Dynamic modulation of short-term synaptic plasticity in the auditory cortex: the role of norepinephrine.
Norepinephrine (NE) is an important modulator of neuronal activity in the auditory cortex. Using patch-clamp recording and a pair pulse protocol on an auditory cortex slice preparation we recently demonstrated that NE affects cortical inhibition in a layer-specific manner, by decreasing apical but increasing basal inhibition onto layer II/III pyramidal cell dendrites. In the present study we used a similar protocol to investigate the dependence of noradrenergic modulation of inhibition on stimulus frequency, using 1s-long train pulses at 5, 10, and 20 Hz. The study was conducted using pharmacologically isolated inhibitory postsynaptic currents (IPSCs) evoked by electrical stimulation of axons either in layer I (LI-eIPSCs) or in layer II/III (LII/III-eIPSCs). We found that: 1) LI-eIPSC display less synaptic depression than LII/III-eIPSCs at all the frequencies tested, 2) in both type of synapses depression had a presynaptic component which could be altered manipulating [Ca²+]₀, 3) NE modestly altered short-term synaptic plasticity at low or intermediate (5-10 Hz) frequencies, but selectively enhanced synaptic facilitation in LI-eIPSCs while increasing synaptic depression of LII/III-eIPSCs in the latest (>250 ms) part of the response, at high stimulation frequency (20 Hz). We speculate that these mechanisms may limit the temporal window for top-down synaptic integration as well as the duration and intensity of stimulus-evoked gamma-oscillations triggered by complex auditory stimuli during alertness.
Salgado
Humberto
H
School of Behavioral and Brain Sciences, Laboratory of Cell and Synaptic Physiology, University of Texas at Dallas, Richardson, TX 75080, USA.
García-Oscos
Francisco
F
Dinh
Lu
L
Atzori
Marco
M
D000818:Animals; D001303:Auditory Cortex / Q000187:drug effects / Q000502:physiology*; D020013:Calcium Signaling; D004558:Electric Stimulation; D005071:Evoked Potentials; D066298:In Vitro Techniques; D053444:Inhibitory Postsynaptic Potentials; D008959:Models, Neurological; D009473:Neuronal Plasticity / Q000502:physiology*; D009638:Norepinephrine / Q000494:pharmacology / Q000502:physiology*; D018408:Patch-Clamp Techniques; D051381:Rats; D017207:Rats, Sprague-Dawley; D013569:Synapses / Q000187:drug effects / Q000502:physiology; D005680:gamma-Aminobutyric Acid / Q000502:physiology
D005680:gamma-Aminobutyric Acid; D009638:Norepinephrine
Hear Res. 2003 Jul;181(1-2):116-30
12855370
J Neurosci. 2004 Jun 2;24(22):5162-71
15175385
Eur J Neurosci. 1997 Apr;9(4):833-47
9153591
J Physiol. 1983 Feb;335:427-47
6875887
J Physiol. 2005 Jan 1;562(Pt 1):149-64
15528242
J Comp Neurol. 1998 Jan 12;390(2):297-310
9453672
Trends Neurosci. 2003 Sep;26(9):489-95
12948660
Neuroscience. 2006 Sep 1;141(3):1553-67
16750887
Brain Res. 1975 Mar 21;86(2):229-42
234774
Nature. 2009 Jun 4;459(7247):663-7
19396156
J Physiol. 2004 Nov 15;561(Pt 1):65-90
15331670
Nature. 2009 Jun 4;459(7247):698-702
19396159
Nat Neurosci. 2001 Dec;4(12):1230-7
11694887
Pharmacol Ther. 2007 Mar;113(3):523-36
17303246
J Neurophysiol. 2000 May;83(5):3031-41
10805698
Neurochem Res. 2009 Nov;34(11):1896-906
19357950
Nat Neurosci. 2007 Jun;10(6):743-53
17515899
Cereb Cortex. 2010 Jul;20(7):1529-38
19875677
Hear Res. 2009 Dec;258(1-2):72-9
19595755
Science. 1979 Jul 20;205(4403):313-6
451605
Neurosci Lett. 1992 Mar 30;137(2):270-3
1316591
Nat Rev Neurosci. 2004 Oct;5(10):793-807
15378039
Prog Neurobiol. 1999 Feb;57(2):165-224
9987805
J Comp Neurol. 1978 Sep 1;181(1):17-39
355267
J Neurosci. 1997 Oct 15;17(20):7926-40
9315911
Brain Res. 1977 Dec 16;138(2):241-57
589474
Brain Res Bull. 1979 Nov-Dec;4(6):849-57
393366
Neuropsychopharmacology. 2008 Aug;33(9):2263-71
17957212
Eur J Neurosci. 1999 Jun;11(6):2134-50
10336682
Exp Brain Res. 2003 Dec;153(4):543-9
12937877
Neuron. 2010 Apr 15;66(1):114-25
20399733
Nat Neurosci. 1998 Dec;1(8):727-31
10196590
Prog Neurobiol. 2002 Jun;67(3):173-202
12169296
BMC Neurosci. 2008 Jan 16;9:8
18199338
Eur J Neurosci. 1995 Dec 1;7(12):2370-8
8845941
Annu Rev Physiol. 2002;64:355-405
11826273
Brain Res. 1979 Sep 14;173(2):337-40
487094
Cereb Cortex. 2008 Jul;18(7):1506-20
17965126
Somatosens Mot Res. 1992;9(1):3-36
1317625
Anat Embryol (Berl). 2004 Nov;209(1):77-91
15526216
Nature. 2004 Sep 16;431(7006):312-6
15372034
J Neurosci. 1997 May 15;17(10):3894-906
9133407
Br J Pharmacol. 1973 Jul;48(3):396-408
4357959
Brain Res. 1978 Jan 13;139(2):219-31
624057
J Neurosci. 1998 Sep 1;18(17):6963-76
9712665
Nat Rev Neurosci. 2004 Apr;5(4):279-90
15034553
Neuroscience. 2005;132(4):1151-7
15857717
Neurosci Lett. 1994 Sep 26;179(1-2):145-8
7845610
Proc Natl Acad Sci U S A. 1997 Jan 21;94(2):719-23
9012851
Cereb Cortex. 2011 Jan;21(1):212-21
20466749
Proc Natl Acad Sci U S A. 2007 Jun 12;104(24):10258-63
17545307
Can J Physiol Pharmacol. 1997 May;75(5):479-87
9250381
J Comp Neurol. 1975 Nov 15;164(2):209-31
810499
J Neurophysiol. 2004 Sep;92(3):1445-63
15084638
Neuron. 1996 Apr;16(4):815-23
8607999
Neuroscience. 1998 Jul;85(2):331-45
9622234
J Neurosci. 1984 Jun;4(6):1607-17
6726348
J Neurosci. 2008 Jan 9;28(2):369-75
18184779
Hear Res. 2009 Dec;258(1-2):121-33
19454307
J Neurosci. 1997 Nov 1;17(21):8427-42
9334415
Nat Rev Neurosci. 2008 Jul;9(7):557-68
18568015
J Neurophysiol. 2007 Nov;98(5):2868-77
17804573
Brain Res. 1968 Apr;8(1):125-31
5650798
Cereb Cortex. 2004 Oct;14(10):1059-70
15115747
J Neurosci. 2009 Aug 19;29(33):10321-34
19692606