AMPA receptors gate spine Ca(2+) transients and spike-timing-dependent potentiation.
Spike timing-dependent long-term potentiation (t-LTP) is the embodiment of Donald Hebb's postulated rule for associative memory formation. Pre- and postsynaptic action potentials need to be precisely correlated in time to induce this form of synaptic plasticity. NMDA receptors have been proposed to detect correlated activity and to trigger synaptic plasticity. However, the slow kinetic of NMDA receptor currents is at odds with the millisecond precision of coincidence detection. Here we show that AMPA receptors are responsible for the extremely narrow time window for t-LTP induction. Furthermore, we visualized synergistic interactions between AMPA and NMDA receptors and back-propagating action potentials on the level of individual spines. Supralinear calcium signals were observed for spike timings that induced t-LTP and were most pronounced in spines well isolated from the dendrite. We conclude that AMPA receptors gate the induction of associative synaptic plasticity by regulating the temporal precision of coincidence detection.
Holbro
Niklaus
N
Friedrich Miescher Institute for Biomedical Research, Basel, Switzerland.
Grunditz
Asa
A
Wiegert
J Simon
JS
Oertner
Thomas G
TG
D000200:Action Potentials; D000818:Animals; D002118:Calcium / Q000378:metabolism*; D006624:Hippocampus / Q000502:physiology; D066298:In Vitro Techniques; D017774:Long-Term Potentiation; D051381:Rats; D017208:Rats, Wistar; D018091:Receptors, AMPA / Q000502:physiology*
D018091:Receptors, AMPA; D002118:Calcium
Proc Natl Acad Sci U S A. 2002 Jun 11;99(12):8366-71
12048251
J Neurosci. 2009 May 27;29(21):6897-903
19474316
Neuron. 2005 Jan 6;45(1):119-31
15629707
J Neurosci. 1996 Mar 15;16(6):1982-9
8604042
J Neurosci. 1999 Mar 15;19(6):1976-87
10066251
J Neurophysiol. 2005 May;93(5):2600-13
15625097
Science. 2009 Mar 6;323(5919):1313-9
19265014
Physiol Rev. 2008 Apr;88(2):769-840
18391179
J Neurophysiol. 2010 Jan;103(1):47-54
19864442
Nature. 1998 Sep 3;395(6697):37-44
9738497
Nat Neurosci. 2000 Sep;3(9):919-26
10966623
J Neurosci. 2006 Apr 19;26(16):4166-77
16624937
J Neurosci. 2006 Oct 25;26(43):11001-13
17065442
Neuron. 2007 Jan 18;53(2):249-60
17224406
Proc Natl Acad Sci U S A. 1998 Aug 4;95(16):9596-601
9689126
Science. 1994 Nov 11;266(5187):1059-62
7973663
J Neurosci. 2008 Dec 10;28(50):13457-66
19074019
J Neurosci. 1998 Dec 15;18(24):10464-72
9852584
J Neurosci. 2007 Oct 31;27(44):11940-8
17978034
Science. 2005 Nov 4;310(5749):866-9
16272125
Nat Neurosci. 2005 May;8(5):642-9
15852011
Neuron. 2009 Apr 30;62(2):254-68
19409270
J Neurosci. 2004 Feb 18;24(7):1689-99
14973235
Biophys J. 2000 May;78(5):2655-67
10777761
J Comput Neurosci. 1999 Jul-Aug;7(1):5-15
10481998
Annu Rev Neurosci. 2002;25:103-26
12052905
Sci STKE. 2004 Feb 03;2004(219):pl5
14872098
Neuron. 2001 Aug 2;31(2):191-201
11502252
Neuron. 2007 Sep 20;55(6):905-18
17880894
Proc Natl Acad Sci U S A. 2006 Nov 21;103(47):17961-6
17093040
Neuron. 2008 Sep 25;59(6):902-13
18817730
Science. 1997 Jan 10;275(5297):213-5
8985014
Nat Neurosci. 2001 Nov;4(11):1086-92
11687814
J Physiol. 2004 Apr 15;556(Pt 2):337-45
14754998
Front Comput Neurosci. 2009 Apr 27;3:7
19564894
J Neurophysiol. 2000 Nov;84(5):2225-36
11067968
PLoS One. 2008 Apr 30;3(4):e2045
18446197
PLoS Biol. 2009 Sep;7(9):e1000190
19753104