Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods
Abstract
Methacrylate‐embedded sections and short‐survival thymidine radiograms of the hippocampal dentate gyrus were examined in perinatal and postnatal rats in order to trace the site of origin and migration of the precursors of granule cells and study the morphogenesis of the granular layer. The densely packed, spindle‐shaped cells of the secondary dentate matrix (a derivative of the primary dentate neuroepithelium) stream in a subpial position towards the granular layer of the internal dentate limb during the perinatal and early postnatal periods. By an accretionary process, the crest of the granular layer forms on day E21 and on the subsequent days the granular layer of the internal dentate limb expands progressively in a lateral direction. Granule cells differentiation, as judged by the transformation of polymorph, darkly staining small cells into rounder, lightly staining larger granule cells, follows the same gradient from the external dentate limb to the internal dentate limb. The secondary dentate matrix is in a process of dissolution by day P5. This matrix is the source of what will later become the outer shell of the granular layer composed of early generated granule cells. The thicker inner shell of the granular layer, formed during the infantile and juvenile periods, derives from an intrinsic, tertiary germinal matrix. On day E22, the dentate migration of the secondary dentate matrix becomes partitioned into two components: (a) the subpial component of extradentate origin, referred to in this context as the first dentate migration, and (b) the second dentate migration. The latter is distributed in the basal polymorph layer throughout the entire dentate gyrus and is henceforth recognized as the tertiary dentate matrix. The tertiary dentate matrix is prominent between days P3 and P10. It is postulated that the great increase in granule cell population during the infantile period is principally due to cells derived from this intrinsic matrix of the dentate gyrus. Between days P20 and P30 the tertiary dentate matrix disappears in the basal polymorph layer and henceforth proliferative cells become largely confined to the subgranular zone at the base of the granular layer. The subgranular zone is the source of granule cells produced during the juvenile and adult periods.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Reduction in PTB triggered radial glial-like cells to convert into new granular neurons through what appears to be the typical developmental process by which new hippocampal neurons mature during development and in young adult animals.
“reduction in PTB triggered radial glial-like cells to convert into new granular neurons through what appears to be the typical developmental process by which new hippocampal neurons mature during development39 and in young adult animals40.”
From Therapeutically viable generation of neurons with antisense oligonucleotide suppression of PTB (2021) · cites this paper as [39]
Cites
Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats
Altman, J., & Das, G. D. (1965) · Journal of Comparative Neurology · doi:10.1002/cne.901240303 · Cited by 3,592 · see citing works
Self-citationBayer, S. A. (1980) · The Journal of Comparative Neurology · doi:10.1002/cne.901900107 · Cited by 913 · see citing works
Self-citationAutoradiographic investigation of cell proliferation in the brains of rats and cats
Altman, J. (1963) · The Anatomical Record · doi:10.1002/ar.1091450409 · Cited by 623 · see citing works
Self-citationTime of neuron origin in the hippocampal region. An autoradiographic study in the mouse.
