peter"},{"first_name":"Kristian","last_name":"Strømgaard","full_name":"Strømgaard, Kristian"},{"full_name":"Tafti, Mehdi","first_name":"Mehdi","last_name":"Tafti"},{"last_name":"Gassmann","first_name":"Martin","full_name":"Gassmann, Martin"},{"full_name":"Fakler, Bernd","first_name":"Bernd","last_name":"Fakler"},{"full_name":"Shigemoto, Ryuichi","first_name":"Ryuichi","id":"499F3ABC-F248-11E8-B48F-1D18A9856A87","last_name":"Shigemoto","orcid":"0000-0001-8761-9444"},{"first_name":"Bernhard","last_name":"Bettler","full_name":"Bettler, Bernhard"}],"file_date_updated":"2024-07-22T06:29:27Z","_id":"17280","citation":{"apa":"Früh, S., Boudkkazi, S., Koppensteiner, P., Sereikaite, V., Chen, L. Y., Fernandez-Fernandez, D., … Bettler, B. (2024). Monoallelic de novo AJAP1 loss-of- function variants disrupt trans-synaptic control of neurotransmitter release. <i>Science Advances</i>. American Association for the Advancement of Science. <a href=\"https://doi.org/10.1126/sciadv.adk5462\">https://doi.org/10.1126/sciadv.adk5462</a>","short":"S. Früh, S. Boudkkazi, P. Koppensteiner, V. Sereikaite, L.Y. Chen, D. Fernandez-Fernandez, P.D. Rem, D. Ulrich, J. Schwenk, Z. Chen, E.L. Monnier, T. Fritzius, S.M. Innocenti, V. Besseyrias, L. Trovò, M. Stawarski, E. Argilli, E.H. Sherr, B. Van Bon, E.J. Kamsteeg, M. Iascone, A. Pilotta, M.R. Cutrì, M.S. Azamian, A. Hernández-García, S.R. Lalani, J.A. Rosenfeld, X. Zhao, T.P. Vogel, H. Ona, D.A. Scott, P. Scheiffele, K. Strømgaard, M. Tafti, M. Gassmann, B. Fakler, R. Shigemoto, B. Bettler, Science Advances 10 (2024).","chicago":"Früh, Simon, Sami Boudkkazi, Peter Koppensteiner, Vita Sereikaite, Li Yuan Chen, Diego Fernandez-Fernandez, Pascal D. Rem, et al. “Monoallelic de Novo AJAP1 Loss-of- Function Variants Disrupt Trans-Synaptic Control of Neurotransmitter Release.” <i>Science Advances</i>. American Association for the Advancement of Science, 2024. <a href=\"https://doi.org/10.1126/sciadv.adk5462\">https://doi.org/10.1126/sciadv.adk5462</a>.","ieee":"S. Früh <i>et al.</i>, “Monoallelic de novo AJAP1 loss-of- function variants disrupt trans-synaptic control of neurotransmitter release,” <i>Science Advances</i>, vol. 10, no. 28. American Association for the Advancement of Science, 2024.","mla":"Früh, Simon, et al. “Monoallelic de Novo AJAP1 Loss-of- Function Variants Disrupt Trans-Synaptic Control of Neurotransmitter Release.” <i>Science Advances</i>, vol. 10, no. 28, adk5462, American Association for the Advancement of Science, 2024, doi:<a href=\"https://doi.org/10.1126/sciadv.adk5462\">10.1126/sciadv.adk5462</a>.","ista":"Früh S, Boudkkazi S, Koppensteiner P, Sereikaite V, Chen LY, Fernandez-Fernandez D, Rem PD, Ulrich D, Schwenk J, Chen Z, Monnier EL, Fritzius T, Innocenti SM, Besseyrias V, Trovò L, Stawarski M, Argilli E, Sherr EH, Van Bon B, Kamsteeg EJ, Iascone M, Pilotta A, Cutrì MR, Azamian MS, Hernández-García A, Lalani SR, Rosenfeld JA, Zhao X, Vogel TP, Ona H, Scott DA, Scheiffele P, Strømgaard K, Tafti M, Gassmann M, Fakler B, Shigemoto R, Bettler B. 2024. Monoallelic de novo AJAP1 loss-of- function variants disrupt trans-synaptic control of neurotransmitter release. Science Advances. 10(28), adk5462.","ama":"Früh S, Boudkkazi S, Koppensteiner P, et al. Monoallelic de novo AJAP1 loss-of- function variants disrupt trans-synaptic control of neurotransmitter release. <i>Science Advances</i>. 2024;10(28). doi:<a href=\"https://doi.org/10.1126/sciadv.adk5462\">10.1126/sciadv.adk5462</a>"},"has_accepted_license":"1","article_number":"adk5462","quality_controlled":"1","scopus_import":"1","department":[{"_id":"RySh"},{"_id":"PreCl"}],"publication_identifier":{"eissn":["2375-2548"]},"acknowledgement":"Ajap1HA/HA and Ajap1W183C/+ mice were generated in collaboration with Pawel Pelczar at the center for transgenic models at the University of Basel, Switzerland. We thank the imaging core facility (IMCF, University of Basel) and in particular A. Ferrand for the technical assistance provided on the OMX 3D-SIM microscope.\r\nThis work was supported by a grant from the Swiss National Science Foundation (SNF) to B.B. (31003A-152970, 310030B-201291), an NIH grant to E.A. and E.H.S. (R01NS058721), DFG grants to B.F. (TRR 152 project ID 239283807, FA 332/15-1, 16-1), and grants to P.S. from AIMS-2-TRIALS, which are supported by the Innovative Medicines Initiatives from the European Commission joint undertaking under grant agreement No 777394.","date_created":"2024-07-21T22:01:01Z","article_processing_charge":"Yes","year":"2024","publication":"Science Advances","title":"Monoallelic de novo AJAP1 loss-of- function variants disrupt trans-synaptic control of neurotransmitter release","external_id":{"pmid":["38985877"],"isi":["001280159000022"]},"article_type":"original","volume":10,"OA_place":"publisher","file":[{"content_type":"application/pdf","relation":"main_file","creator":"dernst","access_level":"open_access","date_updated":"2024-07-22T06:29:27Z","success":1,"file_size":7241489,"file_name":"2024_ScienceAdv_Früh.pdf","checksum":"9cbc4501fcd4ba1c0811fd244031422b","date_created":"2024-07-22T06:29:27Z","file_id":"17287"}],"day":"12","oa":1,"language":[{"iso":"eng"}],"issue":"28","oa_version":"Published Version","date_updated":"2025-09-08T08:15:54Z","doi":"10.1126/sciadv.adk5462","pmid":1,"user_id":"317138e5-6ab7-11ef-aa6d-ffef3953e345","tmp":{"short":"CC BY (4.0)","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode"},"OA_type":"gold","month":"07","status":"public","date_published":"2024-07-12T00:00:00Z","publication_status":"published","abstract":[{"lang":"eng","text":"Adherens junction–associated protein 1 (AJAP1) has been implicated in brain diseases; however, a pathogenic mechanism has not been identified. AJAP1 is widely expressed in neurons and binds to γ-aminobutyric acid type B receptors (GBRs), which inhibit neurotransmitter release at most synapses in the brain. Here, we show that AJAP1 is selectively expressed in dendrites and trans-synaptically recruits GBRs to presynaptic sites of neurons expressing AJAP1. We have identified several monoallelic AJAP1 variants in individuals with epilepsy and/or neurodevelopmental disorders. Specifically, we show that the variant p.(W183C) lacks binding to GBRs, resulting in the inability to recruit them. Ultrastructural analysis revealed significantly decreased presynaptic GBR levels in Ajap1−/− and Ajap1W183C/+ mice. Consequently, these mice exhibited reduced GBR-mediated presynaptic inhibition at excitatory and inhibitory synapses, along with impaired synaptic plasticity. Our study reveals that AJAP1 enables the postsynaptic neuron to regulate the level of presynaptic GBR-mediated inhibition, supporting the clinical relevance of loss-of-function AJAP1 variants."}],"ddc":["570"]},{"acknowledged_ssus":[{"_id":"Bio"},{"_id":"EM-Fac"}],"publication_identifier":{"eissn":["2332-7812"]},"article_processing_charge":"Yes","date_created":"2024-08-25T22:01:07Z","acknowledgement":"The authors thank Claudia Sommer for expert technical assistance, the Electron Microscopy Facility of IST-Austria for resources, and Tereza Belinova in the Imaging and Optics Facility of IST-Austria for 3D reconstruction. ","department":[{"_id":"RySh"}],"related_material":{"link":[{"url":"https://doi.org/10.1101/2023.10.04.560631","relation":"earlier_version"}]},"page":"e200284","OA_place":"publisher","project":[{"name":"LGI1 antibody-induced pathophysiology in synapses","_id":"05970B30-7A3F-11EA-A408-12923DDC885E","grant_number":"I04638"}],"publication":"Neurology, Neuroimmunology and Neuroinflammation","year":"2024","volume":11,"article_type":"original","external_id":{"pmid":["39141878"],"isi":["001291908600001"]},"title":"LGI1 autoantibodies enhance synaptic transmission by presynaptic Kv1 loss and increased action potential broadening","publisher":"Wolters Kluwer","intvolume":"        11","isi":1,"DOAJ_listed":"1","type":"journal_article","citation":{"chicago":"Ritzau-Jost, Andreas, Felix Gsell, Josefine Sell, Stefan Sachs, Jacqueline-Claire Montanaro-Punzengruber, Toni Kirmann, Sebastian Maaß, et al. “LGI1 Autoantibodies Enhance Synaptic Transmission by Presynaptic Kv1 Loss and Increased Action Potential Broadening.” <i>Neurology, Neuroimmunology and Neuroinflammation</i>. Wolters Kluwer, 2024. <a href=\"https://doi.org/10.1212/NXI.0000000000200284\">https://doi.org/10.1212/NXI.0000000000200284</a>.","apa":"Ritzau-Jost, A., Gsell, F., Sell, J., Sachs, S., Montanaro-Punzengruber, J.-C., Kirmann, T., … Hallermann, S. (2024). LGI1 autoantibodies enhance synaptic transmission by presynaptic Kv1 loss and increased action potential broadening. <i>Neurology, Neuroimmunology and Neuroinflammation</i>. Wolters Kluwer. <a href=\"https://doi.org/10.1212/NXI.0000000000200284\">https://doi.org/10.1212/NXI.0000000000200284</a>","short":"A. Ritzau-Jost, F. Gsell, J. Sell, S. Sachs, J.