Early Left Parietal Activity Elicited by Direct Gaze: A High-Density EEG Study

Abstract

Gaze is one of the most important cues for human communication and social interaction. In particular, gaze contact is the most primary form of social contact and it is thought to capture attention. A very early-differentiated brain response to direct versus averted gaze has been hypothesized. Here, we used high-density electroencephalography to test this hypothesis. Topographical analysis allowed us to uncover a very early topographic modulation (40–80 ms) of event-related responses to faces with direct as compared to averted gaze. This modulation was obtained only in the condition where intact broadband faces–as opposed to high-pass or low-pas filtered faces–were presented. Source estimation indicated that this early modulation involved the posterior parietal region, encompassing the left precuneus and inferior parietal lobule. This supports the idea that it reflected an early orienting response to direct versus averted gaze. Accordingly, in a follow-up behavioural experiment, we found faster response times to the direct gaze than to the averted gaze broadband faces. In addition, classical evoked potential analysis showed that the N170 peak amplitude was larger for averted gaze than for direct gaze. Taken together, these results suggest that direct gaze may be detected at a very early processing stage, involving a parallel route to the ventral occipito-temporal route of face perceptual analysis.

Early and late cortical responses to directly gazing faces are task dependent

“…In addition, as noted above, the parieto-occipital P1 has been posited to be sensitive to configural face processing (Halit et al, 2000;Wang et al, 2015). The modulation of the P100 amplitude found in the present study corroborates these reports, suggesting an early pictorial categorisation stage (Desjardins & Segalowitz, 2013), during which a coarse signal is processed, indicating the presence and direction of the eyes (Burra et al, 2016;Doi & Ueda, 2007), possibly based on the strong difference in local contrast between the sclera and the iris, as well as the inherent symmetry associated with gaze direction (Doi & Ueda, 2007;Kobayashi & Kohshima, 1997). Critically, the fact that the P1 effect is abolished in Experiment3 argues unequivocally against the possibility that it may be purely stimulus driven.…”

“…Contrasting with the unequivocal P1 and P3b results, no significant difference emerged between direct and averted gaze at the N170 level. This result is convergent with the literature, which has so far not been able to demonstrate any consistent N170 effect for gaze direction (for instance, Burra et al, 2017;Burra et al, 2016;Conty et al, 2007;Itier, Alain, Kovacevic, et al, 2007a;Latinus et al, 2015;Sato et al, 2008;Taylor, George, et al, 2001b;Watanabe et al, 2002).…”

“…Data revealed that the preference for direct gaze was initiated in the P1 time range and reiterated at P3b, but was absent at the N170 level. These modulations echo the behavioural effect of Macrae et al (2002), replicated in Experiment 1, and further suggest that direct gaze enhances visual encoding at an early stage of visual processing, likely reflecting preferential orienting toward this stimulus (see Burra et al, 2016), which potentially produces an attentional enhancement of the P1. Additionally, at a later stage, we found a similar effect at the P3b levels, as reported in previous studies (Conty et al, 2007;Doi & Shinohara, 2012;Itier, Alain, Kovacevic, et al, 2007a;Naples et al, 2017).…”

“…Such early modulations may be driven mainly by eye detection, which plays a crucial role in the coarse detection of faces (Doi & Ueda, 2007;Fichtenholtz, Hopfinger, Graham, Detwiler, & LaBar, 2009;Itier, Alain, Kovacevic, et al, 2007a;Itier, Villate, & Ryan, 2007c;Kloth, Schweinberger, & Kovacs, 2010). Indeed, it seems plausible that gaze direction may be coded at the P1 level (Akechi et al, 2010;Schmitz, Scheel, Rigon, Gross, & Blechert, 2012), and possibly at an even earlier stage (Burra, Kerzel, & George, 2016). However, although there are indications that the P1 could be associated with an early stage of eye/gaze processing, this effect could also reflect low-level differences and/or attentional enhancements (Rossion & Jacques, 2008).…”

Revealing the neural time-course of direct gaze processing via spatial frequency manipulation of faces

“…On the other hand, it is not clear how the critical spatial frequency bandwidths for gaze processing change throughout development, with HSF information being critical for the explicit discrimination between leftwards and rightwards gaze directions in adults (Vida & Maurer, 2015). Furthermore, early neural differentiation between direct and averted gaze has only been observed for broad spatial frequency, while no effects of gaze direction were found for stimulus displayed only with high or low spatial frequency information (Burra, Kerzel, & George, 2016).…”