Long-term potentiation and depression as putative mechanisms for memory formation

Neural Plasticity and Memory: From Genes to Brain Imaging

Volumn , Issue , 2007, Pages 15-46

  Escobar, Martha L ^a   Derrick, Brian ^b  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 80052172774     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (135)

1. Bliss, T.V.P. and Lomo, T. Long-lasting potentiation of synaptic transmission in thedentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol., 232, 331, 1973.
2. Bliss, T. and Gardner-Medwin, A. Long-lasting potentiation of synaptic transmissionin the dentate area of the unanesthetized rabbit following stimulation of the perforant path. J. Physiol., 232, 357, 1973.
3. Xie, X., Barrionuevo, G., and Berger, T.W. Differential expression of short-termpotentiation by AMPA and NMDA receptors in dentate gyrus. Learn. Mem., 3, 115, 1996.
4. Hanse, E. and Gustafsson, B. Onset and stabilization of NMDA receptor-dependenthippocampal long-term potentiation. Neurosci. Res. 20, 15, 1994.
5. Martinez, C.O., Do, V.H., and Derrick, B.E. Associative LTP among afferents to the CA3 region in vivo. Brain Res. 94, 86, 2002.
6. Mehta, M.R., Barnes, C.A., and McNaughton B.L. Experience-dependent asymmetricexpansion of hippocampal place fields. Proc. Natl. Acad. Sci. USA, 94, 8918, 1997.
7. Kentros, C., Hargreaves, E., Hawkins, R.D., Kandel, E.R., Shapiro, M., and Muller R.V. Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. Science, 280, 2121, 1998.
8. Staubli, U. and Lynch, G. Stable hippocampal long-term potentiation elicited by” theta” pattern stimulation. Brain Res., 435, 227, 1987.
9. McNaughton, B.L., Douglas, R.M., and Goddard, D.V. Synaptic enhancement infascia dentata: cooperativity among coactive afferents. Brain Res., 157, 277, 1978.
10. Gustafsson, B., Wigstrom, H., Abraham, W.C., and Huang, Y.Y. Long-term potentiation in the hippocampus using depolarizing current pulses as the conditioning stimulus to single volley synaptic potentials. J. Neurosci., 7, 774, 1987.
11. Barnes, C.A. Memory deficits associated with senescence: a neurophysiological andbehavioral study in the rat. J. Comp. Physiol. Psychol., 93, 74, 1979.
12. Squire, L.R. Memory and the Brain. Oxford University Press, New York, 1987.
13. Wilson, M.A. and McNaughton, B.L. Reactivation of hippocampal ensemble memories during sleep. Science, 265, 676, 1994.
14. Cartwright, R.D. The role of sleep in changing our minds: a psychologist’s discussionof papers on memory reactivation and consolidation in sleep. Learn. Mem., 11, 660, 2004.
15. Bontempi, B., Laurent-Demir, C., Destrade, C., and Jaffard, R. Time-dependentreorganization of brain circuitry underlying long-term memory storage. Nature, 400, 671, 1999.
16. Villarreal, D., Do, V., Haddad, E., and Derrick, B.E. NMDA antagonists sustain LTPand spatial memory: evidence for active processes underlying LTP decay. Nat. Neurosci., 5, 48, 2002.
17. Hebb, D.O. The Organization of Behavior. John Wiley & Sons, New York, 1949.
18. Barrionuevo, G., Schottler, F., Lynch, G. The effects of repetitive low frequencystimulation on control and “potentiated” synaptic responses in the hippocampus. Life Sci., 27, 2385, 1980.
19. Bear, M.F. Homosynaptic long-term depression: a mechanism for memory? Proc. Natl. Acad. Sci. USA, 96, 9457, 1999.
20. Mulkey, R.M., Herron, C.E., and Malenka, R.C. An essential role for protein phosphatases in hippocampal long-term depression. Science, 261, 1051, 1993.
21. Christie, B.R. and Abraham, W.C. Priming of associative long-term depression in thedentate gyrus by theta frequency synaptic activity. Neuron, 9, 79, 1992.
22. Debanne, D. and Thompson, S.M. Associative long-term depression in the hippocampus in vitro. Hippocampus, 6, 9, 1996.
23. Wickens, J.R. and Abraham, W.C. Involvement of L-type calcium channels in heterosynaptic long-term depression in the hippocampus. Neurosci. Lett. 130, 128, 1991.
24. 2+ channels. J. Neurosci., 15, 8290, 2000.
25. Massey, P.V. et al. Differential roles of NR2A and NR2B-containing NMDA receptorsin cortical long-term potentiation and long-term depression. J. Neurosci. 24, 7821, 2004.
26. Moult, P.R. et al. Tyrosine phosphatases regulate AMPA receptor trafficking during metabotropic glutamate receptor-mediated long-term depression. J. Neurosci., 26, 2544, 2006.
27. 2+ can potentiate and depress mossy fiber synaptic responses in rat hippocampal CA3 pyramidal neurons. J. Neurophysiol., 91, 1596, 2004.
28. Lei S. et al. Depolarization-induced long-term depression at hippocampal mossy fiberCA3 pyramidal neuron synapses. J. Neurosci., 23, 9786, 2003.
29. Domenici, M.R., Berretta, N., and Cherubini, E. Two distinct forms of long-term depression coexist at the mossy fiber-CA3 synapse in the hippocampus during development. Proc. Natl. Acad. Sci. USA, 95, 8310, 1998.
30. Derrick, B.E. and Martinez, J.L., Jr. Associative bidirectional modifications at thehippocampal mossy fibre CA3 synapse. Nature, 381, 429, 1996.
31. Kobayashi, K., Manabe, T., and Takahashi, T. Presynaptic long-term depression atthe hippocampal mossy fiber CA3 synapse. Science, 273, 648, 1996.
32. Brown, G.D., Dalloz, P., and Hulme, C. Mathematical and connectionist models ofhuman memory: a comparison. Memory, 3, 113, 1995.
33. Skaggs, W.E. and McNaughton, B.L. Computational approaches to hippocampal function. Curr. Opin. Neurobiol., 2, 209, 1992.
34. Morris, R.G.M. Computational neuroscience: modeling the brain, in Parallel Distributed Processing Implications for Psychology and Neurobiology. Morris, R.G.M., Ed., Oxford University Press, New York, 1989, p. 203.
35. Gustafsson, B. and Wigstrom, H. Long-term potentiation in the hippocampal CA1 region: its induction and early temporal development. Progr. Brain Res., 83, 223, 1990.
36. Malinow, R. and Miller, J.P. Postsynaptic hyperpolarization during conditioningreversibly blocks long-term potentiation. Nature, 320, 529, 1986.
37. Lynch, G., Larson, J., Kelso, S., Barrionuevo, G., and Schottler, F. Intracellularinjections of EGTA block induction of hippocampal long-term potentiation. Nature, 305, 719, 1983.
38. Johnston, D., Williams, S., Jaffe, D., and Gray, R. NMDA receptor-independentlong-term potentiation. Annu. Rev. Physiol., 54, 489, 1992.
39. Yeckel, M.F., Kapur, A., and Johnston., D., Multiple forms of LTP in hippocampalCA3 neurons use a common postsynaptic mechanism. Nat. Neurosci., 2, 625, 1999.
40. Sanes, J.R. and Lichtman, J.W. Can molecules explain long-term potentiation? Nat. Neurosci., 2, 597, 1999.
41. 2+/calmodulin kinase II enhances channel conductance of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate type glutamate receptors. Proc. Natl. Acad. Sci. USA, 96, 3269, 1999.
42. Oh, M.C. et al. Extrasynaptic membrane trafficking regulated by GluR1 serine 845 phosphorylation primes AMPA receptors for long-term potentiation. J. Biol. Chem., 281, 752, 2006.
43. Bourtchuladze, R. et al. Deficient long-term memory in mice with a targeted mutationof the cAMP-responsive element-binding protein. Cell, 79, 59, 1994.
44. Frey, U. and Morris, R.G. Synaptic tagging: implications for late maintenance ofhippocampal long-term potentiation. Trends Neurosci., 385, 533, 1998.
45. Harris, E.W. and Cotman, C.W. Long-term potentiation of guinea pig mossy fiberresponses is not blocked by N-methyl D-aspartate antagonists. Neurosci. Lett., 70, 132, 1986.
46. French, P.J. et al. Subfield-specific immediate early gene expression associated with hippocampal long-term potentiation in vivo, Eur. J. Neurosci., 13, 968, 2001.
