Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5
Abstract
Recent work has shown that the hippocampus contains a class of receptors for the excitatory amino acid glutamate that are activated by N-methyl-D-aspartate (NMDA) and that exhibit a peculiar dependency on membrane voltage in becoming active only on depolarization. Blockade of these sites with the drug aminophosphonovaleric acid (AP5) does not detectably affect synaptic transmission in the hippocampus, but prevents the induction of hippocampal long-term potentiation (LTP) following brief high-frequency stimulation. We now report that chronic intraventricular infusion of D,L-AP5 causes a selective impairment of place learning, which is highly sensitive to hippocampal damage, without affecting visual discrimination learning, which is not. The L-isomer of AP5 did not produce behavioural effects. AP5 treatment also suppressed LTP in vivo. These results suggest that NMDA receptors are involved in spatial learning, and add support to the hypothesis that LTP is involved in some, but not all, forms of learning.
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Rats that received infusion of AP5 into the hippocampus were deficient in performing a spatial memory task in the water maze.
“Morris et al. (1986) were the first to show that rats that received infusion of AP5 into the hippocampus were deficient in performing a spatial memory task in which the animals are required to form multiple spatial relations between a hidden platform in a circular pool (known as a water maze) and visible objects in the surrounding environment and swim to the platform toescape from the water.”
From The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. (1996) · cites this paper as Morris et al. (1986)
NMDAR-dependent LTP has been most tightly associated with intact animal behavioral memory.
“Additionally, NMDAR-dependent LTP has been most tightly associated with intact animal behavioral memory (19, 43–46).”
From Synaptic memory and CaMKII (2023) · cites this paper as [45]
Although there is considerable evidence linking LTP to behavior memory, more evidence is needed to solidify this link.
“However, although there is considerable evidence linking LTP to behavior memory (45, 441–443), more evidence is needed to solidify this link.”
From Synaptic memory and CaMKII (2023) · cites this paper as [45]
Genetically-modified mouse models of NMDA hypofunction, including the Grin1 hypomorphic mouse and the Srr knockout mouse, revealed schizophrenia-relevant phenotypes and neurochemical deficits.
“Genetically-modified mouse models of NMDA hypofunctionincluding the Grin1 hypomorphic mouse 25 and the Srr knockout mouse 26 -have also revealed schizophrenia-relevant phenotypes and neurochemical deficits.”
From Linking early-life NMDAR hypofunction and oxidative stress in schizophrenia pathogenesis (2016) · cites this paper as [26]
Cites
(1978) · UA Campus Repository (The University of Arizona) · Cited by 8,010 · see citing works
Bliss, T. V. P., & Gardner-Medwin, A. R. (1973) · The Journal of Physiology · doi:10.1113/jphysiol.1973.sp010274 · Cited by 7,460 · see citing works
Developments of a water-maze procedure for studying spatial learning in the rat
Morris, R. (1984) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(84)90007-4 · Cited by 7,180 · see citing works
Self-citationPlace navigation impaired in rats with hippocampal lesions
Morris, R. G. M., Garrud, P., Rawlins, J. N. P., & O'Keefe, J. (1982) · Nature · doi:10.1038/297681a0 · Cited by 6,340 · see citing works
Self-citationThe hippocampus as a cognitive map
