Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus
Open accessAbstract
Knowing the rate of addition of new granule cells to the adult dentate gyrus is critical to understanding the function of adult neurogenesis. Despite the large number of studies of neurogenesis in the adult dentate gyrus, basic questions about the magnitude of this phenomenon have never been addressed. The S-phase marker bromodeoxyuridine (BrdU) has been extensively used in recent studies of adult neurogenesis, but it has been carefully tested only in the embryonic brain. Here, we show that a high dose of BrdU (300 mg/kg) is a specific, quantitative, and nontoxic marker of dividing cells in the adult rat dentate gyrus, whereas lower doses label only a fraction of the S-phase cells. By using this high dose of BrdU along with a second S-phase marker, [(3)H]thymidine, we found that young adult rats have 9,400 dividing cells proliferating with a cell cycle time of 25 hours, which would generate 9,000 new cells each day, or more than 250,000 per month. Within 5-12 days of BrdU injection, a substantial pool of immature granule neurons, 50% of all BrdU-labeled cells in the dentate gyrus, could be identified with neuron-specific antibodies TuJ1 and TUC-4. This number of new granule neurons generated each month is 6% of the total size of the granule cell population and 30-60% of the size of the afferent and efferent populations (West et al. [1991] Anat Rec 231:482-497; Mulders et al. [1997] J Comp Neurol 385:83-94). The large number of the adult-generated granule cells supports the idea that these new neurons play an important role in hippocampal function.
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?
The dentate gyrus of the adult brain represents a key region for neurogenesis.
“As the DG of the adult brain represents a key region for neurogenesis,37”
From Microglia secrete miR-146a-5p-containing exosomes to regulate neurogenesis in depression (2022) · cites this paper as [37]
The proportion of cells labeled by the sensor approximately reflects physiological proportions.
“indicating the proportion of cells labeled by the sensor approximately reflects physiological proportions [21, 22].”
From MiR-338-3p regulates neuronal maturation and suppresses glioblastoma proliferation. (2017) · cites this paper as [21]
The dentate gyrus is mostly comprised of mature neurons (NeuN), with smaller populations of precursor cells (nestin) and newly differentiated neurons (DCX).
“These results indicate the dentate gyrus is mostly comprised of mature neurons (NeuN), along with a smaller population of precursor cells (nestin) and newly differentiated neurons (DCX), which corresponds to prior findings examining the relative number of each cell population in the dentate gyrus, indicating the proportion of cells labeled by the sensor approximately reflects physiological Proport”
From MiR-338-3p regulates neuronal maturation and suppresses glioblastoma proliferation. (2017) · cites this paper as [21]
In the adult rat, 9000 new neurons are born per day, and survive with a half-life of 28 days.
“In the adult rat, 9000 new neurons are born per day, and survive with a half -life of 28 days.64”
From Protective and damaging effects of stress mediators: central role of the brain (2006) · cites this paper as [64]
Cites
Neurogenesis in the adult human hippocampus
Eriksson, P. S., Perfilieva, E., Björk-Eriksson, T., Alborn, A.-M., Nordborg, C., Peterson, D. A., & Gage, F. H. (1998) · Nature Medicine · doi:10.1038/3305 · Cited by 6,369 · see citing works
West, M. J., Slomianka, L., & Gundersen, H. J. G. (1991) · The Anatomical Record · doi:10.1002/ar.1092310411 · Cited by 2,994 · see citing works
Running enhances neurogenesis, learning, and long-term potentiation in mice
van Praag, H., Christie, B. R., Sejnowski, T. J., & Gage, F. H. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.23.13427 · Cited by 2,904 · see citing works
Learning enhances adult neurogenesis in the hippocampal formation
Gould, E., Beylin, A., Tanapat, P., Reeves, A., & Shors, T. J. (1999) · Nature Neuroscience · doi:10.1038/6365 · Cited by 2,157 · 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
