{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,23]],"date-time":"2026-04-23T02:09:50Z","timestamp":1776910190795,"version":"3.51.2"},"reference-count":53,"publisher":"Pharmaceutical Society of Japan","issue":"6","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biological &amp; Pharmaceutical Bulletin","Biol. Pharm. Bull."],"published-print":{"date-parts":[[2016]]},"DOI":"10.1248\/bpb.b16-00125","type":"journal-article","created":{"date-parts":[[2016,5,31]],"date-time":"2016-05-31T22:05:30Z","timestamp":1464732330000},"page":"891-896","source":"Crossref","is-referenced-by-count":18,"title":["Dentate Circuitry as a Model to Study Epileptogenesis"],"prefix":"10.1248","volume":"39","author":[{"given":"Ryuta","family":"Koyama","sequence":"first","affiliation":[{"name":"Laboratory of Chemical Pharmacology, Graduate School of Pharmaceutical Sciences, The University of Tokyo"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"163","reference":[{"key":"1","doi-asserted-by":"crossref","unstructured":"1) Amaral DG, Scharfman HE, Lavenex P. The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). <i>Prog. Brain Res.<\/i>, <b>163<\/b>, 3\u201322, 788\u2013790 (2007).","DOI":"10.1016\/S0079-6123(07)63001-5"},{"key":"2","unstructured":"2) Heinemann U, Beck H, Dreier JP, Ficker E, Stabel J, Zhang CL. The dentate gyrus as a regulated gate for the propagation of epileptiform activity. <i>Epilepsy Res. Suppl.<\/i>, <b>7<\/b>, 273\u2013280 (1992)."},{"key":"3","unstructured":"3) Lothman EW, Stringer JL, Bertram EH. The dentate gyrus as a control point for seizures in the hippocampus and beyond. <i>Epilepsy Res. Suppl.<\/i>, <b>7<\/b>, 301\u2013313 (1992)."},{"key":"4","doi-asserted-by":"crossref","unstructured":"4) Nadler JV. The recurrent mossy fiber pathway of the epileptic brain. <i>Neurochem. Res.<\/i>, <b>28<\/b>, 1649\u20131658 (2003).","DOI":"10.1023\/A:1026004904199"},{"key":"5","doi-asserted-by":"crossref","unstructured":"5) Koyama R, Ikegaya Y. Mossy fiber sprouting as a potential therapeutic target for epilepsy. <i>Curr. Neurovasc. Res.<\/i>, <b>1<\/b>, 3\u201310 (2004).","DOI":"10.2174\/1567202043480242"},{"key":"6","doi-asserted-by":"crossref","unstructured":"6) Sloviter RS, Bumanglag AV, Schwarcz R, Frotscher M. Abnormal dentate gyrus network circuitry in temporal lobe epilepsy. <i>Jasper\u2019s Basic Mechanisms of the Epilepsies<\/i> [Internet]. 4th ed. (Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta AV eds.), National Center for Biotechnology Information U.S.A. (2012).","DOI":"10.1093\/med\/9780199746545.003.0034"},{"key":"7","doi-asserted-by":"crossref","unstructured":"7) Buckmaster PS, Zhang GF, Yamawaki R. Axon sprouting in a model of temporal lobe epilepsy creates a predominantly excitatory feedback circuit. <i>J. Neurosci.<\/i>, <b>22<\/b>, 6650\u20136658 (2002).","DOI":"10.1523\/JNEUROSCI.22-15-06650.2002"},{"key":"8","doi-asserted-by":"crossref","unstructured":"8) Cavazos JE, Zhang P, Qazi R, Sutula TP. Ultrastructural features of sprouted mossy fiber synapses in kindled and kainic acid-treated rats. <i>J. Comp. Neurol.<\/i>, <b>458<\/b>, 272\u2013292 (2003).","DOI":"10.1002\/cne.10581"},{"key":"9","doi-asserted-by":"crossref","unstructured":"9) Masukawa LM, Higashima M, Kim JH, Spencer DD. Epileptiform discharges evoked in hippocampal brain slices from epileptic patients. <i>Brain Res.