Observer’s anxiety facilitates magnocellular processing of clear facial threat cues, but impairs parvocellular processing of ambiguous facial threat cues

Abstract

Facial expression and eye gaze provide a shared signal about threats. While a fear expression with averted gaze clearly points to the source of threat, direct-gaze fear renders the source of threat ambiguous. Separable routes have been proposed to mediate these processes, with preferential attunement of the magnocellular (M) pathway to clear threat, and of the parvocellular (P) pathway to threat ambiguity. Here we investigated how observers’ trait anxiety modulates M- and P-pathway processing of clear and ambiguous threat cues. We scanned subjects (N = 108) widely ranging in trait anxiety while they viewed fearful or neutral faces with averted or directed gaze, with the luminance and color of face stimuli calibrated to selectively engage M- or P-pathways. Higher anxiety facilitated processing of clear threat projected to M-pathway, but impaired perception of ambiguous threat projected to P-pathway. Increased right amygdala reactivity was associated with higher anxiety for M-biased averted-gaze fear, while increased left amygdala reactivity was associated with higher anxiety for P-biased, direct-gaze fear. This lateralization was more pronounced with higher anxiety. Our findings suggest that trait anxiety differentially affects perception of clear (averted-gaze fear) and ambiguous (direct-gaze fear) facial threat cues via selective engagement of M and P pathways and lateralized amygdala reactivity.

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

“…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, ). Together, processing of clear vs. ambiguous threat cues from emotional expression and eye gaze of faces appears to differentially engage the M and P pathways, with differential hemispheric dominance in the right and the left amygdala.…”

“…For the right amygdala responses to neutral face stimuli (Figure d), however, none of the main effects or the interactions was significant ( p 's > .355). Therefore, the fMRI results suggest that male participants show greater right amygdala activation for M‐biased averted fear face stimuli (e.g., clear threat cue; Adams et al, ; Im et al, ) indicating greater attunement of the right amygdala to clear threat conveyed by the magnocellular pathway, whereas female participants show greater left amygdala involvement in processing of faces (both fearful and neutral), compared to male participants.…”

“…Previous studies (Cahill et al, ; Canli et al, ) have shown lateralization in amygdala responses, with males showing greater right amygdala activity, and larger left amygdala activation in females. Recent findings by us (Adams et al, ) suggested that right and left amygdala are engaged preferentially by clear and ambiguous threat, respectively, and that this lateralization is also driven additionally by whether the stimuli are presented to the magnocellular or parvocellular pathway (Im et al, ). Lastly, Hoffmann et al () reported that females outperform males mainly in recognizing subtle rather than more intense expressions.…”

“…Table reports all the significant clusters from the whole brain analysis using the formal threshold of p < .05, FWE whole‐brain corrected. For the left and right amygdalae, the regions of our main interest based on the previous studies (Adams et al, ; Adams et al, ; Im et al, ; Cushing et al, ), significant activation was reported after small volume correction at the threshold of p < .05, FWE‐corrected. The small volume correction was done by using the anatomically defined masks for the left and right amygdala that were automatically segmented and labeled by SPM Anatomy Toolbox (Eickhoff et al, ; Eickhoff, Heim, Zilles, & Amunts, ; Eickhoff et al, ).…”

“…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.…”