Layer-specific noradrenergic modulation of inhibition in cortical layer II/III.
Norepinephrine (NE) is released in the neocortex after activation of the locus coeruleus of the brain stem in response to novel, salient, or fight-or-flight stimuli. The role of adrenergic modulation in sensory cortices is not completely understood. We investigated the possibility that NE modifies the balance of inhibition acting on 2 different γ-aminobutyric acid (GABA)ergic pathways. Using patch-clamp recordings, we found that the application of NE induces an α(1) adrenergic receptor-mediated decrease of the amplitude of inhibitory postsynaptic currents (IPSCs) evoked by stimulation of layer I (LI-eIPSCs) and a β and α(2) receptor-mediated increase in the amplitude of IPSCs evoked by stimulation of layer II/III (LII/III-eIPSCs). Analysis of minimal stimulation IPSCs, IPSC kinetics, and sensitivity to the GABA(A) receptor subunit-selective enhancer zolpidem corroborated the functional difference between LI- and LII/III-eIPSCs, suggestive of a distal versus somatic origin of LI- and LII/III-eIPSCs, respectively. These findings suggest that NE shifts the balance between distal and somatic inhibition to the advantage of the latter. We speculate that such shift modifies the balance of sensory-specific and emotional information in the integration of neural input to the upper layers of the auditory cortex.
Salgado
Humberto
H
Laboratory of Cell and Synaptic Physiology, School of Behavioral and Brain Sciences, University of Texas at Dallas, Richardson, TX 75080, USA. marco.atzori@utdallas.edu
Garcia-Oscos
Francisco
F
Patel
Ankur
A
Martinolich
Laura
L
Nichols
Justin A
JA
Dinh
Lu
L
Roychowdhury
Swagata
S
Tseng
Kuei-Yuan
KY
Atzori
Marco
M
D000818:Animals; D002540:Cerebral Cortex / Q000166:cytology / Q000502:physiology*; D009433:Neural Inhibition / Q000502:physiology*; D009474:Neurons / Q000166:cytology / Q000502:physiology*; D009638:Norepinephrine / Q000502:physiology*; D009924:Organ Culture 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
J Physiol. 1983 Feb;335:427-47
6875887
J Neurophysiol. 2004 Sep;92(3):1718-27
15102896
J Neurosci. 2001 Dec 15;21(24):9608-18
11739571
J Neurosci. 2000 Feb 1;20(3):937-48
10648698
Hear Res. 2003 Jul;181(1-2):116-30
12855370
Nat Neurosci. 2001 Dec;4(12):1230-7
11694887
Pharmacol Ther. 2007 Mar;113(3):523-36
17303246
J Neurophysiol. 2006 Aug;96(2):846-57
16835366
Ann N Y Acad Sci. 2003 Nov;1003:346-8
14684457
Brain Res. 2004 Apr 9;1004(1-2):125-35
15033427
Annu Rev Neurosci. 1998;21:149-86
9530495
Neurochem Res. 2009 Nov;34(11):1896-906
19357950
Nat Neurosci. 2007 Jun;10(6):743-53
17515899
Ann N Y Acad Sci. 2009 Jul;1169:143-50
19673770
Eur J Neurosci. 1997 Apr;9(4):833-47
9153591
Brain Res Brain Res Rev. 2003 Apr;42(1):33-84
12668290
Neurosci Lett. 1992 Mar 30;137(2):270-3
1316591
J Neurosci. 2003 Oct 22;23(29):9664-74
14573546
Science. 1979 Jul 20;205(4403):313-6
451605
Psychol Med. 1993 Aug;23(3):557-64
8234565
Science. 2000 Jan 14;287(5451):273-8
10634775
J Physiol. 2002 Nov 15;545(1):169-81
12433958
J Comp Neurol. 1978 Sep 1;181(1):17-39
355267
Br J Pharmacol. 1975 Aug;54(4):529-39
240474
Synapse. 2000 Sep 15;37(4):273-82
10891864
Histochemie. 1968;16(2):186-94
5710413
Neuropsychopharmacology. 2008 Aug;33(9):2263-71
17957212
Brain Res. 1988 Feb 23;442(1):131-8
2834010
Eur J Neurosci. 1999 Jun;11(6):2134-50
10336682
BMC Neurosci. 2008 Jan 16;9:8
18199338
Neurosci Res. 1995 Feb;21(4):287-99
7777219
Cereb Cortex. 2008 Jul;18(7):1506-20
17965126
Exp Brain Res. 1998 Feb;118(3):361-72
9497143
Nature. 2004 Sep 16;431(7006):312-6
15372034
J Neurosci. 1997 May 15;17(10):3894-906
9133407
Epilepsy Res. 2009 Apr;84(2-3):97-109
19201164
Brain Res. 1978 Jan 13;139(2):219-31
624057
J Neurosci. 1998 Sep 1;18(17):6963-76
9712665
J Neurophysiol. 2002 Dec;88(6):3097-107
12466433
Brain Res Bull. 1983 Apr;10(4):453-7
6860974
Science. 1998 Aug 14;281(5379):985-8
9703513
Brain Res. 1975 Mar 21;86(2):229-42
234774
Nat Neurosci. 2007 Dec;10(12):1594-600
17994013
J Neurosci. 2001 May 1;21(9):3009-16
11312285
Neuroscience. 2004;124(1):161-71
14960348
Trends Neurosci. 2007 Dec;30(12):653-61
17981345
Brain Res Brain Res Rev. 1998 May;26(2-3):113-35
9651498
Can J Physiol Pharmacol. 1997 May;75(5):479-87
9250381
Biol Psychiatry. 2005 Jun 1;57(11):1377-84
15950011
J Physiol. 2004 Nov 15;561(Pt 1):65-90
15331670
J Neurophysiol. 2000 Apr;83(4):1856-63
10758097
J Neurophysiol. 2008 Apr;99(4):2021-5
18256160
J Neurophysiol. 2004 Sep;92(3):1445-63
15084638
Neuron. 1996 Apr;16(4):815-23
8607999
J Neurosci. 1984 Jun;4(6):1607-17
6726348
J Neurosci. 1997 Nov 1;17(21):8427-42
9334415
J Neurophysiol. 2001 Mar;85(3):1078-87
11247978
J Neurosci. 2008 Jan 9;28(2):369-75
18184779
Neuron. 1993 Feb;10(2):189-200
8382497
J Neurosci. 1998 Feb 15;18(4):1305-17
9454840
Curr Opin Neurobiol. 2006 Aug;16(4):371-6
16842988
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
J Neurophysiol. 2002 Dec;88(6):3208-17
12466441
J Neurosci. 2004 Dec 1;24(48):10773-85
15574728