Distinctive classes of GABAergic interneurons provide layer-specific phasic inhibition in the anterior piriform cortex.
The primary olfactory (or piriform) cortex is a trilaminar paleocortex that is seen increasingly as an attractive model system for the study of cortical sensory processing. Recent findings highlight the importance of γ-amino butyric acid (GABA)-releasing interneurons for the function of the piriform cortex (PC), yet little is known about the different types of interneurons in the PC. Here, we provide the first detailed functional characterization of the major classes of GABAergic interneurons in the anterior piriform cortex (aPC) and show how these classes differentially engage in phasic synaptic inhibition. By measuring the electrical properties of interneurons and combining this with information about their morphology, laminar location, and expression of molecular markers, we have identified 5 major classes in the aPC of the mouse. Each layer contains at least one class of interneuron that is tuned to fire either earlier or later in a train of stimuli resembling the input received by the PC in vivo during olfaction. This suggests that the different subtypes of interneuron are specialized for providing synaptic inhibition at different phases of the sniff cycle. Thus, our results suggest mechanisms by which classes of interneurons play specific roles in the processing performed by the PC in order to recognize odors.
Suzuki
Norimitsu
N
Neuroscience Program, The John Curtin School of Medical Research, The Australian National University, Canberra, ACT 0200, Australia.
Bekkers
John M
JM
D000818:Animals; D007150:Immunohistochemistry; D007395:Interneurons / Q000166:cytology / Q000378:metabolism*; D051379:Mice; D008810:Mice, Inbred C57BL; D008822:Mice, Transgenic; D018613:Microscopy, Confocal; D009433:Neural Inhibition / Q000502:physiology*; D009833:Olfactory Pathways / Q000166:cytology / Q000378:metabolism* / Q000502:physiology; D009924:Organ Culture Techniques; D018408:Patch-Clamp Techniques; D012903:Smell / Q000502:physiology*; D009435:Synaptic Transmission / Q000502:physiology*; D005680:gamma-Aminobutyric Acid / Q000378:metabolism
D005680:gamma-Aminobutyric Acid
Science. 2004 Jun 25;304(5679):1926-9
15218136
Neuron. 2006 Feb 2;49(3):357-63
16446140
J Neurosci. 1996 Apr 15;16(8):2701-15
8786446
J Neurosci. 2009 Mar 18;29(11):3642-59
19295167
J Physiol. 1999 Apr 1;516 ( Pt 1):227-48
10066937
Nat Neurosci. 1998 Aug;1(4):279-85
10195160
J Neurophysiol. 2003 Dec;90(6):3921-30
12917385
Clin Exp Pharmacol Physiol. 2007 Oct;34(10):1064-9
17714095
J Neurophysiol. 1983 Jul;50(1):89-101
6875654
Cereb Cortex. 2009 Apr;19(4):938-50
18787231
J Comp Neurol. 1983 Jan 10;213(2):163-87
6841668
Neuron. 2009 Jun 25;62(6):850-61
19555653
Nat Rev Neurosci. 2002 Nov;3(11):884-95
12415296
J Neurophysiol. 2003 Nov;90(5):2987-3000
12815025
Neuron. 2009 Sep 24;63(6):854-64
19778513
Nat Neurosci. 2007 Jun;10(6):743-53
17515899
J Neurosci. 1996 Sep 1;16(17):5290-300
8757242
J Neurosci. 2006 Nov 15;26(46):11938-47
17108168
J Comp Neurol. 2003 Dec 1;467(1):60-79
14574680
Trends Neurosci. 2003 Sep;26(9):484-8
12948659
J Neurosci. 2007 Feb 14;27(7):1534-42
17301162
J Neurophysiol. 2007 Jan;97(1):670-9
16870834
Eur J Pharmacol. 1996 Jun 3;305(1-3):95-100
8813537
Eur J Neurosci. 2003 Jun;17(11):2457-61
12814377
J Comp Neurol. 2001 Jun 4;434(3):308-28
11331531
Cereb Cortex. 2008 Feb;18(2):315-30
17517679
Chem Senses. 2001 Jun;26(5):577-84
11418503
J Neurosci. 2003 May 15;23(10):4108-16
12764098
Nat Rev Neurosci. 2004 Oct;5(10):793-807
15378039
Neuron. 2007 Oct 4;56(1):33-42
17920013
Cereb Cortex. 2009 Dec;19(12):3011-29
19359350
J Neurophysiol. 2007 Nov;98(5):2716-28
17855583
Trends Neurosci. 2009 Apr;32(4):207-14
19243843
Nature. 2009 Oct 29;461(7268):1278-81
19865171
Cereb Cortex. 1997 Sep;7(6):476-86
9276173
Science. 2003 Mar 21;299(5614):1902-5
12649485
J Neurosci. 2004 Mar 24;24(12):2853-65
15044524
Science. 2008 Jul 4;321(5885):53-7
18599766
Prog Brain Res. 2002;136:215-38
12143384
J Neurosci. 2005 Jul 6;25(27):6278-85
16000617
Trends Neurosci. 2003 Oct;26(10):564-71
14522150
J Neurophysiol. 2006 Aug;96(2):834-45
16707715
J Neurosci. 2009 Oct 7;29(40):12641-52
19812339
J Physiol. 1997 May 1;500 ( Pt 3):715-38
9161987
Brain Res. 2000 May 19;865(1):1-11
10814727
J Neurosci. 2009 Oct 28;29(43):13649-61
19864577
J Comp Neurol. 2010 May 15;518(10):1670-87
20235162
J Neurosci. 2008 Aug 27;28(35):8851-9
18753387
J Neurophysiol. 1997 Nov;78(5):2531-45
9356403
J Neurosci. 2005 Jul 20;25(29):6775-86
16033887
Nat Rev Neurosci. 2001 Jan;2(1):11-23
11253355
J Neurosci. 2003 Jan 1;23(1):96-102
12514205
Neuron. 2009 Apr 30;62(2):171-89
19409263
Nat Rev Neurosci. 2008 Jul;9(7):557-68
18568015
J Neurosci. 2007 Jan 17;27(3):553-63
17234587
J Neurosci. 2008 Jul 2;28(27):6974-82
18596171