Simultaneous induction of long-term potentiation in the hippocampus and the amygdala by entorhinal cortex activation: Mechanistic and temporal profiles

Neuroscience

Volumn 120, Issue 4, 2003, Pages 1125-1135

  Yaniv, D ^a,c   Vouimba, R M ^a,b   Diamond, D M ^b   Richter Levin, G ^a  

^a UNIVERSITY OF HAIFA   (Israel)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Emotion; Fear; Memory; NMDA; Plasticity; Rat

Indexed keywords

4 (3 PHOSPHONOPROPYL) 2 PIPERAZINECARBOXYLIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; DENTATE GYRUS; ENTORHINAL CORTEX; HIPPOCAMPUS; LONG TERM POTENTIATION; MALE; MEMORY; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; TEMPORAL CORTEX;

EID: 0041632302     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(03)00386-5     Document Type: Article

References (119)

1. Aggleton J.P. The amygdala: a functional analysis. 2nd edition: 2000;Oxford University Press, New York.
2. Akirav I., Richter-Levin G. Biphasic modulation of hippocampal plasticity by behavioral stress and basolateral amygdala stimulation in the rat. J Neurosci. 19:1999;10530-10535.
3. Akirav I., Richter-Levin G. Mechanisms of amygdala modulation of hippocampal plasticity. J Neurosci. 22:2002;9912-9921.
4. Amaral D.G., Price J.L., Pitkänen A., Carmichael S.T. Anatomical organization of the primate amygdaloid complex. Aggleton J.P. The amygdala: neurobiological aspects of emotion, memory and mental dysfunction. 1992;1-66 Oxford University Press, New York.
5. Amorapanth P., LeDoux J.E., Nader K. Different lateral amygdala outputs mediate reactions and actions elicited by a fear-arousing stimulus. Nat Neurosci. 3:2000;74-79.
6. + channel blocker in the hippocampus. Nature. 349:1991;67-69.
7. Bannerman D.M., Yee B.K., Lemaire M., Jarrard L., Iversen S.D., Rawlins J.N., Good M.A. Contextual fear conditioning is disrupted by lesions of the subcortical, but not entorhinal, connections to the hippocampus. Exp Brain Res. 141:2001;304-311.
8. Bannerman D.M., Yee B.K., Lemaire M., Wilbrecht L., Jarrard L., Iversen S.D., Rawlins J.N., Good M.A. The role of the entorhinal cortex in two forms of spatial learning and memory. Exp Brain Res. 141:2001;281-303.
9. Barnes C.A. Involvement of LTP in memory are we searching under the streetlight? Neuron. 15:1995;751-754.
10. Bauer E.P., Schafe G.E., LeDoux J.E. NMDA receptors and L-type voltage-gated calcium channels contribute to long-term potentiation and different components of fear memory formation in the lateral amygdala. J Neurosci. 22:2002;5239-5249.
11. Blair H.T., Schafe G.E., Bauer E.P., Rodrigues S.M., LeDoux J.E. Synaptic plasticity in the lateral amygdala a cellular hypothesis of fear conditioning . Learn Mem. 8:2001;229-242.
12. Bliss T.V., Collingridge G.L. A synaptic model of memory long-term potentiation in the hippocampus . Nature. 361:1993;31-39.
13. Bliss T.V., Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol. 232:1973;331-356.
14. Bohbot V.D., Allen J.J., Nadel L. Memory deficits characterized by patterns of lesions to the hippocampus and parahippocampal cortex. Ann NY Acad Sci. 911:2000;355-368.
15. Brothers L.A., Finch D.M. Physiological evidence for an excitatory pathway from entorhinal cortex to amygdala in the rat. Brain Res. 359:1985;10-20.
16. Burgess N., Maguire E.A., O'Keefe J. The human hippocampus and spatial and episodic memory. Neuron. 35:2002;625-641.
17. Burwell R.D. The parahippocampal region corticocortical connectivity . Ann NY Acad Sci. 911:2000;25-42.
18. Buzsaki G. Theta oscillations in the hippocampus. Neuron. 33:2003;325-340.
19. Cahill L. Modulation of long-term memory storage in humans by emotional arousal. Aggleton J.P. The amygdala: neurobiological aspects of emotion, memory and mental dysfunction. 2000;425-455 Oxford University Press, New York.
20. Chapman P.F., Bellavance L.L. Induction of long-term potentiation in the basolateral amygdala does not depend on NMDA receptor activation. Synapse. 11:1992;310-318.
