{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T17:39:29Z","timestamp":1791221969858,"version":"4.1.0"},"reference-count":78,"publisher":"MDPI AG","issue":"14","license":[{"start":{"date-parts":[[2024,7,10]],"date-time":"2024-07-10T00:00:00Z","timestamp":1720569600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100012190","name":"Ministry of Science and Higher Education of the Russian Federation","doi-asserted-by":"publisher","award":["075-15-2024-548"],"award-info":[{"award-number":["075-15-2024-548"]}],"id":[{"id":"10.13039\/501100012190","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Epilepsy is known to cause alterations in neural networks. However, many details of these changes remain poorly understood. The objective of this study was to investigate changes in the properties of hippocampal CA1 pyramidal neurons and their synaptic inputs in a rat lithium\u2013pilocarpine model of epilepsy. In the chronic phase of the model, we found a marked loss of pyramidal neurons in the CA1 area. However, the membrane properties of the neurons remained essentially unaltered. The results of the electrophysiological and morphological studies indicate that the direct pathway from the entorhinal cortex to CA1 neurons is reinforced in epileptic animals, whereas the inputs to them from CA3 are either unaltered or even diminished. In particular, the dendritic spine density in the str. lacunosum moleculare, where the direct pathway from the entorhinal cortex terminates, was found to be 2.5 times higher in epileptic rats than in control rats. Furthermore, the summation of responses upon stimulation of the temporoammonic pathway was enhanced by approximately twofold in epileptic rats. This enhancement is believed to be a significant contributing factor to the heightened epileptic activity observed in the entorhinal cortex of epileptic rats using an ex vivo 4-aminopyridine model.<\/jats:p>","DOI":"10.3390\/ijms25147568","type":"journal-article","created":{"date-parts":[[2024,7,12]],"date-time":"2024-07-12T08:16:57Z","timestamp":1720772217000},"page":"7568","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":12,"title":["Morphological and Functional Alterations in the CA1 Pyramidal Neurons of the Rat Hippocampus in the Chronic Phase of the Lithium\u2013Pilocarpine Model of Epilepsy"],"prefix":"10.3390","volume":"25","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7049-4478","authenticated-orcid":false,"given":"Tatyana Y.","family":"Postnikova","sequence":"first","affiliation":[{"name":"Sechenov Institute of Evolutionary Physiology and Biochemistry of RAS, Saint Petersburg 194223, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0002-9598-5123","authenticated-orcid":false,"given":"Georgy P.","family":"Diespirov","sequence":"additional","affiliation":[{"name":"Sechenov Institute of Evolutionary Physiology and Biochemistry of RAS, Saint Petersburg 194223, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9105-6832","authenticated-orcid":false,"given":"Sergey L.","family":"Malkin","sequence":"additional","affiliation":[{"name":"Sechenov Institute of Evolutionary Physiology and Biochemistry of RAS, Saint Petersburg 194223, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1629-7537","authenticated-orcid":false,"given":"Alexander S.","family":"Chernyshev","sequence":"additional","affiliation":[{"name":"Ioffe Institute, Saint Petersburg 194021, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elizaveta N.","family":"Vylekzhanina","sequence":"additional","affiliation":[{"name":"Sechenov Institute of Evolutionary Physiology and Biochemistry of RAS, Saint Petersburg 194223, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4503-0647","authenticated-orcid":false,"given":"Aleksey V.","family":"Zaitsev","sequence":"additional","affiliation":[{"name":"Sechenov Institute of Evolutionary Physiology and Biochemistry of RAS, Saint Petersburg 194223, Russia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,7,10]]},"reference":[{"key":"ref_1","unstructured":"World Health Organization (2024, January 29). Epilepsy. Available online: https:\/\/www.who.int\/news-room\/fact-sheets\/detail\/epilepsy."