Proximal threats promote enhanced acquisition and persistence of reactive fear-learning circuits

Physical proximity to a traumatic event increases the severity of accompanying stress symptoms, an effect that is reminiscent of evolutionarily configured fear responses based on threat imminence. Despite being widely adopted as a model system for stress and anxiety disorders, fear-conditioning rese...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2020-07, Vol.117 (28), p.16678-16689
Main Authors: Faul, Leonard, Stjepanoviać, Daniel, Stivers, Joshua M., Stewart, Gregory W., Graner, John L., Morey, Rajendra A., LaBar, Kevin S.
Format: Article
Language:English
Subjects:
Adult
Amygdala
Anxiety disorders
Biological Sciences
Brain
Brain - diagnostic imaging
Brain - physiology
Brain mapping
Cerebellum
Circuits
Cognitive ability
Computer applications
Conditioning
Conditioning, Classical
Extinction behavior
Fear
Fear conditioning
Female
Functional magnetic resonance imaging
Humans
Learning
Magnetic permeability
Magnetic Resonance Imaging
Male
Neural networks
Neuroimaging
Pattern analysis
Proximity
Reinstatement
Signs and symptoms
Virtual reality
Young Adult
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Summary:Physical proximity to a traumatic event increases the severity of accompanying stress symptoms, an effect that is reminiscent of evolutionarily configured fear responses based on threat imminence. Despite being widely adopted as a model system for stress and anxiety disorders, fear-conditioning research has not yet characterized how threat proximity impacts the mechanisms of fear acquisition and extinction in the human brain. We used threedimensional (3D) virtual reality technology to manipulate the egocentric distance of conspecific threats while healthy adult participants navigated virtual worlds during functional magnetic resonance imaging (fMRI). Consistent with theoretical predictions, proximal threats enhanced fear acquisition by shifting conditioned learning from cognitive to reactive fear circuits in the brain and reducing amygdala–cortical connectivity during both fear acquisition and extinction. With an analysis of representational pattern similarity between the acquisition and extinction phases, we further demonstrate that proximal threats impaired extinction efficacy via persistent multivariate representations of conditioned learning in the cerebellum, which predicted susceptibility to later fear reinstatement. These results show that conditioned threats encountered in close proximity are more resistant to extinction learning and suggest that the canonical neural circuitry typically associated with fear learning requires additional consideration of a more reactive neural fear system to fully account for this effect.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.2004258117