Neural mechanisms of credit assignment for delayed outcomes during contingent learning
Adaptive behavior in complex environments critically relies on the ability to appropriately link specific choices or actions to their outcomes. However, the neural mechanisms that support the ability to credit only those past choices believed to have caused the observed outcomes remain unclear. Here...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2025-04-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/101841 |
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| author | Phillip P Witkowski Lindsay JH Rondot Zeb Kurth-Nelson Mona M Garvert Raymond J Dolan Timothy EJ Behrens Erie Boorman |
| author_facet | Phillip P Witkowski Lindsay JH Rondot Zeb Kurth-Nelson Mona M Garvert Raymond J Dolan Timothy EJ Behrens Erie Boorman |
| author_sort | Phillip P Witkowski |
| collection | DOAJ |
| description | Adaptive behavior in complex environments critically relies on the ability to appropriately link specific choices or actions to their outcomes. However, the neural mechanisms that support the ability to credit only those past choices believed to have caused the observed outcomes remain unclear. Here, we leverage multivariate pattern analyses of functional magnetic resonance imaging (fMRI) data and an adaptive learning task to shed light on the underlying neural mechanisms of such specific credit assignment. We find that the lateral orbitofrontal cortex (lOFC) and hippocampus (HC) code for the causal choice identity when credit needs to be assigned for choices that are separated from outcomes by a long delay, even when this delayed transition is punctuated by interim decisions. Further, we show when interim decisions must be made, learning is additionally supported by lateral frontopolar cortex (lFPC). Our results indicate that lFPC holds previous causal choices in a ‘pending’ state until a relevant outcome is observed, and the fidelity of these representations predicts the fidelity of subsequent causal choice representations in lOFC and HC during credit assignment. Together, these results highlight the importance of the timely reinstatement of specific causes in lOFC and HC in learning choice-outcome relationships when delays and choices intervene, a critical component of real-world learning and decision making. |
| format | Article |
| id | doaj-art-a2edec5920ec407aac3e4ae9f818273d |
| institution | OA Journals |
| issn | 2050-084X |
| language | English |
| publishDate | 2025-04-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj-art-a2edec5920ec407aac3e4ae9f818273d2025-08-20T02:16:13ZengeLife Sciences Publications LtdeLife2050-084X2025-04-011310.7554/eLife.101841Neural mechanisms of credit assignment for delayed outcomes during contingent learningPhillip P Witkowski0https://orcid.org/0000-0001-7377-1592Lindsay JH Rondot1https://orcid.org/0009-0007-6692-3237Zeb Kurth-Nelson2Mona M Garvert3Raymond J Dolan4https://orcid.org/0000-0001-9356-761XTimothy EJ Behrens5https://orcid.org/0000-0003-0048-1177Erie Boorman6https://orcid.org/0000-0002-8438-4499Center for Mind and Brain, University of California Davis, Davis, United States; Department of Psychology, University of California Davis, Davis, United States; National Institute on Drug Abuse Intramural Research Program, National Institutes of Health, Baltimore, United StatesCenter for Mind and Brain, University of California Davis, Davis, United States; Department of Psychology, University of California Davis, Davis, United StatesMax Planck University College London Centre for Computational Psychiatry and Ageing Research, University College London, London, United KingdomFaculty of Human Sciences, Julius-Maximilians-Universität Würzburg, Würzburg, GermanyMax Planck University College London Centre for Computational Psychiatry and Ageing Research, University College London, London, United Kingdom; Wellcome Centre for Human Neuroimaging, University College London, London, United KingdomWellcome Centre for Human Neuroimaging, University College London, London, United Kingdom; Wellcome Centre for Integrative Neuroimaging, University of Oxford, John Radcliffe Hospital, Oxford, United Kingdom; Sainsbury Wellcome Centre for Neural Circuits and Behaviour, University College London, London, United KingdomCenter for Mind and Brain, University of California Davis, Davis, United States; Department of Psychology, University of California Davis, Davis, United StatesAdaptive behavior in complex environments critically relies on the ability to appropriately link specific choices or actions to their outcomes. However, the neural mechanisms that support the ability to credit only those past choices believed to have caused the observed outcomes remain unclear. Here, we leverage multivariate pattern analyses of functional magnetic resonance imaging (fMRI) data and an adaptive learning task to shed light on the underlying neural mechanisms of such specific credit assignment. We find that the lateral orbitofrontal cortex (lOFC) and hippocampus (HC) code for the causal choice identity when credit needs to be assigned for choices that are separated from outcomes by a long delay, even when this delayed transition is punctuated by interim decisions. Further, we show when interim decisions must be made, learning is additionally supported by lateral frontopolar cortex (lFPC). Our results indicate that lFPC holds previous causal choices in a ‘pending’ state until a relevant outcome is observed, and the fidelity of these representations predicts the fidelity of subsequent causal choice representations in lOFC and HC during credit assignment. Together, these results highlight the importance of the timely reinstatement of specific causes in lOFC and HC in learning choice-outcome relationships when delays and choices intervene, a critical component of real-world learning and decision making.https://elifesciences.org/articles/101841credit assignmentorbitofrontal cortexfrontal-polehippocampusLearning |
| spellingShingle | Phillip P Witkowski Lindsay JH Rondot Zeb Kurth-Nelson Mona M Garvert Raymond J Dolan Timothy EJ Behrens Erie Boorman Neural mechanisms of credit assignment for delayed outcomes during contingent learning eLife credit assignment orbitofrontal cortex frontal-pole hippocampus Learning |
| title | Neural mechanisms of credit assignment for delayed outcomes during contingent learning |
| title_full | Neural mechanisms of credit assignment for delayed outcomes during contingent learning |
| title_fullStr | Neural mechanisms of credit assignment for delayed outcomes during contingent learning |
| title_full_unstemmed | Neural mechanisms of credit assignment for delayed outcomes during contingent learning |
| title_short | Neural mechanisms of credit assignment for delayed outcomes during contingent learning |
| title_sort | neural mechanisms of credit assignment for delayed outcomes during contingent learning |
| topic | credit assignment orbitofrontal cortex frontal-pole hippocampus Learning |
| url | https://elifesciences.org/articles/101841 |
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