{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,21]],"date-time":"2026-09-21T02:27:29Z","timestamp":1789957649679,"version":"4.0.1"},"reference-count":108,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,5,9]],"date-time":"2023-05-09T00:00:00Z","timestamp":1683590400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["UIDB\/04046\/2020"],"award-info":[{"award-number":["UIDB\/04046\/2020"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["UIDP\/04046\/2020"],"award-info":[{"award-number":["UIDP\/04046\/2020"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["PTDC\/SAU-NEU\/103639\/2008"],"award-info":[{"award-number":["PTDC\/SAU-NEU\/103639\/2008"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["PTDC\/SAU-PUB\/28311\/2017"],"award-info":[{"award-number":["PTDC\/SAU-PUB\/28311\/2017"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["SFRH\/BPD\/81358\/2011"],"award-info":[{"award-number":["SFRH\/BPD\/81358\/2011"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","doi-asserted-by":"publisher","award":["Norma Transit\u00f3ria - DL57\/2016\/CP1479\/CT0044"],"award-info":[{"award-number":["Norma Transit\u00f3ria - DL57\/2016\/CP1479\/CT0044"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Neurosci."],"abstract":"<jats:p>Non-epileptic seizures are identified as a common epileptogenic trigger. Early metaplasticity following seizures may contribute to epileptogenesis by abnormally altering synaptic strength and homeostatic plasticity. We now studied how <jats:italic>in vitro<\/jats:italic> epileptiform activity (EA) triggers early changes in CA1 long-term potentiation (LTP) induced by theta-burst stimulation (TBS) in rat hippocampal slices and the involvement of lipid rafts in these early metaplasticity events. Two forms of EA were induced: (1) interictal-like EA evoked by Mg<jats:sup>2+<\/jats:sup> withdrawal and K<jats:sup>+<\/jats:sup> elevation to 6 mM in the superfusion medium or (2) ictal-like EA induced by bicuculline (10 \u03bcM). Both EA patterns induced and LTP-like effect on CA1 synaptic transmission prior to LTP induction. LTP induced 30 min post EA was impaired, an effect more pronounced after ictal-like EA. LTP recovered to control levels 60 min post interictal-like EA but was still impaired 60 min after ictal-like EA. The synaptic molecular events underlying this altered LTP were investigated 30 min post EA in synaptosomes isolated from these slices. EA enhanced AMPA GluA1 Ser831 phosphorylation but decreased Ser845 phosphorylation and the GluA1\/GluA2 ratio. Flotillin-1 and caveolin-1 were markedly decreased concomitantly with a marked increase in gephyrin levels and a less prominent increase in PSD-95. Altogether, EA differentially influences hippocampal CA1 LTP thorough regulation of GluA1\/GluA2 levels and AMPA GluA1 phosphorylation suggesting that altered LTP post-seizures is a relevant target for antiepileptogenic therapies. In addition, this metaplasticity is also associated with marked alterations in classic and synaptic lipid raft markers, suggesting these may also constitute promising targets in epileptogenesis prevention.<\/jats:p>","DOI":"10.3389\/fncel.2023.1117697","type":"journal-article","created":{"date-parts":[[2023,5,9]],"date-time":"2023-05-09T04:56:26Z","timestamp":1683608186000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":10,"title":["Epileptiform activity influences theta-burst induced LTP in the adult hippocampus: a role for synaptic lipid raft disruption in early metaplasticity?"],"prefix":"10.3389","volume":"17","author":[{"given":"Jos\u00e9 D.","family":"Carvalho-Rosa","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"N\u00e1dia C.","family":"Rodrigues","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Armando","family":"Silva-Cruz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sandra H.","family":"Vaz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Diana","family":"Cunha-Reis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,5,9]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"126","DOI":"10.1016\/S0166-2236(96)80018-X","article-title":"Metaplasticity: the plasticity of synaptic plasticity.","volume":"19","author":"Abraham","year":"1996","journal-title":"Trends Neurosci."},{"key":"B2","doi-asserted-by":"publisher","first-page":"240","DOI":"10.1016\/j.nlm.2017.09.004","article-title":"Mismatch novelty exploration training enhances hippocampal synaptic plasticity: a tool for cognitive stimulation?","volume":"145","author":"Aidil-Carvalho","year":"2017","journal-title":"Neurobiol. Learn. Mem."