Fear conditioning occludes late-phase long-term potentiation at thalamic input synapses onto the lateral amygdala in rat brain slices

Neuroscience Letters

Volumn 506, Issue 1, 2012, Pages 121-125

  Hong, Ingie ^a   Kim, Jeongyeon ^a   Song, Beomjong ^a   Park, Kyungjoon ^b   Shin, Kisoon ^b   Eom, Khee Dong ^c   Han, Pyung Lim ^d   Lee, Sukwon ^a   Choi, Sukwoo ^a  

^a Seoul National University   (South Korea)

^b Kyung Hee University   (South Korea)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^d Ewha Womans University   (South Korea)

Author keywords

Amygdala; Depotentiation; Fear conditioning; Fear extinction; Late phase LTP; Learning and memory; Synaptic plasticity

Indexed keywords

3,5 DIHYDROXYPHENYLGLYCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN REGION; CONDITIONING; CONTROLLED STUDY; EX VIVO STUDY; FEAR; IN VIVO STUDY; LATERAL AMYGDALA; LONG TERM POTENTIATION; MALE; MEMORY CONSOLIDATION; NONHUMAN; PRIORITY JOURNAL; RAT; SENSITIZATION; STIMULUS RESPONSE; STRESS; SYNAPTIC POTENTIAL; THALAMUS;

AMYGDALA; ANIMALS; BIOPHYSICS; CONDITIONING (PSYCHOLOGY); ELECTRIC STIMULATION; EXTINCTION, PSYCHOLOGICAL; FEAR; LONG-TERM POTENTIATION; MALE; METHOXYHYDROXYPHENYLGLYCOL; NEURAL PATHWAYS; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES; THALAMUS; TIME FACTORS;

EID: 84855195444     PISSN: 03043940     EISSN: 18727972     Source Type: Journal    
DOI: 10.1016/j.neulet.2011.10.063     Document Type: Article

References (41)

