A Disinhibitory Circuit for Contextual Modulation in Primary Visual Cortex.

canonical disinhibitory circuit computational modeling contextual modulation figure-ground segregation inhibitory neurons pop-out effects recurrent neural network saliency stabilized supralinear network visual cortex

Journal

Neuron
ISSN: 1097-4199
Titre abrégé: Neuron
Pays: United States
ID NLM: 8809320

Informations de publication

Date de publication:
23 12 2020
Historique:
received: 30 04 2020
revised: 17 10 2020
accepted: 13 11 2020
pubmed: 11 12 2020
medline: 3 2 2021
entrez: 10 12 2020
Statut: ppublish

Résumé

Context guides perception by influencing stimulus saliency. Accordingly, in visual cortex, responses to a stimulus are modulated by context, the visual scene surrounding the stimulus. Responses are suppressed when stimulus and surround are similar but not when they differ. The underlying mechanisms remain unclear. Here, we use optical recordings, manipulations, and computational modeling to show that disinhibitory circuits consisting of vasoactive intestinal peptide (VIP)-expressing and somatostatin (SOM)-expressing inhibitory neurons modulate responses in mouse visual cortex depending on similarity between stimulus and surround, primarily by modulating recurrent excitation. When stimulus and surround are similar, VIP neurons are inactive, and activity of SOM neurons leads to suppression of excitatory neurons. However, when stimulus and surround differ, VIP neurons are active, inhibiting SOM neurons, which leads to relief of excitatory neurons from suppression. We have identified a canonical cortical disinhibitory circuit that contributes to contextual modulation and may regulate perceptual saliency.

Identifiants

pubmed: 33301712
pii: S0896-6273(20)30891-6
doi: 10.1016/j.neuron.2020.11.013
pmc: PMC7850578
mid: NIHMS1654637
pii:
doi:

Substances chimiques

Vasoactive Intestinal Peptide 37221-79-7
Somatostatin 51110-01-1
Calcium SY7Q814VUP

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

1181-1193.e8

Subventions

Organisme : Howard Hughes Medical Institute
Pays : United States
Organisme : NCRR NIH HHS
ID : G20 RR030893
Pays : United States
Organisme : NINDS NIH HHS
ID : U19 NS107613
Pays : United States

Informations de copyright

Copyright © 2020 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Interests The authors declare no competing interests.

