The amygdala instructs insular feedback for affective learning.

affective learning amygdala cholinergic basal forebrain hierarchical interaction insular cortex interoceptive value mouse neuroscience

Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
20 11 2020
Historique:
received: 23 06 2020
accepted: 04 11 2020
entrez: 20 11 2020
pubmed: 21 11 2020
medline: 23 3 2021
Statut: epublish

Résumé

Affective responses depend on assigning value to environmental predictors of threat or reward. Neuroanatomically, this affective value is encoded at both cortical and subcortical levels. However, the purpose of this distributed representation across functional hierarchies remains unclear. Using fMRI in mice, we mapped a discrete cortico-limbic loop between insular cortex (IC), central amygdala (CE), and nucleus basalis of Meynert (NBM), which decomposes the affective value of a conditioned stimulus (CS) into its salience and valence components. In IC, learning integrated unconditioned stimulus (US)-evoked bodily states into CS valence. In turn, CS salience in the CE recruited these CS representations bottom-up via the cholinergic NBM. This way, the CE incorporated interoceptive feedback from IC to improve discrimination of CS valence. Consequently, opto-/chemogenetic uncoupling of hierarchical information flow disrupted affective learning and conditioned responding. Dysfunctional interactions in the IC↔CE/NBM network may underlie intolerance to uncertainty, observed in autism and related psychiatric conditions.

Identifiants

pubmed: 33216712
doi: 10.7554/eLife.60336
pii: 60336
pmc: PMC7679142
doi:
pii:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : European Commission
ID : 311701
Pays : International
Organisme : Austrian Research Promotion Agency
ID : 852936
Pays : International
Organisme : Austrian Research Promotion Agency
ID : 854174
Pays : International

Informations de copyright

© 2020, Kargl et al.