-C. Montanaro-Punzengruber, T. Kirmann, S. Maaß, S.R. Irani, C. Werner, C. Geis, M. Sauer, R. Shigemoto, S. Hallermann, Neurology, Neuroimmunology and Neuroinflammation 11 (2024) e200284.","ama":"Ritzau-Jost A, Gsell F, Sell J, et al. LGI1 autoantibodies enhance synaptic transmission by presynaptic Kv1 loss and increased action potential broadening. <i>Neurology, Neuroimmunology and Neuroinflammation</i>. 2024;11(5):e200284. doi:<a href=\"https://doi.org/10.1212/NXI.0000000000200284\">10.1212/NXI.0000000000200284</a>","ieee":"A. Ritzau-Jost <i>et al.</i>, “LGI1 autoantibodies enhance synaptic transmission by presynaptic Kv1 loss and increased action potential broadening,” <i>Neurology, Neuroimmunology and Neuroinflammation</i>, vol. 11, no. 5. Wolters Kluwer, p. e200284, 2024.","ista":"Ritzau-Jost A, Gsell F, Sell J, Sachs S, Montanaro-Punzengruber J-C, Kirmann T, Maaß S, Irani SR, Werner C, Geis C, Sauer M, Shigemoto R, Hallermann S. 2024. LGI1 autoantibodies enhance synaptic transmission by presynaptic Kv1 loss and increased action potential broadening. Neurology, Neuroimmunology and Neuroinflammation. 11(5), e200284.","mla":"Ritzau-Jost, Andreas, et al. “LGI1 Autoantibodies Enhance Synaptic Transmission by Presynaptic Kv1 Loss and Increased Action Potential Broadening.” <i>Neurology, Neuroimmunology and Neuroinflammation</i>, vol. 11, no. 5, Wolters Kluwer, 2024, p. e200284, doi:<a href=\"https://doi.org/10.1212/NXI.0000000000200284\">10.1212/NXI.0000000000200284</a>."},"quality_controlled":"1","scopus_import":"1","has_accepted_license":"1","_id":"17457","file_date_updated":"2025-01-09T13:42:42Z","author":[{"first_name":"Andreas","last_name":"Ritzau-Jost","full_name":"Ritzau-Jost, Andreas"},{"full_name":"Gsell, Felix","last_name":"Gsell","first_name":"Felix"},{"full_name":"Sell, Josefine","last_name":"Sell","first_name":"Josefine"},{"first_name":"Stefan","last_name":"Sachs","full_name":"Sachs, Stefan"},{"id":"3786AB44-F248-11E8-B48F-1D18A9856A87","last_name":"Montanaro-Punzengruber","first_name":"Jacqueline-Claire","full_name":"Montanaro-Punzengruber, Jacqueline-Claire"},{"last_name":"Kirmann","first_name":"Toni","full_name":"Kirmann, Toni"},{"full_name":"Maaß, Sebastian","first_name":"Sebastian","last_name":"Maaß"},{"last_name":"Irani","first_name":"Sarosh R.","full_name":"Irani, Sarosh R."},{"last_name":"Werner","first_name":"Christian","full_name":"Werner, Christian"},{"full_name":"Geis, Christian","first_name":"Christian","last_name":"Geis"},{"first_name":"Markus","last_name":"Sauer","full_name":"Sauer, Markus"},{"first_name":"Ryuichi","orcid":"0000-0001-8761-9444","last_name":"Shigemoto","id":"499F3ABC-F248-11E8-B48F-1D18A9856A87","full_name":"Shigemoto, Ryuichi"},{"last_name":"Hallermann","first_name":"Stefan","full_name":"Hallermann, Stefan"}],"OA_type":"gold","month":"09","tmp":{"short":"CC BY (4.0)","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode"},"user_id":"317138e5-6ab7-11ef-aa6d-ffef3953e345","doi":"10.1212/NXI.0000000000200284","pmid":1,"ddc":["570"],"abstract":[{"text":"Autoantibodies against the protein leucine-rich glioma inactivated 1 (LGI1) cause the most\r\ncommon subtype of autoimmune encephalitis with predominant involvement of the limbic\r\nsystem, associated with seizures and memory deficits. LGI1 and its receptor ADAM22 are part\r\nof a transsynaptic protein complex that includes several proteins involved in presynaptic\r\nneurotransmitter release and postsynaptic glutamate sensing. Autoantibodies against LGI1\r\nincrease excitatory synaptic strength, but studies that genetically disrupt the LGI1-ADAM22\r\ncomplex report a reduction in postsynaptic glutamate receptor-mediated responses. Thus, the\r\nmechanisms underlying the increased synaptic strength induced by LGI1 autoantibodies remain elusive, and the contributions of presynaptic molecules to the LGI1-transsynaptic complex remain unclear. We therefore investigated the presynaptic mechanisms that mediate\r\nautoantibody-induced synaptic strengthening.","lang":"eng"}],"publication_status":"published","status":"public","date_published":"2024-09-01T00:00:00Z","day":"01","file":[{"success":1,"file_size":855818,"file_name":"2024_NeurologyNeuroimmNeuroinflamm_RitzauJost.pdf","date_created":"2025-01-09T13:42:42Z","file_id":"18815","checksum":"1e6d1230e0387f72752e3268f5330c9e","content_type":"application/pdf","relation":"main_file","date_updated":"2025-01-09T13:42:42Z","creator":"dernst","access_level":"open_access"}],"date_updated":"2025-09-08T08:59:37Z","oa_version":"Published Version","issue":"5","language":[{"iso":"eng"}],"oa":1},{"tmp":{"short":"CC BY (4.0)","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode"},"month":"01","pmid":1,"doi":"10.1016/j.neuron.2023.11.009","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","abstract":[{"lang":"eng","text":"The superior colliculus (SC) in the mammalian midbrain is essential for multisensory integration and is composed of a rich diversity of excitatory and inhibitory neurons and glia. However, the developmental principles directing the generation of SC cell-type diversity are not understood. Here, we pursued systematic cell lineage tracing in silico and in vivo, preserving full spatial information, using genetic mosaic analysis with double markers (MADM)-based clonal analysis with single-cell sequencing (MADM-CloneSeq). The analysis of clonally related cell lineages revealed that radial glial progenitors (RGPs) in SC are exceptionally multipotent. Individual resident RGPs have the capacity to produce all excitatory and inhibitory SC neuron types, even at the stage of terminal division. While individual clonal units show no pre-defined cellular composition, the establishment of appropriate relative proportions of distinct neuronal types occurs in a PTEN-dependent manner. Collectively, our findings provide an inaugural framework at the single-RGP/-cell level of the mammalian SC ontogeny."}],"publication_status":"published","ddc":["570"],"date_published":"2024-01-17T00:00:00Z","status":"public","day":"17","corr_author":"1","file":[{"date_updated":"2024-02-06T13:56:15Z","creator":"dernst","access_level":"open_access","content_type":"application/pdf","relation":"main_file","date_created":"2024-02-06T13:56:15Z","file_id":"14944","checksum":"32b3788f7085cf44a84108d8faaff3ce","success":1,"file_size":5942467,"file_name":"2024_Neuron_Cheung.pdf"}],"issue":"2","date_updated":"2025-12-30T10:54:12Z","oa_version":"Published Version","language":[{"iso":"eng"}],"oa":1,"acknowledgement":"We thank Liqun Luo for his continued support, for providing essential resources for generating Fzd10-CreER mice which were generated in his laboratory, and for comments on the manuscript; W. Zhong for providing Nestin-Cre transgenic mouse line for this study; A. Heger for mouse colony management; R. Beattie and T. Asenov for designing and producing components of acute slice recovery chamber for MADM-CloneSeq experiments; and K. Leopold, J. Rodarte and N. Amberg for initial experiments, technical support and/or assistance. This study was supported by the Scientific Service Units (SSU) of IST Austria through resources provided by the Imaging & Optics Facility (IOF), Laboratory Support Facility (LSF), Miba Machine Shop, and Pre-clinical Facility (PCF). G.C. received funding from European Commission (IST plus postdoctoral fellowship). This work was supported by ISTA institutional\r\nfunds; the Austrian Science Fund Special Research Programmes (FWF SFB F78 Neuro Stem Modulation) to S.H. ","date_created":"2023-04-27T09:41:48Z","article_processing_charge":"Yes (via OA deal)","publication_identifier":{"issn":["0896-6273"]},"acknowledged_ssus":[{"_id":"Bio"},{"_id":"M-Shop"},{"_id":"LifeSc"},{"_id":"PreCl"}],"department":[{"_id":"SiHi"},{"_id":"RySh"}],"page":"230-246.e11","related_material":{"link":[{"description":"News on ISTA Website","url":"https://ista.ac.at/en/news/the-pedigree-of-brain-cells/","relation":"press_release"}]},"title":"Multipotent progenitors instruct ontogeny of the superior colliculus","article_type":"original","external_id":{"pmid":["38096816"],"isi":["001163937900001"]},"volume":112,"year":"2024","project":[{"grant_number":"F7805","_id":"059F6AB4-7A3F-11EA-A408-12923DDC885E","name":"Stem Cell Modulation in Neural Development and Regeneration/ P05-Molecular Mechanisms of Neural Stem Cell Lineage Progression"}],"publication":"Neuron","intvolume":"       112","publisher":"Elsevier","type":"journal_article","isi":1,"has_accepted_license":"1","scopus_import":"1","quality_controlled":"1","citation":{"short":"G.T. Cheung, F. Pauler, P. Koppensteiner, T. Krausgruber, C. Streicher, M. Schrammel, N.Y. Özgen, A. Ivec, C. Bock, R. Shigemoto, S. Hippenmeyer, Neuron 112 (2024) 230–246.e11.","apa":"Cheung, G. T., Pauler, F., Koppensteiner, P., Krausgruber, T., Streicher, C., Schrammel, M., … Hippenmeyer, S. (2024). Multipotent progenitors instruct ontogeny of the superior colliculus. <i>Neuron</i>. Elsevier. <a href=\"https://doi.org/10.1016/j.neuron.2023.11.009\">https://doi.org/10.1016/j.neuron.2023.11.009</a>","chicago":"Cheung, Giselle T, Florian Pauler, Peter Koppensteiner, Thomas Krausgruber, Carmen Streicher, Martin Schrammel, Natalie Y Özgen, et al. “Multipotent Progenitors Instruct Ontogeny of the Superior Colliculus.” <i>Neuron</i>. Elsevier, 2024. <a href=\"https://doi.org/10.1016/j.neuron.2023.11.009\">https://doi.org/10.1016/j.neuron.2023.11.009</a>.","mla":"Cheung, Giselle T., et al. “Multipotent Progenitors Instruct Ontogeny of the Superior Colliculus.” <i>Neuron</i>, vol. 112, no. 2, Elsevier, 2024, p. 230–246.e11, doi:<a href=\"https://doi.org/10.1016/j.neuron.2023.11.009\">10.1016/j.neuron.2023.11.009</a>.","ieee":"G. T. Cheung <i>et al.