Ambiguity drives higher-order Pavlovian learning.


Journal

PLoS computational biology
ISSN: 1553-7358
Titre abrégé: PLoS Comput Biol
Pays: United States
ID NLM: 101238922

Informations de publication

Date de publication:
09 2022
Historique:
received: 10 09 2021
accepted: 19 07 2022
revised: 21 09 2022
pubmed: 10 9 2022
medline: 24 9 2022
entrez: 9 9 2022
Statut: epublish

Résumé

In the natural world, stimulus-outcome associations are often ambiguous, and most associations are highly complex and situation-dependent. Learning to disambiguate these complex associations to identify which specific outcomes will occur in which situations is critical for survival. Pavlovian occasion setters are stimuli that determine whether other stimuli will result in a specific outcome. Occasion setting is a well-established phenomenon, but very little investigation has been conducted on how occasion setters are disambiguated when they themselves are ambiguous (i.e., when they do not consistently signal whether another stimulus will be reinforced). In two preregistered studies, we investigated the role of higher-order Pavlovian occasion setting in humans. We developed and tested the first computational model predicting direct associative learning, traditional occasion setting (i.e., 1st-order occasion setting), and 2nd-order occasion setting. This model operationalizes stimulus ambiguity as a mechanism to engage in higher-order Pavlovian learning. Both behavioral and computational modeling results suggest that 2nd-order occasion setting was learned, as evidenced by lack and presence of transfer of occasion setting properties when expected and the superior fit of our 2nd-order occasion setting model compared to the 1st-order occasion setting or direct associations models. These results provide a controlled investigation into highly complex associative learning and may ultimately lead to improvements in the treatment of Pavlovian-based mental health disorders (e.g., anxiety disorders, substance use).

Identifiants

pubmed: 36084131
doi: 10.1371/journal.pcbi.1010410
pii: PCOMPBIOL-D-21-01660
pmc: PMC9491594
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1010410

