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.
“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
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 · see citing works
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 4,033 · see citing works
Morris, R. G. M., Anderson, E., Lynch, G. S., & Baudry, M. (1986) · Nature · doi:10.1038/319774a0 · Cited by 3,640 · see citing works
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 · see citing works
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 2,906 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Gustafsson, B., Wigstrom, H., Abraham, W., & Huang, Y. (1987) · The Journal of Neuroscience · doi:10.1523/jneurosci.07-03-00774.1987 · Cited by 583 · see citing works
Harris, E. W., & Cotman, C. W. (1986) · Neuroscience Letters · doi:10.1016/0304-3940(86)90451-9 · Cited by 540 · see citing works
The current excitement in long term potentiation
Nicoll, R. A., Kauer, J. A., & Malenka, R. C. (1988) · Neuron · doi:10.1016/0896-6273(88)90193-6 · Cited by 535 · see citing works
Voltage clamp analysis of cholinergic action in the hippocampus
Madison, D. V., Lancaster, B., & Nicoll, R. A. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-03-00733.1987 · Cited by 503 · see citing works
Long-Term Synaptic Potentiation
Brown, T. H., Chapman, P. F., Kairiss, E. W., & Keenan, C. L. (1988) · Science · doi:10.1126/science.2903551 · Cited by 415 · see citing works
Andersen, P. N., Sundberg, S. H., Sveen, O., Swann, J. W., & Wigström, H. (1980) · The Journal of Physiology · doi:10.1113/jphysiol.1980.sp013256 · Cited by 366 · see citing works
Presynaptic inhibitory effect of acetylcholine in the hippocampus
Valentino, R. J., & Dingledine, R. J. (1981) · Journal of Neuroscience · doi:10.1523/jneurosci.01-07-00784.1981 · Cited by 340 · see citing works
Low, W. C., Lewis, P. R., Bunch, S., Dunnett, S. B., Thomas, S. R., Iversen, S. D., Björklund, A., & Stenevi, U. (1982) · Nature · doi:10.1038/300260a0 · Cited by 316 · see citing works
Ionic mechanisms of cholinergic excitation in mammalian hippocampal pyramidal cells
Benardo, L. S., & Prince, D. A. (1982) · Brain Research · doi:10.1016/0006-8993(82)90067-1 · Cited by 246 · see citing works
Presynaptic inhibitory action of acetylcholine in area CA1 of the hippocampus
Hounsgaard, J. (1978) · Experimental Neurology · doi:10.1016/0014-4886(78)90284-4 · Cited by 221 · see citing works
Krnjević, K., & Ropert, N. (1982) · Neuroscience · doi:10.1016/0306-4522(82)90128-2 · Cited by 161 · see citing works
Muscarinic Depression of Long-Term Potentiation in CA3 Hippocampal Neurons
Williams, S., & Johnston, D. (1988) · Science · doi:10.1126/science.2845578 · Cited by 143 · see citing works
Benson, D. M., Blitzer, R. D., & Landau, E. M. (1988) · The Journal of Physiology · doi:10.1113/jphysiol.1988.sp017301 · Cited by 119 · see citing works
Self-citationSantucci, A. C., Kanof, P. D., & Haroutunian, V. H. (1989) · Psychopharmacology · doi:10.1007/bf00634455 · Cited by 63 · see citing works
Ineffectiveness of organic calcium channel blockers in antagonizing long-term potentiation
Taube, J. S., & Schwartzkroin, P. A. (1986) · Brain Research · doi:10.1016/0006-8993(86)90781-x · Cited by 43 · see citing works
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The cholinergic system in the pathophysiology and treatment of Alzheimer’s disease
Hampel, H., Mesulam, M.-M., Cuello, A. C., Farlow, M. R., Giacobini, E., Grossberg, G. T., Khachaturian, A. S., Vergallo, A., Cavedo, E., Snyder, P. J., et al. (2018) · Brain · doi:10.1093/brain/awy132 · Cited by 1,918 · see citing works
Modes and models of forebrain cholinergic neuromodulation of cognition
Hasselmo, M. E., & Sarter, M. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.104 · Cited by 733 · see citing works
Neuromodulation and cortical function: modeling the physiological basis of behavior
Hasselmo, M. E. (1995) · Behavioural Brain Research · doi:10.1016/0166-4328(94)00113-t · Cited by 552 · see citing works
Hasselmo, M. E., & McGaughy, J. (2004) · Progress in Brain Research · doi:10.1016/s0079-6123(03)45015-2 · Cited by 525 · see citing works
Hasselmo, M., & Schnell, E. (1994) · The Journal of Neuroscience · doi:10.1523/jneurosci.14-06-03898.1994 · Cited by 466 · see citing works