Self-citationExperience-Induced Neurogenesis in the Senescent Dentate Gyrus
Kempermann, G., Kuhn, H. G., & Gage, F. H. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-09-03206.1998 · Cited by 1,150 · see citing works
Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus
Cameron, H. A., & Gould, E. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90224-0 · Cited by 999 · see citing works
Self-citationTanapat, P., Hastings, N. B., Reeves, A. J., & Gould, E. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-14-05792.1999 · Cited by 978 · see citing works
New stereological methods for counting neurons
West, M. J. (1993) · Neurobiology of Aging · doi:10.1016/0197-4580(93)90112-o · Cited by 940 · see citing works
Hippocampal neurogenesis in adult Old World primates
Gould, E., Reeves, A. J., Fallah, M., Tanapat, P., Gross, C. G., & Fuchs, E. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.9.5263 · Cited by 815 · see citing works
The Concept of a Blood-Brain Barrier
(1980) · General Pharmacology The Vascular System · doi:10.1016/0306-3623(80)90073-7 · Cited by 805 · see citing works
Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures
Bengzon, J., Kokaia, Z., Elmér, E., Nanobashvili, A., Kokaia, M., & Lindvall, O. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.19.10432 · Cited by 782 · see citing works
Continuation of neurogenesis in the hippocampus of the adult macaque monkey
Kornack, D. R., & RAKIC, P. T. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.10.5768 · Cited by 779 · see citing works
Nowakowski, R. S., Lewin, S. B., & Miller, M. W. (1989) · Journal of Neurocytology · doi:10.1007/bf01190834 · Cited by 755 · see citing works
Cameron, H. A., McEwen, B., & Gould, E. A. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-06-04687.1995 · Cited by 743 · see citing works
Self-citationSchlessinger, A. R., Cowan, W. M., & Gottlieb, D. I. (1975) · The Journal of Comparative Neurology · doi:10.1002/cne.901590202 · Cited by 731 · see citing works
Restoring production of hippocampal neurons in old age
Cameron, H. A., & McKay, R. D. G. (1999) · Nature Neuroscience · doi:10.1038/13197 · Cited by 710 · see citing works
Self-citationThe cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall
Takahashi, T., Nowakowski, R. S., & Caviness, V. S. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-09-06046.1995 · Cited by 673 · see citing works
Miller, M. W., & Nowakowski, R. S. (1988) · Brain Research · doi:10.1016/0006-8993(88)90055-8 · Cited by 610 · see citing works
Opiates inhibit neurogenesis in the adult rat hippocampus
Eisch, A. J., Barrot, M., Schad, C. A., Self, D. W., & Nestler, E. J. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.120552597 · Cited by 599 · see citing works
Brezun, J. M., & Daszuta, A. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00693-9 · Cited by 549 · 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
Age-related production of new granule cells in the adult dentate gyrus
Seki, T., & Arai, Y. (1995) · Neuroreport · doi:10.1097/00001756-199512150-00010 · Cited by 386 · see citing works
Cameron, H. A., Tanapat, P., & Gould, E. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00303-5 · Cited by 381 · see citing works
Self-citationThe Concept of a Blood-Brain Barrier
Dunn, J. S. (1980) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.43.4.374-c · Cited by 380 · see citing works
Apoptosis and Its Relation to the Cell Cycle in the Developing Cerebral Cortex
Thomaidou, D., Mione, M., Cavanagh, J. F. R., & Parnavelas, J. G. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-03-01075.1997 · Cited by 362 · see citing works
Implications of the Blood-Brain Barrier and Its Manipulation
Neuwelt, E. A. (1989) · Springer eBooks · doi:10.1007/978-1-4613-0701-3 · Cited by 316 · see citing works
Late DNA Synthesis in Heterochromatin
Lima-de-Faria, A., & Jaworska, H. (1968) · Nature · doi:10.1038/217138a0 · Cited by 267 · see citing works
Takahashi, T., Nowakowski, R. S., & Caviness, V. S. (1992) · Journal of Neurocytology · doi:10.1007/bf01194977 · Cited by 237 · see citing works