21. Chapman P.F., Chattarji S. Synaptic plasticity in the amygdala. Aggleton J.P. The amygdala: a functional analysis, 2nd edition. 2000;117-153 Oxford University Press, New York.
22. Clugnet M.C., LeDoux J.E. 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. 10:1990;2818-2824.
23. Cotman C.W., Monaghan D.T. Anatomical organization of excitatory amino acid receptors and their properties. Adv Exp Med Biol. 203:1986;237-252.
24. Cotman C.W., Monaghan D.T., Ottersen O.P., Storm-Mathisen J. Anatomical organization of excitatory amino-acid receptors and their pathways. Trends Neurosci. 10:1987;273-280.
25. Davis M. The role of the amygdala in conditioned and unconditioned fear and anxiety. Aggleton J.P. The amygdala: a functional analysis, 2nd edition. 2000;213-287 Oxford University Press, New York.
26. Davis M., Whalen P.J. The amygdala vigilance and emotion . Mol Psychiatry. 6:2001;13-34.
27. Danober L., Heinbockel T., Driesang R.B., Pape H.C. Synaptic mechanisms of NMDA-mediated hyperpolarization in lateral amygdaloid projection neurons. Neuroreport. 11:2000;2501-2506.
28. Dolorfo C.L., Amaral D.G. Entorhinal cortex of the rat organization of intrinsic connections . J Comp Neurol. 398:1998;49-82.
29. Eichenbaum H. Declarative memory insights from cognitive neurobiology . Annu Rev Psychol. 48:1997;547-572.
30. Farb C.R., LeDoux J.E. Afferents from rat temporal cortex synapse on lateral amygdala neurons that express NMDA and AMPA receptors. Synapse. 33:1999;218-229.
31. Ferry B., Magistretti P.J., Pralong E. High potency of the orally-active NMDA-receptor antagonist CGP 40 116 in inhibiting excitatory postsynaptic potentials of rat basolateral amygdala neurones in vitro. Neuropharmacology. 36:1997;1555-1559.
32. Franks K.M., Sejnowski T.J. Complexity of calcium signaling in synaptic spines. Bioessays. 24:2002;1130-1144.
33. Frey U., Huang Y.Y., Kandel E.R. Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science. 260:1993;1661-1664.
34. Gean P.W., Chang F.C., Huang C.C., Lin J.H., Way L.J. Long-term enhancement of EPSP and NMDA receptor-mediated synaptic transmission in the amygdala. Brain Res Bull. 31:1993;7-11.
35. Gloor P. The temporal lobe and the limbic system. 1997;Oxford University Press, New York.
36. Goosens K.A., Maren S. Long-term potentiation as a substrate for memory evidence from studies of amygdaloid plasticity and Pavlovian fear conditioning . Hippocampus. 12:2002;592-599.
37. Grover L.M., Teyler T.J. Two components of long-term potentiation induced by different patterns of afferent activation. Nature. 347:1990;477-479.
38. Harris E.W., Ganong A.H., Monaghan D.T., Watkins J.C., Cotman C.W. Action of 3-((+/-)-2-carboxypiperazin-4-yl)-propyl-1-phosphonic acid (CPP) a new and highly potent antagonist of N-methyl-D-aspartate receptors in the hippocampus . Brain Res. 382:1986;174-177.
39. Huang E.P. Synaptic plasticity going through phases with LTP . Curr Biol. 8:1998;R350-R352.
40. Huang Y.Y., Kandel E.R. Postsynaptic induction and PKA-dependent expression of LTP in the lateral amygdala. Neuron. 21:1998;169-178.
41. Huang Y.Y., Li X.C., Kandel E.R. cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase. Cell. 79:1994;69-79.
42. 2+ channels in the induction of LTP . J Neurosci. 13:1993;568-576.
43. Huang Y.Y., Martin K.C., Kandel E.R. Both protein kinase A and mitogen-activated protein kinase are required in the amygdala for the macromolecular synthesis-dependent late phase of long-term potentiation. J Neurosci. 20:2000;6317-6325.
44. Huang Y.Y., Nguyen P.V., Abel T., Kandel E.R. Long-lasting forms of synaptic potentiation in the mammalian hippocampus. Learn Mem. 3:1996;74-85.
45. Ikegaya Y., Saito H., Abe K. The basomedial and basolateral amygdaloid nuclei contribute to the induction of long-term potentiation in the dentate gyrus in vivo. Eur J Neurosci. 8:1996;1833-1839.
46. Insel T.R., Miller L.P., Gelhard R.E. The ontogeny of excitatory amino acid receptors in rat forebrain: I. N-methyl-D-aspartate and quisqualate receptors. Neuroscience. 35:1990;31-43.
