Serotonin modulates asymmetric learning from reward and punishment in healthy human volunteers.


Journal

Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179

Informations de publication

Date de publication:
12 08 2022
Historique:
received: 19 11 2020
accepted: 08 07 2022
entrez: 12 8 2022
pubmed: 13 8 2022
medline: 17 8 2022
Statut: epublish

Résumé

Instrumental learning is driven by a history of outcome success and failure. Here, we examined the impact of serotonin on learning from positive and negative outcomes. Healthy human volunteers were assessed twice, once after acute (single-dose), and once after prolonged (week-long) daily administration of the SSRI citalopram or placebo. Using computational modelling, we show that prolonged boosting of serotonin enhances learning from punishment and reduces learning from reward. This valence-dependent learning asymmetry increases subjects' tendency to avoid actions as a function of cumulative failure without leading to detrimental, or advantageous, outcomes. By contrast, no significant modulation of learning was observed following acute SSRI administration. However, differences between the effects of acute and prolonged administration were not significant. Overall, these findings may help explain how serotonergic agents impact on mood disorders.

Identifiants

pubmed: 35962142
doi: 10.1038/s42003-022-03690-5
pii: 10.1038/s42003-022-03690-5
pmc: PMC9374781
doi:

Substances chimiques

Serotonin Uptake Inhibitors 0
Serotonin 333DO1RDJY

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

812

Subventions

Organisme : Wellcome Trust
ID : 098362/Z/12/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 091593/Z/10/Z
Pays : United Kingdom

Informations de copyright

© 2022. The Author(s).

