{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,2]],"date-time":"2025-12-02T15:06:57Z","timestamp":1764688017278,"version":"build-2065373602"},"reference-count":48,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2022,9,1]],"date-time":"2022-09-01T00:00:00Z","timestamp":1661990400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2022,9,1]],"date-time":"2022-09-01T00:00:00Z","timestamp":1661990400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2022,7,23]],"date-time":"2022-07-23T00:00:00Z","timestamp":1658534400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["clinicalkey.com","clinicalkey.com.au","clinicalkey.es","clinicalkey.fr","clinicalkey.jp","ibroneuroscience.org","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Neuroscience"],"published-print":{"date-parts":[[2022,9]]},"DOI":"10.1016\/j.neuroscience.2022.07.020","type":"journal-article","created":{"date-parts":[[2022,7,22]],"date-time":"2022-07-22T11:48:00Z","timestamp":1658490480000},"page":"142-151","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":5,"special_numbering":"C","title":["Spatio-Temporal Alterations in Synaptic Density During Epileptogenesis in the Rat Brain"],"prefix":"10.1016","volume":"499","author":[{"given":"Jens D.","family":"Mikkelsen","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sanjay S.","family":"Aripaka","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Pablo","family":"Bascu\u00f1ana","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Marion","family":"Bankstahl","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jens P.","family":"Bankstahl","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Burcu A.","family":"Pazarlar","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"78","reference":[{"key":"10.1016\/j.neuroscience.2022.07.020_b0005","doi-asserted-by":"crossref","first-page":"101879","DOI":"10.1016\/j.pneurobio.2020.101879","article-title":"Distinct synaptic vesicle recycling in inhibitory nerve terminals is coordinated by SV2A","volume":"194","author":"Bae","year":"2020","journal-title":"Prog Neurobiol"},{"issue":"4","key":"10.1016\/j.neuroscience.2022.07.020_b0010","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1016\/j.trci.2017.08.004","article-title":"Measuring brain synaptic vesicle protein 2A with positron emission tomography and [(18)F]UCB-H","volume":"3","author":"Bahri","year":"2017","journal-title":"Alzheimers Dement (N Y)"},{"issue":"9","key":"10.1016\/j.neuroscience.2022.07.020_b0015","doi-asserted-by":"crossref","first-page":"5223","DOI":"10.1523\/JNEUROSCI.14-09-05223.1994","article-title":"Differential expression of synaptic vesicle protein 2 (SV2) isoforms","volume":"14","author":"Bajjalieh","year":"1994","journal-title":"J Neurosci"},{"issue":"11","key":"10.1016\/j.neuroscience.2022.07.020_b0020","doi-asserted-by":"crossref","first-page":"2325","DOI":"10.1111\/epi.16353","article-title":"Ex vivo characterization of neuroinflammatory and neuroreceptor changes during epileptogenesis using candidate positron emission tomography biomarkers","volume":"60","author":"Bascunana","year":"2019","journal-title":"Epilepsia"},{"issue":"10","key":"10.1016\/j.neuroscience.2022.07.020_b0025","doi-asserted-by":"crossref","first-page":"2303","DOI":"10.3390\/molecules25102303","article-title":"The Rise of Synaptic Density PET Imaging","volume":"25","author":"Becker","year":"2020","journal-title":"Molecules"},{"issue":"1","key":"10.1016\/j.neuroscience.2022.07.020_b0030","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.eplepsyres.2006.11.008","article-title":"Preferential neuron loss in the rat piriform cortex following pilocarpine-induced status epilepticus","volume":"74","author":"Chen","year":"2007","journal-title":"Epilepsy Res"},{"issue":"10","key":"10.1016\/j.neuroscience.2022.07.020_b0035","doi-asserted-by":"crossref","first-page":"1215","DOI":"10.1001\/jamaneurol.2018.1836","article-title":"Assessing