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

Abstract

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.

Sex‐related differences in behavioral and amygdalar responses to compound facial threat cues

“…Thus, greater right amygdala reactivity to M‐biased averted‐gaze fear faces in male participants suggests that processing of facial expression by eye gaze interactions in male observers is tuned more to detection of a clear, congruent threat cue from face stimuli, compared to female observers. Conversely, female observers showed more involvement of the left amygdala, which has been suggested to play a role in more detailed analysis and reflective processing (Adams et al, ; Cushing et al, ; Im et al, ). Together, our findings suggest that brain activations elicited by interactions of facial expression and eye gaze direction are modulated by the observer's sex.…”

“…Male participants showed greater right amygdala responses, but only to M‐biased averted‐gaze fear faces (congruent, clear threat cues) whereas the female participants showed greater left amygdala responses to both fearful and neutral faces. Prior work suggests that a fearful face with averted eye gaze tends to be perceived as a clear threat (“pointing with the eyes” to the threat; Hadjikhani et al, ) because both emotional expression and eye gaze direction signal congruent avoidance motivation (Adams et al, ; Cushing et al, ; Im et al, ). Moreover, we previously showed that the right amygdala is highly responsive to such a clear threat cue (averted‐gaze fear; e.g., Adams et al, ; Cushing et al, ), especially when presented to the magnocellular pathway (Im et al, ).…”

“…We previously had observed greater right amygdala activation for M‐biased objects stimuli than for P‐biased objects stimuli (Kveraga, Boshyan, & Bar, ). Using fearful face stimuli with direct or averted eye gaze, we had also observed that stimuli depicting clear threat (averted‐gaze fear) tended to activate the right amygdala more, particularly with brief stimulus exposure, whereas ambiguous threat stimuli (direct‐gaze fear) activated the left amygdala more, particularly with longer stimulus exposures (Adams et al, ; Cushing et al, ). These findings were also replicated and extended in a recent study in which we showed that higher observer anxiety was associated with increased right amygdala activity with facilitated processing of M‐biased clear‐threat stimuli, whereas higher anxiety was associated with increased left amygdala activity with impaired processing of P‐biased ambiguous threat stimuli (Im et al, ).…”

“…An emerging hypothesis posits that reflexive processing of clear threat cues may be predominantly associated with the more primitive, coarse, and action‐oriented M pathway, while reflective, sustained processing of threat ambiguity may preferentially engage the slower, analysis‐oriented P pathway (Adams et al, ; Adams & Kveraga, ; Kveraga, 2014). Indeed, recent fMRI studies compared M versus P pathway involvement in threat perception and supported this hypothesis by showing that congruent threat and incongruent threat signals in both face (Cushing et al, ; Im et al, ) and scene images (Kveraga, ) were processed preferentially by the M and P visual pathways, respectively. Moreover, Im et al () showed that observers’ trait anxiety levels differentially modulated M and P processing of clear and ambiguous facial threat cues such that higher anxiety facilitated processing of averted‐gaze fear projected to M pathway, whereas higher anxiety impaired perception of direct‐gaze fear projected to P pathway.…”

“…Prior work has investigated how observers read such signals from a facial expression combined with direct or averted eye gaze, which imparts different meanings. For example, a fearful face tends to be perceived as more fearful when presented with an averted eye gaze because the combination of fearful facial expression and averted gaze provides a congruent social signal (both the expression and the gaze direction signal avoidance), leading to facilitated processing of the congruent signals (e.g., Adams et al, ; Adams & Kleck, ; Cushing et al, ; Hadjikhani, Hoge, Snyder, & de Gelder, ; Im et al, ). Furthermore, in a fearful face this “pointing with the eyes” (Hadjikhani et al, ) to the source of threat disambiguates whence the threat is coming.…”