Abraham H, Richter Z, Gyimesi C, Horvath Z, Janszky J, Doczi T, Seress L (2011) Degree and pattern of calbindin immunoreactivity in granule cells of the dentate gyrus differ in mesial temporal sclerosis, cortical malformation- and tumor-related epilepsies. Brain Res 1399:66–78. https://doi.org/10.1016/j.brainres.2011.05.010
Article
PubMed
CAS
Google Scholar
Abraham H, Veszpremi B, Kravjak A, Kovacs K, Gomori E, Seress L (2009) Ontogeny of calbindin immunoreactivity in the human hippocampal formation with a special emphasis on granule cells of the dentate gyrus. Int J Dev Neurosci 27:115–127. https://doi.org/10.1016/j.ijdevneu.2008.12.004
Article
PubMed
CAS
Google Scholar
Alcantara D, Timms AE, Gripp K, Baker L, Park K, Collins S, Cheng C, Stewart F, Mehta SG, Saggar A, Sztriha L, Zombor M, Caluseriu O, Mesterman R, Van Allen MI, Jacquinet A, Ygberg S, Bernstein JA, Wenger AM, Guturu H, Bejerano G, Gomez-Ospina N, Lehman A, Alfei E, Pantaleoni C, Conti V, Guerrini R, Moog U, Graham JM Jr, Hevner R, Dobyns WB, O'Driscoll M, Mirzaa GM (2017) Mutations of AKT3 are associated with a wide spectrum of developmental disorders including extreme megalencephaly. Brain 140:2610–2622. https://doi.org/10.1093/brain/awx203
Article
PubMed
PubMed Central
Google Scholar
Amaral DG, Scharfman HE, Lavenex P (2007) The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res 163:3–22. https://doi.org/10.1016/S0079-6123(07)63001-5
Article
PubMed
PubMed Central
Google Scholar
Armstrong DD (1993) The neuropathology of temporal lobe epilepsy. J Neuropathol Exp Neurol 52:433–443
Article
CAS
PubMed
Google Scholar
Bae EK, Jung KH, Chu K, Lee ST, Kim JH, Park KI, Kim M, Chung CK, Lee SK, Roh JK (2010) Neuropathologic and clinical features of human medial temporal lobe epilepsy. J Clin Neurol 6:73–80. https://doi.org/10.3988/jcn.2010.6.2.73
Article
PubMed
PubMed Central
Google Scholar
Bayer SA, Altman J (1974) Hippocampal development in the rat: cytogenesis and morphogenesis examined with autoradiography and low-level X-irradiation. J Comp Neurol 158:55–79. https://doi.org/10.1002/cne.901580105
Article
PubMed
CAS
Google Scholar
Blumcke I, Kistner I, Clusmann H, Schramm J, Becker AJ, Elger CE, Bien CG, Merschhemke M, Meencke HJ, Lehmann T, Buchfelder M, Weigel D, Buslei R, Stefan H, Pauli E, Hildebrandt M (2009) Towards a clinico-pathological classification of granule cell dispersion in human mesial temporal lobe epilepsies. Acta Neuropathol 117:535–544. https://doi.org/10.1007/s00401-009-0512-5
Article
PubMed
Google Scholar
Blumcke I, Pauli E, Clusmann H, Schramm J, Becker A, Elger C, Merschhemke M, Meencke HJ, Lehmann T, von Deimling A, Scheiwe C, Zentner J, Volk B, Romstock J, Stefan H, Hildebrandt M (2007) A new clinico-pathological classification system for mesial temporal sclerosis. Acta Neuropathol 113:235–244. https://doi.org/10.1007/s00401-006-0187-0
Article
PubMed
PubMed Central
Google Scholar
Caboclo LO, Neves RS, Jardim AP, Hamad AP, Centeno RS, Lancellotti CL, Scorza CA, Cavalheiro EA, Yacubian EM, Sakamoto AC (2012) Surgical and postmortem pathology studies: contribution for the investigation of temporal lobe epilepsy. Arq Neuropsiquiatr 70:945–952. https://doi.org/10.1590/s0004-282x2012001200009
Article
PubMed
Google Scholar
Chai X, Munzner G, Zhao S, Tinnes S, Kowalski J, Haussler U, Young C, Haas CA, Frotscher M (2014) Epilepsy-induced motility of differentiated neurons. Cereb Cortex 24:2130–2140. https://doi.org/10.1093/cercor/bht067
