Temporal patterns of fos expression in the dentate gyrus after spontaneous seizures in a mouse model of temporal lobe epilepsy
Open accessAbstract
Identifying the brain regions and neuronal cell types that become active at the time of spontaneous seizures remains an important challenge for epilepsy research, and the involvement of dentate granule cells in early seizure events continues to be debated. Although Fos expression is commonly used to evaluate patterns of neuronal activation, there have been few studies of Fos localization after spontaneous seizures. Thus, in a pilocarpine model of recurrent seizures in C57BL/6 mice, Fos expression was examined at multiple time points after spontaneous seizures to follow the temporal and spatial patterns of Fos activation. By 15 min after the beginning of a spontaneous behavioral seizure, Fos labeling was evident in dentate granule cells. This labeling was particularly striking because of its wide extent and relatively uniform appearance in the granule cell layer. At later time points, from 30 min to 4 h after a spontaneous seizure, Fos labeling was also detected in interneurons within the dentate gyrus and in widespread regions of the temporal lobe. Interestingly, the timing of Fos activation appeared to differ among different types of GABAergic interneurons in the dentate gyrus, with labeling of parvalbumin neurons along the base of the granule cell layer preceding that of GABA neurons in the molecular layer. The findings in this mouse model are consistent with previous suggestions that spontaneous seizures in temporal lobe epilepsy may result from a periodic breakdown of the normal filter functions of the dentate gyrus and a resulting increase in hypersynchronous activity of dentate granule cells.
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?
c-fos is an immediate early gene used as a proxy for neuronal activation.
“Mice were perfused 2h after the EPM test to allow for maximal accumulation of the protein products of c-fos, an immediate early gene used as a proxy for neuronal activation, in interneurons (44).”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [44]
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
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · see citing works
Modification of seizure activity by electrical stimulation: II. Motor seizure
Racine, R. J. (1972) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(72)90177-0 · Cited by 7,141 · see citing works
Interneurons of the hippocampus
Freund, T. F., & Buzsáki, G. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:4 · Cited by 3,423 · 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
Mapping Patterns of c- fos Expression in the Central Nervous System After Seizure
Morgan, J. I., Cohén, D., Hempstead, J. L., & Curran, T. (1987) · Science · doi:10.1126/science.3037702 · Cited by 1,778 · see citing works
Herdegen, T., & Leah, J. D. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(98)00018-6 · Cited by 1,352 · see citing works
The glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system
Shu, S., Ju, G., & Fan, L. (1988) · Neuroscience Letters · doi:10.1016/0304-3940(88)90346-1 · Cited by 1,235 · 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
Sheng, M., McFadden, G., & Greenberg, M. E. (1990) · Neuron · doi:10.1016/0896-6273(90)90115-v · Cited by 1,076 · see citing works
Synaptic Reorganization in the Hippocampus Induced by Abnormal Functional Activity
Sutula, T. P., He, X.-X., Cavazos, J. E., & Scott, G. (1988) · Science · doi:10.1126/science.2449733 · Cited by 902 · see citing works
Stimulation of Neuronal Acetylcholine Receptors Induces Rapid Gene Transcription
Greenberg, M. E., Ziff, E. B., & Greene, L. A. (1986) · Science · doi:10.1126/science.3749894 · Cited by 761 · see citing works
Herrera, D., & Robertson, H. A. (1996) · Progress in Neurobiology · doi:10.1016/s0301-0082(96)00021-4 · Cited by 713 · 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
Kindling stimulation induces c-fos protein(s) in granule cells of the rat dentate gyrus
Dragunow, M., & Robertson, H. A. (1987) · Nature · doi:10.1038/329441a0 · Cited by 576 · see citing works
Schauwecker, P. E., & Steward, O. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.8.4103 · Cited by 510 · see citing works
Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo
Henze, D. A., Wittner, L., & Buzsáki, G. (2002) · Nature Neuroscience · doi:10.1038/nn887 · Cited by 480 · see citing works
Han, Z., Buhl, E. H., Lörinczi, Z., & Somogyi, P. (1993) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1993.tb00507.x · Cited by 411 · see citing works
Zinc-Induced Collapse of Augmented Inhibition by GABA in a Temporal Lobe Epilepsy Model
Buhl, E. H., Otis, T. S., & Módy, I. (1996) · Science · doi:10.1126/science.271.5247.369 · Cited by 409 · 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
Cronin, J., & Dudek, F. E. (1988) · Brain Research · doi:10.1016/0006-8993(88)90681-6 · Cited by 336 · see citing works
Calcium regulation of gene expression in neuronal cells
Ghosh, A., Ginty, D. D., Bading, H., & Greenberg, M. E. (1994) · Journal of Neurobiology · doi:10.1002/neu.480250309 · Cited by 326 · see citing works
Peng, Z., Huang, C., Stell, B. M., Módy, I., & Houser, C. R. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2877-04.2004 · Cited by 321 · see citing works
Self-citationObenaus, A., Esclapez, M., & Houser, C. R. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-10-04470.1993 · Cited by 319 · see citing works
Self-citationThe dentate gyrus as a regulated gate for the propagation of epileptiform activity.
