Reward and avoidance learning in the context of aversive environments and possible implications for depressive symptoms.
Affective modulation
Avoidance learning
Computational psychiatry
Decision-making
Depression symptoms
Reinforcement learning
Reward learning
Journal
Psychopharmacology
ISSN: 1432-2072
Titre abrégé: Psychopharmacology (Berl)
Pays: Germany
ID NLM: 7608025
Informations de publication
Date de publication:
Aug 2019
Aug 2019
Historique:
received:
11
01
2019
accepted:
05
06
2019
pubmed:
30
6
2019
medline:
27
11
2019
entrez:
30
6
2019
Statut:
ppublish
Résumé
Aversive stimuli in the environment influence human actions. This includes valence-dependent influences on action selection, e.g., increased avoidance but decreased approach behavior. However, it is yet unclear how aversive stimuli interact with complex learning and decision-making in the reward and avoidance domain. Moreover, the underlying computational mechanisms of these decision-making biases are unknown. To elucidate these mechanisms, 54 healthy young male subjects performed a two-step sequential decision-making task, which allows to computationally model different aspects of learning, e.g., model-free, habitual, and model-based, goal-directed learning. We used a within-subject design, crossing task valence (reward vs. punishment learning) with emotional context (aversive vs. neutral background stimuli). We analyzed choice data, applied a computational model, and performed simulations. Whereas model-based learning was not affected, aversive stimuli interacted with model-free learning in a way that depended on task valence. Thus, aversive stimuli increased model-free avoidance learning but decreased model-free reward learning. The computational model confirmed this effect: the parameter lambda that indicates the influence of reward prediction errors on decision values was increased in the punishment condition but decreased in the reward condition when aversive stimuli were present. Further, by using the inferred computational parameters to simulate choice data, our effects were captured. Exploratory analyses revealed that the observed biases were associated with subclinical depressive symptoms. Our data show that aversive environmental stimuli affect complex learning and decision-making, which depends on task valence. Further, we provide a model of the underlying computations of this affective modulation. Finally, our finding of increased decision-making biases in subjects reporting subclinical depressive symptoms matches recent reports of amplified Pavlovian influences on action selection in depression and suggests a potential vulnerability factor for mood disorders. We discuss our findings in the light of the involvement of the neuromodulators serotonin and dopamine.
Sections du résumé
BACKGROUND
BACKGROUND
Aversive stimuli in the environment influence human actions. This includes valence-dependent influences on action selection, e.g., increased avoidance but decreased approach behavior. However, it is yet unclear how aversive stimuli interact with complex learning and decision-making in the reward and avoidance domain. Moreover, the underlying computational mechanisms of these decision-making biases are unknown.
METHODS
METHODS
To elucidate these mechanisms, 54 healthy young male subjects performed a two-step sequential decision-making task, which allows to computationally model different aspects of learning, e.g., model-free, habitual, and model-based, goal-directed learning. We used a within-subject design, crossing task valence (reward vs. punishment learning) with emotional context (aversive vs. neutral background stimuli). We analyzed choice data, applied a computational model, and performed simulations.
RESULTS
RESULTS
Whereas model-based learning was not affected, aversive stimuli interacted with model-free learning in a way that depended on task valence. Thus, aversive stimuli increased model-free avoidance learning but decreased model-free reward learning. The computational model confirmed this effect: the parameter lambda that indicates the influence of reward prediction errors on decision values was increased in the punishment condition but decreased in the reward condition when aversive stimuli were present. Further, by using the inferred computational parameters to simulate choice data, our effects were captured. Exploratory analyses revealed that the observed biases were associated with subclinical depressive symptoms.
CONCLUSION
CONCLUSIONS
Our data show that aversive environmental stimuli affect complex learning and decision-making, which depends on task valence. Further, we provide a model of the underlying computations of this affective modulation. Finally, our finding of increased decision-making biases in subjects reporting subclinical depressive symptoms matches recent reports of amplified Pavlovian influences on action selection in depression and suggests a potential vulnerability factor for mood disorders. We discuss our findings in the light of the involvement of the neuromodulators serotonin and dopamine.