<\/i>, <b>493<\/b>, 168\u2013174 (1989).","DOI":"10.1016\/0006-8993(89)91012-3"},{"key":"10","doi-asserted-by":"crossref","unstructured":"10) Isokawa M, Fried I. Extracellular slow negative transient in the dentate gyrus of human epileptic hippocampus <i>in vitro<\/i>. <i>Neuroscience<\/i>, <b>72<\/b>, 31\u201337 (1996).","DOI":"10.1016\/0306-4522(95)00544-7"},{"key":"11","doi-asserted-by":"crossref","unstructured":"11) Patrylo PR, Schweitzer JS, Dudek FE. Abnormal responses to perforant path stimulation in the dentate gyrus of slices from rats with kainate-induced epilepsy and mossy fiber reorganization. <i>Epilepsy Res.<\/i>, <b>36<\/b>, 31\u201342 (1999).","DOI":"10.1016\/S0920-1211(99)00022-4"},{"key":"12","doi-asserted-by":"crossref","unstructured":"12) Sutula T, He XX, Cavazos J, Scott G. Synaptic reorganization in the hippocampus induced by abnormal functional activity. <i>Science<\/i>, <b>239<\/b>, 1147\u20131150 (1988).","DOI":"10.1126\/science.2449733"},{"key":"13","unstructured":"13) Cavazos JE, Golarai G, Sutula TP. Mossy fiber synaptic reorganization induced by kindling: time course of development, progression, and permanence. <i>J. Neurosci.<\/i>, <b>11<\/b>, 2795\u20132803 (1991)."},{"key":"14","doi-asserted-by":"crossref","unstructured":"14) Koyama R, Yamada MK, Nishiyama N, Matsuki N, Ikegaya Y. Group II metabotropic glutamate receptor activation is required for normal hippocampal mossy fibre development in the rat. <i>J. Physiol.<\/i>, <b>539<\/b>, 157\u2013162 (2002).","DOI":"10.1113\/jphysiol.2001.013505"},{"key":"15","doi-asserted-by":"crossref","unstructured":"15) Koyama R, Yamada MK, Nishiyama N, Matsuki N, Ikegaya Y. Developmental switch in axon guidance modes of hippocampal mossy fibers <i>in vitro.<\/i> <i>Dev. Biol.<\/i>, <b>267<\/b>, 29\u201342 (2004a).","DOI":"10.1016\/j.ydbio.2003.11.008"},{"key":"16","doi-asserted-by":"crossref","unstructured":"16) Koyama R, Yamada MK, Fujisawa S, Katoh-Semba R, Matsuki N, Ikegaya Y. Brain-derived neurotrophic factor induces hyperexcitable reentrant circuits in the dentate gyrus. <i>J. Neurosci.<\/i>, <b>24<\/b>, 7215\u20137224 (2004b).","DOI":"10.1523\/JNEUROSCI.2045-04.2004"},{"key":"17","doi-asserted-by":"crossref","unstructured":"17) Koyama R, Ikegaya Y. To BDNF or not to BDNF: that is the epileptic hippocampus. <i>Neuroscientist<\/i>, <b>11<\/b>, 282\u2013287 (2005).","DOI":"10.1177\/1073858405278266"},{"key":"18","doi-asserted-by":"crossref","unstructured":"18) Zhou Z, Tanaka KF, Matsunaga S, Iseki M, Watanabe M, Matsuki N, Ikegaya Y, Koyama R. Photoactivated adenylyl cyclase (PAC) reveals novel mechanisms underlying cAMP-dependent axonal morphogenesis. <i>Sci. Rep.<\/i>, <b>5<\/b>, 19679 (2016).","DOI":"10.1038\/srep19679"},{"key":"19","doi-asserted-by":"crossref","unstructured":"19) Muramatsu R, Nakahara S, Ichikawa J, Watanabe K, Matsuki N, Koyama R. The ratio of \u2018deleted in colorectal cancer\u2019 to \u2018uncoordinated-5A\u2019 netrin-1 receptors on the growth cone regulates mossy fibre directionality. <i>Brain<\/i>, <b>133<\/b>, 60\u201375 (2010).","DOI":"10.1093\/brain\/awp266"},{"key":"20","doi-asserted-by":"crossref","unstructured":"20) Shibata K, Nakahara S, Shimizu E, Yamashita T, Matsuki N, Koyama R. Repulsive guidance molecule a regulates hippocampal mossy fiber branching <i>in vitro.<\/i> <i>Neuroreport<\/i>, <b>24<\/b>, 609\u2013615 (2013).","DOI":"10.1097\/WNR.0b013e3283632c08"},{"key":"21","doi-asserted-by":"crossref","unstructured":"21) Tao K, Matsuki N, Koyama R. AMP-activated protein kinase mediates activity-dependent axon branching by recruiting mitochondria to axon. <i>Dev. Neurobiol.