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Cholinergic stimulation enhances long-term potentiation in the CA1 region of rat hippocampus
Abstract
The effect of the cholinergic agonist carbachol on a putative substrate for memory (long-term potentiation; LTP) was investigated in slices of rat hippocampus (CA1 region). Carbachol (5 microM) increased LTP when the presynaptic depression of the EPSP was controlled. The results indicate that carbachol enhances the effectiveness of the tetanus, probably through postsynaptic mechanisms. This effect may have implications for the role of acetylcholine in memory and the use of cholinergics in memory disorders.
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“The enhancement of long-term encoding could be at least partially mediated by the cholinergic enhancement of long-term potentiation in the hippocampus (Blitzer et al., 1990; Burgard and Sarvey, 1990; Auerbach and Segal, 1994; Isaac et al., 2009).”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as Blitzer et al., 1990
Citations
Cites
The cholinergic hypothesis of geriatric memory dysfunction
Bartus, R. T., Dean, R. L., Beer, B., & Lippa, A. S. (1982) · Science · doi:10.1126/science.7046051 · Cited by 5,545
Magnesium gates glutamate-activated channels in mouse central neurones
Nowak, L. M., Bregestovski, P. D., Ascher, P., Herbet, A., & Prochiantz, A. (1984) · Nature · doi:10.1038/307462a0 · Cited by 4,116
Morris, R. G. M., Anderson, E., Lynch, G. S., & Baudry, M. (1986) · Nature · doi:10.1038/319774a0 · Cited by 3,640
Psychopharmacology: The third generation of progress
O’Connell, R. A. (1988) · Comprehensive Psychiatry · doi:10.1016/0010-440x(88)90057-0 · Cited by 3,020
Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones
Mayer, M. L., Westbrook, G. L., & Guthrie, P. B. (1984) · Nature · doi:10.1038/309261a0 · Cited by 2,941
Intracellular injections of EGTA block induction of hippocampal long-term potentiation
Lynch, G., Larson, J., Kelso, S., Barrionuevo, G., & Schottler, F. (1983) · Nature · doi:10.1038/305719a0 · Cited by 1,116
Postsynaptic Calcium Is Sufficient for Potentiation of Hippocampal Synaptic Transmission
Malenka, R. C., Kauer, J. A., Zucker, R. S., & Nicoll, R. A. (1988) · Science · doi:10.1126/science.2845577 · Cited by 829
Synaptic enhancement in fascia dentata: Cooperativity among coactive afferents
McNaughton, B. L., Douglas, R. M., & Goddard, G. V. (1978) · Brain Research · doi:10.1016/0006-8993(78)90030-6 · Cited by 647
Gustafsson, B., Wigstrom, H., Abraham, W., & Huang, Y. (1987) · The Journal of Neuroscience · doi:10.1523/jneurosci.07-03-00774.1987 · Cited by 583
Harris, E. W., & Cotman, C. W. (1986) · Neuroscience Letters · doi:10.1016/0304-3940(86)90451-9 · Cited by 540
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Effect of vitamin E on memory retention in rats: Possible involvement of cholinergic system
Eidi, A., Eidi, M., Mahmoodi, G., & Oryan, S. (2005) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2005.06.006 · Cited by 32
SAKATA, K., Tokue, A., & Kawai, N. (2000) · The Journal of Urology · doi:10.1016/s0022-5347(05)67773-7 · Cited by 32
Zhang, L., Weiner, J. L., & Carlen, P. L. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-11-04510.1992 · Cited by 31
Iga, Y., Arisawa, H., Ise, M., Yasuda, H., & Takeshita, Y. (1996) · European Journal of Pharmacology · doi:10.1016/0014-2999(96)00268-3 · Cited by 31
The effects of galanin on long-term synaptic plasticity in the CA1 area of rodent hippocampus
Coumis, U., & Davies, C. H. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00007-6 · Cited by 30
Beldhuis, H. J. A., Everts, H. G. J., van der Zee, E. A., Luiten, P. G. M., & Bohus, B. (1992) · Hippocampus · doi:10.1002/hipo.450020408 · Cited by 30
Luo, L., Chen, W., Wang, M., Zhu, D., She, J., & Ruan, D. (2008) · Hippocampus · doi:10.1002/hipo.20461 · Cited by 29
Presynaptic Gating of Postsynaptic Synaptic Plasticity
Blundon, J. A., & Zakharenko, S. S. (2013) · The Neuroscientist · doi:10.1177/1073858413482983 · Cited by 29
Impaired brain plasticity as a potential therapeutic target for treatment and prevention of dementia