Angevine, J. B. (1965) · PubMed · Cited by 476 · see citing works
Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections
Stanfield, B. B., & Trice, J. (1988) · Experimental Brain Research · doi:10.1007/bf00250261 · Cited by 431 · see citing works
Altman, J., & Bayer, S. A. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.903010302 · Cited by 401 · see citing works
Self-citationBayer, S. A. (1982) · Experimental Brain Research · doi:10.1007/bf00238626 · Cited by 285 · see citing works
Self-citationEckenhoff, M. F., & RAKIC, P. T. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902230102 · Cited by 239 · see citing works
Altman, J., & Bayer, S. A. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.903010303 · Cited by 198 · see citing works
Self-citationOn the number of neurons in the dentate gyrus of the rat
Boss, B. D., Peterson, G. M., & Cowan, W. M. (1985) · Brain Research · doi:10.1016/0006-8993(85)90257-4 · Cited by 178 · see citing works
Postnatal Development of the Hippocampal Dentate Gyrus Under Normal and Experimental Conditions
Altman, J., & Bayer, S. A. (1975) · Springer eBooks · doi:10.1007/978-1-4684-2976-3_5 · Cited by 163 · see citing works
Self-citationSubgranular Zone of the Dentate Gyrus of Young Rabbits As a Secondary Matrix
Guéneau, G., Privat, A., Drouet, J.-B., & Court, L. (2007) · Developmental Neuroscience · doi:10.1159/000112694 · Cited by 108 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Kuhn, H., Dickinson-Anson, H., & Gage, F. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-06-02027.1996 · Cited by 3,139 · see citing works
A hot/cool-system analysis of delay of gratification: dynamics of willpower
Metcalfe, J., & Mischel, W. (1999) · Psychological Review · doi:10.1037/0033-295x.106.1.3 · Cited by 2,931 · see citing works
Gould, E., McEwen, B. S., Tanapat, P., Galea, L. A. M., & Fuchs, E. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-07-02492.1997 · Cited by 1,496 · see citing works
Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat
Cameron, H. A., Woolley, C. S., McEwen, B. S., & Gould, E. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90335-d · Cited by 1,215 · see citing works
Blümcke, I., Thom, M., Aronica, E., Armstrong, D. D., Bartoloméi, F., Bernasconi, A., Bernasconi, N., Bien, C. G., Cendes, F., Coras, R., et al. (2013) · Epilepsia · doi:10.1111/epi.12220 · Cited by 1,010 · see citing works
Nakashiba, T., Cushman, J. D., Pelkey, K. A., Renaudineau, S., Buhl, D. L., McHugh, T. J., Barrera, V. R., Chittajallu, R., Iwamoto, K. S., McBain, C. J., et al. (2012) · Cell · doi:10.1016/j.cell.2012.01.046 · Cited by 805 · see citing works
Stress and hippocampal neurogenesis
Gould, E., & Tanapat, P. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00247-4 · Cited by 805 · see citing works
Neuronal differentiation in the adult hippocampus recapitulates embryonic development
Espósito, M. S., Piatti, V. C., Laplagne, D. A., Morgenstern, N. A., Ferrari, C. C., Pitossi, F. J., & Schinder, A. F. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3114-05.2005 · Cited by 679 · see citing works
Potential role for adult neurogenesis in the encoding of time in new memories
Aimone, J. B., Wiles, J., & Gage, F. H. (2006) · Nature Neuroscience · doi:10.1038/nn1707 · Cited by 644 · see citing works
Beck, K. D., Powell-Braxtont, L., Widmer, H.-R., Valverde, J., & Hefti, F. (1995) · Neuron · doi:10.1016/0896-6273(95)90216-3 · Cited by 636 · see citing works
TrkB Regulates Hippocampal Neurogenesis and Governs Sensitivity to Antidepressive Treatment
Li, Y., Luikart, B. W., Birnbaum, S., Chen, J., Kwon, C.-H., Kernie, S. G., Bassel-Duby, R., & Parada, L. F. (2008) · Neuron · doi:10.1016/j.neuron.2008.06.023 · Cited by 634 · see citing works
Neal, C. R., Mansour, A., Reinscheid, R. K., Nothacker, H., Civelli, O., & Watson, S. J. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990419)406:4 · Cited by 399 · see citing works
Modulation of the Hypothalamic-Pituitary-Adrenal Axis by Early Life Stress Exposure
van Bodegom, M., Homberg, J. R., & Henckens, M. J. A. G. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00087 · Cited by 562 · see citing works
Fricker, R. A., Carpenter, M. K., Winkler, C., Greco, C., Gates, M. A., & Björklund, A. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-14-05990.1999 · Cited by 561 · see citing works
Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells
Han, Y.-G., Spassky, N., Romaguera-Ros, M., Garcia-Verdugo, J.-M., Aguilar, A., Schneider-Maunoury, S., & Alvarez-Buylla, A. (2008) · Nature Neuroscience · doi:10.1038/nn2059 · Cited by 547 · see citing works
De novo generation of neuronal cells from the adult mouse brain.
