Seizures accelerate functional integration of adult-generated granule cells
Open accessAbstract
In humans and experimental animals, structural and functional changes in neural circuits can accompany the development of epilepsy. In the dentate gyrus, seizures enhance adult neurogenesis, but it is unclear to what extent newborn granule cells participate in seizure-induced synaptic reorganization. During the first weeks of their existence, mouse newborn granule cells labeled with enhanced green fluorescent protein have only short dendrites that lack excitatory input. We report that pilocarpine-induced seizures accelerated the morphological development of labeled granule cells, causing their dendrites to extend through the molecular layer. In whole-cell recordings 5-16 d after seizure induction, perforant-path stimulation now evoked glutamatergic input to newborn granule cells. These synaptic responses were mediated by monosynaptic as well as recurrent polysynaptic input. Thus, seizures facilitated functional integration of adult-generated granule cells. One month later, subsequent generations of newborn cells also showed alterations in dendrite morphology, suggesting persistent effects of seizures on granule cell maturation. The sensitivity of newborn granule cells to seizures could contribute to hyperexcitability during the latent period.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Seizures induce faster maturation of new granule neurons including early and more extensive mossy fiber sprouting and dendritic outgrowth as well as aberrant basal dendritic trees extending into the hilus.
“In fact, seizures induce faster maturation of new granule neurons including early and more extensive mossy fiber sprouting and dendritic outgrowth as well as aberrant basal dendritic trees extending into the hilus, which receive recurrent excitatory drive from mossy fibers (Overstreet-Wadiche et al., 2006; Shapiro and Ribak, 2006) (Table 1).”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Overstreet-Wadiche et al., 2006
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Shrestha, S., & Offer, S. M. (2016) · Medical Epigenetics · doi:10.1159/000444713 · Cited by 8,949 · see citing works
Functional neurogenesis in the adult hippocampus
van Praag, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D., & Gage, F. H. (2002) · Nature · doi:10.1038/4151030a · Cited by 2,853 · see citing works
Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus
Cowley, M. A., Smart, J. L., Rubinstein, M., Cerdán, M. G., Diano, S., Horvath, T. L., Cone, R. D., & Low, M. J. (2001) · Nature · doi:10.1038/35078085 · Cited by 2,356 · see citing works
Parent, J. M., Yu, T. W., Leibowitz, R. T., Geschwind, D. H., Sloviter, R. S., & Lowenstein, D. H. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-10-03727.1997 · Cited by 1,853 · see citing works
ADULT NEUROGENESIS IN THE MAMMALIAN CENTRAL NERVOUS SYSTEM
Ming, G., & Song, H. (2005) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.28.051804.101459 · Cited by 1,829 · see citing works
Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images
Meijering, E. H. W., Jacob, M., Sarria, J. ‐. F., Steiner, P., Hirling, H., & Unser, M. A. (2004) · Cytometry Part A · doi:10.1002/cyto.a.20022 · Cited by 1,611 · 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
GABA regulates synaptic integration of newly generated neurons in the adult brain
Ge, S., Goh, E. L. K., Sailor, K. A., Kitabatake, Y., Ming, G., & Song, H. (2005) · Nature · doi:10.1038/nature04404 · Cited by 1,261 · see citing works
Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats
Tauck, D., & Nadler, J. V. (1985) · Journal of Neuroscience · doi:10.1523/jneurosci.05-04-01016.1985 · Cited by 1,087 · see citing works
Tovar, K. R., & Westbrook, G. L. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-10-04180.1999 · Cited by 786 · see citing works
Self-citationGABAergic Excitation Promotes Neuronal Differentiation in Adult Hippocampal Progenitor Cells