},{"key":"ref_2","first-page":"583","article-title":"Cellular Basis of Neuronal Synchrony in Epilepsy","volume":"44","author":"Wong","year":"1986","journal-title":"Adv. Neurol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"107966","DOI":"10.1016\/j.neuropharm.2020.107966","article-title":"Mechanisms of Action of Currently Used Antiseizure Drugs","volume":"168","author":"Sills","year":"2020","journal-title":"Neuropharmacology"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1026","DOI":"10.1002\/hipo.20022","article-title":"Two Reentrant Pathways in the Hippocampal-entorhinal System","volume":"14","author":"Kloosterman","year":"2004","journal-title":"Hippocampus"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.pneurobio.2006.04.005","article-title":"A Computational Theory of Hippocampal Function, and Empirical Tests of the Theory","volume":"79","author":"Rolls","year":"2006","journal-title":"Prog. Neurobiol."},{"key":"ref_6","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":"ref_7","doi-asserted-by":"crossref","first-page":"1103","DOI":"10.1002\/hbm.23090","article-title":"In Vivo MRI Signatures of Hippocampal Subfield Pathology in Intractable Epilepsy","volume":"37","author":"Goubran","year":"2016","journal-title":"Hum. Brain Mapp."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1111\/j.1528-1167.2008.01931.x","article-title":"Hippocampal Epileptogenesis in Animal Models of Mesial Temporal Lobe Epilepsy with Hippocampal Sclerosis: The Importance of the \u201cLatent Period\u201d and Other Concepts","volume":"49","author":"Sloviter","year":"2008","journal-title":"Epilepsia"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"534","DOI":"10.1002\/hipo.10031","article-title":"Entorhinal Axons Exhibit Sprouting in CA1 Subfield of the Adult Hippocampus in a Rat Model of Temporal Lobe Epilepsy","volume":"12","author":"Shetty","year":"2002","journal-title":"Hippocampus"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"E2209","DOI":"10.1212\/WNL.0000000000007447","article-title":"Temporal Lobe Epilepsy: Hippocampal Pathology Modulates Connectome Topology and Controllability","volume":"92","author":"Bernhardt","year":"2019","journal-title":"Neurology"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"985","DOI":"10.1111\/j.1528-1157.1993.tb02123.x","article-title":"Circuit Mechanisms of Seizures in the Pilocarpine Model of Chronic Epilepsy: Cell Loss and Mossy Fiber Sprouting","volume":"34","author":"Mello","year":"1993","journal-title":"Epilepsia"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"663","DOI":"10.2174\/0929867320666131119152201","article-title":"Pathophysiogenesis of Mesial Temporal Lobe Epilepsy: Is Prevention of Damage Antiepileptogenic?","volume":"21","author":"Curia","year":"2014","journal-title":"Curr. Med. Chem."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1134\/S0006297923030057","article-title":"Alterations in the Properties of the Rat Hippocampus Glutamatergic System in the Lithium-Pilocarpine Model of Temporal Lobe Epilepsy","volume":"88","author":"Diespirov","year":"2023","journal-title":"Biochemistry (Mosc.)"},{"key":"ref_14","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"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1038\/nrn2148","article-title":"The Action Potential in Mammalian Central Neurons","volume":"8","author":"Bean","year":"2007","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Aksoy-Aksel, A., and Manahan-Vaughan, D. (2013). The Temporoammonic Input to the Hippocampal CA1 Region Displays Distinctly Different Synaptic Plasticity Compared to the Schaffer Collateral Input In Vivo: Significance for Synaptic Information Processing. Front. Synaptic Neurosci., 5.","DOI":"10.3389\/fnsyn.2013.00005"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"11850","DOI":"10.1523\/JNEUROSCI.2354-06.2006","article-title":"Massive and Specific Dysregulation of Direct Cortical Input to the Hippocampus in Temporal Lobe Epilepsy","volume":"26","author":"Ang","year":"2006","journal-title":"J. Neurosci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1016\/j.yebeh.2005.08.005","article-title":"Models of Epilepsy in the Developing and Adult Brain: Implications for Neuroprotection","volume":"7","author":"Stafstrom","year":"2005","journal-title":"Epilepsy Behav."