Synaptic Density in Alzheimer Disease With Synaptic Vesicle Glycoprotein 2A Positron Emission Tomographic Imaging","volume":"75","author":"Chen","year":"2018","journal-title":"JAMA Neurol"},{"key":"10.1016\/j.neuroscience.2022.07.020_b0040","doi-asserted-by":"crossref","first-page":"6606","DOI":"10.1038\/ncomms7606","article-title":"Aberrant hippocampal neurogenesis contributes to epilepsy and associated cognitive decline","volume":"6","author":"Cho","year":"2015","journal-title":"Nat Commun"},{"key":"10.1016\/j.neuroscience.2022.07.020_b0045","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1016\/j.yebeh.2018.08.023","article-title":"Differential expression of synaptic vesicle protein 2A after status epilepticus and during epilepsy in a lithium-pilocarpine model","volume":"88","author":"Contreras-Garcia","year":"2018","journal-title":"Epilepsy Behav"},{"issue":"2","key":"10.1016\/j.neuroscience.2022.07.020_b0050","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1016\/S0920-1211(99)00119-9","article-title":"Temporal profile of neuronal injury following pilocarpine or kainic acid-induced status epilepticus","volume":"39","author":"Covolan","year":"2000","journal-title":"Epilepsy Res"},{"issue":"2","key":"10.1016\/j.neuroscience.2022.07.020_b0055","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1111\/nan.12054","article-title":"Expression pattern of synaptic vesicle protein 2 (SV2) isoforms in patients with temporal lobe epilepsy and hippocampal sclerosis","volume":"40","author":"Crevecoeur","year":"2014","journal-title":"Neuropathol Appl Neurobiol"},{"issue":"26","key":"10.1016\/j.neuroscience.2022.07.020_b0060","doi-asserted-by":"crossref","first-page":"15268","DOI":"10.1073\/pnas.96.26.15268","article-title":"Abnormal neurotransmission in mice lacking synaptic vesicle protein 2A (SV2A)","volume":"96","author":"Crowder","year":"1999","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"2","key":"10.1016\/j.neuroscience.2022.07.020_b0065","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1016\/j.jneumeth.2008.04.019","article-title":"The pilocarpine model of temporal lobe epilepsy","volume":"172","author":"Curia","year":"2008","journal-title":"J Neurosci Methods"},{"issue":"3","key":"10.1016\/j.neuroscience.2022.07.020_b0070","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1016\/j.neulet.2011.03.071","article-title":"The time course of acquired epilepsy: implications for therapeutic intervention to suppress epileptogenesis","volume":"497","author":"Dudek","year":"2011","journal-title":"Neurosci Lett"},{"issue":"348","key":"10.1016\/j.neuroscience.2022.07.020_b0075","doi-asserted-by":"crossref","first-page":"348ra396","DOI":"10.1126\/scitranslmed.aaf6667","article-title":"Imaging synaptic density in the living human brain","volume":"8","author":"Finnema","year":"2016","journal-title":"Sci Transl Med"},{"issue":"10","key":"10.1016\/j.neuroscience.2022.07.020_b0080","doi-asserted-by":"crossref","first-page":"2183","DOI":"10.1111\/epi.16653","article-title":"Reduced synaptic vesicle protein 2A binding in temporal lobe epilepsy: A [(11) C]UCB-J positron emission tomography study","volume":"61","author":"Finnema","year":"2020","journal-title":"Epilepsia"},{"issue":"24","key":"10.1016\/j.neuroscience.2022.07.020_b0085","doi-asserted-by":"crossref","first-page":"13311","DOI":"10.1073\/pnas.94.24.13311","article-title":"Disruption of the m1 receptor gene ablates muscarinic receptor-dependent M current regulation and seizure activity in mice","volume":"94","author":"Hamilton","year":"1997","journal-title":"Proc Natl Acad Sci U S A"},{"key":"10.1016\/j.neuroscience.2022.07.020_b0090","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.mcn.2019.02.001","article-title":"Synaptic vesicle protein 2A as a potential biomarker in