47. Stanton, P.K. and Sarvey, J.M. Rapid spine delivery and redistribution of AMPAreceptors after synaptic NMDA receptor activation: blockade of long-term potentiation in rat hippocampal CA1 region by inhibitors of protein synthesis. J. Neurosci., 4, 3080, 1984.
48. Krug, M., Lossner, B. and Ott, T. Anisomycin blocks the late phase of long-termpotentiation in the dentate gyrus of freely moving rats. Brain Res. Bull., 13, 39, 1984.
49. Otani, S., Marshall, C.J., Tate, W.P., Goddard, G.V., and Abraham, W.C. Maintenanceof long-term potentiation in rat dentate gyrus requires protein synthesis but not messenger RNA synthesis immediately post-tetanization. Neuroscience, 28, 519, 1989.
50. Jaffe, D. and Johnston, D. Induction of long-term potentiation at hippocampal mossyfibers follow a Hebbian rule. J. Neurophys., 64, 948, 1990.
51. Williams, S. and Johnston, D. Long-term potentiation of hippocampal mossy fibersynapses is blocked by postsynaptic injection of calcium chelators. Neuron, 3, 583, 1989.
52. Derrick, B.E. and Martinez, J.L., Jr. Opioid receptor activation is one factor underlying the frequency dependence of mossy fiber LTP induction. J. Neurosci., 14, 4359, 1994.
53. Jung, M.W. and McNaughton, B.L. Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus, 3, 165, 1993.
54. Marr, D. Simple memory: a theory for archicorticortex. Proc. R. Soc. London B, 262, 23, 1971.
55. Morris, R.G.M. and McNaughton, B.L. Memory storage in a distributed model ofhippocampal formation. Trends Neurosci., 10, 408, 1987.
56. Abraham, W. and Bear, M. Metaplasticity: plasticity of synaptic plasticity. Trends Neurosci, 19, 126, 1996.
57. Escobar, M., Barea-Rodriguez, E.J., Derrick, B.E., and Martinez, J.L., Jr. Mossy fibersynaptogenesis is induced by high frequency stimulation of mossy fibers. Brain Res., 751, 330, 1997.
58. Derrick, B.E., York, A., and Martinez, J.L., Jr. Increases in granule cell neurogenesisfollowing stimulation that induces mossy fiber LTP. Brain Res., 857, 800, 2000.
59. Morgan, S.L. and Teyler, T.J. Electrical stimuli patterned after the theta-rhythm inducemultiple forms of LTP. J. Neurophysiol., 86, 1289, 2001.
60. Raymond, C.R. and Redman S.J. Different calcium sources are narrowly tuned tothe induction of different forms of LTP. J. Neurophysiol., 88, 249, 2002.
61. Hoffman, D.A., Sprengel, R., and Sakmann, B. Molecular dissection of hippocampaltheta-burst pairing potentiation. Proc. Natl. Acad. Sci. USA, 99, 7740, 2002.
62. Davis, C.D., Jones, F.L., and Derrick, B.E. Novel environments enhance the inductionand maintenance of long-term potentiation in the dentate gyrus. J. Neurosci., 24, 6497, 2004.
63. Li, S., Cullen, W.K., Anwyl, R., and Rowan, M.J. Dopamine-dependent facilitationof LTP induction in hippocampal CA1 by exposure to spatial novelty. Nat. Neurosci., 6, 526, 2003.
64. Straube, T., Korz, V., Balschun, D., and Frey, J.U. Requirement of beta-adrenergicreceptor activation and protein synthesis for LTP-reinforcement by novelty in rat dentate gyrus. J. Physiol., 552, 953, 2003.
65. Turrigiano, G.G., Leslie, K.R., Desai, N.S., Ruterford, L.C., and Nelson, S.B. Activitydependent scaling of quantal amplitude in neocortical neurons. Nature, 391, 892, 1998.
66. Bienenstock, E.L., Cooper, L.N., and Munro, P.W. Theory for the development ofneuron selectivity: orientation specificity and binocular interaction in visual cortex. J. Neurosci., 2, 32, 1982.
67. Quinlan, E.M., Olstein, D.H., and Bear, M.F. Bidirectional, experience-dependentregulation of N-methyl-D-aspartate receptor subunit composition in the rat visual cortex during postnatal development. Proc. Natl. Acad. Sci. USA, 96, 876, 1999.