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2623","DOI":"10.1111\/epi.17378","article-title":"Atrophy of the Hippocampal CA1 Subfield Relates to Long-Term Forgetting in Focal Epilepsy","volume":"63","author":"Mukaino","year":"2022","journal-title":"Epilepsia"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"780","DOI":"10.1111\/epi.12955","article-title":"Beyond the CA1 Subfield: Local Hippocampal Shape Changes in MRI-Negative Temporal Lobe Epilepsy","volume":"56","author":"Maccotta","year":"2015","journal-title":"Epilepsia"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"699","DOI":"10.1016\/j.neuroscience.2011.05.022","article-title":"Lithium Pilocarpine-Induced Status Epilepticus in Postnatal Day 20 Rats Results in Greater Neuronal Injury in Ventral versus Dorsal Hippocampus","volume":"192","author":"Ekstrand","year":"2011","journal-title":"Neuroscience"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1016\/j.neuroscience.2015.11.045","article-title":"TRPV1 Receptors Augment Basal Synaptic Transmission in CA1 and CA3 Pyramidal Neurons in Epilepsy","volume":"314","author":"Saffarzadeh","year":"2016","journal-title":"Neuroscience"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1112","DOI":"10.1002\/hipo.23219","article-title":"Downregulation of Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels (HCN) in the Hippocampus of Patients with Medial Temporal Lobe Epilepsy and Hippocampal Sclerosis (MTLE-HS)","volume":"30","author":"Lin","year":"2020","journal-title":"Hippocampus"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"ENEURO.0036-19.2019","DOI":"10.1523\/ENEURO.0036-19.2019","article-title":"Epilepsy-Induced Reduction in HCN Channel Expression Contributes to an Increased Excitability in Dorsal, but Not Ventral, Hippocampal CA1 Neurons","volume":"6","author":"Arnold","year":"2019","journal-title":"eNeuro"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"13012","DOI":"10.1523\/JNEUROSCI.3605-07.2007","article-title":"Progressive Dendritic HCN Channelopathy during Epileptogenesis in the Rat Pilocarpine Model of Epilepsy","volume":"27","author":"Jung","year":"2007","journal-title":"J. Neurosci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/j.nbd.2011.08.019","article-title":"Network Excitability in a Model of Chronic Temporal Lobe Epilepsy Critically Depends on SK Channel-Mediated AHP Currents","volume":"45","author":"Schulz","year":"2012","journal-title":"Neurobiol. Dis."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/j.eplepsyres.2013.06.006","article-title":"Expression of Sodium Channel \u03b1 Subunits 1.1, 1.2 and 1.6 in Rat Hippocampus after Kainic Acid-Induced Epilepsy","volume":"106","author":"Qiao","year":"2013","journal-title":"Epilepsy Res."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1152\/jn.00184.2010","article-title":"An Increase in Persistent Sodium Current Contributes to Intrinsic Neuronal Bursting after Status Epilepticus","volume":"105","author":"Chen","year":"2011","journal-title":"J. Neurophysiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1016\/S0306-4522(01)00176-2","article-title":"Sodium Currents in Isolated Rat CA1 Pyramidal and Dentate Granule Neurones in the Post-Status Epilepticus Model of Epilepsy","volume":"105","author":"Ketelaars","year":"2001","journal-title":"Neuroscience"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"550","DOI":"10.1016\/j.neuroscience.2008.07.057","article-title":"Altered Expression and Localization of Hippocampal A-Type Potassium Channel Subunits in the Pilocarpine-Induced Model of Temporal Lobe Epilepsy","volume":"156","author":"Monaghan","year":"2008","journal-title":"Neuroscience"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1506","DOI":"10.1152\/jn.00385.2017","article-title":"A Computational Model for How the Fast Afterhyperpolarization Paradoxically Increases Gain in Regularly Firing Neurons","volume":"119","author":"Jaffe","year":"2018","journal-title":"J. Neurophysiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1007\/s10827-010-0246-3","article-title":"Phase-Resetting Curve Determines How BK Currents Affect Neuronal Firing","volume":"30","author":"Ly","year":"2011","journal-title":"J. Comput. Neurosci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1002\/1098-1063(2000)10:5<617::AID-HIPO13>3.0.CO;2-R","article-title":"Spine Loss and Other Dendritic Abnormalities in Epilepsy","volume":"10","author":"Swann","year":"2000","journal-title":"Hippocampus"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/j.pnpbp.2019.01.005","article-title":"Dendritic Spines: Revisiting the Physiological Role","volume":"92","author":"Chidambaram","year":"2019","journal-title":"Prog. Neuropsychopharmacol. Biol. Psychiatry"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1016\/j.brainres.2007.02.089","article-title":"Status Epilepticus Induces Region-Specific Changes in Dendritic Spines, Dendritic Length and TrkB Protein Content of Rat Brain Cortex","volume":"1150","author":"Ampuero","year":"2007","journal-title":"Brain Res."