Richards, L. J., Kilpatrick, T. J., & Bartlett, P. F. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.18.8591 · Cited by 544 · see citing works
Gritti, A., Frolichsthal, P., Galli, R., Parati, E. A., Cova, L., Pagano, S., Bjornson, C. R. R., & Vescovi, A. L. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-09-03287.1999 · Cited by 523 · see citing works
Hochgerner, H., Zeisel, A., Lönnerberg, P., & Linnarsson, S. (2018) · Nature Neuroscience · doi:10.1038/s41593-017-0056-2 · Cited by 482 · see citing works
Renfranz, P. J., Cunningham, M. G., & McKay, R. D. G. (1991) · Cell · doi:10.1016/0092-8674(91)90116-g · Cited by 472 · see citing works
Seki, T., & Arai, Y. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-06-02351.1993 · Cited by 461 · see citing works
DiFranza, J. R. (2002) · Tobacco Control · doi:10.1136/tc.11.3.228 · Cited by 445 · see citing works
Neurogenesis in adulthood: a possible role in learning
Gould, E. (1999) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(99)01310-8 · Cited by 430 · see citing works
Stress, stress hormones, and adult neurogenesis
Schoenfeld, T. J., & Gould, E. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.01.008 · Cited by 425 · see citing works
Abnormal development of the hippocampal dentate gyrus in mice lacking the CXCR4 chemokine receptor
Lü, M., Grove, E. A., & Miller, R. J. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.092013799 · Cited by 415 · see citing works
Altman, J., & Bayer, S. A. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.903010302 · Cited by 401 · see citing works
Self-citationHippocampus development and generation of dentate gyrus granule cells is regulated by LEF1
Galcerán, J., Miyashita-Lin, E. M., Devaney, E. J., Rubenstein, J. L. R., & Grosschedl, R. (2000) · Development · doi:10.1242/dev.127.3.469 · Cited by 399 · see citing works
Seki, T., & Arai, Y. (1993) · Neuroscience Research · doi:10.1016/0168-0102(93)90111-3 · Cited by 397 · see citing works
The chemokine SDF1 regulates migration of dentate granule cells
Bagri, A., Gurney, T. A., He, X., Zou, Y.-R., Littman, D. R., Tessier‐Lavigne, M., & Pleasure, S. J. (2002) · Development · doi:10.1242/dev.129.18.4249 · Cited by 387 · see citing works
Wagner, J. P., Black, I. B., & DiCicco-Bloom, E. M. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-14-06006.1999 · Cited by 373 · see citing works
Ammon's Horn Sclerosis: A Maldevelopmental Disorder Associated with Temporal Lobe Epilepsy
Blümcke, I., Thom, M., & Wiestler, O. D. (2002) · Brain Pathology · doi:10.1111/j.1750-3639.2002.tb00436.x · Cited by 375 · see citing works
Oomen, C. A., Soeters, H., Audureau, N., Vermunt, L., van Hasselt, F. N., Manders, E. M. M., Joëls, M., Lucassen, P. J., & Krugers, H. J. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0247-10.2010 · Cited by 352 · see citing works
Functional Convergence of Neurons Generated in the Developing and Adult Hippocampus
Laplagne, D. A., Esposito, M. S., Piatti, V. C., Morgenstern, N. A., Zhao, C., van Praag, H., Gage, F. H., & Schinder, A. F. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040409 · Cited by 359 · see citing works
Stratmann, G., Sall, J. W., May, L. D. V., Bell, J. S., Magnusson, K. R., Rau, V., Visrodia, K., Alvi, R. S., Ku, B., Lee, M. T., et al. (2009) · Anesthesiology · doi:10.1097/aln.0b013e31819c463d · Cited by 356 · see citing works
Niculescu, M. D., Craciunescu, C. N., & Zeisel, S. H. (2006) · The FASEB Journal · doi:10.1096/fj.05-4707com · Cited by 330 · see citing works
The T-box transcription factor Eomes/Tbr2 regulates neurogenesis in the cortical subventricular zonePreprint
Arnold, S. J., Huang, G., Cheung, A. F. P., Era, T., Nishikawa, S. I., Bikoff, E. K., Molnár, Z., Robertson, E. J., & Groszer, M. (2008) · Genes & Development · doi:10.1101/gad.475408 · Cited by 325 · see citing works
Serotonin and Hippocampal Neurogenesis
Gould, E. (1999) · Neuropsychopharmacology · doi:10.1016/s0893-133x(99)00045-7 · Cited by 328 · see citing works
Heine, V. M., Maslam, S., Joëls, M., & Lucassen, P. J. (2004) · Neurobiology of Aging · doi:10.1016/s0197-4580(03)00090-3 · Cited by 318 · see citing works
Arvidsson, A., Kokaia, Z., & Lindvall, O. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01611.x · Cited by 311 · see citing works
Vaynman, S., & Gomez‐Pinilla, F. (2006) · Journal of Neuroscience Research · doi:10.1002/jnr.20979 · Cited by 299 · see citing works
Chemokine receptors: signposts to brain development and disease
Tran, P. B., & Miller, R. J. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1116 · Cited by 295 · see citing works
Stress & sleep: A relationship lasting a lifetime
Martire, V. L., Caruso, D., Palagini, L., Zoccoli, G., & Bastianini, S. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.08.024 · Cited by 296 · see citing works
Naninck, E. F. G., Hoeijmakers, L., Kakava-Georgiadou, N., Meesters, A., Lazic, S. E., Lucassen, P. J., & Kőrösi, A. (2014) · Hippocampus · doi:10.1002/hipo.22374 · Cited by 281 · see citing works
Nicotine and the adolescent brain: insights from an animal model
Slotkin, T. (2002) · Neurotoxicology and Teratology · doi:10.1016/s0892-0362(02)00199-x · Cited by 284 · see citing works
FGF-2 Is Sufficient to Isolate Progenitors Found in the Adult Mammalian Spinal Cord
Shihabuddin, L. S., Ray, J., & Gage, F. H. (1997) · Experimental Neurology · doi:10.1006/exnr.1997.6697 · Cited by 283 · see citing works
Loss of BETA2/NeuroD leads to malformation of the dentate gyrus and epilepsy
Liu, M., Pleasure, S. J., Collins, A. E., Noebels, J. L., Naya, F. J., Tsai, M., & Lowenstein, D. H. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.2.865 · Cited by 282 · see citing works
Zhu, C., Gao, J., Karlsson, N., Li, Q., Zhang, Y., Huang, Z., Li, H., Kuhn, H. G., & Blomgren, K. (2010) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2009.274 · Cited by 283 · see citing works
Contestabile, A., Fila, T., Ceccarelli, C., Bonasoni, P., Bonapace, L., Santini, D., Bartesaghi, R., & Ciani, E. (2007) · Hippocampus · doi:10.1002/hipo.20308 · Cited by 281 · see citing works
Exosomes regulate neurogenesis and circuit assembly
Sharma, P., Mesci, P., Carromeu, C., Mcclatchy, D., Schiapparelli, L., Yates, J., Muotri, A., & Cline, H. (2019) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1902513116 · Cited by 257 · see citing works
Schwab, M. H., Bartholomä, A., Heimrich, B., Feldmeyer, D., Druffel‐Augustin, S., Goebbels, S., Naya, F. J., Zhao, S., Frotscher, M., Tsai, M., et al. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-10-03714.2000 · Cited by 258 · see citing works
Stress effects in the hippocampus: Synaptic plasticity and memory
Kim, J. J., Song, E. Y., Kim, J. J., Song, E. Y., & Kosten, T. A. (2006) · Stress · doi:10.1080/10253890600678004 · Cited by 255 · see citing works
Perinatal Iron Deficiency Alters the Neurochemical Profile of the Developing Rat Hippocampus
Rao, R., Tkáč, I., Townsend, E. L., Rolf Gruetter, A., & Georgieff, M. (2003) · Journal of Nutrition · doi:10.1093/jn/133.10.3215 · Cited by 252 · see citing works
Blockade of NMDA receptors increases cell death and birth in the developing rat dentate gyrus