Subventions

Organisme : Wellcome Trust
ID : 206460/Z/17/Z
Pays : United Kingdom

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

Neurobiol Learn Mem. 2016 May;131:201-6
pubmed: 27112314
J Neurosci. 2013 Oct 2;33(40):15989-98
pubmed: 24089503
J Exp Psychol Anim Behav Process. 1991 Jul;17(3):231-48
pubmed: 1890383
Neurobiol Learn Mem. 2011 Feb;95(2):176-84
pubmed: 20643219
Psychon Bull Rev. 2017 Apr;24(2):557-565
pubmed: 27418259
Depress Anxiety. 2015 Apr;32(4):239-53
pubmed: 25703487
Biol Psychiatry. 2007 Sep 1;62(5):446-54
pubmed: 17217927
Nature. 2015 Jan 15;517(7534):284-92
pubmed: 25592533
J Abnorm Psychol. 2012 May;121(2):315-24
pubmed: 21988452
Neuron. 2014 Jan 22;81(2):267-279
pubmed: 24462094
J Exp Psychol Anim Behav Process. 2002 Jan;28(1):83-96
pubmed: 11868237
Biol Psychiatry. 2008 Aug 1;64(3):203-10
pubmed: 18423574
Neuron. 2014 Dec 17;84(6):1143-56
pubmed: 25521376
Behav Neurosci. 2019 Apr;133(2):145-175
pubmed: 30907616
J Exp Psychol Anim Behav Process. 1994 Jan;20(1):51-65
pubmed: 8308493
Psychol Bull. 1993 Jul;114(1):80-99
pubmed: 8346330
Neurobiol Learn Mem. 2001 Mar;75(2):121-7
pubmed: 11222054
Behav Processes. 2017 Apr;137:5-18
pubmed: 27425659
J Anxiety Disord. 2012 Apr;26(3):468-79
pubmed: 22366534
Emotion. 2006 Feb;6(1):40-61
pubmed: 16637749
Behav Processes. 2012 Jul;90(3):311-22
pubmed: 22459561
J Neurosci. 2012 Apr 18;32(16):5356-61
pubmed: 22514300
Science. 2011 Dec 9;334(6061):1415-20
pubmed: 22052975
Anat Embryol (Berl). 2005 Dec;210(5-6):343-52
pubmed: 16208455
Eur J Neurosci. 2013 Sep;38(5):2751-61
pubmed: 23758059
Behav Res Ther. 2005 Nov;43(11):1391-424
pubmed: 15885654
Science. 2014 Feb 21;343(6173):896-901
pubmed: 24457215
J Exp Psychol Anim Behav Process. 1984 Oct;10(4):461-75
pubmed: 6491607
J Comp Neurol. 2011 Dec 15;519(18):3766-801
pubmed: 21800317
Hippocampus. 1991 Jan;1(1):107-17
pubmed: 1669340
Neuropsychopharmacology. 2005 Feb;30(2):296-309
pubmed: 15483559
Psychopharmacology (Berl). 2002 Apr;160(4):425-33
pubmed: 11919670
Front Neural Circuits. 2017 Oct 31;11:86
pubmed: 29163066
Front Behav Neurosci. 2014 May 06;8:129
pubmed: 24834031
Behav Processes. 2017 Apr;137:64-72
pubmed: 27720958
Biol Psychiatry. 2002 Nov 15;52(10):976-86
pubmed: 12437938
Q J Exp Psychol B. 1990 Feb;42(1):41-58
pubmed: 2326493
J Exp Psychol Anim Behav Process. 1995 Oct;21(4):275-84
pubmed: 7595235
J Exp Psychol Anim Behav Process. 1989 Oct;15(4):311-28
pubmed: 2794868
J Exp Psychol Anim Behav Process. 2010 Jan;36(1):126-36
pubmed: 20141323
Learn Behav. 2012 Sep;40(3):255-68
pubmed: 22927000
Behav Processes. 2017 Apr;137:73-83
pubmed: 28108345
J Neurosci. 2019 Apr 24;39(17):3264-3276
pubmed: 30782974
PLoS One. 2013 Dec 19;8(12):e84543
pubmed: 24367674
Neuron. 2004 Sep 16;43(6):897-905
pubmed: 15363399
J Neurosci. 2009 Jun 24;29(25):8087-93
pubmed: 19553448
Behav Neurosci. 1984 Apr;98(2):211-25
pubmed: 6721923
J Comp Neurol. 2003 Jun 2;460(3):425-49
pubmed: 12692859
Neurosci Biobehav Rev. 2015 Oct;57:271-83
pubmed: 26341938
Hippocampus. 1999;9(2):143-57
pubmed: 10226775
Learn Mem. 2015 Aug 18;22(9):438-43
pubmed: 26286654
J Comp Neurol. 1995 Dec 25;363(4):615-641
pubmed: 8847421
J Neurosci. 2017 Sep 27;37(39):9415-9423
pubmed: 28847808
Behav Processes. 2017 Apr;137:19-32
pubmed: 27346424
Nature. 2002 Nov 7;420(6911):70-4
pubmed: 12422216
Neuropsychopharmacology. 2011 Feb;36(3):711-20
pubmed: 21124303
Clin Neurophysiol. 2005 Aug;116(8):1779-84
pubmed: 16002335
Q J Exp Psychol (Hove). 2006 Jan;59(1):53-67
pubmed: 16556558
Behav Res Ther. 2014 Jul;58:10-23
pubmed: 24864005
Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):11771-6
pubmed: 7991534
J Neurosci. 2003 Sep 10;23(23):8410-6
pubmed: 12968003
Ann N Y Acad Sci. 2011 Dec;1239:43-50
pubmed: 22145874
Behav Res Ther. 2021 Dec;147:103986
pubmed: 34740100
Ann N Y Acad Sci. 2000 Jun;911:369-91
pubmed: 10911886
Behav Processes. 2018 Sep;154:52-59
pubmed: 29444454
Nat Rev Neurosci. 2002 Jul;3(7):563-73
pubmed: 12094212
Learn Mem. 2013 Jan 15;20(2):80-4
pubmed: 23322556
J Comp Neurol. 2014 Mar;522(4):772-93
pubmed: 23897637
PLoS Comput Biol. 2019 Oct 10;15(10):e1007341
pubmed: 31600187
J Exp Psychol Anim Behav Process. 2001 Jul;27(3):279-95
pubmed: 11497326
Cogn Behav Ther. 2016 Nov;45(6):431-44
pubmed: 27314213
Front Syst Neurosci. 2017 Jun 28;11:46
pubmed: 28701931
Neuropsychopharmacology. 2020 Feb;45(3):534-541
pubmed: 31352467

Auteurs

Tomislav D Zbozinek (TD)

California Institute of Technology, Humanities and Social Sciences, Pasadena, California, United States of America.

Omar D Perez (OD)

California Institute of Technology, Humanities and Social Sciences, Pasadena, California, United States of America.
University of Santiago, CESS-Santiago, Faculty of Business and Economics, Santiago, Chile.
University of Chile, Department of Industrial Engineering, Santiago, Chile.

Toby Wise (T)

California Institute of Technology, Humanities and Social Sciences, Pasadena, California, United States of America.

Michael Fanselow (M)

University of California, Los Angeles, Department of Psychology, Los Angeles, California, United States of America.
University of California, Los Angeles, Department of Psychiatry & Biobehavioral Sciences, Los Angeles, California, United States of America.
University of California, Los Angeles, Staglin Center for Brain and Behavioral Health, Los Angeles, California, United States of America.
University of California, Los Angeles, Brain Research Institute, Los Angeles, California, United States of America.

Dean Mobbs (D)

California Institute of Technology, Humanities and Social Sciences, Pasadena, California, United States of America.
California Institute of Technology, Computation and Neural Systems Program, Pasadena, California, United States of America.

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