Tozuka, Y., Fukuda, S., Namba, T., Seki, T., & Hisatsune, T. (2005) · Neuron · doi:10.1016/j.neuron.2005.08.023 · Cited by 741 · see citing works
Activity-Dependent Decrease in NMDA Receptor Responses During Development of the Visual Cortex
Carmignoto, G., & Vicini, S. (1992) · Science · doi:10.1126/science.1279803 · Cited by 716 · see citing works
Isackson, P. J., Huntsman, M. M., Murray, K. D., & Gall, C. M. (1991) · Neuron · doi:10.1016/0896-6273(91)90234-q · Cited by 711 · 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
Excitation-Neurogenesis Coupling in Adult Neural Stem/Progenitor Cells
Deisseroth, K., Singla, S., Toda, H., Monje, M., Palmer, T. D., & Malenka, R. C. (2004) · Neuron · doi:10.1016/s0896-6273(04)00266-1 · Cited by 674 · see citing works
Ernfors, P., Bengzon, J., Kokaia, Z., Persson, H., & Lindvall, O. (1991) · Neuron · doi:10.1016/0896-6273(91)90084-d · Cited by 628 · see citing works
Turski, L., Ikonomidou, C., Turski, W. A., Bortolotto, Z. A., & Cavalheiro, É. A. (1989) · Synapse · doi:10.1002/syn.890030207 · Cited by 626 · see citing works
Scharfman, H. E., Goodman, J. H., & Sollas, A. L. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-16-06144.2000 · Cited by 605 · see citing works
Acquired Dendritic Channelopathy in Temporal Lobe Epilepsy
Bernard, C., Anderson, A. E., Becker, A. J., Poolos, N. P., Beck, H., & Johnston, D. (2004) · Science · doi:10.1126/science.1097065 · Cited by 450 · see citing works
Reduced Inhibition of Dentate Granule Cells in a Model of Temporal Lobe Epilepsy
Kobayashi, M., & Buckmaster, P. S. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-06-02440.2003 · Cited by 391 · see citing works
Multiple facets of GABAergic neurons and synapses: multiple fates of GABA signalling in epilepsies
Cossart, R., Bernard, C., & Ben‐Ari, Y. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.11.011 · Cited by 340 · see citing works
Adult‐born hippocampal neurons mature into activity‐dependent responsiveness
Jessberger, S., & Kempermann, G. (2003) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2003.02986.x · Cited by 330 · see citing works
Buckmaster, P. S., Zhang, G. F., & Yamawaki, R. M. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-15-06650.2002 · Cited by 311 · see citing works
Conditional Deletion of TrkB but Not BDNF Prevents Epileptogenesis in the Kindling Model
He, X.-P., Kotloski, R. J., Nef, S., Luikart, B. W., Parada, L. F., & McNamara, J. O. (2004) · Neuron · doi:10.1016/j.neuron.2004.06.019 · Cited by 304 · see citing works
Hattiangady, B., Rao, M. S. R., & Shetty, A. K. (2004) · Neurobiology of Disease · doi:10.1016/j.nbd.2004.08.008 · Cited by 303 · see citing works
Parent, J. M., Tada, E., Fike, J. R., & Lowenstein, D. H. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-11-04508.1999 · Cited by 287 · see citing works
GABAergic Signaling to Newborn Neurons in Dentate Gyrus
Overstreet‐Wadiche, L., Bromberg, D. A., Bensen, A. L., & Westbrook, G. L. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00633.2005 · Cited by 270 · see citing works
Self-citationThe Recurrent Mossy Fiber Pathway of the Epileptic Brain
Nadler, J. V. (2003) · Neurochemical Research · doi:10.1023/a:1026004904199 · Cited by 241 · see citing works
Impaired and repaired inhibitory circuits in the epileptic human hippocampus
Maglóczky, Z., & Freund, T. F. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.04.002 · Cited by 217 · see citing works
A Transgenic Marker for Newly Born Granule Cells in Dentate Gyrus
Overstreet‐Wadiche, L., Hentges, S. T., Bumaschny, V. F., de Souza, F. S. J., Smart, J. L., Santangelo, A. M., Low, M. J., Westbrook, G. L., & Rubinstein, M. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5173-03.2004 · Cited by 205 · see citing works
Self-citationShibley, H., & Smith, B. N. (2002) · Epilepsy Research · doi:10.1016/s0920-1211(02)00012-8 · Cited by 201 · see citing works
Seizure-induced neurogenesis: are more new neurons good for an adult brain?