</i>, “Multipotent progenitors instruct ontogeny of the superior colliculus,” <i>Neuron</i>, vol. 112, no. 2. Elsevier, p. 230–246.e11, 2024.","ista":"Cheung GT, Pauler F, Koppensteiner P, Krausgruber T, Streicher C, Schrammel M, Özgen NY, Ivec A, Bock C, Shigemoto R, Hippenmeyer S. 2024. Multipotent progenitors instruct ontogeny of the superior colliculus. Neuron. 112(2), 230–246.e11.","ama":"Cheung GT, Pauler F, Koppensteiner P, et al. Multipotent progenitors instruct ontogeny of the superior colliculus. <i>Neuron</i>. 2024;112(2):230-246.e11. doi:<a href=\"https://doi.org/10.1016/j.neuron.2023.11.009\">10.1016/j.neuron.2023.11.009</a>"},"author":[{"full_name":"Cheung, Giselle T","first_name":"Giselle T","orcid":"0000-0001-8457-2572","last_name":"Cheung","id":"471195F6-F248-11E8-B48F-1D18A9856A87"},{"full_name":"Pauler, Florian","orcid":"0000-0002-7462-0048","id":"48EA0138-F248-11E8-B48F-1D18A9856A87","last_name":"Pauler","first_name":"Florian"},{"full_name":"Koppensteiner, Peter","first_name":"Peter","orcid":"0000-0002-3509-1948","id":"3B8B25A8-F248-11E8-B48F-1D18A9856A87","last_name":"Koppensteiner"},{"full_name":"Krausgruber, Thomas","first_name":"Thomas","last_name":"Krausgruber"},{"full_name":"Streicher, Carmen","first_name":"Carmen","id":"36BCB99C-F248-11E8-B48F-1D18A9856A87","last_name":"Streicher"},{"full_name":"Schrammel, Martin","last_name":"Schrammel","id":"f13e7cae-e8bd-11ed-841a-96dedf69f46d","first_name":"Martin"},{"full_name":"Özgen, Natalie Y","id":"e68ece33-f6e0-11ea-865d-ae1031dcc090","last_name":"Özgen","first_name":"Natalie Y"},{"full_name":"Ivec, Alexis","last_name":"Ivec","id":"1d144691-e8be-11ed-9b33-bdd3077fad4c","first_name":"Alexis"},{"full_name":"Bock, Christoph","last_name":"Bock","first_name":"Christoph"},{"orcid":"0000-0001-8761-9444","last_name":"Shigemoto","id":"499F3ABC-F248-11E8-B48F-1D18A9856A87","first_name":"Ryuichi","full_name":"Shigemoto, Ryuichi"},{"id":"37B36620-F248-11E8-B48F-1D18A9856A87","last_name":"Hippenmeyer","orcid":"0000-0003-2279-1061","first_name":"Simon","full_name":"Hippenmeyer, Simon"}],"file_date_updated":"2024-02-06T13:56:15Z","_id":"12875"},{"day":"01","file":[{"relation":"main_file","content_type":"application/pdf","access_level":"open_access","creator":"dernst","date_updated":"2025-01-09T07:48:01Z","file_size":26065165,"file_name":"2024_NatureBiotech_Michalska.pdf","success":1,"checksum":"57d5fafb16f02dcb9f7dddb1bd7e2a71","file_id":"18784","date_created":"2025-01-09T07:48:01Z"}],"corr_author":"1","oa_version":"Published Version","date_updated":"2026-04-14T08:34:35Z","oa":1,"ec_funded":1,"language":[{"iso":"eng"}],"month":"07","OA_type":"hybrid","tmp":{"short":"CC BY (4.0)","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode"},"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","doi":"10.1038/s41587-023-01911-8","pmid":1,"ddc":["570"],"abstract":[{"lang":"eng","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."}],"publication_status":"published","status":"public","date_published":"2024-07-01T00:00:00Z","publisher":"Springer Nature","intvolume":"        42","isi":1,"type":"journal_article","citation":{"ama":"Michalska JM, Lyudchik J, Velicky P, et al. Imaging brain tissue architecture across millimeter to nanometer scales. <i>Nature Biotechnology</i>. 2024;42:1051-1064. doi:<a href=\"https://doi.org/10.1038/s41587-023-01911-8\">10.1038/s41587-023-01911-8</a>","ista":"Michalska JM, Lyudchik J, Velicky P, Korinkova H, Watson J, Cenameri A, Sommer CM, Amberg N, Venturino A, Roessler K, Czech T, Höftberger R, Siegert S, Novarino G, Jonas PM, Danzl JG. 2024. Imaging brain tissue architecture across millimeter to nanometer scales. Nature Biotechnology. 42, 1051–1064.","mla":"Michalska, Julia M., et al. “Imaging Brain Tissue Architecture across Millimeter to Nanometer Scales.” <i>Nature Biotechnology</i>, vol. 42, Springer Nature, 2024, pp. 1051–64, doi:<a href=\"https://doi.org/10.1038/s41587-023-01911-8\">10.1038/s41587-023-01911-8</a>.","ieee":"J. M. Michalska <i>et al.</i>, “Imaging brain tissue architecture across millimeter to nanometer scales,” <i>Nature Biotechnology</i>, vol. 42. Springer Nature, pp. 1051–1064, 2024.","chicago":"Michalska, Julia M, Julia Lyudchik, Philipp Velicky, Hana Korinkova, Jake Watson, Alban Cenameri, Christoph M Sommer, et al. “Imaging Brain Tissue Architecture across Millimeter to Nanometer Scales.” <i>Nature Biotechnology</i>. Springer Nature, 2024. <a href=\"https://doi.org/10.1038/s41587-023-01911-8\">https://doi.org/10.1038/s41587-023-01911-8</a>.","apa":"Michalska, J. M., Lyudchik, J., Velicky, P., Korinkova, H., Watson, J., Cenameri, A., … Danzl, J. G. (2024). Imaging brain tissue architecture across millimeter to nanometer scales. <i>Nature Biotechnology</i>. Springer Nature. <a href=\"https://doi.org/10.1038/s41587-023-01911-8\">https://doi.org/10.1038/s41587-023-01911-8</a>","short":"J.M. Michalska, J. Lyudchik, P. Velicky, H. Korinkova, J. Watson, A. Cenameri, C.M. Sommer, N. Amberg, A. Venturino, K. Roessler, T. Czech, R. Höftberger, S. Siegert, G. Novarino, P.M. Jonas, J.G. Danzl, Nature Biotechnology 42 (2024) 1051–1064."},"scopus_import":"1","quality_controlled":"1","has_accepted_license":"1","_id":"14257","file_date_updated":"2025-01-09T07:48:01Z","author":[{"full_name":"Michalska, Julia M","orcid":"0000-0003-3862-1235","id":"443DB6DE-F248-11E8-B48F-1D18A9856A87","last_name":"Michalska","first_name":"Julia M"},{"first_name":"Julia","id":"46E28B80-F248-11E8-B48F-1D18A9856A87","last_name":"Lyudchik","full_name":"Lyudchik, Julia"},{"full_name":"Velicky, Philipp","first_name":"Philipp","id":"39BDC62C-F248-11E8-B48F-1D18A9856A87","last_name":"Velicky","orcid":"0000-0002-2340-7431"},{"full_name":"Korinkova, Hana","first_name":"Hana","last_name":"Korinkova","id":"ee3cb6ca-ec98-11ea-ae11-ff703e2254ed"},{"full_name":"Watson, Jake","first_name":"Jake","id":"63836096-4690-11EA-BD4E-32803DDC885E","last_name":"Watson","orcid":"0000-0002-8698-3823"},{"id":"9ac8f577-2357-11eb-997a-e566c5550886","last_name":"Cenameri","first_name":"Alban","full_name":"Cenameri, Alban"},{"last_name":"Sommer","id":"4DF26D8C-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0003-1216-9105","first_name":"Christoph M","full_name":"Sommer, Christoph M"},{"full_name":"Amberg, Nicole","first_name":"Nicole","orcid":"0000-0002-3183-8207","last_name":"Amberg","id":"4CD6AAC6-F248-11E8-B48F-1D18A9856A87"},{"orcid":"0000-0003-2356-9403","last_name":"Venturino","id":"41CB84B2-F248-11E8-B48F-1D18A9856A87","first_name":"Alessandro","full_name":"Venturino, Alessandro"},{"first_name":"Karl","last_name":"Roessler","full_name":"Roessler, Karl"},{"last_name":"Czech","first_name":"Thomas","full_name":"Czech, Thomas"},{"last_name":"Höftberger","first_name":"Romana","full_name":"Höftberger, Romana"},{"full_name":"Siegert, Sandra","id":"36ACD32E-F248-11E8-B48F-1D18A9856A87","last_name":"Siegert","orcid":"0000-0001-8635-0877","first_name":"Sandra"},{"id":"3E57A680-F248-11E8-B48F-1D18A9856A87","last_name":"Novarino","orcid":"0000-0002-7673-7178","first_name":"Gaia","full_name":"Novarino, Gaia"},{"first_name":"Peter M","orcid":"0000-0001-5001-4804","id":"353C1B58-F248-11E8-B48F-1D18A9856A87","last_name":"Jonas","full_name":"Jonas, Peter M"},{"full_name":"Danzl, Johann G","last_name":"Danzl","id":"42EFD3B6-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0001-8559-3973","first_name":"Johann G"}],"acknowledged_ssus":[{"_id":"ScienComp"},{"_id":"Bio"},{"_id":"PreCl"},{"_id":"LifeSc"},{"_id":"M-Shop"},{"_id":"E-Lib"}],"publication_identifier":{"issn":["1087-0156"],"eissn":["1546-1696"]},"article_processing_charge":"Yes (in subscription journal)","acknowledgement":"We thank J. Vorlaufer, N. Agudelo-Dueñas, W. Jahr and A. Wartak for microscope maintenance and troubleshooting; C. Kreuzinger, A. Freeman