Neurobiological after-effects of non-invasive brain stimulation
Cirillo, G., Di Pino, G., Capone, F., Ranieri, F., Florio, L., Todisco, V., Tedeschi, G., Funke, K., & Di Lazzaro, V. (2017) · Brain Stimulation · doi:10.1016/j.brs.2016.11.009 · Cited by 446 · see citing works
Hasselmo, M. E., & Bower, J. M. (1993) · Trends in Neurosciences · doi:10.1016/0166-2236(93)90159-j · Cited by 429 · see citing works
Levey, A. I., Edmunds, S. M., Koliatsos, V. E., Wiley, R. G., & Heilman, C. J. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-05-04077.1995 · Cited by 423 · see citing works
Sharp, P. E., Blair, H. T., & Brown, M. A., Sr. (1996) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:6 · Cited by 64 · see citing works
Hasselmo, M. E., & Wyble, B. (1997) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00048-x · Cited by 337 · see citing works
Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine
Kirkwood, A., Rozas, C., Kirkwood, J., Perez, F., & Bear, M. F. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-05-01599.1999 · Cited by 315 · see citing works
alpha-Bungarotoxin-sensitive hippocampal nicotinic receptor channel has a high calcium permeability
Castro, N. G., & Albuquerque, E. X. (1995) · Biophysical Journal · doi:10.1016/s0006-3495(95)80213-4 · Cited by 273 · see citing works
The role of acetylcholine in cortical synaptic plasticity
Rasmusson, D. D. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00259-x · Cited by 267 · see citing works
Muscarinic cholinergic influences in memory consolidation
Power, A. (2003) · Neurobiology of Learning and Memory · doi:10.1016/s1074-7427(03)00086-8 · Cited by 261 · see citing works
van der Zee, E. A., & Luiten, P. G. M. (1999) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00092-6 · Cited by 261 · see citing works
The cholinergic system and hippocampal plasticity
Drever, B. D., Riedel, G., & Platt, B. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.11.037 · Cited by 240 · see citing works
Hasselmo, M. E., & Barkai, E. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-10-06592.1995 · Cited by 215 · see citing works
Focusing Effect of Acetylcholine on Neuroplasticity in the Human Motor Cortex
Kuo, M., Grosch, J., Fregni, F., Paulus, W., & Nitsche, M. A. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4104-07.2007 · Cited by 212 · see citing works
Specific basal forebrain-cortical cholinergic circuits coordinate cognitive operations
Záborszky, L., Gombkoto, P., Varsanyi, P., Gielow, M. R., Poe, G., Role, L. W., Ananth, M., Rajebhosale, P., Talmage, D. A., Hasselmo, M. E., et al. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.1676-18.2018 · Cited by 202 · see citing works
Nitsche, M. A., Müller‐Dahlhaus, F., Paulus, W., & Ziemann, U. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.232975 · Cited by 199 · see citing works
Changes in Acetylcholine Extracellular Levels During Cognitive Processes: Table 1.Preprint
Pepeu, G., & Giovannini, M. G. (2004) · Learning & Memory · doi:10.1101/lm.68104 · Cited by 193 · see citing works
Cholinergic modulation of cognitive processing: insights drawn from computational models
Newman, E. L., Gupta, K., Climer, J. R., Monaghan, C. K., & Hasselmo, M. E. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00024 · Cited by 185 · see citing works
NGF Is Essential for Hippocampal Plasticity and Learning
Conner, J. M., Franks, K. M., Titterness, A. K., Russell, K., Merrill, D. A., Christie, B. R., Sejnowski, T. J., & Tuszynski, M. H. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.2594-09.2009 · Cited by 189 · see citing works
Gąsiorowska, A., Wydrych, M., Drapich, P., Zadrożny, M., Steczkowska, M., Niewiadomski, W., & Niewiadomska, G. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.654931 · Cited by 192 · see citing works
Cholinergic Inhibition of Neocortical Pyramidal Neurons
Gulledge, A. T., & Stuart, G. J. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2697-05.2005 · Cited by 182 · see citing works
Pyapali, G. K., Turner, D. A., Williams, C. L., Meck, W. H., & Swartzwelder, H. S. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.4.1790 · Cited by 169 · see citing works
Muscarinic receptors mediating depression and long‐term potentiation in rat hippocampus.
