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 (an approach signal) is incongruent with it. We have previously shown using fMRI that the amygdala is engaged more strongly by fear with averted gaze 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 performed two experiments: one replicating the exposure time by gaze direction interaction in fMRI (N = 23), and another where we confirmed greater early phase locking to averted-gaze fear (congruent threat signal) with MEG (N = 60) in a network of face processing regions, regardless of exposure duration. 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.

Impairment in recognition of emotional facial expressions in Alzheimer's disease is represented by EEG theta and alpha responses

“…Over 50 years ago, Gray Walter (1950) had already pointed out that there are many alpha rhythms that were not merely related to a single function. In a recent magnetoencephalography (MEG) study, Cushing et al (2018) found alpha band activity to be sensitive to negative valence, as alpha phase locking was stronger both in the initial reflexive processing of averted-gaze fear and in the late reflective processing of direct-gaze fear. The results of the present study indicated that an increase in alpha power during the perception of facial expressions was impaired in AD patients, especially in the right hemisphere.…”

Magnocellular and parvocellular pathway contributions to facial threat cue processing

“…(2011). Such interaction effects have also been demonstrated in fMRI studies examining amygdala responses to congruent and incongruent facial threat cues (Sato et al ., 2004; Hadjikhani et al ., 2008; N’Diaye et al ., 2009) and most recently in in a magnetoencephalography (MEG) study (Cushing et al ., 2018).…”

“…STS, OFC and amygdala comprise the major nodes of the proposed ‘social brain’ (Baron-Cohen et al ., 1999), and pSTS specifically has been shown to specialize in inferring intentionality from social cues (Nummenmaa and Calder, 2009; Rhodes et al ., 2012). Importantly, the amygdala has been the primary focus of previous investigations into facial fear and eye gaze (Adams et al ., 2003, 2012; Hadjikhani et al ., 2008; Van Der Zwaag et al ., 2012; Im et al ., 2017, 2018; Cushing et al ., 2018), and this set of brain regions was the focus of our recent MEG investigation into how exposure duration modulates the sensitivity and neurodynamics of congruent and incongruent facial threat cues (Cushing et al ., 2018).…”

The Effect of Object Type on Building Scene Imagery—an MEG Study

“…Images were spatially smoothed using a 12 mm Gaussian kernel and entered into second-level random-effects paired t -test to determine power differences between SD objects and SA objects across the whole brain. An uncorrected threshold of p < 0.001 with a cluster extent threshold of >100 voxels was applied to each contrast, in line with numerous other MEG studies (e.g., Lieberman and Cunningham, 2009 ; Hanslmayr et al, 2011 ; Kveraga et al, 2011 ; Kaplan et al, 2012 ; Cushing et al, 2018 ; Barry et al, 2019a ). This is held to provide a balance between protecting against false positives whilst enabling the detection of subtler signals.…”