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

Publication ,  Journal Article
Faul, L; Stjepanović, D; Stivers, JM; Stewart, GW; Graner, JL; Morey, RA; LaBar, KS
Published in: Proc Natl Acad Sci U S A
July 14, 2020

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 three-dimensional (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.

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Published In

Proc Natl Acad Sci U S A

DOI

EISSN

1091-6490

Publication Date

July 14, 2020

Volume

117

Issue

28

Start / End Page

16678 / 16689

Location

United States

Related Subject Headings

  • Young Adult
  • Male
  • Magnetic Resonance Imaging
  • Humans
  • Female
  • Fear
  • Conditioning, Classical
  • Brain
  • Adult
 

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Faul, L., Stjepanović, D., Stivers, J. M., Stewart, G. W., Graner, J. L., Morey, R. A., & LaBar, K. S. (2020). Proximal threats promote enhanced acquisition and persistence of reactive fear-learning circuits. Proc Natl Acad Sci U S A, 117(28), 16678–16689. https://doi.org/10.1073/pnas.2004258117
Faul, Leonard, Daniel Stjepanović, Joshua M. Stivers, Gregory W. Stewart, John L. Graner, Rajendra A. Morey, and Kevin S. LaBar. “Proximal threats promote enhanced acquisition and persistence of reactive fear-learning circuits.Proc Natl Acad Sci U S A 117, no. 28 (July 14, 2020): 16678–89. https://doi.org/10.1073/pnas.2004258117.
Faul L, Stjepanović D, Stivers JM, Stewart GW, Graner JL, Morey RA, et al. Proximal threats promote enhanced acquisition and persistence of reactive fear-learning circuits. Proc Natl Acad Sci U S A. 2020 Jul 14;117(28):16678–89.
Faul, Leonard, et al. “Proximal threats promote enhanced acquisition and persistence of reactive fear-learning circuits.Proc Natl Acad Sci U S A, vol. 117, no. 28, July 2020, pp. 16678–89. Pubmed, doi:10.1073/pnas.2004258117.
Faul L, Stjepanović D, Stivers JM, Stewart GW, Graner JL, Morey RA, LaBar KS. Proximal threats promote enhanced acquisition and persistence of reactive fear-learning circuits. Proc Natl Acad Sci U S A. 2020 Jul 14;117(28):16678–16689.
Journal cover image

Published In

Proc Natl Acad Sci U S A

DOI

EISSN

1091-6490

Publication Date

July 14, 2020

Volume

117

Issue

28

Start / End Page

16678 / 16689

Location

United States

Related Subject Headings

  • Young Adult
  • Male
  • Magnetic Resonance Imaging
  • Humans
  • Female
  • Fear
  • Conditioning, Classical
  • Brain
  • Adult