},{"key":"B3","doi-asserted-by":"publisher","first-page":"56","DOI":"10.1016\/j.brainres.2003.11.010","article-title":"Activation of long-term synaptic plasticity causes suppression of epileptiform activity in rat hippocampal slices.","volume":"998","author":"Albensi","year":"2004","journal-title":"Brain Res."},{"key":"B4","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.expneurol.2006.12.009","article-title":"Electrical stimulation protocols for hippocampal synaptic plasticity and neuronal hyper-excitability: are they effective or relevant?","volume":"204","author":"Albensi","year":"2007","journal-title":"Exp. Neurol."},{"key":"B5","doi-asserted-by":"publisher","first-page":"128","DOI":"10.1038\/nrn2059","article-title":"Lipid raft microdomains and neurotransmitter signalling.","volume":"8","author":"Allen","year":"2007","journal-title":"Nat. Rev. Neurosci."},{"key":"B6","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1016\/s0165-0270(01)00374-0","article-title":"The LTP Program: a data acquisition program for on-line analysis of long-term potentiation and other synaptic events.","volume":"108","author":"Anderson","year":"2001","journal-title":"J. Neurosci. Methods"},{"key":"B7","doi-asserted-by":"publisher","first-page":"346","DOI":"10.1016\/j.jneumeth.2006.12.018","article-title":"Capabilities of the WinLTP data acquisition program extending beyond basic LTP experimental functions.","volume":"162","author":"Anderson","year":"2007","journal-title":"J. Neurosci. Methods"},{"key":"B8","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1016\/j.jneumeth.2015.08.014","article-title":"In vitro seizure like events and changes in ionic concentration.","volume":"260","author":"Antonio","year":"2016","journal-title":"J. Neurosci. Methods"},{"key":"B9","doi-asserted-by":"publisher","first-page":"530","DOI":"10.1111\/j.1471-4159.2010.07133.x","article-title":"LTP in hippocampal neurons is associated with a CaMKII-mediated increase in GluA1 surface expression.","volume":"116","author":"Appleby","year":"2011","journal-title":"J. Neurochem."},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.1016\/j.expneurol.2021.113808","article-title":"Intermittent Hypoxia causes targeted disruption to NMDA receptor dependent synaptic plasticity in area CA1 of the hippocampus.","volume":"344","author":"Arias-Cavieres","year":"2021","journal-title":"Exp. Neurol."},{"key":"B11","doi-asserted-by":"publisher","first-page":"20","DOI":"10.1016\/j.brainresbull.2017.11.012","article-title":"Disinhibition in learning and memory circuits: new vistas for somatostatin interneurons and long-term synaptic plasticity.","volume":"141","author":"Artinian","year":"2018","journal-title":"Brain Res. Bull."},{"key":"B12","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1007\/978-94-017-8914-1_8","article-title":"Are there really \u201cEpileptogenic\u201d mechanisms or only corruptions of \u201cNormal\u201d plasticity?","author":"Avanzini","year":"2014","journal-title":"Issues in Clinical Epileptology: A View from the Bench. Advances in Experimental Medicine and Biology"},{"key":"B13","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1046\/j.1528-1157.2001.042suppl.3002.x","article-title":"Do interictal discharges promote or control seizures? Experimental evidence from an in vitro model of epileptiform discharge.","volume":"42","author":"Avoli","year":"2001","journal-title":"Epilepsia"},{"key":"B14","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1111\/j.1535-7511.2006.00146.x","article-title":"Do interictal spikes sustain seizures and epileptogenesis?","volume":"6","author":"Avoli","year":"2006","journal-title":"Epilepsy Curr."},{"key":"B15","doi-asserted-by":"publisher","DOI":"10.3389\/fncir.2022.984802","article-title":"GABAA signaling, focal epileptiform synchronization and epileptogenesis.","volume":"16","author":"Avoli","year":"2022","journal-title":"Front. Neural Circuits"},{"key":"B16","doi-asserted-by":"publisher","first-page":"312","DOI":"10.1038\/s41422-020-00433-1","article-title":"Gephyrin-mediated formation of inhibitory postsynaptic density sheet via phase separation.","volume":"31","author":"Bai","year":"2021","journal-title":"Cell Res."