and I. Erber for technical assistance; and M. Tomschik for support with obtaining human samples. We gratefully acknowledge E. Miguel for setting up webKnossos and M. Šuplata for computational support and hardware control. We are grateful to R. Shigemoto and B. Bickel for generous support and M. Sixt and S. Boyd (Stanford University) for discussions and critical reading of the paper. PSD95-HaloTag mice were kindly provided by S. Grant (University of Edinburgh). We acknowledge expert support by Institute of Science and Technology Austria’s scientific computing, imaging and optics, preclinical and lab support facilities and by the Miba machine shop and library. We gratefully acknowledge funding by the following sources: Austrian Science Fund (FWF) grant I3600-B27 (J.G.D.); Austrian Science Fund (FWF) grant DK W1232 (J.G.D. and J.M.M.); Austrian Science Fund (FWF) grant Z 312-B27, Wittgenstein award (P.J.); Austrian Science Fund (FWF) projects I4685-B, I6565-B (SYNABS) and DOC 33-B27 (R.H.); Gesellschaft für Forschungsförderung NÖ (NFB) grant LSC18-022 (J.G.D.); European Union’s Horizon 2020 research and innovation programme, European Research Council (ERC) grant 715508 – REVERSEAUTISM (G.N.); European Union’s Horizon 2020 research and innovation programme, European Research Council (ERC) grant 692692 – GIANTSYN (P.J.); Marie Skłodowska-Curie Actions Fellowship GA no. 665385 under the EU Horizon 2020 program (J.M.M. and J.L.); and Marie Skłodowska-Curie Actions Individual Fellowship no. 101026635 under the EU Horizon 2020 program (J.F.W.).","date_created":"2023-09-03T22:01:15Z","department":[{"_id":"SaSi"},{"_id":"GaNo"},{"_id":"PeJo"},{"_id":"JoDa"},{"_id":"Bio"},{"_id":"RySh"}],"related_material":{"record":[{"status":"deleted","id":"18660","relation":"dissertation_contains"},{"relation":"research_data","id":"13126","status":"public"},{"status":"public","id":"18674","relation":"dissertation_contains"}],"link":[{"url":"https://github.com/danzllab/CATS","relation":"software"}]},"page":"1051-1064","OA_place":"publisher","project":[{"call_identifier":"FWF","grant_number":"I03600","name":"Optical control of synaptic function via adhesion molecules","_id":"265CB4D0-B435-11E9-9278-68D0E5697425"},{"name":"Molecular Drug Targets","_id":"2548AE96-B435-11E9-9278-68D0E5697425","grant_number":"W1232","call_identifier":"FWF"},{"_id":"25C5A090-B435-11E9-9278-68D0E5697425","name":"Synaptic communication in neuronal microcircuits","call_identifier":"FWF","grant_number":"Z00312"},{"grant_number":"LS18-022","_id":"23889792-32DE-11EA-91FC-C7463DDC885E","name":"High content imaging to decode human immune cell interactions in health and allergic disease"},{"grant_number":"715508","call_identifier":"H2020","name":"Probing the Reversibility of Autism Spectrum Disorders by Employing in vivo and in vitro Models","_id":"25444568-B435-11E9-9278-68D0E5697425"},{"call_identifier":"H2020","grant_number":"692692","_id":"25B7EB9E-B435-11E9-9278-68D0E5697425","name":"Biophysics and circuit function of a giant cortical glutamatergic synapse"},{"name":"International IST Doctoral Program","_id":"2564DBCA-B435-11E9-9278-68D0E5697425","grant_number":"665385","call_identifier":"H2020"},{"name":"Synaptic computations of the hippocampal CA3 circuitry","_id":"fc2be41b-9c52-11eb-aca3-faa90aa144e9","call_identifier":"H2020","grant_number":"101026635"}],"publication":"Nature Biotechnology","year":"2024","volume":42,"external_id":{"isi":["001065254200001"],"pmid":["37653226"]},"title":"Imaging brain tissue architecture across millimeter to nanometer scales","article_type":"original"},{"file":[{"relation":"main_file","content_type":"application/pdf","date_updated":"2024-12-03T08:56:53Z","access_level":"open_access","creator":"dernst","file_name":"2024_PloSBio_Kim.pdf","file_size":3057631,"success":1,"file_id":"18608","date_created":"2024-12-03T08:56:53Z","checksum":"7de2dcb50deb65dde05c80082bb85a82"}],"corr_author":"1","day":"18","APC_amount":"6248,82 EUR","language":[{"iso":"eng"}],"oa":1,"ec_funded":1,"oa_version":"Published Version","date_updated":"2026-04-16T12:20:34Z","issue":"11","user_id":"317138e5-6ab7-11ef-aa6d-ffef3953e345","doi":"10.1371/journal.pbio.3002879","pmid":1,"month":"11","OA_type":"gold","tmp":{"short":"CC BY (4.0)","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode"},"status":"public","date_published":"2024-11-18T00:00:00Z","ddc":["570"],"abstract":[{"lang":"eng","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 rodent 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."}],"publication_status":"published","isi":1,"DOAJ_listed":"1","type":"journal_article","publisher":"Public Library of Science","intvolume":"        22","_id":"18603","file_date_updated":"2024-12-03T08:56:53Z","author":[{"full_name":"Kim, Olena","first_name":"Olena","last_name":"Kim","id":"3F8ABDDA-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0003-2344-1039"},{"first_name":"Yuji","id":"3337E116-F248-11E8-B48F-1D18A9856A87","last_name":"Okamoto","orcid":"0000-0003-0408-6094","full_name":"Okamoto, Yuji"},{"id":"3F99E422-F248-11E8-B48F-1D18A9856A87","last_name":"Kaufmann","orcid":"0000-0001-9735-5315","first_name":"Walter","full_name":"Kaufmann, Walter"},{"full_name":"Brose, Nils","first_name":"Nils","last_name":"Brose"},{"full_name":"Shigemoto, Ryuichi","orcid":"0000-0001-8761-9444","last_name":"Shigemoto","id":"499F3ABC-F248-11E8-B48F-1D18A9856A87","first_name":"Ryuichi"},{"first_name":"Peter M","orcid":"0000-0001-5001-4804","last_name":"Jonas","id":"353C1B58-F248-11E8-B48F-1D18A9856A87","full_name":"Jonas, Peter M"}],"citation":{"ama":"Kim O, Okamoto Y, Kaufmann W, Brose N, Shigemoto R, Jonas PM. Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons. <i>PLoS Biology</i>. 2024;22(11). doi:<a href=\"https://doi.org/10.1371/journal.pbio.3002879\">10.1371/journal.pbio.3002879</a>","ieee":"O. Kim, Y. Okamoto, W. Kaufmann, N. Brose, R. Shigemoto, and P. M. Jonas, “Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons,” <i>PLoS Biology</i>, vol. 22, no. 11. Public Library of Science, 2024.","ista":"Kim O, Okamoto Y, Kaufmann W, Brose N, Shigemoto R, Jonas PM. 2024. Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons. PLoS Biology. 22(11), e3002879.","mla":"Kim, Olena, et al. “Presynaptic CAMP-PKA-Mediated Potentiation Induces Reconfiguration of Synaptic Vesicle Pools and Channel-Vesicle Coupling at Hippocampal Mossy Fiber Boutons.” <i>PLoS Biology</i>, vol. 22, no. 11, e3002879, Public Library of Science, 2024, doi:<a href=\"https://doi.org/10.1371/journal.pbio.3002879\">10.1371/journal.pbio.3002879</a>.","chicago":"Kim, Olena, Yuji Okamoto, Walter Kaufmann, Nils Brose, Ryuichi Shigemoto, and Peter M Jonas. “Presynaptic CAMP-PKA-Mediated Potentiation Induces Reconfiguration of Synaptic Vesicle Pools and Channel-Vesicle Coupling at Hippocampal Mossy Fiber Boutons.” <i>PLoS Biology</i>. Public Library of Science, 2024. <a href=\"https://doi.org/10.1371/journal.pbio.3002879\">https://doi.org/10.1371/journal.pbio.3002879</a>.","apa":"Kim, O., Okamoto, Y., Kaufmann, W., Brose, N., Shigemoto, R., &#38; Jonas, P. M. (2024). Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons. <i>PLoS Biology</i>. Public Library of Science. <a href=\"https://doi.org/10.1371/journal.pbio.3002879\">https://doi.org/10.1371/journal.pbio.3002879</a>","short":"O. Kim, Y. Okamoto, W. Kaufmann, N. Brose, R. Shigemoto, P.M. Jonas, PLoS Biology 22 (2024)."},"scopus_import":"1","article_number":"e3002879","quality_controlled":"1","has_accepted_license":"1","department":[{"_id":"PeJo"},{"_id":"EM-Fac"},{"_id":"RySh"}],"publication_identifier":{"eissn":["1545-7885"],"issn":["1544-9173"]},"acknowledged_ssus":[{"_id":"EM-Fac"},{"_id":"PreCl"}],"article_processing_charge":"Yes","date_created":"2024-12-01T23:01:54Z","acknowledgement":"We thank Carolina Borges-Merjane, Jing-Jing Chen, Katharina Lichter, and Samuel Young for critically reading the manuscript; the Electron Microscopy Facility of ISTA, in particular Vanessa Zheden, for extensive support, advice, and experimental assistance; the Preclinical Facility of ISTA, in particular Victoria Wimmer and Michael Schunn, for experimental assistance; Florian Marr and Christina Altmutter for technical support; Alois Schlögl for help with analysis; and Eleftheria Kralli-Beller for manuscript editing. We also thank Cordelia Imig for providing Munc13-1cKO-Munc13-2/3(−/−) mutant mice. Part of the work has been published in O.K.’s thesis in partial fulfillment of the requirements for the degree of Doctor of Philosophy.