47. Izquierdo I., Medina J.H. Role of the amygdala, hippocampus and entorhinal cortex in memory consolidation and expression. Braz J Med Biol Res. 26:1993;573-589.
48. Johnston D., Amaral D.G. Hippocampus. Shepherd G.M. The synaptic organization of the brain, 4th edition. 1998;417-458 Oxford University Press, New York.
49. Jones R.S.G. Entorhinal-hippocampal connections a speculative view of their function . Trends Neurosci. 16:1993;58-64.
50. Kandel E.R. Genes, synapses, and long-term memory. J Cell Physiol. 173:1997;124-125.
51. Kapp B.S., Frysinger R.C., Gallagher M., Haselton J.R. Amygdala central nucleus lesions effect on heart rate conditioning in the rabbit . Physiol Behav. 23:1979;1109-1117.
52. Killcross S., Robbins T.W., Everitt B.J. Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala. Nature. 388:1997;377-380.
53. Kim J.J., Diamond D.M. The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci. 3:2002;453-462.
54. Kohler C. Cytochemical architecture of the entorhinal area. Adv Exp Med Biol. 203:1986;83-98.
55. Krettek L.E., Price J.L. A description of the amygdaloid complex in the rat and cat with observations on intra-amygdaloid axonal connections. J Comp Neurol. 178:1978;255-280.
56. Krug M., Lossner B., Ott T. Anisomycin blocks the late phase of long-term potentiation in the dentate gyrus of freely moving rats. Brain Res Bull. 13:1984;39-42.
57. Lang E.J., Paré D. Synaptic responsiveness of interneurons of the cat lateral amygdaloid nucleus. Neuroscience. 83:1998;877-889.
58. LeDoux J.E. Emotion circuits in the brain. Annu Rev Neurosci. 23:2000;155-184.
59. Lee O., Lee C.J., Choi S. Induction mechanisms for L-LTP at thalamic input synapses to the lateral amygdala requirement of mGluR5 activation . Neuroreport. 13:2002;685-691.
60. Lehmann J., Schneider J., McPherson S., Murphy D.E., Bernard P., Tsai C., Bennett D.A., Pastor G., Steel D.J., Boehm C., et al. CPP, a selective N-methyl-D-aspartate (NMDA)-type receptor antagonist characterization in vitro and in vivo . J Pharmacol Exp Ther. 240:1987;737-746.
61. Li X.F., Armony J.L., LeDoux J.E. GABAA and GABAB receptors differentially regulate synaptic transmission in the auditory thalamo-amygdala pathway an in vivo microiontophoretic study and a model . Synapse. 24:1996;115-124.
62. Li H., Weiss S.R., Chuang D.M., Post R.M., Rogawski M.A. Bidirectional synaptic plasticity in the rat basolateral amygdala characterization of an activity-dependent switch sensitive to the presynaptic metabotropic glutamate receptor antagonist 2S-alpha-ethylglutamic acid . J Neurosci. 18:1998;1662-1670.
63. Lin C.H., Yeh S.H., Lin C.H., Lu K.T., Leu T.H., Chang W.C., Gean P.W. A role for the PI-3 kinase signaling pathway in fear conditioning and synaptic plasticity in the amygdala. Neuron. 31:2001;841-851.
64. Liu Z., Murray E.A., Richmond B.J. Learning motivational significance of visual cues for reward schedules requires rhinal cortex. Nat Neurosci. 3:2000;1307-1315.
65. Lynch G. Memory enhancement the search for mechanism-based drugs . Nat Neurosci. 5:2002;1035-1038.
66. Maren S., Fanselow M.S. Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulation in vivo. J Neurosci. 15:1995;7548-7564.
67. Martin S.J., Grimwood P.D., Morris R.G. Synaptic plasticity and memory an evaluation of the hypothesis . Annu Rev Neurosci. 23:2000;649-711.
68. Mascagni F., McDonald A.J., Coleman J.R. Corticoamygdaloid and corticocortical projections of the rat temporal cortex a Phaseolus vulgaris leucoagglutinin study . Neuroscience. 57:1993;697-715.
69. Matzel L.D., Shors T.J. Long-term potentiation and associative memory: can the mechanism subserve the process? Holscher C. Neuronal mechanisms of memory formation: concepts of long-term potentiation and beyond. 2001;294-324 Cambridge University Press, Cambridge, UK.
70. McDonald A.J. Cortical pathways to the mammalian amygdala. Prog Neurobiol. 55:1998;257-332.
71. McDonald A.J., Mascagni F. Projections of the lateral entorhinal cortex to the amygdala a Phaseolus vulgaris leucoagglutinin study in the rat . Neuroscience. 77:1997;445-459.
72. McGaugh J.L. Memory consolidation and the amygdala a systems perspective . Trends Neurosci. 25:2002;456-461.
73. Metcalfe J., Jacobs W.J. Emotional memory the effects of stress on "cool" and "hot" memory systems . Psychol Learn Mem. 38:1998;187-222.
74. Morris R.G., Anderson E., Lynch G.S., Baudry M. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature. 319:1986;774-776.
75. Morris R.G., Frey U. Hippocampal synaptic plasticity role in spatial learning or the automatic recording of attended experience? Philos Trans R Soc Lond B Biol Sci. 352:1997;1489-1503.
76. Nguyen P.V., Abel T., Kandel E.R. Requirement of a critical period of transcription for induction of a late phase of LTP. Science. 265:1994;1104-1107.
77. Okulski P., Hess G., Kaczmarek L. Anisomycin treatment paradigm affects duration of long-term potentiation in slices of the amygdala. Neuroscience. 114:2002;1-5.
78. Otani S., Abraham W.C. Inhibition of protein synthesis in the dentate gyrus, but not the entorhinal cortex, blocks maintenance of long-term potentiation in rats. Neurosci Lett. 106:1989;175-180.
79. Packard M.G., Cahill L. Affective modulation of multiple memory systems. Curr Opin Neurobiol. 11:2001;752-756.
80. Paré D., Collins D.R. Neuronal correlates of fear in the lateral amygdala multiple extracellular recordings in conscious cats . J Neurosci. 20:2000;2701-2710.
81. Paré D., Collins D.R., Pelletier J.G. Amygdala oscillations and the consolidation of emotional memories. Trends Cogn Sci. 6:2002;306-314.
82. Paré D., Gaudreau H. Projection cells and interneurons of the lateral and basolateral amygdala distinct firing patterns and differential relation to theta and delta rhythms in conscious cats . J Neurosci. 16:1996;3334-3350.
83. Paré D., Smith Y. Intrinsic circuitry of the amygdaloid complex common principles of organization in rats and cats . Trends Neurosci. 21:1998;240-241.
84. Paxinos G., Watson C. The rat brain in stereotaxic coordinates. 3rd ed: 1997;Academic Press, New York.
85. Pikkarainen M., Ronkko S., Savander V., Insausti R., Pitkanen A. Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the hippocampal formation in rat. J Comp Neurol. 403:1999;229-260.
86. Pitkänen A. Connectivity of the rat amygdaloid complex. Aggleton J.P. The amygdala: a functional analysis, 2nd edition. 2000;31-115 Oxford University Press, New York.
87. Pitkänen A., Pikkarainen M., Nurminen N., Ylinen A. Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat a review . Ann NY Acad Sci. 911:2000;369-391.
88. Pitkänen A., Savander V., LeDoux J.E. Organization of intra-amygdaloid circuitries in the rat an emerging framework for understanding functions of the amygdala . Trends Neurosci. 20:1997;517-523.
89. Repa J.C., Muller J., Apergis J., Desrochers T.M., Zhou Y., LeDoux J.E. Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nat Neurosci. 4:2001;724-731.
90. Rescorla R.A. Experimental extinction. Mowrer R.R., Klein S. Handbook of contemporary learning theories. 2001;119-154 Erlbaum, Mahwah, NJ.
91. Richter-Levin G., Akirav I. Amygdala-hippocampus dynamic interaction in relation to memory. Mol Neurobiol. 22:2000;11-20.
92. Rogan M.T., LeDoux J.E. LTP is accompanied by commensurate enhancement of auditory-evoked responses in a fear conditioning circuit. Neuron. 15:1995;127-136.
93. Rogan M.T., Staubli U.V., LeDoux J.E. Fear conditioning induces associative long-term potentiation in the amygdala. Nature. 390:1997;604-607.
94. Rosenkranz J.A., Grace A.A. Dopamine-mediated modulation of odour-evoked amygdala potentials during pavlovian conditioning. Nature. 417:2002;282-287.
95. Royer S., Paré D. Bidirectional synaptic plasticity in intercalated amygdala neurons and the extinction of conditioned fear responses. Neuroscience. 115:2002;455-462.
