{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,2]],"date-time":"2026-10-02T00:01:11Z","timestamp":1790899271296,"version":"4.1.0"},"reference-count":59,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2025,5,20]],"date-time":"2025-05-20T00:00:00Z","timestamp":1747699200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Calcium-binding proteins (CaBPs) are known to modulate neuronal excitability and calcium signaling, and they may play a role in the imbalances of excitation and inhibition of temporal lobe epilepsy (TLE). While parvalbumin and calretinin are well-characterized CaBPs, N-Terminal EF-Hand Calcium-Binding Protein 1 (NECAB1) remains understudied in epilepsy, despite its association with neurodegenerative conditions. In this study, we used fluorescent immunolabeling to determine the distribution of NECAB1, as well as its co-expression with parvalbumin and calretinin, in brain regions associated with the epileptic circuitry using a kainic acid-induced TLE model. Additionally, we examined the impact of levetiracetam and brivaracetam on NECAB1 expression. In our study, NECAB1-positive cells were prominently localized to the paraventricular nucleus of the thalamus (PVT), endopiriform nucleus (EPN), and amygdala in healthy brain regions involved in epileptic circuitry. A NECAB1\u2013calretinin co-expressing subpopulation was detected in the amygdala, PVT, and hippocampus but was nearly absent in the EPN. In chronic epilepsy, NECAB1 expression was significantly upregulated in the PVT and bilaterally in the amygdala. These findings suggest that NECAB1 upregulation may compensate for epileptic hyperexcitability, potentially contributing to circuit remodeling via thalamocortical regulation and interneuron diversity. Levetiracetam and brivaracetam treatments partially reduced the NECAB1 density increase in TLE, indicating a modulatory effect on NECAB1 expression.<\/jats:p>","DOI":"10.3390\/ijms26104906","type":"journal-article","created":{"date-parts":[[2025,5,20]],"date-time":"2025-05-20T11:50:31Z","timestamp":1747741831000},"page":"4906","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Distribution of NECAB1-Positive Neurons in Normal and Epileptic Brain\u2014Expression Changes in Temporal Lobe Epilepsy and Modulation by Levetiracetam and Brivaracetam"],"prefix":"10.3390","volume":"26","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6113-3419","authenticated-orcid":false,"given":"Krisztina","family":"Kelemen","sequence":"first","affiliation":[{"name":"Department of Physiology, George Emil Palade University of Medicine, Pharmacy, Science, and Technology of Targu Mures, 540142 T\u00e2rgu Mure\u0219, Romania"},{"name":"Doctoral School, George Emil Palade University of Medicine, Pharmacy, Science, and Technology of Targu Mures, 540142 T\u00e2rgu Mure\u0219, Romania"},{"name":"Molecular Neurobiology Research Group, HUN-REN Institute of Experimental Medicine, Szigony st 43, H-1083 Budapest, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7786-0899","authenticated-orcid":false,"given":"K\u00e1roly","family":"Orb\u00e1n-Kis","sequence":"additional","affiliation":[{"name":"Department of Physiology, George Emil Palade University of Medicine, Pharmacy, Science, and Technology of Targu Mures, 540142 T\u00e2rgu Mure\u0219, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"\u00c1d\u00e1m","family":"Szentes","sequence":"additional","affiliation":[{"name":"Faculty of Medicine, George Emil Palade University of Medicine, Pharmacy, Science, and Technology of Targu Mures, 540142 T\u00e2rgu Mure\u0219, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zsolt Andr\u00e1s","family":"Nagy","sequence":"additional","affiliation":[{"name":"Faculty of Medicine, George Emil Palade University of Medicine, Pharmacy, Science, and Technology of Targu Mures, 540142 T\u00e2rgu Mure\u0219, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0004-7894-8050","authenticated-orcid":false,"given":"Hanga","family":"Kelemen","sequence":"additional","affiliation":[{"name":"Translational Behavioural Neuroscience Research Group, HUN-REN Institute of Experimental Medicine, Szigony st 43, H-1083 Budapest, Hungary"},{"name":"J\u00e1nos Szent\u00e1gothai Neurosciences Division, Doctoral College, Semmelweis University, Ulloi st 26, H-1085 Budapest, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna","family":"Feh\u00e9r","sequence":"additional","affiliation":[{"name":"Faculty of Medicine, George Emil Palade University of Medicine, Pharmacy, Science, and Technology of Targu Mures, 540142 T\u00e2rgu Mure\u0219, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8682-0429","authenticated-orcid":false,"given":"L\u00e1szl\u00f3-Istv\u00e1n","family":"B\u00e1ba","sequence":"additional","affiliation":[{"name":"Department