Dissociable neural systems for unconditioned acute and sustained fear

Matthew Hudson*, Kerttu Seppälä, Vesa Putkinen, Lihua Sun, Enrico Glerean, Tomi Karjalainen, Henry K. Karlsson, Jussi Hirvonen, Lauri Nummenmaa

*Corresponding author for this work

Research output: Contribution to journalArticleScientificpeer-review

Abstract

Fear protects organisms by increasing vigilance and preparedness, and by coordinating survival responses during life-threatening encounters. The fear circuit must thus operate on multiple timescales ranging from preparatory sustained alertness to acute fight-or-flight responses. Here we studied the brain basis of sustained and acute fear using naturalistic functional magnetic resonance imaging (fMRI) enabling analysis of different time-scales of fear responses. Subjects (N ​= ​37) watched feature-length horror movies while their hemodynamic brain activity was measured with fMRI. Time-variable intersubject correlation (ISC) was used to quantify the reliability of brain activity across participants, and seed-based phase synchronization was used for characterizing dynamic connectivity. Subjective ratings of fear were used to assess how synchronization and functional connectivity varied with emotional intensity. These data suggest that acute and sustained fear are supported by distinct neural pathways, with sustained fear amplifying mainly sensory responses, and acute fear increasing activity in brainstem, thalamus, amygdala and cingulate cortices. Sustained fear increased ISC in regions associated with acute fear, and also amplified functional connectivity within this network. The results were replicated in an independent experiment with a different subject sample and stimulus movie. The functional interplay between cortical networks involved in sustained anticipation of, and acute response to, threat involves a complex and dynamic interaction that depends on the proximity of threat, and the need to employ threat appraisals and vigilance for decision making and response selection.

Original languageEnglish
Article number116522
JournalNeuroImage
DOIs
Publication statusE-pub ahead of print - 1 Jan 2020
MoE publication typeA1 Journal article-refereed

Keywords

  • Fear
  • Horror movies
  • Naturalistic fMRI
  • Neural synchronization
  • Threat

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    Hudson, M., Seppälä, K., Putkinen, V., Sun, L., Glerean, E., Karjalainen, T., ... Nummenmaa, L. (2020). Dissociable neural systems for unconditioned acute and sustained fear. NeuroImage, [116522]. https://doi.org/10.1016/j.neuroimage.2020.116522