68. Philpot, B.D., Sekhar, A.K., Shouval, H.Z. and Bear, M.F. Visual experience anddeprivation bidirectionally modify the composition and function of NMDA receptors in visual cortex. Neuron, 29, 157, 2001.
69. Rogan, M.T., Staubli, U.V., and LeDoux, J.E. Fear conditioning induces associativelong-term potentiation in the amygdala. Nature, 390, 604, 1997.
70. McKernan, M.G. and Shinnick-Gallagher, P. Fear conditioning induces a lastingpotentiation of synaptic currents in vitro. Nature, 390, 607, 1997.
71. Rioult-Pedotti, M.S., Friedman, D., Hess, G., and Donoghue, J.P., Strengthening ofhorizontal cortical connections following skill learning. Nat. Neurosci., 1, 230, 1998.
72. Escobar, M.L. and Bermúdez-Rattoni, F. Long-term potentiation in the insular cortexenhances conditioned taste aversion retention. Brain Res., 852, 208, 2000.
73. Malenka, R.C. and Bear, M. LTP and LTD: an embarrassment of riches. Neuron, 44, 5, 2004.
74. Rittenhouse, C.D., Shouval, H.Z., Paradiso, M.A., and Bear, M.F. Monocular deprivation induces homosynaptic long-term depression in visual cortex. Nature, 397, 347, 1999.
75. Allen, C.B., Celikel, T., and Feldman, D.E. Long-term depression induced by sensorydeprivation during cortical map plasticity in vivo. Nat. Neurosci., 6, 291, 2003.
76. Celikel, T., Szostak, V.A., and Feldman, D.E. Modulation of spike timing by sensorydeprivation during induction of cortical map plasticity. Nat. Neurosci., 7, 534, 2004.
77. Heynen, A.J. et al. Molecular mechanisms for loss of visual cortical responsivenessfollowing brief monocular deprivation. Nat. Neurosci., 6, 854, 2003.
78. Sawtell, N.B., Huber, K.M., Roder, J.C., and Bear, M.F. Induction of NMDA receptordependent long-term depression in visual cortex does not require metabotropic glutamate receptors. J. Neurophysiol., 82, 3594, 1999.
79. Hyman, S.E. and Malenka, R.C. Addiction and the brain: the neurobiology of compulsion and its persistence. Nat. Rev. Neurosci., 2, 695, 2001.
80. Kelley, A.E. Memory and addiction: Shared neural circuitry and molecular mechanisms. Neuron, 44, 161, 2004.
81. Ungless, M.A., Whistier, J.L., Malenka, R.C., and Bonci, A. Single cocaine exposurein vivo induces long-term potentiation in dopamine neurons. Nature, 411, 583, 2001.
82. Faleiro, L.J., Jones, S., and Kauer, J.A. Rapad synaptic plasticity of glutamatergicsynapses on dopamine neurons in the ventral tegmental area in response to acute amphetamine injection. Neuropsychopharmacology, 29, 2115, 2004.
83. Liao, D., Hessler, N.A., and Malinow, R. Activation of post-synaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature, 375, 400, 1995.
84. Malinow, R. and Malenka, R.C. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci., 25, 103, 2002.
85. Collingridge, G.L., Isaac, J.T.R., and Wang, Y.T. Receptor trafficking and synapticplasticity. Nat. Rev. Neurosci., 5, 952, 2004.
86. Emptage, N.J., Reid, C.A., Fine, A., and Bliss, T.V. Optical quantal analysis revealsa presynaptic component of LTP at hippocampal Schaffer-associational synapses. Neuron, 38, 797, 2003.
87. Choi, S., Klingauf, J., and Tsien, R.W. Fusion pore modulation as a presynapticmechanism contributing to expression of long-term potentiation. Philos. Trans. R. Soc. London B, 358, 695, 2003.
88. Zakharenko, S.S. et al. Presynaptic BDNF required for a presynaptic but not postsynaptic component of LTP at hippocampal CA1-CA3 synapses. Neuron, 39, 975, 2003.
89. Lauri, S.E. et al. Functional maturation of CA1 synapses involves activity-dependentloss of tonic kainate receptor-mediated inhibition of glutamate release. Neuron, 50, 415, 2006.
90. Schulz, P.E., Cook, E.P., and Johnston, D. Changes in paired-pulse facilitation suggestpresynaptic involvement in long-term potentiation. J. Neurosci., 14, 5325, 1994.