Auerbach, J. M., & Segal, M. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021323 · Cited by 168 · see citing works
Kumar, A. (2011) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2011.00007 · Cited by 169 · see citing works
Atri, A., Sherman, S. J., Norman, K. A., Kirchhoff, B. A., Nicolas, M. M., Greicius, M. D., Cramer, S. C., Breiter, H. C., Hasselmo, M. E., & Stern, C. E. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.1.223 · Cited by 162 · see citing works
Tsubokawa, H., & Ross, W. N. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-15-05782.1997 · Cited by 157 · see citing works
What do grid cells contribute to place cell firing?
Bush, D., Barry, C., & Burgess, N. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2013.12.003 · Cited by 156 · see citing works
Watabe, A. M., Zaki, P. A., & O’Dell, T. J. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-16-05924.2000 · Cited by 147 · see citing works
Meeter, M., Murre, J. M. J., & Talamini, L. M. (2004) · Hippocampus · doi:10.1002/hipo.10214 · Cited by 138 · see citing works
Newman, E. L., Gillet, S. N., Climer, J. R., & Hasselmo, M. E. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2586-13.2013 · Cited by 137 · see citing works
Cholinergic Activity Enhances Hippocampal Long-Term Potentiation in CA1 during Walking in Rats
Leung, L.-W. S., Bixia Shen, A., Rajakumar, N., & Ma, J. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-28-09297.2003 · Cited by 129 · see citing works
Lindefors, N., Ernfors, P., Falkenberg, T., & Persson, H. (1992) · Experimental Brain Research · doi:10.1007/bf02259130 · Cited by 121 · see citing works
Hanania, T., Hillman, G. R., & Johnson, K. M. (1999) · Synapse · doi:10.1002/(sici)1098-2396(19990301)31:3 · Cited by 46 · see citing works
Molecular Mechanisms of Long-Term Potentiation in the Insular CortexIn Vivo
Jones, M. W., French, P. J., Bliss, T. V. P., & Rosenblum, K. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-21-j0002.1999 · Cited by 116 · see citing works
Lin, Y., Min, M., Chiu, T., & Yang, H. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-10-04173.2003 · Cited by 116 · see citing works
Muscarinic receptors involved in hippocampal plasticity
Segal, M., & Auerbach, J. M. (1997) · Life Sciences · doi:10.1016/s0024-3205(97)00051-9 · Cited by 107 · see citing works
Matthies, H., Becker, A., Schröeder, H., Kraus, J., Höllt, V., & Krug, M. (1997) · Neuroreport · doi:10.1097/00001756-199711100-00023 · Cited by 106 · see citing works
Matsumoto, M., Togashi, H., Mori, K., Ueno, K.-I., Ohashi, S., Kojima, T., & Yoshioka, M. (2001) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)38802-0 · Cited by 104 · see citing works
Berkeley, J. L., Gomeza, J., Wess, J., Hamilton, S. E., Nathanson, N. M., & Levey, A. I. (2001) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.2001.1042 · Cited by 98 · see citing works
Gutierres, J. M., Carvalho, F. B., Schetinger, M. R. C., Agostinho, P. M., Marisco, P. C., Vieira, J. M., da Rosa, M. M., Bohnert, C., Rubin, M. A., Morsch, V. M., et al. (2013) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2013.12.006 · Cited by 97 · see citing works
New perspectives on the basal forebrain cholinergic system in Alzheimer’s disease
Berry, A. S., & Harrison, T. M. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105192 · Cited by 97 · see citing works
A specific role for septohippocampal acetylcholine in memory?