Heinemann, U., Beck, H., Dreier, J. P., et al. (1992) · PubMed · Cited by 290 · see citing works
Cronin, J., Obenaus, A., Houser, C. R., & Dudek, F. E. (1992) · Brain Research · doi:10.1016/0006-8993(92)90777-7 · Cited by 272 · see citing works
Self-citationThe dentate gyrus as a control point for seizures in the hippocampus and beyond.
Lothman, E. W., Stringer, J. L., & Bertram, E. H. (1992) · PubMed · Cited by 240 · 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
Induction of c-fos mRNA by kindled seizures: complex relationship with neuronal burst firing
Labiner, D., Butler, L., Cao, Z., Hosford, D. A., Shin, C., & McNamara, J. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-02-00744.1993 · Cited by 221 · see citing works
Functional anatomy of limbic seizures: Focal discharges from medial entorhinal cortex in rat
Collins, R. C., Tearse, R. G., & Lothman, E. W. (1983) · Brain Research · doi:10.1016/0006-8993(83)91170-8 · Cited by 191 · see citing works
Lerea, L., Butler, L., & McNamara, J. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-08-02973.1992 · Cited by 181 · 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
Patrylo, P. R., & Dudek, F. E. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.1.418 · Cited by 135 · see citing works
Cohen, A. S., Lin, D. D., Quirk, G. L., & Coulter, D. A. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02597.x · Cited by 129 · see citing works
Dragunow, M., & Robertson, H. A. (1988) · Brain Research · doi:10.1016/0006-8993(88)90993-6 · Cited by 128 · see citing works
Scharfman, H. E., Sollas, A. L., & Goodman, J. H. (2002) · Neuroscience · doi:10.1016/s0306-4522(01)00599-1 · Cited by 119 · see citing works
Maximal dentate gyrus activation: characteristics and alterations after repeated seizures
Stringer, J. L., & Lothman, E. W. (1989) · Journal of Neurophysiology · doi:10.1152/jn.1989.62.1.136 · Cited by 111 · 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
Motte, J. E., Fernandes, M. J. D. S., Baram, T. Z., & Nehlig, A. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00135-8 · Cited by 88 · see citing works
Schweitzer, J. S., Patrylo, P. R., & Dudek, F. E. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.68.6.2016 · Cited by 88 · see citing works
Dragunow, M., Yamada, N., Bilkey, D. K., et al. (1992) · Molecular Brain Research · doi:10.1016/0169-328x(92)90051-c · Cited by 87 · see citing works
Bertaina‐Anglade, V., Tramu, G., & Destrade, C. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00258.x · Cited by 85 · see citing works
Coulter, D. A. (2000) · Epilepsia · doi:10.1111/j.1528-1157.2000.tb01565.x · Cited by 82 · see citing works
Woldbye, D. P. D., Greisen, M. H., Bolwig, T. G., Larsen, P. J., & Mikkelsen, J. D. (1996) · Brain Research · doi:10.1016/0006-8993(96)00158-8 · Cited by 76 · see citing works
The Imaging of Individual Atoms
Jefferson, D. A. (1996) · Science · doi:10.1126/science.274.5286.369 · Cited by 73 · see citing works
Willoughby, J. O., Mackenzie, L., Medvedev, A. V., & Hiscock, J. J. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00462-9 · Cited by 59 · see citing works
Expression of c‐fos protein in the experimental epilepsy induced by pilocarpine
Barone, P., Morelli, M., Cicarelli, G., Cozzolino, A., DeJoanna, G., Campanella, G., & DiChiara, G. (1993) · Synapse · doi:10.1002/syn.890140102 · Cited by 58 · see citing works
Gap Junctions, Fast Oscillations and the Initiation of Seizures
Traub, R. D., Michelson-Law, H., Bibbig, A., Buhl, E. H., & Whittington, M. A. (2004) · Advances in experimental medicine and biology · doi:10.1007/978-1-4757-6376-8_9 · Cited by 54 · see citing works
Modest Increase in Extracellular Potassium Unmasks Effect of Recurrent Mossy Fiber Growth
