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Spatial Long-Term Memory Is Related to Mossy Fiber Synaptogenesis
Open accessAbstract
Structural synaptic changes have been suggested to underlie long-term memory formation. In this work, we investigate if hippocampal mossy fiber synaptogenesis induced by water maze overtraining can be related with long-term spatial memory performance. Rats were trained in a Morris water maze for one to five identical daily sessions and tested for memory retrieval 1 week and 1 month after training. After the last test session, the rat brains were obtained and processed for Timm's staining to analyze mossy fiber projection. The behavioral results showed that with more training, animals showed a better performance in the memory tests, and this performance positively correlates with Timm's staining in the stratum oriens. Furthermore, with the use of the NMDA antagonist MK801 before, but not after acquisition, water maze spatial memory was impaired. Increased Timm's staining in the stratum oriens was observed in the animals treated with MK801 after acquisition but not in those treated before. Finally, we observed that mossy fiber synaptogenesis occurs mainly in the septal region of the dorsal hippocampus, supporting the idea that this anterior region is important for spatial memory. Altogether, these results suggest that mossy fiber synaptogenesis can be related with spatial long-term memory formation.
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“ATRAmediated prevention of synaptic loss in the stratum lucidum of the CA3 area, in which the mossy fibers from the dentate gyrus synapse with the dendrites of the pyramidal neurons, may play a key role in rescuing deficits of learning and memory”
From Retinoic Acid Attenuates β-Amyloid Deposition and Rescues Memory Deficits in an Alzheimer's Disease Transgenic Mouse Model (2008) · cites this paper as Ramirez-Amaya et al., 2001
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Cites
The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585
AChE-stained horizontal sections of the rat brain in stereotaxic coordinates
Paxinos, G., WATSON, C. R. R., & Emson, P. C. (1980) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(80)90021-7 · Cited by 4,514
More hippocampal neurons in adult mice living in an enriched environment
Kempermann, G., Kuhn, H. G., & Gage, F. H. (1997) · Nature · doi:10.1038/386493a0 · Cited by 3,586
Kuhn, H., Dickinson-Anson, H., & Gage, F. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-06-02027.1996 · Cited by 3,139
Long-Term Potentiation--A Decade of Progress?
Malenka, R. C., & Nicoll, A. R. A. (1999) · Science · doi:10.1126/science.285.5435.1870 · Cited by 2,729
The three-dimensional organization of the hippocampal formation: A review of anatomical data
Amaral, D. G., & Witter, M. P. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90424-7 · Cited by 2,180
Neurogenesis in the adult is involved in the formation of trace memories
Shors, T. J., Miesegaes, G. R., Beylin, A. V., Zhao, M., Rydel, T. A., & Gould, E. (2001) · Nature · doi:10.1038/35066584 · Cited by 2,014
Hippocampal synaptic enhancement and information storage within a distributed memory system
McNaughton, B. L., & Morris, R. G. M. (1987) · Trends in Neurosciences · doi:10.1016/0166-2236(87)90011-7 · Cited by 1,304
Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat
Ishizuka, N., Weber, J., & Amaral, D. G. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902950407 · Cited by 899
Research works printed but not linked: 1
- Dudai Y (1989) Some basic notions and their ontogenesis. In: The neurobiology of memory: concepts, findings, trends, Chap 1, pp 3-18. New York: Oxford UP.
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Llorens-Martı́n, M. (2018) · Brain Plasticity · doi:10.3233/bpl-180065 · Cited by 24
Kim, J.-I., Jeon, S. G., Kim, K., Kim, J.-J., Song, E., Jeon, Y., Kim, E., Lee, K., Kwak, J. H., & Moon, M. (2017) · Nutrients · doi:10.3390/nu9070794 · Cited by 23
Hernández, E. R., Mendieta, L., Flores, G., & Limón, I. D. (2017) · Neuropeptides · doi:10.1016/j.npep.2017.11.001 · Cited by 23
Plastic processes in the dentate gyrus: a computational perspective
Derrick, B. E. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)63024-6 · Cited by 22
Gusev, P. A. (2010) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2010.00015 · Cited by 24
Morin, J., Cerón-Solano, G., Velázquez-Campos, G., Pacheco‐López, G., Bermúdez‐Rattoni, F., & Díaz-Cintra, S. Y. (2016) · Journal of Alzheimer s Disease · doi:10.3233/jad-150975 · Cited by 22
Salcido, F. A. M., Torres-Flores, M. I., Ordaz, B., & Peña‐Ortega, F. (2022) · Glia · doi:10.1002/glia.24185 · Cited by 21
Isgor, C., Pare, C., McDole, B., Coombs, P., & Guthrie, K. M. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.12.036 · Cited by 21
Holahan, M. R., Honegger, K. S., & Routtenberg, A. (2009) · Hippocampus · doi:10.1002/hipo.20635 · Cited by 21
Trinchero, M. F., Koehl, M., Bechakra, M., Delage, P., Charrier, V., Grosjean, N., Ladevèze, E., Schinder, A. F., & Abrous, D. N. (2015) · Hippocampus · doi:10.1002/hipo.22438 · Cited by 21
Shanmugasundaram, B., Sase, A., Miklosi, A. G., Sialana, F. J., Subramaniyan, S., Aher, Y. D., Gröger, M., Höger, H., Bennett, K. L., & Lübec, G. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.04.043 · Cited by 18
Kim, J., Park, D., Seo, N., Yoon, T.-H., Kim, G. H., Lee, S.-H., Seo, J., Um, J. W., Lee, K. J., & Ko, J. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2110196119 · Cited by 18
Yamada, K., Ono, Y., Kubo, K., Yamamoto, T., & Onozuka, M. (2013) · The Tohoku Journal of Experimental Medicine · doi:10.1620/tjem.230.49 · Cited by 17
McGonigal, R., Tabatadze, N., & Routtenberg, A. (2011) · Hippocampus · doi:10.1002/hipo.20998 · Cited by 18
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Middei, S., Vetere, G., Sgobio, C., & Ammassari‐Teule, M. (2006) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2006.08.004 · Cited by 17
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Méndez-López, M., Méndez, M., Begega, A., & Arias, J. L. (2010) · Neuroscience Letters · doi:10.1016/j.neulet.2010.07.054 · Cited by 15
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McNamara, R. K., & Lenox, R. H. (2004) · Clinical Neuroscience Research · doi:10.1016/j.cnr.2004.09.008 · Cited by 14
Kokhan, V. S., & Dobynde, M. I. (2023) · Biology · doi:10.3390/biology12030400 · Cited by 23
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Carasatorre, M., & Ramı́rez-Amaya, V. (2012) · Current topics in behavioral neurosciences · doi:10.1007/7854_2012_229 · Cited by 14
Wartman, B. C., Gervais, N. J., Smith, C., Comba, R., Mumby, D. G., & Holahan, M. R. (2012) · Brain Research · doi:10.1016/j.brainres.2012.08.012 · Cited by 13
Aussel, A., Ranta, R., Aron, O., Colnat‐Coulbois, S., Maillard, L., & Buhry, L. (2022) · Journal of Computational Neuroscience · doi:10.1007/s10827-022-00829-5 · Cited by 13
Carasatorre, M., Ochoa-Alvarez, A., Velázquez-Campos, G., Lozano‐Flores, C., Díaz-Cintra, S. Y., & Ramírez-Amaya, V. (2015) · PLoS ONE · doi:10.1371/journal.pone.0132676 · Cited by 14
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Miranda, R., Blanco, E., Begega, A., Santín, L. J., & Arias, J. L. (2005) · Synapse · doi:10.1002/syn.20229 · Cited by 12
Martínez-Moreno, A., Rivera-Olvera, A., & Escobar, M. L. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2019.107125 · Cited by 12
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Chau, L. S., Davis, A. S., & Galvez, R. (2013) · Behavioral Neuroscience · doi:10.1037/a0031890 · Cited by 12
Comba, R., Gervais, N. J., Mumby, D. G., & Holahan, M. R. (2015) · F1000Research · doi:10.12688/f1000research.6822.1 · Cited by 11
Zorzo, C., Arias, J. L., & Méndez, M. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113204 · Cited by 13
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Zorzo, C., Arias, J. L., & Méndez, M. (2020) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2020.107312 · Cited by 8
