Bidirectional synaptic plasticity in intercalated amygdala neurons and the extinction of conditioned fear responses

Neuroscience

Volumn 115, Issue 2, 2002, Pages 455-462

  Royer, S ^a   Pare D ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

Amygdaloid complex; Fear conditioning; Infralimbic cortex; Inhibition

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT;

AMYGDALOID NUCLEUS; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; DEPRESSION; FEAR; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PULSE RATE; SYNAPSE;

AMYGDALA; ANIMALS; CONDITIONING (PSYCHOLOGY); ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; EXTINCTION, PSYCHOLOGICAL; FEAR; GUINEA PIGS; LONG-TERM DEPRESSION (PHYSIOLOGY); LONG-TERM POTENTIATION; MEMBRANE POTENTIALS; NEURONAL PLASTICITY; NEURONS; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 0037146621     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(02)00455-4     Document Type: Article

References (50)

1. Baker J.D., Azorlosa J.L. The NMDA antagonist MK-801 blocks the extinction of Pavlovian fear conditioning. Behav. Neurosci. 110:1996;618-620.
2. Bear M.F., Abraham W.C. Long-term depression in hippocampus. Annu. Rev. Neurosci. 19:1996;437-462.
3. Bliss T., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 361:1993;31-39.
4. Cahill L., Weinberger N.M., Roozendaal B., McGaugh J.L. Is the amygdala a locus of 'conditioned fear'? Some questions and caveats. Neuron. 23:1999;227-228.
5. Carroll R.C., Beattie E.C., von Zastrow M., Malenka R.C. Role of AMPA receptor endocytosis in synaptic plasticity. Nat. Rev. Neurosci. 2:2001;315-324.
6. Chapman, P.F., Chattarji, S., 2000. Synaptic plasticity in the amygdala. In: Aggleton, J.P. (Ed.), The Amygdala: A Functional Analysis. Oxford University, Oxford, pp. 117-153.
7. Chapman P.F., Kairiss E.W., Keenan C.L., Brown T.H. Long-term synaptic potentiation in the amygdala. Synapse. 6:1990;271-278.
8. Cox J., Westbrook R.F. The NMDA receptor antagonist MK-801 blocks acquisition and extinction of conditioned hypoalgesia responses in the rat. Q. J. Exp. Psychol. B. 47B:1994;187-210.
9. Creager R., Dunwiddie T., Lynch G. Paired-pulse and frequency facilitation in the CA1 region of the in vitro rat hippocampus. J. Physiol. Lond. 299:1980;409-424.
10. Danober L., Pape H.C. Mechanisms and functional significance of a slow inhibitory potential in neurons of the lateral amygdala. Eur. J. Neurosci. 10:1998;853-867.
11. Davis, M., 2000. The role of the amygdala in conditioned and unconditioned fear and anxiety. In: Aggleton, J.P. (Ed.), The Amygdala: A Functional Analysis. Oxford University, Oxford, pp. 213-287.
12. Falls W.A., Miserendino M.J.D., Davis M. Extinction of fear-potentiated startle: blockade by infusion of an NMDA antagonist into the amygdala. J. Neurosci. 12:1992;854-863.
13. Hopkins D.A., Holstege G. Amygdaloid projections to the mesencephalon, pons and medulla oblongata in the cat. Exp. Brain Res. 32:1978;529-547.
14. Huang Y.-Y., Kandel E.R. Postsynaptic induction and PKA-dependent expression of LTP in the lateral amygdala. Neuron. 21:1998;169-178.
15. Kapp B.S., Frysinger R.C., Gallagher M., Haselton J.R. Amygdala central nucleus lesions: effects on heart rate conditioning in the rabbit. Physiol. Behav. 23:1979;1109-1117.
16. Katz B., Miledi R. The role of calcium in neuromuscular facilitation. J. Physiol. Lond. 195:1968;481-492.
17. Krettek J.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.
18. LeDoux, J.E., 2000. The amygdala and emotion: A view through fear. In: Aggleton, J.P. (Ed.), The Amygdala: A Functional Analysis. Oxford University, Oxford, pp. 289-310.
19. Lee H., Kim J.J. Amygdalar NMDA receptors are critical for new fear learning in previously fear-conditioned rats. J. Neurosci. 18:1998;8444-8454.
20. Lee H.K., Barbarosie M., Kameyama K., Bear M.F., Huganir R.L. Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature. 405:2000;955-959.
21. Lisman J.E., Zhabotinsky A.M. A model of synaptic memory: a CaMKII/PP1 switch that potentiates transmission by organizing an AMPA receptor anchoring assembly. Neuron. 31:2001;191-201.
22. Liu X.B., Jones E.G. Localization of alpha type II calcium calmodulin-dependent protein kinase at glutamatergic but not gamma-aminobutyric acid (GABAergic) synapses in thalamus and cerebral cortex. Proc. Natl. Acad. Sci. USA. 93:1996;7332-7336.