},{"key":"B17","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuropharm.2019.05.020","article-title":"Postsynaptic plasticity of GABAergic synapses.","volume":"169","author":"Barberis","year":"2020","journal-title":"Neuropharmacology"},{"key":"B18","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1038\/nrn2371","article-title":"Plasticity of intrinsic neuronal properties in CNS disorders.","volume":"9","author":"Beck","year":"2008","journal-title":"Nat. Rev. Neurosci."},{"key":"B19","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1046\/j.1528-1157.2001.042Suppl.3005.x","article-title":"Cell death and synaptic reorganizations produced by seizures.","volume":"42","author":"Ben-Ari","year":"2001","journal-title":"Epilepsia"},{"key":"B20","author":"Bento-Oliveira","year":"2018","journal-title":"Changes in Synaptic Plasticity and Lipid Raft Composition in a Rat Model of Temporal Lobe Epilepsy."},{"key":"B21","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1177\/2398212819848213","article-title":"Persistent memories of long-term potentiation and the N -methyl-d-aspartate receptor.","volume":"3","author":"Bliss","year":"2019","journal-title":"Brain Neurosci. Adv."},{"key":"B22","doi-asserted-by":"publisher","first-page":"A103","DOI":"10.1515\/nf-2017-A059","article-title":"Long-term potentiation in the hippocampus: discovery, mechanisms and function.","volume":"24","author":"Bliss","year":"2018","journal-title":"Neuroforum"},{"key":"B23","doi-asserted-by":"publisher","first-page":"2662","DOI":"10.1016\/j.bbamem.2016.07.005","article-title":"The lipid habitats of neurotransmitter receptors in brain.","volume":"1858","author":"Borroni","year":"2016","journal-title":"Biochim. Biophys. Acta Biomembr."},{"key":"B24","doi-asserted-by":"publisher","DOI":"10.3389\/conf.fncel.2019.01.00028","article-title":"Endogenous VIP VPAC1 receptor activation during ictal and interictal-like activity induced in vitro by biccuculine and 0-Mg2+ modulates subsequent LTP expression in the rat hippocampus.","volume":"13","author":"Carvalho-Rosa","year":"2019","journal-title":"Front. Cell. Neurosci."},{"key":"B25","doi-asserted-by":"publisher","DOI":"10.3390\/BIOLOGY11050627","article-title":"Endogenous VIP VPAC1 receptor activation modulates hippocampal theta burst induced LTP: transduction pathways and GABAergic mechanisms.","volume":"11","author":"Caulino-Rocha","year":"2022","journal-title":"Biology"},{"key":"B26","doi-asserted-by":"publisher","DOI":"10.3389\/fnsyn.2022.833782","article-title":"The shaping of AMPA receptor surface distribution by neuronal activity.","volume":"14","author":"Chater","year":"2022","journal-title":"Front. Synaptic Neurosci."},{"key":"B27","doi-asserted-by":"publisher","first-page":"953","DOI":"10.1113\/jphysiol.2004.068080","article-title":"Long-term potentiation is impaired in rat hippocampal slices that produce spontaneous sharp waves.","volume":"558","author":"Colgin","year":"2004","journal-title":"J. Physiol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"469","DOI":"10.1038\/nn.2781","article-title":"Flotillin-1 is essential for PKC-triggered endocytosis and membrane microdomain localization of DAT.","volume":"14","author":"Cremona","year":"2011","journal-title":"Nat. Neurosci."},{"key":"B29","doi-asserted-by":"publisher","DOI":"10.3389\/fncel.2020.00153","article-title":"VIP modulation of hippocampal synaptic plasticity: a role for VIP Receptors as therapeutic targets in cognitive decline and mesial temporal lobe epilepsy.","volume":"14","author":"Cunha-Reis","year":"2020","journal-title":"Front. Cell. Neurosci."},{"key":"B30","doi-asserted-by":"publisher","DOI":"10.1016\/j.phrs.2020.105356","article-title":"VIPergic neuroprotection in epileptogenesis: challenges and opportunities.","volume":"164","author":"Cunha-Reis","year":"2021","journal-title":"Pharmacol. Res."},{"key":"B31","doi-asserted-by":"publisher","first-page":"4725","DOI":"10.1111\/bph.14051","article-title":"VPAC1 and VPAC2 receptor activation on GABA release from hippocampal nerve terminals involve several different signalling pathways.","volume":"174","author":"Cunha-Reis","year":"2017","journal-title":"Br. J. Pharmacol."},{"key":"B32","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1113\/jphysiol.1990.sp018080","article-title":"Paired-pulse depression of monosynaptic GABA-mediated inhibitory postsynaptic responses in rat hippocampus.","volume":"424","author":"Davies","year":"1990","journal-title":"J. Physiol."},{"key":"B33","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1113\/JPHYSIOL.1996.SP021204","article-title":"Paired-pulse facilitation and depression at unitary synapses in rat hippocampus: quantal fluctuation affects subsequent release.","volume":"491","author":"Debanne","year":"1996","journal-title":"J. Physiol."