\r\nThis project received funding from the European Research Council and European Union’s Horizon 2020 research and innovation programme (ERC 692692 to P.J.; https://cordis.europa.eu/project/id/692692/de) and from the Fond zur Förderung der Wissenschaftlichen Forschung (Z312-B27 Wittgenstein award to P.J., https://www.fwf.ac.at/en/funding/portfolio/projects/fwf-wittgenstein-award; W1205-B09 and P36232-B to P.J., https://www.fwf.ac.at/en/funding; I6166-B to R.S.; https://www.fwf.ac.at/en/funding). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.","project":[{"_id":"25B7EB9E-B435-11E9-9278-68D0E5697425","name":"Biophysics and circuit function of a giant cortical glutamatergic synapse","call_identifier":"H2020","grant_number":"692692"},{"grant_number":"Z00312","call_identifier":"FWF","_id":"25C5A090-B435-11E9-9278-68D0E5697425","name":"Synaptic communication in neuronal microcircuits"},{"_id":"bd88be38-d553-11ed-ba76-81d5a70a6ef5","name":"Mechanisms of GABA release in hippocampal circuits","grant_number":"P36232"},{"grant_number":"I06166","_id":"b1b85715-d554-11ed-a5ad-84a07fc9f18e","name":"Structural & functional basis of presynaptic plasticity"},{"call_identifier":"FWF","grant_number":"W01205","_id":"25C3DBB6-B435-11E9-9278-68D0E5697425","name":"Zellkommunikation in Gesundheit und Krankheit"},{"call_identifier":"FWF","name":"FWF Open Access Fund","_id":"3AC91DDA-15DF-11EA-824D-93A3E7B544D1"}],"publication":"PLoS Biology","year":"2024","volume":22,"external_id":{"pmid":["39556620"],"isi":["001358568700003"]},"title":"Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons","article_type":"original","related_material":{"record":[{"relation":"research_data","id":"18296","status":"public"}]},"OA_place":"publisher"},{"author":[{"full_name":"Kim, Olena","last_name":"Kim","id":"3F8ABDDA-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0003-2344-1039","first_name":"Olena"}],"_id":"18296","file_date_updated":"2024-10-11T10:04:23Z","has_accepted_license":"1","citation":{"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).","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>.","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.","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>.","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>.","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>"},"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"],"type":"research_data","publisher":"Institute of Science and Technology Austria","title":"Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons","year":"2024","project":[{"_id":"25B7EB9E-B435-11E9-9278-68D0E5697425","name":"Biophysics and circuit function of a giant cortical glutamatergic synapse","call_identifier":"H2020","grant_number":"692692"}],"related_material":{"record":[{"id":"18603","status":"public","relation":"used_in_publication"}]},"department":[{"_id":"PeJo"},{"_id":"RySh"},{"_id":"EM-Fac"}],"date_created":"2024-10-11T10:12:17Z","article_processing_charge":"No","contributor":[{"first_name":"Olena","id":"3F8ABDDA-F248-11E8-B48F-1D18A9856A87","last_name":"Kim","contributor_type":"researcher"},{"id":"3337E116-F248-11E8-B48F-1D18A9856A87","last_name":"Okamoto","orcid":"0000-0003-0408-6094","first_name":"Yuji","contributor_type":"researcher"},{"first_name":"Walter","orcid":"0000-0001-9735-5315","last_name":"Kaufmann","id":"3F99E422-F248-11E8-B48F-1D18A9856A87","contributor_type":"researcher"},{"last_name":"Brose","first_name":"Nils ","contributor_type":"researcher"},{"contributor_type":"researcher","orcid":"0000-0001-8761-9444","id":"499F3ABC-F248-11E8-B48F-1D18A9856A87","last_name":"Shigemoto","first_name":"Ryuichi"},{"first_name":"Peter M","orcid":"0000-0001-5001-4804","id":"353C1B58-F248-11E8-B48F-1D18A9856A87","last_name":"Jonas","contributor_type":"supervisor"}],"oa":1,"ec_funded":1,"date_updated":"2026-04-16T12:20:33Z","oa_version":"Submitted Version","corr_author":"1","file":[{"file_id":"18297","date_created":"2024-10-11T10:04:19Z","checksum":"0a977e7df54c418251b10dfd3f8a015c","file_name":"Kim_et_al_2024_PlosBio_Source_data.zip","file_size":164382,"success":1,"date_updated":"2024-10-11T10:04:19Z","access_level":"open_access","creator":"okim","relation":"main_file","content_type":"application/zip"},{"checksum":"5b9343d6b2035ac3185e390fad4d3830","file_id":"18298","date_created":"2024-10-11T10:04:23Z","file_name":"info.txt","file_size":654,"success":1,"access_level":"open_access","creator":"okim","date_updated":"2024-10-11T10:04:23Z","relation":"main_file","content_type":"text/plain"}],"day":"11","date_published":"2024-10-11T00:00:00Z","status":"public","abstract":[{"lang":"eng","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."}],"ddc":["570"],"doi":"10.15479/AT:ISTA:18296","user_id":"68b8ca59-c5b3-11ee-8790-cd641c68093d","tmp":{"short":"CC BY (4.0)","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode"},"month":"10"},{"day":"20","file":[{"date_created":"2024-03-12T13:42:42Z","file_id":"15110","checksum":"b25b2a057c266ff317a48b0d54d6fc8a","success":1,"file_name":"2024_PNAS_Koppensteiner.pdf","file_size":13648221,"date_updated":"2024-03-12T13:42:42Z","creator":"dernst","access_level":"open_access","content_type":"application/pdf","relation":"main_file"}],"corr_author":"1","oa_version":"Published Version","date_updated":"2026-05-02T22:30:24Z","issue":"8","APC_amount":"5887,8 EUR","oa":1,"ec_funded":1,"language":[{"iso":"eng"}],"month":"02","OA_type":"hybrid","tmp":{"name":"Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0)","legal_code_url":"https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode","short":"CC BY-NC-ND (4.0)","image":"/images/cc_by_nc_nd.png"},"user_id":"317138e5-6ab7-11ef-aa6d-ffef3953e345","doi":"10.1073/pnas.2301449121","pmid":1,"ddc":["570"],"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."}],"publication_status":"published","status":"public","date_published":"2024-02-20T00:00:00Z","publisher":"National Academy of Sciences","intvolume":"       121","isi":1,"type":"journal_article","citation":{"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.","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>.","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>","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>","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).","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>."},"quality_controlled":"1","article_number":"e2301449121","scopus_import":"1","has_accepted_license":"1","file_date_updated":"2024-03-12T13:42:42Z","_id":"15084","author":[{"full_name":"Koppensteiner, Peter","first_name":"Peter","orcid":"0000-0002-3509-1948","last_name":"Koppensteiner","id":"3B8B25A8-F248-11E8-B48F-1D18A9856A87"},{"orcid":"0000-0003-0863-4481","last_name":"Bhandari","id":"45EDD1BC-F248-11E8-B48F-1D18A9856A87","first_name":"Pradeep","full_name":"Bhandari, Pradeep"},{"full_name":"Önal, Hüseyin C","first_name":"Hüseyin C","orcid":"0000-0002-2771-2011","id":"4659D740-F248-11E8-B48F-1D18A9856A87","last_name":"Önal"},{"full_name":"Borges Merjane, Carolina","orcid":"0000-0003-0005-401X","last_name":"Borges Merjane","id":"4305C450-F248-11E8-B48F-1D18A9856A87","first_name":"Carolina"},{"full_name":"Le Monnier, Elodie","id":"3B59276A-F248-11E8-B48F-1D18A9856A87","last_name":"Le Monnier","first_name":"Elodie"},{"first_name":"Utsa","last_name":"Roy","id":"4d26cf11-5355-11ee-ae5a-eb05e255b9b2","full_name":"Roy, Utsa"},{"full_name":"Nakamura, Yukihiro","last_name":"Nakamura","first_name":"Yukihiro"},{"full_name":"Sadakata, Tetsushi","first_name":"Tetsushi","last_name":"Sadakata"},{"last_name":"Sanbo","first_name":"Makoto","full_name":"Sanbo, Makoto"},{"full_name":"Hirabayashi, Masumi","first_name":"Masumi","last_name":"Hirabayashi"},{"full_name":"Rhee, JeongSeop","first_name":"JeongSeop","last_name":"Rhee"},{"first_name":"Nils","last_name":"Brose","full_name":"Brose, Nils"},{"orcid":"0000-0001-5001-4804","id":"353C1B58-F248-11E8-B48F-1D18A9856A87","last_name":"Jonas","first_name":"Peter M","full_name":"Jonas, Peter M"},{"full_name":"Shigemoto, Ryuichi","orcid":"0000-0001-8761-9444","id":"499F3ABC-F248-11E8-B48F-1D18A9856A87","last_name":"Shigemoto","first_name":"Ryuichi"}],"acknowledged_ssus":[{"_id":"M-Shop"},{"_id":"PreCl"},{"_id":"EM-Fac"}],"publication_identifier":{"eissn":["1091-6490"],"issn":["0027-8424"]},"article_processing_charge":"Yes (in subscription journal)","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.","date_created":"2024-03-05T09:23:55Z","department":[{"_id":"RySh"},{"_id":"PeJo"}],"related_material":{"record":[{"relation":"research_data","status":"public","id":"13173"},{"status":"public","id":"19271","relation":"dissertation_contains"}],"link":[{"relation":"press_release","description":"News on ISTA Website","url":"https://ista.ac.at/en/news/neuronal-insights-flash-and-freeze-fracture/"}]},"OA_place":"publisher","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","grant_number":"694539","call_identifier":"H2020"},{"_id":"2564DBCA-B435-11E9-9278-68D0E5697425","name":"International IST Doctoral Program","call_identifier":"H2020","grant_number":"665385"}],"publication":"Proceedings of the National Academy of Sciences of the United States of America","year":"2024","volume":121,"external_id":{"pmid":["38346189"],"isi":["001208567300006"]},"article_type":"original","title":"GABAB receptors induce phasic release from medial habenula terminals through activity-dependent recruitment of release-ready vesicles"},{"status":"public","date_published":"2024-03-06T00:00:00Z","ddc":["570"],"publication_status":"published","abstract":[{"lang":"eng","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."