23. Mahanty N.K., Sah P. Calcium-permeable AMPA receptors mediate long-term potentiation in interneurons in the amygdala. Nature. 394:1998;683-687.
24. Malenka R.C., Nicoll R.A. NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms. Trends Neurosci. 16:1993;521-527.
25. Manabe T., Wyllie D., Perkel D.J., Nicoll R.A. Modulation of synaptic transmission and long-term potentiation: CA1 region of the hippocampus. J. Neurophysiol. 70:1993;1451-1459.
26. Maren S., Fanselow M.S. Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulation in vivo. J. Neurosci. 15:1995;7548-7564.
27. McBain C.J., Freund T.E., Mody I. Glutamatergic synapses onto hippocampal interneurons: precision timing without lasting plasticity. Trends Neurosci. 22:1999;228-235.
28. McDonald A.J., Augustine J.R. Localization of GABA-like immunoreactivity in the monkey amygdala. Neuroscience. 52:1993;281-294.
29. McDonald A.J., Mascagni F., Guo L. Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience. 71:1996;55-75.
30. McDonald A.J., Muller J.F., Mascagni F. GABAergic innervation of alpha type II calcium/calmodulin-dependent protein kinase immunoreactive pyramidal neurons in the rat basolateral amygdala. J. Comp. Neurol. 446:2002;199-218.
31. McKernan M.G., Shinnick-Gallagher P. Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature. 390:1997;607-611.
32. Milad, M.R., Quirk, G.J., 2002. Neurons in medial prefrontal cortex signal memory for fear extinction. Nature (in press).
33. Morgan M.A., Romanski L.M., LeDoux J.E. Extinction of emotional learning: contribution of medial prefrontal cortex. Neurosci. Lett. 163:1993;109-113.
34. Nitecka L., Ben-Ari Y. Distribution of GABA-like immunoreactivity in the rat amygdaloid complex. J. Comp. Neurol. 266:1987;45-55.
35. Paré, D., Royer, S., Smith, Y., Lang, E.J., 2002. Contextual inhibitory gating of impulse traffic in the intra-amygdaloid network. Ann. N.Y. Acad. Sci., in press.
36. Paré D., Smith Y. Distribution of GABA immunoreactivity in the amygdaloid complex of the cat. Neuroscience. 57:1993;1061-1076.
37. Paré D., Smith Y. The intercalated cell masses project to the central and medial nuclei of the amygdala in cats. Neuroscience. 57:1993;1077-1090.
38. Quirk G.J., Repa J.C., LeDoux J.E. Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat. Neuron. 15:1995;1029-1039.
39. Quirk G.J., Russo G.K., Barron J.L., Lebron K. The role of ventromedial prefrontal cortex in the recovery of extinguished fear. J. Neurosci. 20:2000;6225-6231.
40. Rammes G., Eder M., Dodt H.-U., Kochs E., Zieglgänsberger W. Long-term depression in the basolateral amygdala of the mouse involves the activation of interneurons. Neuroscience. 107:2001;85-97.
41. 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.
42. Rescorla, R.A., 2001. Experimental extinction. In: Mowrer, R.R., Klein, S. (Eds.), Handbook of Contemporary Learning Theories. Erlbaum, Mahwah, NJ, pp. 119-154.
43. Rescorla R.A., Heth C.D. Reinstatement of fear to an extinguished conditioned stimulus. J. Exp. Psychol. 1:1975;88-96.
44. Royer S., Martina M., Paré D. An inhibitory interface gates impulse traffic between the input and output stations of the amygdala. J. Neurosci. 19:1999;10575-10583.
45. Royer S., Martina M., Paré D. Polarized synaptic interactions between intercalated neurons of the amygdala. J. Neurophysiol. 83:2000;3509-3518.
46. Santini E., Muller R.U., Quirk G.J. Consolidation of extinction learning involves transfer from NMDA-independent to NMDA-dependent memory. J. Neurosci. 21:2001;9009-9017.
47. 2+ signaling pathway in GABAergic neurons of the hippocampus. Proc. Natl. Acad. Sci. USA. 95:1998;3245-3250.
48. Veening J.G., Swanson L.W., Sawchenko P.E. The organization of projections from the central nucleus of the amygdala to brainstem sites involved in central autonomic regulation: a combined retrograde transport-immunohistochemical study. Brain Res. 303:1984;337-357.
49. Walker D.L., Ressler K.J., Lu K.T., Davis M. Facilitation of conditioned fear extinction by systemic administration or intra-amygdala infusions of D-cycloserine as assessed with fear-potentiated startle in rats. J. Neurosci. 22:2002;2343-2351.
50. Wang S.-J., Gean P.-W. Long-term depression of excitatory synaptic transmission in the rat amygdala. J. Neurosci. 19:1999;10656-10663.