Passingham, R. E. (1979) · Neuroscience · doi:10.1016/0306-4522(79)90015-0 · Cited by 5,128 · 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
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
Excitatory Amino Acid Transmitters
Watkins, J. C., & Evans, R. H. (1981) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pa.21.040181.001121 · Cited by 2,497 · see citing works
Neurobiology of the hippocampus
Rawlins, J. N. P. (1984) · Neuroscience · doi:10.1016/0306-4522(84)90113-1 · Cited by 1,100 · see citing works
The Biochemistry of Memory: A New and Specific Hypothesis
LYNCH, G. S., & Baudry, M. (1984) · Science · doi:10.1126/science.6144182 · Cited by 1,045 · see citing works
Self-citationLong-term potentiation in the hippocampus involves activation of N-methyl-D-aspartate receptors
Harris, E. W., Ganong, A. H., & Cotman, C. W. (1984) · Brain Research · doi:10.1016/0006-8993(84)90275-0 · Cited by 903 · see citing works
Anticonvulsant Action of Excitatory Amino Acid Antagonists
Croucher, M. J., Collins, J. F., & Meldrum, B. S. (1982) · Science · doi:10.1126/science.7079744 · Cited by 695 · see citing works
Sutherland, R. J., Whishaw, I. Q., & Kolb, B. (1983) · Behavioural Brain Research · doi:10.1016/0166-4328(83)90188-2 · Cited by 592 · see citing works
Possible Therapeutic Applications of Antagonists of Excitatory Amino acid Neurotransmitters
Meldrum, B. S. (1985) · Clinical Science · doi:10.1042/cs0680113 · Cited by 554 · see citing works
Neurobiology of the hippocampus
Seifert, W. E. (1983) · Academic Press eBooks · Cited by 530 · see citing works
Kolb, B. E., Sutherland, R. J., & Whishaw, I. Q. (1983) · Behavioral Neuroscience · doi:10.1037//0735-7044.97.1.13 · Cited by 432 · see citing works
The antagonism of amino acid‐induced excitations of rat hippocampal CA1 neurones in vitro.
Collingridge, G. L., Kehl, S. J., & McLennan, H. (1983) · The Journal of Physiology · doi:10.1113/jphysiol.1983.sp014477 · Cited by 370 · see citing works
Kolb, B. E., Sutherland, R. J., & Whishaw, I. Q. (1983) · Behavioral Neuroscience · doi:10.1037/0735-7044.97.1.13 · Cited by 333 · see citing works
The effects of central catecholamine depletions on spatial learning in rats
Hagan, J. J. (1983) · Behavioural Brain Research · doi:10.1016/0166-4328(83)90015-3 · Cited by 104 · see citing works
Possible Cellular Basis for Prolonged Changes of Synaptic Efficiency – A Simple Case of Learning
Andersen, P. N. (1983) · Progress in brain research · doi:10.1016/s0079-6123(08)60044-8 · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
McClelland, J. L., McNaughton, B. L., & O'Reilly, R. C. (1995) · Psychological Review · doi:10.1037/0033-295x.102.3.419 · Cited by 5,256 · see citing works
The molecular biology of memory storage: a dialogue between genes and synapses
Kandel, E. R. (2001) · Science · doi:10.1126/science.1067020 · Cited by 3,917 · see citing works
Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus
van Praag, H., Kempermann, G., & Gage, F. H. (1999) · Nature Neuroscience · doi:10.1038/6368 · Cited by 3,880 · see citing works
Krystal, J. H. (1994) · Archives of General Psychiatry · doi:10.1001/archpsyc.1994.03950030035004 · Cited by 3,330 · see citing works
Meaney, M. J. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1161 · Cited by 2,708 · see citing works
Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning
Buzsáki, G. (2015) · Hippocampus · doi:10.1002/hipo.22488 · Cited by 1,759 · see citing works
Intracellular amyloid-β in Alzheimer's disease
LaFerla, F. M., Green, K. N., & Oddo, S. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2168 · Cited by 1,942 · see citing works
The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory.
Tsien, J. Z., Huerta, P. T., & Tonegawa, S. (1996) · Cell · doi:10.1016/s0092-8674(00)81827-9 · Cited by 1,782 · see citing works
Stress, memory and the amygdala
Roozendaal, B., McEwen, B. S., & Chattarji, S. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2651 · Cited by 1,760 · see citing works
Two-stage model of memory trace formation: A role for “noisy” brain states
Buzsáki, G. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90423-5 · Cited by 1,709 · see citing works
The stressed hippocampus, synaptic plasticity and lost memories
Kim, J. J., & Diamond, D. M. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn849 · Cited by 1,543 · see citing works
Life and Death of Neurons in the Aging Brain
Morrison, J. H., & Hof, P. R. (1997) · Science · doi:10.1126/science.278.5337.412 · Cited by 1,344 · see citing works
Subregion- and Cell Type–Restricted Gene Knockout in Mouse Brain
Tsien, J. Z., Chen, D. F., Gerber, D., Tom, C., Mercer, E. H., Anderson, D. J., Mayford, M., Kandel, E. R., & Tonegawa, S. (1996) · Cell · doi:10.1016/s0092-8674(00)81826-7 · Cited by 1,280 · see citing works
GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus
Freund, T. F., & Antal, M. (1988) · Nature · doi:10.1038/336170a0 · Cited by 1,283 · see citing works
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 · see citing works
Self-citationMaternal care, hippocampal synaptogenesis and cognitive development in rats
Liu, D., Diorio, J., Day, J. C., Francis, D. D., & Meaney, M. J. (2000) · Nature Neuroscience · doi:10.1038/77702 · Cited by 1,195 · see citing works
The Molecular and Systems Biology of Memory
Kandel, E. R., Dudai, Y., & Mayford, M. R. (2014) · Cell · doi:10.1016/j.cell.2014.03.001 · Cited by 1,134 · see citing works
Engineering a memory with LTD and LTP
Nabavi, S., Fox, R., Proulx, C. D., Lin, J. Y., Tsien, R. Y., & Malinow, R. (2014) · Nature · doi:10.1038/nature13294 · Cited by 980 · see citing works
The hippocampus—what does it do?
Eichenbaum, H., Otto, T., & Cohen, N. J. (1992) · Behavioral and Neural Biology · doi:10.1016/0163-1047(92)90724-i · Cited by 867 · see citing works
The reorganization and reactivation of hippocampal maps predict spatial memory performance
Dupret, D., O'Neill, J., Pleydell-Bouverie, B., & Csicsvari, J. (2010) · Nature Neuroscience · doi:10.1038/nn.2599 · Cited by 769 · see citing works
Miserendino, M. J. D., Sananes, C. B., Melia, K. R., & Davis, M. (1990) · Nature · doi:10.1038/345716a0 · Cited by 824 · see citing works
Functional antagonists at the NMDA receptor complex exhibit antidepressant actions
Trullas, R., & Skolnick, P. (1990) · European Journal of Pharmacology · doi:10.1016/0014-2999(90)90204-j · Cited by 785 · see citing works
Epigenetic mechanisms in memory formation
Levenson, J. M., & Sweatt, J. D. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1604 · Cited by 767 · see citing works
Stress effects on memory: An update and integration
Schwabe, L., Joëls, M., Roozendaal, B., Wolf, O. T., & Oitzl, M. S. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.07.002 · Cited by 714 · see citing works
Carlén, M., Meletis, K., Siegle, J. H., Cardin, J. A., Futai, K., Vierling-Claassen, D., Rühlmann, C., Jones, S. R., Deisseroth, K., Sheng, M., et al. (2012) · Molecular Psychiatry · doi:10.1038/mp.2011.31 · Cited by 669 · see citing works
Hippocampal synaptic plasticity, spatial memory and anxiety
Bannerman, D. M., Sprengel, R., Sanderson, D. J., McHugh, S. B., Rawlins, J. N. P., Monyer, H., & Seeburg, P. H. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3677 · Cited by 688 · see citing works
The Restless Engram: Consolidations Never End
Dudai, Y. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150500 · Cited by 644 · see citing works
Effects of Moderate Alcohol Consumption on the Central Nervous System*
Eckardt, M. J., File, S. E., Gessa, G. L., Grant, K. A., Guerri, C., Hoffman, P. L., Kalant, H., Koob, G. F., Li, T., & Tabakoff, B. (1998) · Alcoholism: Clinical and Experimental Research · doi:10.1111/j.1530-0277.1998.tb03695.x · Cited by 622 · see citing works
NMDA receptors, place cells and hippocampal spatial memory
Nakazawa, K., McHugh, T. J., Wilson, M. A., & Tonegawa, S. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1385 · Cited by 619 · see citing works
Aiba, A. (1994) · Cell · doi:10.1016/0092-8674(94)90204-6 · Cited by 614 · see citing works
Insel, T. R., Miller, L. P., & Gelhard, R. E. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90117-m · Cited by 529 · see citing works
Korotkova, T., Fuchs, E. C., Ponomarenko, A., von Engelhardt, J., & Monyer, H. (2010) · Neuron · doi:10.1016/j.neuron.2010.09.017 · Cited by 480 · see citing works
Impaired Spatial Learning after Saturation of Long-Term Potentiation
Moser, E. I., Krobert, K. A., Moser, M.-B., & Morris, R. G. M. (1998) · Science · doi:10.1126/science.281.5385.2038 · Cited by 505 · see citing works
Self-citationTargeting glutamate signalling in depression: progress and prospects
Murrough, J. W., Abdallah, C. G., & Mathew, S. J. (2017) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2017.16 · Cited by 482 · see citing works
Reconsolidation and Extinction of Conditioned Fear: Inhibition and Potentiation
Lee, J. L. C., Milton, A. L., & Everitt, B. J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.2466-06.2006 · Cited by 479 · see citing works
Pharmacology and behavioral pharmacology of the mesocortical dopamine system
Tzschentke, T. M. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00033-2 · Cited by 481 · see citing works
On the delay-dependent involvement of the hippocampus in object recognition memory
HAMMOND, R. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.03.005 · Cited by 476 · see citing works
Sleep states and memory processes
Smith, C. (1995) · Behavioural Brain Research · doi:10.1016/0166-4328(95)00024-n · Cited by 473 · see citing works
Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus
Shors, T. J., Seib, T. B., Levine, S., & Thompson, R. F. (1989) · Science · doi:10.1126/science.2704997 · Cited by 458 · see citing works
Izquierdo, I., Furini, C. R. G., & Myskiw, J. C. (2016) · Physiological Reviews · doi:10.1152/physrev.00018.2015 · Cited by 453 · see citing works
Impairment of long-term potentiation and spatial memory in leptin receptor-deficient rodents
Li, X.-L., Aou, S., Oomura, Y., Hori, N., Fukunaga, K., & Hori, T. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00162-8 · Cited by 440 · see citing works
Foster, D. J. (2017) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-072116-031538 · Cited by 375 · see citing works
Murphy, K. P. S. J., Carter, R. J., Lione, L. A., Mangiarini, L., Mahal, A., Bates, G. P., Dunnett, S. B., & Morton, A. J. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-13-05115.2000 · Cited by 398 · see citing works
General anaesthetic actions on ligand-gated ion channels
Krasowski, M. D., & Harrison, N. L. (1999) · Cellular and Molecular Life Sciences (CMLS) · doi:10.1007/s000180050371 · Cited by 384 · see citing works
Altered behavior and long-term potentiation in type I adenylyl cyclase mutant mice.
Wu, Z. L., Thomas, S. A., Villacres, E. C., Xia, Z., Simmons, M. L., Chavkin, C., Palmiter, R. D., & Storm, D. R. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.1.220 · Cited by 370 · see citing works
A Model of Spatial Map Formation in the Hippocampus of the Rat
Blum, K. I., & Abbott, L. F. (1996) · Neural Computation · doi:10.1162/neco.1996.8.1.85 · Cited by 352 · see citing works
Meningeal γδ T cell-derived IL-17 controls synaptic plasticity and short-term memory
Ribeiro, M., Brigas, H. C., Temido-Ferreira, M., Pousinha, P. A., Regen, T., Santa, C., Coelho, J. E., Marques-Morgado, I., Valente, C. A., Omenetti, S., et al. (2019) · Science Immunology · doi:10.1126/sciimmunol.aay5199 · Cited by 335 · see citing works
Age-Dependent Impairment of Cognitive and Synaptic Function in the htau Mouse Model of Tau Pathology
Polydoro, M., Acker, C. M., Duff, K., Castillo, P. E., & Davies, P. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1065-09.2009 · Cited by 329 · see citing works
Pettit, D. L., Perlman, S., & Malinow, R. (1994) · Science · doi:10.1126/science.7997883 · Cited by 329 · see citing works
Differential Effects of Ethanol on Memory in Adolescent and Adult Rats
Markwiese, B. J., Acheson, S. K., Levin, E. D., Wilson, W. A., & Swartzwelder, H. S. (1998) · Alcoholism: Clinical and Experimental Research · doi:10.1111/j.1530-0277.1998.tb03668.x · Cited by 320 · see citing works
Kreutzmann, J. C., Havekes, R., Abel, T., & Meerlo, P. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.04.053 · Cited by 309 · see citing works
Linking early-life NMDAR hypofunction and oxidative stress in schizophrenia pathogenesis
Hardingham, G. E., & Do, K. Q. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2015.19 · Cited by 304 · see citing works
NMDA receptors and memory encoding
Morris, R. G. M. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.04.014 · Cited by 295 · see citing works
Self-citationTemporal memory deficits in Alzheimer’s mouse models: Rescue by genetic deletion of BACE1
Ohno, M., Chang, L., Tseng, W., Oakley, H., Citron, M., Klein, W. L., Vassar, R., & Disterhoft, J. F. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04551.x · Cited by 298 · see citing works
Pugh, C. R., Kumagawa, K., Fleshner, M., Watkins, L. R., Maier, S. F., & Rudy, J. W. (1998) · Brain, Behavior, and Immunity · doi:10.1006/brbi.1998.0524 · Cited by 286 · see citing works
New Experiences Enhance Coordinated Neural Activity in the Hippocampus
Cheng, S., & Frank, L. M. (2008) · Neuron · doi:10.1016/j.neuron.2007.11.035 · Cited by 286 · see citing works
Bidirectional synaptic plasticity: from theory to reality
Bear, M. F. (2003) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2002.1255 · Cited by 260 · see citing works
Monahan, J. B., Handelmann, G. E., Hood, W. F., & Cordi, A. A. (1989) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(89)90571-6 · Cited by 257 · see citing works
Innervation of different peptide-containing neurons in the hippocampus by gabaergic septal afferents
Gulyás, A. I., Görcs, T. J., & Freund, T. F. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90189-b · Cited by 234 · see citing works
Long-term potentiation and memory
Morris, R. G. M. (2003) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2002.1230 · Cited by 232 · see citing works
Self-citationBarrientos, R. M., Frank, M. G., Hein, A. M., Higgins, E. A., Watkins, L. R., Rudy, J. W., & Maier, S. F. (2009) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2008.07.002 · Cited by 226 · see citing works
Balu, D. T., Li, Y., Puhl, M. D., Benneyworth, M. A., Basu, A. C., Takagi, S., Bolshakov, V. Y., & Coyle, J. T. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1304308110 · Cited by 217 · see citing works
Mildly impaired water maze performance in maleFmr1 knockout mice
D'Hooge, R., Nagels, G., Franck, F., Bakker, C. E., Reyniers, E., Storm, K., Kooy, R. F., Oostra, B. A., Willems, P. J., & De Deyn, P. P. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00224-2 · Cited by 208 · see citing works
Age‐Dependent Inhibition of Long‐Term Potentiation by Ethanol in Immature Versus Mature Hippocampus
Swartzwelder, H. S., Wilson, W. A., & Tayyeb, M. I. (1995) · Alcoholism: Clinical and Experimental Research · doi:10.1111/j.1530-0277.1995.tb01011.x · Cited by 196 · see citing works
Chapter 6 Regulation of hippocampus-dependent memory by cyclic AMP-dependent protein kinase
Abel, T., & Nguyen, P. V. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(07)00006-4 · Cited by 198 · see citing works
Fontán-Lozano, Á., Sáez-Cassanelli, J. L., Inda, M. C., de los Santos-Arteaga, M., Sierra-Domínguez, S. A., López-Lluch, G., Delgado-García, J. M., & Carrión, Á. M. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2757-07.2007 · Cited by 195 · see citing works
Milton, A. L., Merlo, E., Ratano, P., Gregory, B. L., Dumbreck, J. K., & Everitt, B. J. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.3273-12.2013 · Cited by 183 · see citing works
Barrientos, R. M., Sprunger, D. B., Campeau, S., Watkins, L. R., Rudy, J. W., & Maier, S. F. (2004) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2004.06.009 · Cited by 192 · see citing works
Cholinergic stimulation enhances long-term potentiation in the CA1 region of rat hippocampus
Blitzer, R. D., Gil, O., & Landau, E. M. (1990) · Neuroscience Letters · doi:10.1016/0304-3940(90)90835-w · Cited by 192 · see citing works
Quartermain, D., Mower, J., Rafferty, M. F., Herting, R. L., & Lanthorn, T. H. (1994) · European Journal of Pharmacology · doi:10.1016/0014-2999(94)90687-4 · Cited by 190 · see citing works
Beal, M. F., Henshaw, D. R., Jenkins, B. G., Rosen, B. R., & Schulz, J. B. (1994) · Annals of Neurology · doi:10.1002/ana.410360613 · Cited by 189 · see citing works
Kim, J. J., Koo, J. W., Lee, H. J., & Han, J.-S. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.4623-04.2005 · Cited by 184 · see citing works
Time-dependent involvement of the dorsal hippocampus in trace fear conditioning in mice
Misane, I., Tovote, P., Meyer, M., Spiess, J., Ögren, S. O., & Stiedl, O. (2005) · Hippocampus · doi:10.1002/hipo.20067 · Cited by 183 · see citing works
Duffy, S., Labrie, V., & Roder, J. C. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301486 · Cited by 173 · see citing works
Neural basis of psychosis-related behaviour in the infection model of schizophrenia
Meyer, U., & Feldon, J. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.12.022 · Cited by 158 · see citing works
Seidenbecher, T., Reymann, K. G., & Balschun, D. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.4.1494 · Cited by 154 · see citing works
Denis, I., Potier, B., Vancassel, S., Heberden, C., & Lavialle, M. (2013) · Ageing Research Reviews · doi:10.1016/j.arr.2013.01.007 · Cited by 150 · see citing works
Manahan‐Vaughan, D., von Haebler, D., Winter, C., Juckel, G., & Heinemann, U. (2008) · Hippocampus · doi:10.1002/hipo.20367 · Cited by 149 · see citing works
Fanselow, M. S., Kim, J. J., Yipp, J., & De Oca, B. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.2.235 · Cited by 142 · see citing works
Neurodevelopmental damage after prenatal infection: role of oxidative stress in the fetal brain
Lanté, F., Meunier, J., Guiramand, J., Maurice, T., Cavalier, M., de Jesus Ferreira, M.-C., Aimar, R., Cohen-Solal, C., Vignes, M., & Barbanel, G. (2007) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.01.027 · Cited by 140 · see citing works
Hinrich, A. J., Jodelka, F. M., Chang, J. L., Brutman, D., Bruno, A. M., Briggs, C. A., James, B. D., Stutzmann, G. E., Bennett, D. A., Miller, S. A., et al. (2016) · EMBO Molecular Medicine · doi:10.15252/emmm.201505846 · Cited by 127 · see citing works
Leon, J., Moreno, A. J., Garay, B. I., Chalkley, R. J., Burlingame, A. L., Wang, D., & Dubal, D. B. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.07.024 · Cited by 123 · see citing works
Kao, A. C.-C., Spitzer, S., Anthony, D. C., Lennox, B., & Burnet, P. W. J. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0116-8 · Cited by 128 · see citing works
The N-methyl-d-aspartate receptor, synaptic plasticity, and depressive disorder
Petrie, R. X. A., Reid, I. C., & Stewart, C. A. (2000) · Pharmacology & Therapeutics · doi:10.1016/s0163-7258(00)00063-2 · Cited by 129 · see citing works
Yang, J., Hou, C., Ma, N., Liu, J., Zhang, Y., Zhou, J., Xu, L., & Li, L. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2006.09.001 · Cited by 127 · see citing works
Nicoll, R. A., & Schulman, H. (2023) · Physiological Reviews · doi:10.1152/physrev.00034.2022 · Cited by 126 · see citing works
“However, although there is considerable evidence linking LTP to behavior memory (45, 441 – 443), more evidence is needed to solidify this link.”
BackgroundMismatch negativity encoding of prediction errors predicts S-ketamine-induced cognitive impairments
Schmidt, A., Bachmann, R., Kometer, M., Csomor, P. A., Stephan, K. E., Seifritz, E., & Vollenweider, F. X. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2011.261 · Cited by 121 · see citing works
Wang, H. L., Wayner, M. J., Chai, C. Y., & Lee, E. H. Y. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00352.x · Cited by 97 · see citing works
Neurosteroid Actions in Memory and Neurologic/Neuropsychiatric Disorders
Ratner, M. H., Kumaresan, V., & Farb, D. H. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00169 · Cited by 96 · see citing works
Cooke, S. F., Wu, J., Plattner, F., Errington, M., Rowan, M., Peters, M., Hirano, A., Bradshaw, K. D., Anwyl, R., Bliss, T. V. P., et al. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.111559 · Cited by 77 · see citing works
The requirement of BDNF for hippocampal synaptic plasticity is experience‐dependent
Aarse, J., Herlitze, S., & Manahan‐Vaughan, D. (2016) · Hippocampus · doi:10.1002/hipo.22555 · Cited by 74 · see citing works
Muhia, M., Yee, B. K., Feldon, J., Markopoulos, F., & Knuesel, I. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07079.x · Cited by 71 · see citing works
Bagot, R. C., Tse, Y. C., Nguyen, H.-B., Wong, A. S., Meaney, M. J., & Wong, T. P. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.03.016 · Cited by 65 · see citing works
Effects of chronic ketamine use on frontal and medial temporal cognition
Chan, K. W. S., Lee, T. M. C., Siu, A. M. H., Wong, D. P. L., Kam, C.-M., Tsang, S. K. M., & Chan, C. C. H. (2013) · Addictive Behaviors · doi:10.1016/j.addbeh.2013.01.014 · Cited by 65 · see citing works
Electrophysiological assessment of auditory stimulus-specific plasticity in schizophrenia
Mears, R. P., & Spencer, K. M. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.12.016 · Cited by 64 · see citing works
Land, C., & Riccio, D. C. (1999) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1998.3897 · Cited by 61 · see citing works
Burns, L. H., Everitt, B. J., & Robbins, T. W. (1994) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(05)80007-x · Cited by 61 · see citing works
Drink, drugs and disruption: memory manipulation for the treatment of addiction
Milton, A. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.11.008 · Cited by 56 · see citing works
Thompson, L. T., & Disterhoft, J. F. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.6.1303 · Cited by 57 · see citing works
Power, A. E., & McGaugh, J. L. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2001.4030 · Cited by 57 · see citing works
- Authors
- Morris, R. G. M., Anderson, E., Lynch, G. S., & Baudry, M.
- Affiliations
- University of St Andrews (GB)
- University of California, Irvine (US)
- Venue
- Nature
- Published
- 1986-02
- Volume
- 319
- Issue
- 6056
- Pages
- 774-776
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2025801062
- Cited by
- 3,640
- References
- 20
- Citations by year
- 2026: 25 · 2025: 30 · 2024: 44 · 2023: 31 · 2022: 42 · 2021: 63 · 2020: 52 · 2019: 65 · 2018: 83 · 2017: 85 · 2016: 82 · 2015: 89 · 2014: 103 · 2013: 98 · 2012: 101
- FWCI
- 31.77
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- NMDA receptor, AP5, long-term potentiation, hippocampus, place learning, spatial learning, visual discrimination learning, glutamate receptors, intraventricular infusion, synaptic plasticity
- MeSH terms
- Animals, Electric Stimulation, Hippocampus, Isomerism, Learning, Valine, Visual Perception, 2-Amino-5-phosphonovalerate, Receptors, N-Methyl-D-Aspartate, Receptors, Neurotransmitter, Rats
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