}],"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","doi":"10.1016/j.neuron.2023.12.002","pmid":1,"month":"03","OA_type":"hybrid","tmp":{"short":"CC BY (4.0)","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode"},"oa":1,"ec_funded":1,"language":[{"iso":"eng"}],"oa_version":"Published Version","date_updated":"2026-05-02T22:30:25Z","issue":"5","file":[{"relation":"main_file","content_type":"application/pdf","date_updated":"2025-04-23T14:02:08Z","access_level":"open_access","creator":"dernst","file_size":8192355,"file_name":"2024_Neuron_Chen.pdf","success":1,"file_id":"19614","date_created":"2025-04-23T14:02:08Z","checksum":"30098b4f0209556ddfb3540a23d07ca5"}],"corr_author":"1","day":"06","project":[{"name":"Biophysics and circuit function of a giant cortical glutamatergic synapse","_id":"25B7EB9E-B435-11E9-9278-68D0E5697425","grant_number":"692692","call_identifier":"H2020"},{"name":"Synaptic communication in neuronal microcircuits","_id":"25C5A090-B435-11E9-9278-68D0E5697425","call_identifier":"FWF","grant_number":"Z00312"},{"grant_number":"P36232","name":"Mechanisms of GABA release in hippocampal circuits","_id":"bd88be38-d553-11ed-ba76-81d5a70a6ef5"},{"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"}],"publication":"Neuron","year":"2024","volume":112,"external_id":{"pmid":["38215739"],"isi":["001202925700001"]},"article_type":"original","title":"Developmental transformation of Ca2+ channel-vesicle nanotopography at a central GABAergic synapse","related_material":{"link":[{"url":"https://ista.ac.at/en/news/synapses-brought-to-the-point/","description":"News on ISTA Website","relation":"press_release"}],"record":[{"relation":"dissertation_contains","id":"15101","status":"public"}]},"page":"755-771.e9","OA_place":"publisher","department":[{"_id":"PeJo"},{"_id":"EM-Fac"},{"_id":"RySh"}],"acknowledged_ssus":[{"_id":"EM-Fac"},{"_id":"PreCl"},{"_id":"M-Shop"}],"publication_identifier":{"eissn":["1097-4199"],"issn":["0896-6273"]},"article_processing_charge":"Yes (via OA deal)","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.","date_created":"2024-01-21T23:00:56Z","_id":"14843","file_date_updated":"2025-04-23T14:02:08Z","author":[{"last_name":"Chen","id":"2C4E65C8-F248-11E8-B48F-1D18A9856A87","first_name":"JingJing","full_name":"Chen, JingJing"},{"full_name":"Kaufmann, Walter","first_name":"Walter","orcid":"0000-0001-9735-5315","last_name":"Kaufmann","id":"3F99E422-F248-11E8-B48F-1D18A9856A87"},{"full_name":"Chen, Chong","first_name":"Chong","last_name":"Chen","id":"3DFD581A-F248-11E8-B48F-1D18A9856A87"},{"last_name":"Arai","id":"32A73F6C-F248-11E8-B48F-1D18A9856A87","first_name":"Itaru","full_name":"Arai, Itaru"},{"full_name":"Kim, Olena","last_name":"Kim","id":"3F8ABDDA-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0003-2344-1039","first_name":"Olena"},{"full_name":"Shigemoto, Ryuichi","orcid":"0000-0001-8761-9444","id":"499F3ABC-F248-11E8-B48F-1D18A9856A87","last_name":"Shigemoto","first_name":"Ryuichi"},{"id":"353C1B58-F248-11E8-B48F-1D18A9856A87","last_name":"Jonas","orcid":"0000-0001-5001-4804","first_name":"Peter M","full_name":"Jonas, Peter M"}],"citation":{"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.","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>.","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.","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>","short":"J. Chen, W. Kaufmann, C. Chen,  itaru Arai, O. Kim, R. Shigemoto, P.M. Jonas, Neuron 112 (2024) 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>","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>."},"scopus_import":"1","quality_controlled":"1","has_accepted_license":"1","isi":1,"type":"journal_article","PlanS_conform":"1","publisher":"Elsevier","intvolume":"       112"},{"day":"26","file":[{"relation":"main_file","content_type":"application/pdf","access_level":"open_access","creator":"dernst","date_updated":"2023-09-06T06:50:07Z","file_name":"2023_NatureComm_Vierra.pdf","file_size":9412549,"success":1,"checksum":"6ab8aab4e957f626a09a1c73db3388fb","file_id":"14270","date_created":"2023-09-06T06:50:07Z"}],"date_updated":"2025-09-09T12:50:49Z","oa_version":"Published Version","oa":1,"language":[{"iso":"eng"}],"month":"08","tmp":{"short":"CC BY (4.0)","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode"},"user_id":"317138e5-6ab7-11ef-aa6d-ffef3953e345","pmid":1,"doi":"10.1038/s41467-023-40930-6","ddc":["570"],"abstract":[{"lang":"eng","text":"Junctions between the endoplasmic reticulum (ER) and the plasma membrane (PM) are specialized membrane contacts ubiquitous in eukaryotic cells. Concentration of intracellular signaling machinery near ER-PM junctions allows these domains to serve critical roles in lipid and Ca2+ signaling and homeostasis. Subcellular compartmentalization of protein kinase A (PKA) signaling also regulates essential cellular functions, however, no specific association between PKA and ER-PM junctional domains is known. Here, we show that in brain neurons type I PKA is directed to Kv2.1 channel-dependent ER-PM junctional domains via SPHKAP, a type I PKA-specific anchoring protein. SPHKAP association with type I PKA regulatory subunit RI and ER-resident VAP proteins results in the concentration of type I PKA between stacked ER cisternae associated with ER-PM junctions. This ER-associated PKA signalosome enables reciprocal regulation between PKA and Ca2+ signaling machinery to support Ca2+ influx and excitation-transcription coupling. These data reveal that neuronal ER-PM junctions support a receptor-independent form of PKA signaling driven by membrane depolarization and intracellular Ca2+, allowing conversion of information encoded in electrical signals into biochemical changes universally recognized throughout the cell."}],"publication_status":"published","status":"public","date_published":"2023-08-26T00:00:00Z","publisher":"Springer Nature","intvolume":"        14","isi":1,"type":"journal_article","citation":{"ama":"Vierra NC, Ribeiro-Silva L, Kirmiz M, et al. Neuronal ER-plasma membrane junctions couple excitation to Ca2+-activated PKA signaling. <i>Nature Communications</i>. 2023;14. doi:<a href=\"https://doi.org/10.1038/s41467-023-40930-6\">10.1038/s41467-023-40930-6</a>","mla":"Vierra, Nicholas C., et al. “Neuronal ER-Plasma Membrane Junctions Couple Excitation to Ca2+-Activated PKA Signaling.” <i>Nature Communications</i>, vol. 14, 5231, Springer Nature, 2023, doi:<a href=\"https://doi.org/10.1038/s41467-023-40930-6\">10.1038/s41467-023-40930-6</a>.","ista":"Vierra NC, Ribeiro-Silva L, Kirmiz M, Van Der List D, Bhandari P, Mack OA, Carroll J, Le Monnier E, Aicher SA, Shigemoto R, Trimmer JS. 2023. Neuronal ER-plasma membrane junctions couple excitation to Ca2+-activated PKA signaling. Nature Communications. 14, 5231.","ieee":"N. C. Vierra <i>et al.</i>, “Neuronal ER-plasma membrane junctions couple excitation to Ca2+-activated PKA signaling,” <i>Nature Communications</i>, vol. 14. Springer Nature, 2023.","chicago":"Vierra, Nicholas C., Luisa Ribeiro-Silva, Michael Kirmiz, Deborah Van Der List, Pradeep Bhandari, Olivia A. Mack, James Carroll, et al. “Neuronal ER-Plasma Membrane Junctions Couple Excitation to Ca2+-Activated PKA Signaling.” <i>Nature Communications</i>. Springer Nature, 2023. <a href=\"https://doi.org/10.1038/s41467-023-40930-6\">https://doi.org/10.1038/s41467-023-40930-6</a>.","short":"N.C. Vierra, L. Ribeiro-Silva, M. Kirmiz, D. Van Der List, P. Bhandari, O.A. Mack, J. Carroll, E. Le Monnier, S.A. Aicher, R. Shigemoto, J.S. Trimmer, Nature Communications 14 (2023).","apa":"Vierra, N. C., Ribeiro-Silva, L., Kirmiz, M., Van Der List, D., Bhandari, P., Mack, O. A., … Trimmer, J. S. (2023). Neuronal ER-plasma membrane junctions couple excitation to Ca2+-activated PKA signaling. <i>Nature Communications</i>. Springer Nature. <a href=\"https://doi.org/10.1038/s41467-023-40930-6\">https://doi.org/10.1038/s41467-023-40930-6</a>"},"quality_controlled":"1","article_number":"5231","scopus_import":"1","has_accepted_license":"1","_id":"14253","file_date_updated":"2023-09-06T06:50:07Z","author":[{"first_name":"Nicholas C.","last_name":"Vierra","full_name":"Vierra, Nicholas C."