91. Bayer, K.U., De Koninck, P., Leonard, A.S., Hell, J.W., and Schulman, H. Interactionwith the NMDA receptor locks CaMKII in an active conformation. Nature, 411, 801, 2001.
92. Leonard, A.S. et al. Regulation of calcium/calmodulin-dependent protein kinase IIdocking to N-methyl-D-aspartate receptors by calcium/calmodulin and alpha-actinin. J. Biol. Chem., 277, 48441, 2002.
93. Si, S.H. et al. Phosphorylation of the AMPA receptor GluR1 subunit is required forsynaptic plasticity and retention of spatial memory. Science, 284, 1755, 1999.
94. Luthi, A. et al. Hippocampal LTD expression involves a pool of AMPARs regulatedby the NSF-GluR2 interaction. Neuron, 24, 389, 1999.
95. Lynch, G. and Baudry, M. The biochemistry of memory: a new and specific hypothesis. Science, 224, 1057, 1984.
96. Lisman, J.E. and McIntyre, C.C. Synaptic plasticity: a molecular memory switch. Curr. Biol., 11, 788, 2001.
97. Boehm, J. and Malinow, R. AMPA receptor phosphorylation during synaptic plasticity. Biochem. Soc. Trans., 33, 1354, 2005.
98. Perez-Otaño, I. and Ehlers, M.D. Homeostatic plasticity and NMDA receptor trafficking. Trends Neurosci., 28, 229, 2002.
99. Lohof, A.M., Ip, N.Y., and Poo, M.M. Potentiation of developing neuromuscularsynapses by the neurotrophins NT-3 and BDNF. Nature, 363, 350, 1993.
100. Kang, H. and Schuman, E.M. Long-lasting neurotrophin-induced enhancement ofsynaptic transmission in the adult hippocampus. Science, 267, 1658, 1995.
101. Ying, S.W. et al. Brain-derived neurotrophic factor induces long-term potentiation inintact adult hippocampus: requirement for ERK activation coupled to CREB and upregulation of Arc synthesis. J. Neurosci., 22, 1532, 2002.
102. Bramham, C.R. and Messaoudi, E. BDNF function in adult synaptic plasticity: thesynaptic consolidation hypothesis. Progr. Neurobiol., 76, 99, 2005.
103. Pang, P.T. et al. Cleavage of proBDNF by tPA/plasmin is essential for long-termhippocampal plasticity. Science, 306, 487, 2004.
104. McAllister, A.K., Katz, L.C., and Lo, D.C. Neurotrophins and synaptic plasticity. Annu. Rev. Neurosci., 22, 295, 1999.
105. Jiang, B. et al. Brain-derived neurotrophic factor induces long-lasting potentiation ofsynaptic transmission in visual cortex in vivo in young rats, but not in the adult. Eur. J. Neurosci., 14, 1219, 2001.
106. Tokuyama, W., Okuno, H., Hashimoto, T., Li, Y.X., and Miyashita, Y. BDNF upregulation during declarative memory formation in monkey inferior temporal cortex. Nat. Neurosci., 3, 1134, 2000.
107. Escobar, M.L., Figueroa-Guzmán, Y., and Gómez-Palacio Schjetnan, A. In vivo insular cortex LTP induced by brain-derived neurotrophic factor. Brain Res., 991, 274, 2003.
108. Castillo, V., Figueroa-Guzmán, Y., and Escobar, M.L. Brain-derived neurotrophicfactor enhances conditioned taste aversion retention. Brain Res., 1067, 250, 2006.
109. Yamada, K., Mizuno, M., and Nabeshima, T. Role for brain-derived neurotrophicfactor in learning and memory. Life Sci., 70, 735, 2002.
110. Minichiello, L. et al. Mechanism of Trk-mediated hippocampal long-term potentiation. Neuron, 36, 121, 2002.
111. Tyler, W.J., Alonso, M., Bramham, C.R., and Pozzo-Miller, L.D. From acquisition toconsolidation: on the role of brain-derived neurotrophic factor signaling in hippocampal-dependent learning. Learn. Mem. 9, 224, 2002.
112. Morris, R.G., Anderson, E., Lynch, G.S., and Baudry, M. Selective impairment oflearning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist AP5. Nature, 319, 774, 1986.