Zhang, B., Chuang, K., Tjio, C., Chen, W. C., Sheu, F., & Routtenberg, A. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.07.084 · Cited by 8
Activity maintains structural plasticity of mossy fiber terminals in the hippocampus
Chierzi, S., Stachniak, T. J., Trudel, E., Bourque, C. W., & Murai, K. K. (2012) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2012.05.004 · Cited by 9
Carasatorre, M., Ramı́rez-Amaya, V., & Díaz-Cintra, S. Y. (2016) · Neurología (English Edition) · doi:10.1016/j.nrleng.2012.12.006 · Cited by 8
Juárez-Muñoz, Y., Rivera-Olvera, A., Ramos-Languren, L. E., & Escobar, M. L. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.12.015 · Cited by 9
Wang, H., Liu, J., Lu, Z., Dai, Y., Xie, J., Xu, S., Song, Y., Xiao, G., Gao, F., Qu, L., et al. (2020) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2020.07.079 · Cited by 7
Abulaiti, X., Wang, A., Zhang, H., Su, H., Gao, R., Chen, J., Gao, S., & Li, L. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04206-4 · Cited by 8
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Housh, A. A., Berkowitz, L. E., Ybarra, I., Kim, E. U., Lee, B. R., & Calton, J. L. (2014) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2014.09.012 · Cited by 4
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Fuchs, S. A., Roeleveld, M. W., Klomp, L. W. J., Berger, R., & de Koning, T. J. (2012) · JIMD Reports · doi:10.1007/8904_2011_116 · Cited by 4
Alteration of sensorineural circuits in spinal cord by chronic contact dermatitis
Seike, M., Hamada, R., Ikeda, M., & Kodama, H. (2005) · Somatosensory & Motor Research · doi:10.1080/089900220400015334 · Cited by 4
Hansen, S. N., Schjoldager, J. G., Paidi, M. D., Lykkesfeldt, J., & Tveden‐Nyborg, P. (2016) · Nutrition Research · doi:10.1016/j.nutres.2016.03.004 · Cited by 4
Shobe, J. L., Ghanbarian, E., Bain, R., Saxena, R., Chandrasekaran, M., & McNaughton, B. L. (2025) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2025.1646883 · Cited by 3
Cansev, M., & Ulus, İ. H. (2011) · Springer eBooks · doi:10.1007/978-0-387-92271-3_32 · Cited by 3
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Stenstrom, P. (2010) · doi:10.71781/18000 · Cited by 3
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Holahan, M. R., & Routtenberg, A. (2006) · Springer eBooks · doi:10.1007/0-387-25443-9_24 · Cited by 2
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Padilla‐Gómez, E., Campos, V., Montes, S., Dı́az-Ruiz, A., Quirarte, G. L., Rı́os, C., & Díaz-Cintra, S. Y. (2012) · BioMetals · doi:10.1007/s10534-012-9575-1 · Cited by 2
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Khoutorsky, A., Gkogkas, C. G., & Sonenberg, N. (2012) · Springer eBooks · doi:10.1007/978-1-4614-3991-2_14 · Cited by 1
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Routtenberg, A., Tabatadze, N., & McGonigal, R. (2011) · Hippocampus · doi:10.1002/hipo.20976 · Cited by 1
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Miyamoto, M., Sugioka, K., Arakawa, T., Kawamata, T., & Miki, A. (2009) · Institutional Repositories DataBase (IRDB) · doi:10.24546/81002144
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Metadata
- Authors
- Ramı́rez-Amaya, V., Balderas, I., Sandoval, J., Escobar, M. L., & Bermúdez-Rattoni, F.
- Affiliations
- Universidad Nacional Autónoma de México (MX)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2001-09-15
- Volume
- 21
- Issue
- 18
- Pages
- 7340-7348
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6763009
- OpenAlex
- W1840921431
- Cited by
- 177
- References
- 52
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 1 · 2023: 1 · 2022: 4 · 2021: 2 · 2020: 4 · 2019: 6 · 2018: 3 · 2017: 7 · 2016: 9 · 2015: 11 · 2014: 3 · 2013: 11 · 2012: 12
- FWCI
- 4.02
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Dirección General de Asuntos del Personal Académico, Universidad Nacional Autónoma de México
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- hippocampus, dorsal hippocampus, stratum oriens, MK-801, NMDA receptor, memory consolidation, septal area
- MeSH terms
- Animals, Behavior, Animal, Coloring Agents, Hippocampus, Learning, Male, Memory, Retention, Psychology, Synapses, Receptors, N-Methyl-D-Aspartate, Rats, Wistar, Excitatory Amino Acid Antagonists, Maze Learning, Mossy Fibers, Hippocampal, Rats
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