Wray, S., & Hoffman, G. E. (1986) · The Journal of comparative neurology · doi:10.1002/cne.902520408 · Cited by 155 · see citing works
Packard, D. S., Menzies, R. A., & Skalko, R. G. (1973) · Differentiation · doi:10.1111/j.1432-0436.1973.tb00137.x · Cited by 154 · see citing works
Hayes, N. L., & Nowakowski, R. S. (2000) · Developmental Neuroscience · doi:10.1159/000017426 · Cited by 147 · see citing works
Discussion point stem cells and neurogenesis in the adult brain
Cameron, H. A., & McKay, R. D. G. (1998) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(98)80099-8 · Cited by 140 · see citing works
Self-citationKolb, B. E., Pedersen, B., Ballermann, M. A., Gibb, R. L., & Whishaw, I. Q. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-06-02337.1999 · Cited by 127 · see citing works
Popken, G. J., & Farel, P. B. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970915)386:1 · Cited by 117 · see citing works
Early postmitotic neurons transiently express TOAD‐64, a neural specific protein
Minturn, J. E., Geschwind, D. H., Fryer, H. J. L., & Hockfield, S. J. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903550304 · Cited by 114 · see citing works
Liu, Y. B., Lio, P., Pasternak, J. F., & Trommer, B. L. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.76.2.1074 · Cited by 104 · see citing works
Local Homogeneity of Cell Cycle Length in Developing Mouse Cortex
Cai, L., Hayes, N. L., & Nowakowski, R. S. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-06-02079.1997 · Cited by 87 · see citing works
Specificity and Sodium Dependence of the Active Nucleoside Transport System in Choroid Plexus
Spector, R., & Huntoon, S. (1984) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1984.tb12709.x · Cited by 64 · see citing works
Kaplan, M. (1983) · PubMed · Cited by 64 · see citing works
Effect of fluorodeoxyuridine, colcemid, and bromodeoxyuridine on developing neocortex of the mouse
Webster, W., Shimada, M., & Langman, J. (1973) · American Journal of Anatomy · doi:10.1002/aja.1001370106 · Cited by 62 · see citing works
Nucleoside transport in choroid plexus: Mechanism and specificity
Spector, R. (1982) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(82)90259-4 · Cited by 61 · see citing works
Cerebral blood flow and metabolism during exercise.
Ide, K., & Secher, N. (2000) · Progress in neurobiology · doi:10.1016/s0301-0082(99)00057-x · Cited by 60 · see citing works
Age-related changes of DNA repair and mitochondrial DNA synthesis in the mouse brain
Schmitz, C., Axmacher, B., Zunker, U., & Korr, H. (1999) · Acta Neuropathologica · doi:10.1007/s004010050957 · Cited by 60 · see citing works
The cellular effect of 5-bromodeoxyuridine on the mammalian embryo
Bannigan, J., & Langman, J. (1979) · Development · doi:10.1242/dev.50.1.123 · Cited by 58 · see citing works
Lowry, C. A., Richardson, C., Zoeller, T. R., Miller, L. J., Muske, L. E., & Moore, F. L. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970818)385:1 · Cited by 56 · see citing works
Okano, H. J., Pfaff, D. W., & Gibbs, R. B. (1996) · Developmental Neuroscience · doi:10.1159/000111408 · Cited by 53 · see citing works
Prasad, K. N., Mandal, B., & Kumar, S. (1973) · Experimental Biology and Medicine · doi:10.3181/00379727-144-37522 · Cited by 49 · see citing works
Localization and Mechanism of Thymidine Transport in the Central Nervous System
Spector, R., & Berlinger, W. G. (1982) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1982.tb07968.x · Cited by 48 · see citing works
Molecular analysis of developmental plasticity in neocortex
Nedivi, E. (1999) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(199910)41:1 · Cited by 47 · see citing works
Selden, J. R., Dolbeare, F. A., Clair, J. H., Nichols, W. W., Miller, J. E., Kleemeyer, K. M., Hyland, R. J., & DeLuca, J. G. (1993) · Cytometry · doi:10.1002/cyto.990140207 · Cited by 47 · see citing works
Pont, F., Collet, A., & Lallement, G. (1995) · Neuroscience Letters · doi:10.1016/0304-3940(94)11166-g · Cited by 46 · see citing works
Ontogeny and Phylogeny of the Blood-Brain Barrier