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.neulet.2004.03.035","article-title":"Density, but Not Shape, of Hippocampal Dendritic Spines Varies after a Seizure-Inducing Acute Dose of Monosodium Glutamate in Rats","volume":"363","year":"2004","journal-title":"Neurosci. Lett."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/S0304-3940(98)00848-9","article-title":"Remodeling Dendritic Spines in the Rat Pilocarpine Model of Temporal Lobe Epilepsy","volume":"258","author":"Isokawa","year":"1998","journal-title":"Neurosci. Lett."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1227\/00006123-198008000-00005","article-title":"Dendritic Alterations in Rat Isocortex within an Iron-Induced Chronic Epileptic Focus","volume":"7","author":"Willmore","year":"1980","journal-title":"Neurosurgery"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"8356","DOI":"10.1523\/JNEUROSCI.18-20-08356.1998","article-title":"Spine Loss and Other Persistent Alterations of Hippocampal Pyramidal Cell Dendrites in a Model of Early-Onset Epilepsy","volume":"18","author":"Jiang","year":"1998","journal-title":"J. Neurosci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1093\/brain\/awaa387","article-title":"Dendritic Pathology, Spine Loss and Synaptic Reorganization in Human Cortex from Epilepsy Patients","volume":"144","author":"Rossini","year":"2021","journal-title":"Brain"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"e13141","DOI":"10.1111\/bpa.13141","article-title":"Dendritic Spine Loss in Epileptogenic Type II Focal Cortical Dysplasia: Role of Enhanced Classical Complement Pathway Activation","volume":"33","author":"Rossini","year":"2023","journal-title":"Brain Pathol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1655","DOI":"10.1152\/jn.00581.2001","article-title":"Network Interactions Mediated by New Excitatory Connections between CA1 Pyramidal Cells in Rats with Kainate-Induced Epilepsy","volume":"87","author":"Smith","year":"2002","journal-title":"J. Neurophysiol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"S14","DOI":"10.1111\/j.1528-1157.2000.tb01550.x","article-title":"Remodeling Dendritic Spines of Dentate Granule Cells in Temporal Lobe Epilepsy Patients and the Rat Pilocarpine Model","volume":"41","author":"Isokawa","year":"2000","journal-title":"Epilepsia"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1016\/j.nbd.2005.01.016","article-title":"Entorhinal Cortex Entrains Epileptiform Activity in CA1 in Pilocarpine-Treated Rats","volume":"19","author":"Wozny","year":"2005","journal-title":"Neurobiol. Dis."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1016\/S0306-4522(02)00567-5","article-title":"Increased Dendritic Excitability in Hippocampal CA1 In Vivo in the Kainic Acid Model of Temporal Lobe Epilepsy: A Study Using Current Source Density Analysis","volume":"116","author":"Wu","year":"2003","journal-title":"Neuroscience"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"4001","DOI":"10.1113\/JP282753","article-title":"Long-Term Potentiation in Neurogliaform Interneurons Modulates Excitation\u2013Inhibition Balance in the Temporoammonic Pathway","volume":"600","author":"Mercier","year":"2022","journal-title":"J. Physiol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1016\/j.neuroscience.2020.10.025","article-title":"D-Serine Intervention In The Medial Entorhinal Area Alters TLE-Related Pathology In CA1 Hippocampus Via The Temporoammonic Pathway","volume":"453","author":"Beesley","year":"2021","journal-title":"Neuroscience"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"6171","DOI":"10.1093\/cercor\/bhac493","article-title":"Cell-Specific Switch for Epileptiform Activity: Critical Role of Interneurons in the Mouse Subicular Network","volume":"33","author":"Wickham","year":"2023","journal-title":"Cereb. Cortex"},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Caron, D., Canal-Alonso, \u00c1., and Panuccio, G. (2022). Mimicking CA3 Temporal Dynamics Controls Limbic Ictogenesis. Biology, 11.","DOI":"10.3390\/biology11030371"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1016\/j.jneumeth.2015.10.006","article-title":"Models of Drug-Induced Epileptiform Synchronization In Vitro","volume":"260","author":"Avoli","year":"2016","journal-title":"J. Neurosci. Methods"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"7873","DOI":"10.1523\/JNEUROSCI.23-21-07873.2003","article-title":"Transition from Interictal to Ictal Activity in Limbic Networks In Vitro","volume":"23","author":"Dzhala","year":"2003","journal-title":"J. Neurosci."