Références

Neuropsychopharmacology. 2010 May;35(6):1290-301
pubmed: 20107431
Pharmacotherapy. 2000 Dec;20(12):1441-7
pubmed: 11130216
Biol Cybern. 2013 Dec;107(6):711-9
pubmed: 24085507
Psychopharmacology (Berl). 2014 Mar;231(5):955-66
pubmed: 24232442
J Neurosci. 2015 Jul 8;35(27):9811-22
pubmed: 26156984
Lancet Psychiatry. 2017 May;4(5):409-418
pubmed: 28153641
Eur J Pharmacol. 2015 Apr 15;753:2-18
pubmed: 25446560
PLoS Comput Biol. 2011 Apr;7(4):e1002028
pubmed: 21556131
Psychopharmacology (Berl). 2021 May;238(5):1265-1278
pubmed: 31938879
Neuron. 2012 Dec 6;76(5):998-1009
pubmed: 23217747
Neuropsychopharmacology. 2018 Dec;43(13):2645-2651
pubmed: 30305705
Proc Natl Acad Sci U S A. 2014 Aug 19;111(33):12252-7
pubmed: 25092308
Neuropsychopharmacology. 2011 Jan;36(2):402-10
pubmed: 20980990
Trends Cogn Sci. 2014 Apr;18(4):194-202
pubmed: 24581556
J Neurosci. 2009 Jan 14;29(2):436-43
pubmed: 19144843
Proc Natl Acad Sci U S A. 2009 Mar 31;106(13):5035-40
pubmed: 19289824
Proc Natl Acad Sci U S A. 2009 Nov 10;106(45):19179-84
pubmed: 19850878
Nat Commun. 2015 Jan 21;6:6149
pubmed: 25608088
PLoS One. 2018 Nov 28;13(11):e0206923
pubmed: 30485304
J Neurosci. 2012 Jul 25;32(30):10318-30
pubmed: 22836265
Curr Biol. 2018 May 7;28(9):1433-1439.e7
pubmed: 29706512
Proc Natl Acad Sci U S A. 2016 Apr 26;113(17):4812-7
pubmed: 27071092
J Neurosci. 2009 Dec 16;29(50):15669-74
pubmed: 20016081
Psychol Med. 2014 Feb;44(3):579-92
pubmed: 23672737
Neuroimage. 2014 Oct 1;99:434-42
pubmed: 24857827
Science. 2006 Feb 10;311(5762):861-3
pubmed: 16469930
Eur Neuropsychopharmacol. 2013 Aug;23(8):919-30
pubmed: 23051938
PLoS Comput Biol. 2012;8(3):e1002410
pubmed: 22412360
J Pers Soc Psychol. 1988 Jun;54(6):1063-70
pubmed: 3397865
Elife. 2017 Oct 04;6:
pubmed: 28976304
Brain Res. 2014 Mar 27;1556:19-27
pubmed: 24508910
Neuron. 2013 Nov 20;80(4):1090-100
pubmed: 24267657
Front Hum Neurosci. 2014 Aug 28;8:639
pubmed: 25221492
Biol Psychiatry. 2010 Jul 15;68(2):118-24
pubmed: 20303067
J Neurosci. 2009 Feb 4;29(5):1538-43
pubmed: 19193900
Science. 2008 Apr 18;320(5874):385-8
pubmed: 18420937
Psychol Med. 2003 Apr;33(3):455-67
pubmed: 12701666
Nat Commun. 2020 May 11;11(1):2335
pubmed: 32393738
Biol Psychiatry. 2004 Jun 15;55(12):1171-8
pubmed: 15184036
Arch Gen Psychiatry. 2006 Nov;63(11):1217-23
pubmed: 17088502
Nat Commun. 2015 Aug 25;6:8096
pubmed: 26302782
Neuropsychopharmacology. 2008 Aug;33(9):2291-9
pubmed: 17940553
Mol Psychiatry. 2018 Aug;23(8):1731-1736
pubmed: 29155804
Elife. 2017 Feb 14;6:
pubmed: 28193320
Mol Psychiatry. 2012 Feb;17(2):121-3
pubmed: 21876544
Cognition. 2015 Jun;139:154-67
pubmed: 25824862
J Exp Psychol Gen. 2020 Sep;149(9):1755-1766
pubmed: 32039625
Science. 2004 Dec 10;306(5703):1940-3
pubmed: 15528409
Nature. 2007 Nov 1;450(7166):102-5
pubmed: 17960136
Neurosci Biobehav Rev. 2014 Oct;46 Pt 3:365-78
pubmed: 25195164
Biol Psychiatry. 2012 Aug 1;72(3):244-50
pubmed: 22325972
Front Behav Neurosci. 2015 Jul 24;9:153
pubmed: 26257616
Mol Psychiatry. 2011 Jul;16(7):695-713
pubmed: 21339754
Neuroimage. 2014 Mar;88:252-62
pubmed: 24121201
Trends Cogn Sci. 2016 Jan;20(1):15-24
pubmed: 26545853
Psychon Bull Rev. 2015 Oct;22(5):1320-7
pubmed: 25582684
J Neurosci. 2012 Jan 11;32(2):551-62
pubmed: 22238090
Neuron. 2012 Oct 4;76(1):240-56
pubmed: 23040818
Br J Psychiatry. 1995 Jul;167(1):99-103
pubmed: 7551619
PLoS Biol. 2017 Feb 16;15(2):e2000756
pubmed: 28207733
JAMA Psychiatry. 2016 Nov 1;73(11):1196-1197
pubmed: 27654061
Brain. 2009 Sep;132(Pt 9):2385-95
pubmed: 19416950
Am J Psychiatry. 2010 Nov;167(11):1305-20
pubmed: 20843874
Science. 2011 Dec 23;334(6063):1731-4
pubmed: 22194582
Neuroscience. 2013 Sep 5;247:253-72
pubmed: 23732229
Curr Biol. 2012 Aug 21;22(16):1477-81
pubmed: 22795698

Auteurs

Jochen Michely (J)

Department of Psychiatry and Neurosciences, Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany. jochen.michely@charite.de.
Berlin Institute of Health at Charité - Universitätsmedizin Berlin, BIH Charité Clinician Scientist Program, Berlin, Germany. jochen.michely@charite.de.
Max Planck UCL Centre for Computational Psychiatry and Ageing Research, University College London, London, UK. jochen.michely@charite.de.
Wellcome Centre for Human Neuroimaging, University College London, London, UK. jochen.michely@charite.de.

Eran Eldar (E)

Psychology and Cognitive Sciences Departments, Hebrew University of Jerusalem, Jerusalem, Israel.

Alon Erdman (A)

Psychology and Cognitive Sciences Departments, Hebrew University of Jerusalem, Jerusalem, Israel.

Ingrid M Martin (IM)

Wellcome Centre for Human Neuroimaging, University College London, London, UK.
Institute of Cognitive Neuroscience, University College London, London, UK.

Raymond J Dolan (RJ)

Max Planck UCL Centre for Computational Psychiatry and Ageing Research, University College London, London, UK.
Wellcome Centre for Human Neuroimaging, University College London, London, UK.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

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

Classifications MeSH