Parent, J. M., & Lowenstein, D. H. (2002) · Progress in brain research · doi:10.1016/s0079-6123(02)35012-x · Cited by 183 · 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
Delayed Development of Adult-Generated Granule Cells in Dentate Gyrus
Overstreet‐Wadiche, L., Bensen, A. L., & Westbrook, G. L. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4111-05.2006 · Cited by 179 · see citing works
Self-citationJung, K., Chu, K., Kim, M., Jeong, S., Song, Y., Lee, S., Kim, J. Y., Lee, S. K., & Roh, J. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2004.03412.x · Cited by 171 · see citing works
A subpopulation of precursor cells in the mouse dentate gyrus receives synaptic GABAergic input
Wang, L.-P., Kempermann, G., & Kettenmann, H. (2005) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2005.02.002 · Cited by 170 · see citing works
Sayın, Ü., Osting, S., Hagen, J., Rutecki, P. A., & Sutula, T. P. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-07-02759.2003 · Cited by 166 · see citing works
Scharfman, H. E., Sollas, A. L., Berger, R. E., & Goodman, J. H. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00251.2003 · Cited by 160 · see citing works
Elliott, R. C., Miles, M. F., & Lowenstein, D. H. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-06-02218.2003 · Cited by 144 · see citing works
Mossy cells in epilepsy: rigor mortis or vigor mortis?
Ratzliff, A., Santhakumar, V., Howard, A. L., & Soltész, I. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)02122-6 · Cited by 144 · see citing works
Tongiorgi, E., Armellin, M., Giulianini, P. G., Bregola, G., Zucchini, S., Paradiso, B., Steward, O., Cattaneo, A., & Simonato, M. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5471-03.2004 · Cited by 143 · see citing works
Functional maturation of adult‐generated granule cells
Overstreet‐Wadiche, L., & Westbrook, G. L. (2006) · Hippocampus · doi:10.1002/hipo.20152 · Cited by 132 · see citing works
Self-citationOkazaki, M. M., Molnár, P., & Nadler, J. V. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.81.4.1645 · Cited by 132 · see citing works
Mohapel, P., Ekdahl, C. T., & Lindvall, O. (2004) · Neurobiology of Disease · doi:10.1016/j.nbd.2003.11.010 · Cited by 129 · see citing works
Morphological changes in the dentate gyrus in human temporal lobe epilepsy.
Houser, C. R. (1992) · PubMed · Cited by 116 · see citing works
Harvey, B. D., & Sloviter, R. S. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20594 · Cited by 110 · see citing works
Shapiro, L. A., & Ribak, C. E. (2004) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.08.003 · Cited by 100 · see citing works
Functional Implications of Seizure-Induced Neurogenesis
Scharfman, H. E. (2004) · Advances in experimental medicine and biology · doi:10.1007/978-1-4757-6376-8_14 · Cited by 100 · see citing works
Shapiro, L. A., Korn, M. J., & Ribak, C. E. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.03.059 · Cited by 92 · see citing works
New Neurons in the Adult Mammalian Brain: Synaptogenesis and Functional Integration
Song, H., Kempermann, G., Overstreet‐Wadiche, L., Zhao, C., Schinder, A. F., & Bischofberger, J. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3452-05.2005 · Cited by 91 · see citing works
Self-citationZappone, C. A., & Sloviter, R. S. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1619-03.2004 · Cited by 90 · see citing works
Austin, J. E., & Buckmaster, P. S. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20182 · Cited by 80 · see citing works
Young, J. I., Otero, V., Cerdán, M. G., Falzone, T. L., Chan, E., Low, M. J., & Rubinstein, M. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-17-06631.1998 · Cited by 80 · see citing works
Morphologic and electrophysiologic maturation in developing dentate gyrus granule cells
Liu, X., Tilwalli, S., Ye, G.-L., Lio, P., Pasternak, J. F., & Trommer, B. L. (2000) · Brain Research · doi:10.1016/s0006-8993(99)02421-x · Cited by 74 · see citing works
