Experiential, autonomic, and neural responses during threat anticipation vary as a function of threat intensity and neuroticism

Emily M. Drabant, Janice R. Kuo, Wiveka Ramel, Jens Blechert, Michael D. Edge, Jeff R. Cooper, Philip R Goldin, Ahmad R. Hariri, James J. Gross

Research output: Contribution to journalArticle

70 Scopus citations

Abstract

Anticipatory emotional responses play a crucial role in preparing individuals for impending challenges. They do this by triggering a coordinated set of changes in behavioral, autonomic, and neural response systems. In the present study, we examined the biobehavioral impact of varying levels of anticipatory anxiety, using a shock anticipation task in which unpredictable electric shocks were threatened and delivered to the wrist at variable intervals and intensities (safe, medium, strong). This permitted investigation of a dynamic range of anticipatory anxiety responses. In two studies, 95 and 51 healthy female participants, respectively, underwent this shock anticipation task while providing continuous ratings of anxiety experience and electrodermal responding (Study 1) and during fMRI BOLD neuroimaging (Study 2). Results indicated a step-wise pattern of responding in anxiety experience and electrodermal responses. Several brain regions showed robust responses to shock anticipation relative to safe trials, including the hypothalamus, periaqueductal gray, caudate, precentral gyrus, thalamus, insula, ventrolateral PFC, dorsomedial PFC, and ACC. A subset of these regions demonstrated a linear pattern of increased responding from safe to medium to strong trials, including the bilateral insula, ACC, and inferior frontal gyrus. These responses were modulated by individual differences in neuroticism, such that those high in neuroticism showed exaggerated anxiety experience across the entire task, and reduced brain activation from medium to strong trials in a subset of brain regions. These findings suggest that individual differences in neuroticism may influence sensitivity to anticipatory threat and provide new insights into the mechanism through which neuroticism may confer risk for developing anxiety disorders via dysregulated anticipatory responses.

Original languageEnglish (US)
Pages (from-to)401-410
Number of pages10
JournalNeuroImage
Volume55
Issue number1
DOIs
StatePublished - Mar 1 2011
Externally publishedYes

Keywords

  • Anterior cingulate
  • Anticipation
  • Anxiety
  • FMRI
  • Insula
  • Neuroticism
  • Unpredictability

ASJC Scopus subject areas

  • Cognitive Neuroscience
  • Neurology

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  • Cite this

    Drabant, E. M., Kuo, J. R., Ramel, W., Blechert, J., Edge, M. D., Cooper, J. R., Goldin, P. R., Hariri, A. R., & Gross, J. J. (2011). Experiential, autonomic, and neural responses during threat anticipation vary as a function of threat intensity and neuroticism. NeuroImage, 55(1), 401-410. https://doi.org/10.1016/j.neuroimage.2010.11.040