Instructed knowledge shapes feedback-driven aversive learning in striatum and orbitofrontal cortex, but not the amygdala

Socially-conveyed rules and instructions strongly shape expectations and emotions. Yet most neuroscientific studies of learning consider reinforcement history alone, irrespective of knowledge acquired through other means. We examined fear conditioning and reversal in humans to test whether instructe...

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Main Authors: Lauren Y Atlas, Bradley B Doll, Jian Li, Nathaniel D Daw, Elizabeth A Phelps
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2016-05-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/15192
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author Lauren Y Atlas
Bradley B Doll
Jian Li
Nathaniel D Daw
Elizabeth A Phelps
author_facet Lauren Y Atlas
Bradley B Doll
Jian Li
Nathaniel D Daw
Elizabeth A Phelps
author_sort Lauren Y Atlas
collection DOAJ
description Socially-conveyed rules and instructions strongly shape expectations and emotions. Yet most neuroscientific studies of learning consider reinforcement history alone, irrespective of knowledge acquired through other means. We examined fear conditioning and reversal in humans to test whether instructed knowledge modulates the neural mechanisms of feedback-driven learning. One group was informed about contingencies and reversals. A second group learned only from reinforcement. We combined quantitative models with functional magnetic resonance imaging and found that instructions induced dissociations in the neural systems of aversive learning. Responses in striatum and orbitofrontal cortex updated with instructions and correlated with prefrontal responses to instructions. Amygdala responses were influenced by reinforcement similarly in both groups and did not update with instructions. Results extend work on instructed reward learning and reveal novel dissociations that have not been observed with punishments or rewards. Findings support theories of specialized threat-detection and may have implications for fear maintenance in anxiety.
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spelling doaj.art-482e43a6eebd4d5db90caa7621dd8fea2023-09-04T09:14:53ZengeLife Sciences Publications LtdeLife2050-084X2016-05-01510.7554/eLife.15192Instructed knowledge shapes feedback-driven aversive learning in striatum and orbitofrontal cortex, but not the amygdalaLauren Y Atlas0https://orcid.org/0000-0001-5693-4169Bradley B Doll1Jian Li2Nathaniel D Daw3https://orcid.org/0000-0001-5029-1430Elizabeth A Phelps4National Center for Complementary and Integrative Health, National Institutes of Health, Bethesda, United States; National Institute on Drug Abuse, National Institutes of Health, Bayview, United StatesCenter for Neural Sciences, New York University, New York, United States; Department of Psychology, Columbia University, New York, United StatesDepartment of Psychology, Beijing Key Laboratory of Behavior and Mental Health, Peking University, Beijing, China; PKU-IDG/McGovern Institute for Brain Research, Peking University, Beijing, ChinaDepartment of Psychology, Princeton Neuroscience Institute, Princeton University, Princeton, United StatesCenter for Neural Sciences, New York University, New York, United States; Department of Psychology, New York University, New York, United States; Nathan Kline Institute, Orangeburg, United StatesSocially-conveyed rules and instructions strongly shape expectations and emotions. Yet most neuroscientific studies of learning consider reinforcement history alone, irrespective of knowledge acquired through other means. We examined fear conditioning and reversal in humans to test whether instructed knowledge modulates the neural mechanisms of feedback-driven learning. One group was informed about contingencies and reversals. A second group learned only from reinforcement. We combined quantitative models with functional magnetic resonance imaging and found that instructions induced dissociations in the neural systems of aversive learning. Responses in striatum and orbitofrontal cortex updated with instructions and correlated with prefrontal responses to instructions. Amygdala responses were influenced by reinforcement similarly in both groups and did not update with instructions. Results extend work on instructed reward learning and reveal novel dissociations that have not been observed with punishments or rewards. Findings support theories of specialized threat-detection and may have implications for fear maintenance in anxiety.https://elifesciences.org/articles/15192fear conditioningamygdalalearningFMRIorbitofrontalreversal
spellingShingle Lauren Y Atlas
Bradley B Doll
Jian Li
Nathaniel D Daw
Elizabeth A Phelps
Instructed knowledge shapes feedback-driven aversive learning in striatum and orbitofrontal cortex, but not the amygdala
eLife
fear conditioning
amygdala
learning
FMRI
orbitofrontal
reversal
title Instructed knowledge shapes feedback-driven aversive learning in striatum and orbitofrontal cortex, but not the amygdala
title_full Instructed knowledge shapes feedback-driven aversive learning in striatum and orbitofrontal cortex, but not the amygdala
title_fullStr Instructed knowledge shapes feedback-driven aversive learning in striatum and orbitofrontal cortex, but not the amygdala
title_full_unstemmed Instructed knowledge shapes feedback-driven aversive learning in striatum and orbitofrontal cortex, but not the amygdala
title_short Instructed knowledge shapes feedback-driven aversive learning in striatum and orbitofrontal cortex, but not the amygdala
title_sort instructed knowledge shapes feedback driven aversive learning in striatum and orbitofrontal cortex but not the amygdala
topic fear conditioning
amygdala
learning
FMRI
orbitofrontal
reversal
url https://elifesciences.org/articles/15192
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