Article
PubMed
Google Scholar
Cipriani S, Journiac N, Nardelli J, Verney C, Delezoide AL, Guimiot F, Gressens P, Adle-Biassette H (2017) Dynamic expression patterns of progenitor and neuron layer markers in the developing human dentate Gyrus and fimbria. Cereb Cortex 27:358–372. https://doi.org/10.1093/cercor/bhv223
Article
PubMed
Google Scholar
D'Arcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, Curran T (1995) A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374:719–723. https://doi.org/10.1038/374719a0
Article
PubMed
CAS
Google Scholar
Davies KG, Hermann BP, Dohan FC Jr, Foley KT, Bush AJ, Wyler AR (1996) Relationship of hippocampal sclerosis to duration and age of onset of epilepsy, and childhood febrile seizures in temporal lobectomy patients. Epilepsy Res 24:119–126. https://doi.org/10.1016/0920-1211(96)00008-3
Article
PubMed
CAS
Google Scholar
de Lanerolle NC, Lee TS, Spencer DD. Histopathology of Human Epilepsy. In: Noebels JL, Avoli M, Rogawski MA, et al., editors. Jasper's Basic Mechanisms of the Epilepsies [Internet]. 4th edition. Bethesda (MD): National Center for Biotechnology Information (US); 2012. Available from: https://www.ncbi.nlm.nih.gov/books/NBK98141/
Duveau V, Madhusudan A, Caleo M, Knuesel I, Fritschy JM (2011) Impaired reelin processing and secretion by Cajal-Retzius cells contributes to granule cell dispersion in a mouse model of temporal lobe epilepsy. Hippocampus 21:935–944. https://doi.org/10.1002/hipo.20793
Article
PubMed
CAS
Google Scholar
El Bahh B, Lespinet V, Lurton D, Coussemacq M, Le Gal La Salle G, Rougier A (1999) Correlations between granule cell dispersion, mossy fiber sprouting, and hippocampal cell loss in temporal lobe epilepsy. Epilepsia 40:1393–1401. https://doi.org/10.1111/j.1528-1157.1999.tb02011.x
Article
PubMed
Google Scholar
Eng LF, Ghirnikar RS (1994) GFAP and astrogliosis. Brain Pathol 4:229–237. https://doi.org/10.1111/j.1750-3639.1994.tb00838.x
Article
PubMed
CAS
Google Scholar
Etzerodt A, Moestrup SK (2013) CD163 and inflammation: biological, diagnostic, and therapeutic aspects. Antioxid Redox Signal 18:2352–2363. https://doi.org/10.1089/ars.2012.4834
Article
PubMed
PubMed Central
CAS
Google Scholar
Fahrner A, Kann G, Flubacher A, Heinrich C, Freiman TM, Zentner J, Frotscher M, Haas CA (2007) Granule cell dispersion is not accompanied by enhanced neurogenesis in temporal lobe epilepsy patients. Exp Neurol 203:320–332. https://doi.org/10.1016/j.expneurol.2006.08.023
Article
PubMed
Google Scholar
Freiman TM, Eismann-Schweimler J, Frotscher M (2011) Granule cell dispersion in temporal lobe epilepsy is associated with changes in dendritic orientation and spine distribution. Exp Neurol 229:332–338. https://doi.org/10.1016/j.expneurol.2011.02.017
Article
PubMed
Google Scholar
Frotscher M, Haas CA, Forster E (2003) Reelin controls granule cell migration in the dentate gyrus by acting on the radial glial scaffold. Cereb Cortex 13:634–640. https://doi.org/10.1093/cercor/13.6.634
Article
PubMed
Google Scholar
Girgis F, Pace J, Sweet J, Miller JP (2016) Hippocampal neurophysiologic changes after mild traumatic brain injury and potential Neuromodulation treatment approaches. Front Syst Neurosci 10:8. https://doi.org/10.3389/fnsys.2016.00008
Article
PubMed
PubMed Central
CAS
Google Scholar
Haas CA, Dudeck O, Kirsch M, Huszka C, Kann G, Pollak S, Zentner J, Frotscher M (2002) Role for reelin in the development of granule cell dispersion in temporal lobe epilepsy. J Neurosci 22:5797–5802 Doi:20026621
Article
CAS
PubMed
PubMed Central
Google Scholar
Harding B, Thom M (2001) Bilateral hippocampal granule cell dispersion: autopsy study of 3 infants. Neuropathol Appl Neurobiol 27:245–251
Article
CAS
PubMed
Google Scholar
Hefti MM, Cryan JB, Haas EA, Chadwick AE, Crandall LA, Trachtenberg FL, Armstrong DD, Grafe M, Krous HF, Kinney HC (2016) Hippocampal malformation associated with sudden death in early childhood: a neuropathologic study: part 2 of the investigations of the San Diego SUDC research project. Forensic Sci Med Pathol 12:14–25. https://doi.org/10.1007/s12024-015-9731-3
Article
PubMed
Google Scholar
Heinrich C, Nitta N, Flubacher A, Muller M, Fahrner A, Kirsch M, Freiman T, Suzuki F, Depaulis A, Frotscher M, Haas CA (2006) Reelin deficiency and displacement of mature neurons, but not neurogenesis, underlie the formation of granule cell dispersion in the epileptic hippocampus. J Neurosci 26:4701–4713. https://doi.org/10.1523/JNEUROSCI.5516-05.2006
Article
PubMed
PubMed Central
CAS
Google Scholar
Hendrickx DAE, van Eden CG, Schuurman KG, Hamann J, Huitinga I (2017) Staining of HLA-DR, Iba1 and CD68 in human microglia reveals partially overlapping expression depending on cellular morphology and pathology. J Neuroimmunol 309:12–22. https://doi.org/10.1016/j.jneuroim.2017.04.007
Article
PubMed
CAS
Google Scholar
Hossmann KA (1999) The hypoxic brain. Insights from ischemia research. Adv Exp Med Biol 474:155–169
Article
CAS
PubMed
Google Scholar
Houser CR (1990) Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. Brain Res 535:195–204
Article
CAS
PubMed
Google Scholar
Kinney HC, Cryan JB, Haynes RL, Paterson DS, Haas EA, Mena OJ, Minter M, Journey KW, Trachtenberg FL, Goldstein RD, Armstrong DD (2015) Dentate gyrus abnormalities in sudden unexplained death in infants: morphological marker of underlying brain vulnerability. Acta Neuropathol 129:65–80. https://doi.org/10.1007/s00401-014-1357-0
Article
PubMed
CAS
Google Scholar
Kinney HC, Hefti MM, Goldstein RD, Haynes RL (2018) Sudden infant death syndrome. In developmental neuropathology. In: Adle-Biassette H, Harding BN, Golden J (eds) Developmental neuropathology. https://doi.org/10.1002/9781119013112.ch25
Chapter
Google Scholar
Koyama R, Tao K, Sasaki T, Ichikawa J, Miyamoto D, Muramatsu R, Matsuki N, Ikegaya Y (2012) GABAergic excitation after febrile seizures induces ectopic granule cells and adult epilepsy. Nat Med 18:1271–1278. https://doi.org/10.1038/nm.2850
Article
PubMed
CAS
Google Scholar
Lavado A, Oliver G (2007) Prox1 expression patterns in the developing and adult murine brain. Dev Dynamics 236:518–524. https://doi.org/10.1002/dvdy.21024
Article
CAS
Google Scholar
Lurton D, Sundstrom L, Brana C, Bloch B, Rougier A (1997) Possible mechanisms inducing granule cell dispersion in humans with temporal lobe epilepsy. Epilepsy Res 26:351–361. https://doi.org/10.1016/s0920-1211(96)01002-9
Article
PubMed
CAS
Google Scholar
Marucci G, Rubboli G, Giulioni M (2010) Role of dentate gyrus alterations in mesial temporal sclerosis. Clin Neuropathol 29:32–35. https://doi.org/10.5414/npp29032
Article
PubMed
CAS
Google Scholar
Mathern GW, Kuhlman PA, Mendoza D, Pretorius JK (1997) Human fascia dentata anatomy and hippocampal neuron densities differ depending on the epileptic syndrome and age at first seizure. J Neuropathol Exp Neurol 56:199–212. https://doi.org/10.1097/00005072-199702000-00011
Article
PubMed
CAS
Google Scholar
Matsue K, Minakawa S, Kashiwagi T, Toda K, Sato T, Shioda S, Seki T (2018) Dentate granule progenitor cell properties are rapidly altered soon after birth. Brain Struct Funct 223:357–369. https://doi.org/10.1007/s00429-017-1499-7
Article
PubMed
CAS
Google Scholar
McGuone D, Leitner D, William C, Faustin A, Leelatian N, Reichard R, Shepherd TM, Snuderl M, Crandall L, Wisniewski T, Devinsky O (2020) Neuropathologic changes in sudden unexplained death in childhood. J Neuropathol Exp Neurol. https://doi.org/10.1093/jnen/nlz136
Mello LE, Cavalheiro EA, Tan AM, Pretorius JK, Babb TL, Finch DM (1992) Granule cell dispersion in relation to mossy fiber sprouting, hippocampal cell loss, silent period and seizure frequency in the pilocarpine model of epilepsy. Epilepsy Res Suppl 9:51–59 discussion 59-60
PubMed
CAS
Google Scholar
Muller MC, Osswald M, Tinnes S, Haussler U, Jacobi A, Forster E, Frotscher M, Haas CA (2009) Exogenous reelin prevents granule cell dispersion in experimental epilepsy. Exp Neurol 216:390–397. https://doi.org/10.1016/j.expneurol.2008.12.029
Article
PubMed
CAS
Google Scholar
Orcinha C, Munzner G, Gerlach J, Kilias A, Follo M, Egert U, Haas CA (2016) Seizure-induced motility of differentiated dentate granule cells is prevented by the central Reelin fragment. Front Cell Neurosci 10:183. https://doi.org/10.3389/fncel.2016.00183
Article
PubMed
PubMed Central
CAS
Google Scholar
Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH (1997) Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17:3727–3738
Article
CAS
PubMed
PubMed Central
Google Scholar
Prayson RA, Cohen ML (2000) Practical differential diagnosis in surgical neuropathology, 1st edn. Humana Press. https://doi.org/10.1007/978-1-59259-037-7
Rakic P, Nowakowski RS (1981) The time of origin of neurons in the hippocampal region of the rhesus monkey. J Comp Neurol 196:99–128. https://doi.org/10.1002/cne.901960109
Article
PubMed
CAS
Google Scholar
Riviere JB, Mirzaa GM, O'Roak BJ, Beddaoui M, Alcantara D, Conway RL, St-Onge J, Schwartzentruber JA, Gripp KW, Nikkel SM, Worthylake T, Sullivan CT, Ward TR, Butler HE, Kramer NA, Albrecht B, Armour CM, Armstrong L, Caluseriu O, Cytrynbaum C, Drolet BA, Innes AM, Lauzon JL, Lin AE, Mancini GM, Meschino WS, Reggin JD, Saggar AK, Lerman-Sagie T, Uyanik G, Weksberg R, Zirn B, Beaulieu CL, Majewski J, Bulman DE, O'Driscoll M, Shendure J, Graham JM Jr, Boycott KM, Dobyns WB (2012) De novo germline and postzygotic mutations in AKT3, PIK3R2 and PIK3CA cause a spectrum of related megalencephaly syndromes. Nat Genet 44:934–940. https://doi.org/10.1038/ng.2331
Article
PubMed
PubMed Central
CAS
Google Scholar
Roy A, Murphy RM, Deng M, MacDonald JW, Bammler TK, Aldinger KA, Glass IA, Millen KJ (2019) PI3K-yap activity drives cortical gyrification and hydrocephalus in mice. eLife 8:e45961. https://doi.org/10.7554/eLife.45961
Article
PubMed
PubMed Central
Google Scholar
Roy A, Skibo J, Kalume F, Ni J, Rankin S, Lu Y, Dobyns WB, Mills GB, Zhao JJ, Baker SJ, Millen KJ (2015) Mouse models of human PIK3CA-related brain overgrowth have acutely treatable epilepsy. eLife 4:e12703. https://doi.org/10.7554/eLife.12703
Article
PubMed
PubMed Central
Google Scholar
Seress L (1992) Morphological variability and developmental aspects of monkey and human granule cells: differences between the rodent and primate dentate gyrus. Epilepsy Res Suppl 7:3–28
PubMed
CAS
Google Scholar
Seress L, Abraham H, Tornoczky T, Kosztolanyi G (2001) Cell formation in the human hippocampal formation from mid-gestation to the late postnatal period. Neuroscience 105:831–843. https://doi.org/10.1016/s0306-4522(01)00156-7
Article
PubMed
CAS
Google Scholar
Seress L, Mrzljak L (1987) Basal dendrites of granule cells are normal features of the fetal and adult dentate gyrus of both monkey and human hippocampal formations. Brain Res 405:169–174. https://doi.org/10.1016/0006-8993(87)91003-1
Article
PubMed
CAS
Google Scholar
Somani A, Zborovschi AB, Liu Y, Patodia S, Michalak Z, Sisodiya SM, Thom M (2019) Hippocampal morphometry in sudden and unexpected death in epilepsy. Neurology 93:e804–e814. https://doi.org/10.1212/WNL.0000000000007969
Article
PubMed
CAS
PubMed Central
Google Scholar
Sorrells SF, Paredes MF, Cebrian-Silla A, Sandoval K, Qi D, Kelley KW, James D, Mayer S, Chang J, Auguste KI, Chang EF, Gutierrez AJ, Kriegstein AR, Mathern GW, Oldham MC, Huang EJ, Garcia-Verdugo JM, Yang Z, Alvarez-Buylla A (2018) Human hippocampal neurogenesis drops sharply in children to undetectable levels in adults. Nature 555:377–381. https://doi.org/10.1038/nature25975
Article
PubMed
PubMed Central
CAS
Google Scholar
Thom M (2014) Review: hippocampal sclerosis in epilepsy: a neuropathology review. Neuropathol Appl Neurobiol 40:520–543. https://doi.org/10.1111/nan.12150
Article
PubMed
PubMed Central
Google Scholar
Thom M, Martinian L, Williams G, Stoeber K, Sisodiya SM (2005) Cell proliferation and granule cell dispersion in human hippocampal sclerosis. J Neuropathol Exp Neurol 64:194–201. https://doi.org/10.1093/jnen/64.3.194
Article
PubMed
Google Scholar
Thom M, Sisodiya SM, Beckett A, Martinian L, Lin WR, Harkness W, Mitchell TN, Craig J, Duncan J, Scaravilli F (2002) Cytoarchitectural abnormalities in hippocampal sclerosis. J Neuropathol Exp Neurol 61:510–519. https://doi.org/10.1093/jnen/61.6.510
Article
PubMed
Google Scholar
Turtzo LC, Lescher J, Janes L, Dean DD, Budde MD, Frank JA (2014) Macrophagic and microglial responses after focal traumatic brain injury in the female rat. J Neuroinflammation 11:82. https://doi.org/10.1186/1742-2094-11-82
Article
PubMed
PubMed Central
CAS
Google Scholar
Weiss KH, Johanssen C, Tielsch A, Herz J, Deller T, Frotscher M, Forster E (2003) Malformation of the radial glial scaffold in the dentate gyrus of reeler mice, scrambler mice, and ApoER2/VLDLR-deficient mice. J Comp Neurol 460:56–65. https://doi.org/10.1002/cne.10644
Article
PubMed
CAS
Google Scholar
Wieser HG, Epilepsy ICoNo (2004) ILAE commission report. Mesial temporal lobe epilepsy with hippocampal sclerosis. Epilepsia 45:695–714. https://doi.org/10.1111/j.0013-9580.2004.09004.x
Article
PubMed
Google Scholar
Yamawaki R, Thind K, Buckmaster PS (2015) Blockade of excitatory synaptogenesis with proximal dendrites of dentate granule cells following rapamycin treatment in a mouse model of temporal lobe epilepsy. J Comp Neurol 523:281–297. https://doi.org/10.1002/cne.23681
Article
PubMed
CAS
Google Scholar
Yu DX, Marchetto MC, Gage FH (2014) How to make a hippocampal dentate gyrus granule neuron. Development 141:2366–2375. https://doi.org/10.1242/dev.096776
Article
PubMed
CAS
Google Scholar
Zhao S, Chai X, Forster E, Frotscher M (2004) Reelin is a positional signal for the lamination of dentate granule cells. Development 131:5117–5125. https://doi.org/10.1242/dev.01387
Article
PubMed
CAS
Google Scholar