},{"key":"B34","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1111\/j.1528-1167.2006.00416.x","article-title":"A brief period of epileptiform activity strengthens excitatory synapses in the rat hippocampus in vitro.","volume":"47","author":"Debanne","year":"2006","journal-title":"Epilepsia"},{"key":"B35","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.1001908","article-title":"Palmitoylation of gephyrin controls receptor clustering and plasticity of GABAergic synapses.","volume":"12","author":"Dejanovic","year":"2014","journal-title":"PLoS Biol."},{"key":"B36","doi-asserted-by":"publisher","first-page":"3269","DOI":"10.1073\/pnas.96.6.3269","article-title":"Ca2+\/calmodulin-kinase II enhances channel conductance of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate type glutamate receptors.","volume":"96","author":"Derkach","year":"1999","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B37","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1038\/nrn2055","article-title":"Regulatory mechanisms of AMPA receptors in synaptic plasticity.","volume":"8","author":"Derkach","year":"2007","journal-title":"Nat. Rev. Neurosci."},{"key":"B38","doi-asserted-by":"publisher","DOI":"10.1038\/nrdp.2018.24","article-title":"Epilepsy.","volume":"4","author":"Devinsky","year":"2018","journal-title":"Nat. Rev. Dis. Prim."},{"key":"B39","doi-asserted-by":"publisher","first-page":"460","DOI":"10.1002\/epi4.12277","article-title":"How do we use in vitro models to understand epileptiform and ictal activity? A report of the TASK1-WG4 group of the ILAE\/AES Joint Translational Task Force.","volume":"3","author":"Dulla","year":"2018","journal-title":"Epilepsia Open"},{"key":"B40","doi-asserted-by":"publisher","DOI":"10.3390\/biomedicines9101374","article-title":"Short-term epileptiform activity potentiates excitatory synapses but does not affect intrinsic membrane properties of pyramidal neurons in the rat hippocampus in vitro.","volume":"9","author":"Ergina","year":"2021","journal-title":"Biomedicines"},{"key":"B41","doi-asserted-by":"publisher","first-page":"1006","DOI":"10.1002\/syn.20928","article-title":"Downregulation of gephyrin in temporal lobe epilepsy neurons in humans and a rat model.","volume":"65","author":"Fang","year":"2011","journal-title":"Synapse"},{"key":"B42","doi-asserted-by":"publisher","first-page":"3012","DOI":"10.1152\/jn.00058.2014","article-title":"Homeostatic plasticity induced by brief activity deprivation enhances long-term potentiation in the mature rat hippocampus.","volume":"112","author":"F\u00e9lix-Oliveira","year":"2014","journal-title":"J. Neurophysiol."},{"key":"B43","doi-asserted-by":"publisher","first-page":"18098","DOI":"10.1073\/pnas.1908051116","article-title":"Gangliosides interact with synaptotagmin to form the high-affinity receptor complex for botulinum neurotoxin B.","volume":"116","author":"Flores","year":"2019","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B44","doi-asserted-by":"publisher","first-page":"126","DOI":"10.1038\/nn1178","article-title":"LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites.","volume":"7","author":"Frick","year":"2004","journal-title":"Nat. Neurosci."},{"key":"B45","doi-asserted-by":"publisher","first-page":"1151","DOI":"10.1016\/j.cub.2007.05.078","article-title":"Coassembly of flotillins induces formation of membrane microdomains, membrane curvature, and vesicle budding.","volume":"17","author":"Frick","year":"2007","journal-title":"Curr. Biol."},{"key":"B46","doi-asserted-by":"publisher","DOI":"10.1016\/j.eplepsyres.2019.106224","article-title":"Epileptiform activity promotes decreasing of Ca2+ conductivity of NMDARs, AMPARs, KARs, and voltage-gated calcium channels in Mg2+-free model.","volume":"158","author":"Gaidin","year":"2019","journal-title":"Epilepsy Res."},{"key":"B47","doi-asserted-by":"publisher","first-page":"421","DOI":"10.1016\/j.phrs.2016.09.019","article-title":"Pharmacological modulation in mesial temporal lobe epilepsy: current status and future perspectives.","volume":"113","author":"Gambardella","year":"2016","journal-title":"Pharmacol. Res."},{"key":"B48","doi-asserted-by":"publisher","first-page":"831","DOI":"10.1111\/j.1471-4159.2004.02917.x","article-title":"A role for caveolin-1 in post-injury reactive neuronal plasticity.","volume":"92","author":"Gaudreault","year":"2005","journal-title":"J. Neurochem."},{"key":"B49","doi-asserted-by":"publisher","first-page":"356","DOI":"10.1074\/jbc.M304777200","article-title":"The caveolin scaffolding domain modifies 2-amino-3-hydroxy-5-methyl-4-isoxazole propionate receptor binding properties by inhibiting phospholipase A2 activity.","volume":"279","author":"Gaudreault","year":"2004","journal-title":"J. Biol. Chem."},{"key":"B50","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1016\/0165-3806(95)00069-P","article-title":"Properties of low Mg2+ induced epileptiform activity in rat hippocampal and entorhinal cortex slices during adolescence.","volume":"87","author":"Gloveli","year":"1995","journal-title":"Dev. Brain Res."},{"key":"B51","doi-asserted-by":"publisher","first-page":"4476","DOI":"10.1046\/J.1460-9568.1999.00920.X","article-title":"Cyclical changes in endogenous levels of oestrogen modulate the induction of LTD and LTP in the hippocampal CA1 region.","volume":"11","author":"Good","year":"1999","journal-title":"Eur. J. Neurosci."},{"key":"B52","doi-asserted-by":"publisher","first-page":"2527","DOI":"10.1523\/JNEUROSCI.3426-07.2008","article-title":"Subunit-specific trafficking of GABA(A) receptors during status epilepticus.","volume":"28","author":"Goodkin","year":"2008","journal-title":"J. Neurosci."},{"key":"B53","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.apsb.2014.12.002","article-title":"S-palmitoylation regulates AMPA receptors trafficking and function: a novel insight into synaptic regulation and therapeutics.","volume":"5","author":"Han","year":"2015","journal-title":"Acta Pharm. Sin. B"},{"key":"B54","doi-asserted-by":"publisher","first-page":"3262","DOI":"10.1523\/jneurosci.23-08-03262.2003","article-title":"Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability.","volume":"23","author":"Hering","year":"2003","journal-title":"J. Neurosci."},{"key":"B55","doi-asserted-by":"publisher","first-page":"1033","DOI":"10.1016\/j.neurobiolaging.2009.07.006","article-title":"Oxidative stress activates the pro-survival TrkA pathway through membrane cholesterol loss.","volume":"32","author":"Iannilli","year":"2011","journal-title":"Neurobiol. Aging"},{"key":"B56","doi-asserted-by":"publisher","first-page":"10220","DOI":"10.1523\/JNEUROSCI.1590-18.2018","article-title":"Deficiency of AMPAR\u2013palmitoylation aggravates seizure susceptibility.","volume":"38","author":"Itoh","year":"2018","journal-title":"J. Neurosci."},{"key":"B57","doi-asserted-by":"publisher","first-page":"721","DOI":"10.1161\/01.RES.0000260180.42709.29","article-title":"Caveolin-1 deficiency increases cerebral ischemic injury.","volume":"100","author":"Jasmin","year":"2007","journal-title":"Circ. Res."},{"key":"B58","doi-asserted-by":"publisher","first-page":"657","DOI":"10.1016\/j.neuron.2008.08.029","article-title":"Rapid, bidirectional remodeling of synaptic NMDA receptor subunit composition by A-type K+ channel activity in hippocampal CA1 pyramidal neurons.","volume":"60","author":"Jung","year":"2008","journal-title":"Neuron"},{"key":"B59","doi-asserted-by":"publisher","first-page":"276","DOI":"10.1177\/1073858408315041","article-title":"Potassium channels: newly found players in synaptic plasticity.","volume":"14","author":"Kim","year":"2008","journal-title":"Neuroscience"},{"key":"B60","doi-asserted-by":"publisher","first-page":"933","DOI":"10.1016\/j.neuron.2007.05.026","article-title":"Regulation of dendritic excitability by activity-dependent trafficking of the A-Type K+ channel subunit Kv4.2 in hippocampal neurons.","volume":"54","author":"Kim","year":"2007","journal-title":"Neuron"},{"key":"B61","doi-asserted-by":"publisher","DOI":"10.3390\/ijms18091935","article-title":"Metabolic and homeostatic changes in seizures and acquired epilepsy\u2014mitochondria, calcium dynamics and reactive oxygen species.","volume":"18","author":"Kovac","year":"2017","journal-title":"Int. J. Mol. Sci."},{"key":"B62","doi-asserted-by":"publisher","first-page":"1191","DOI":"10.1097\/WNR.0000000000000656","article-title":"Status epilepticus alters hippocampal long-term synaptic potentiation in a rat lithium-pilocarpine model.","volume":"27","author":"Kryukov","year":"2016","journal-title":"Neuroreport"},{"key":"B63","doi-asserted-by":"publisher","first-page":"374","DOI":"10.3109\/02688697.2013.841854","article-title":"Comparison of therapeutic effects between selective amygdalohippocampectomy and anterior temporal lobectomy for the treatment of temporal lobe epilepsy: a meta-analysis.","volume":"28","author":"Kuang","year":"2014","journal-title":"Br. J. Neurosurg."},{"key":"B64","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1152\/JN.1994.72.1.121","article-title":"Temporally distinct mechanisms of use-dependent depression at inhibitory synapses in the rat hippocampus in vitro.","volume":"121","author":"Lambert","year":"1994","journal-title":"J. Neurophysiol."},{"key":"B65","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1016\/j.brainres.2014.10.034","article-title":"Theta-burst LTP.","volume":"1621","author":"Larson","year":"2015","journal-title":"Brain Res."},{"key":"B66","doi-asserted-by":"publisher","first-page":"631","DOI":"10.1016\/S0092-8674(03)00122-3","article-title":"Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory.","volume":"112","author":"Lee","year":"2003","journal-title":"Cell"},{"key":"B67","doi-asserted-by":"publisher","first-page":"134","DOI":"10.1111\/j.1528-1167.2005.01021.x","article-title":"Plasticity, synaptic strength, and epilepsy: what can we learn from ultrastructural data?","volume":"46","author":"Leite","year":"2005","journal-title":"Epilepsia"},{"key":"B68","doi-asserted-by":"publisher","DOI":"10.1016\/j.nbd.2022.105794","article-title":"Bilateral optogenetic activation of inhibitory cells favors ictogenesis.","volume":"171","author":"L\u00e9vesque","year":"2022","journal-title":"Neurobiol. Dis."},{"key":"B69","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1097\/YCT.0b013e31824a47ca","article-title":"Effects of electroconvulsive stimulation on long-term potentiation and synaptophysin in the hippocampus of rats with depressive behavior.","volume":"28","author":"Li","year":"2012","journal-title":"J. ECT"},{"key":"B70","doi-asserted-by":"publisher","DOI":"10.3389\/fnsyn.2020.588785","article-title":"The requirement of the C-terminal domain of GluA1 in different forms of long-term potentiation in the hippocampus is age-dependent.","volume":"12","author":"Liu","year":"2020","journal-title":"Front. Synaptic Neurosci."},{"key":"B71","doi-asserted-by":"publisher","first-page":"3115","DOI":"10.1093\/brain\/aws147","article-title":"Neuropathology of the blood-brain barrier and pharmaco-resistance in human epilepsy.","volume":"135","author":"Liu","year":"2012","journal-title":"Brain"},{"key":"B72","doi-asserted-by":"publisher","first-page":"757","DOI":"10.1016\/j.neuropharm.2010.12.014","article-title":"Excitatory synaptic activity is associated with a rapid structural plasticity of inhibitory synapses on hippocampal CA1 pyramidal cells.","volume":"60","author":"Lushnikova","year":"2011","journal-title":"Neuropharmacology"},{"key":"B73","doi-asserted-by":"publisher","first-page":"344","DOI":"10.1177\/1073858418805002","article-title":"GABAergic interneurons in seizures: investigating causality with optogenetics.","volume":"25","author":"Magloire","year":"2019","journal-title":"Neuroscientist"},{"key":"B74","doi-asserted-by":"publisher","DOI":"10.3389\/fnmol.2019.00008","article-title":"Role of palmitoylation of postsynaptic proteins in promoting synaptic plasticity.","volume":"12","author":"Matt","year":"2019","journal-title":"Front. Mol. Neurosci."},{"key":"B75","doi-asserted-by":"publisher","first-page":"527","DOI":"10.1016\/S0306-4522(00)00496-6","article-title":"Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells.","volume":"102","author":"Meg\u00edas","year":"2001","journal-title":"Neuroscience"},{"key":"B76","doi-asserted-by":"publisher","first-page":"884","DOI":"10.1016\/S0140-6736(14)60456-6","article-title":"Epilepsy: new advances.","volume":"385","author":"Mosh\u00e9","year":"2015","journal-title":"Lancet"},{"key":"B77","doi-asserted-by":"publisher","first-page":"1704","DOI":"10.1152\/JN.1991.66.5.1704","article-title":"Depression of the fast IPSP underlies paired-pulse facilitation in area CA1 of the rat hippocampus.","volume":"66","author":"Nathan","year":"1991","journal-title":"J. Neurophysiol."},{"key":"B78","doi-asserted-by":"publisher","first-page":"1160","DOI":"10.1074\/jbc.M116.771592","article-title":"Endosomal phosphatidylinositol 3-phosphate promotes gephyrin clustering and GABAergic neurotransmission at inhibitory postsynapses.","volume":"292","author":"Papadopoulos","year":"2017","journal-title":"J. Biol. Chem."},{"key":"B79","doi-asserted-by":"publisher","first-page":"8256","DOI":"10.1074\/jbc.M114.633024","article-title":"Lipid binding defects and perturbed synaptogenic activity of a collybistin R290H mutant that causes epilepsy and intellectual disability.","volume":"290","author":"Papadopoulos","year":"2015","journal-title":"J. Biol. Chem."},{"key":"B80","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-020-20523-3","article-title":"PKA drives an increase in AMPA receptor unitary conductance during LTP in the hippocampus.","volume":"12","author":"Park","year":"2021","journal-title":"Nat. Commun."},{"key":"B81","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a022822","article-title":"Epileptogenesis.","volume":"5","author":"Pitk\u00e4nen","year":"2015","journal-title":"Cold Spring Harb. Perspect. Med."},{"key":"B82","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1016\/j.neuroscience.2019.07.036","article-title":"Tuning GABAergic inhibition: gephyrin molecular organization and functions.","volume":"439","author":"Pizzarelli","year":"2020","journal-title":"Neuroscience"},{"key":"B83","doi-asserted-by":"publisher","first-page":"1145","DOI":"10.1016\/j.bbrc.2020.06.121","article-title":"Calcium-permeable AMPA receptors are essential to the synaptic plasticity induced by epileptiform activity in rat hippocampal slices.","volume":"529","author":"Postnikova","year":"2020","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"B84","doi-asserted-by":"publisher","first-page":"282","DOI":"10.1134\/S0006297917030063","article-title":"Status epilepticus impairs synaptic plasticity in rat hippocampus and is followed by changes in expression of NMDA receptors.","volume":"82","author":"Postnikova","year":"2017","journal-title":"Biochemistry"},{"key":"B85","doi-asserted-by":"publisher","first-page":"5272","DOI":"10.1111\/ejn.15390","article-title":"Hippocampal CA1 theta burst-induced LTP from weaning to adulthood: cellular and molecular mechanisms in young male rats revisited.","volume":"54","author":"Rodrigues","year":"2021","journal-title":"Eur. J. Neurosci."},{"key":"B86","doi-asserted-by":"publisher","first-page":"324","DOI":"10.1007\/s12017-013-8221-6","article-title":"AMPA receptor properties are modulated in the early stages following pilocarpine-induced status epilepticus.","volume":"15","author":"Russo","year":"2013","journal-title":"NeuroMol. Med."},{"key":"B87","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0079077","article-title":"Acute physiological stress promotes clustering of synaptic markers and alters spine morphology in the hippocampus.","volume":"8","author":"Sebastian","year":"2013","journal-title":"PLoS One"},{"key":"B88","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1016\/j.neuropharm.2012.06.053","article-title":"Lipid rafts, synaptic transmission and plasticity: impact in age-related neurodegenerative diseases.","volume":"64","author":"Sebasti\u00e3o","year":"2013","journal-title":"Neuropharmacology"},{"key":"B89","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuint.2022.105383","article-title":"Opposing reduced VPAC1 and enhanced VPAC2 VIP receptors in the hippocampus of the Li2+-pilocarpine rat model of temporal lobe epilepsy.","volume":"158","author":"Serpa","year":"2022","journal-title":"Neurochem. Int."},{"key":"B90","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1016\/j.coph.2017.07.012","article-title":"Epileptogenesis meets Occam\u2019s Razor.","volume":"35","author":"Sloviter","year":"2017","journal-title":"Curr. Opin. Pharmacol."},{"key":"B91","doi-asserted-by":"publisher","first-page":"1043","DOI":"10.1016\/j.neurobiolaging.2010.06.001","article-title":"Cellular stress from excitatory neurotransmission contributes to cholesterol loss in hippocampal neurons aging in vitro.","volume":"32","author":"Sodero","year":"2011","journal-title":"Neurobiol. Aging"},{"key":"B92","doi-asserted-by":"publisher","first-page":"76","DOI":"10.1016\/j.conb.2021.02.006","article-title":"Mechanism of synaptic protein turnover and its regulation by neuronal activity.","volume":"69","author":"Soykan","year":"2021","journal-title":"Curr. Opin. Neurobiol."},{"key":"B93","doi-asserted-by":"publisher","first-page":"292","DOI":"10.1016\/j.bbr.2009.02.027","article-title":"Alterations of NR2B and PSD-95 expression in hippocampus of kainic acid-exposed rats with behavioural deficits.","volume":"201","author":"Sun","year":"2009","journal-title":"Behav. Brain Res."},{"key":"B94","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuropharm.2022.109383","article-title":"A role of GABAA receptor \u03b11 subunit in the hippocampus for rapid-acting antidepressant-like effects of ketamine.","volume":"225","author":"Tang","year":"2023","journal-title":"Neuropharmacology"},{"key":"B95","doi-asserted-by":"publisher","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":"B96","doi-asserted-by":"publisher","DOI":"10.1016\/j.expneurol.2020.113437","article-title":"The potassium channel Kv4.2 regulates dendritic spine morphology, electroencephalographic characteristics and seizure susceptibility in mice.","volume":"334","author":"Tiwari","year":"2020","journal-title":"Exp. Neurol."},{"key":"B97","doi-asserted-by":"publisher","first-page":"3480","DOI":"10.1091\/mbc.E16-06-0420","article-title":"Remodeling of the postsynaptic plasma membrane during neural development.","volume":"27","author":"Tulodziecka","year":"2016","journal-title":"Mol. Biol. Cell"},{"key":"B98","doi-asserted-by":"publisher","DOI":"10.3389\/fphys.2019.01544","article-title":"Microtubules Stabilization by mutant spastin affects ER morphology and Ca2+ handling.","volume":"10","author":"Vajente","year":"2019","journal-title":"Front. Physiol."},{"key":"B99","doi-asserted-by":"publisher","first-page":"923","DOI":"10.1002\/hipo.20118","article-title":"Hippocampal theta rhythm: a tag for short-term memory.","volume":"15","author":"Vertes","year":"2005","journal-title":"Hippocampus"},{"key":"B100","doi-asserted-by":"publisher","first-page":"459","DOI":"10.1038\/s41582-019-0217-x","article-title":"Neuroinflammatory pathways as treatment targets and biomarkers in epilepsy.","volume":"15","author":"Vezzani","year":"2019","journal-title":"Nat. Rev. Neurol."},{"key":"B101","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1016\/j.conb.2021.03.004","article-title":"The synaptic life of microtubules.","volume":"69","author":"Waites","year":"2021","journal-title":"Curr. Opin. Neurobiol."},{"key":"B102","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1016\/0006-8993(95)01059-9","article-title":"LTP varies across the estrous cycle: enhanced synaptic plasticity in proestrus rats.","volume":"703","author":"Warren","year":"1995","journal-title":"Brain Res."},{"key":"B103","doi-asserted-by":"publisher","first-page":"3010","DOI":"10.1021\/acs.biochem.0c00524","article-title":"Understanding the link between lipid diversity and the biophysical properties of the neuronal plasma membrane.","volume":"59","author":"Wilson","year":"2020","journal-title":"Biochemistry"},{"key":"B104","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0012818","article-title":"A role for calcium-permeable AMPA receptors in synaptic plasticity and learning.","volume":"5","author":"Wiltgen","year":"2010","journal-title":"PLoS One"},{"key":"B105","doi-asserted-by":"publisher","first-page":"645","DOI":"10.1523\/JNEUROSCI.14-02-00645.1994","article-title":"Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of hippocampus.","volume":"14","author":"Wu","year":"1994","journal-title":"J. Neurosci."},{"key":"B106","doi-asserted-by":"publisher","first-page":"7697","DOI":"10.1523\/JNEUROSCI.2086-05.2005","article-title":"Hippocampal synaptic metaplasticity requires inhibitory autophosphorylation of Ca2+\/calmodulin-dependent kinase II.","volume":"25","author":"Zhang","year":"2005","journal-title":"J. Neurosci."},{"key":"B107","doi-asserted-by":"publisher","first-page":"288","DOI":"10.1002\/hipo.20748","article-title":"Dendritic mechanisms controlling the threshold and timing requirement of synaptic plasticity.","volume":"21","author":"Zhao","year":"2011","journal-title":"Hippocampus"},{"key":"B108","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1146\/ANNUREV.NE.12.030189.000305","article-title":"Short-term synaptic plasticity.","volume":"12","author":"Zucker","year":"2003","journal-title":"Annu. Rev. Neurosci."}],"container-title":["Frontiers in Cellular Neuroscience"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fncel.2023.1117697\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,9]],"date-time":"2023-05-09T04:56:32Z","timestamp":1683608192000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fncel.2023.1117697\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,5,9]]},"references-count":108,"alternative-id":["10.3389\/fncel.2023.1117697"],"URL":"https:\/\/doi.org\/10.3389\/fncel.2023.1117697","relation":{},"ISSN":["1662-5102"],"issn-type":[{"value":"1662-5102","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,5,9]]},"article-number":"1117697"}}