Déclaration de conflit d'intérêts

DK, JK, SU, FG, LP, JL, KB, WH No competing interests declared

Références

Neuron. 2020 Jun 17;106(6):1026-1043.e9
pubmed: 32294466
Neuron. 2006 Jun 15;50(6):963-74
pubmed: 16772176
J Neurosci. 2010 Mar 3;30(9):3210-9
pubmed: 20203180
J Neurophysiol. 2009 Jun;101(6):3270-83
pubmed: 19339462
Nat Rev Neurosci. 2015 Jan;16(1):55-61
pubmed: 25406711
Psychol Rev. 1980 Nov;87(6):532-52
pubmed: 7443916
Trends Cogn Sci. 2016 Feb;20(2):96-106
pubmed: 26704857
Nat Neurosci. 2019 Sep;22(9):1424-1437
pubmed: 31455886
Cereb Cortex. 2015 Jan;25(1):118-37
pubmed: 23964066
Neuroimage. 2009 Oct 1;47(4):1408-16
pubmed: 19442749
Neuroimage. 2007 Aug 15;37(2):579-88
pubmed: 17604651
J Cogn Neurosci. 2014 Jul;26(7):1546-54
pubmed: 24392894
Trends Neurosci. 2013 Dec;36(12):706-16
pubmed: 24157198
Neuron. 2017 Jul 5;95(1):70-77.e3
pubmed: 28683271
Nat Neurosci. 2014 Jan;17(1):106-13
pubmed: 24241397
Neuroimage. 2008 Jan 1;39(1):538-47
pubmed: 17904386
Nat Neurosci. 2015 Apr;18(4):499-500
pubmed: 25751532
Neuroimage. 2009 Feb 1;44(3):893-905
pubmed: 18976716
Proc Natl Acad Sci U S A. 2003 Nov 25;100(24):13940-5
pubmed: 14615590
J Neurosci. 2006 Apr 5;26(14):3791-7
pubmed: 16597732
Behav Neurosci. 1994 Feb;108(1):81-93
pubmed: 8192853
J Cogn Neurosci. 2007 Dec;19(12):2082-99
pubmed: 17892391
Trends Cogn Sci. 2018 Apr;22(4):294-306
pubmed: 29475638
J Neurosci. 2018 Feb 21;38(8):1942-1958
pubmed: 29348191
Hum Brain Mapp. 2017 Apr;38(4):2150-2164
pubmed: 28070928
Neuron. 2010 Aug 26;67(4):656-66
pubmed: 20797541
Annu Rev Neurosci. 2000;23:473-500
pubmed: 10845072
Nat Neurosci. 2004 Feb;7(2):189-95
pubmed: 14730305
Nature. 2017 Jun 29;546(7660):611-616
pubmed: 28614299
Nat Neurosci. 2018 Jul;21(7):952-962
pubmed: 29950668
Elife. 2016 Aug 30;5:
pubmed: 27572258
Neuroimage. 2007 Aug 1;37(1):90-101
pubmed: 17560126
Front Hum Neurosci. 2014 May 14;8:302
pubmed: 24860482
Cell Rep. 2017 Nov 14;21(7):1770-1782
pubmed: 29141212
Brain Connect. 2012;2(1):25-32
pubmed: 22432927
Autism Res. 2018 Apr;11(4):636-644
pubmed: 29316350
Learn Mem. 2001 May-Jun;8(3):148-55
pubmed: 11390634
Neuroimage. 2005 Feb 1;24(3):810-21
pubmed: 15652316
Soc Cogn Affect Neurosci. 2017 Jan 1;12(1):1-23
pubmed: 27798257
Neuron. 2002 Feb 14;33(4):615-24
pubmed: 11856534
Neuron. 2008 Jul 10;59(1):138-49
pubmed: 18614035
Nat Commun. 2019 Mar 4;10(1):1022
pubmed: 30833582
J Comp Neurol. 1982 Jul 10;208(4):401-18
pubmed: 7119168
Elife. 2017 May 19;6:
pubmed: 28524817
J Am Acad Child Adolesc Psychiatry. 2008 Aug;47(8):921-9
pubmed: 18645422
Cell. 2015 Aug 27;162(5):1155-68
pubmed: 26317475
Neuron. 2017 Mar 22;93(6):1464-1479.e5
pubmed: 28334609
Neural Netw. 2002 Jun-Jul;15(4-6):495-506
pubmed: 12371507
PLoS One. 2013 Jul 04;8(7):e68910
pubmed: 23861951
Prog Neurobiol. 1991;37(6):475-524
pubmed: 1763188
J Neurophysiol. 2007 Jul;98(1):253-65
pubmed: 17460101
J Neurosci. 2018 Feb 7;38(6):1418-1429
pubmed: 29305535
Schizophr Res. 2016 Oct;176(2-3):83-94
pubmed: 27450778
Mol Psychiatry. 2018 Nov 30;:
pubmed: 30504824
Neuroscience. 2002;111(1):133-49
pubmed: 11955718
Neuroimage. 2017 Jul 1;154:169-173
pubmed: 27888059
Front Hum Neurosci. 2010 Dec 02;4:215
pubmed: 21160551
Nat Neurosci. 2017 Sep;20(9):1293-1299
pubmed: 28758996
Front Neural Circuits. 2010 Mar 22;4:8
pubmed: 20407636
J Autism Dev Disord. 2006 Jan;36(1):5-25
pubmed: 16450045
Proc Natl Acad Sci U S A. 2009 Sep 1;106(35):15031-6
pubmed: 19706473
Front Syst Neurosci. 2010 May 14;4:13
pubmed: 20577591
Curr Opin Neurobiol. 2018 Apr;49:141-147
pubmed: 29522976
Neuroimage. 2018 Mar;168:392-402
pubmed: 28392491
eNeuro. 2018 Sep 11;5(3):
pubmed: 30211307
Nat Rev Neurosci. 2015 Jul;16(7):419-29
pubmed: 26016744
Neuron. 2017 Oct 11;96(2):414-427.e8
pubmed: 29024664
Neuron. 2005 May 19;46(4):681-92
pubmed: 15944135
Ann N Y Acad Sci. 1999 Jun 29;877:217-41
pubmed: 10415652
Cereb Cortex. 2012 Mar;22(3):509-26
pubmed: 21693490
Front Hum Neurosci. 2012 Aug 23;6:242
pubmed: 22936906
Neural Netw. 2018 Jun;102:120-137
pubmed: 29571122
Neuron. 2020 Mar 18;105(6):1094-1111.e10
pubmed: 31955944
Cereb Cortex. 2015 Jul;25(7):1815-26
pubmed: 24451658
Nat Neurosci. 2016 Apr;19(4):605-12
pubmed: 26878674
Nat Neurosci. 2013 Mar;16(3):332-9
pubmed: 23354330
Proc Natl Acad Sci U S A. 2017 Sep 12;114(37):9972-9977
pubmed: 28847938
Nature. 2017 Mar 30;543(7647):670-675
pubmed: 28329757
J Comput Neurosci. 2011 Feb;30(1):85-107
pubmed: 20799057
Neuron. 2015 Oct 7;88(1):220-35
pubmed: 26447583
Nat Neurosci. 2017 Dec;20(12):1680-1685
pubmed: 29184202
Annu Rev Neurosci. 2000;23:155-84
pubmed: 10845062
PLoS One. 2011;6(9):e25031
pubmed: 21949842
Science. 2020 Apr 3;368(6486):89-94
pubmed: 32241948
Nat Rev Neurosci. 2002 Aug;3(8):655-66
pubmed: 12154366
Nature. 2010 Nov 11;468(7321):270-6
pubmed: 21068836
Nat Rev Neurosci. 2001 May;2(5):352-63
pubmed: 11331919
Magn Reson Med. 1996 Mar;35(3):346-55
pubmed: 8699946
Curr Opin Neurobiol. 2010 Dec;20(6):704-16
pubmed: 20850966
Brain. 2015 Oct;138(Pt 10):3061-75
pubmed: 26264514
J Comp Neurol. 1997 Jun 30;383(2):163-77
pubmed: 9182846
PLoS One. 2012;7(5):e37828
pubmed: 22666397
Neuron. 2013 Oct 16;80(2):519-30
pubmed: 24139048
Neuron. 2007 Sep 20;55(6):970-84
pubmed: 17880899
Behav Neurosci. 1999 Feb;113(1):143-51
pubmed: 10197914

Auteurs

Dominic Kargl (D)

Research Institute of Molecular Pathology (IMP), Vienna Biocenter (VBC), Vienna, Austria.

Joanna Kaczanowska (J)

Research Institute of Molecular Pathology (IMP), Vienna Biocenter (VBC), Vienna, Austria.

Sophia Ulonska (S)

VRVis Zentrum für Virtual Reality und Visualisierung Forschungs-GmbH (VRVis), Vienna, Austria.

Florian Groessl (F)

Research Institute of Molecular Pathology (IMP), Vienna Biocenter (VBC), Vienna, Austria.

Lukasz Piszczek (L)

Research Institute of Molecular Pathology (IMP), Vienna Biocenter (VBC), Vienna, Austria.

Jelena Lazovic (J)

Preclinical Imaging Facility (pcIMAG), Vienna Biocenter Core Facilities (VBCF), Vienna, Austria.

Katja Buehler (K)

VRVis Zentrum für Virtual Reality und Visualisierung Forschungs-GmbH (VRVis), Vienna, Austria.

Wulf Haubensak (W)

Research Institute of Molecular Pathology (IMP), Vienna Biocenter (VBC), Vienna, Austria.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH