Crossref journal-article
Annual Reviews
Annual Review of Neuroscience (22)
Abstract

Changing the strength of connections between neurons is widely assumed to be the mechanism by which memory traces are encoded and stored in the central nervous system. In its most general form, the synaptic plasticity and memory hypothesis states that “activity-dependent synaptic plasticity is induced at appropriate synapses during memory formation and is both necessary and sufficient for the information storage underlying the type of memory mediated by the brain area in which that plasticity is observed.” We outline a set of criteria by which this hypothesis can be judged and describe a range of experimental strategies used to investigate it. We review both classical and newly discovered properties of synaptic plasticity and stress the importance of the neural architecture and synaptic learning rules of the network in which it is embedded. The greater part of the article focuses on types of memory mediated by the hippocampus, amygdala, and cortex. We conclude that a wealth of data supports the notion that synaptic plasticity is necessary for learning and memory, but that little data currently supports the notion of sufficiency.

Bibliography

Martin, S. J., Grimwood, P. D., & Morris, R. G. M. (2000). Synaptic Plasticity and Memory: An Evaluation of the Hypothesis. Annual Review of Neuroscience, 23(1), 649–711.

Authors 3
  1. S. J. Martin (first)
  2. P. D. Grimwood (additional)
  3. R. G. M. Morris (additional)
References 360 Referenced 2,240
  1. Abraham WC. 1996. Activity-dependent regulation of synaptic plasticity (metaplasticity) in the hippocampus. InThe Hippocampus: Functions and Clinical Relevance,ed. N Kato, pp. 15–34. Amsterdam: Elsevier Sci.
  2. Abraham WC, Bear MF. 1996. Metaplasticity: the plasticity of synaptic plasticity.Trends Neurosci.19:126–30 (10.1016/S0166-2236(96)80018-X)
  3. 10.1002/(SICI)1098-1063(1997)7:2<137::AID-HIPO3>3.0.CO;2-K
  4. Abraham WC, Kairiss EW. 1988. Effects of the NMDA antagonist 2AP5 on complex spike discharge by hippocampal pyramidal cells.Neurosci. Lett.89:36–42 (10.1016/0304-3940(88)90477-6)
  5. Abraham WC, Mason SE. 1988. Effects of the NMDA receptor/channel antagonists CPP and MK801 on hippocampal field potentials and long-term potentiation in anesthetized rats.Brain Res.462:40–46 (10.1016/0006-8993(88)90582-3)
  6. Abraham WC, Tate WP. 1997. Metaplasticity: a new vista across the field of synaptic plasticity.Prog. Neurobiol.52:303–23 (10.1016/S0301-0082(97)00018-X)
  7. Aggleton JP. 1992.The Amygdala.New York: Wiley-Liss. 615 pp.
  8. 10.1016/S0028-3908(98)00068-9
  9. Ahissar E, Ahissar M. 1994. Plasticity in auditory cortical circuitry.Curr. Opin. Neurobiol.4:580–87 (10.1016/0959-4388(94)90060-4)
  10. Ahissar M, Ahissar E, Bergman H, Vaadia E. 1992. Encodings of sounds-source location and movement—activity of single neurons and interactions between adjacent neurons in the monkey auditory cortex.J. Neurophysiol.67:203–15 (10.1152/jn.1992.67.1.203)
  11. Amaral D. 1993. Emerging principles of intrinsic hippocampal organization.Curr. Opin. Neurobiol.3:225–29 (10.1016/0959-4388(93)90214-J)
  12. 10.1016/0306-4522(89)90185-1
  13. Anonymous. 1997. Mutant mice and neuroscience: recommendations concerning genetic background.Neuron19:755–59 (10.1016/S0896-6273(00)80958-7)
  14. Anwyl R. 1999. Metabotropic glutamate receptors: electrophysiological properties and role in plasticity.Brain Res. Brain Res. Rev.29:83–120 (10.1016/S0165-0173(98)00050-2)
  15. 10.1016/0306-4522(96)00263-1
  16. Arai A, Kessler M, Xiao P, Ambros-Ingerson J, Rogers G, Lynch G. 1994. A centrally active drug that modulates AMPA receptor gated currents.Brain Res.638:343–46 (10.1016/0006-8993(94)90669-6)
  17. 10.1093/cercor/5.4.353
  18. 10.1038/347069a0
  19. 10.1038/330649a0
  20. 10.1016/0092-8674(95)90010-1
  21. Bannerman DM, Chapman PF, Kelly PAT, Butcher SP, Morris RGM. 1994. Inhibition of nitric-oxide synthase does not prevent the induction of long-term potentiationin vivo.J. Neurosci.14:7415–25 (10.1523/JNEUROSCI.14-12-07415.1994)
  22. 10.1038/378182a0
  23. Barnes CA. 1979. Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat.J. Comp. Physiol. Psychol.93:74–104 (10.1037/h0077579)
  24. Barnes CA. 1995. Involvement of LTP in memory: are we searching under the street light?Neuron15:751–54 (10.1016/0896-6273(95)90166-3)
  25. Barnes CA, Jung MW, McNaughton BL, Korol DL, Andreasson K, Worley PF. 1994. LTP saturation and spatial learning disruption: effects of task variables and saturation levels.J. Neurosci.14:5793–806 (10.1523/JNEUROSCI.14-10-05793.1994)
  26. Barnes CA, McNaughton BL. 1985. An age comparison of the rates of acquisition and forgetting of spatial information in relation to long-term enhancement of hippocampal synapses.Behav. Neurosci.99:1040–48 (10.1037/0735-7044.99.6.1040)
  27. Barrionuevo G, Schottler F, Lynch G. 1980. The effects of repetitive low frequency stimualtion on control and “potentiated” synaptic responses in the hippocampus.Life Sci.27:2385–91 (10.1016/0024-3205(80)90509-3)
  28. 10.1038/363347a0
  29. Bashir ZI, Collingridge GL. 1994. An investigation of depotentiation of long-term potentiation in the CA1 region of the hippocampus.Exp. Brain Res.100:437–43 (10.1007/BF02738403)
  30. 10.1016/0896-6273(95)90035-7
  31. 10.1093/cercor/8.5.407
  32. 10.1126/science.6324350
  33. 10.1523/JNEUROSCI.18-23-10037.1998
  34. Bienenstock EL, Cooper LN, Munro PW. 1982. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex.J. Neurosci.2:32–48 (10.1523/JNEUROSCI.02-01-00032.1982)
  35. Bliss TVP, Collingridge GL. 1993. A synaptic model of memory: long-term potentiation in the hippocampus.Nature361:31–39 (10.1038/361031a0)
  36. 10.1113/jphysiol.1986.sp016193
  37. 10.1113/jphysiol.1973.sp010273
  38. 10.1002/hipo.450030203
  39. Böhme GA, Bon C, Lemaire M, Reibaud M, Piot O, et al. 1993. Altered synaptic plasticity and memory formation in nitric oxide synthase inhibitor-treated rats.Proc. Natl. Acad. Sci. USA90:9191–94 (10.1073/pnas.90.19.9191)
  40. Bolhuis JJ, Reid IC. 1992. Effects of intraventricular infusion of theN-methyl-D-aspartate (NMDA) receptor antagonist AP5 on spatial memory of rats in a radial arm maze.Behav. Brain Res.47:151–57 (10.1016/S0166-4328(05)80121-4)
  41. 10.1016/S0028-3908(96)00101-3
  42. 10.1016/0014-2999(94)00756-W
  43. 10.1038/368740a0
  44. 10.1038/36849
  45. Breakwell NA, Rowan MJ, Anwyl R. 1996. Metabotropic glutamate receptor dependent EPSP and EPSP-spike potentiation in area CA1 of the submerged rat CA1 slice.J. Neurophysiol.76:3126–35 (10.1152/jn.1996.76.5.3126)
  46. Breakwell NA, Rowan MJ, Anwyl R. 1998. (+)-MCPG blocks induction of LTP in CA1 of rat hippocampus via agonist action at an mGluR group II receptor.J. Neurophysiol.79:1270–76 (10.1152/jn.1998.79.3.1270)
  47. Buonomano DV, Merzenich MM. 1998. Cortical plasticity: from synapses to maps.Annu. Rev. Neurosci.21:149–86 (10.1146/annurev.neuro.21.1.149)
  48. Bures J, Bermudez-Rattoni F, Yamamoto T. 1998.Conditioned Taste Aversion: Memory of a Special Kind.London: Oxford Univ. Press. 192 pp. (10.1093/acprof:oso/9780198523475.001.0001)
  49. Burns LH, Everitt BJ, Robbins TW. 1994. Intra-amygdala infusion of theN-methyl-Daspartate receptor antagonist AP5 impairs acquisition but not performance of discriminated approach to an appetitive CS.Behav. Neural Biol.61:242–50 (10.1016/S0163-1047(05)80007-X)
  50. Butcher SP, Hamberger A, Morris RGM. 1991. Intracerebral distribution of DL-2-aminophosphonopentanoic acid (AP5) and the dissociation of different types of learning.Exp. Brain Res.83:521–26 (10.1007/BF00229829)
  51. Buzsáki G. 1989. Two-stage model of memory-trace formation: a role for ‘noisy’ brain states.Neuroscience31:551–70 (10.1016/0306-4522(89)90423-5)
  52. Cahill L, Weinberger NM, Roozendaal B, McGaugh JL. 1999. Is the amygdala a locus of “conditioned fear”? Some questions and caveats.Neuron23:227–28 (10.1016/S0896-6273(00)80774-6)
  53. 10.1002/hipo.450030208
  54. Cain DP, Saucier D, Hall J, Hargreaves EL, Boon F. 1996. Detailed behavioral analysis of water maze acquisition under APV or CNQX: contribution of sensorimotor disturbances to drug-induced acquisition deficits.Behav. Neurosci.110:86–102 (10.1037/0735-7044.110.1.86)
  55. Campeau S, Miserendino MJD, Davis M. 1992. Intra-amygdala infusion of theNmethyl-D-aspartate receptor antagonist AP5 blocks acquisition but not expression of fear-potentiated startle to an auditory conditioned stimulus.Behav. Neurosci.106:569–74 (10.1037/0735-7044.106.3.569)
  56. 10.1126/science.2660260
  57. Caramanos Z, Shapiro ML. 1994. Spatial memory andN-methyl-D-aspartate receptor antagonists APV and MK-801: memory impairments depend on familiarity with the environment, drug dose and training duration.Behav. Neurosci.108:30–43 (10.1037/0735-7044.108.1.30)
  58. 10.1038/342545a0
  59. 10.1523/JNEUROSCI.15-07-05324.1995
  60. {'key': 'b60', 'first-page': '343', 'volume': '90', 'year': '1996', 'journal-title': 'J. Physiol.'} / J. Physiol. (1996)
  61. 10.1097/00001756-199207000-00005
  62. 10.1002/syn.890110406
  63. Chapman PF, White GL, Jones MW, CooperBlacketer D, Marshall VJ, et al. 1999. Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice.Nat. Neurosci.2:271–76 (10.1038/6374)
  64. Chen C, Tonegawa S. 1997. Molecular genetic analysis of synaptic plasticity, activitydependent neural development, learning, and memory in the mammalian brain.Annu. Rev. Neurosci.20:157–84 (10.1146/annurev.neuro.20.1.157)
  65. Chinestra P, Aniksztejn L, Diabira D, Ben-Ari Y. 1993. (RS)-a-methyl-4-carboxyphenylglycine neither prevents induction of LTP nor antagonizes metabotropic glutamate receptors in CA1 hippocampal neurons.J. Neurophysiol.70:2684–89 (10.1152/jn.1993.70.6.2684)
  66. 10.1126/science.279.5352.867
  67. 10.1016/0896-6273(92)90222-Y
  68. Churchland PS, Sejnowski TJ. 1992.The Computational Brain.Cambridge, MA: MIT Press. 544 pp. (10.7551/mitpress/2010.001.0001)
  69. Clugnet M-C, LeDoux JE. 1990. Synaptic plasticity in fear conditioning circuits: induction of LTP in the lateral nucleus of the amygdala by stimulation of the medial geniculate body.J. Neurosci.10:2818–24 (10.1523/JNEUROSCI.10-08-02818.1990)
  70. Cohen AS, Abraham WC. 1996. Facilitation of long-term potentiation by prior activation of metabotropic glutamate receptors.J. Neurophysiol.76:953–62 (10.1152/jn.1996.76.2.953)
  71. Cohen NJ, Eichenbaum HE. 1993.Memory, Amnesia and the Hippocampal System.Cambridge, MA: MIT Press. 330 pp.
  72. 10.1007/BF02253537
  73. Danysz W, Wroblewski JT, Costa E. 1988. Learning impairment in rats byN-methyl-D-aspartate receptor antagonists.Neuropharmacology27:653–56 (10.1016/0028-3908(88)90189-X)
  74. {'key': 'b74', 'first-page': '455', 'volume': '6', 'year': '1995', 'journal-title': 'Behav. Pharmacol.'} / Behav. Pharmacol. (1995)
  75. Davis M, Falls WA, Campeau S, Kim M. 1993. Fear-potentiated startle: a neural and pharmacological analysis.Behav. Brain Res.58:175–98 (10.1016/0166-4328(93)90102-V)
  76. Davis M, Rainnie D, Cassell M. 1994. Neurotransmission in the rat amygdala related to fear and anxiety.Trends Neurosci.17:208–14 (10.1016/0166-2236(94)90106-6)
  77. Davis S, Butcher SP, Morris RGM. 1992. The NMDA receptor antagonist D-2-amino-5phosphonopentanoate (D-aAP5) impairs spatial-learning and LTP in vivo at intracerebral concentrations comparable to those that block LTP in vitro.J. Neurosci.12:21–34 (10.1523/JNEUROSCI.12-01-00021.1992)
  78. 10.1038/381429a0
  79. Diamond DM, Rose GM. 1994. Does associative LTP underlie classical conditioning?Psychobiology22:263–69 (10.3758/BF03327109)
  80. 10.1016/S0896-6273(00)80551-6
  81. 10.1038/297496a0
  82. 10.1002/(SICI)1098-1063(1996)6:1<52::AID-HIPO9>3.3.CO;2-Q
  83. Dudek SM, Bear MF. 1992. Homosynaptic long-term depression and effects ofNmethyl-D-aspartate receptor blockade.Proc. Natl. Acad. Sci. USA89:4363–67 (10.1073/pnas.89.10.4363)
  84. Dunwiddie T, Lynch G. 1978. Long-term potentiation and depression of synaptic responses in the rat hippocampus: localization and frequency dependency.J. Physiol.276:353–67 (10.1113/jphysiol.1978.sp012239)
  85. Edeline JM, Weinberger NM. 1992. Associative retuning in the thalamic source of input to the amygdala and auditory cortex: receptive field plasticity in the medial division of the medial geniculate body.Behav. Neurosci.106:81–105 (10.1037/0735-7044.106.1.81)
  86. Engert F, Bonhoeffer T. 1997. Synapse specificity of long-term potentiation breaks down at short distances.Nature388:279– 84 (10.1038/40870)
  87. English JD, Sweatt JD. 1997. A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation.J. Biol. Chem.272:19103–6 (10.1074/jbc.272.31.19103)
  88. 10.1038/42625
  89. 10.1152/jn.1995.74.4.1793
  90. Errington ML, Lynch MA, Bliss TVP. 1987. Long-term potentiation in the dentate gyrus: induction and increased glutamate release are blocked by D(-) aminophosphonovalerate.Neuroscience20:279–84 (10.1016/0306-4522(87)90019-4)
  91. Escobar ML, Alcocer I, Chao V. 1998. The NMDA receptor antagonist CPP impairs conditioned taste aversion and insular cortex long-term potentiation in vivo.Brain Res.812:246–51 (10.1016/S0006-8993(98)00931-7)
  92. Fanselow MS, Kim JJ, Yipp J, De Oca B. 1994. Differential effects of theN-methyl-Daspartate antagonist DL-2-amino-5-phosphonovalerate on acquisition of fear of auditory and contextual cues.Behav. Neurosci.108:235–40 (10.1037/0735-7044.108.2.235)
  93. 10.1016/S0896-6273(00)80775-8
  94. 10.1016/S0028-3908(98)00145-2
  95. Fontana DJ, Daniels SE, Wong EH, Clark RD, Eglen RM. 1997. The effects of novel, selective 5-hydroxytryptamine (5-HT)4 receptor ligands in rat spatial navigation.Neuropharmacology36:689–96 (10.1016/S0028-3908(97)00055-5)
  96. Frankland PW, Cestari V, Filipkowski RK, McDonald RJ, Silva AJ. 1998. The dorsal hippocampus is essential for context discrimination but not for contextual conditioning.Behav. Neurosci.112:863–74 (10.1037/0735-7044.112.4.863)
  97. Fregnac Y. 1997. Synaptic Plasticity, Learning and Cortical Dynamics. Amsterdam: Elsevier. 323 pp.
  98. 10.1002/(SICI)1098-1063(1996)6:4<347::AID-HIPO1>3.0.CO;2-I
  99. 10.1038/385533a0
  100. Frey U, Morris RGM. 1998a. Weak before strong: dissociating synaptic-tagging and plasticity-factor accounts of late-LTP.Neuropharmacology37:545–52 (10.1016/S0028-3908(98)00040-9)
  101. Frey U, Morris RGM. 1998b. Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation.Trends Neurosci.21:181–88 (10.1016/S0166-2236(97)01189-2)
  102. 10.1002/neu.480190402
  103. Fujii S, Saito K, Miyakawa H, Ito K, Kato H. 1991. Reversal of long-term potentiation (depotentiation) induced by tetanus stimulation of the input to CA1 neurons of guinea pig hippocampal slices.Brain Res.555:112–22 (10.1016/0006-8993(91)90867-U)
  104. Furth PA, St. Onge L, Böger H, Gruss P, Gossen M, et al. 1994. Temporal control of gene expression in transgenic mice by a tetracycline-responsive promoter.Proc. Natl. Acad. Sci. USA91:9302–6 (10.1073/pnas.91.20.9302)
  105. 10.1006/nlme.1998.3835
  106. 10.1046/j.1460-9568.1998.00027.x
  107. Gerlai R. 1996. Gene-targeting studies of mammalian behaviour: Is it the mutation or the background genotype?Trends Neurosci.19:177–81 (10.1016/S0166-2236(96)20020-7)
  108. 10.1038/41325
  109. 10.1126/science.279.5352.870
  110. 10.1038/322419a0
  111. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ. 1999. Learning enhances adult neurogenesis in the hippocampal formation.Nat. Neurosci.2:260–65 (10.1038/6365)
  112. Grant SG, Karl KA, Kiebler MA, Kandel ER. 1995. Focal adhesion kinase in the brain: novel subcellular localization and specific regulation byFyntyrosine kinase in mutant mice.Genes Dev.9:1909–21 (10.1101/gad.9.15.1909)
  113. Grant SGN, O’Dell TJ, Karl KA, Stein PL, Sorian OP, Kandel ER. 1992. Impaired long-term potentiation, spatial learning, and hippocampal development infynmutant mice.Science258:1903–10 (10.1126/science.1361685)
  114. Green EJ, Greenough WT. 1986. Altered synaptic transmission in dentate gyrus of rats reared in complex environments: evidence from hippocampal slices maintained in vitro.J. Neurophysiol.55:739–50 (10.1152/jn.1986.55.4.739)
  115. Green EJ, McNaughton BL, Barnes CA. 1990. Exploration-dependent modulation of evoked responses in fascia dentata: dissociation of motor, EEG, and sensory factors and evidence for a synaptic efficacy change.J. Neurosci.10:1455–71 (10.1523/JNEUROSCI.10-05-01455.1990)
  116. Grillner S, Ekeberg EL, Manira A, Lansner A, Parker D, et al. 1998. Intrinsic function of a neuronal network—a vertebrate central pattern generator.Brain Res. Brain Res. Rev.26:184–97 (10.1016/S0165-0173(98)00002-2)
  117. Gutierrez H, Hernandez-Esheagaray E, Ramirez-Amaya V, Bermudez-Rattoni F. 1999. Blockade ofN-methyl-D-aspartate receptors in the insular cortex disrupts taste aversion and spatial memory formation.Neuroscience89:751–58 (10.1016/S0306-4522(98)00360-1)
  118. Hasselmo ME, Schnell E, Barkai E. 1995. Dynamics of learning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3.J. Neurosci.15:5249–62 (10.1523/JNEUROSCI.15-07-05249.1995)
  119. Hawkins RD, Greene W, Kandel ER. 1998a. Classical conditioning, differential conditioning, and second-order conditioning of the Aplysia gill-withdrawal reflex in a simplified mantle organ preparation.Behav. Neurosci.112:636–45 (10.1037/0735-7044.112.3.636)
  120. Hawkins RD, Kandel ER. 1984. Is there a cellbiological alphabet for simple forms of learning?Psychol. Rev.91:375–91 (10.1037/0033-295X.91.3.375)
  121. Hawkins RD, Son H, Arancio O. 1998b. Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus.Prog. Brain Res.118:155–72 (10.1016/S0079-6123(08)63206-9)
  122. Hebb DO. 1949.The Organization of Behavior.New York: Wiley
  123. Hess US, Lynch G, Gall CM. 1995a. Changes in c-fosmRNA expression in rat brain during odor discrimination learning: differential involvement of hippocampal subfields CA1 and CA3.J. Neurosci.15:4786–95 (10.1523/JNEUROSCI.15-07-04786.1995)
  124. Hess US, Lynch G, Gall CM. 1995b. Regional patterns of c-fosmRNA expression in rat hippocampus following exploration of a novel environment versus performance of a well-learned discrimination.J. Neurosci.15:7796–809 (10.1523/JNEUROSCI.15-12-07796.1995)
  125. Heynen AJ, Abraham WC, Bear MF. 1996. Bidirectional modification of CA1 synapses in the adult hippocampusin vivo.Nature381:163–66 (10.1038/381163a0)
  126. 10.1101/lm.5.4.344 / Learn. Mem. (1998)
  127. Hoh T, Beiko J, Boon F, Weiss S, Cain DP. 1999. Complex behavioral strategy and reversal learning the water maze without NMDA receptor dependent long term potentiation.J. Neurosci.19:1–5 (10.1523/JNEUROSCI.19-10-j0003.1999)
  128. Holland LL, Wagner JJ. 1998. Primed facilitation of homosynaptic long-term depression and depotentiation in rat hippocampus.J. Neurosci.18:887–94 (10.1523/JNEUROSCI.18-03-00887.1998)
  129. Holland PC. 1990. Forms of memory in Pavlovian conditioning. InBrain Organization and Memory: Calls, Systems, and Circuits,ed. JL McGaugh, NM Weinberger, G Lynch, pp. 78–105. New York: Oxford Univ. Press (10.1093/oso/9780195077124.003.0005)
  130. Holland PC, Gallagher M. 1999. Amygdala circuitry in attentional and representational processes.Trends Cogn. Sci.3:65–73 (10.1016/S1364-6613(98)01271-6)
  131. Hölscher C, Anwyl R, Rowan MJ. 1997. Stimulation on the positive phase of hippocampal theta rhythm induces long-term potentiation that can be depotentiated by stimulation on the negative phase in area CA1 in vivo.J. Neurosci.17:6470–77 (10.1523/JNEUROSCI.17-16-06470.1997)
  132. 10.1101/lm.2.6.267
  133. 10.1126/science.274.5284.99
  134. 10.1126/science.1346729
  135. 10.1016/S0896-6273(00)80524-3
  136. 10.1038/364723a0
  137. 10.1016/0896-6273(95)90094-2
  138. Huerta PT, Lisman JE. 1996. Low-frequency stimulation at the troughs of theta-oscillation induces long-term depression of previously potentiated CA1 synapses.J. Neurophysiol.75:877–84 (10.1152/jn.1996.75.2.877)
  139. Impey S, Obrietan K, Storm DR. 1999. Making new connections: role of ERK/MAP Kinase signalling in neuronal plasticity.Neuron23:11–14 (10.1016/S0896-6273(00)80747-3)
  140. Impey S, Smith DM, Obrietan K, Donahue R, Wade C, Storm DR. 1998. Stimulation of cAMP response element (CRE)-mediated transcription during contextual learning.Nat. Neurosci.1:595–601 (10.1038/2830)
  141. 10.1126/science.2551038
  142. Isaac JT, Nicoll RA, Malenka RC. 1995. Evidence for silent synapses: implications for the expression of LTP.Neuron15:427–34 (10.1016/0896-6273(95)90046-2)
  143. Ishihara K, Mitsuno K, Ishikawa M, Sasa M. 1997. Behavioral LTP during learning in rat hippocampal CA3.Behav. Brain Res.83:235–38 (10.1016/S0166-4328(97)86077-9)
  144. Izquierdo I, Medina JH. 1995. Correlation between the pharmacology of long-term potentiation and the pharmacology of memory.Neurobiol. Learn. Mem.63:19–32 (10.1006/nlme.1995.1002)
  145. Izquierdo I, Quillfeldt JA, Zanatta MS, Quevedo J, Schaeffer E, et al. 1997. Sequential role of hippocampus and amygdala, entorhinal cortex and parietal cortex in formation and retrieval of memory for inhibitory avoidance in rats.Eur. J. Neurosci.9:786– 93 (10.1111/j.1460-9568.1997.tb01427.x)
  146. Izquierdo I, Schroder N, Netto CA, Medina JH. 1999. Novelty causes time-dependent retrograde amnesia for one-trial avoidance in rats through NMDA receptor- and CaMKIIdependent mechanisms in hippocampus.Eur. J. Neurosci.In press (10.1046/j.1460-9568.1999.00742.x)
  147. {'key': 'b147', 'first-page': '339', 'volume': '90', 'year': '1996', 'journal-title': 'J. Physiol.'} / J. Physiol. (1996)
  148. Jay TM, Burette F, Laroche S. 1995. NMDA receptor-dependent long-term potentiation in the hippocampal afferent fibre system to the prefrontal cortex in the rat.Eur. J. Neurosci.7:247–50 (10.1111/j.1460-9568.1995.tb01060.x)
  149. Jeffery KJ. 1997. LTP and spatial learning— where to next?Hippocampus7:95–110 (10.1002/(SICI)1098-1063(1997)7:1<95::AID-HIPO10>3.0.CO;2-D)
  150. 10.1002/hipo.450030205
  151. Johnston D, Williams S, Jaffe D, Gray R. 1992. NMDA-receptor-independent long-term potentiation.Annu. Rev. Physiol.54:489– 505 (10.1146/annurev.ph.54.030192.002421)
  152. 10.1002/syn.890060307
  153. Kaczmarek L. 1992. Expression of c-fosand other genes encoding transcription factors in long-term potentiation.Behav. Neural Biol.57:263–66 (10.1016/0163-1047(92)90276-A)
  154. Kagan J. 1998. Animal fear and human guilt. InCerebrum: The DANA Forum on Brain Science,ed. W Donway, CA Read, pp. 16– 25. New York: DANA
  155. Kandel ER. 1978.A Cell-Biological Approach to Learning.Bethesda, MD: Soc. Neurosci. 90 pp.
  156. Kandel ER, Schwartz JH. 1982. Molecular biology of learning: modulation of transmitter release.Science218:433–43 (10.1126/science.6289442)
  157. Keith JR, Rudy JW. 1990. Why NMDAreceptor-dependent long-term potentiation may not be a mechanism of learning and memory: reappraisal of the NMDAreceptor blockade strategy.Psychobiology18:251–57 (10.3758/BF03327238)
  158. 10.1038/386493a0
  159. 10.1523/JNEUROSCI.18-09-03206.1998
  160. 10.1038/41765
  161. 10.1126/science.280.5372.2121
  162. Kim JJ, Yoon KS. 1998. Stress: metaplastic effects in the hippocampus.Trends Neurosci.21:505–9 (10.1016/S0166-2236(98)01322-8)
  163. 10.1016/0163-1047(93)91075-X
  164. Kim M, McGaugh JL. 1992. Effects of intraamygdala injections of NMDA receptor antagonists on acquisition and retention of inhibitory avoidance.Brain Res.585:35–48 (10.1016/0006-8993(92)91188-K)
  165. Kirkwood A, Bear MF. 1994. Homosynaptic long-term depression in the visual cortex.J. Neurosci.14:3404–12 (10.1523/JNEUROSCI.14-05-03404.1994)
  166. 10.1038/381526a0
  167. Kistner A, Gossen M, Zimmermann F, Jerecic J, Ullmer C, et al. 1996. Doxycycline-mediated quantitative and tissue-specific control of gene expression in transgenic mice.Proc. Natl. Acad. Sci. USA93:10933–38 (10.1073/pnas.93.20.10933)
  168. Kiyama Y, Manabe T, Sakimura K, Kawakami F, Mori H, Mishina M. 1998. Increased thresholds for long-term potentiation and contextual learning in mice lacking the NMDA-type glutamate receptor epsilon1 subunit.J. Neurosci.18:6704–12 (10.1523/JNEUROSCI.18-17-06704.1998)
  169. Kleim JA, Barbay S, Nudo RJ. 1998. Functional reorganization of the rat motor cortex following motor skill learning.J. Neurophysiol.80:3321–25 (10.1152/jn.1998.80.6.3321)
  170. Koek W, Woods JH, Winger GD. 1988. MK801, a proposed noncompetitive antagonist of excitatory amino acid neurotransmission, produces phencyclidine-like behavioral effects in pigeons, rats and rhesus monkeys.J. Pharmacol. Exp. Ther.245:969–74
  171. 10.1093/cercor/4.6.664
  172. Korol DL, Abel TW, Church LT, Barnes CA, McNaughton BL. 1993. Hippocampal synaptic enhancement and spatial learning in the Morris swim task.Hippocampus3:127– 32 (10.1002/hipo.450030204)
  173. Krug M, Lossner B, Ott T. 1984. Anisomycin blocks the late phase of long-term potentiation in the dentate gyrus of freely moving rats.Brain Res. Bull.13:39–42 (10.1016/0361-9230(84)90005-4)
  174. Kullmann DM. 1994. Amplitude fluctuations of dual-component EPSCs in hippocampal pyramidal cells: implications for long-term potentiation.Neuron12:1111–20 (10.1016/0896-6273(94)90318-2)
  175. Lamprecht R, Hazvi S, Dudai Y. 1997. cAMP response element-binding protein in the amygdala is required for long- but not short-term conditioned taste aversion memory.J. Neurosci.17:8443–50 (10.1523/JNEUROSCI.17-21-08443.1997)
  176. Larson J, Wong D, Lynch G. 1986. Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation.Brain Res.368:347–50 (10.1016/0006-8993(86)90579-2)
  177. 10.1111/j.1365-2990.1994.tb00980.x
  178. 10.1016/0163-1047(93)90409-B
  179. LeDoux JE. 1995. Emotion: clues from the brain.Annu. Rev. Psychol.46:209–35 (10.1146/annurev.ps.46.020195.001233)
  180. LeDoux JE, Cicchetti P, Xagoraris A, Romanski LM. 1990. The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning.J. Neurosci.10:1062– 69 (10.1523/JNEUROSCI.10-04-01062.1990)
  181. LeDoux JE, Ruggiero DA, Forest R, Stornetta R, Reis DJ. 1987. Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat.J. Comp. Neurol.264:123– 46 (10.1002/cne.902640110)
  182. LeDoux JE, Ruggiero DA, Reis DJ. 1985. Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat.J. Comp. Neurol.242:182–213 (10.1002/cne.902420204)
  183. 10.1523/JNEUROSCI.18-20-08444.1998
  184. 10.1016/S0028-3908(96)00169-4
  185. Leung LW, Desborough KA. 1988. APV, anN-methyl-D-aspartate receptor antagonist, blocks the hippocampal theta rhythm in behaving rats.Brain Res.463:148–52 (10.1016/0006-8993(88)90538-0)
  186. 10.1002/(SICI)1098-1063(1996)6:6<579::AID-HIPO3>3.0.CO;2-C
  187. 10.1016/0006-8993(79)91003-5
  188. 10.1016/S0091-3057(97)00015-4
  189. Li H, Weiss SRB, Chuang D-M, Post RM, Rogawski MA. 1998. Bi-directional synaptic plasticity in the rat basolateral amygdala: characterization of an activitydependent switch sensitive to the presynaptic metabotropic glutamate receptor antagonist 2S-alpha-ethylglutamic acid.J. Neurosci.18:1662–70 (10.1523/JNEUROSCI.18-05-01662.1998)
  190. 10.1007/BF00242185
  191. Li XF, Stutzmann GE, LeDoux JE. 1996. Convergent but temporally separated inputs to lateral amygdala neurons from the auditory thalamus and auditory cortex use different postsynaptic receptors: in vivo intracellular and extracellular recordings in fear conditioning pathways.Learn. Mem.3:229–42 (10.1101/lm.3.2-3.229)
  192. 10.1038/375400a0
  193. Linden DJ, Connor JA. 1995. Long-term synaptic depression.Annu. Rev. Neurosci.18:319–57 (10.1146/annurev.ne.18.030195.001535)
  194. Link W, Konietzko U, Kauselmann G, Krug M, Schwanke B, et al. 1995. Somatodendritic expression of an immediate early gene is regulated by synaptic activity.Proc. Natl. Acad. Sci. USA92:5734–38 (10.1073/pnas.92.12.5734)
  195. Lipp HP, Wolfer DP. 1998. Genetically modified mice and cognition.Curr. Opin. Neurobiol.8:272–80 (10.1016/S0959-4388(98)80151-7)
  196. Lisman JE. 1999. Relating hippocampal circuitry to function: recall of memory sequences by reciprocal dentate-CA3 interactions.Neuron22:233–42 (10.1016/S0896-6273(00)81085-5)
  197. Lovinger DM, Wong K, Murikami K, Routtenberg A. 1987. Protein kinase C inhibitors eliminate hippocampal long-term potentiation.Brain Res.436:177–83 (10.1016/0006-8993(87)91573-3)
  198. 10.1016/S0896-6273(00)80553-X
  199. 10.1016/0028-3932(93)90034-W
  200. 10.1016/0896-6273(95)90299-6
  201. Lynch G. 1998. Memory and the brain: unexpected chemistries and a new pharmacology.Neurobiol. Learn. Mem.70:82–100 (10.1006/nlme.1998.3840)
  202. Lynch G, Baudry M. 1984. The biochemistry of memory: a new and specific hypothesis.Science224:1057–63 (10.1126/science.6144182)
  203. Lynch GS, Dunwiddie T, Gribkoff V. 1977. Heterosynaptic depression: a postsynaptic correlate of long-term potentiation.Nature266:737–39 (10.1038/266737a0)
  204. 10.1126/science.275.5297.209
  205. 10.1016/0896-6273(91)90121-F
  206. 10.1038/29073
  207. Manahan-Vaughan D. 1997. Group 1 and 2 metabotropic glutamate receptors play differential roles in hippocampal long-term depression and long-term potentiation in freely moving rats.J. Neurosci.17:3303– 11 (10.1523/JNEUROSCI.17-09-03303.1997)
  208. 10.1016/S0028-3908(98)00150-6
  209. 10.1016/S0092-8674(00)80897-1
  210. 10.1016/S0896-6273(00)80533-4
  211. 10.1111/j.1460-9568.1994.tb00599.x
  212. 10.1016/S0028-3908(97)00058-0
  213. Maren S, Aharonov G, Stote DL, Fanselow MS. 1996.N-methyl-D-aspartate receptors in the basolateral amygdala are required for both acquisition and expression of conditional fear in rats.Behav. Neurosci.110:1365–74 (10.1037/0735-7044.110.6.1365)
  214. 10.1126/science.275.5297.213
  215. 10.1038/382807a0
  216. Marr D. 1971. Simple memory: a theory for archicortex.Philos. Trans. R. Soc. London Ser. B262:23–81 (10.1098/rstb.1971.0078)
  217. 10.1097/00001756-199812010-00003
  218. Martin SJ, Morris RGM. 1997. (R,S)-αMethyl-4-carboxyphenylgline (MCPG) fails to block LTP under urethane anaesthesiain vivo.Neuropharmacology36:1339– 54 (10.1016/S0028-3908(97)00129-9)
  219. 10.1126/science.274.5293.1678
  220. Mayford M, Mansuy IM, Muller RU, Kandel ER. 1997. Memory and behavior: a second generation of genetically modified mice.Curr. Biol.7:R580–89 (10.1016/S0960-9822(06)00287-9)
  221. 10.1016/0092-8674(95)90009-8
  222. McCaughey SA, Giza BK, Nolan LJ, Scott TR. 1997. Extinction of a conditioned taste aversion in rats. II. Neural effects in the nucleus of the solitary tract.Physiol. Behav.61:373–79 (10.1016/S0031-9384(96)00412-X)
  223. McClelland JL, McNaughton BL, O’Reilly RC. 1995. Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory.Psychol. Rev.102:419–57 (10.1037/0033-295X.102.3.419)
  224. McEachern JC, Shaw CA. 1996. An alternative to the LTP orthodoxy: a plasticity-pathology continuum model.Brain Res. Brain Res. Rev.22:51–92 (10.1016/0165-0173(96)00006-9)
  225. McEwen BS. 1999. Stress and hippocampal plasticity.Annu. Rev. Neurosci.22:105–22 (10.1146/annurev.neuro.22.1.105)
  226. 10.1101/lm.3.4.296
  227. 10.1126/science.153.3742.1351
  228. McHugh TJ, Blum KI, Tsien JZ, Tonegawa S, Wilson MA. 1996. Impaired hippocampal representation of space in CA1-specific NMDAR1 knockout mice.Cell87:1339– 49 (10.1016/S0092-8674(00)81828-0)
  229. McKernan MG, Shinnick-Gallagher P. 1997. Fear conditioning induces a lasting potentiation of synaptic currentsin vitro.Nature390:607–11 (10.1038/37605)
  230. McNaughton BL. 1983. Activity-dependent modulation of hippocampal synaptic efficacy: some implications for memory processes. InNeurobiology of the Hippocampus,ed. W Siefert, pp. 233–52. London: Academic
  231. 10.1523/JNEUROSCI.06-02-00563.1986
  232. McNaughton BL, Morris RGM. 1987. Hippocampal synaptic enhancement and information storage within a distributed memory system.Trends Neurosci.10:408–15 (10.1016/0166-2236(87)90011-7)
  233. 10.1016/0896-6273(94)90060-4
  234. Meiri N, Ghelardini C, Tesco G, Galeotti N, Dahl D, et al. 1997. Reversible antisense inhibition of Shaker-like Kv1.1 potassium channel expression impairs associative memory in mouse and rat.Proc. Natl. Acad. Sci. USA94:4430–34 (10.1073/pnas.94.9.4430)
  235. Meiri N, Sun MK, Segal Z, Alkon DL. 1998. Memory and long-term potentiation (LTP) dissociated: normal spatial memory despite CA1 LTP elimination with Kv1.4 antisense.Proc. Natl. Acad. Sci. USA95:15037–42 (10.1073/pnas.95.25.15037)
  236. 10.1038/24790
  237. 10.1038/345716a0
  238. 10.1007/s002130050148
  239. Mondadori C, Weiskrantz L. 1991. Memory facilitation by NMDA receptor blockade. InLong-Term Potentiation: A Debate of Current Issues,ed. M Baudry, J Davis, pp. 259–66. Cambridge, MA: MIT Press
  240. 10.1016/0163-1047(93)90371-N
  241. Mondadori C, Weiskrantz L, Buerki H, Petschke F, Fagg GE. 1989. NMDA receptor antagonists can enhance or impair learning performance in animals.Exp. Brain Res.75:449–56 (10.1007/BF00249896)
  242. Montague PR, Sejnowski TJ. 1994. The predictive brain: temporal coincidence and temporal order in synaptic learning mechanisms.Learn. Mem.1:1–33 (10.1101/lm.1.1.1)
  243. Morris RGM. 1989. Synaptic plasticity and learning: selective impairment in learning in rats and blockade of long-term potentiation in vivo by theN-methyl-D-aspartate receptor antagonist AP5.J. Neurosci.9:3040–57 (10.1523/JNEUROSCI.09-09-03040.1989)
  244. Morris RGM. 1990. Synaptic plasticity, neural architecture, and forms of memory. See McGaugh et al 1990, pp. 53–77
  245. Morris RGM, Anderson E, Lynch GS, Baudry M. 1986. Selective impairment of learning and blockade of long-term potentiation by anN-methyl-D-aspartate receptor antagonist, AP5.Nature319:774–76 (10.1038/319774a0)
  246. Morris RGM, Davis M. 1994. The role of NMDA receptors in learning and memory. InThe NMDA Receptor,ed. GL Collingridge, JC Watkins, pp. 340–75. Oxford, UK: Oxford Univ. Press (10.1093/acprof:oso/9780192625021.003.0015)
  247. Morris RGM, Davis S, Butcher SP. 1990. Hippocampal synaptic plasticity and NMDA receptors: a role in information storage?Philos. Trans. R. Soc. London Ser. B329:187–204 (10.1098/rstb.1990.0164)
  248. Morris RGM, Frey U. 1997. Hippocampal synaptic plasticity: role in spatial learning or the automatic recording of attended experience?Philos. Trans. R. Soc. London Ser. B352:1489–503 (10.1098/rstb.1997.0136)
  249. Morris RGM, Halliwell RF, Bowery N. 1989. Synaptic plasticity and learning II: Do different kinds of plasticity underlie different kinds of learning?Neuropsychologica27:41–59 (10.1016/0028-3932(89)90089-4)
  250. Morris RGM, Kennedy MB. 1992. The Pierian Spring.Curr. Biol.2:511–14 (10.1016/0960-9822(92)90001-Q)
  251. Moser E, Moser M-B. 1999. Is learning blocked by saturation of synaptic weights in the hippocampus?Neurosci. Biobehav. Rev.23:661–72 (10.1016/S0149-7634(98)00060-8)
  252. 10.1126/science.281.5385.2038
  253. 10.1126/science.8446900
  254. 10.1097/00001756-199312000-00035
  255. {'key': 'b255', 'first-page': '437', 'volume': '19', 'year': '1993', 'journal-title': 'Soc. Neurosci. Abstr.'} / Soc. Neurosci. Abstr. (1993)
  256. 10.1126/science.8066450
  257. 10.1038/377115a0
  258. Nielsen KS, Macphail EM, Riedel G. 1997. Class I mGlu receptor antagonist 1-aminoindan-1,5-dicarboxylic acid blocks contextual but not cue conditioning in rats.Eur. J. Pharmacol.36:105–8 (10.1016/S0014-2999(97)85402-7)
  259. Nosten-Bertrand M, Errington ML, Murphy KPSJ, Morris RGM, Silver J, et al. 1996. Normal spatial learning despite regional inhibition of LTP in mice lackingThy-1.Nature379:826–29 (10.1038/379826a0)
  260. 10.1523/JNEUROSCI.16-02-00785.1996
  261. Oda Y, Kawasaki K, Morita M, Korn H, Matsui H. 1998. Inhibitory long-term potentiation underlies auditory conditioning of goldfish escape behavior.Nature394:182– 85 (10.1038/28172)
  262. O’Keefe J, Nadel L. 1978.The Hippocampus as a Cognitive Map.Oxford, UK: Clarendon
  263. Orban PC, Chapman PF, Brambilla R. 1999. Is the Ras-MAPK signalling pathway necessary for long-term memory formation?Trends Neurosci.22:38–44 (10.1016/S0166-2236(98)01306-X)
  264. O’Reilly RC. 1998. Six principles for biologically-based computational models of cortical cognition.Trends Cogn. Sci.2:455–62 (10.1016/S1364-6613(98)01241-8)
  265. Otawa S, Takagi K, Ogawa H. 1995. NMDA and non-NMDA receptors mediate taste afferent inputs to cortical taste neurons in rats.Exp. Brain Res.106:391–402 (10.1007/BF00231062)
  266. Parsons CG, Danysz W, Quack G. 1999. Memantine is a clinically well toleratedN-methyl-D-aspartate (NMDA) receptor antagonist—a review of preclinical data.Neuropharmacology38:735–67 (10.1016/S0028-3908(99)00019-2)
  267. Paulsen O, Moser EI. 1998. A model of hippocampal memory encoding and retrieval: GABAergic control of synaptic plasticity.Trends Neurosci.21:273–78 (10.1016/S0166-2236(97)01205-8)
  268. Pavlides C, Greenstein YJ, Grudman M, Winson J. 1988. Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of the theta rhythm.Brain Res.439:383–87 (10.1016/0006-8993(88)91499-0)
  269. Petersen CC, Malenka RC, Nicoll RA, Hopfield JJ. 1998. All-or-none potentiation at CA3-CA1 synapses.Proc. Natl. Acad. Sci. USA95:4732–37 (10.1073/pnas.95.8.4732)
  270. Pike FG, Meredith RM, Olding AWA, Paulsen O. 1999. Postsynaptic bursting is essential for ‘Hebbian’ induction of LTP at excitatory synapses in rat hippocampus.J. Physiol.In press (10.1111/j.1469-7793.1999.0571p.x)
  271. Pitkanen A, Savander V, LeDoux JE. 1997. Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala.Trends Neurosci.20:517–23 (10.1016/S0166-2236(97)01125-9)
  272. 10.1016/S1059-1311(97)80034-9
  273. Rescorla RA, Wagner AR. 1972. A theory of pavlovian conditioning: the effectiveness of reinforcement and nonreinforcement. InClassical Conditioning. II: Current Research and Theory,ed. AH Black, WF Prokasy, pp. 64–69. New York: AppletonCentury-Crofts
  274. Richter-Levin G, Canevari L, Bliss TVP. 1995. Long-term potentiation and glutamate release in the dentate gyrus: links to spatial learning.Behav. Brain Res.66:37–40 (10.1016/0166-4328(94)00121-U)
  275. {'key': 'b275', 'first-page': '445', 'volume': '4', 'year': '1997', 'journal-title': 'Learn. Mem.'} / Learn. Mem. (1997)
  276. 10.1016/0028-3908(94)90181-3
  277. Riedel G, Casabona G, Reymann KG. 1995. Inhibition of long-term potentiation in the dentate gyrus of freely moving rats by the metabotropic glutamate receptor antagonist MCPG.J. Neurosci.15:87–98 (10.1523/JNEUROSCI.15-01-00087.1995)
  278. Riedel G, Wetzel W, Reymann KG. 1994. (R,S)-α-Methyl-4-carboxyphenylglycine (MCPG) blocks spatial learning in rats and long-term potentiation in the dentate gyrusin vivo.Neurosci. Lett.167:141–44 (10.1016/0304-3940(94)91047-2)
  279. Rioult-Pedotti MS, Friedman D, Hess G, Donoghue JP. 1998. Strengthening of horizontal cortical connections following skill learning.Nat. Neurosci.1:230–34 (10.1038/678)
  280. 10.1016/0896-6273(95)90070-5
  281. 10.1523/JNEUROSCI.17-15-05928.1997
  282. 10.1038/37601
  283. Rolls ET, Treves A. 1998.Neural Networks and Brain Function.Oxford, UK: Oxford Univ. Press. 418 pp. (10.1093/acprof:oso/9780198524328.001.0001)
  284. Roman FS, Simonetto I, Soumireu-Mourat B. 1993. Learning and memory of odor-reward association: selective impairment following horizontal diagonal band lesions.Behav. Neurosci.107:72–81 (10.1037/0735-7044.107.1.72)
  285. 10.1037//0735-7044.107.3.444
  286. 10.1523/JNEUROSCI.12-11-04501.1992
  287. 10.1016/0304-3940(86)90487-8
  288. 10.1523/JNEUROSCI.17-13-05129.1997
  289. Rosenblum K, Dudai Y, Richter-Levin G. 1996. Long-term potentiation increases tyrosine phosphorylation of theN-methyl-D-aspartate receptor subunit 2B in rat dentate gyrus in vivo.Proc. Natl. Acad. Sci. USA93:10457–60 (10.1073/pnas.93.19.10457)
  290. 10.1016/S0092-8674(00)81829-2
  291. 10.1038/322263a0
  292. Salt TE, Eaton SA. 1989. Function of nonNMDA receptors and NMDA receptors in synaptic responses to natural somatosensory stimulation in the ventrobasal thalamus.Exp. Brain Res.77:646–52 (10.1007/BF00249618)
  293. Sananes C, Davis M. 1992.N-methyl-D-aspartate lesions of the lateral and basolateral nuclei of the amygdala block fear-potentiated startle and shock sensitization of startle.Behav. Neurosci.106:72–80 (10.1037/0735-7044.106.1.72)
  294. 10.1038/378186a0
  295. Saucier D, Hargreaves EL, Boon F, Vanderwolf CH, Cain DP. 1996. Detailed behavioral analysis of water maze acquisition under systemic NMDA or muscarinic antagonism: nonspatial pretraining eliminates spatial learning deficits.Behav. Neurosci.110:103–16 (10.1037/0735-7044.110.1.103)
  296. 10.1016/S0028-3908(97)00040-3
  297. {'key': 'b297', 'first-page': '1', 'volume': '38', 'year': '1998', 'journal-title': 'Neuropharmacology'} / Neuropharmacology (1998)
  298. Seidenbecher T, Balschun D, Reymann KG. 1995. Drinking after water deprivation prolongs unsaturated LTP in the dentate gyrus of rats.Physiol. Behav.57:1001–4 (10.1016/0031-9384(94)00352-6)
  299. Selig DK, Nicoll RA, Malenka RC. 1999. Hippocampal long-term potentiation preserves the fidelity of postsynaptic responses to presynaptic bursts.J. Neurosci.19:1236–46 (10.1523/JNEUROSCI.19-04-01236.1999)
  300. 10.3758/BF03327232 / Psychobiology (1990)
  301. Sharp PE, McNaughton BL, Barnes CA. 1989. Exploration-dependent modulation of evoked response in fascia dentata: fundamental observations and time-course.Psychobiology17:257–69 (10.1007/BF03337777)
  302. 10.1016/S0306-4522(97)00188-7
  303. Shors TJ, Matzel LD. 1997. Long-term potentiation: What’s learning got to do with it?Behav. Brain Sci.20:597–655 (10.1017/S0140525X97001593)
  304. Sillito AM. 1985. Inhibitory circuits and orientation selectivity in the visual cortex. InModels of the Visual Cortex,ed. D Rose, VG Dobson, pp. 396–407. New York: Wiley
  305. Sillito AM, Murphy PC, Salt TE, Moody CI. 1990. Dependence of retinogeniculate transmission in cat on NMDA receptors.J. Neurophysiol.63:347–55 (10.1152/jn.1990.63.2.347)
  306. Silva AJ, Kogan JH, Frankland PW, Kida S. 1998. CREB and memory.Annu. Rev. Neurosci.21:127–48 (10.1146/annurev.neuro.21.1.127)
  307. 10.1126/science.1321493
  308. Silva AJ, Rosahl TW, Chapman PF, Marowitz Z, Friedman E, et al. 1996. Impaired learning in mice with abnormal short-lived plasticity.Curr. Biol.6:1509–18 (10.1016/S0960-9822(96)00756-7)
  309. 10.1126/science.1378648
  310. Squire LR. 1992. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans.Psychol. Rev.99:195–231 (10.1037/0033-295X.99.2.195)
  311. Stäubli U, Chun D. 1996. Factors regulating the reversibility of long-term potentiation.J. Neurosci.16:853–60 (10.1523/JNEUROSCI.16-02-00853.1996)
  312. Stäubli U, Chun D, Lynch G. 1998. Timedependent reversal of long-term potentiation by an integrin antagonist.J. Neurosci.18:3460–69 (10.1523/JNEUROSCI.18-09-03460.1998)
  313. Stäubli U, Ivy G, Lynch G. 1984. Hippocampal denervation causes rapid forgetting of olfactory information in rats.Proc. Natl. Acad. Sci. USA.81:5885–87 (10.1073/pnas.81.18.5885)
  314. Stäubli U, Lynch G. 1987. Stable hippocampal long-term potentiation elicited by theta pattern stimulation.Brain Res.435:227–34 (10.1016/0006-8993(87)91605-2)
  315. Stäubli U, Lynch G. 1990. Stable depression of potentiated synaptic responses in the hippocampus with 1–5 Hz stimulation.Brain Res.513:113–18 (10.1016/0006-8993(90)91096-Y)
  316. Stäubli U, Perez Y, Xu FB, Rogers G, Ingvar M, et al. 1994. Centrally active modulators of glutamate receptors facilitate the induction of long-term potentiation in vivo.Proc. Natl. Acad. Sci. USA91:11158–62 (10.1073/pnas.91.23.11158)
  317. 10.1037//0735-7044.103.1.54
  318. 10.1002/(SICI)1098-1063(1998)8:5<444::AID-HIPO5>3.0.CO;2-X
  319. 10.1002/(SICI)1098-1063(1999)9:2<118::AID-HIPO4>3.0.CO;2-8
  320. 10.1097/00001756-199808240-00002
  321. Stevens CF. 1998. A million dollar question: Does LTP equal memory?Neuron20:1–2 (10.1016/S0896-6273(00)80426-2)
  322. 10.1038/364147a0
  323. 10.1002/hipo.450030206
  324. Sutherland RJ, Whishaw IQ, Kolb B. 1988. Contributions of cingulate cortex to two forms of spatial learning and memory.J. Neurosci.8:1863–72 (10.1523/JNEUROSCI.08-06-01863.1988)
  325. Tang Y-P, Shimizi E, Dube GR, Rampon C, Kerchner GA, et al. 1999. Genetic enhancement of learning and memory in mice.Nature.In press (10.1038/43432)
  326. 10.1038/7217
  327. Thiels E, Barrionuevo G, Berger TW. 1994. Excitatory stimulation during postsynaptic inhibition induces long-term depression in hippocamapusin vivo.J. Neurophysiol.72:3009–16 (10.1152/jn.1994.72.6.3009)
  328. Thiels E, Norman ED, Barrionuevo G, Klann E. 1998. Transient and persistent increases in protein phosphatase activity during longterm depression in the adult hippocampusin vivo.Neuroscience86:1023–29 (10.1016/S0306-4522(98)00135-3)
  329. 10.1002/(SICI)1098-1063(1996)6:1<43::AID-HIPO8>3.0.CO;2-8
  330. Thomas MJ, Watabe AM, Moody TD, Makhinson M, O’Dell TJ. 1998. Postsynaptic complex spike bursting enables the induction of LTP by theta frequency synaptic stimulation.J. Neurosci.18:7118–26 (10.1523/JNEUROSCI.18-18-07118.1998)
  331. 10.1007/BF01245040
  332. Tompa P, Friedrich P. 1998. Synaptic metaplasticity and the local charge effect in postsynaptic densities.Trends Neurosci.21:97– 102 (10.1016/S0166-2236(97)01176-4)
  333. Tonkiss J, Morris RGM, Rawlins JNP. 1988. Intra-ventricular infusion of the NMDA antagonist AP5 impairs performance on a non-spatial operant DRL task in the rat.Exp. Brain Res.73:181–88 (10.1007/BF00279671)
  334. Tonkiss J, Rawlins JNP. 1991. The competitive NMDA antagonist AP5, but not the noncompetitive antagonist MK801, induces a delay-related impairment in spatial working memory in rats.Exp. Brain Res.85:349–58 (10.1007/BF00229412)
  335. 10.1093/cercor/8.8.719
  336. Tricklebank MD, Singh L, Oles RJ, Preston C, Iversen SD. 1989. The behavioral effects of MK-801: a comparison with antagonists acting non-competitively and competitively at the NMDA receptor.Eur. J. Pharmacol.167:127–35 (10.1016/0014-2999(89)90754-1)
  337. 10.1016/S0092-8674(00)81826-7
  338. 10.1016/S0092-8674(00)81827-9
  339. Tucci S, Rada P, Hernandez L. 1998. Role of glutamate in the amygdala and lateral hypothalamus in conditioned taste aversion.Brain Res.813:44–49 (10.1016/S0006-8993(98)00884-1)
  340. Turski L, Klockgether T, Turski WA, Schwarz M, Sontag KH. 1990. Blockade of excitatory neurotransmission in the globus pallidus induces rigidity and akinesia in the rat: implications for excitatory neurotransmission in pathogenesis of Parkinson’s diseases.Brain Res.512:125–31 (10.1016/0006-8993(90)91180-O)
  341. van Praag H, Kempermann G, Gage F. 1999. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus.Nat. Neurosci.2:266–70 (10.1038/6368)
  342. 10.1126/science.277.5324.376
  343. Vazdarjanova A, McGaugh JL. 1998. Basolateral amygdala is not critical for cognitive memory of contextual fear conditioning.Proc. Natl. Acad. Sci. USA95:15003–7 (10.1073/pnas.95.25.15003)
  344. Wagner JJ, Alger BE. 1995. GABAergic and developmental influences on homosynaptic LTD and depotentiation in rat hippocampus.J. Neurosci.15:1577–86 (10.1523/JNEUROSCI.15-02-01577.1995)
  345. Wallenstein GV, Eichenbaum H, Hasselmo ME. 1998. The hippocampus as an associator of discontiguous events.Trends Neurosci.21:317–23 (10.1016/S0166-2236(97)01220-4)
  346. Wan H, Aggleton JP, Brown MW. 1999. Different contributions of the hippocampus and perirhinal cortex to recognition memory.J. Neurosci.19:1142–48 (10.1523/JNEUROSCI.19-03-01142.1999)
  347. Wang Y, Rowan MJ, Anwyl R. 1997. Induction of LTD in the dentate gyrusin vitrois NMDA receptor independent, but dependent on Ca2+influx via low-voltage-activated Ca2+channels and release of Ca2+from intracellular stores.J. Neurophysiol.77:812–25 (10.1152/jn.1997.77.2.812)
  348. Weinberger NM. 1998. Physiological memory in primary auditory cortex: characteristics and mechanisms.Neurobiol. Learn. Mem.70:226–51 (10.1006/nlme.1998.3850)
  349. 10.1523/JNEUROSCI.19-23-10512.1999
  350. Willshaw D, Dayan P. 1990. Optimal plasticity from matrix memories: What goes up must come down.Neural Commun.2:85–93 (10.1162/neco.1990.2.1.85)
  351. 10.1126/science.8036517
  352. 10.1016/S0092-8674(00)80896-X
  353. 10.1038/37333
  354. 10.1038/29783
  355. 10.1073/pnas.95.6.3204
  356. 10.1016/0361-9230(91)90133-5
  357. 10.1097/00001756-199704140-00009
  358. Yeckel MF, Berger TW. 1998. Spatial distribution of potentiated synapses in hippocampus: dependence on cellular mechanisms and network properties.J. Neurosci.18:438–50 (10.1523/JNEUROSCI.18-01-00438.1998)
  359. 10.1126/science.284.5421.1805
  360. Zhu XO, Brown MW, McCabe BJ, Aggleton JP. 1995. Effects of the novelty or familiarity of visual stimuli on the expression of the immediate early gene c-fosin rat brain.Neuroscience69:821–29 (10.1016/0306-4522(95)00320-I)
Dates
Type When
Created 23 years, 1 month ago (July 27, 2002, 7:45 a.m.)
Deposited 1 year, 7 months ago (Jan. 6, 2024, 12:02 a.m.)
Indexed 2 days, 15 hours ago (Aug. 30, 2025, 12:20 p.m.)
Issued 25 years, 6 months ago (March 1, 2000)
Published 25 years, 6 months ago (March 1, 2000)
Published Print 25 years, 6 months ago (March 1, 2000)
Funders 0

None

@article{Martin_2000, title={Synaptic Plasticity and Memory: An Evaluation of the Hypothesis}, volume={23}, ISSN={1545-4126}, url={http://dx.doi.org/10.1146/annurev.neuro.23.1.649}, DOI={10.1146/annurev.neuro.23.1.649}, number={1}, journal={Annual Review of Neuroscience}, publisher={Annual Reviews}, author={Martin, S. J. and Grimwood, P. D. and Morris, R. G. M.}, year={2000}, month=mar, pages={649–711} }