<\/i>, <b>74<\/b>, 557\u2013573 (2014).","DOI":"10.1002\/dneu.22149"},{"key":"22","doi-asserted-by":"crossref","unstructured":"22) M\u00fcnster-Wandowski A, Gomez-Lira G, Gutierrez R. Mixed neurotransmission in the hippocampal mossy fibers. <i>Front. Cell. Neurosci.<\/i>, <b>7<\/b>, 210 (2013).","DOI":"10.3389\/fncel.2013.00210"},{"key":"23","doi-asserted-by":"crossref","unstructured":"23) Ram\u00edrez M, Gutierrez R. Activity-dependent expression of GAD67 in the granule cells of the rat hippocampus. <i>Brain Res.<\/i>, <b>917<\/b>, 139\u2013146 (2001).","DOI":"10.1016\/S0006-8993(01)02794-9"},{"key":"24","doi-asserted-by":"crossref","unstructured":"24) G\u00f3mez-Lira G, Trillo E, Ramirez M, Asai M, Sitges M, Gutierrez R. The expression of GABA in mossy fiber synaptosomes coincides with the seizure-induced expression of GABAergic transmission in the mossy fiber synapse. <i>Exp. Neurol.<\/i>, <b>177<\/b>, 276\u2013283 (2002).","DOI":"10.1006\/exnr.2002.7986"},{"key":"25","doi-asserted-by":"crossref","unstructured":"25) Cohen I, Navarro V, Clemenceau S, Baulac M, Miles R. On the origin of interictal activity in human temporal lobe epilepsy <i>in vitro.<\/i> <i>Science<\/i>, <b>298<\/b>, 1418\u20131421 (2002).","DOI":"10.1126\/science.1076510"},{"key":"26","doi-asserted-by":"crossref","unstructured":"26) Nissinen J, Lukasiuk K, Pitkanen A. Is mossy fiber sprouting present at the time of the first spontaneous seizures in rat experimental temporal lobe epilepsy? <i>Hippocampus<\/i>, <b>11<\/b>, 299\u2013310 (2001).","DOI":"10.1002\/hipo.1044"},{"key":"27","doi-asserted-by":"crossref","unstructured":"27) Houser CR. Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. <i>Brain Res.<\/i>, <b>535<\/b>, 195\u2013204 (1990).","DOI":"10.1016\/0006-8993(90)91601-C"},{"key":"28","doi-asserted-by":"crossref","unstructured":"28) Lurton D, El Bahh B, Sundstrom L, Rougier A. Granule cell dispersion is correlated with early epileptic events in human temporal lobe epilepsy. <i>J. Neurol. Sci.<\/i>, <b>154<\/b>, 133\u2013136 (1998).","DOI":"10.1016\/S0022-510X(97)00220-7"},{"key":"29","doi-asserted-by":"crossref","unstructured":"29) Riban V, Bouilleret V, Pham-L\u00eaBT, L, Fritschy JM, Marescaux C, Depaulis A. Evolution of hippocampal epileptic activity during the development of hippocampal sclerosis in a mouse model of temporal lobe epilepsy. <i>Neuroscience<\/i>, <b>112<\/b>, 101\u2013111 (2002).","DOI":"10.1016\/S0306-4522(02)00064-7"},{"key":"30","doi-asserted-by":"crossref","unstructured":"30) Parent JM, Murphy GG. Mechanisms and functional significance of aberrant seizure-induced hippocampal neurogenesis. <i>Epilepsia<\/i>, <b>49<\/b> (Suppl. 5), 19\u201325 (2008).","DOI":"10.1111\/j.1528-1167.2008.01634.x"},{"key":"31","doi-asserted-by":"crossref","unstructured":"31) Scharfman H, Goodman J, McCloskey D. Ectopic granule cells of the rat dentate gyrus. <i>Dev. Neurosci.<\/i>, <b>29<\/b>, 14\u201327 (2007).","DOI":"10.1159\/000096208"},{"key":"32","doi-asserted-by":"crossref","unstructured":"32) Muramatsu R, Ikegaya Y, Matsuki N, Koyama R. Early-life status epilepticus induces ectopic granule cells in adult mice dentate gyrus. <i>Exp. Neurol.