1. Barnes C.A., Jung M.W., McNaughton B.L., Korol D.L., Andreasson K., Worley P.F. LTP saturation and spatial learning disruption: effects of task variables and saturation levels. J. Neurosci. 1994, 14:5793-5806.
2. Bashir Z.I., Collingridge G.L. An investigation of depotentiation of long-term potentiation in the CA1 region of the hippocampus. Exp. Brain Res. 1994, 100:437-443.
3. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361:31-39.
4. Bordi F., LeDoux J.E. Response properties of single units in areas of rat auditory thalamus that project to the amygdala. I. Acoustic discharge patterns and frequency receptive fields. Exp. Brain Res. 1994, 98:261-274.
5. Clem R.L., Huganir R.L. Calcium-permeable AMPA receptor dynamics mediate fear memory erasure. Science 2010, 330:1108-1112.
6. Collingridge G.L., Peineau S., Howland J.G., Wang Y.T. Long-term depression in the CNS. Nat. Rev. Neurosci. 2010, 11:459-473.
7. Dalton G.L., Wang Y.T., Floresco S.B., Phillips A.G. Disruption of AMPA receptor endocytosis impairs the extinction, but not acquisition of learned fear. Neuropsychopharmacology 2008, 33:2416-2426.
8. Davis M. The role of the amygdala in fear and anxiety. Annu. Rev. Neurosci. 1992, 15:353-375.
9. Ehrlich I., Humeau Y., Grenier F., Ciocchi S., Herry C., Luthi A. Amygdala inhibitory circuits and the control of fear memory. Neuron 2009, 62:757-771.
10. Frey U., Schollmeier K., Reymann K.G., Seidenbecher T. Asymptotic hippocampal long-term potentiation in rats does not preclude additional potentiation at later phases. Neuroscience 1995, 67:799-807.
11. Gale G.D., Anagnostaras S.G., Godsil B.P., Mitchell S., Nozawa T., Sage J.R., Wiltgen B., Fanselow M.S. Role of the basolateral amygdala in the storage of fear memories across the adult lifetime of rats. J. Neurosci. 2004, 24:3810-3815.
12. Hong I., Song B., Lee S., Kim J., Kim J., Choi S. Extinction of cued fear memory involves a distinct form of depotentiation at cortical input synapses onto the lateral amygdala. Eur. J. Neurosci. 2009, 30:2089-2099.
13. 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. 2000, 20:6317-6325.
14. Kim J., Lee S., Park K., Hong I., Song B., Son G., Park H., Kim W.R., Park E., Choe H.K., Kim H., Lee C., Sun W., Kim K., Shin K.S., Choi S. Amygdala depotentiation and fear extinction. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:20955-20960.
15. Kim J., Park S., Lee S., Choi S. Amygdala depotentiation ex vivo requires mitogen-activated protein kinases and protein synthesis. Neuroreport 2009, 20:517-520.
16. Kim J., Song B., Hong I., Lee J., Park S., Eom J.Y., Lee C.J., Lee S., Choi S. Reactivation of fear memory renders consolidated amygdala synapses labile. J. Neurosci. 2010, 30:9631-9640.
17. Lüscher C., Huber K.M. Group 1 mGluR-dependent synaptic long-term depression: mechanisms and implications for circuitry and disease. Neuron 2010, 65:445-459.
18. 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 2002, 13:685-691.
19. Lin C.H., Yeh S.H., Leu T.H., Chang W.C., Wang S.T., Gean P.W. Identification of calcineurin as a key signal in the extinction of fear memory. J. Neurosci. 2003, 23:1574-1579.
20. Malenka R.C., Bear M.F. LTP and LTD: an embarrassment of riches. Neuron 2004, 44:5-21.
21. McCormack S.G., Stornetta R.L., Zhu J.J. Synaptic AMPA receptor exchange maintains bidirectional plasticity. Neuron 2006, 50:75-88.
22. McKernan M.G., Shinnick-Gallagher P. Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 1997, 390:607-611.
23. Monfils M.H., Cowansage K.K., Klann E., LeDoux J.E. Extinction-reconsolidation boundaries: key to persistent attenuation of fear memories. Science 2009, 324:951-955.
24. Myers K.M., Davis M. Mechanisms of fear extinction. Mol. Psychiatry 2007, 12:120-150.
25. Pape H.C., Pare D. Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol. Rev. 2010, 90:419-463.
26. Pitkanen 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. 1997, 20:517-523.
27. Quirk G.J., Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 2008, 33:56-72.
28. Reymann K.G., Frey J.U. The late maintenance of hippocampal LTP: requirements, phases, 'synaptic tagging', 'late-associativity' and implications. Neuropharmacology 2007, 52:24-40.
29. Rioult-Pedotti M.S., Friedman D., Donoghue J.P. Learning-induced LTP in neocortex. Science 2000, 290:533-536.
30. Rodrigues S.M., Schafe G.E., LeDoux J.E. Molecular mechanisms underlying emotional learning and memory in the lateral amygdala. Neuron 2004, 44:75-91.
31. Rogan M.T., Staubli U.V., LeDoux J.E. Fear conditioning induces associative long-term potentiation in the amygdala. Nature 1997, 390:604-607.
32. Rumpel S., LeDoux J., Zador A., Malinow R. Postsynaptic receptor trafficking underlying a form of associative learning. Science 2005, 308:83-88.
33. Sajikumar S., Navakkode S., Frey J.U. Protein synthesis-dependent long-term functional plasticity: methods and techniques. Curr. Opin. Neurobiol. 2005, 15:607-613.
34. Schroeder B.W., Shinnick-Gallagher P. Fear learning induces persistent facilitation of amygdala synaptic transmission. Eur. J. Neurosci. 2005, 22:1775-1783.
35. Shi S., Hayashi Y., Esteban J.A., Malinow R. Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 2001, 105:331-343.
36. Snyder E.M., Philpot B.D., Huber K.M., Dong X., Fallon J.R., Bear M.F. Internalization of ionotropic glutamate receptors in response to mGluR activation. Nat. Neurosci. 2001, 4:1079-1085.
37. Staubli U., Lynch G. Stable hippocampal long-term potentiation elicited by 'theta' pattern stimulation. Brain Res. 1987, 435:227-234.
38. 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 2002, 34:289-300.
39. Weinberger N.M. Learning-induced changes of auditory receptive fields. Curr. Opin. Neurobiol. 1993, 3:570-577.
40. Whitlock J.R., Heynen A.J., Shuler M.G., Bear M.F. Learning induces long-term potentiation in the hippocampus. Science 2006, 313:1093-1097.
41. Yao Y., Kelly M.T., Sajikumar S., Serrano P., Tian D., Bergold P.J., Frey J.U., Sacktor T.C. PKM zeta maintains late long-term potentiation by N-ethylmaleimide-sensitive factor/GluR2-dependent trafficking of postsynaptic AMPA receptors. J. Neurosci. 2008, 28:7820-7827.