Journal
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Volume 117, Issue 28, Pages 16678-16689Publisher
NATL ACAD SCIENCES
DOI: 10.1073/pnas.2004258117
Keywords
proximity; fear conditioning; virtual reality; representational similarity analysis; cerebellum
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Funding
- National Science Foundation Graduate Research Fellowship Program
- National Science Foundation [BCS 1460909]
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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 immi-nence. Despite being widely adopted as a model system for stress and anxiety disorders, fear-conditioning research has not yet char-acterized how threat proximity impacts the mechanisms of fear acquisition and extinction in the human brain. We used three-dimensional (3D) virtual reality technology to manipulate the ego-centric distance of conspecific threats while healthy adult partici-pants 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 acquisi-tion and extinction. With an analysis of representational pattern similarity between the acquisition and extinction phases, we fur-ther demonstrate that proximal threats impaired extinction effi-cacy 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.
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