<\/i>, <b>211<\/b>, 503\u2013510 (2008).","DOI":"10.1016\/j.expneurol.2008.02.026"},{"key":"33","doi-asserted-by":"crossref","unstructured":"33) Scharfman HE, Sollas AL, Goodman JH. Spontaneous recurrent seizures after pilocarpine-induced status epilepticus activate calbindin-immunoreactive hilar cells of the rat dentate gyrus. <i>Neuroscience<\/i>, <b>111<\/b>, 71\u201381 (2002).","DOI":"10.1016\/S0306-4522(01)00599-1"},{"key":"34","unstructured":"34) Scharfman HE, Goodman JH, Sollas AL. Granule-like neurons at the hilar\/CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: functional implications of seizure-induced neurogenesis. <i>J. Neurosci.<\/i>, <b>20<\/b>, 6144\u20136158 (2000)."},{"key":"35","doi-asserted-by":"crossref","unstructured":"35) Bell B, Lin JJ, Seidenberg M, Hermann B. The neurobiology of cognitive disorders in temporal lobe epilepsy. <i>Nat. Rev. Neurol.<\/i>, <b>7<\/b>, 154\u2013164 (2011).","DOI":"10.1038\/nrneurol.2011.3"},{"key":"36","doi-asserted-by":"crossref","unstructured":"36) Myers CE, Bermudez-Hernandez K, Scharfman HE. The influence of ectopic migration of granule cells into the hilus on dentate gyrus-CA3 function. <i>PLoS ONE<\/i>, <b>8<\/b>, e68208 (2013).","DOI":"10.1371\/journal.pone.0068208"},{"key":"37","doi-asserted-by":"crossref","unstructured":"37) Tao K, Ichikawa J, Matsuki N, Ikegaya Y, Koyama R. Experimental febrile seizures induce age-dependent structural plasticity and improve memory in mice. <i>Neuroscience<\/i>, <b>318<\/b>, 34\u201344 (2016).","DOI":"10.1016\/j.neuroscience.2016.01.011"},{"key":"38","doi-asserted-by":"crossref","unstructured":"38) Koyama R, Tao K, Sasaki T, Ichikawa J, Miyamoto D, Muramatsu R, Matsuki N, Ikegaya Y. GABAergic excitation after febrile seizures induces ectopic granule cells and adult epilepsy. <i>Nat. Med.<\/i>, <b>18<\/b>, 1271\u20131278 (2012).","DOI":"10.1038\/nm.2850"},{"key":"39","doi-asserted-by":"crossref","unstructured":"39) Koyama R. The use of organotypic slice cultures for the study of epileptogenesis. <i>Neuropathology<\/i>, <b>33<\/b>, 475\u2013479 (2013).","DOI":"10.1111\/neup.12019"},{"key":"40","doi-asserted-by":"crossref","unstructured":"40) Koyama R, Matsuki N. Novel etiological and therapeutic strategies for neurodiseases: mechanisms and consequences of febrile seizures: lessons from animal models. <i>J. Pharmacol. Sci.<\/i>, <b>113<\/b>, 14\u201322 (2010).","DOI":"10.1254\/jphs.09R19FM"},{"key":"41","doi-asserted-by":"crossref","unstructured":"41) Muramatsu R, Ikegaya Y, Matsuki N, Koyama R. Neonatally born granule cells numerically dominate adult mice dentate gyrus. <i>Neuroscience<\/i>, <b>148<\/b>, 593\u2013598 (2007).","DOI":"10.1016\/j.neuroscience.2007.06.040"},{"key":"42","doi-asserted-by":"crossref","unstructured":"42) Sajo M, Sugiyama H, Yamamoto H, Tanii T, Matsuki N, Ikegaya Y, Koyama R. Neuraminidase-dependent degradation of polysialic acid is required for the lamination of newly generated neurons. <i>PLoS ONE<\/i>, <b>11<\/b>, e0146398 (2016).","DOI":"10.1371\/journal.pone.0146398"},{"key":"43","doi-asserted-by":"crossref","unstructured":"43) Rakhade SN, Jensen FE. Epileptogenesis in the immature brain: emerging mechanisms. <i>Nat. Rev. Neurol.<\/i>, <b>5<\/b>, 380\u2013391 (2009).","DOI":"10.1038\/nrneurol.2009.80"},{"key":"44","doi-asserted-by":"crossref","unstructured":"44) Ben-Ari Y. Excitatory actions of gaba during development: the nature of the nurture. <i>Nat. Rev. Neurosci.<\/i>, <b>3<\/b>, 728\u2013739 (2002).","DOI":"10.1038\/nrn920"},{"key":"45","doi-asserted-by":"crossref","unstructured":"45) L\u00f6scher W, Klitgaard H, Twyman RE, Schmidt D. New avenues for anti-epileptic drug discovery and development. <i>Nat. Rev. Drug Discov.