Identifiants
pubmed: 31254091
doi: 10.1007/s00213-019-05299-9
pii: 10.1007/s00213-019-05299-9
pmc: PMC6695365
doi:
Types de publication
Clinical Trial
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2437-2449Références
Neuropsychopharmacology. 1999 Aug;21(2 Suppl):99S-105S
pubmed: 10432495
Neurosci Biobehav Rev. 2001 May;25(3):205-18
pubmed: 11378177
Cereb Cortex. 2001 Dec;11(12):1136-43
pubmed: 11709484
J Exp Psychol. 1957 Nov;54(5):345-52
pubmed: 13481281
Science. 2004 Dec 10;306(5703):1940-3
pubmed: 15528409
Pers Soc Psychol Bull. 2005 Jan;31(1):121-35
pubmed: 15574667
Nat Neurosci. 2005 Jan;8(1):20-1
pubmed: 15592465
Arch Gen Psychiatry. 2005 Feb;62(2):146-52
pubmed: 15699291
J Cogn Neurosci. 2005 Jan;17(1):51-72
pubmed: 15701239
Behav Brain Res. 2005 Apr 30;159(2):221-33
pubmed: 15817185
Proc Natl Acad Sci U S A. 2005 Aug 23;102(34):12224-9
pubmed: 16093315
Q J Exp Psychol (Hove). 2006 Jun;59(6):1003-20
pubmed: 16885140
Neuropsychopharmacology. 2007 Jan;32(1):206-15
pubmed: 16900105
Neural Netw. 2006 Oct;19(8):1153-60
pubmed: 16938432
Trends Cogn Sci. 2008 Jan;12(1):31-40
pubmed: 18069045
N Engl J Med. 2008 Jan 3;358(1):55-68
pubmed: 18172175
Cognition. 2009 Dec;113(3):293-313
pubmed: 19427635
Nat Neurosci. 2009 Aug;12(8):1062-8
pubmed: 19620978
J Neurosci. 2009 Sep 23;29(38):11993-9
pubmed: 19776285
Biol Psychiatry. 2010 Jul 15;68(2):118-24
pubmed: 20303067
J Cogn Neurosci. 2011 Jul;23(7):1587-96
pubmed: 20666595
Neuron. 2011 Mar 24;69(6):1204-15
pubmed: 21435563
J Neurosci. 2011 May 25;31(21):7867-75
pubmed: 21613500
Mol Psychiatry. 2012 Feb;17(2):121-3
pubmed: 21876544
Proc Natl Acad Sci U S A. 2012 May 8;109(19):7511-6
pubmed: 22529363
Neuropsychopharmacology. 2012 Sep;37(10):2244-52
pubmed: 22643930
Neuron. 2012 Aug 9;75(3):418-24
pubmed: 22884326
Front Neurosci. 2012 Oct 08;6:134
pubmed: 23060738
J Cogn Neurosci. 2013 Sep;25(9):1428-41
pubmed: 23691985
Int J Methods Psychiatr Res. 2013 Jun;22(2):83-99
pubmed: 23788523
Eur J Neurosci. 2013 Dec;38(12):3740-8
pubmed: 24118624
J Neurosci. 2013 Nov 27;33(48):18932-9
pubmed: 24285898
Proc Natl Acad Sci U S A. 2013 Dec 24;110(52):20941-6
pubmed: 24324166
Trends Cogn Sci. 2014 Apr;18(4):194-202
pubmed: 24581556
Cogn Affect Behav Neurosci. 2014 Jun;14(2):473-92
pubmed: 24647659
Psychopharmacology (Berl). 2015 Jan;232(2):437-51
pubmed: 25034118
Front Behav Neurosci. 2014 Jul 03;8:237
pubmed: 25071491
Neuropsychopharmacology. 2015 Jan;40(2):454-62
pubmed: 25074639
Front Hum Neurosci. 2014 Aug 04;8:587
pubmed: 25136310
Psychopharmacology (Berl). 2015 Apr;232(7):1303-12
pubmed: 25326051
Neuropsychobiology. 2014;70(2):111-21
pubmed: 25359491
Neuropsychobiology. 2014;70(2):122-31
pubmed: 25359492
Front Psychol. 2014 Dec 17;5:1450
pubmed: 25566131
Psychoneuroendocrinology. 2015 Mar;53:268-80
pubmed: 25662093
Int J Neuropsychopharmacol. 2015 Feb 05;18(10):pyv013
pubmed: 25663044
Annu Rev Neurosci. 2015 Jul 8;38:1-23
pubmed: 25705929
Cogn Affect Behav Neurosci. 2015 Sep;15(3):523-36
pubmed: 25801925
Addict Biol. 2016 May;21(3):719-31
pubmed: 25828702
Mol Psychiatry. 2016 May;21(5):624-9
pubmed: 25869808
Front Psychol. 2015 Nov 03;6:1667
pubmed: 26579048
Eur Neuropsychopharmacol. 2016 May;26(5):828-40
pubmed: 26774661
PLoS One. 2016 Mar 16;11(3):e0150165
pubmed: 26982326
Neuropsychiatr Dis Treat. 2016 Dec 22;13:25-33
pubmed: 28053534
Addict Biol. 2018 Jan;23(1):379-393
pubmed: 28111829
Philos Trans R Soc Lond B Biol Sci. 2017 Apr 19;372(1718):null
pubmed: 28242739
Front Behav Neurosci. 2017 Apr 12;11:63
pubmed: 28446868
J Neurosci. 2017 Oct 18;37(42):10215-10229
pubmed: 28924006
Front Behav Neurosci. 2017 Sep 25;11:179
pubmed: 28993726
Sci Rep. 2018 Aug 22;8(1):12582
pubmed: 30135491
Behav Res Ther. 2018 Dec;111:19-26
pubmed: 30273768
Neuroimage. 2019 Feb 1;186:113-125
pubmed: 30381245
Sci Rep. 2019 May 1;9(1):6770
pubmed: 31043685
Psychol Bull. 1988 May;103(3):345-66
pubmed: 3289072
Ergonomics. 1971 Nov;14(6):679-93
pubmed: 5149050
Acta Psychiatr Scand. 1983 Jun;67(6):361-70
pubmed: 6880820
Pharmacol Biochem Behav. 1996 May;54(1):129-41
pubmed: 8728550