Activity-dependent long-term potentiation of intrinsic excitability in hippocampal CA1 pyramidal neurons.
The efficiency of neural circuits is enhanced not only by increasing synaptic strength but also by increasing intrinsic excitability. In contrast to the detailed analysis of long-term potentiation (LTP), less attention has been given to activity-dependent changes in the intrinsic neuronal excitability. By stimulating hippocampal CA1 pyramidal neurons with synaptic inputs correlating with postsynaptic neuronal spikes, we elicited an LTP of intrinsic excitability (LTP-IE) concurring with synaptic LTP. LTP-IE was manifested as a decrease in the action potential threshold that was attributable to a hyperpolarized shift in the activation curve of voltage-gated sodium channels (VGSCs) rather than activity-dependent changes in synaptic inputs or A-type K+ channels. Cell-attached patch recording of VGSC activities indicated such an activity-dependent change in VGSCs. Induction of LTP-IE was blocked by the NMDA receptor antagonist APV, intracellular BAPTA, the CaM kinase inhibitors KN-62 and autocamtide-2-related inhibitory peptide, and the protein synthesis inhibitors emetine and anisomycin. The results suggest that induction of LTP-IE shares a similar signaling pathway with the late phase of synaptic LTP and requires activation of the NMDA glutamate receptor subtype, Ca2+ influx, activity of CaM kinase II, and function of the protein synthesis. This new form of hippocampal neuronal plasticity could be a cellular correlate of learning and memory besides synaptic LTP.
Xu
Jun
J
Department of Cell Biology and Anatomy, New York Medical College, Valhalla, New York 10595, USA.
Kang
Ning
N
Jiang
Li
L
Nedergaard
Maiken
M
Kang
Jian
J
D019307:1-(5-Isoquinolinesulfonyl)-2-Methylpiperazine / Q000031:analogs & derivatives / Q000494:pharmacology; D015763:2-Amino-5-phosphonovalerate / Q000494:pharmacology; D015761:4-Aminopyridine / Q000494:pharmacology; D018750:6-Cyano-7-nitroquinoxaline-2,3-dione / Q000494:pharmacology; D000818:Animals; D000841:Anisomycin / Q000494:pharmacology; D001640:Bicuculline / Q000494:pharmacology; D002118:Calcium / Q000378:metabolism; D054732:Calcium-Calmodulin-Dependent Protein Kinase Type 2; D017871:Calcium-Calmodulin-Dependent Protein Kinases / Q000502:physiology; D004533:Egtazic Acid / Q000031:analogs & derivatives / Q000494:pharmacology; D004640:Emetine / Q000494:pharmacology; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology; D007858:Learning / Q000502:physiology; D017774:Long-Term Potentiation / Q000502:physiology*; D018408:Patch-Clamp Techniques; D010721:Phosphinic Acids; D015221:Potassium Channels / Q000187:drug effects / Q000502:physiology; D011412:Propanolamines; D017966:Pyramidal Cells / Q000502:physiology*; D051381:Rats; D017207:Rats, Sprague-Dawley; D016194:Receptors, N-Methyl-D-Aspartate / Q000037:antagonists & inhibitors; D015222:Sodium Channels / Q000187:drug effects / Q000502:physiology
