Post-tetanic increase in the fast-releasing synaptic vesicle pool at the expense of the slowly releasing pool.
Post-tetanic potentiation (PTP) at the calyx of Held synapse is caused by increases not only in release probability (P(r)) but also in the readily releasable pool size estimated from a cumulative plot of excitatory post-synaptic current amplitudes (RRP(cum)), which contribute to the augmentation phase and the late phase of PTP, respectively. The vesicle pool dynamics underlying the latter has not been investigated, because PTP is abolished by presynaptic whole-cell patch clamp. We found that supplement of recombinant calmodulin to the presynaptic pipette solution rescued the increase in the RRP(cum) after high-frequency stimulation (100 Hz for 4-s duration, HFS), but not the increase in P(r). Release-competent synaptic vesicles (SVs) are heterogeneous in their releasing kinetics. To investigate post-tetanic changes of fast and slowly releasing SV pool (FRP and SRP) sizes, we estimated quantal release rates before and 40 s after HFS using the deconvolution method. After HFS, the FRP size increased by 19.1% and the SRP size decreased by 25.4%, whereas the sum of FRP and SRP sizes did not increase. Similar changes in the RRP were induced by a single long depolarizing pulse (100 ms). The post-tetanic complementary changes of FRP and SRP sizes were abolished by inhibitors of myosin II or myosin light chain kinase. The post-tetanic increase in the FRP size coupled to a decrease in the SRP size provides the first line of evidence for the idea that a slowly releasing SV can be converted to a fast releasing one.
Lee
Jae Sung
JS
Department of Physiology and Biomembrane Plasticity Research Center, Seoul National University College of Medicine and Neuroscience Research Institute, Seoul 110-799, Korea.
Ho
Won-Kyung
WK
Lee
Suk-Ho
SH
D000818:Animals; D001933:Brain Stem / Q000166:cytology / Q000187:drug effects / Q000378:metabolism*; D002118:Calcium / Q000378:metabolism; D002147:Calmodulin / Q000378:metabolism; D004558:Electric Stimulation; D004791:Enzyme Inhibitors / Q000494:pharmacology; D005071:Evoked Potentials; D019706:Excitatory Postsynaptic Potentials; D066298:In Vitro Techniques; D007700:Kinetics; D024462:Myosin Type II / Q000037:antagonists & inhibitors / Q000378:metabolism; D009219:Myosin-Light-Chain Kinase / Q000037:antagonists & inhibitors / Q000378:metabolism; D009473:Neuronal Plasticity / Q000187:drug effects; D009474:Neurons / Q000187:drug effects / Q000378:metabolism*; D018408:Patch-Clamp Techniques; D017729:Presynaptic Terminals / Q000378:metabolism; D051381:Rats; D017207:Rats, Sprague-Dawley; D011994:Recombinant Proteins / Q000378:metabolism; D009435:Synaptic Transmission / Q000187:drug effects; D013572:Synaptic Vesicles / Q000187:drug effects / Q000378:metabolism*
D002147:Calmodulin; D004791:Enzyme Inhibitors; D011994:Recombinant Proteins; D009219:Myosin-Light-Chain Kinase; D024462:Myosin Type II; D002118:Calcium
Trends Neurosci. 2002 Apr;25(4):206-12
11998689
Neuron. 2008 Sep 25;59(6):861-72
18817727
Neuron. 2005 Oct 6;48(1):109-21
16202712
Neuron. 1999 Aug;23(4):821-32
10482247
Nature. 1996 Oct 3;383(6599):431-4
8837774
J Neurosci. 2006 Feb 1;26(5):1366-77
16452660
J Neurosci. 2005 Jun 29;25(26):6057-65
15987935
J Physiol. 2005 Apr 1;564(Pt 1):173-87
15695246
J Neurosci. 2005 May 25;25(21):5127-37
15917453
Nature. 2009 May 7;459(7243):93-7
19279571
J Neurophysiol. 2008 Apr;99(4):1810-24
18256166
J Neurosci. 2002 Mar 1;22(5):1648-67
11880495
Neuron. 2007 Feb 15;53(4):563-75
17296557
J Neurosci. 2005 Apr 13;25(15):3842-50
15829636
Biophys J. 2005 Sep;89(3):2091-102
15980175
J Neurosci. 2007 Dec 26;27(52):14286-98
18160636
Proc Natl Acad Sci U S A. 2007 Oct 2;104(40):15923-8
17884983
Pflugers Arch. 1988 Feb;411(2):204-11
2451806
J Physiol. 2007 Jun 1;581(Pt 2):467-78
17363387
J Neurosci. 2008 Feb 20;28(8):1949-60
18287511
Science. 2008 Mar 14;319(5869):1543-6
18339943
J Neurosci. 2007 Mar 21;27(12):3198-210
17376981
Neuron. 2001 Dec 20;32(6):1119-31
11754842
J Neurosci. 2008 Aug 6;28(32):7945-53
18685020
Science. 2002 Mar 22;295(5563):2276-9
11910115
J Neurosci. 2006 May 31;26(22):5863-71
16738227
J Neurosci. 2006 Nov 8;26(45):11606-14
17093082
J Neurosci. 2002 Dec 15;22(24):10567-79
12486149
J Neurophysiol. 2006 Dec;96(6):2868-76
16899643
J Neurosci. 2008 Aug 13;28(33):8257-67
18701688
Proc Natl Acad Sci U S A. 2001 Jan 2;98(1):331-6
11134533
J Neurosci. 2000 Nov 15;20(22):8377-83
11069944
Protein Sci. 1997 Apr;6(4):794-807
9098889
Neuron. 2003 Mar 6;37(5):801-11
12628170
J Neurosci. 2001 Jan 15;21(2):444-61
11160425