Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex.
Different subtypes of GABAergic neurons in sensory cortex exhibit diverse morphology, histochemical markers, and patterns of connectivity. These subtypes likely play distinct roles in cortical function, but their in vivo response properties remain unclear. We used in vivo calcium imaging, combined with immunohistochemical and genetic labels, to record visual responses in excitatory neurons and up to three distinct subtypes of GABAergic neurons (immunoreactive for parvalbumin, somatostatin, or vasoactive intestinal peptide) in layer 2/3 of mouse visual cortex. Excitatory neurons had sharp response selectivity for stimulus orientation and spatial frequency, while all GABAergic subtypes had broader selectivity. Further, bias in the responses of GABAergic neurons toward particular orientations or spatial frequencies tended to reflect net biases of the surrounding neurons. These results suggest that the sensory responses of layer 2/3 GABAergic neurons reflect the pooled activity of the surrounding population--a principle that may generalize across species and sensory modalities.
Kerlin
Aaron M
AM
Department of Neurobiology, Harvard Medical School, Goldenson 243, 220 Longwood Avenue, Boston, MA 02115, USA.
Andermann
Mark L
ML
Berezovskii
Vladimir K
VK
Reid
R Clay
RC
D000818:Animals; D002118:Calcium / Q000378:metabolism; D004533:Egtazic Acid / Q000031:analogs & derivatives / Q000378:metabolism; D005456:Fluorescent Dyes / Q000378:metabolism; D005968:Glutamate Decarboxylase / Q000235:genetics; D049452:Green Fluorescent Proteins / Q000235:genetics; D021621:Imaging, Three-Dimensional / Q000379:methods; D051379:Mice; D008810:Mice, Inbred C57BL; D008822:Mice, Transgenic; D009433:Neural Inhibition / Q000502:physiology*; D009474:Neurons / Q000145:classification* / Q000502:physiology*; D009949:Orientation / Q000502:physiology*; D010320:Parvalbumins / Q000378:metabolism; D010775:Photic Stimulation / Q000379:methods; D013004:Somatostatin / Q000378:metabolism; D014660:Vasoactive Intestinal Peptide / Q000378:metabolism; D014793:Visual Cortex / Q000166:cytology*; D014795:Visual Pathways / Q000502:physiology; D005680:gamma-Aminobutyric Acid / Q000378:metabolism
D005456:Fluorescent Dyes; D010320:Parvalbumins; C070379:1,2-bis(2-aminophenoxy)ethane N,N,N',N'-tetraacetic acid acetoxymethyl ester; D049452:Green Fluorescent Proteins; D014660:Vasoactive Intestinal Peptide; D013004:Somatostatin; D004533:Egtazic Acid; D005680:gamma-Aminobutyric Acid; D005968:Glutamate Decarboxylase; C402565:glutamate decarboxylase 1; D002118:Calcium
Proc R Soc Lond B Biol Sci. 1987 Jul 22;231(1263):251-88
2889214
Neuron. 2009 Nov 12;64(3):404-18
19914188
J Neurophysiol. 1978 May;41(3):798-820
660231
Neuroscience. 1984 Aug;12(4):1027-44
6384816
Nature. 2009 Apr 2;458(7238):627-31
19158677
Nat Biotechnol. 2003 Nov;21(11):1369-77
14595365
Neuron. 2009 Jun 25;62(6):850-61
19555653
J Neurosci. 2002 Sep 1;22(17):7389-97
12196560
J Neurosci. 2010 Jan 27;30(4):1551-9
20107082
Neuron. 2009 Sep 24;63(6):854-64
19778513
J Neurosci. 2000 Jan 1;20(1):470-84
10627623
Nat Methods. 2004 Oct;1(1):31-7
15782150
Nat Methods. 2010 May;7(5):399-405
20400966
Neuron. 2010 Feb 11;65(3):422-35
20159454
J Neurophysiol. 2010 Aug;104(2):840-53
20554844
J Neurosci. 2007 Sep 26;27(39):10333-44
17898205
J Neurosci. 2000 May 1;20(9):3354-68
10777798
J Neurophysiol. 1985 Oct;54(4):782-806
2999347
Nat Neurosci. 2005 Nov;8(11):1552-9
16222228
Front Neurosci. 2008 Dec 15;2(2):155-67
19225588
J Comp Neurol. 2010 Feb 1;518(3):389-404
19950390
Nat Neurosci. 2010 Jan;13(1):133-40
20023653
Nat Neurosci. 2010 Jan;13(1):89-96
19946318
Nat Neurosci. 2000 Sep;3(9):904-10
10966621
J Comp Neurol. 2003 Dec 1;467(1):60-79
14574680
J Comp Neurol. 1993 Mar 22;329(4):519-38
7681071
J Neurosci. 2007 Feb 21;27(8):2145-9
17314309
J Neurosci. 2002 Jul 1;22(13):5639-51
12097515
J Neurophysiol. 1983 Apr;49(4):1051-72
6854357
Doc Ophthalmol. 2004 May;108(3):181-4
15573941
J Physiol. 2003 Aug 15;551(Pt 1):49-65
12844506
J Neurophysiol. 1999 Jul;82(1):301-11
10400959
Nature. 2010 Apr 29;464(7293):1307-12
20428163
Exp Brain Res. 1983;50(2-3):193-200
6641854
J Neurosci. 2003 Nov 12;23(32):10201-13
14614078
Biomed Eng Online. 2003 May 17;2:13
12801419
Nat Rev Neurosci. 2004 Oct;5(10):793-807
15378039
Proc Natl Acad Sci U S A. 2005 Sep 27;102(39):14063-8
16157876
J Neurosci. 1987 May;7(5):1414-27
3572486
Nat Protoc. 2009;4(8):1145-56
19617886
Neuron. 2002 Dec 5;36(5):969-78
12467599
Nat Methods. 2006 May;3(5):377-83
16628208
Trends Neurosci. 2005 Jun;28(6):304-9
15927686
Nat Neurosci. 2006 Apr;9(4):543-51
16547511
Nature. 2006 Aug 24;442(7105):925-8
16906137
Cereb Cortex. 1997 Sep;7(6):534-45
9276178
Cereb Cortex. 1997 Sep;7(6):476-86
9276173
J Neurophysiol. 2008 Nov;100(5):2640-52
18799598
J Comp Neurol. 1975 Apr 1;160(3):269-90
1112925
Neuron. 2009 Aug 27;63(4):508-22
19709632
Nature. 1981 Sep 24;293(5830):300-2
7278987
Nature. 2005 Feb 10;433(7026):597-603
15660108
J Neurosci. 1999 Jul 1;19(13):5228-35
10377334
Nat Neurosci. 2010 Mar;13(3):361-8
20118924
Cereb Cortex. 2008 May;18(5):1058-78
17720684
J Neurosci. 2004 Jun 2;24(22):5101-8
15175379
J Neurosci. 1998 Sep 1;18(17):6963-76
9712665
J Physiol. 2003 Aug 15;551(Pt 1):139-53
12813147
Science. 1998 Aug 14;281(5379):985-8
9703513
J Comp Neurol. 2006 Nov 1;499(1):144-60
16958092
Proc Natl Acad Sci U S A. 2009 Nov 17;106(46):19557-62
19889973
Nat Protoc. 2006;1(1):380-6
17406260
Nat Neurosci. 2005 Feb;8(2):194-201
15665876
Neuron. 2007 Jun 21;54(6):961-72
17582335
Proc Natl Acad Sci U S A. 2003 Jun 10;100(12):7319-24
12777621
J Neurosci. 2004 Feb 11;24(6):1272-9
14960597
Neuron. 2010 Feb 25;65(4):472-9
20188652
Front Cell Neurosci. 2010 Mar 12;4:3
20407583
Nature. 2009 Jun 4;459(7247):663-7
19396156
J Comp Neurol. 1978 Jun 15;179(4):761-93
346619
J Neurosci. 2005 Jan 5;25(1):19-28
15634763
J Physiol. 2005 Jan 1;562(Pt 1):9-26
15539390
Neuron. 2008 Mar 13;57(5):673-9
18341988
Neuron. 2009 Jan 29;61(2):168-85
19186161
J Neurosci. 2008 Jul 23;28(30):7520-36
18650330
J Comp Neurol. 1985 Apr 8;234(2):242-63
3988984
Nature. 1991 Oct 3;353(6343):429-31
1896085
J Neurophysiol. 2003 Feb;89(2):1003-15
12574476
J Comp Neurol. 1997 Apr 7;380(2):230-42
9100134
Nat Neurosci. 2010 Mar;13(3):353-60
20118927
Nat Rev Neurosci. 2008 Jul;9(7):557-68
18568015
Science. 2004 Mar 12;303(5664):1681-3
15017002
PLoS Biol. 2005 May;3(5):e159
15836427
J Neurophysiol. 1988 Apr;59(4):1162-87
3373273
J Comp Neurol. 1980 Sep 1;193(1):203-22
6776165
Biol Cybern. 1987;57(6):349-55
3435723
Brain Res. 1977 Nov 4;136(1):154-8
589442
Nature. 2009 Jun 4;459(7247):698-702
19396159
Nat Neurosci. 2003 Dec;6(12):1300-8
14625553
J Neurosci. 1997 Nov 1;17(21):8621-44
9334433
J Neurosci. 2009 Jan 7;29(1):70-85
19129386
J Neurosci. 2009 Aug 26;29(34):10520-32
19710305