of Pharmacology and Clinical Pharmacy, George Emil Palade University of Medicine, Pharmacy, Science and Technology of Targu Mures, 540142 T\u00e2rgu Mures, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9091-277X","authenticated-orcid":false,"given":"Zsolt","family":"G\u00e1ll","sequence":"additional","affiliation":[{"name":"Department of Pharmacology and Clinical Pharmacy, George Emil Palade University of Medicine, Pharmacy, Science and Technology of Targu Mures, 540142 T\u00e2rgu Mures, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eszter","family":"Horv\u00e1th","sequence":"additional","affiliation":[{"name":"Molecular Neurobiology Research Group, HUN-REN Institute of Experimental Medicine, Szigony st 43, H-1083 Budapest, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Istv\u00e1n","family":"Katona","sequence":"additional","affiliation":[{"name":"Molecular Neurobiology Research Group, HUN-REN Institute of Experimental Medicine, Szigony st 43, H-1083 Budapest, Hungary"},{"name":"Department of Psychological and Brain Sciences, Indiana University Bloomington, 702 N Walnut Grove Ave, Bloomington, IN 47405-2204, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8197-3231","authenticated-orcid":false,"given":"Szabolcs","family":"Szatm\u00e1ri","sequence":"additional","affiliation":[{"name":"Department of Neurology, George Emil Palade University of Medicine, Pharmacy, Science, and Technology of Targu Mures, 540142 T\u00e2rgu Mure\u0219, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1675-036X","authenticated-orcid":false,"given":"J\u00f3zsef Attila","family":"Sz\u00e1sz","sequence":"additional","affiliation":[{"name":"Department of Neurology, George Emil Palade University of Medicine, Pharmacy, Science, and Technology of Targu Mures, 540142 T\u00e2rgu Mure\u0219, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6261-1163","authenticated-orcid":false,"given":"Tibor","family":"Szil\u00e1gyi","sequence":"additional","affiliation":[{"name":"Department of Physiology, George Emil Palade University of Medicine, Pharmacy, Science, and Technology of Targu Mures, 540142 T\u00e2rgu Mure\u0219, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,5,20]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1097\/WNP.0000000000000160","article-title":"The Role of Inhibition in Epileptic Networks","volume":"32","author":"Trevelyan","year":"2015","journal-title":"J. Clin. Neurophysiol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2406835","DOI":"10.1002\/advs.202406835","article-title":"Temporal Lobe Epilepsy Perturbs the Brain-Wide Excitation-Inhibition Balance: Associations with Microcircuit Organization, Clinical Parameters, and Cognitive Dysfunction","volume":"12","author":"Xie","year":"2025","journal-title":"Adv. Sci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"340","DOI":"10.1177\/107385840100700410","article-title":"Mesial Temporal Lobe Epilepsy: What Have We Learned?","volume":"7","author":"Engel","year":"2001","journal-title":"Neuroscient"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1038\/nrn1728","article-title":"Drug resistance in brain diseases and the role of drug efflux transporters","volume":"6","author":"Potschka","year":"2005","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_5","unstructured":"Engel, J., Pedley, T.A., and Aicardi, J. (2007). Epilepsy: A Comprehensive Textbook, Lippincott Williams & Wilkins, A Wolters Kluwer Business. [2nd ed.]."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/j.neuropharm.2014.09.011","article-title":"Tasks for inhibitory interneurons in intact brain circuits","volume":"88","author":"Roux","year":"2015","journal-title":"Neuropharmacology"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.tins.2004.11.011","article-title":"Multiple facets of GABAergic neurons and synapses: Multiple fates of GABA signalling in epilepsies","volume":"28","author":"Cossart","year":"2005","journal-title":"Trends Neurosci."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1016\/0166-2236(92)90081-I","article-title":"Calcium-binding proteins in the nervous system","volume":"15","author":"Baimbridge","year":"1992","journal-title":"Trends Neurosci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1007\/s00018-008-8564-6","article-title":"The continuing disappearance of \u201cpure\u201d Ca2+ buffers","volume":"66","author":"Schwaller","year":"2009","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1042\/bj3530001","article-title":"The neuronal calcium sensor family of Ca2+-binding proteins","volume":"353","author":"Burgoyne","year":"2001","journal-title":"Biochem. J."