Rajji, T. K. (2018) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2019.1550074 · Cited by 30
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Connor, J. A., Pozzo‐Miller, L. D., Petrozzino, J. J., & Müller, W. S. (1994) · Journal of Neurobiology · doi:10.1002/neu.480250304 · Cited by 29
Chapman, C. A., & Racine, R. J. (1997) · Hippocampus · doi:10.1002/(sici)1098-1063(1997)7:3 · Cited by 28
Maeda, T., Kaneko, S., & Satoh, M. (1993) · Brain Research · doi:10.1016/0006-8993(93)91628-6 · Cited by 29
Appleyard, M. E. (1995) · Neuroscience Letters · doi:10.1016/0304-3940(95)11491-e · Cited by 28
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Kojima, J., Onodera, K., Ozeki, M., & Nakayama, K. (1998) · CNS Drug Reviews · doi:10.1111/j.1527-3458.1998.tb00067.x · Cited by 27
Kunitake, A., Kunitake, T., & Stewart, M. (2004) · Hippocampus · doi:10.1002/hipo.20016 · Cited by 27
Greenwood, J. M., & Dragunow, M. (2002) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2002.00992.x · Cited by 27
Farchi, N., Shoham, S., Hochner, B., & Soreq, H. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05249.x · Cited by 26
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de Vente, J. (2004) · Neurochemistry International · doi:10.1016/j.neuint.2004.03.010 · Cited by 26
Katsuki, H., Saitō, H., & Satoh, M. (1992) · Neuroscience Letters · doi:10.1016/0304-3940(92)90384-j · Cited by 26
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Kanju, P. M., Parameshwaran, K., Sims‐Robinson, C., Uthayathas, S., Josephson, E. M., Rajakumar, N., Dhanasekaran, M., & Suppiramaniam, V. D. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031073 · Cited by 28
Kocsis, K., Knapp, L., Gellért, L., Oláh, G., Kis, Z., Takakuwa, H., Iwamori, N., Ono, E., Toldi, J., & Farkas, T. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.03.055 · Cited by 24
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Egorov, A. V., Angelova, P. R., Heinemann, U., & Müller, W. S. (2003) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2003.03050.x · Cited by 24
Feasey‐Truger, K. J., Li, B.-H., & ten Bruggencate, G. (1992) · Brain Research · doi:10.1016/0006-8993(92)91711-m · Cited by 24
Trebbastoni, A., Gilio, F., D’Antonio, F., Cambieri, C., Ceccanti, M., de Lena, C., & Inghilleri, M. (2011) · Clinical Neurophysiology · doi:10.1016/j.clinph.2011.09.010 · Cited by 24
Guillem, F., Chouinard, S., Poulin, J., Godbout, R., Lalonde, P., Melun, P., Bentaleb, L. A., & Stip, É. (2006) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2006.02.009 · Cited by 23
Markevich, V. A., Scorsa, A. M., Dawe, G. S., & Stephenson, J. D. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00055-3 · Cited by 23
Matsuoka, N., Yamaguchi, I., & Satoh, M. (1993) · European Journal of Pharmacology · doi:10.1016/0014-2999(93)90928-b · Cited by 21
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Müller, W. S., & Connor, J. A. (1992) · Journal of Physiology-Paris · doi:10.1016/s0928-4257(05)80008-7 · Cited by 22
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Hasselmo, M. E., & Stern, C. E. (2018) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2017.0275 · Cited by 20
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Skrebitsky, V. G., & Chepkova, A. N. (1998) · Reviews in the Neurosciences · doi:10.1515/revneuro.1998.9.4.243 · Cited by 19
Nakao, K., Ikegaya, Y., Yamada, M. K., Nishiyama, N., & Matsuki, N. (2001) · Neuroscience Letters · doi:10.1016/s0304-3940(01)01961-9 · Cited by 19
Retrieval associated cholinergic activity and its inhibition by memory updating
Popik, P., Nalepa, I., Mamczarz, J., & Vetulani, J. (1994) · Life Sciences · doi:10.1016/0024-3205(94)00852-3 · Cited by 19
Cholinergic modulation of neocortical long-term potentiation in the awake, freely moving rat
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Yliopisto, K., & Ikonen, S. (2001) · Cited by 19
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McDevitt, E. A., Rowe, K. M., Brady, M., Duggan, K. A., & Mednick, S. C. (2014) · Experimental Brain Research · doi:10.1007/s00221-014-3830-3 · Cited by 19