Easton, A., Douchamps, V., Eacott, M. J., & Lever, C. (2012) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2012.07.022 · Cited by 99 · see citing works
Shin, J., Kong, C., Lee, J. J., Choi, B., Sim, J., Koh, C., Park, M., Na, Y. C., Suh, S., Chang, W., et al. (2019) · Alzheimer's Research & Therapy · doi:10.1186/s13195-019-0569-x · Cited by 82 · see citing works
Müller, W. S., & Connor, J. A. (1991) · Neuron · doi:10.1016/0896-6273(91)90230-w · Cited by 92 · see citing works
Cholinergic Agonist Carbachol Enables Associative Long-Term Potentiation in Piriform Cortex Slices
Patil, M. M., Linster, C., Lubenov, E., & Hasselmo, M. E. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.5.2467 · Cited by 91 · see citing works
Massey, P. V., Bhabra, G., Cho, K., Brown, M. W., & Bashir, Z. I. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01631.x · Cited by 90 · see citing works
Histaminergic modulation of synaptic plasticity in area CA1 of rat hippocampal slices
Brown, R. E., Fedorov, N. B., Haas, H. I., & Reymann, K. (1995) · Neuropharmacology · doi:10.1016/0028-3908(94)00138-i · Cited by 90 · see citing works
Endocannabinoids restrict hippocampal long-term potentiation via CB1
Slanina, K. A., Roberto, M., & Schweitzer, P. (2005) · Neuropharmacology · doi:10.1016/j.neuropharm.2005.04.021 · Cited by 89 · see citing works
Possible role of acetylcholine in regulating spatial novelty effects on theta rhythm and grid cells
Barry, C., Heys, J. G., & Hasselmo, M. E. (2012) · Frontiers in Neural Circuits · doi:10.3389/fncir.2012.00005 · Cited by 79 · see citing works
Hippocampal representations as a function of time, subregion, and brain state
Duncan, K. D., & Schlichting, M. L. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.03.006 · Cited by 78 · see citing works
Le, X. T., Pham, H. T. N., Do, P. T., Fujiwara, H., Tanaka, K., Li, F., Van Nguyen, T., Nguyen, K. M., & Matsumoto, K. (2013) · Neurochemical Research · doi:10.1007/s11064-013-1129-6 · Cited by 79 · see citing works
Acetylcholine and the complex interdependence of memory and attention
Decker, A. L., & Duncan, K. D. (2020) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2020.01.013 · Cited by 78 · see citing works
Pennartz, C. M. A. (1995) · Brain Research Reviews · doi:10.1016/0165-0173(95)00014-3 · Cited by 75 · see citing works
Memory processes during sleep: beyond the standard consolidation theory
Axmacher, N., Draguhn, A., Elger, C. E., & Fell, J. (2009) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-009-0019-1 · Cited by 73 · see citing works
LTD: Many means to how many ends?
Kerr, D. S., & Abraham, W. C. (1996) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:1 · Cited by 7 · see citing works
Bergado, J. A., Frey, S., Lopez‐Rojas, J., Almaguer‐Melian, W., & Frey, J. U. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.05.003 · Cited by 66 · see citing works
Shiozaki, K., Iseki, E., Hino, H., & Kosaka, K. (2001) · Journal of the Neurological Sciences · doi:10.1016/s0022-510x(01)00638-4 · Cited by 60 · see citing works
A model for experience-dependent changes in the responses of inferotemporal neurons
Sohal, V. S., & Hasselmo, M. E. (2000) · Network Computation in Neural Systems · doi:10.1088/0954-898x_11_3_301 · Cited by 60 · see citing works
Sobreviela, T., Pagcatipunan, M., Kroin, J. S., & Mufson, E. J. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19961118)375:3 · Cited by 69 · see citing works
Muscarinic receptor-mediated induction of Fos protein in rat brain
Hughes, P. E., & Dragunow, M. (1993) · Neuroscience Letters · doi:10.1016/0304-3940(93)90122-2 · Cited by 60 · see citing works
Effects of acetylcholine on neuronal properties in entorhinal cortex
Heys, J. G., Schultheiss, N. W., Shay, C. F., Tsuno, Y., & Hasselmo, M. E. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00032 · Cited by 56 · see citing works
Age-related decline in cholinergic synaptic transmission in hippocampus
Taylor, L., & Griffith, W. H. (1993) · Neurobiology of Aging · doi:10.1016/0197-4580(93)90110-w · Cited by 59 · see citing works
Bourgin, P., Lebrand, C., Escourrou, P., Gaultier, C., Franc, B., Hamon, M., & Adrien, J. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00455-1 · Cited by 59 · see citing works
The role of cortical cholinergic pre- and post-synaptic receptors in taste memory formation
Ramı́rez-Lugo, L., Miranda, M. I., Escobar, M. L., Espinosa, E., & Bermúdez‐Rattoni, F. (2003) · Neurobiology of Learning and Memory · doi:10.1016/s1074-7427(02)00038-2 · Cited by 55 · see citing works
Caruana, D. A., Warburton, E. C., & Bashir, Z. I. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4719-11.2011 · Cited by 55 · see citing works
Yun, S. H., Cheong, M. Y., Mook‐Jung, I., Huh, K. H., Lee, C.-J., & Jung, M. W. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00108-1 · Cited by 54 · see citing works
Wang, Y., Greig, N. H., Yu, Q.-S., & Mattson, M. P. (2008) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.10.009 · Cited by 53 · see citing works
Differential Effects of PACAP-38 on Synaptic Responses in Rat Hippocampal CA1 RegionPreprint
Roberto, M., Scuri, R., & Brunelli, M. (2001) · Learning & Memory · doi:10.1101/lm.40501 · Cited by 55 · see citing works
Hess, G., & Donoghue, J. P. (1999) · Experimental Brain Research · doi:10.1007/s002210050797 · Cited by 54 · see citing works
Linster, C., Maloney, M. E., Patil, M. M., & Hasselmo, M. E. (2003) · Neurobiology of Learning and Memory · doi:10.1016/s1074-7427(03)00078-9 · Cited by 53 · see citing works
PACAP-38 Enhances Excitatory Synaptic Transmission in the Rat Hippocampal CA1 RegionPreprint
Roberto, M., & Brunelli, M. (2000) · Learning & Memory · doi:10.1101/lm.34200 · Cited by 53 · see citing works
Xing, T., Chen, L., Tao, Y., Wang, M., Chen, J., & Ruan, D. (2009) · Toxicological Sciences · doi:10.1093/toxsci/kfp114 · Cited by 52 · see citing works
Kremin, T., GERBER, D., Giocomo, L. M., Huang, S., Tonegawa, S., & Hasselmo, M. E. (2005) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.09.005 · Cited by 52 · see citing works
Metrifonate improves associative learning and retention in aging rabbits.