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1038\/nrm1155","article-title":"Calcium signalling: Dynamics, homeostasis and remodelling","volume":"4","author":"Berridge","year":"2003","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1786","DOI":"10.1093\/cercor\/bhaa326","article-title":"Necab1 and necab2 are prevalent calcium-binding proteins of cb1\/cck-positive gabaergic interneurons","volume":"31","author":"Kelemen","year":"2021","journal-title":"Cereb. Cortex"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"4007","DOI":"10.1007\/s12035-021-02356-3","article-title":"Proteomic and Transcriptomic Analyses Reveal Pathological Changes in the Entorhinal Cortex Region that Correlate Well with Dysregulation of Ion Transport in Patients with Alzheimer\u2019s Disease","volume":"58","author":"Jia","year":"2021","journal-title":"Mol. Neurobiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1186\/s40478-020-01110-5","article-title":"14-3-3 mitigates alpha-synuclein aggregation and toxicity in the in vivo preformed fibril model","volume":"9","author":"Underwood","year":"2021","journal-title":"Acta Neuropathol. Commun."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"e20152469","DOI":"10.1542\/peds.2015-2469","article-title":"Genome-Wide Association and Exome Sequencing Study of Language Disorder in an Isolated Population","volume":"137","author":"Kornilov","year":"2016","journal-title":"Pediatrics"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1016\/j.seizure.2023.09.021","article-title":"Epilepsy-Associated Genes: An Update","volume":"116","author":"Zhang","year":"2024","journal-title":"Seizure: Eur. J. Epilepsy"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1111\/j.1460-9568.1997.tb01634.x","article-title":"Interneurons in the Hippocampal Dentate Gyrus: An In Vivo intracellular Study","volume":"9","author":"Sik","year":"1997","journal-title":"Eur. J. Neurosci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1124\/pr.110.003046","article-title":"Prevention or Modification of Epileptogenesis after Brain Insults: Experimental Approaches and Translational Research","volume":"62","author":"Brandt","year":"2010","journal-title":"Pharmacol. Rev."},{"key":"ref_19","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":"Gillard","year":"2016","journal-title":"CNS Drugs"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1016\/j.brainres.2015.03.005","article-title":"Prevention of status epilepticus-induced brain edema and neuronal cell loss by repeated treatment with high-dose levetiracetam","volume":"1608","author":"Itoh","year":"2015","journal-title":"Brain Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/j.expneurol.2012.01.028","article-title":"Neuronal circuits in epilepsy: Do they matter?","volume":"244","author":"Bertram","year":"2013","journal-title":"Exp. Neurol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Kelemen, K., and Szil\u00e1gyi, T. (2021). New approach for untangling the role of uncommon calcium-binding proteins in the central nervous system. Brain Sci., 11.","DOI":"10.3390\/brainsci11050634"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Malikovi\u0107, J., Amrein, I., Vinciguerra, L., Wolfer, D.P., and Slomianka, L. (2024). NECAB1-3, parvalbumin, calbindin, and calretinin in the hippocampus of the European mole. Front. Neuroanat., 18.","DOI":"10.3389\/fnana.2024.1452722"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1016\/j.brainres.2017.10.028","article-title":"Hemispheric differences in the number of parvalbumin-positive neurons in subdivisions of the rat basolateral amygdala complex","volume":"1678","author":"Butler","year":"2018","journal-title":"Brain Res."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"e64875","DOI":"10.7554\/eLife.64875","article-title":"Single-cell and single-nucleus RNA-seq uncovers shared and distinct axes of variation in dorsal LGN neurons in mice, non-human primates, and humans","volume":"10","author":"Bakken","year":"2021","journal-title":"Elife"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1802","DOI":"10.1038\/nn.3550","article-title":"Network state-dependent inhibition of identified hippocampal CA3 axo-axonic cells in vivo","volume":"16","author":"Viney","year":"2013","journal-title":"Nat. Neurosci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1038\/s41593-021-00996-1","article-title":"Thalamic Subnetworks as Units of Function","volume":"25","author":"Roy","year":"2022","journal-title":"Nat. Neurosci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1925","DOI":"10.1038\/s41593-019-0483-3","article-title":"A repeated molecular architecture across thalamic pathways","volume":"22","author":"Phillips","year":"2019","journal-title":"Nat. Neurosci."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"113842","DOI":"10.1016\/j.celrep.2024.113842","article-title":"The cell-type-specific spatial organization of the anterior thalamic nuclei of the mouse brain","volume":"43","author":"Kapustina","year":"2024","journal-title":"Cell Rep."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1016\/j.seizure.2022.11.007","article-title":"Intracellular calcium homeostasis and its dysregulation underlying epileptic seizures","volume":"103","author":"Zhou","year":"2022","journal-title":"Seizure Eur. J. Epilepsy"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Xu, J.-H., and Tang, F.-R. (2018). Voltage-Dependent Calcium Channels, Calcium Binding Proteins, and Their Interaction in the Pathological Process of Epilepsy. Int. J. Mol. Sci., 19.","DOI":"10.3390\/ijms19092735"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Thomas, N.L., Dart, C., and Helassa, N. (2023). Editorial: The role of calcium and calcium binding proteins in cell physiology and disease. Front. Physiol., 14.","DOI":"10.3389\/fphys.2023.1228885"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1021\/ar100110d","article-title":"Relating Form and Function of EF-Hand Calcium Binding Proteins","volume":"44","author":"Chazin","year":"2011","journal-title":"Acc. Chem. Res."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Schwaller, B. (2010). Cytosolic Ca2+ Buffers. Cold Spring Harb. Perspect. Biol., 2.","DOI":"10.1101\/cshperspect.a004051"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1207","DOI":"10.1111\/epi.13053","article-title":"Calcium-binding proteins in focal cortical dysplasia","volume":"56","author":"Kuchukhidze","year":"2015","journal-title":"Epilepsia"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Mih\u00e1ly, I., Moln\u00e1r, T., Berki, \u00c1.-J., Bod, R.-B., Orb\u00e1n-Kis, K., G\u00e1ll, Z., and Szil\u00e1gyi, T. (2021). Short-Term Amygdala Low-Frequency Stimulation Does not Influence Hippocampal Interneuron Changes Observed in the Pilocarpine Model of Epilepsy. Cells, 10.","DOI":"10.3390\/cells10030520"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Godoy, L.D., Prizon, T., Rossignoli, M.T., Leite, J.P., and Liberato, J.L. (2022). Parvalbumin Role in Epilepsy and Psychiatric Comorbidities: From Mechanism to Intervention. Front. Integr. Neurosci., 16.","DOI":"10.3389\/fnint.2022.765324"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1111\/j.1528-1167.2010.02624.x","article-title":"Dynamic changes of CB1-receptor expression in hippocampi of epileptic mice and humans","volume":"51","author":"Nagy","year":"2010","journal-title":"Epilepsia"},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Karl\u00f3cai, M.R., T\u00f3th, K., Watanabe, M., Ledent, C., Juh\u00e1sz, G., Freund, T.F., and Magl\u00f3czky, Z. (2011). Redistribution of CB1 Cannabinoid Receptors in the Acute and Chronic Phases of Pilocarpine-Induced Epilepsy. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0027196"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Lazarini-Lopes, W., da Silva-J\u00fanior, R.M.P., Servilha-Menezes, G., Do Val-da Silva, R.A., and Garcia-Cairasco, N. (2020). Cannabinoid Receptor Type 1 (CB1R) Expression in Limbic Brain Structures After Acute and Chronic Seizures in a Genetic Model of Epilepsy. Front. Behav. Neurosci., 14.","DOI":"10.3389\/fnbeh.2020.602258"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1038\/nrn3937","article-title":"Weeding out bad waves: Towards selective cannabinoid circuit control in epilepsy","volume":"16","author":"Soltesz","year":"2015","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2976","DOI":"10.1523\/JNEUROSCI.4465-07.2008","article-title":"Downregulation of the CB1 cannabinoid receptor and related molecular elements of the endocannabinoid system in epileptic human hippocampus","volume":"28","author":"Eross","year":"2008","journal-title":"J. Neurosci."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1007\/s12264-021-00753-1","article-title":"Revealing the Precise Role of Calretinin Neurons in Epilepsy: We Are on the Way","volume":"38","author":"Qi","year":"2022","journal-title":"Neurosci. Bull."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"2763","DOI":"10.1093\/brain\/awq149","article-title":"Loss and reorganization of calretinin-containing interneurons in the epileptic human hippocampus","volume":"133","author":"Toth","year":"2010","journal-title":"Brain"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Navarro, D., Alvarado, M., Figueroa, A., Gonzalez-Liencres, C., Salas-Lucia, F., Pacheco, P., Sanzhez-Vives, M.V., and Berbel, P. (2019). Distribution of GABAergic Neurons and VGluT1 and VGAT Immunoreactive Boutons in the Ferret (Mustela putorius) Piriform Cortex and Endopiriform Nucleus. Comparison With Visual Areas 17, 18 and 19. Front. Neuroanat., 13.","DOI":"10.3389\/fnana.2019.00054"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1586\/ern.10.3","article-title":"Levetiracetam: A comprehensive review","volume":"10","author":"Crepeau","year":"2010","journal-title":"Expert. Rev. Neurother."},{"key":"ref_47","first-page":"1","article-title":"A review of the pharmacology and clinical efficacy of brivaracetam","volume":"10","author":"Klein","year":"2018","journal-title":"Clin. Pharmacol."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Kelemen, K., S\u00e1rosi, M., Cs\u00fcd\u00f6r, \u00c1., Orb\u00e1n-Kis, K., Kelemen, H., B\u00e1ba, L., G\u00e1ll, Z., Horv\u00e1th, E., Katona, I., and Szil\u00e1gyi, T. (2025). Marked differences in the effects of levetiracetam and its analogue brivaracetam on microglial, astrocytic, and neuronal density in the rat model of kainic acid-induced temporal lobe epilepsy. Front. Pharmacol., 16.","DOI":"10.3389\/fphar.2025.1553545"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"e16308","DOI":"10.1111\/jnc.16308","article-title":"Control of Synaptotagmin-1 Trafficking by SV2A\u2014Mechanism and Consequences for Presynaptic Function and Dysfunction","volume":"169","author":"Hogg","year":"2025","journal-title":"J. Neurochem."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"10415","DOI":"10.1073\/pnas.94.19.10415","article-title":"Impaired long-term potentiation induction in dentate gyrus of calretinin-deficient\u2009mice","volume":"94","author":"Schurmans","year":"1997","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1016\/S0306-4522(96)00440-X","article-title":"Loss of Calbindin-D28K immunoreactivity from dentate granule cells in human temporal lobe epilepsy","volume":"76","author":"Vajda","year":"1997","journal-title":"Neuroscience"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1002\/cne.10630","article-title":"\u201cDormant basket cell\u201d hypothesis revisited: Relative vulnerabilities of dentate gyrus mossy cells and inhibitory interneurons after hippocampal status epilepticus in the rat","volume":"459","author":"Sloviter","year":"2003","journal-title":"J. Comp. Neurol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1016\/S0306-4522(01)00446-8","article-title":"Preservation of perisomatic inhibitory input of granule cells in the epileptic human dentate gyrus","volume":"108","author":"Wittner","year":"2001","journal-title":"Neuroscience"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1378","DOI":"10.1111\/ejn.15032","article-title":"Cholinergic modulation of Up\u2013Down states in the mouse medial entorhinal cortex in vitro","volume":"53","author":"Hay","year":"2021","journal-title":"Eur. J. Neurosci."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"15812","DOI":"10.1523\/JNEUROSCI.2639-15.2015","article-title":"Synaptic Targets of Medial Septal Projections in the Hippocampus and Extrahippocampal Cortices of the Mouse","volume":"35","author":"Unal","year":"2015","journal-title":"J. Neurosci."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"ENEURO.0337-20.2021","DOI":"10.1523\/ENEURO.0337-20.2021","article-title":"The kainic acid models of temporal lobe epilepsy","volume":"8","author":"Rusina","year":"2021","journal-title":"ENeuro"},{"key":"ref_57","unstructured":"Paxinos, G., Watson, C., Paxinos, G., and Watson, C. (2007). The Rat Brain in Stereotaxic Coordinates: Hard Cover Edition, Academic Press. [6th ed.]."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1016\/j.physbeh.2009.09.005","article-title":"A revised Racine\u2019s scale for PTZ-induced seizures in rats","volume":"98","author":"Fabene","year":"2009","journal-title":"Physiol. Behav."},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"B\u00e1ba, L.I., G\u00e1ll, Z., Kolcs\u00e1r, M., Pap, Z., Varga, Z.V., Kov\u00e1cs, B., Hack, B., and Kun, I.-Z. (2020). Effect on body weight and adipose tissue by cariprazine: A head-to-head comparison study to olanzapine and aripiprazole in rats. Sci. Pharm., 88.","DOI":"10.3390\/scipharm88040050"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/10\/4906\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T17:35:58Z","timestamp":1760031358000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/10\/4906"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,5,20]]},"references-count":59,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2025,5]]}},"alternative-id":["ijms26104906"],"URL":"https:\/\/doi.org\/10.3390\/ijms26104906","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,5,20]]}}}