Magnocellular and parvocellular pathway contributions to facial threat cue processing

Abstract

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.

Keywords: connectivity; emotion perception; eye gaze; magnetoencephalography; magnocellular; parvocellular.

Fig. 1

Task design and behavioral performance. (A) Experimental trial design beginning with 200–400 ms of attending to a central red fixation followed by stimulus (examples below) presentation for 1 s. Participants were instructed to indicate via key press as quickly and accurately as they could whether the presented face appears fearful or neutral. Participants were then shown a green central fixation inversely timed to the pre-stimulus jitter, then presented feedback on whether their response was correct, incorrect or if they took too long to respond (maximum RT allowed was 1.5 s post-stimulus). Trials were always 2.5 s. (B) RTs of participants responding to M-biased (gray) vs P-biased (red) congruent (bright hues) and incongruent (dark hues) facial threat cues. Upper horizontal black bar indicates a significant interaction between pathway bias and facial threat cue congruency (F(1,56) = 16.98, p<0.001). Lower horizontal black bar indicates significant difference in RT for incongruent facial threat cues (t(56)=3.36, p=0.0014). Participants were faster to respond to M-biased congruent cues and P-biased incongruent cues, supporting our main hypothesis of congruent cues being preferentially processed by the M pathway and incongruent cues being preferentially processed by the P pathway.

Fig. 2

Phase-locking results. Time-frequency maps depicting results of planned non-parametric cluster-based t-test of M-biased (blue) vs P-biased (red) clear, congruent (averted-gaze fear, ‘top’) and ambiguous, incongruent (direct-gaze fear, ‘bottom’) facial threat cues. Significant and marginally significant clusters are marked with a letter and traced in white. Corresponding Monte-Carlo P-values for marked clusters based on 3000 permutations listed below each time-frequency plot. Note that frequency on the y-axis is plotted logarithmically. Greek letters on the right y-axis denote canonical frequency ranges demarcated by dashed black lines across time-frequency plots. Color bars to the right of each vertical pair of time-frequency plots denote statistic being plotted and pixel value color mapping.