Associative plasticity at excitatory synapses facilitates recruitment of fast-spiking interneurons in the dentate gyrus.
Fast-spiking perisomatic-inhibitory interneurons (PIIs) receive convergent excitation and mediate both feedforward and feedback inhibition in cortical microcircuits. However, it remains poorly understood how convergent excitatory inputs recruit PIIs to produce precisely timed inhibition. Here, we analyzed the interaction of inputs from the entorhinal cortex [perforant path (PP)] and from local granule cells [mossy fibers (MFs)] onto PIIs in the rat dentate gyrus (DG). PP stimulation alone activates PIIs with low temporal precision. Interestingly, when PP and MFs are coactivated with a 10 ms delay, PIIs discharge with precise timing. Moreover, repeated coactivation of the two inputs induces associative long-term potentiation (LTP) at MF synapses. Under these conditions, a single potentiated MF input is sufficient to recruit PIIs in a reliable and highly precise manner to provide feedback inhibition. MF-LTP depends on the discharge of PIIs, indicating Hebbian plasticity. However, MF-LTP is preserved when NMDA receptors are blocked but depends on transmission through Ca(2+)-permeable AMPA receptors (AMPARs). PP-PII synapses, in contrast, lack Ca(2+)-permeable AMPARs and do not show plasticity on associative activation. Thus, precise recruitment of PIIs requires excitation through MF-PII synapses during feedforward activation. We propose that associative plasticity at these synapses is a central mechanism that adjusts inhibition levels to maintain sparse activity and to improve signal-to-noise ratio in the DG network.
Sambandan
Sivakumar
S
Institute of Medical Sciences, University of Aberdeen, Foresterhill, Aberdeen, United Kingdom.
Sauer
Jonas-Frederic
JF
Vida
Imre
I
Bartos
Marlene
M
D000200:Action Potentials / Q000502:physiology*; D000818:Animals; D018891:Dentate Gyrus / Q000502:physiology*; D019706:Excitatory Postsynaptic Potentials / Q000502:physiology*; D006624:Hippocampus / Q000502:physiology; D007395:Interneurons / Q000502:physiology*; D009473:Neuronal Plasticity / Q000502:physiology*; D051381:Rats; D017208:Rats, Wistar; D011930:Reaction Time / Q000502:physiology*; D013569:Synapses / Q000502:physiology*
Neuron. 2008 Feb 28;57(4):536-45
18304483
Nat Rev Neurosci. 2007 Jan;8(1):45-56
17180162
Nature. 1986 Jul 17-23;322(6076):265-8
2874493
Science. 2007 Jul 6;317(5834):94-9
17556551
Neuron. 1994 Jun;12(6):1281-9
8011338
Neuron. 2005 Apr 7;46(1):89-102
15820696
Nature. 1999 Oct 7;401(6753):594-8
10524627
J Neurosci. 2004 Mar 3;24(9):2112-21
14999062
Science. 2007 Feb 16;315(5814):961-6
17303747
Brain Res. 1997 Sep 5;767(2):220-7
9367251
Hippocampus. 1994 Jun;4(3):374-91
7842058
Neuron. 1995 Aug;15(2):453-62
7646897
J Physiol. 1995 Jul 15;486 ( Pt 2):305-12
7473198
J Neurosci. 2008 Dec 24;28(52):14042-55
19109487
J Physiol. 2008 Mar 15;586(6):1481-6
18187472
J Neurophysiol. 1996 Dec;76(6):3798-806
8985877
Neuron. 2007 Dec 6;56(5):866-79
18054862
Nature. 1993 Jan 7;361(6407):31-9
8421494
Neuron. 2002 Mar 14;33(6):921-33
11906698
Neuron. 2006 Jul 20;51(2):227-38
16846857
Neuron. 2002 Jan 31;33(3):325-40
11832222
Neuron. 2007 Jun 21;54(6):859-71
17582328
J Neurosci. 1992 Jan;12(1):21-34
1345945
J Neurosci. 2000 Nov 15;20(22):8279-89
11069934
Nat Neurosci. 2009 Oct;12(10):1219-21
19734896
Biophys J. 1993 Jul;65(1):450-68
8369449
Nature. 2005 Aug 11;436(7052):801-6
15965463
Proc Natl Acad Sci U S A. 2001 Dec 4;98(25):14708-13
11734656
Brain Res. 1989 Aug 21;495(1):161-6
2776034
J Neurosci. 2007 Aug 1;27(31):8184-9
17670965
Science. 2007 Mar 2;315(5816):1262-6
17332410
Proc Natl Acad Sci U S A. 2010 Jan 12;107(2):894-9
20080772
J Neurosci. 2008 Nov 26;28(48):12956-68
19036989
J Neurosci. 2009 Jun 10;29(23):7497-503
19515917
Nat Neurosci. 1998 Nov;1(7):572-8
10196564
J Neurophysiol. 1999 Sep;82(3):1295-302
10482748
J Neurosci. 2005 Jan 26;25(4):990-1001
15673681
Trends Neurosci. 1998 Jul;21(7):273-8
9683315
J Neurosci. 1995 Jan;15(1 Pt 1):47-60
7823151
Hippocampus. 1993 Apr;3(2):165-82
8353604
Nat Rev Neurosci. 2005 Nov;6(11):863-76
16261180
J Neurosci. 2001 Apr 15;21(8):2687-98
11306622
Neuron. 1988 Apr;1(2):97-103
2856092
Neuron. 1995 Jul;15(1):193-204
7619522
J Neurophysiol. 2004 Dec;92(6):3575-81
15331617
Nature. 1998 Aug 13;394(6694):683-7
9716132
Science. 2008 Jul 4;321(5885):53-7
18599766
Nature. 1988 Jul 21;334(6179):250-2
2840582
J Neurosci. 2009 Apr 8;29(14):4658-63
19357290
J Neurosci. 1998 May 1;18(9):3386-403
9547246
Proc Natl Acad Sci U S A. 2002 Oct 1;99(20):13222-7
12235359
J Neurosci. 1997 Oct 15;17(20):7606-25
9315883
Exp Brain Res. 1971;13(2):222-38
5570425
Nat Rev Neurosci. 2007 Sep;8(9):687-99
17704811
Science. 2001 Aug 10;293(5532):1159-63
11498596
J Physiol. 1973 Jul;232(2):331-56
4727084
Neuron. 1997 Jun;18(6):1009-23
9208867
Trends Neurosci. 2004 Jan;27(1):30-40
14698608
J Physiol. 2008 Apr 15;586(8):2061-75
18276734
Nature. 2007 Mar 8;446(7132):190-4
17322902
Neuron. 2009 Apr 16;62(1):102-11
19376070
Hippocampus. 1996;6(4):347-470
8915675
Nat Neurosci. 2005 Jul;8(7):916-24
15937481
J Neurophysiol. 2004 Sep;92(3):1615-24
15128754
J Neurophysiol. 2004 Feb;91(2):863-72
14523073
Annu Rev Neurosci. 2008;31:25-46
18275283