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/0304-3940(90)90125-S","article-title":"Epileptiform Discharges and a Synchronous GABAergic Potential Induced by 4-Aminopyridine in the Rat Immature Hippocampus","volume":"117","author":"Avoli","year":"1990","journal-title":"Neurosci. Lett."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1016\/0304-3940(90)90210-Z","article-title":"Synchronization of Epileptiform Bursts Induced by 4-Aminopyridine in the In Vitro Hippocampal Slice Preparation","volume":"112","author":"Ives","year":"1990","journal-title":"Neurosci. Lett."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1914","DOI":"10.1111\/j.1528-1167.2005.00342.x","article-title":"Propagation Dynamics of Epileptiform Activity Acutely Induced by Bicuculline in the Hippocampal\u2013Parahippocampal Region of the Isolated Guinea Pig Brain","volume":"46","author":"Uva","year":"2005","journal-title":"Epilepsia"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1016\/0920-1211(89)90003-X","article-title":"Effects of NMDA Antagonists on Picrotoxin-, Low Mg2+- and Low Ca2+-Induced Epileptogenesis and on Evoked Changes in Extracellular Na+ and Ca2+ Concentrations in Rat Hippocampal Slices","volume":"4","author":"Heinemann","year":"1989","journal-title":"Epilepsy Res."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Landucci, E., Mazzantini, C., Lana, D., Calvani, M., Magni, G., Giovannini, M.G., and Pellegrini-Giampietro, D.E. (2022). Cannabidiol Inhibits Microglia Activation and Mitigates Neuronal Damage Induced by Kainate in an In-Vitro Seizure Model. Neurobiol. Dis., 174.","DOI":"10.1016\/j.nbd.2022.105895"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"869","DOI":"10.1152\/jn.1987.57.3.869","article-title":"Low Extracellular Magnesium Induces Epileptiform Activity and Spreading Depression in Rat Hippocampal Slices","volume":"57","author":"Mody","year":"1987","journal-title":"J. Neurophysiol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"2210","DOI":"10.1093\/brain\/awu133","article-title":"On the Nature of Seizure Dynamics","volume":"137","author":"Jirsa","year":"2014","journal-title":"Brain"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/S0301-0082(02)00077-1","article-title":"Network and Pharmacological Mechanisms Leading to Epileptiform Synchronization in the Limbic System In Vitro","volume":"68","author":"Avoli","year":"2002","journal-title":"Prog. Neurobiol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"627","DOI":"10.1038\/nn.2790","article-title":"Glutamatergic Pre-Ictal Discharges Emerge at the Transition to Seizure in Human Epilepsy","volume":"14","author":"Huberfeld","year":"2011","journal-title":"Nat. Neurosci."},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Amakhin, D.V., Ergina, J.L., Chizhov, A.V., and Zaitsev, A.V. (2016). Synaptic Conductances during Interictal Discharges in Pyramidal Neurons of Rat Entorhinal Cortex. Front. Cell. Neurosci., 10.","DOI":"10.3389\/fncel.2016.00233"},{"key":"ref_62","doi-asserted-by":"crossref","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":"ref_63","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1016\/j.nbd.2012.12.004","article-title":"Two Different Interictal Spike Patterns Anticipate Ictal Activity In Vitro","volume":"52","author":"Avoli","year":"2013","journal-title":"Neurobiol. Dis."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/j.nbd.2004.11.012","article-title":"Repetitive Low-Frequency Stimulation Reduces Epileptiform Synchronization in Limbic Neuronal Networks","volume":"19","author":"Panuccio","year":"2005","journal-title":"Neurobiol. Dis."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"9308","DOI":"10.1523\/JNEUROSCI.17-23-09308.1997","article-title":"CA3-Driven Hippocampal-Entorhinal Loop Controls Rather than Sustains In Vitro Limbic Seizures","volume":"17","author":"Barbarosie","year":"1997","journal-title":"J. Neurosci."