Neurodynamics and connectivity during facial fear perception: The role of threat exposure and signal congruity

Fearful faces convey threat cues whose meaning is contextualized by eye gaze: While averted gaze is congruent with facial fear (both signal avoidance), direct gaze is incongruent with it, as direct gaze signals approach. We have previously shown using fMRI that the amygdala is engaged more strongly by fear with averted gaze, which has been found to be processed more efficiently, during brief exposures. However, the amygdala also responds more to fear with direct gaze during longer exposures. Here we examined previously unexplored brain oscillatory responses to characterize the neurodynamics and connectivity during brief (∼250 ms) and longer (∼883 ms) exposures of fearful faces with direct or averted eye gaze. We replicated the exposure time by gaze direction interaction in fMRI (N=23), and observed greater early phase locking to averted-gaze fear (congruent threat signal) with MEG (N=60) in a network of face processing regions, with both brief and longer exposures. Phase locking to direct-gaze fear (incongruent threat signal) then increased significantly for brief exposures at ∼350 ms, and at ∼700 ms for longer exposures. Our results characterize the stages of congruent and incongruent facial threat signal processing and show that stimulus exposure strongly affects the onset and duration of these stages.