},{"last_name":"Ribeiro-Silva","first_name":"Luisa","full_name":"Ribeiro-Silva, Luisa"},{"full_name":"Kirmiz, Michael","first_name":"Michael","last_name":"Kirmiz"},{"full_name":"Van Der List, Deborah","last_name":"Van Der List","first_name":"Deborah"},{"full_name":"Bhandari, Pradeep","orcid":"0000-0003-0863-4481","last_name":"Bhandari","id":"45EDD1BC-F248-11E8-B48F-1D18A9856A87","first_name":"Pradeep"},{"full_name":"Mack, Olivia A.","first_name":"Olivia A.","last_name":"Mack"},{"first_name":"James","last_name":"Carroll","full_name":"Carroll, James"},{"id":"3B59276A-F248-11E8-B48F-1D18A9856A87","last_name":"Le Monnier","first_name":"Elodie","full_name":"Le Monnier, Elodie"},{"last_name":"Aicher","first_name":"Sue A.","full_name":"Aicher, Sue A."},{"full_name":"Shigemoto, Ryuichi","orcid":"0000-0001-8761-9444","id":"499F3ABC-F248-11E8-B48F-1D18A9856A87","last_name":"Shigemoto","first_name":"Ryuichi"},{"full_name":"Trimmer, James S.","last_name":"Trimmer","first_name":"James S."}],"publication_identifier":{"eissn":["2041-1723"]},"article_processing_charge":"Yes","acknowledgement":"We thank Kayla Templeton and Peter Turcanu for technical assistance, Michelle Salemi for assistance with LC-MS data acquisition and analysis, Dr. Belvin Gong for advice on monoclonal antibody generation, Drs. Maria Casas Prat and Eamonn Dickson for assistance with super-resolution TIRF microscopy, Dr. Oscar Cerda for assistance with the design of TAT-FFAT peptides, Dr. Fernando Santana for helpful discussions, and Dr. Jodi Nunnari for a careful reading of our manuscript. We also thank Dr. Alan Howe, Dr. Sohum Mehta, and Dr. Jin Zhang for providing plasmids used in this study. This project was funded by NIH Grants R01NS114210 and R21NS101648 (J.S.T.), and F32NS108519 (N.C.V.).","date_created":"2023-09-03T22:01:14Z","department":[{"_id":"RySh"}],"publication":"Nature Communications","year":"2023","volume":14,"title":"Neuronal ER-plasma membrane junctions couple excitation to Ca2+-activated PKA signaling","external_id":{"pmid":["37633939"],"isi":["001064563400013"]},"article_type":"original"},{"day":"29","publisher":"Institute of Science and Technology Austria","corr_author":"1","file":[{"creator":"shigemot","access_level":"closed","description":"After review an updated version of the data is provided","date_updated":"2023-11-17T14:30:44Z","title":"Outdated Version","content_type":"application/x-zip-compressed","relation":"main_file","checksum":"ed59170869ba621f89f7c1894092192f","date_created":"2023-06-29T13:11:22Z","file_id":"13174","file_size":542873672,"file_name":"Raw data for Koppensteiner et al.zip"},{"date_updated":"2023-11-17T14:13:02Z","creator":"patrickd","access_level":"open_access","content_type":"application/vnd.openxmlformats-officedocument.spreadsheetml.sheet","relation":"main_file","date_created":"2023-11-17T14:13:02Z","file_id":"14550","checksum":"c07860eb82b4d367245f1b589fe5c250","success":1,"file_name":"11-17-23 Updated Koppensteiner et al. raw data.xlsx","file_size":915079},{"success":1,"file_name":"EM_Images.zip","file_size":544868924,"date_created":"2024-02-06T07:21:43Z","file_id":"14942","checksum":"abf84b1699edac4349dc3a92d466fb7b","content_type":"application/x-zip-compressed","relation":"main_file","date_updated":"2024-02-06T07:21:43Z","creator":"dernst","access_level":"open_access"}],"type":"research_data","oa_version":"Published Version","date_updated":"2025-09-04T12:16:24Z","has_accepted_license":"1","keyword":["medial habenula","GABAB receptor","vesicle release","Flash and Freeze","Flash and Freeze-fracture"],"citation":{"ama":"Shigemoto R. Transition from tonic to phasic neurotransmitter release by presynaptic GABAB receptor activation in medial habenula terminals. 2023. doi:<a href=\"https://doi.org/10.15479/AT:ISTA:13173\">10.15479/AT:ISTA:13173</a>","ieee":"R. Shigemoto, “Transition from tonic to phasic neurotransmitter release by presynaptic GABAB receptor activation in medial habenula terminals.” Institute of Science and Technology Austria, 2023.","mla":"Shigemoto, Ryuichi. <i>Transition from Tonic to Phasic Neurotransmitter Release by Presynaptic GABAB Receptor Activation in Medial Habenula Terminals</i>. Institute of Science and Technology Austria, 2023, doi:<a href=\"https://doi.org/10.15479/AT:ISTA:13173\">10.15479/AT:ISTA:13173</a>.","ista":"Shigemoto R. 2023. Transition from tonic to phasic neurotransmitter release by presynaptic GABAB receptor activation in medial habenula terminals, Institute of Science and Technology Austria, <a href=\"https://doi.org/10.15479/AT:ISTA:13173\">10.15479/AT:ISTA:13173</a>.","chicago":"Shigemoto, Ryuichi. “Transition from Tonic to Phasic Neurotransmitter Release by Presynaptic GABAB Receptor Activation in Medial Habenula Terminals.” Institute of Science and Technology Austria, 2023. <a href=\"https://doi.org/10.15479/AT:ISTA:13173\">https://doi.org/10.15479/AT:ISTA:13173</a>.","short":"R. Shigemoto, (2023).","apa":"Shigemoto, R. (2023). Transition from tonic to phasic neurotransmitter release by presynaptic GABAB receptor activation in medial habenula terminals. Institute of Science and Technology Austria. <a href=\"https://doi.org/10.15479/AT:ISTA:13173\">https://doi.org/10.15479/AT:ISTA:13173</a>"},"_id":"13173","oa":1,"file_date_updated":"2024-02-06T07:21:43Z","author":[{"first_name":"Ryuichi","last_name":"Shigemoto","id":"499F3ABC-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0001-8761-9444","full_name":"Shigemoto, Ryuichi"}],"month":"07","article_processing_charge":"No","date_created":"2023-06-29T13:16:42Z","tmp":{"name":"Creative Commons Attribution-NonCommercial 4.0 International (CC BY-NC 4.0)","legal_code_url":"https://creativecommons.org/licenses/by-nc/4.0/legalcode","short":"CC BY-NC (4.0)","image":"/images/cc_by_nc.png"},"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","doi":"10.15479/AT:ISTA:13173","department":[{"_id":"RySh"}],"ddc":["571"],"abstract":[{"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 at the presynaptic active zone (AZ). Strikingly, tonic and phasic release exhibit distinct coupling distances and are selectively affected by deletion of synaptoporin (SPO) and Ca2+-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. Double pre-embedding immunolabeling confirmed the co-localization of CAPS2 and SPO inside the same terminal. The cytosolic protein CAPS2 showed a synaptic vesicle (SV)-associated distribution similar to the vesicular transmembrane protein SPO. A newly developed “Flash and Freeze-fracture” method 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 a persistent RRP increase. Thus, we discovered structural and molecular mechanisms underlying tonic and phasic neurotransmitter release and their transition by GBR activation in MHb terminals.","lang":"eng"}],"related_material":{"record":[{"relation":"used_in_publication","status":"public","id":"15084"}]},"date_published":"2023-07-29T00:00:00Z","title":"Transition from tonic to phasic neurotransmitter release by presynaptic GABAB receptor activation in medial habenula terminals","year":"2023","status":"public"},{"has_accepted_license":"1","quality_controlled":"1","scopus_import":"1","citation":{"apa":"Eguchi, K., Le Monnier, E., &#38; Shigemoto, R. (2023). Nanoscale phosphoinositide distribution on cell membranes of mouse cerebellar neurons. <i>The Journal of Neuroscience</i>. Society for Neuroscience. <a href=\"https://doi.org/10.1523/JNEUROSCI.1514-22.2023\">https://doi.org/10.1523/JNEUROSCI.1514-22.2023</a>","short":"K. Eguchi, E. Le Monnier, R. Shigemoto, The Journal of Neuroscience 43 (2023) 4197–4216.","chicago":"Eguchi, Kohgaku, Elodie Le Monnier, and Ryuichi Shigemoto. “Nanoscale Phosphoinositide Distribution on Cell Membranes of Mouse Cerebellar Neurons.” <i>The Journal of Neuroscience</i>. Society for Neuroscience, 2023. <a href=\"https://doi.org/10.1523/JNEUROSCI.1514-22.2023\">https://doi.org/10.1523/JNEUROSCI.1514-22.2023</a>.","ieee":"K. Eguchi, E. Le Monnier, and R. Shigemoto, “Nanoscale phosphoinositide distribution on cell membranes of mouse cerebellar neurons,” <i>The Journal of Neuroscience</i>, vol. 43, no. 23. Society for Neuroscience, pp. 4197–4216, 2023.","mla":"Eguchi, Kohgaku, et al. “Nanoscale Phosphoinositide Distribution on Cell Membranes of Mouse Cerebellar Neurons.” <i>The Journal of Neuroscience</i>, vol. 43, no. 23, Society for Neuroscience, 2023, pp. 4197–216, doi:<a href=\"https://doi.org/10.1523/JNEUROSCI.1514-22.2023\">10.1523/JNEUROSCI.1514-22.2023</a>.","ista":"Eguchi K, Le Monnier E, Shigemoto R. 2023. Nanoscale phosphoinositide distribution on cell membranes of mouse cerebellar neurons. The Journal of Neuroscience. 43(23), 4197–4216.","ama":"Eguchi K, Le Monnier E, Shigemoto R. Nanoscale phosphoinositide distribution on cell membranes of mouse cerebellar neurons. <i>The Journal of Neuroscience</i>. 