96. Saucier D., Cain D.P. Spatial learning without NMDA receptor-dependent long-term potentiation. Nature. 378:1995;186-189.
97. Schwartz S.P., Coleman P.D. Neurons of origin of the perforant path. Exp Neurol. 74:1981;305-312.
98. Schafe G.E., Nader K., Blair H.T., LeDoux J.E. Memory consolidation of Pavlovian fear conditioning a cellular and molecular perspective . Trends Neurosci. 24:2001;540-546.
99. Silva A.J. Molecular and cellular cognitive studies of the role of synaptic plasticity in memory. J Neurobiol. 54:2003;224-237.
100. Stevens C.F. A million dollar question does LTP = memory? Neuron. 20:1998;1-2.
101. Steward O., Scoville S.A. Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J Comp Neurol. 169:1976;347-370.
102. Stoop R., Pralong E. Functional connections and epileptic spread between hippocampus, entorhinal cortex and amygdala in a modified horizontal slice preparation of the rat brain. Eur J Neurosci. 12:2000;3651-3663.
103. Storm-Mathisen J., Ottersen O.P. Anatomy of putative glutamatergic neurons. Avoli M., Reader T.A., Dykes R.W., Gloor P. Neurotransmitters and cortical function: from molecules to mind. 1988;39-70 Plenum Press, New York.
104. Suzuki W.A. The anatomy, physiology and functions of the perirhinal cortex. Curr Opin Neurobiol. 6:1996;179-186.
105. Tsvetkov E., Carlezon W.A., Benes F.M., Kandel E.R., Bolshakov V.Y. Fear conditioning occludes LTP-induced presynaptic enhancement of synaptic transmission in the cortical pathway to the lateral amygdala. Neuron. 34:2002;289-300.
106. Veening J.G. Cortical afferents of the amygdaloid complex in the rat an HRP study . Neurosci Lett. 8:1978;191-195.
107. Walker D.L., Davis M. The role of amygdala glutamate receptors in fear learning, fear-potentiated startle, and extinction. Pharmacol Biochem Behav. 71:2002;379-392.
108. Watanabe Y., Ikegaya Y., Saito H., Abe K. Roles of GABAA, NMDA and muscarinic receptors in induction of long-term potentiation in the medial and lateral amygdala in vitro. Neurosci Res. 21:1995;317-322.
109. Weisskopf M.G., Bauer E.P., LeDoux J.E. L-type voltage-gated calcium channels mediate NMDA-independent associative long-term potentiation at thalamic input synapses to the amygdala. J Neurosci. 19:1999;10512-10519.
110. Weisskopf M.G., LeDoux J.E. Distinct populations of NMDA receptors at subcortical and cortical inputs to principal cells of the lateral amygdala. J Neurophysiol. 81:1999;930-934.
111. White N.M., McDonald R.J. Multiple parallel memory systems in the brain of the rat. Neurobiol Learn Mem. 77:2002;125-184.
112. Witter M.P., Groenewegen H.J. Laminar origin and septotemporal distribution of entorhinal and perirhinal projections to the hippocampus in the cat. J Comp Neurol. 224:1984;371-385.
113. Witter M.P., Groenewegen H.J., Lopes da Silva F.H., Lohman A.H. Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog Neurobiol. 33:1989;161-253.
114. Witter M.P., Van Hoesen G.W., Amaral D.G. Topographical organization of the entorhinal projection to the dentate gyrus of the monkey. J Neurosci. 9:1989;216-228.
115. Witter M.P., Wouterlood F.G., Naber P.A., Van Haeften T. Anatomical organization of the parahippocampal-hippocampal network. Ann NY Acad Sci. 911:2000;1-24.
116. Wu J., Rush A., Rowan M.J., Anwyl R. NMDA receptor- and metabotropic glutamate receptor-dependent synaptic plasticity induced by high frequency stimulation in the rat dentate gyrus in vitro. J Physiol. 533:2001;745-755.
117. Wyss J.M. An autoradiographic study of the efferent connections of the entorhinal cortex in the rat. J Comp Neurol. 199:1981;495-512.
118. Yaniv D., Schafe G.E., LeDoux J.E., Richter-Levin G. A gradient of plasticity in the amygdala revealed by cortical and subcortical stimulation, in vivo. Neuroscience. 106:2001;613-620.
119. Yaniv D., Vouimba R.M., Diamond D., Richter-Levin G. Late-phase long-term potentiation in the amygdala induced by entorhinal cortex stimulation, in vivo. Behav Pharm. 12:2001;S111.