Tai, S. K., & Leung, L.-W. S. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.04.013 · Cited by 18
Kumar, A. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00278.2010 · Cited by 18
Almeida, V. N. (2021) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2021.06.001 · Cited by 18
Natsume, K., & Kometani, K. (1999) · Neuroscience Research · doi:10.1016/s0168-0102(99)00007-3 · Cited by 17
Tang, M., Luo, L., Zhu, D., Wang, M., Luo, Y., Wang, H., & Ruan, D. (2008) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-008-0344-1 · Cited by 17
Salavati, B., Daskalakis, Z. J., Zomorrodi, R., Blumberger, D. M., Chen, R. E., Pollock, B. G., & Rajji, T. K. (2018) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2018.00155 · Cited by 16
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Silkis, I. G. (2009) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-009-9163-1 · Cited by 16
Wang, L., Luo, L., Luo, Y., Gu, Y., & Ruan, D. (2006) · NeuroToxicology · doi:10.1016/j.neuro.2006.11.003 · Cited by 15
Lampe, B. J., Gaskill, J. L., Keim, S. C., & Brown, B. S. (1997) · Neuroscience Letters · doi:10.1016/s0304-3940(97)13347-x · Cited by 15
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Wang, M., Chen, W., Zhu, D.-M., She, J., & Ruan, D. (2006) · Food and Chemical Toxicology · doi:10.1016/j.fct.2006.08.025 · Cited by 13
González, I., Arévalo‐Serrano, J., Pérez, J. L. M., Gonzalo, P., & Gonzalo‐Ruiz, A. (2008) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2007.00932.x · Cited by 13
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Hasselmo, M. E. (2000) · Springer eBooks · doi:10.1007/978-1-4612-1302-4_5 · Cited by 13
Yoshida, A., Chen, K., Moritani, M., Yabuta, N. H., Nagase, Y., Takemura, M., & Shigenaga, Y. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970623)383:1 · Cited by 57
Ahnaou, A., White, E., Biermans, R., Manyakov, N., & Drinkenburg, W. (2020) · Journal of Neural Transplantation and Plasticity · doi:10.1155/2020/6249375 · Cited by 11
Kojima, J., & Onodera, K. (1998) · General Pharmacology The Vascular System · doi:10.1016/s0306-3623(97)00436-9 · Cited by 12
Gonzalez, J., Lignani, G., Maroto, M., Baldelli, P., & Hernández-Guijo, J. M. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht032 · Cited by 12
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Samanta, A., Alonso, A., & Genzel, L. (2020) · Current Opinion in Physiology · doi:10.1016/j.cophys.2020.01.003 · Cited by 12
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Pirazzini, G., & Ursino, M. (2024) · Frontiers in Neural Circuits · doi:10.3389/fncir.2024.1326609 · Cited by 10
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Cuello, A. C. (2025) · Handbook of clinical neurology · doi:10.1016/b978-0-443-19088-9.00005-6 · Cited by 8
Carette, B. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.3.1042 · Cited by 8
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Stein, E. S., Dori, A., Shimon, M. B., Gofrit, S. G., & Maggio, N. (2021) · Neural Plasticity · doi:10.1155/2021/8813734 · Cited by 7
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Kassab, R. (2023) · Hippocampus · doi:10.1002/hipo.23533 · Cited by 7
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Giovannini, M. G., & Lana, D. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802733-2.00018-9 · Cited by 7
Sato, D., Yamashiro, K., Yamazaki, Y., Ikarashi, K., Onishi, H., Baba, Y., & Maruyama, A. (2019) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph17010215 · Cited by 7
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Nathanson, N. M. (1996) · Progress in brain research · doi:10.1016/s0079-6123(08)62098-1 · Cited by 6
Kanamori, T., Matsukawa, N., Kobayashi, H., Uematsu, N., Sagisaka, T., Toyoda, T., Kato, D., Oikawa, S., & Ojika, K. (2010) · Brain Research · doi:10.1016/j.brainres.2010.07.081 · Cited by 5
Lee, J., Kwon, H., Yu, J., Cho, E., Jeon, J., Lee, S., Ryu, J. H., Lee, Y. C., Kim, D. H., & Jung, J. W. (2018) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2018.05.017 · Cited by 4