<\/i>, <b>12<\/b>, 757\u2013776 (2013).","DOI":"10.1038\/nrd4126"},{"key":"46","doi-asserted-by":"crossref","unstructured":"46) L\u00f6scher W, Puskarjov M, Kaila K. Cation\u2013chloride cotransporters NKCC1 and KCC2 as potential targets for novel antiepileptic and antiepileptogenic treatments. <i>Neuropharmacology<\/i>, <b>69<\/b>, 62\u201374 (2013).","DOI":"10.1016\/j.neuropharm.2012.05.045"},{"key":"47","doi-asserted-by":"crossref","unstructured":"47) Dzhala VI, Talos DM, Sdrulla DA, Brumback AC, Mathews GC, Benke TA, Delpire E, Jensen FE, Staley KJ. NKCC1 transporter facilitates seizures in the developing brain. <i>Nat. Med.<\/i>, <b>11<\/b>, 1205\u20131213 (2005).","DOI":"10.1038\/nm1301"},{"key":"48","doi-asserted-by":"crossref","unstructured":"48) Brandt C, Nozadze M, Heuchert N, Rattka M, Loscher W. Disease-modifying effects of phenobarbital and the NKCC1 inhibitor bumetanide in the pilocarpine model of temporal lobe epilepsy. <i>J. Neurosci.<\/i>, <b>30<\/b>, 8602\u20138612 (2010).","DOI":"10.1523\/JNEUROSCI.0633-10.2010"},{"key":"49","doi-asserted-by":"crossref","unstructured":"49) Eftekhari S, Mehvari Habibabadi J, Najafi Ziarani M, Hashemi Fesharaki SS, Gharakhani M, Mostafavi H, Joghataei MT, Beladimoghadam N, Rahimian E, Hadjighassem MR. Bumetanide reduces seizure frequency in patients with temporal lobe epilepsy. <i>Epilepsia<\/i>, <b>54<\/b>, e9\u2013e12 (2013).","DOI":"10.1111\/j.1528-1167.2012.03654.x"},{"key":"50","doi-asserted-by":"crossref","unstructured":"50) Ben-Ari Y, Tyzio R. Is it safe to use a diuretic to treat seizures early in development? <i>Epilepsy Curr.<\/i>, <b>11<\/b>, 192\u2013195 (2011).","DOI":"10.5698\/1535-7511-11.6.192"},{"key":"51","doi-asserted-by":"crossref","unstructured":"51) Sillanp\u00e4\u00e4 M, Schmidt D. Natural history of treated childhood-onset epilepsy: prospective, long-term population-based study. <i>Brain<\/i>, <b>129<\/b>, 617\u2013624 (2006).","DOI":"10.1093\/brain\/awh726"},{"key":"52","doi-asserted-by":"crossref","unstructured":"52) Brodie MJ, Barry SJ, Bamagous GA, Norrie JD, Kwan P. Patterns of treatment response in newly diagnosed epilepsy. <i>Neurology<\/i>, <b>78<\/b>, 1548\u20131554 (2012).","DOI":"10.1212\/WNL.0b013e3182563b19"},{"key":"53","doi-asserted-by":"crossref","unstructured":"53) Devinsky O, Vezzani A, Najjar S, De Lanerolle NC, Rogawski MA. Glia and epilepsy: excitability and inflammation. <i>Trends Neurosci.<\/i>, <b>36<\/b>, 174\u2013184 (2013).","DOI":"10.1016\/j.tins.2012.11.008"}],"container-title":["Biological &amp; Pharmaceutical Bulletin","Biological and Pharmaceutical Bulletin"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.jstage.jst.go.jp\/article\/bpb\/39\/6\/39_b16-00125\/_pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2019,9,9]],"date-time":"2019-09-09T02:48:54Z","timestamp":1567997334000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.jstage.jst.go.jp\/article\/bpb\/39\/6\/39_b16-00125\/_article"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016]]},"references-count":53,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2016]]}},"URL":"https:\/\/doi.org\/10.1248\/bpb.b16-00125","relation":{},"ISSN":["0918-6158","1347-5215"],"issn-type":[{"value":"0918-6158","type":"print"},{"value":"1347-5215","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016]]}}}