Magnocellular and parvocellular pathway contributions to facial threat cue processing

Human faces evolved to signal emotions, with their meaning contextualized by eye gaze. For instance, a fearful expression paired with averted gaze clearly signals both presence of threat and its probable location. Conversely, direct gaze paired with facial fear leaves the source of the fear-evoking threat ambiguous. Given that visual perception occurs in parallel streams with different processing emphases, our goal was to test a recently developed hypothesis that clear and ambiguous threat cues would differentially engage the magnocellular (M) and parvocellular (P) pathways, respectively. We employed two-tone face images to characterize the neurodynamics evoked by stimuli that were biased toward M or P pathways. Human observers (N = 57) had to identify the expression of fearful or neutral faces with direct or averted gaze while their magnetoencephalogram was recorded. Phase locking between the amygdaloid complex, orbitofrontal cortex (OFC) and fusiform gyrus increased early (0–300 ms) for M-biased clear threat cues (averted-gaze fear) in the β-band (13–30 Hz) while P-biased ambiguous threat cues (direct-gaze fear) evoked increased θ (4–8 Hz) phase locking in connections with OFC of the right hemisphere. We show that M and P pathways are relatively more sensitive toward clear and ambiguous threat processing, respectively, and characterize the neurodynamics underlying emotional face processing in the M and P pathways.