Altered patterning of dentate granule cell mossy fiber inputs onto CA3 pyramidal cells in limbic epilepsy
Open accessAbstract
Impaired gating by hippocampal dentate granule cells may promote the development of limbic epilepsy by facilitating seizure spread through the hippocampal trisynaptic circuit. The second synapse in this circuit, the dentate granule cell≫CA3 pyramidal cell connection, may be of particular importance because pathological changes occurring within the dentate likely exert their principal effect on downstream CA3 pyramids. Here, we utilized GFP-expressing mice and immunolabeling for the zinc transporter ZnT-3 to reveal the pre- and postsynaptic components of granule cell≫CA3 pyramidal cell synapses following pilocarpine-epileptogenesis. Confocal analyses of these terminals revealed that while granule cell presynaptic giant boutons increased in size and complexity 1 month after status epilepticus, individual thorns making up the postsynaptic thorny excrescences of the CA3 pyramidal cells were reduced in number. This reduction, however, was transient, and 3 months after status, thorn density recovered. This recovery was accompanied by a significant change in the distribution of thorns along pyramidal cells dendrites. While thorns in control animals tended to be tightly clustered, thorns in epileptic animals were more evenly distributed. Computational modeling of thorn distributions predicted an increase in the number of boutons required to cover equivalent numbers of thorns in epileptic vs. control mice. Confirming this prediction, ZnT-3 labeling of presynaptic giant boutons apposed to GFP-expressing thorns revealed a near doubling in bouton density, while the number of individual thorns per bouton was reduced by half. Together, these data provide clear evidence of novel plastic changes occurring within the epileptic hippocampus.
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Limbic epileptogenesis involves a partially-understood molecular cascade that results in aberrant neuronal connectivity and chronic recurrent spontaneous seizures.
“Development of TLE or limbic epileptogenesis [4, 5] involves a partially-understood molecular cascade [6] that results in aberrant neuronal connectivity [7, 8] from a multi-architecture neuronal network of the limbic system connected to hippocampal formation [9] that contributes to a systemic process in the brain that leads to chronic recurrent spontaneous seizures [10].”
From Hippocampal neuro-networks and dendritic spine perturbations in epileptogenesis are attenuated by neuroprotectin D1 (2015) · cites this paper as [7]
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Ni, H., Feng, X., Gong, Y., Tao, L., & Wu, X. (2010) · Biological Trace Element Research · doi:10.1007/s12011-010-8836-5 · Cited by 11 · see citing works
Hippocampal glucocorticoid receptors modulate status epilepticus severity
Kraus, K. L., Nawreen, N., Godale, C. M., Chordia, A. P., Packard, B. A., LaSarge, C. L., Herman, J. P., & Danzer, S. C. (2023) · Neurobiology of Disease · doi:10.1016/j.nbd.2023.106014 · Cited by 9 · see citing works
Self-citationGlutamate Imaging Reveals Multiple Sites of Stochastic Release in the CA3 Giant Mossy Fiber Boutons
Rama, S., Jensen, T. P., & Rusakov, D. A. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00243 · Cited by 9 · see citing works
Guo, D., Han, L., Godale, C. M., Rensing, N. R., Danzer, S. C., & Wong, M. L. (2024) · Epilepsia · doi:10.1111/epi.18011 · Cited by 7 · see citing works
Self-citationPark, S. Y., Sheridan, A., An, B., Jarvis, E., Lyudchik, J., Patton, W., Axup, J. Y., Chan, S., Damstra, H. G. J., Leible, D., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.09.26.678648 · Cited by 6 · see citing works
Somatostatin interneuron fate-mapping and structure in a Pten knockout model of epilepsy
Drake, A. W., Jerow, L. G., Ruksenas, J. V., McCoy, C., & Danzer, S. C. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1474613 · Cited by 3 · see citing works
Self-citation(2014) · Molecular & Cellular Epilepsy · doi:10.14800/mce.128 · Cited by 3 · see citing works
Epilepsia del lóbulo temporal y las neuronas hipocampales de las áreas CA1 y CA3
López-Hernández, E., & Solís, H. (2012) · Revista de la Facultad de Medicina (México) · Cited by 1 · see citing works
- Authors
- McAuliffe, J. J., Bronson, S. L., Hester, M. S., Murphy, B. L., Dahlquist‐Topalá, R., Richards, D. A., & Danzer, S. C.
- Affiliations
- Cincinnati Children's Hospital Medical Center (US)
- University of Cincinnati (US)
- Corresponding author
- Danzer, Steve C.
- Venue
- Hippocampus
- Publisher
- Wiley
- Published
- 2010-12-23
- Volume
- 21
- Issue
- 1
- Pages
- 93-107
- ISSN
- 1050-9631 (ISSN-L)
- 1098-1063
- PMC
- PMC2888689
- OpenAlex
- W2041510888
- Cited by
- 47
- References
- 62
- Citations by year
- 2025: 1 · 2024: 2 · 2023: 1 · 2022: 1 · 2021: 2 · 2020: 1 · 2019: 2 · 2018: 5 · 2017: 3 · 2016: 4 · 2015: 6 · 2014: 4 · 2013: 3 · 2012: 4
- FWCI
- 2.47
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Hippocampus (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Korea Electrotechnology Research Institute
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (R01NS054750, R01NS065020, R01NS062806)
- 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
- limbic epilepsy, dentate gyrus granule cells, CA3 pyramidal cells, mossy fiber synapses, status epilepticus, synaptic plasticity, computational modeling, seizure propagation
- MeSH terms
- Animals, Epilepsy, Immunohistochemistry, Male, Mice, Inbred C57BL, Mice, Transgenic, Neural Pathways, Neuronal Plasticity, Pilocarpine, Presynaptic Terminals, Pyramidal Cells, Microscopy, Confocal, Muscarinic Agonists, Mossy Fibers, Hippocampal, 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.
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