D018691:Excitatory Amino Acid Antagonists; D010721:Phosphinic Acids; D015221:Potassium Channels; D011412:Propanolamines; D016194:Receptors, N-Methyl-D-Aspartate; D015222:Sodium Channels; C085075:CGP 55845A; D004533:Egtazic Acid; C063302:KN 62; D000841:Anisomycin; D018750:6-Cyano-7-nitroquinoxaline-2,3-dione; D015763:2-Amino-5-phosphonovalerate; D019307:1-(5-Isoquinolinesulfonyl)-2-Methylpiperazine; D015761:4-Aminopyridine; D054732:Calcium-Calmodulin-Dependent Protein Kinase Type 2; D017871:Calcium-Calmodulin-Dependent Protein Kinases; C025603:1,2-bis(2-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid; D002118:Calcium; D004640:Emetine; D001640:Bicuculline
Nat Neurosci. 1998 Dec;1(8):683-92
10196584
Science. 1999 Sep 17;285(5435):1870-4
10489359
J Neurophysiol. 1999 Dec;82(6):2903-13
10601428
J Neurophysiol. 2000 Jan;83(1):70-80
10634854
Nat Neurosci. 2000 Feb;3(2):109-11
10649564
Nat Neurosci. 2000 Apr;3(4):330-6
10725921
Neuron. 2000 Apr;26(1):13-25
10798388
J Neurosci. 2000 Jul 15;20(14):5208-16
10884304
Nat Neurosci. 2000 Oct;3(10):1018-26
11017175
J Neurosci. 2001 Feb 15;21(4):1385-92
11160410
J Neurosci. 2001 Feb 15;21(4):1401-12
11160412
Neuron. 2001 May;30(2):503-13
11395010
J Neurosci. 2001 Aug 15;21(16):6413-22
11487665
Neuron. 2002 Jan 31;33(3):439-52
11832230
Neuron. 2002 Mar 28;34(1):107-14
11931745
J Neurophysiol. 2002 Jul;88(1):107-16
12091536
Proc Natl Acad Sci U S A. 2002 Oct 29;99(22):14512-7
12391303
Neuron. 2003 Feb 6;37(3):463-72
12575953
J Neurophysiol. 2003 Oct;90(4):2171-9
12815013
Neuron. 2003 Aug 28;39(5):831-42
12948449
J Neurosci. 1992 Feb;12(2):607-18
1311034
Nat Rev Neurosci. 2003 Nov;4(11):885-900
14595400
J Neurosci. 2003 Nov 12;23(32):10238-48
14614082
Hippocampus. 2003;13(7):801-5
14620875
Nat Neurosci. 2004 Feb;7(2):126-35
14730307
J Neurophysiol. 2004 Jul;92(1):341-8
14973317
Nat Neurosci. 2004 May;7(5):518-24
15048122
J Neurosci. 2004 May 12;24(19):4530-4
15140923
Methods Enzymol. 1992;207:123-31
1528115
Neuron. 1991 Jan;6(1):53-60
1670922
Exp Brain Res. 1990;79(3):633-41
2340880
Science. 1989 Aug 25;245(4920):862-6
2549638
J Physiol. 1987 Dec;394:367-80
3443970
Behav Neural Biol. 1985 Sep;44(2):278-300
4062781
J Physiol. 1973 Jul;232(2):331-56
4727084
Pflugers Arch. 1981 Aug;391(2):85-100
6270629
J Physiol. 1983 Jan;334:33-46
6306230
J Physiol. 1983 Mar;336:285-300
6875910
J Physiol. 1980 May;302:463-82
7411464
J Physiol. 1995 Aug 15;487(1):67-90
7473260
Trends Neurosci. 1993 Dec;16(12):521-7
7509523
J Physiol. 1995 May 1;484 ( Pt 3):689-705
7623285
Biochem Biophys Res Commun. 1995 Jul 26;212(3):806-12
7626114
Annu Rev Physiol. 1995;57:417-45
7778873
Neuroscience. 1994 Oct;62(4):1021-32
7845583
J Biol Chem. 1994 Jun 3;269(22):15520-7
8195196
Science. 1993 Jun 11;260(5114):1661-4
8389057
Nature. 1993 Jan 7;361(6407):31-9
8421494
Brain Res Brain Res Rev. 1993 Jan-Apr;18(1):115-22
8467347
J Biol Chem. 1996 Oct 4;271(40):24329-32
8798683
J Neurosci. 1996 Nov 1;16(21):6676-86
8824308
J Neurophysiol. 1996 Nov;76(5):3126-35
8930260
Science. 1997 Jan 10;275(5297):209-13
8985013
Science. 1997 Jan 10;275(5297):213-5
8985014
Cell. 1997 Mar 7;88(5):615-26
9054501
J Neurophysiol. 1997 Jan;77(1):86-92
9120599
Science. 1997 Jun 27;276(5321):2001-2
9221509
J Biol Chem. 1997 Aug 1;272(31):19103-6
9235897
J Physiol. 1998 Feb 15;507 ( Pt 1):237-47
9490845
J Neurosci. 1998 Jul 15;18(14):5498-507
9651230
J Neurosci. 1998 Aug 1;18(15):5988-98
9671684
Eur J Neurosci. 1998 Apr;10(4):1518-23
9749805
J Neurosci. 1998 Dec 15;18(24):10464-72
9852584
J Neurophysiol. 1999 Jan;81(1):277-87
9914288