Impaired long-term potentiation and enhanced neuronal excitability in the amygdala of CaV1.3 knockout mice

Neurobiology of Learning and Memory

Volumn 92, Issue 4, 2009, Pages 519-528

  McKinney, Brandon C ^a,b   Sze, Wilson ^c   Lee, Benjamin ^c   Murphy, Geoffrey G ^b,c  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Afterhyperpolarization; Conditioned fear; L type voltage gated calcium channels; Long term potentiation; Memory mechanisms; Spike accommodation

Indexed keywords

CALCIUM CHANNEL L TYPE;

AFTERHYPERPOLARIZATION; AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONDITIONING; CONTROLLED STUDY; FEAR; FEMALE; GENE DELETION; IN VITRO STUDY; KNOCKOUT MOUSE; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE STEADY POTENTIAL; NONHUMAN; SPIKE WAVE; SYNAPTIC TRANSMISSION; WILD TYPE;

ACTION POTENTIALS; AMYGDALA; ANIMALS; CALCIUM CHANNELS, L-TYPE; ELECTRIC STIMULATION; FEMALE; LONG-TERM POTENTIATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS;

EID: 69949090356     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2009.06.012     Document Type: Article

References (59)

1. Alger B.E., and Nicoll R.A. Epileptiform burst afterhyperpolarization: Calcium-dependent potassium potential in hippocampal CA1 pyramidal cells. Science 210 (1980) 1122-1124
2. Axmacher N., Mormann F., Fernández G., Elger C.E., and Fell J. Memory formation by neuronal synchronization. Brain Research Reviews 52 (2006) 170-182
3. Bauer E.P., LeDoux J.E., and Nader K. Fear conditioning and LTP in the lateral amygdala are sensitive to the same stimulus contingencies. Nature Neuroscience 4 (2001) 687-688
4. Bauer E.P., Schafe G.E., and 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. Journal of Neuroscience 22 (2002) 5239-5249
5. Blanchard R.J., Blanchard D.C., and Fial R.A. Hippocampal lesions in rats and their effect on activity, avoidance, and aggression. The Journal of Comparative and Physiological Psychology 71 (1970) 92-101
6. Blanton M.G., Lo Turco J.J., and Kriegstein A.R. Whole cell recording from neurons in slices of reptilian and mammalian cerebral cortex. Journal of Neuroscience Methods 30 (1989) 203-210
7. + current in hippocampal pyramidal neurons. Hippocampus 10 (2000) 198-206
8. Burwell R.D., Saddoris M.P., Bucci D.J., and Wiig K.A. Corticohippocampal contributions to spatial and contextual learning. Journal of Neuroscience 24 (2004) 3826-3836
9. Chapman P.F., Kairiss E.W., Keenan C.L., and Brown T.H. Long-term synaptic potentiation in the amygdala. Synapse 6 (1990) 271-278
10. Disterhoft J.F., Thompson L.T., Moyer Jr. J.R., and Mogul D.J. Calcium-dependent afterhyperpolarization and learning in young and aging hippocampus. Life Sciences 59 (1996) 413-420
11. Doyere V., Schafe G.E., Sigurdsson T., and LeDoux J.E. Long-term potentiation in freely moving rats reveals asymmetries in thalamic and cortical inputs to the lateral amygdala. European Journal of Neuroscience 17 (2003) 2703-2715
12. Drephal C., Schubert M., and Albrecht D. Input-specific long-term potentiation in the rat lateral amygdala of horizontal slices. Neurobiology of Learning and Memory 85 (2006) 272-282
13. Faber E.S., Callister R.J., and Sah P. Morphological and electrophysiological properties of principal neurons in the rat lateral amygdala in vitro. Journal of Neurophysiology 85 (2001) 714-723
14. Faber E.S., and Sah P. Physiological role of calcium-activated potassium currents in the rat lateral amygdala. Journal of Neuroscience 22 (2002) 1618-1628
15. + (BK) channel inactivation contributes to spike broadening during repetitive firing in the rat lateral amygdala. Journal of Physiology 552 (2003) 483-497
16. Faber E.S., and Sah P. Independent roles of calcium and voltage-dependent potassium currents in controlling spike frequency adaptation in lateral amygdala pyramidal neurons. European Journal of Neuroscience 22 (2005) 1627-1635
17. Faber E.S., and Sah P. Functions of SK channels in central neurons. Clinical and Experimental Pharmacology and Physiology 34 (2007) 1077-1083
18. Gean P.W., and Shinnick-Gallagher P. The transient potassium current, the A-current, is involved in spike frequency adaptation in rat amygdala neurons. Brain Research 480 (1989) 160-169
19. + channel inactivation, spike broadening, and after-hyperpolarization in Kvβ1.1-deficient mice with impaired learning. Learning and Memory 5 25 (1998) 7-273
20. Helton T.D., Xu W., and Lipscombe D. Neuronal L-type calcium channels open quickly and are inhibited slowly. Journal of Neuroscience 25 (2005) 10247-10251
21. Hotson J.R., and Prince D.A. A calcium-activated hyperpolarization follows repetitive firing in hippocampal neurons. Journal of Neurophysiology 43 (1980) 409-419
22. Huang Y.-Y., Martin K.C., and 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. Journal of Neuroscience 20 (2000) 6317-6325
23. Kim J.J., and Fanselow M.S. Modality-specific retrograde amnesia of fear. Science 256 (1992) 675-677
24. Kim J.J., and Jung M.W. Neural circuits and mechanisms involved in Pavlovian fear conditioning: A critical review. Neuroscience and Biobehavioral Reviews 30 (2006) 188-202
25. V1.3 contributes significantly to the generation of the AHP in CA1 pyramidal neurons. Abstract viewer/itinerary planner (2006), Society for Neuroscience, Atlanta, GA (online, program no. 131.6)
26. Lima, P. A., & Marrion, N. V. (2007). Mechanisms underlying activation of the slow AHP in rat hippocampal neurons. Brain Research.
27. Madison D.V., and Nicoll R.A. Control of the repetitive discharge of rat CA1 pyramidal neurones in vitro. Journal of Physiology 354 (1984) 319-331
28. Mahanty N.K., and Sah P. Calcium-permeable AMPA receptors mediate long-term potentiation in interneurons in the amygdala. Nature 394 (1998) 683-687
29. Maren S., Aharonov G., and Fanselow M.S. Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behavioural Brain Research 88 (1997) 261-274
30. 2+ channels in hippocampal neurons. Nature 395 (1998) 900-905
31. McKernan M.G., and Shinnick-Gallagher P. Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 390 (1997) 607-611
32. V1.3 mediates consolidation, but not extinction, of contextually conditioned fear in mice. Learning and Memory (2006) 584-589
33. Moyer Jr. J.R., Thompson L.T., Black J.P., and Disterhoft J.F. Nimodipine increases excitability of rabbit CA1 pyramidal neurons in an age- and concentration-dependent manner. Journal of Neurophysiology 68 (1992) 2100-2109
34. Murphy G.G., Fedorov N.B., Giese K.P., Ohno M., Friedman E., Chen R., et al. Increased neuronal excitability, synaptic plasticity, and learning in aged Kvβ1.1 knockout mice. Current Biology 14 190 (2004) 7-1915
35. Phillips R.G., and LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behavioral Neuroscience 106 (1992) 274-285
36. 2+ channels. Cell 102 (2000) 89-97
37. Power J.M., and Sah P. Intracellular calcium store filling by an L-type calcium current in the basolateral amygdala at subthreshold membrane potentials. Journal of Physiology 562 (2005) 439-453
38. + channels determines cholinergic action on firing properties of basolateral amygdala projection neurons. Journal of Neuroscience 28 (2008) 3209-3220
39. Power J.M., Wu W.W., Sametsky E., Oh M.M., and Disterhoft J.F. Age-related enhancement of the sow outward calcium-activated potassium current in hippocampal CA1 pyramidal neurons in vitro. Journal of Neuroscience 22 (2002) 7234-7243
40. Rodrigues S.M., Schafe G.E., and LeDoux J.E. Molecular mechanisms underlying emotional learning and memory in the lateral amygdala. Neuron 44 (2004) 75-91
41. Rogan M.T., Staubli U.V., and LeDoux J.E. Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390 (1997) 604-607
42. Romanski L.M., Clugnet M.-C., Bordi F., and LeDoux J.E. Somatosensory and auditory convergence in the lateral nucleus of the amygdala. Behavioral Neuroscience 107 (1993) 444-450
43. Sah P., Westbrook R.F., and Lüthi A. Fear conditioning and long-term potentiation in the amygdala. Annals of the New York Academy of Sciences 1129 (2008) 88-95
44. Schafe G.E., Nader K., Blair H.T., and LeDoux J.E. Memory consolidation of Pavlovian fear conditioning: A cellular and molecular perspective. Trends in Neurosciences 24 (2001) 540-546
45. Schroeder B.W., and Shinnick-Gallagher P. Fear memories induce a switch in stimulus response and signaling mechanisms for long-term potentiation in the lateral amygdala. European Journal of Neuroscience 20 (2004) 549-556
46. 2+ channels involved in the generation of the slow afterhyperpolarization in cultured rat hippocampal pyramidal neurons. Journal of Neurophysiology 83 (2000) 2554-2561
47. Sigurdsson T., Doyère V., Cain C.K., and LeDoux J.E. Long-term potentiation in the amygdala: A cellular mechanism of fear learning and memory. Neuropharmacology 52 (2007) 215-227
48. Stoop R., and Pralong E. Functional connections and epileptic spread between hippocampus, entorhinal cortex and amygdala in a modified horizontal slice preparation of the rat brain. European Journal of Neuroscience 12 (2000) 3651-3663
49. 2+-dependent afterhyperpolarization current in rat CA3 pyramidal cells in vitro. Journal of Neurophysiology 80 (1998) 2268-2273
50. 4 receptors reduce afterhyperpolarization in hippocampus by inhibiting calcium-induced calcium release. Molecular Pharmacology 50 (1996) 1316-1322
51. Tsvetkov E., Carlezon Jr. W.A., Benes F.M., Kandel E.R., and 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
52. sAHP in mouse hippocampus CA1 pyramidal neurons by RyR3-mediated calcium-induced calcium release. Pflugers Archive 455 (2007) 297-308
53. Von Bohlen und Halbach O., and Albrecht D. Tracing of axonal connectivities in a combined slice preparation of rat brains - A study by rhodamine-dextran-amine-application in the lateral nucleus of the amygdala. Journal of Neuroscience Methods 81 (1998) 169-175
54. Von Bohlen und Halbach O., and Albrecht D. Reciprocal connections of the hippocampal area CA1, the lateral nucleus of the amygdala and cortical areas in a combined horizontal slice preparation. Neuroscience Research 44 (2002) 91-100
55. Washburn M.S., and Moises H.C. Muscarinic responses of rat basolateral amygdaloid neurons recorded in vitro. Journal of Physiology 449 (1992) 121-154
56. Watanabe Y., Saito H., and Abe K. Nitric oxide is involved in long-term potentiation in the medial but not lateral amygdala neuron synapses in vitro. Brain Research 688 (1995) 233-236
57. Weisskopf M.G., Bauer E.P., and LeDoux J.E. L-type voltage-gated calcium channels mediate NMDA-independent associative long-term potentiation at thalamic input synapses to the amygdala. Journal of Neuroscience 19 (1999) 10512-10519
58. 1 L-type channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines. Journal of Neuroscience 21 (2001) 5944-5951
59. Zhang W., and Linden D.J. The other side of the engram: Experience-driven changes in neuronal intrinsic excitability. Nature Reviews Neuroscience 4 (2003) 885-900