Johanson, C. E. (1989) · Springer eBooks · doi:10.1007/978-1-4613-0701-3_7 · Cited by 44 · see citing works
Postnatal neurogenesis in the cerebellum of the cat and tritiated thymidine autoradiography
Das, G. D., & Altman, J. (1971) · Brain Research · doi:10.1016/0006-8993(71)90082-5 · Cited by 40 · see citing works
Thomas, S. A., & Segal, M. B. (1996) · Brain Research · doi:10.1016/s0006-8993(96)00930-4 · Cited by 39 · see citing works
Unscheduled DNA synthesis in various types of cells of the mouse brain in vivo
Korr, H., & Schultze, B. L. (1989) · Experimental Brain Research · doi:10.1007/bf00247359 · Cited by 37 · see citing works
The effects of 5‐bromodeoxyuridine on fusion of the cranial neural folds in the mouse embryo
Bannigan, J. (1985) · Teratology · doi:10.1002/tera.1420320211 · Cited by 33 · see citing works
Validation of a flow cytometric in vitro DNA repair (UDS) assay in rat hepatocytes
Selden, J. R., Dolbeare, F. A., Clair, J. H., et al. (1994) · Mutation Research/DNA Repair · doi:10.1016/0921-8777(94)90015-9 · Cited by 33 · see citing works
Korr, H., Koeser, K., Oldenkott, S., et al. (1989) · Radiation and Environmental Biophysics · doi:10.1007/bf01209719 · Cited by 31 · see citing works
Thomas, S. A., & Segal, M. B. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00276-x · Cited by 30 · see citing works
Influence of Sex on the Blood Brain Barrier Permeability During Bicuculline-Induced Seizures
Öztaş, B., Ćmurcu, S., & Kaya, M. (1992) · International Journal of Neuroscience · doi:10.3109/00207459209003284 · Cited by 28 · see citing works
Morris, J. E. (1973) · Developmental Biology · doi:10.1016/0012-1606(73)90011-0 · Cited by 27 · see citing works
Nagao, T., Kuwagata, M., & Saito, Y. (1998) · Reproductive Toxicology · doi:10.1016/s0890-6238(98)00020-3 · Cited by 23 · see citing works
KINETICS OF CELL PROLIFERATION IN THE POSTNATAL RAT DENTATE GYRUS
LEWIS, P. D. (1978) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.1978.tb00536.x · Cited by 22 · see citing works
Defective transport of thymidine by cultured cells resistant to 5‐bromodeoxyuridine
Lynch, T. P., Cass, C. E., & Paterson, A. R. P. (1977) · Journal of Supramolecular Structure · doi:10.1002/jss.400060309 · Cited by 20 · see citing works
Gap junctional coupling between progenitor cells of regenerating retina in the adult newt
Chiba, C., & Saito, T. (2000) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(20000205)42:2 · Cited by 19 · see citing works
Delay of oligodendrocyte differentiation by 5-bromodeoxyuridine (BUdR)
Younkin, L. H., & Silberberg, D. H. (1976) · Brain Research · doi:10.1016/0006-8993(76)90485-6 · Cited by 16 · see citing works
Wang, S., Wang, H., Niemi-Junkola, U., Westby, G. W. M., McHaffie, J. G., Stein, B. E., & Redgrave, P. (2000) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20001002)425:4 · Cited by 11 · see citing works
Thomas, S., Davson, H., & Mb, S. (1997) · Experimental Physiology · doi:10.1113/expphysiol.1997.sp004003 · Cited by 9 · see citing works
Day, H. E. W., Curran, E. J., Watson, S. J., & Akil, H. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19991011)413:1
Flagged first, then by citations
Cited by
Sorted by citations
Physiology and neurobiology of stress and adaptation: central role of the brain
McEwen, B. S. (2007) · Physiological Reviews · doi:10.1152/physrev.00041.2006 · Cited by 4,981 · see citing works
McEwen, B. S. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.11.071 · Cited by 1,864 · see citing works
McEwen, B. S., & Gianaros, P. J. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.05331.x · Cited by 1,715 · see citing works
Inflammation is detrimental for neurogenesis in adult brain
Ekdahl, C. T., Claasen, J.-H., Bonde, S., Kokaia, Z., & Lindvall, O. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2234031100 · Cited by 1,559 · see citing works
Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus
Schmidt-Hieber, C., Jonas, P., & Bischofberger, J. (2004) · Nature · doi:10.1038/nature02553 · Cited by 1,292 · see citing works
Ziv, Y., Ron, N., Butovsky, O., Landa, G., Sudai, E., Greenberg, N., Cohen, H., Kipnis, J., & Schwartz, M. (2006) · Nature Neuroscience · doi:10.1038/nn1629 · Cited by 1,209 · see citing works
Protective and damaging effects of stress mediators: central role of the brain
McEwen, B. S. (2006) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2006.8.4/bmcewen · Cited by 1,220 · see citing works
Adult hippocampal neurogenesis and cognitive flexibility — linking memory and mood
Anacker, C., & Hen, R. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.45 · Cited by 1,014 · see citing works
Bridging animal and human models of exercise-induced brain plasticity
Voss, M. W., Vivar, C., Kramer, A. F., & van Praag, H. (2013) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2013.08.001 · Cited by 1,030 · see citing works
The stress system in the human brain in depression and neurodegeneration
Swaab, D. F., Bao, A.-M., & Lucassen, P. J. (2005) · Ageing Research Reviews · doi:10.1016/j.arr.2005.03.003 · Cited by 984 · see citing works
Adult neurogenesis: from precursors to network and physiology
Abrous, D. N., Koehl, M., & Le Moal, M. (2005) · Physiological Reviews · doi:10.1152/physrev.00055.2003 · Cited by 971 · see citing works
Kee, N., Teixeira, C. M., Wang, A. H., & Frankland, P. W. (2007) · Nature Neuroscience · doi:10.1038/nn1847 · Cited by 875 · see citing works
Mirescu, C., & Gould, E. (2006) · Hippocampus · doi:10.1002/hipo.20155 · Cited by 701 · 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
Hippocampal Neurogenesis: Regulation by Stress and Antidepressants
Dranovsky, A., & Hen, R. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.03.082 · Cited by 663 · see citing works
Taupin, P. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2006.08.002 · Cited by 645 · see citing works
Regulation and function of adult neurogenesis: from genes to cognition.
Aimone, J. B., Li, Y., Lee, S. W., Clemenson, G. D., Deng, W., & Gage, F. H. (2014) · Physiological Reviews · doi:10.1152/physrev.00004.2014 · Cited by 635 · see citing works
Early life experience alters response of adult neurogenesis to stress
Mirescu, C., Peters, J. D., & Gould, E. (2004) · Nature Neuroscience · doi:10.1038/nn1290 · Cited by 625 · see citing works
Stress and anxiety: Structural plasticity and epigenetic regulation as a consequence of stress
McEwen, B. S., Eiland, L., Hunter, R. G., & Miller, M. M. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.07.014 · Cited by 596 · see citing works
Moylan, S., Maes, M., Wray, N. R., & Berk, M. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.33 · Cited by 529 · see citing works
Jiang, W. (2005) · Journal of Clinical Investigation · doi:10.1172/jci25509 · Cited by 527 · see citing works
Gao, Y., Vasilyev, D. V., Goncalves, M. B., Howell, F. V., Hobbs, C., Reisenberg, M., Shen, R., Zhang, M.-Y., Strassle, B. W., Lu, P., et al. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5693-09.2010 · Cited by 473 · see citing works
Eadie, B. D., Redila, V. A., & Christie, B. R. (2005) · Journal of Comparative Neurology · doi:10.1002/cne.20493 · Cited by 466 · see citing works
Bramham, C. R., Alme, M. N., Bittins, M., Kuipers, S. D., Nair, R. R., Pai, B., Panja, D., Schubert, M., Soule, J., Tiron, A., et al. (2010) · Experimental Brain Research · doi:10.1007/s00221-009-1959-2 · Cited by 452 · see citing works
Regulation of adult neurogenesis by antidepressant treatment
Duman, R. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00358-x · Cited by 463 · see citing works
Adenosine receptors and brain diseases: neuroprotection and neurodegeneration
Gomes, C. V., Kaster, M. P., Tomé, A. R., Agostinho, P. M., & Cunha, R. A. (2011) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2010.12.001 · Cited by 419 · see citing works
High-speed imaging reveals neurophysiological links to behavior in an animal model of depression
Airan, R. D., Meltzer, L. A., Roy, M., Gong, Y., Chen, H., & Deisseroth, K. (2007) · Science · doi:10.1126/science.1144400 · Cited by 396 · see citing works
Kodama, M., Fujioka, T., & Duman, R. S. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.07.008 · Cited by 387 · see citing works
Chronic stress: Implications for neuronal morphology, function and neurogenesis
Joëls, M., Karst, H., Krugers, H. J., & Lucassen, P. J. (2007) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2007.04.001 · Cited by 381 · see citing works
Stimulation of neural regeneration in the mouse retina
Karl, M. O., Hayes, S., Nelson, B. R., Tan, K., Buckingham, B., & Reh, T. A. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807453105 · Cited by 368 · see citing works
Isgor, C., Kabbaj, M., Akil, H., & Watson, S. J. (2004) · Hippocampus · doi:10.1002/hipo.10207 · Cited by 341 · see citing works
New neurons in the adult brain: the role of sleep and consequences of sleep loss
Meerlo, P., Mistlberger, R. E., Jacobs, B. L., Craig Heller, H., & McGinty, D. (2009) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2008.07.004 · Cited by 318 · see citing works
Simon, C., Götz, M., & Dimou, L. (2011) · Glia · doi:10.1002/glia.21156 · Cited by 313 · see citing works
Vaynman, S., & Gomez‐Pinilla, F. (2006) · Journal of Neuroscience Research · doi:10.1002/jnr.20979 · Cited by 299 · see citing works
Noble, E. E., Billington, C. J., Kotz, C. M., & Wang, C. (2011) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00776.2010 · Cited by 284 · see citing works
McCormick, C. M., Mathews, I. Z., Thomas, C., & Waters, P. (2010) · Brain and Cognition · doi:10.1016/j.bandc.2009.06.003 · Cited by 276 · see citing works
Neurogenesis in adolescent brain is potently inhibited by ethanol
Crews, F. T., Mdzinarishvili, A., Kim, D., He, J., & Nixon, K. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.08.090 · Cited by 265 · see citing works
Bone marrow-derived cells that populate the adult mouse brain preserve their hematopoietic identity
Vallières, L., & Sawchenko, P. E. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-12-05197.2003 · Cited by 245 · see citing works
Rao, M. S., Hattiangady, B., & Shetty, A. K. (2006) · Aging Cell · doi:10.1111/j.1474-9726.2006.00243.x · Cited by 241 · see citing works
Adult neurogenesis, glia, and the extracellular matrix
Cope, E. C., & Gould, E. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2019.03.023 · Cited by 236 · see citing works
He, C., Qu, X., Cui, L., Wang, J., & Kang, J. X. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0904835106 · Cited by 233 · see citing works
Vollmayr, B., Simonis, C., Weber, S., Gass, P., & Henn, F. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00527-4 · Cited by 229 · see citing works
Zhou, Q., Hu, Y., Hua, Y., Hu, M., Luo, C., Han, X., Zhu, X., Wang, B., Xu, J., & Zhu, D. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04914.x · Cited by 225 · see citing works
Microglia secrete miR-146a-5p-containing exosomes to regulate neurogenesis in depression
Fan, C., Li, Y., Lan, T., Wang, W., Long, Y., & Yu, S. Y. (2022) · Molecular Therapy · doi:10.1016/j.ymthe.2021.11.006 · Cited by 227 · see citing works
Sleep restriction suppresses neurogenesis induced by hippocampus-dependent learning
Hairston, I. S., Little, M. T. M., Scanlon, M. D., Barakat, M. T., Palmer, T. D., Sapolsky, R. M., & Heller, H. C. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00218.2005 · Cited by 223 · see citing works
Implications of adult hippocampal neurogenesis in antidepressant action
Malberg, J. E. (2004) · Journal of Psychiatry and Neuroscience · doi:10.1139/jpn.0422 · Cited by 217 · see citing works
Reversal of hippocampal neuronal maturation by serotonergic antidepressants
Kobayashi, K., Ikeda, Y., Sakai, A., Yamasaki, N., Haneda, E., Miyakawa, T., & Suzuki, H. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0912690107 · Cited by 212 · see citing works
Sleep deprivation reduces proliferation of cells in the dentate gyrus of the hippocampus in rats
Guzmán‐Marín, R., Suntsova, N., Stewart, D. R., Gong, H., Szymusiak, R., & McGinty, D. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.041665 · Cited by 197 · see citing works
The role of serotonin in adult hippocampal neurogenesis
Alenina, N., & Klempin, F. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.07.038 · Cited by 195 · see citing works
Cellular and molecular mechanisms in the long-term action of antidepressants.