Gould, E., Cameron, H. A., & McEwen, B. S. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903400408 · Cited by 244 · see citing works
Förster, E., Zhao, S., & Frotscher, M. (2006) · Nature reviews. Neuroscience · doi:10.1038/nrn1882 · Cited by 242 · see citing works
Dentate gyrus formation requires Emx2
Pellegrini, M., Mansouri, A., Simeone, A., Boncinelli, E., & Gruss, P. (1996) · Development · doi:10.1242/dev.122.12.3893 · Cited by 242 · see citing works
MRI of normal fetal brain development
Prayer, D., Kasprian, G., Krampl, E., Ulm, B., Witzani, L., Prayer, L., & Brugger, P. C. (2006) · European Journal of Radiology · doi:10.1016/j.ejrad.2005.11.020 · Cited by 240 · see citing works
Redila, V. A., & Christie, B. R. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.10.050 · Cited by 235 · see citing works
Reduced Neurogenesis after Neonatal Seizures
McCabe, B. K., Silveira, D. C., Cilio, M. R., Cha, B. H., Liu, X., Sogawa, Y., & Holmes, G. L. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-06-02094.2001 · Cited by 234 · see citing works
Pleasure, S. J., Collins, A. E., & Lowenstein, D. H. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06095.2000 · Cited by 231 · see citing works
Trauth, J. A., Seidler, F. J., McCook, E. C., & Slotkin, T. A. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01994-0 · Cited by 230 · see citing works
Postnatal growth and morphological development of the brain: a species comparison
Watson, R. E., DeSesso, J. M., Hurtt, M. E., & Cappon, G. D. (2006) · Birth Defects Research Part B Developmental and Reproductive Toxicology · doi:10.1002/bdrb.20090 · Cited by 229 · see citing works
Comparative Milestones in Rodent and Human Postnatal Central Nervous System Development
Zeiss, C. J. (2021) · Toxicologic Pathology · doi:10.1177/01926233211046933 · Cited by 231 · see citing works
Cellular targets and trophic functions of neurotrophin-3 in the developing rat hippocampus
Collazo, D., Takahashi, H., & McKay, R. D. G. (1992) · Neuron · doi:10.1016/0896-6273(92)90028-c · Cited by 224 · see citing works
Ambrogini, P., Lattanzi, D., Ciuffoli, S., Agostini, D., Bertini, L., Stocchi, V., Santi, S., & Cuppini, R. (2004) · Brain Research · doi:10.1016/j.brainres.2004.05.039 · Cited by 222 · see citing works
Chen, V. S., Morrison, J. P., Southwell, M. F., Foley, J. F., Bolon, B. N., & Elmore, S. A. (2017) · Toxicologic Pathology · doi:10.1177/0192623317728134 · Cited by 213 · see citing works
In vivo neurogenesis in the adult brain: regulation and functional implications
Fuchs, E., & Gould, E. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00130.x · Cited by 215 · see citing works
Maternal Dietary (n-3) Fatty Acid Deficiency Alters Neurogenesis in the Embryonic Rat Brain
Bertrand, P. C., OʼKusky, J. R., & Innis, S. M. (2006) · Journal of Nutrition · doi:10.1093/jn/136.6.1570 · Cited by 214 · see citing works
Common and distinct fusion proteins in axonal growth and transmitter release
Osen‐Sand, A., Staple, J. K., Naldi, E., Schiavo, G., Rossetto, O., Petitpierre, S., Malgaroli, A., Montecucco, C., & Catsicas, S. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960401)367:2 · Cited by 206 · see citing works
Garcia, A. D. R., Steiner, B., Kronenberg, G., Bick‐Sander, A., & Kempermann, G. (2004) · Aging Cell · doi:10.1111/j.1474-9728.2004.00130.x · Cited by 209 · see citing works
Maternal care influences neuronal survival in the hippocampus of the rat
Bredy, T. W., Grant, R. J., Champagne, D. L., & Meaney, M. J. (2003) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2003.02965.x · Cited by 208 · see citing works
Sexual dimorphism in the mammalian limbic system
Madeira, M. D., & Lieberman, A. R. (1995) · Progress in Neurobiology · doi:10.1016/0301-0082(94)00052-j · Cited by 202 · see citing works
Alcántara, S., Frisén, J., del Rı́o, J. A., Soriano, E., Barbacid, M., & Silos‐Santiago, I. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-10-03623.1997 · Cited by 202 · see citing works
Broekman, M. L. D., Comer, L. A., Hyman, B. T., & Sena‐Esteves, M. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.11.057 · Cited by 201 · see citing works
Temprana, S. G., Mongiat, L. A., Yang, S. M., Trinchero, M. F., Alvarez, D. D., Kropff, E., Giacomini, D., Beltramone, N., Lanuza, G. M., & Schinder, A. F. (2014) · Neuron · doi:10.1016/j.neuron.2014.11.023 · Cited by 200 · see citing works
Altman, J., & Bayer, S. A. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.903010303 · Cited by 198 · see citing works
Self-citationCilia in the nervous system: linking cilia function and neurodevelopmental disorders
Lee, J. E., & Gleeson, J. G. (2011) · Current Opinion in Neurology · doi:10.1097/wco.0b013e3283444d05 · Cited by 185 · see citing works
Coras, R., Pauli, E., Li, J., Schwarz, M., Rössler, K., Buchfelder, M., Hamer, H. M., Stefan, H., & Blümcke, I. (2014) · Brain · doi:10.1093/brain/awu100 · Cited by 195 · see citing works
Early-life stress mediated modulation of adult neurogenesis and behavior
Korosi, A., Naninck, E. F. G., Oomen, C. A., Schouten, M., Krugers, H., Fitzsimons, C., & Lucassen, P. J. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.07.037 · Cited by 194 · see citing works
Gil‐Mohapel, J., Ehret, F., Kainer, L., & Christie, B. R. (2010) · Brain Research Reviews · doi:10.1016/j.brainresrev.2010.04.011 · Cited by 194 · see citing works
Roles of Sox4 in central nervous system development
Cheung, M. C. H., Abu-Elmagd, M. M., Clevers, H. C., & Scotting, P. J. (2000) · Molecular Brain Research · doi:10.1016/s0169-328x(00)00109-1 · Cited by 193 · see citing works
Opposite effects of early maternal deprivation on neurogenesis in male versus female rats
Oomen, C. A., Girardi, C. E. N., Cahyadi, R., Verbeek, E. C., Krugers, H., Joëls, M., & Lucassen, P. J. (2009) · PLoS ONE · doi:10.1371/journal.pone.0003675 · Cited by 190 · see citing works
Blümcke, I., Coras, R., Miyata, H., & Özkara, Ç. (2012) · Brain Pathology · doi:10.1111/j.1750-3639.2012.00583.x · Cited by 190 · see citing works
Sex differences in microglial phagocytosis in the neonatal hippocampus
Nelson, L. H., Warden, S., & Lenz, K. M. (2017) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2017.03.010 · Cited by 189 · see citing works
Molecular neuropathology of human mesial temporal lobe epilepsy
Blümcke, I., Beck, H., Lie, A. A., & Wiestler, O. D. (1999) · Epilepsy Research · doi:10.1016/s0920-1211(99)00052-2 · Cited by 188 · see citing works
Blümcke, I., Schewe, J., Normann, S., Brüstle, O., Schramm, J., Elger, C. E., & Wiestler, O. D. (2001) · Hippocampus · doi:10.1002/hipo.1045 · Cited by 187 · see citing works
Danzer, S. C., Crooks, K., Lo, D. C., & McNamara, J. O. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-22-09754.2002 · Cited by 183 · see citing works
Evolution of the hippocampus in reptiles and birds
Striedter, G. (2016) · The Journal of comparative neurology · doi:10.1002/cne.23803 · Cited by 161 · see citing works
Roy, T. S., Seidler, F. J., & Slotkin, T. A. (2002) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.300.1.124 · Cited by 183 · see citing works
Posttraining Ablation of Adult-Generated Neurons Degrades Previously Acquired Memories
Arruda-Carvalho, M., Sakaguchi, M., Akers, K. G., Josselyn, S. A., & Frankland, P. W. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3432-11.2011 · Cited by 176 · see citing works
Lucassen, P. J., Naninck, E. F. G., van Goudoever, J. B., Fitzsimons, C. P., Joëls, M., & Kőrösi, A. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.08.002 · Cited by 173 · see citing works
Bender, R. A., Dubé, C. M., Gonzalez‐Vega, R., Mina, E. W., & Baram, T. Z. (2003) · Hippocampus · doi:10.1002/hipo.10089 · Cited by 173 · see citing works
Uncoupling Dendrite Growth and Patterning: Single-Cell Knockout Analysis of NMDA Receptor 2B
Espinosa, J. S., Wheeler, D. G., Tsien, R. W., & Luo, L. (2009) · Neuron · doi:10.1016/j.neuron.2009.03.006 · Cited by 171 · see citing works
Disruption of hippocampal development <i>in vivo</i> by CR-50 mAb against Reelin
Nakajima, K., Mikoshiba, K., Miyata, T., Kudo, C., & Ogawa, M. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.15.8196 · Cited by 171 · see citing works
The Ventral Hippocampus Is the Embryonic Origin for Adult Neural Stem Cells in the Dentate Gyrus
Li, G., Fang, L., Fernández, G., & Pleasure, S. J. (2013) · Neuron · doi:10.1016/j.neuron.2013.03.019 · Cited by 171 · see citing works
Soumier, A., Banasr, M., Lortet, S., Masmejean, F., Bernard, N., Goff, L. K., Gabriel, C., Millan, M. J., Mocaër, E., & Daszuta, A. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.72 · Cited by 169 · see citing works
Cipriani, S., Ferrer, I., Aronica, E., Kovacs, G. G., Verney, C., Nardelli, J., Khung, S., Delezoide, A.-L., Milenkovic, I., Rasika, S., et al. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy096 · Cited by 169 · see citing works
Hulshof, H. J., Novati, A., Sgoifo, A., Luiten, P. G. M., den Boer, J. A., & Meerlo, P. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.08.038 · Cited by 169 · see citing works
Stone, S. S. D., Teixeira, C. M., Zaslavsky, K., Wheeler, A. L., Martínez-Canabal, A., Wang, A. H., Sakaguchi, M., Lozano, A. M., & Frankland, P. W. (2010) · Hippocampus · doi:10.1002/hipo.20845 · Cited by 167 · see citing works
Kuhn, H. G., Biebl, M., Wilhelm, D., Li, M., Friedlander, R. M., & Winkler, J. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04377.x · Cited by 168 · see citing works
The development of hippocampal interneurons in rodents
Danglot, L., Triller, A., & Marty, S. (2006) · Hippocampus · doi:10.1002/hipo.20225 · Cited by 167 · see citing works
Enomoto, A., Asai, N., Namba, T., Wang, Y., Kato, T., Tanaka, M., Tatsumi, H., Taya, S., Tsuboi, D., Kuroda, K., et al. (2009) · Neuron · doi:10.1016/j.neuron.2009.08.015 · Cited by 167 · see citing works
- Authors
- Altman, J., & Bayer, S. A.
- Affiliations
- Purdue University West Lafayette (US)
- Indiana University – Purdue University Indianapolis (US)
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 1990-11-15
- Volume
- 301
- Issue
- 3
- Pages
- 365-381
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W2006624547
- Cited by
- 819
- References
- 12
- Citations by year
- 2026: 8 · 2025: 11 · 2024: 9 · 2023: 9 · 2022: 18 · 2021: 17 · 2020: 24 · 2019: 29 · 2018: 28 · 2017: 37 · 2016: 33 · 2015: 35 · 2014: 31 · 2013: 35 · 2012: 39
- FWCI
- 3.40
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- hippocampal granule cells, granule cell precursors, dentate gyrus, subgranular zone, perinatal development, postnatal development, cell migration, granule cell differentiation
- MeSH terms
- Aging, Animals, Autoradiography, Cell Differentiation, Cell Division, Cell Movement, Gestational Age, Hippocampus, Morphogenesis, Rats, Inbred Strains, Thymidine, Tritium, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review