Tu, B., Timofeeva, O., Jiao, Y., & Nadler, J. V. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4835-04.2005 · Cited by 74 · see citing works
Epileptogenesis Is Associated With Enhanced Glutamatergic Transmission in the Perforant Path
Scimemi, A., Schorge, S., Kullmann, D. M., & Walker, M. C. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00680.2005 · Cited by 69 · see citing works
Suzuki, F., Makiura, Y., Guilhem, D., Sørensen, J. C. H., & Onteniente, B. (1997) · Experimental Neurology · doi:10.1006/exnr.1997.6469 · Cited by 68 · see citing works
Temporal profile of hilar basal dendrite formation on dentate granule cells after status epilepticus
Dashtipour, K., Wong, A. M., Obenaus, A., et al. (2003) · Epilepsy Research · doi:10.1016/s0920-1211(03)00082-2 · Cited by 47 · see citing works
Sayın, Ü., Rutecki, P. A., & Sutula, T. P. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.81.2.564 · Cited by 40 · see citing works
Behr, J., Heinemann, U., & Módy, I. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.5.2195 · Cited by 35 · see citing works
Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse
Van Pett, K., Viau, V., Bittencourt, J. C., Chan, R. K. W., Li, H.-Y., Arias, C., Prins, G. S., Perrin, M., Vale, W., & Sawchenko, P. E. (2000) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20001211)428:2
Flagged first, then by citations
Cited by
Sorted by citations
Adult Neurogenesis in the Mammalian Brain: Significant Answers and Significant Questions
Ming, G.-L., & Song, H. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.001 · Cited by 2,651 · see citing works
New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?
Deng, W., Aimone, J. B., & Gage, F. H. (2010) · Nature reviews. Neuroscience · doi:10.1038/nrn2822 · Cited by 2,120 · see citing works
Adult hippocampal neurogenesis in depression
Sahay, A., & Hen, R. (2007) · Nature Neuroscience · doi:10.1038/nn1969 · Cited by 1,206 · see citing works
Neurogenesis in the adult hippocampus
Kempermann, G., Song, H., & Gage, F. H. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018812 · Cited by 1,072 · see citing works
The role of adult hippocampal neurogenesis in brain health and disease
Toda, T., Parylak, S. L., Linker, S. B., & Gage, F. H. (2019) · Molecular Psychiatry · doi:10.1038/s41380-018-0036-2 · Cited by 719 · see citing works
Wang, J.-W., David, D. J., Monckton, J. E., Battaglia, F., & Hen, R. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.3632-07.2008 · Cited by 550 · see citing works
Kim, J. Y., Duan, X., Liu, C. Y., Jang, M.-H., Guo, J. U., Pow-anpongkul, N., Kang, E., Song, H., & Ming, G.-L. (2009) · Neuron · doi:10.1016/j.neuron.2009.08.008 · Cited by 319 · 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
- Authors
- Overstreet-Wadiche, L. S., Bromberg, D. A., Bensen, A. L., & Westbrook, G. L.
- Affiliations
- Oregon Health & Science University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2006-04-12
- Volume
- 26
- Issue
- 15
- Pages
- 4095-4103
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6673901
- OpenAlex
- W2067128446
- Cited by
- 266
- References
- 61
- Citations by year
- 2026: 10 · 2025: 6 · 2024: 7 · 2023: 3 · 2022: 4 · 2021: 6 · 2020: 9 · 2019: 18 · 2018: 7 · 2017: 12 · 2016: 10 · 2015: 18 · 2014: 15 · 2013: 15 · 2012: 12
- FWCI
- 6.50
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (#NS 26494)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Health Sciences › Medicine › Psychiatry and Mental health › Epilepsy research and treatment
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- adult neurogenesis, dentate gyrus granule cells, pilocarpine-induced seizures, epilepsy, synaptic remodeling, dendrite formation, glutamatergic synapses, granule cell maturation, molecular layer
- MeSH terms
- Animals, Animals, Newborn, Cell Division, Crosses, Genetic, Dendrites, Female, Humans, Male, Mice, Transgenic, Pilocarpine, Seizures, Green Fluorescent Proteins, Mice
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