Different time course of visuocortical signal changes to fear-conditioned faces with direct or averted gaze: a ssVEP study with single-trial analysis

Social organisms fundamentally rely on experience to successfully navigate in a social world by associating social stimuli with aversive versus safe qualities. Cognitive neuroscience research has shown that visual cues reliably paired with danger are processed more efficiently than neutral cues, and that such facilitated sensory processing extends to low levels of the visual system. The present study aimed at determining the extent to which visual cortical engagement elicited by a face stimulus with learned affective value is modulated by relatively subtle facial features such as gaze direction and emotional expression. To this end, electro-cortical processing of direct-gaze compared to averted-gaze faces serving as CS+ cues was investigated in a differential fear conditioning paradigm. Furthermore it was investigated whether gaze shift interacted with angry facial expressions to confer greater immunity to extinction of learned associations. Behavioral ratings and visually evoked steady-state potentials (ssVEP) were recorded in healthy human participants. As expected, direct-gaze CS+ compared to averted-gaze CS- cues elicited larger ssVEP amplitudes during conditioning, whereas this differentiation was not observed when averted-gaze faces were paired with the aversive US. Importantly, a more fine-grained analysis examining trial-by-trial changes in visual cortical activation across the learning phases revealed that this effect was not necessarily due to lack of learning per se, but mainly due to a delayed build-up of cortical amplification for the averted-gaze CS+ cues. This suggests that the temporal dynamics of cortical engagement with aversively conditioned faces vary as a function of the cue with gaze direction as an important modulator of the speed of the acquisition of the aversive response.