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"674","DOI":"10.1002\/ana.21519","article-title":"Fast Activity at Seizure Onset Is Mediated by Inhibitory Circuits in the Entorhinal Cortex In Vitro","volume":"64","author":"Gnatkovsky","year":"2008","journal-title":"Ann. Neurol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"3048","DOI":"10.1523\/JNEUROSCI.3692-14.2015","article-title":"Synchronous Inhibitory Potentials Precede Seizure-like Events in Acute Models of Focal Limbic Seizures","volume":"35","author":"Uva","year":"2015","journal-title":"J. Neurosci."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"634","DOI":"10.1152\/jn.00351.2001","article-title":"Limbic Network Interactions Leading to Hyperexcitability in a Model of Temporal Lobe Epilepsy","volume":"87","author":"Benini","year":"2002","journal-title":"J. Neurophysiol."},{"key":"ref_69","doi-asserted-by":"crossref","unstructured":"Trofimova, A.M., Amakhin, D.V., Postnikova, T.Y., Tiselko, V.S., Alekseev, A., Podoliak, E., Gordeliy, V.I., Chizhov, A.V., and Zaitsev, A.V. (2023). Light-Driven Sodium Pump as a Potential Tool for the Control of Seizures in Epilepsy. Mol. Neurobiol.","DOI":"10.1007\/s12035-023-03865-z"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"2999","DOI":"10.1523\/JNEUROSCI.2244-16.2017","article-title":"Optogenetic Low-Frequency Stimulation of Specific Neuronal Populations Abates Ictogenesis","volume":"37","author":"Shiri","year":"2017","journal-title":"J. Neurosci."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1134\/S0022093021020058","article-title":"Age-Dependent Generation of Epileptiform Activity in the 4-Aminopyridine Model with Slices of the Rat Entorhinal Cortex","volume":"57","author":"Smirnova","year":"2021","journal-title":"J. Evol. Biochem. Physiol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1016\/0920-1211(94)90054-X","article-title":"Quantitative Evaluation of Neuronal Loss in the Dorsal Hippocampus in Rats with Long-Term Pilocarpine Seizures","volume":"17","author":"Liut","year":"1994","journal-title":"Epilepsy Res."},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Postnikova, T.Y., Diespirov, G.P., Amakhin, D.V., Vylekzhanina, E.N., Soboleva, E.B., and Zaitsev, A.V. (2021). Impairments of Long-Term Synaptic Plasticity in the Hippocampus of Young Rats during the Latent Phase of the Lithium-Pilocarpine Model of Temporal Lobe Epilepsy. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms222413355"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1016\/0013-4694(72)90177-0","article-title":"Modification of Seizure Activity by Electrical Stimulation. II. Motor Seizure","volume":"32","author":"Racine","year":"1972","journal-title":"Electroencephalogr. Clin. Neurophysiol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1134\/S0022093022010197","article-title":"The Electrophysiological Properties of Cortical Neurons in the Epileptic Foci of Children with Refractory Temporal Lobe Epilepsy","volume":"58","author":"Malkin","year":"2022","journal-title":"J. Evol. Biochem. Physiol."},{"key":"ref_76","doi-asserted-by":"crossref","unstructured":"Amakhin, D.V., Soboleva, E.B., Ergina, J.L., Malkin, S.L., Chizhov, A.V., and Zaitsev, A.V. (2018). Seizure-Induced Potentiation of AMPA Receptor-Mediated Synaptic Transmission in the Entorhinal Cortex. Front. Cell. Neurosci., 12.","DOI":"10.3389\/fncel.2018.00486"},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"Postnikova, T.Y., Griflyuk, A.V., Amakhin, D.V., Kovalenko, A.A., Soboleva, E.B., Zubareva, O.E., and Zaitsev, A.V. (2021). Early Life Febrile Seizures Impair Hippocampal Synaptic Plasticity in Young Rats. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms22158218"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"2490","DOI":"10.1093\/bioinformatics\/btw172","article-title":"2dSpAn: Semiautomated 2-d Segmentation, Classification and Analysis of Hippocampal Dendritic Spine Plasticity","volume":"32","author":"Basu","year":"2016","journal-title":"Bioinformatics"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/14\/7568\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T15:12:46Z","timestamp":1760109166000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/25\/14\/7568"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,7,10]]},"references-count":78,"journal-issue":{"issue":"14","published-online":{"date-parts":[[2024,7]]}},"alternative-id":["ijms25147568"],"URL":"https:\/\/doi.org\/10.3390\/ijms25147568","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,7,10]]}}}