Activity-dependent long-term potentiation of intrinsic excitability in hippocampal CA1 pyramidal neurons

Journal of Neuroscience

Volumn 25, Issue 7, 2005, Pages 1750-1760

  Xu, Jun ^a   Kang, Ning ^a   Jiang, Li ^b   Nedergaard, Maiken ^c   Kang, Jian ^a  

^a NEW YORK MEDICAL COLLEGE   (United States)

^b Columbia University ^*  (United States)

^c UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

CaM kinases; Intrinsic excitability; Long term potentiation; Na+ channel; NMDA receptors; Protein synthesis

Indexed keywords

1 [N,O BIS(5 ISOQUINOLINESULFONYL) N METHYLTYROSYL] 4 PHENYLPIPERAZINE; 2 AMINO 5 PHOSPHONOVALERIC ACID; ANISOMYCIN; EMETINE; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; POTASSIUM CHANNEL; PROTEIN KINASE (CALCIUM,CALMODULIN) II; VOLTAGE GATED SODIUM CHANNEL;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; ENZYME ACTIVITY; HIPPOCAMPUS; LEARNING; LONG TERM POTENTIATION; MEMORY; NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT;

1-(5-ISOQUINOLINESULFONYL)-2-METHYLPIPERAZINE; 2-AMINO-5-PHOSPHONOVALERATE; 4-AMINOPYRIDINE; 6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ANIMALS; ANISOMYCIN; BICUCULLINE; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM; EGTAZIC ACID; EMETINE; EXCITATORY AMINO ACID ANTAGONISTS; LEARNING; LONG-TERM POTENTIATION; PATCH-CLAMP TECHNIQUES; PHOSPHINIC ACIDS; POTASSIUM CHANNELS; PROPANOLAMINES; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SODIUM CHANNELS;

EID: 14044276407     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4217-04.2005     Document Type: Article

References (64)

1. Abel T, Nguyen PV, Barad M, Deuel TA, Kandel ER, Bourtchouladze R (1997) Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88:615-626.
2. Abraham WC, Gustafsson B, Wigstrom H (1987) Long-term potentiation involves enhanced synaptic excitation relative to synaptic inhibition in guinea-pig hippocampus. J Physiol (Lond) 394:367-380.
3. Aizenman CD, Linden DJ (2000) Rapid, synaptically driven increases in the intrinsic excitability of cerebellar deep nuclear neurons. Nat Neurosci 3:109-111.
4. Aizenman CD, Akerman CJ, Jensen KR, Cline HT (2003) Visually driven regulation of intrinsic neuronal excitability improves stimulus detection in vivo. Neuron 39:831-842.
5. Alkon DL, Sakakibara M, Forman R, Harrigan J, Lederhendler I, Farley J (1985) Reduction of two voltage-dependent K+ currents mediates retention of a learned association. Behav Neural Biol 44:278-300.
6. Andersen P, Sundberg SH, Sveen O, Swann JW, Wigstrom H (1980) Possible mechanisms for long-lasting potentiation of synaptic transmission in hippocampal slices from guinea-pigs. J Physiol (Lond) 302:463-482.
7. Antonov I, Antonova I, Kandel ER, Hawkins RD (2001) The contribution of activity-dependent synaptic plasticity to classical conditioning in Aplysia. J Neurosci 21:6413-6422.
8. Armano S, Rossi P, Taglietti V, D'Angelo E (2000) Long-term potentiation of intrinsic excitability at the mossy fiber-granule cell synapse of rat cerebellum. J Neurosci 20:5208-5216.
9. Bi GQ, Poo MM (1998) Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18:10464-10472.
10. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
11. Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol (Lond) 232:331-356.
12. Braun AP, Schulman H (1995) The multifunctional calcium/calmodulin- dependent protein kinase: from form to function. Annu Rev Physiol 57:417-445.
13. Breakwell NA, Rowan MJ, Anwyl R (1996) Metabotropic glutamate receptor dependent EPSP and EPSP-spike potentiation in area CA1 of the submerged rat hippocampal slice. J Neurophysiol 76:3126-3135.
14. Burrell BD, Sahley CL, Muller KJ (2001) Non-associative learning and serotonin induce similar bi-directional changes in excitability of a neuron critical for learning in the medicinal leech. J Neurosci 21:1401-1412.
15. Catterall WA (2000) From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 26:13-25.
16. Chavez-Noriega LE, Hailiwell JV, Bliss TV (1990) A decrease in firing threshold observed after induction of the EPSP-spike (E-S) component of long-term potentiation in rat hippocampal slices. Exp Brain Res 79:633-641.
17. ChoiS, Klingauf J, Tsien RW (2000) Postfusional regulation of cleft glutamate concentration during LTP at "silent synapses." Nat Neurosci 3:330-336.
18. Cleary LJ, Lee WL, Byrne JH (1998) Cellular correlates of long-term sensitization in Aplysia. J Neurosci 18:5988-5998.
19. + channel densities in the soma and axon initial segment of subicular pyramidal neurons. J Neurosci 16:6676-6686.
20. Colley PA, Routtenberg A (1993) Long-term potentiation as synaptic dialogue. Brain Res Brain Res Rev 18:115-122.
21. Collingridge GL, Kehl SJ, McLennan H (1983) Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J Physiol (Lond) 334:33-46.
22. Cudmore RH, Turrigiano GG (2004) Long-term potentiation of intrinsic excitability in LV visual cortical neurons. J Neurophysiol 92:341-348.
23. D'Angelo E, Rossi P, Armano S, Taglietti V (1999) Evidence for NMDA and mGlu receptor-dependent long-term potentiation of mossy fiber-granule cell transmission in rat cerebellum. J Neurophysiol 81:277-287.
24. Daoudal G, Hanada Y, Debanne D (2002) Bidirectional plasticity of excitatory postsynaptic potential (EPSP)-spike coupling in CA1 hippocampal pyramidal neurons. Proc Natl Acad Sci USA 99:14512-14517.
25. Debanne D, Gahwiler BH, Thompson SM (1998) Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. J Physiol (Lond) 507:237-247.
26. English JD, Sweatt JD (1996) Activation of p42 mitogen-activated protein kinase in hippocampal long term potentiation. J Biol Chem 271:24329-24332.
27. English JD, Sweatt JD (1997) A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J Biol Chem 272:19103-19106.
28. 2+/calmodulin-dependent protein kinase IV. Role in transcriptional regulation. J Biol Chem 269:15520-15527.
29. Frey U, Huang YY, Kandel ER (1993) Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260:1661-1664.
30. Frick A, Magee J, Johnston D (2004) LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat Neurosci 7:126-135.
31. Ganguly K, Kiss L, Poo M (2000) Enhancement of presynaptic neuronal excitability by correlated presynaptic and postsynaptic spiking. Nat Neurosci 3:1018-1026.
32. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391:85-100.
33. Ireland DR, Abraham WC (2002) Group I mGluRs increase excitability of hippocampal CA1 pyramidal neurons by a PLC-independent mechanism. J Neurophysiol 88:107-116.
34. Ishida A, Kameshita I, Okuno S, Kitani T, Fujisawa H (1995) A novel highly specific and potent inhibitor of calmodulin-dependent protein kinase II. Biochem Biophys Res Commun 212:806-812.
35. Jester JM, Campbell LW, Sejnowski TJ (1995) Associative EPSP-spike potentiation induced by pairing orthodromic and antidromic stimulation in rat hippocampal slices. J Physiol (Lond) 484:689-705.
36. Jiang L, Xu J, Nedergaard M, Kang J (2001) A kainate receptor increases the efficacy of GABAergic synapses. Neuron 30:503-513.
37. Kang J, Jiang L, Goldman SA, Nedergaard M (1998) Astrocyte-mediated potentiation of inhibitory synaptic transmission. Nat Neurosci 1:683-692.
38. Kang J, Huguenard JR, Prince DA (2000) Voltage-gated potassium channels activated during action potentials in layer V neocortical pyramidal neurons. J Neurophysiol 83:70-80.
39. Lisman J, Malenka RC, Nicoll RA, Malinow R (1997) Learning mechanisms: the case for CaM-KII. Science 276:2001-2002.
40. 2+ channels in apical dendrites of rat CA1 pyramidal neurons. J Physiol (Lond) 487:67-90.
41. Magee JC, Johnston D (1997) A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275:209-213.
42. Malenka RC (1991) Postsynaptic factors control the duration of synaptic enhancement in area CA1 of the hippocampus. Neuron 6:53-60.
43. Malenka RC, Nicoll RA (1993) NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms. Trends Neurosci 16:521-527.
44. Malenka RC, Nicoll RA (1999) Long-term potentiation-a decade of progress? Science 285:1870-1874.
45. Malinow R, Schulman H, Tsien RW (1989) Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. Science 245:862-866.
46. Markram H, Lubke J, Frotscher M, Sakmann B (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275:213-215.
47. Melyan Z, Wheal HV, Lancaster B (2002) Metabotropic-mediated kainate receptor regulation of IsAHP and excitability in pyramidal cells. Neuron 34:107-114.
48. Melyan Z, Lancaster B, Wheal HV (2004) Metabotropic regulation of intrinsic excitability by synaptic activation of kainate receptors. J Neurosci 24:4530-4534.
49. Moore JW, Westerfield M (1983) Action potential propagation and threshold parameters in inhomogeneous regions of squid axons. J Physiol (Lond) 336:285-300.
50. Nedergaard S (1999) Regulation of action potential size and excitability in substantia nigra compacta neurons: sensitivity to 4-aminopyridine. J Neurophysiol 82:2903-2913.
51. Neher E (1992) Correction for liquid junction potentials in patch clamp experiments. Methods Enzymol 207:123-131.
52. Oh MM, Kuo AG, Wu WW, Sametsky EA, Disterhoft JF (2003) Watermaze learning enhances excitability of CA1 pyramidal neurons. J Neurophysiol 90:2171-2179.
53. Pugliese AM, Ballerini L, Passani MB, Corradetti R (1994) KPSP-spike potentiation during primed burst-induced long-term potentiation in the CA1 region of rat hippocampal slices. Neuroscience 62:1021-1032.
54. Saar D, Grossman Y, Barkai E (1998) Reduced after-hyperpolarization in rat piriform cortex pyramidal neurons is associated with increased learning capability during operant conditioning. Eur J Neurosci 10:1518-1523.
55. Saar D, Grossman Y, Barkai E (2001) Long-lasting cholinergic modulation underlies rule learning in rats. J Neurosci 21:1385-1392.
56. 2+ ions in dendritic spines. Neuron 33:439-452.
57. Schreurs BG, Tomsic D, Gusev PA, Alkon DL (1997) Dendritic excitability microzones and occluded long-term depression after classical conditioning of the rabbit's nictitating membrane response. J Neurophysiol 77:86-92.
58. Schreurs BG, Gusev PA, Tomsic D, Alkon DL, Shi T (1998) Intracellular correlates of acquisition and long-term memory of classical conditioning in Purkinje cell dendrites in slices of rabbit cerebellar lobule HVI. J Neurosci 18:5498-5507.
59. Sourdet V, Russier M, Daoudal G, Ankri N, Debanne D (2003) Long-term enhancement of neuronal excitability and temporal fidelity mediated by metabotropic glutamate receptor subtype 5. J Neurosci 23:10238-10248.
60. Staff NP, Spruston N (2003) Intracellular correlate of EPSP-spike potentiation in CA1 pyramidal neurons is controlled by GABAergic modulation. Hippocampus 13:801-805.
61. Wang Z, Xu NL, Wu CP, Duan S, Poo MM (2003) Bidirectional changes in spatial dendritic integration accompanying long-term synaptic modifications. Neuron 37:463-472.
62. Wathey JC, Lytton WW, Jester JM, Sejnowski TJ (1992) Computer simulations of EPSP-spike (E-S) potentiation in hippocampal CA1 pyramidal cells. J Neurosci 12:607-618.
63. Watt AJ, Sjostrom PJ, Hausser M, Nelson SB, Turrigiano GG (2004) A proportional but slower NMDA potentiation follows AMPA potentiation in LTP. Nat Neurosci 7:518-524.
64. Zhang W, Linden DJ (2003) The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat Rev Neurosci 4:885-900.