113. Davis, S., Butcher, S.P., and Morris, R.G. The NMDA receptor antagonist D-2-amino5-phosphonopentanoate (D-AP5) impairs spatial learning and LTP in vivo at intracerebral concentrations comparable to those that block LTP in vitro. J. Neurosci., 12, 21, 1992.
114. Buzsaki, G. Theta oscillations in the hippocampus. Neuron, 33, 325, 2002.
115. Pitkanen, M., Sirvio, J., Ylinen, A., Koivisto, E., and Riekkinen, P., Sr. Effects ofNMDA receptor modulation on hippocampal type 2 theta activity in rats. Gen. Pharmacol., 26, 1065, 1995.
116. Leung, L.W. and Desborough, K.A. APV, an N-methyl-D-aspartate receptor antagonist, blocks the hippocampal theta rhythm in behaving rats. Brain Res., 463, 148, 1988.
117. Tsien, J.Z., Huerta, P.T., and Tonegawa, S. The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell, 87, 1327, 1996.
118. Hinds, H.L., Tonegawa, S., and Malinow, R. CA1 long-term potentiation is diminishedbut present in hippocampal slices from alpha-CaMKII mutant mice. Learn. Mem., 5, 344, 1998.
119. Giese, K.P., Fedorov, N.B., Filipkowski, R.K., and Silva, A.J. Auto-phosphorylationat Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. Science, 279, 870, 1998.
120. Nakazawa, K. et al. Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science. 297, 211, 2002.
121. Castro, C.A., Silbert, L.H., McNaughton, B.L., and Barnes, C.A. Recovery of spatiallearning deficits after decay of electrically induced synaptic enhancement in the hippocampus. Nature, 342, 545, 1989.
122. Barnes, C.A. et al. LTP saturation and spatial learning disruption: effects of taskvariables and saturation levels. J. Neurosci., 14, 5793, 1994.
123. McNaughton, B.L., Barnes, C.A., Meltzer, J., and Sutherland, R.J. Hippocampalgranule cells are necessary for normal spatial learning but not for spatially selective pyramidal cell discharge. Exp. Brain Res., 76, 485, 1989.
124. Moser, E.I., Krobert, K.A., Moser, M.B., and Morris, R.G. Impaired spatial learningafter saturation of long-term potentiation. Science, 281, 2038, 1998.
125. O’Keefe, J. and Nadel, L. The Hippocampus as a Cognitive Map. Oxford University Press, New York, 1978.
126. Wilson, M.A. and McNaughton, B.L. Dynamics of the hippocampal ensemble codefor space. Science, 261, 1055, 1993.
127. Jeffery, K.J. et al. A proposed architecture for the neural representation of spatialcontext. Neurosci. Biobehav. Rev., 28, 201, 2004.
128. Dragoi, G., Harris, K.D., and Buzsaki, G. Place representation within hippocampalnetworks is modified by long-term potentiation. Neuron, 39, 843, 2003.
129. Treves, A. and Rolls, E.T. Computational analysis of the role of the hippocampus inmemory. Hippocampus, 4, 374, 1994.
130. Henze, D.A., Wittner, L., and Buzsaki, G. Single granule cells reliably dischargetargets in the hippocampal CA3 network in vivo. Nat. Neurosci., 5, 790, 2002.
131. Derrick, B.E. and Martinez, J.L., Jr. A unique opioid peptide-dependent form oflong-term potentiation is found in the CA3 region of the rat hippocampus. Adv. Biosci., 75, 213, 1989.
132. Do, V., Martinez, C.O., Martinez, J.L.M., and Derrick, B.E. Long-term potentiationin direct perforant path projections to hippocampal area CA3 in vivo. J. Neurophys., 87, 669, 2002.
133. Kosub, K.A., Do, V.H., and Derrick, B.E. NMDA receptor antagonists block heterosynaptic long-term depression (LTD) but not long-term potentiation (UP) in the CA3 region following lateral perforant path stimulation. Neurosci. Lett., 374, 29, 2005.
134. Ekstrom, A.D., Meltzer, J., McNaughton, B.L., and Barnes C.A. NMDA receptorantagonism blocks experience-dependent expansion of hippocampal “place fields”. Neuron, 31, 631, 2001.
135. Guzowski, J.F., Knierim, J.J., and Moser, E.I. Ensemble dynamics of hippocampalregions CA3 and CA1. Neuron, 44, 581, 2005.