Kronforst-Collins, M. A., Moriearty, P. L., Schmidt, B. H., & Disterhoft, J. F. (1997) · Behavioral Neuroscience · doi:10.1037//0735-7044.111.5.1031 · Cited by 52 · see citing works
Pesavento, E., Capsoni, S., Domenici, L., & Cattaneo, A. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.01937.x · Cited by 52 · see citing works
Karashima, A., Nakao, M., Katayama, N., & Honda, K. (2005) · Brain Research · doi:10.1016/j.brainres.2005.05.055 · Cited by 51 · see citing works
Rouse, S. T., Gilmor, M. L., & Levey, A. I. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00681-7 · Cited by 50 · see citing works
Sakurai, E., Maeda, T., Kaneko, S., Akaike, A., & Satoh, M. (1996) · Neuroscience Letters · doi:10.1016/0304-3940(96)12772-5 · Cited by 49 · see citing works
Cholinergic modulation of hippocampal CA1 basal-dendritic long-term potentiation
Doralp, S., & Leung, L.-W. S. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.05.013 · Cited by 47 · see citing works
Acetylcholine and associative memory in the piriform cortex
Barkai, E., & Hasselmo, M. E. (1997) · Molecular Neurobiology · doi:10.1007/bf02740613 · Cited by 45 · see citing works
Taube, J. S., & Muller, R. U. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1998)8:2 · Cited by 119 · see citing works
Kremin, T., & Hasselmo, M. E. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.07.007 · Cited by 43 · see citing works
Adams, S. V., Winterer, J., & Müller, W. S. (2004) · Hippocampus · doi:10.1002/hipo.10197 · Cited by 44 · see citing works
Parfitt, G. M., Campos, R. C., Barbosa, Â. K., Koth, A. P., & Barros, D. M. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.12.001 · Cited by 43 · see citing works
Lopes Aguiar, C., Romcy-Pereira, R. N., Escorsim Szawka, R., Galvis-Alonso, O. Y., Anselmo-Franci, J. A., & Pereira Leite, J. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.02.040 · Cited by 42 · see citing works
Navakkode, S., & Körte, M. (2011) · Hippocampus · doi:10.1002/hipo.20902 · Cited by 42 · see citing works
Matthies, H., Schröeder, H., Becker, A., Loh, H. H., Höllt, V., & Krug, M. (2000) · Neuropharmacology · doi:10.1016/s0028-3908(99)00203-8 · Cited by 40 · see citing works
Strategies That Support Declining Cholinergic Neurotransmission in Alzheimer’s Disease Patients
Sirviö, J. (1999) · Gerontology · doi:10.1159/000052759 · Cited by 40 · see citing works
Dickinson-Anson, H., Aubert, I., Gage, F. H., & Fisher, L. J. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00543-5 · Cited by 40 · see citing works
Shimoshige, Y., Maeda, T., Kaneko, S., Akaike, A., & Satoh, M. (1997) · Neuroscience Research · doi:10.1016/s0168-0102(96)01147-9 · Cited by 39 · see citing works
Adaptive control of synaptic plasticity integrates micro- and macroscopic network function
Scott, D. N., & Frank, M. J. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01374-6 · Cited by 39 · see citing works
Cholinergic plasticity in the hippocampus
Colgin, L. L., Kubota, D., & LYNCH, G. S. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0530289100 · Cited by 37 · see citing works
Hughes, P. E., & Dragunow, M. (1994) · Molecular Brain Research · doi:10.1016/0169-328x(94)90129-5 · Cited by 35 · see citing works
Natsume, K., & Kometani, K. (1997) · Neuroscience Research · doi:10.1016/s0168-0102(97)01167-x · Cited by 34 · see citing works
Alteration of cardiovascular and neuronal function in M1 knockout mice
Hamilton, S. E., Hardouin, S. N., Anagnostaras, S., Murphy, G. G., Richmond, K. N., Silva, A. J., Feigl, E. O., & Nathanson, N. M. (2001) · Life Sciences · doi:10.1016/s0024-3205(01)01043-8 · Cited by 34 · see citing works
Cellular Mechanisms Of Long-Term Potentiation: Late Maintenance
Frey, U. (1997) · Advances in psychology · doi:10.1016/s0166-4115(97)80092-1 · Cited by 33 · see citing works
- 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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