Racagni, G., & Popoli, M. (2008) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2008.10.4/gracagni · Cited by 192 · see citing works
Use it or lose it: how neurogenesis keeps the brain fit for learning
Shors, T. J., Anderson, M. L., Curlik, D. M., & Nokia, M. S. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.04.023 · Cited by 190 · see citing works
Speisman, R. B., Kumar, A., Rani, A., Foster, T. C., & Ormerod, B. K. (2013) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2012.09.013 · Cited by 187 · see citing works
Circumventricular organs: A novel site of neural stem cells in the adult brain
Bennett, L., Yang, M., Enikolopov, G., & Iacovitti, L. (2009) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2009.04.007 · Cited by 186 · see citing works
Neurogenesis decreases during brain maturation from adolescence to adulthood
He, J., & Crews, F. T. (2007) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.11.003 · Cited by 187 · see citing works
Dempsey, R. J., Sailor, K. A., Bowen, K. K., Türeyen, K., & Vemuganti, R. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.02022.x · Cited by 176 · see citing works
Increasing hippocampal neurogenesis: a novel mechanism for antidepressant drugs
Malberg, J., & Schechter, L. (2005) · Current Pharmaceutical Design · doi:10.2174/1381612053382223 · Cited by 167 · see citing works
A time to remember: The role of circadian clocks in learning and memory.
Smarr, B. L., Jennings, K. J., Driscoll, J. R., & Kriegsfeld, L. J. (2014) · Behavioral Neuroscience · doi:10.1037/a0035963 · Cited by 166 · see citing works
Differential effects of prenatal stress on the morphological maturation of hippocampal neurons
Fujioka, A., Fujioka, T., Ishida, Y., Maekawa, T., & Nakamura, S. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.04.046 · Cited by 165 · see citing works
Leuner, B., Glasper, E. R., & Gould, E. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.07.003 · Cited by 159 · see citing works
Jensen, C. B., Pyke, C., Rasch, M. G., Dahl, A. B., Knudsen, L. B., & Secher, A. (2018) · Endocrinology · doi:10.1210/en.2017-00812 · Cited by 145 · see citing works
Thymidine analogues for tracking DNA synthesis.
Cavanagh, B. L., Walker, T., Norazit, A., & Meedeniya, A. C. B. (2011) · Molecules · doi:10.3390/molecules16097980 · Cited by 143 · see citing works
Joggin’ the Noggin: Towards a Physiological Understanding of Exercise-Induced Cognitive Benefits
Stimpson, N. J., Davison, G., & Javadi, A.-H. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.03.018 · Cited by 134 · see citing works
Mandyam, C. D., Norris, R. D., & Eisch, A. J. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20090 · Cited by 116 · see citing works
The lullaby of the sun: The role of vitamin D in sleep disturbance
Muscogiuri, G., Barrea, L., Scannapieco, M., Di Somma, C., Scacchi, M., Aimaretti, G., Savastano, S., Colao, A., & Marzullo, P. (2019) · Sleep Medicine · doi:10.1016/j.sleep.2018.10.033 · Cited by 102 · see citing works
Aβ40 promotes neuronal cell fate in neural progenitor cells
Chen, Y., & Dong, C. (2009) · Cell Death & Differentiation · doi:10.1038/cdd.2008.94 · Cited by 94 · see citing works
Sleep restriction by forced activity reduces hippocampal cell proliferation
Roman, V., Van der Borght, K., Leemburg, S. A., Van der Zee, E. A., & Meerlo, P. (2005) · Brain Research · doi:10.1016/j.brainres.2005.10.020 · Cited by 93 · see citing works
Isgor, C., & Watson, S. J. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.05.008 · Cited by 87 · see citing works
‘One night’ sleep deprivation stimulates hippocampal neurogenesis
Grassi Zucconi, G., Cipriani, S., Balgkouranidou, I., & Scattoni, R. (2006) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2006.01.009 · Cited by 86 · see citing works
Yang, F., Liu, Z., Chen, J., Zhang, S., Quan, Q., Huang, Y., & Jiang, W. (2010) · Journal of Neuroscience Research · doi:10.1002/jnr.22224 · Cited by 80 · see citing works
Sun, D., Daniels, T. E., Rolfe, A., Waters, M., & Hamm, R. (2015) · Journal of Neurotrauma · doi:10.1089/neu.2014.3545 · Cited by 77 · see citing works