Natsume, K., & Kometani, K. (1997) · Neuroscience Research · doi:10.1016/s0168-0102(97)00079-5 · Cited by 4
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Gupta, K., & Hasselmo, M. E. (2014) · Springer eBooks · doi:10.1007/978-3-7091-1292-2_7 · Cited by 3
Xia, M., Zhao, F., Zhang, Y., Zheng, Z., Zhou, Y., & Liu, T. (2022) · European journal of medical research · doi:10.1186/s40001-022-00666-3 · Cited by 2
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Auerbach, J. M., & Segal, M. (1998) · Advances in behavioral biology · doi:10.1007/978-1-4615-5337-3_93 · Cited by 2
Ahmed, S., Allam, A. T., Eid, O., Zaki, E. S., Shaheen, A. M., Al-Nazer, M. A., Shalaby, M. E., El‐Dessouki, A. M., Kotb, S. S., El‐Shiekh, R. A., et al. (2026) · Scientific African · doi:10.1016/j.sciaf.2026.e03640 · Cited by 1
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Kuo, M. (2007) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-225 · Cited by 1
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Adams, C. B. (1998) · Library and Archives Canada (Government of Canada) · doi:10.71548/8718
Role of the Cannabinoid Receptor Type 1 (CB1) in Synaptic Plasticity, Memory and Emotionality
Jacob, W. (2007) · Electronic Theses of LMU Munich (Ludwig-Maximilians-Universität München) · doi:10.5282/edoc.7230
Vu, T. H. (2016) · Scholarship@Western (Western University)
Thirugnanasambandam, N. (2011) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-3251
Cholinergic Neuromodulation of Activity-dependent Disinhibition-mediated Plasticity
Takkala, P. (2012) · Library and Archives Canada (Government of Canada)
Vassilis Cutsuridis, A. (2018) · Springer series in computational neuroscience · doi:10.1007/978-3-319-99103-0_18
Hoeller, A. A., Lach, G., Costa, A. P., Walz, R., Bortolotto, Z. A., & de Lima, T. C. M. (2019) · Neurology Psychiatry and Brain Research · doi:10.1016/j.npbr.2019.10.004
The Effects of Rhythmical Waves Induced by Carbachol on LTP in Guinea Pig Hippocampal Slices
Natsume, K., & Kometani, K. (1996) · The Brain & Neural Networks · doi:10.3902/jnns.3.135
(1997) · Advances in psychology · doi:10.1016/s0166-4115(97)80114-8
&NA;, K. S., Tokue, A., & Kawai, N. (2000) · The Journal of Urology · doi:10.1097/00005392-200004000-00080
Aguiar, C. L. (2010) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/d.17.2010.tde-06052024-160628
Cholinergic modulation of the superficial layers of the parasubiculum.
Glasgow, S. D. (2011) · Spectrum Research Repository (Concordia University)
Efeito do tratamento com drogas amnésicas na memória emocional de ratos no LCE
Belmonte, L. M. (2006) · Americanae (AECID Library)
Muscarinic receptors in schizophrenia: is there a role for synaptic plasticity?
Raedler, T. J. (2004) · International review of neurobiology · doi:10.1016/s0074-7742(04)59005-0
Müller, W. S., Winterer, J., & Stanton, P. K. (2005) · Springer eBooks · doi:10.1007/0-387-25443-9_3
Metadata
- Authors
- Blitzer, R. D., Gil, O., & Landau, E. M.
- Affiliations
- United States Department of Veterans Affairs (US)
- Mount Sinai Hospital (US)
- Corresponding author
- Blitzer, Robert D.
- ORCID
- Blitzer, Robert D.
- Venue
- Neuroscience Letters
- Publisher
- Elsevier BV
- Published
- 1990-11
- Volume
- 119
- Issue
- 2
- Pages
- 207-210
- ISSN
- 0304-3940 (ISSN-L)
- OpenAlex
- W2071637530
- Cited by
- 192
- References
- 23
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 2 · 2023: 2 · 2022: 3 · 2021: 3 · 2020: 4 · 2019: 4 · 2018: 8 · 2016: 3 · 2015: 1 · 2014: 4 · 2013: 5 · 2012: 8
- FWCI
- 1.70
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience Letters (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Aging (AG-02219, P50AG005138, 5-P50-AG05138-02, P01AG002219)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Keywords
- long-term potentiation, cholinergic stimulation, carbachol, acetylcholine, hippocampal CA1, tetanic stimulation, presynaptic depression, postsynaptic mechanisms, memory
- MeSH terms
- Animals, Atropine, Carbachol, Electric Stimulation, Hippocampus, Male, Parasympathomimetics, Rats, Inbred Strains, Rats
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