Références

Curr Biol. 2019 Dec 16;29(24):4268-4275.e7
pubmed: 31786063
Elife. 2020 May 27;9:
pubmed: 32458798
Nature. 2014 Jul 31;511(7511):596-600
pubmed: 25043046
Nature. 2020 Mar;579(7798):256-259
pubmed: 32132709
Neuron. 2018 May 16;98(4):846-860.e5
pubmed: 29772203
Neuron. 2012 Nov 21;76(4):695-711
pubmed: 23177956
Neuron. 2008 Feb 28;57(4):482-97
pubmed: 18304479
Science. 2015 Nov 27;350(6264):aac9462
pubmed: 26612957
Nature. 1986 Mar 27-Apr 2;320(6060):362-5
pubmed: 3960119
Nat Commun. 2018 Jun 11;9(1):2281
pubmed: 29892057
J Neurophysiol. 1965 Mar;28:229-89
pubmed: 14283058
Nature. 1983 Jun 23-29;303(5919):696-8
pubmed: 6855915
J Neurophysiol. 1992 Apr;67(4):961-80
pubmed: 1588394
J Neurosci. 2014 Jul 9;34(28):9290-304
pubmed: 25009262
Brain Res. 1978 Jan 13;139(2):359-65
pubmed: 624064
Cogn Neurodyn. 2010 Mar;4(1):1-24
pubmed: 19898958
J Neurosci. 1997 Jun 1;17(11):4382-8
pubmed: 9151754
J Neurosci. 2006 Aug 23;26(34):8715-26
pubmed: 16928860
Neuron. 2020 May 6;106(3):388-403.e18
pubmed: 32142648
Neuron. 2007 Oct 4;56(1):43-57
pubmed: 17920014
J Neurophysiol. 2001 Oct;86(4):2011-28
pubmed: 11600658
J Neurosci. 2012 Nov 7;32(45):15946-51
pubmed: 23136432
Nat Commun. 2019 Jun 3;10(1):2431
pubmed: 31160566
Invest Ophthalmol. 1972 May;11(5):302-11
pubmed: 5028229
J Neurosci. 2001 Mar 1;21(5):1698-709
pubmed: 11222659
Neuron. 2018 May 2;98(3):602-615.e8
pubmed: 29656873
Nat Neurosci. 2016 Feb;19(2):299-307
pubmed: 26691828
Nat Neurosci. 2004 Oct;7(10):1113-22
pubmed: 15338009
Proc Natl Acad Sci U S A. 1999 Oct 12;96(21):12073-8
pubmed: 10518578
J Neurosci. 2010 Oct 27;30(43):14371-9
pubmed: 20980594
Elife. 2016 Aug 23;5:
pubmed: 27552056
J Neurosci. 1999 Dec 1;19(23):10536-53
pubmed: 10575050
Front Neural Circuits. 2014 Mar 28;8:30
pubmed: 24734005
Neuron. 2016 Apr 6;90(1):86-100
pubmed: 27021171
J Vis Exp. 2014 Feb 20;(84):e50885
pubmed: 24637961
Neuron. 2017 Aug 30;95(5):1147-1159.e4
pubmed: 28858618
Nature. 2011 May 5;473(7345):87-91
pubmed: 21478872
Exp Brain Res. 1972;15(4):439-40
pubmed: 5079475
Proc Natl Acad Sci U S A. 2015 Jun 2;112(22):7085-90
pubmed: 25901330
Elife. 2018 Sep 26;7:
pubmed: 30256194
J Physiol. 1962 Jan;160:106-54
pubmed: 14449617
Cell. 2017 Jun 15;169(7):1291-1302.e14
pubmed: 28602353
Science. 2014 Aug 8;345(6197):660-5
pubmed: 25104383
Neuron. 2009 May 28;62(4):578-92
pubmed: 19477158
Nature. 2012 Oct 11;490(7419):226-31
pubmed: 23060193
Front Comput Neurosci. 2017 Apr 25;11:28
pubmed: 28487644
Nat Neurosci. 1999 Jan;2(1):79-87
pubmed: 10195184
Neural Comput. 2013 Aug;25(8):1994-2037
pubmed: 23663149
Front Syst Neurosci. 2011 Apr 13;5:18
pubmed: 21811444
Nat Neurosci. 2011 Jul 17;14(8):1045-52
pubmed: 21765421
Nat Neurosci. 2003 Dec;6(12):1251-2
pubmed: 14595442
Neuron. 2015 May 6;86(3):740-54
pubmed: 25892300
J Neurophysiol. 1964 Nov;27:1154-73
pubmed: 14223976
Sci Rep. 2018 Dec 12;8(1):17800
pubmed: 30542060
Neuroscientist. 2013 Jun;19(3):228-37
pubmed: 22922685
J Neurosci. 1995 Feb;15(2):1605-15
pubmed: 7869121
J Neurophysiol. 2016 Mar;115(3):1399-409
pubmed: 26740531
Elife. 2020 Jun 29;9:
pubmed: 32598278
Neuron. 2008 Jan 10;57(1):135-46
pubmed: 18184570
J Neurosci. 2010 Dec 15;30(50):16796-808
pubmed: 21159951
Curr Opin Neurobiol. 2000 Aug;10(4):438-43
pubmed: 10981611
Elife. 2020 Oct 27;9:
pubmed: 33108272
IEEE Trans Neural Netw. 1994;5(2):157-66
pubmed: 18267787
Neuron. 2010 Jan 14;65(1):107-21
pubmed: 20152117
Neuron. 2015 Jan 21;85(2):402-17
pubmed: 25611511
Cogn Psychol. 1980 Jan;12(1):97-136
pubmed: 7351125
Nature. 2003 May 22;423(6938):401-8
pubmed: 12754524
Neuron. 2018 Oct 24;100(2):424-435
pubmed: 30359606
J Neurophysiol. 2000 Oct;84(4):2048-62
pubmed: 11024097
Nature. 1995 Nov 30;378(6556):492-6
pubmed: 7477405
Cell. 2014 Mar 13;156(6):1139-1152
pubmed: 24630718
Nat Commun. 2016 Jul 19;7:12190
pubmed: 27432255
Nat Neurosci. 2015 Nov;18(11):1648-55
pubmed: 26436902
Nat Methods. 2019 Jul;16(7):649-657
pubmed: 31209382
Nature. 2020 Jun;582(7813):545-549
pubmed: 32499655
Nature. 2015 Feb 19;518(7539):399-403
pubmed: 25652823
Nature. 2013 Nov 28;503(7477):521-4
pubmed: 24097352
Nat Neurosci. 2013 Aug;16(8):1068-76
pubmed: 23817549
Annu Rev Neurosci. 2017 Jul 25;40:425-451
pubmed: 28471714
Front Psychol. 2017 Sep 12;8:1551
pubmed: 28955272
J Physiol Paris. 2003 Jul-Nov;97(4-6):453-74
pubmed: 15242657
Neuron. 2016 Jul 20;91(2):260-92
pubmed: 27477017

Auteurs

Andreas J Keller (AJ)

Department of Physiology, University of California, San Francisco, San Francisco, CA 94158-0444, USA; Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, CA, USA. Electronic address: andreasjakob.keller@ucsf.edu.

Mario Dipoppa (M)

Center for Theoretical Neuroscience, College of Physicians and Surgeons and Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York City, NY 10027, USA. Electronic address: md3681@columbia.edu.

Morgane M Roth (MM)

Department of Physiology, University of California, San Francisco, San Francisco, CA 94158-0444, USA; Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, CA, USA. Electronic address: morgane.roth@ucsf.edu.

Matthew S Caudill (MS)

Center for Neural Circuits and Behavior, Neurobiology Section and Department of Neuroscience, University of California, San Diego, La Jolla, CA 92093-0634, USA; Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, CA, USA.

Alessandro Ingrosso (A)

Center for Theoretical Neuroscience, College of Physicians and Surgeons and Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York City, NY 10027, USA.

Kenneth D Miller (KD)

Center for Theoretical Neuroscience, College of Physicians and Surgeons and Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York City, NY 10027, USA; Department of Neuroscience, Swartz Program in Theoretical Neuroscience, Kavli Institute for Brain Science, College of Physicians and Surgeons and Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University, New York City, NY, USA. Electronic address: kdm2103@columbia.edu.

Massimo Scanziani (M)

Department of Physiology, University of California, San Francisco, San Francisco, CA 94158-0444, USA; Center for Neural Circuits and Behavior, Neurobiology Section and Department of Neuroscience, University of California, San Diego, La Jolla, CA 92093-0634, USA; Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, CA, USA. Electronic address: massimo@ucsf.edu.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH