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

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Abstract

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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Lauren Y Atlas

National Center for Complementary and Integrative Health, National Institutes of Health, Bethesda, United States

For correspondence
lauren.atlas@nih.gov

Competing interests
The authors declare that no competing interests exist.
Bradley B Doll

Center for Neural Sciences, New York University, New York, United States

Competing interests
The authors declare that no competing interests exist.
Jian Li

Department of Psychology, Beijing Key Laboratory of Behavior and Mental Health, Peking University, Beijing, China

Competing interests
The authors declare that no competing interests exist.
Nathaniel D Daw

Department of Psychology, Princeton Neuroscience Institute, Princeton University, Princeton, United States

Competing interests
The authors declare that no competing interests exist.
Elizabeth A Phelps

Center for Neural Sciences, New York University, New York, United States

Competing interests
The authors declare that no competing interests exist.

Ethics

Human subjects: Informed consent was obtained from all subjects. Research was approved by New York University's Institutional Review Board.

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This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.