synaptopathies","volume":"97","author":"Heurling","year":"2019","journal-title":"Mol Cell Neurosci"},{"issue":"1","key":"10.1016\/j.neuroscience.2022.07.020_b0095","doi-asserted-by":"crossref","first-page":"1529","DOI":"10.1038\/s41467-019-09562-7","article-title":"Lower synaptic density is associated with depression severity and network alterations","volume":"10","author":"Holmes","year":"2019","journal-title":"Nat Commun"},{"issue":"4","key":"10.1016\/j.neuroscience.2022.07.020_b0100","doi-asserted-by":"crossref","first-page":"1003","DOI":"10.1016\/S0896-6273(00)81046-6","article-title":"SV2A and SV2B function as redundant Ca2+ regulators in neurotransmitter release","volume":"24","author":"Janz","year":"1999","journal-title":"Neuron"},{"issue":"7","key":"10.1016\/j.neuroscience.2022.07.020_b0105","doi-asserted-by":"crossref","first-page":"1729","DOI":"10.1111\/j.1528-1167.2009.02089.x","article-title":"Proepileptic phenotype of SV2A-deficient mice is associated with reduced anticonvulsant efficacy of levetiracetam","volume":"50","author":"Kaminski","year":"2009","journal-title":"Epilepsia"},{"issue":"2","key":"10.1016\/j.neuroscience.2022.07.020_b0110","doi-asserted-by":"crossref","first-page":"396","DOI":"10.1007\/s00259-018-4119-8","article-title":"Quantifying SV2A density and drug occupancy in the human brain using [(11)C]UCB-J PET imaging and subcortical white matter as reference tissue","volume":"46","author":"Koole","year":"2019","journal-title":"Eur J Nucl Med Mol Imaging"},{"key":"10.1016\/j.neuroscience.2022.07.020_b0115","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1016\/j.neubiorev.2021.08.020","article-title":"The pilocarpine model of mesial temporal lobe epilepsy: Over one decade later, with more rodent species and new investigative approaches","volume":"130","author":"Levesque","year":"2021","journal-title":"Neurosci Biobehav Rev"},{"issue":"12","key":"10.1016\/j.neuroscience.2022.07.020_b0120","doi-asserted-by":"crossref","first-page":"2326","DOI":"10.1111\/j.1528-1167.2011.03315.x","article-title":"Is there a critical period for mossy fiber sprouting in a mouse model of temporal lobe epilepsy?","volume":"52","author":"Lew","year":"2011","journal-title":"Epilepsia"},{"issue":"11","key":"10.1016\/j.neuroscience.2022.07.020_b0125","doi-asserted-by":"crossref","first-page":"1055","DOI":"10.1007\/s40263-016-0384-x","article-title":"Synaptic Vesicle Glycoprotein 2A Ligands in the Treatment of Epilepsy and Beyond","volume":"30","author":"Loscher","year":"2016","journal-title":"CNS Drugs"},{"issue":"26","key":"10.1016\/j.neuroscience.2022.07.020_b0130","doi-asserted-by":"crossref","first-page":"9861","DOI":"10.1073\/pnas.0308208101","article-title":"The synaptic vesicle protein SV2A is the binding site for the antiepileptic drug levetiracetam","volume":"101","author":"Lynch","year":"2004","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"6","key":"10.1016\/j.neuroscience.2022.07.020_b0135","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1016\/j.tins.2005.04.002","article-title":"Impaired and repaired inhibitory circuits in the epileptic human hippocampus","volume":"28","author":"Magloczky","year":"2005","journal-title":"Trends Neurosci"},{"issue":"3","key":"10.1016\/j.neuroscience.2022.07.020_b0140","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1002\/ana.25682","article-title":"Synaptic Changes in Parkinson Disease Assessed with in vivo Imaging","volume":"87","author":"Matuskey","year":"2020","journal-title":"Ann Neurol"},{"issue":"1","key":"10.1016\/j.neuroscience.2022.07.020_b0145","doi-asserted-by":"crossref","first-page":"204","DOI":"10.3390\/ijms23010204","article-title":"Hippocampal Sclerosis in Pilocarpine Epilepsy: Survival of Peptide-Containing Neurons and Learning and Memory Disturbances in the Adult NMRI Strain Mouse","volume":"23","author":"M\u00e1ty\u00e1s","year":"2021","journal-title":"Int J Mol Sci"},{"issue":"4","key":"10.1016\/j.neuroscience.2022.07.020_b0150","doi-asserted-by":"crossref","first-page":"1461","DOI":"10.1523\/JNEUROSCI.3805-10.2011","article-title":"Protein quantification at the single vesicle level reveals that a subset of synaptic vesicle proteins are trafficked with high precision","volume":"31","author":"Mutch","year":"2011","journal-title":"J Neurosci"},{"issue":"5","key":"10.1016\/j.neuroscience.2022.07.020_b0155","doi-asserted-by":"crossref","first-page":"C960","DOI":"10.1152\/ajpcell.00259.2010","article-title":"SV2 regulates neurotransmitter release via multiple mechanisms","volume":"299","author":"Nowack","year":"2010","journal-title":"Am J Physiol Cell Physiol"},{"issue":"2","key":"10.1016\/j.neuroscience.2022.07.020_b0160","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.neulet.2012.01.009","article-title":"Kindling-associated SV2A expression in hilar GABAergic interneurons of the mouse dentate gyrus","volume":"510","author":"Ohno","year":"2012","journal-title":"Neurosci Lett"},{"key":"10.1016\/j.neuroscience.2022.07.020_b0165","doi-asserted-by":"crossref","DOI":"10.1016\/j.eplepsyres.2022.106926","article-title":"Temporal and spatial changes in synaptic vesicle glycoprotein 2A (SV2A) under kainic acid iduced epileptogensis: An autoradiographic study","author":"Pazarlar","year":"2022","journal-title":"Epilepsy Res"},{"issue":"10","key":"10.1016\/j.neuroscience.2022.07.020_b0170","doi-asserted-by":"crossref","first-page":"a022822","DOI":"10.1101\/cshperspect.a022822","article-title":"Epileptogenesis","volume":"5","author":"Pitk\u00e4nen","year":"2015","journal-title":"Cold Spring Harb Perspect Med"},{"issue":"1","key":"10.1016\/j.neuroscience.2022.07.020_b0175","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1016\/j.expneurol.2010.03.014","article-title":"The COX-2 inhibitor parecoxib is neuroprotective but not antiepileptogenic in the pilocarpine model of temporal lobe epilepsy","volume":"224","author":"Polascheck","year":"2010","journal-title":"Exp Neurol"},{"issue":"3","key":"10.1016\/j.neuroscience.2022.07.020_b0180","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1016\/0013-4694(72)90178-2","article-title":"Modification of seizure activity by electrical stimulation. 3. Mechanisms","volume":"32","author":"Racine","year":"1972","journal-title":"Electroencephalogr Clin Neurophysiol"},{"issue":"2\u20133","key":"10.1016\/j.neuroscience.2022.07.020_b0185","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1016\/j.neuropharm.2010.11.005","article-title":"Enhanced susceptibility to the GABA antagonist pentylenetetrazole during the latent period following a pilocarpine-induced status epilepticus in rats","volume":"60","author":"Rattka","year":"2011","journal-title":"Neuropharmacology"},{"key":"10.1016\/j.neuroscience.2022.07.020_b0190","doi-asserted-by":"crossref","first-page":"864514","DOI":"10.3389\/fnins.2022.864514","article-title":"Synaptic Vesicle Glycoprotein 2A: Features and Functions","volume":"16","author":"Rossi","year":"2022","journal-title":"Front Neurosci"},{"issue":"5","key":"10.1016\/j.neuroscience.2022.07.020_b0195","doi-asserted-by":"crossref","first-page":"1197","DOI":"10.1007\/s11307-020-01488-7","article-title":"Exploring with [(18)F]UCB-H the in vivo Variations in SV2A Expression through the Kainic Acid Rat Model of Temporal Lobe Epilepsy","volume":"22","author":"Serrano","year":"2020","journal-title":"Mol Imaging Biol"},{"issue":"1","key":"10.1016\/j.neuroscience.2022.07.020_b0200","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1002\/hipo.450010106","article-title":"Permanently altered hippocampal structure, excitability, and inhibition after experimental status epilepticus in the rat: the \u201cdormant basket cell\u201d hypothesis and its possible relevance to temporal lobe epilepsy","volume":"1","author":"Sloviter","year":"1991","journal-title":"Hippocampus"},{"issue":"5","key":"10.1016\/j.neuroscience.2022.07.020_b0205","doi-asserted-by":"crossref","first-page":"520","DOI":"10.1111\/nan.12150","article-title":"Review: Hippocampal sclerosis in epilepsy: a neuropathology review","volume":"40","author":"Thom","year":"2014","journal-title":"Neuropathol Appl Neurobiol"},{"key":"10.1016\/j.neuroscience.2022.07.020_b0210","doi-asserted-by":"crossref","first-page":"27420","DOI":"10.1038\/srep27420","article-title":"Synaptic vesicle glycoprotein 2A (SV2A) regulates kindling epileptogenesis via GABAergic neurotransmission","volume":"6","author":"Tokudome","year":"2016","journal-title":"Sci Rep"},{"issue":"2","key":"10.1016\/j.neuroscience.2022.07.020_b0215","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1002\/syn.890030207","article-title":"Review: cholinergic mechanisms and epileptogenesis. The seizures induced by pilocarpine: a novel experimental model of intractable epilepsy","volume":"3","author":"Turski","year":"1989","journal-title":"Synapse"},{"issue":"3","key":"10.1016\/j.neuroscience.2022.07.020_b0220","doi-asserted-by":"crossref","first-page":"422","DOI":"10.1111\/j.1528-1167.2008.01727.x","article-title":"Decreased expression of synaptic vesicle protein 2A, the binding site for levetiracetam, during epileptogenesis and chronic epilepsy","volume":"50","author":"Van Vliet","year":"2009","journal-title":"Epilepsia"},{"issue":"10","key":"10.1016\/j.neuroscience.2022.07.020_b0225","doi-asserted-by":"crossref","first-page":"e22157","DOI":"10.1002\/syn.22157","article-title":"Autoradiographic mapping of synaptic vesicle glycoprotein 2A in non-human primate and human brain","volume":"74","author":"Varnas","year":"2020","journal-title":"Synapse"},{"key":"10.1016\/j.neuroscience.2022.07.020_b0230","doi-asserted-by":"crossref","first-page":"259","DOI":"10.3389\/fneur.2014.00259","article-title":"The piriform cortex and human focal epilepsy","volume":"5","author":"Vaughan","year":"2014","journal-title":"Front Neurol"},{"issue":"12","key":"10.1016\/j.neuroscience.2022.07.020_b0235","doi-asserted-by":"crossref","first-page":"2317","DOI":"10.1002\/jnr.23111","article-title":"Altered balance between excitatory and inhibitory inputs onto CA1 pyramidal neurons from SV2A-deficient but not SV2B-deficient mice","volume":"90","author":"Venkatesan","year":"2012","journal-title":"J Neurosci Res"},{"issue":"6187","key":"10.1016\/j.neuroscience.2022.07.020_b0240","doi-asserted-by":"crossref","first-page":"1023","DOI":"10.1126\/science.1252884","article-title":"Composition of isolated synaptic boutons reveals the amounts of vesicle trafficking proteins","volume":"344","author":"Wilhelm","year":"2014","journal-title":"Science"}],"container-title":["Neuroscience"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0306452222003888?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0306452222003888?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,10,5]],"date-time":"2025-10-05T16:13:47Z","timestamp":1759680827000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0306452222003888"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,9]]},"references-count":48,"alternative-id":["S0306452222003888"],"URL":"https:\/\/doi.org\/10.1016\/j.neuroscience.2022.07.020","relation":{},"ISSN":["0306-4522"],"issn-type":[{"type":"print","value":"0306-4522"}],"subject":[],"published":{"date-parts":[[2022,9]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Spatio-Temporal Alterations in Synaptic Density During Epileptogenesis in the Rat Brain","name":"articletitle","label":"Article Title"},{"value":"Neuroscience","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.neuroscience.2022.07.020","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2022 The Authors. Published by Elsevier Ltd on behalf of IBRO.","name":"copyright","label":"Copyright"}]}}