Whittemore, K., Derevyanko, A., Martinez, P., Serrano, R., Pumarola, M., Bosch, F., & Blasco, M. A. (2019) · Aging · doi:10.18632/aging.101982 · Cited by 69 · see citing works
Jayatissa, M. N., Henningsen, K., Nikolajsen, G., West, M. J., & Wiborg, O. (2010) · Stress · doi:10.3109/10253890902951786 · Cited by 69 · see citing works
Glasper, E. R., Kozorovitskiy, Y., Pavlic, A., & Gould, E. (2011) · Journal of Comparative Neurology · doi:10.1002/cne.22628 · Cited by 66 · see citing works
Xu, M.-X., Yu, R., Shao, L.-F., Zhang, Y.-X., Ge, C.-X., Liu, X.-M., Wu, W.-Y., Li, J.-M., & Kong, L.-D. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.01.001 · Cited by 61 · see citing works
Ambrogini, P., Lattanzi, D., Ciuffoli, S., Betti, M., Fanelli, M., & Cuppini, R. (2013) · Brain Research · doi:10.1016/j.brainres.2013.08.023 · Cited by 61 · see citing works
Overall, R. W., Walker, T. L., Fischer, T. J., Brandt, M. D., & Kempermann, G. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00362 · Cited by 48 · see citing works
White, E. R., Pinar, C., Bostrom, C. A., Meconi, A., & Christie, B. R. (2017) · Journal of Neurotrauma · doi:10.1089/neu.2016.4638 · Cited by 49 · see citing works
Wang, S.-H., Huang, Y., Yuan, Y., Xia, W.-Q., Wang, P., & Huang, R. (2014) · Lipids in Health and Disease · doi:10.1186/1476-511x-13-175 · Cited by 44 · see citing works
MiR-338-3p regulates neuronal maturation and suppresses glioblastoma proliferation.
Howe, J. R., Li, E. S., Streeter, S. E., Rahme, G. J., Chipumuro, E., Russo, G. B., Litzky, J. F., Hills, L. B., Rodgers, K. R., Skelton, P. D., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0177661 · Cited by 41 · see citing works
Weng, J.-C., Tikhonova, M. A., Chen, J.-H., Shen, M.-S., Meng, W.-Y., Chang, Y.-T., Chen, K.-H., Liang, K.-C., Hung, C.-S., Amstislavskaya, T. G., et al. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.02.034 · Cited by 39 · see citing works
Plasticity of 5‐HT<sub>1A</sub> receptor‐mediated signaling during early postnatal brain development
Mehta, M., Ahmed, Z., Fernando, S. S., Cano‐Sanchez, P., Adayev, T., Ziemnicka, D., Wieraszko, A., & Banerjee, P. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04448.x · Cited by 30 · see citing works
Hippocampal miR-211-5p regulates neurogenesis and depression-like behaviors in the rat
Li, Y., Fan, C., Gao, R., Lan, T., Wang, W., & Yu, S. Y. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108618 · Cited by 29 · see citing works
Li, A., Yau, S.-Y., Machado, S., Wang, P., Yuan, T.-F., & So, K.-F. (2019) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527318666190308102804 · Cited by 27 · see citing works
Neuronal plasticity and antidepressants in the diabetic brain
Beauquis, J., Roig, P., De Nicola, A. F., & Saravia, F. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2008.03983.x · Cited by 16 · see citing works
- Authors
- Cameron, H. A., & Mckay, R. D. G.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Cameron, Heather A.
- ORCID
- Cameron, Heather A.
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 2001-06-08
- Volume
- 435
- Issue
- 4
- Pages
- 406-417
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W2139481908
- Cited by
- 1,585
- References
- 71
- Citations by year
- 2026: 10 · 2025: 16 · 2024: 19 · 2023: 27 · 2022: 28 · 2021: 37 · 2020: 44 · 2019: 59 · 2018: 42 · 2017: 58 · 2016: 77 · 2015: 70 · 2014: 81 · 2013: 74 · 2012: 86
- FWCI
- 13.50
- Type
- journal article
- Language
- en
- Open access
- green
- zenodo.org
- Licence
- public-domain
- onlinelibrary.wiley.com/termsAndConditions#vor (vor)
- Locations
- The Journal of Comparative Neurology (publishedVersion, public-domain)
- PubMed (publishedVersion)
- Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, public-domain)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- adult neurogenesis, dentate gyrus, granule cells, bromodeoxyuridine, cell proliferation, cell cycle duration, thymidine, hippocampus, hippocampal function
- MeSH terms
- Animals, Antimetabolites, Bromodeoxyuridine, Cell Cycle, Cell Survival, Male, Tissue Fixation, Dentate Gyrus, 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