Hardison, J. L., Okazaki, M. M., & Nadler, J. V. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.84.5.2380 · Cited by 52 · see citing works
Klein, B. D., Fu, Y., Ptáček, L. J., et al. (2004) · Epilepsy Research · doi:10.1016/j.eplepsyres.2004.06.007 · Cited by 40 · see citing works
Mello, L. E., Kohman, C. M., Tan, A. M., Cavalheiro, É. A., & Finch, D. M. (1996) · Neuroscience Letters · doi:10.1016/0304-3940(96)12562-3 · Cited by 30 · see citing works
Pan, E., & Stringer, J. L. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.75.1.124 · Cited by 30 · see citing works
Mihály, A., Szakács, R., Bohata, C., Dobó, E., & Krisztin‐Péva, B. (2001) · Epilepsy Research · doi:10.1016/s0920-1211(01)00190-5 · Cited by 29 · see citing works
Stringer, J. L., & Sowell, K. L. (1994) · Epilepsy Research · doi:10.1016/0920-1211(94)90029-9 · Cited by 18 · see citing works
“Out of the Shadows”: The Political View
Bowis, J. (2002) · Epilepsia · doi:10.1046/j.1528-1157.43.s.6.8.x · Cited by 10 · see citing works
John A. Walker, Ph.D. July 25, 1952 to August 1, 2003
Marks, W. J. (2004) · Epilepsia · doi:10.1111/j.0013-9580.2004.55303.x · Cited by 2 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Palop, J. J., Chin, J., Roberson, E. D., Wang, J., Thwin, M. T., Bien-Ly, N., Yoo, J., Ho, K. O., Yu, G.-Q., Kreitzer, A., et al. (2007) · Neuron · doi:10.1016/j.neuron.2007.07.025 · Cited by 1,653 · see citing works
Schoenfeld, T. J., Rada, P., Pieruzzini, P. R., Hsueh, B., & Gould, E. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.5352-12.2013 · Cited by 138 · see citing works
Fenoglio, K. A., Chen, Y., & Baram, T. Z. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4080-05.2006 · Cited by 124 · see citing works
Murthy, S., Kane, G. A., Katchur, N. J., Lara Mejia, P. S., Obiofuma, G., Buschman, T. J., McEwen, B. S., & Gould, E. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.02.021 · Cited by 118 · see citing works
Peng, Z., Zhang, N., Wei, W., Huang, C. S., Cetina, Y., Otis, T. S., & Houser, C. R. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.2045-13.2013 · Cited by 114 · see citing works
Self-citationTong, X., Peng, Z., Zhang, N., Cetina, Y., Huang, C. S., Wallner, M., Otis, T. S., & Houser, C. R. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.2853-15.2015 · Cited by 15 · see citing works
Self-citation
- Authors
- Peng, Z., & Houser, C. R.
- Affiliations
- University of California, Los Angeles (US)
- Corresponding author
- Houser, Carolyn R.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2005-08-03
- Volume
- 25
- Issue
- 31
- Pages
- 7210-7220
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6725230
- OpenAlex
- W1999508923
- Cited by
- 106
- References
- 56
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 6 · 2023: 2 · 2022: 7 · 2021: 7 · 2020: 2 · 2019: 5 · 2018: 5 · 2017: 6 · 2016: 4 · 2015: 4 · 2014: 5 · 2013: 11 · 2012: 7
- FWCI
- 4.83
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Department of Veterans Affairs (I01 BX000404)
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (R01NS046524, NS046524)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Epilepsy research and treatment
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- Fos expression, dentate gyrus, dentate gyrus granule cells, temporal lobe epilepsy, spontaneous seizures, pilocarpine-induced seizures, GABAergic interneurons, parvalbumin neurons, GABAergic neurons, neuronal activation
- MeSH terms
- Animals, Disease Models, Animal, Epilepsy, Temporal Lobe, gamma-Aminobutyric Acid, Hippocampus, Immunohistochemistry, Interneurons, Male, Mice, Inbred C57BL, Neurons, Parvalbumins, Pilocarpine, Recurrence, Seizures, Temporal Lobe, Time Factors, Proto-Oncogene Proteins c-fos, Dentate Gyrus, 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