Recruitment of inhibition and excitation across mouse visual cortex depends on the hierarchy of interconnecting areas.
Diverse features of sensory stimuli are selectively processed in distinct brain areas. The relative recruitment of inhibitory and excitatory neurons within an area controls the gain of neurons for appropriate stimulus coding. We examined how such a balance of inhibition and excitation is differentially recruited across multiple levels of a cortical hierarchy by mapping the locations and strengths of synaptic inputs to pyramidal and parvalbumin (PV)-expressing neurons in feedforward and feedback pathways interconnecting primary (V1) and two higher visual areas. While interareal excitation was stronger in PV than in pyramidal neurons in all layer 2/3 pathways, we observed a gradual scaling down of the inhibition/excitation ratio from the most feedforward to the most feedback pathway. Our results indicate that interareal gain control depends on the hierarchical position of the source and the target, the direction of information flow through the network, and the laminar location of target neurons.
Department of Neuroscience, Washington University School of Medicine, St. Louis, United States.
Rinaldo David
0000-0001-9028-1990
RD
D'Souza
Department of Neuroscience, Washington University School of Medicine, St. Louis, United States.
Andrew Max
AM
Meier
Department of Neuroscience, Washington University School of Medicine, St. Louis, United States.
Pawan
P
Bista
Allen Institute for Brain Science, Seattle, United States.
Quanxin
Q
Wang
Department of Neuroscience, Washington University School of Medicine, St. Louis, United States.
Andreas
0000-0002-5140-3657
A
Burkhalter
D000818:Animals; D051379:Mice; D009433:Neural Inhibition; D009434:Neural Pathways / Q000502:physiology; D009474:Neurons / Q000502:physiology*; D014793:Visual Cortex / Q000502:physiology*
circuit mapping; extrastriate cortex; mouse; neuroscience; parvalbumin interneurons; visual cortex
J Neurosci. 2003 Nov 26;23(34):10904-12
14645486
J Comp Neurol. 1996 May 6;368(3):383-98
8725346
Elife. 2016 Aug 23;5:null
27552056
Front Neural Circuits. 2010 Aug 26;4:100
21960959
Neuron. 2002 Jan 17;33(2):163-75
11804565
J Neurosci. 2013 Oct 30;33(44):17373-84
24174670
Behav Brain Res. 1995 Nov;71(1-2):163-70
8747184
Front Neuroanat. 2008 Mar 28;1:3
18958197
Cell. 2014 Mar 13;156(6):1139-52
24630718
Cereb Cortex. 1991 Jan-Feb;1(1):1-47
1822724
Neuron. 2014 Oct 22;84(2):355-62
25374359
Nat Neurosci. 2008 May;11(5):535-7
18376400
Nature. 2009 Jun 4;459(7247):663-7
19396156
Nat Neurosci. 2009 Dec;12(12):1577-85
19881502
Nat Commun. 2015 Apr 14;6:6802
25869033
Neuron. 2012 Jan 12;73(1):159-70
22243754
Neuron. 2015 Jan 21;85(2):390-401
25556836
Science. 2015 Nov 27;350(6264):aac9462
26612957
Brain Struct Funct. 2007 Sep;212(2):107-19
17717691
J Neurosci. 2011 Feb 2;31(5):1905-18
21289200
J Comp Neurol. 2004 Jul 26;475(3):361-73
15221951
Cereb Cortex. 2003 Nov;13(11):1124-38
14576205
J Neurosci. 1993 Sep;13(9):3749-72
7690066
J Neurophysiol. 2000 May;83(5):2626-38
10805663
J Neurophysiol. 2014 Jun 1;111(11):2287-97
24623509
Nature. 2014 Jul 31;511(7511):596-600
25043046
Nat Neurosci. 2005 Nov;8(11):1552-9
16222228
Neuron. 2015 Aug 5;87(3):632-43
26247867
J Neurosci. 2009 Jul 15;29(28):9127-36
19605650
Neuron. 2015 Dec 16;88(6):1253-67
26671462
Neuron. 2011 Mar 24;69(6):1188-203
21435562
Neuron. 2011 Oct 20;72(2):231-43
22017986
Neuron. 2011 Dec 22;72(6):1040-54
22196338
Nature. 2013 Nov 7;503(7474):51-8
24201278
J Comp Neurol. 2007 May 20;502(3):339-57
17366604
Nat Neurosci. 2013 Aug;16(8):1068-76
23817549
Nature. 2013 Nov 28;503(7477):521-4
24097352
J Neurosci. 2000 Dec 15;20(24):RC117
11125016
J Neurosci. 2012 Mar 28;32(13):4386-99
22457489
Neuron. 2011 Dec 22;72(6):1025-39
22196337
J Neurosci. 1998 May 15;18(10):3870-96
9570816
J Neurosci. 2010 Mar 10;30(10):3652-62
20219999
J Comp Neurol. 1999 Apr 12;406(3):346-60
10102500
J Neurosci. 2011 Sep 14;31(37):13260-71
21917809
J Neurosci. 1989 Feb;9(2):600-13
2918380
Nature. 2009 Feb 26;457(7233):1142-5
19151697
Nature. 2014 Jan 16;505(7483):318-26
24429630
Science. 2013 Jun 28;340(6140):1591-4
23812718
Cereb Cortex. 2009 Oct;19(10):2281-9
19176638
J Neurosci. 2012 Jul 11;32(28):9716-26
22787057
Neuron. 2011 Oct 6;72(1):111-23
21982373
Brain Res. 2006 Aug 23;1106(1):99-110
16854386
Trends Neurosci. 2013 Mar;36(3):141-51
23273272
Curr Opin Neurobiol. 2014 Feb;24(1):28-33
24492075
Science. 2001 Aug 10;293(5532):1159-63
11498596
Neuron. 2007 Mar 1;53(5):735-46
17329212
Curr Opin Neurobiol. 2011 Oct;21(5):701-8
21723114
Exp Brain Res. 1990;80(1):49-53
2358036
Eur J Neurosci. 1991;3(2):186-200
12106217
Nature. 2012 Aug 16;488(7411):343-8
22878717
J Neurosci. 2016 Mar 23;36(12):3471-80
27013676
Curr Opin Neurobiol. 2014 Jun;26:117-24
24508565
J Comp Neurol. 1989 Jul 1;285(1):54-72
2754047
Neuron. 2005 Oct 20;48(2):315-27
16242411
Cereb Cortex. 2006 Apr;16(4):541-52
16033926