2023;43(23):4197-4216. doi:<a href=\"https://doi.org/10.1523/JNEUROSCI.1514-22.2023\">10.1523/JNEUROSCI.1514-22.2023</a>"},"author":[{"full_name":"Eguchi, Kohgaku","first_name":"Kohgaku","id":"2B7846DC-F248-11E8-B48F-1D18A9856A87","last_name":"Eguchi","orcid":"0000-0002-6170-2546"},{"full_name":"Le Monnier, Elodie","last_name":"Le Monnier","id":"3B59276A-F248-11E8-B48F-1D18A9856A87","first_name":"Elodie"},{"full_name":"Shigemoto, Ryuichi","orcid":"0000-0001-8761-9444","last_name":"Shigemoto","id":"499F3ABC-F248-11E8-B48F-1D18A9856A87","first_name":"Ryuichi"}],"_id":"13202","file_date_updated":"2023-07-10T09:04:58Z","intvolume":"        43","publisher":"Society for Neuroscience","type":"journal_article","isi":1,"page":"4197-4216","article_type":"original","title":"Nanoscale phosphoinositide distribution on cell membranes of mouse cerebellar neurons","external_id":{"pmid":["37160366"],"isi":["001020132100005"]},"volume":43,"year":"2023","project":[{"call_identifier":"H2020","grant_number":"793482","name":"Ultrastructural analysis of phosphoinositides in nerve terminals: distribution, dynamics and physiological roles in synaptic transmission","_id":"2659CC84-B435-11E9-9278-68D0E5697425"},{"_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"}],"publication":"The Journal of Neuroscience","acknowledgement":"This work was supported by The Institute of Science and Technology (IST) Austria, the European Union's Horizon 2020 Research and Innovation Program under the Marie Skłodowska-Curie Grant Agreement No. 793482 (to K.E.) and by the European Research Council (ERC) Grant Agreement No. 694539 (to R.S.). We thank Nicoleta Condruz (IST Austria, Klosterneuburg, Austria) for technical assistance with sample preparation, the Electron Microscopy Facility of IST Austria (Klosterneuburg, Austria) for technical support with EM works, Natalia Baranova (University of Vienna, Vienna, Austria) and Martin Loose (IST Austria, Klosterneuburg, Austria) for advice on liposome preparation, and Yugo Fukazawa (University of Fukui, Fukui, Japan) for comments.","date_created":"2023-07-09T22:01:12Z","article_processing_charge":"No","acknowledged_ssus":[{"_id":"EM-Fac"}],"publication_identifier":{"eissn":["1529-2401"],"issn":["0270-6474"]},"department":[{"_id":"RySh"}],"issue":"23","date_updated":"2025-04-14T07:27:15Z","oa_version":"Published Version","oa":1,"language":[{"iso":"eng"}],"ec_funded":1,"day":"07","corr_author":"1","file":[{"content_type":"application/pdf","relation":"main_file","creator":"alisjak","access_level":"open_access","date_updated":"2023-07-10T09:04:58Z","success":1,"file_name":"2023_JN_Eguchi.pdf","file_size":7794425,"checksum":"70b2141870e0bf1c94fd343e18fdbc32","date_created":"2023-07-10T09:04:58Z","file_id":"13205"}],"abstract":[{"text":"Phosphatidylinositol-4,5-bisphosphate (PI(4,5)P2) plays an essential role in neuronal activities through interaction with various proteins involved in signaling at membranes. However, the distribution pattern of PI(4,5)P2 and the association with these proteins on the neuronal cell membranes remain elusive. In this study, we established a method for visualizing PI(4,5)P2 by SDS-digested freeze-fracture replica labeling (SDS-FRL) to investigate the quantitative nanoscale distribution of PI(4,5)P2 in cryo-fixed brain. We demonstrate that PI(4,5)P2 forms tiny clusters with a mean size of ∼1000 nm2 rather than randomly distributed in cerebellar neuronal membranes in male C57BL/6J mice. These clusters show preferential accumulation in specific membrane compartments of different cell types, in particular, in Purkinje cell (PC) spines and granule cell (GC) presynaptic active zones. Furthermore, we revealed extensive association of PI(4,5)P2 with CaV2.1 and GIRK3 across different membrane compartments, whereas its association with mGluR1α was compartment specific. These results suggest that our SDS-FRL method provides valuable insights into the physiological functions of PI(4,5)P2 in neurons.","lang":"eng"}],"publication_status":"published","ddc":["570"],"date_published":"2023-06-07T00:00:00Z","status":"public","tmp":{"short":"CC BY (4.0)","image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode"},"month":"06","pmid":1,"doi":"10.1523/JNEUROSCI.1514-22.2023","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87"},{"title":"Research data for the publication \"Imaging brain tissue architecture across millimeter to nanometer scales\"","year":"2023","project":[{"_id":"265CB4D0-B435-11E9-9278-68D0E5697425","name":"Optical control of synaptic function via adhesion molecules","call_identifier":"FWF","grant_number":"I03600"},{"grant_number":"W1232-B24","call_identifier":"FWF","_id":"26AA4EF2-B435-11E9-9278-68D0E5697425","name":"Molecular Drug Targets"},{"_id":"25C5A090-B435-11E9-9278-68D0E5697425","name":"Synaptic communication in neuronal microcircuits","grant_number":"Z00312","call_identifier":"FWF"},{"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"},{"grant_number":"715508","call_identifier":"H2020","name":"Probing the Reversibility of Autism Spectrum Disorders by Employing in vivo and in vitro Models","_id":"25444568-B435-11E9-9278-68D0E5697425"},{"_id":"25B7EB9E-B435-11E9-9278-68D0E5697425","name":"Biophysics and circuit function of a giant cortical glutamatergic synapse","call_identifier":"H2020","grant_number":"692692"},{"name":"International IST Doctoral Program","_id":"2564DBCA-B435-11E9-9278-68D0E5697425","grant_number":"665385","call_identifier":"H2020"},{"call_identifier":"H2020","grant_number":"101026635","name":"Synaptic computations of the hippocampal CA3 circuitry","_id":"fc2be41b-9c52-11eb-aca3-faa90aa144e9"}],"related_material":{"record":[{"relation":"used_in_publication","status":"public","id":"14257"}],"link":[{"url":"https://pub.ista.ac.at/group_danzl/data/CATS/","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. ","relation":"research_data"}]},"department":[{"_id":"JoDa"},{"_id":"SaSi"},{"_id":"GaNo"},{"_id":"PeJo"},{"_id":"Bio"},{"_id":"RySh"}],"acknowledgement":"We 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)","date_created":"2023-06-07T07:15:12Z","article_processing_charge":"No","acknowledged_ssus":[{"_id":"ScienComp"},{"_id":"Bio"},{"_id":"PreCl"},{"_id":"LifeSc"},{"_id":"M-Shop"},{"_id":"E-Lib"}],"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","id":"39BDC62C-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0002-2340-7431","first_name":"Philipp"},{"first_name":"Hana","last_name":"Stefanickova","id":"ee3cb6ca-ec98-11ea-ae11-ff703e2254ed"},{"first_name":"Jake","id":"63836096-4690-11EA-BD4E-32803DDC885E","last_name":"Watson","orcid":"0000-0002-8698-3823"},{"last_name":"Cenameri","id":"9ac8f577-2357-11eb-997a-e566c5550886","first_name":"Alban"},{"first_name":"Christoph M","orcid":"0000-0003-1216-9105","last_name":"Sommer","id":"4DF26D8C-F248-11E8-B48F-1D18A9856A87"},{"last_name":"Amberg","id":"4CD6AAC6-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0002-3183-8207","first_name":"Nicole"},{"orcid":"0000-0003-2356-9403","last_name":"Venturino","id":"41CB84B2-F248-11E8-B48F-1D18A9856A87","first_name":"Alessandro"},{"first_name":"Karl","last_name":"Roessler"},{"first_name":"Thomas","last_name":"Czech"},{"first_name":"Romana","last_name":"Höftberger"},{"last_name":"Siegert","id":"36ACD32E-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0001-8635-0877","first_name":"Sandra"},{"orcid":"0000-0002-7673-7178","id":"3E57A680-F248-11E8-B48F-1D18A9856A87","last_name":"Novarino","first_name":"Gaia"},{"last_name":"Jonas","id":"353C1B58-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0001-5001-4804","first_name":"Peter M"}],"author":[{"first_name":"Johann G","id":"42EFD3B6-F248-11E8-B48F-1D18A9856A87","last_name":"Danzl","orcid":"0000-0001-8559-3973","full_name":"Danzl, Johann G"}],"_id":"13126","file_date_updated":"2023-08-04T13:19:47Z","has_accepted_license":"1","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>.","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>","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>.","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."},"type":"research_data","publisher":"Institute of Science and Technology Austria","date_published":"2023-08-04T00:00:00Z","status":"public","abstract":[{"lang":"eng","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."}],"ddc":["610"],"doi":"10.15479/AT:ISTA:13126","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","tmp":{"short":"CC BY-NC-SA (4.0)","image":"/images/cc_by_nc_sa.png","name":"Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)","legal_code_url":"https://creativecommons.org/licenses/by-nc-sa/4.0/legalcode"},"month":"08","ec_funded":1,"oa":1,"oa_version":"Published 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