Abstract

The perception of eye-gaze is thought to be a key component of our everyday social interactions. While the neural correlates of direct and averted gaze processing have been investigated, there is little consensus about how these gaze directions may be processed differently as a function of the task being performed. In a within-subject design, we examined how perception of direct and averted gaze affected performance on tasks requiring participants to use directly available facial cues to infer the individuals’ emotional state (emotion discrimination), direction of attention (attention discrimination) and gender (gender discrimination). Neural activity was recorded throughout the three tasks using EEG, and ERPs time-locked to face onset were analyzed. Participants were most accurate at discriminating emotions with direct gaze faces, but most accurate at discriminating attention with averted gaze faces, while gender discrimination was not affected by gaze direction. At the neural level, direct and averted gaze elicited different patterns of activation depending on the task over frontal sites, from approximately 220–290 ms. More positive amplitudes were seen for direct than averted gaze in the emotion discrimination task. In contrast, more positive amplitudes were seen for averted gaze than for direct gaze in the gender discrimination task. These findings are among the first direct evidence that perceived gaze direction modulates neural activity differently depending on task demands, and that at the behavioral level, specific gaze directions functionally overlap with emotion and attention discrimination, precursors to more elaborated theory of mind processes.

Highlights

  • Eye-gaze has long been considered one of the most important cues during social interactions and seems central to social cognition (Kleinke, 1986; Emery, 2000; George and Conty, 2008; Itier and Batty, 2009 for reviews)

  • The clinical significance of altered eye-gaze processing has led to a field of research devoted to understanding how direct and averted gaze are processed in the brain, and how we use them as cues to inform our social interactions

  • While there has been much interest in examining the neural correlates of eye-gaze processing, there does not seem to be a consensus about where and when direct and averted gaze are differentiated in the brain

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Summary

Introduction

Eye-gaze has long been considered one of the most important cues during social interactions and seems central to social cognition (Kleinke, 1986; Emery, 2000; George and Conty, 2008; Itier and Batty, 2009 for reviews). Direct gaze has been heavily implicated in emotion processing (see Hamilton, 2016 for a review), as it is associated with increased ventral striatum activation (Kampe et al, 2001; Strick et al, 2008; see Cardinal et al, 2002, for a review of the ventral striatum’s implication in emotion processing) It is behaviorally more arousing than averted gaze (Nichols and Champness, 1971; Conty et al, 2010; McCrackin and Itier, 2018c) and it has been shown that participants are better at reporting their own emotional state after seeing direct gaze faces than averted gaze faces (Baltazar et al, 2014). Direct gaze is self-referential, indicating that the observer is the focus of attention (George and Conty, 2008; Itier and Batty, 2009; Conty et al, 2016), and direct gaze has been shown to produce similar brain activation as hearing one’s name being called (Kampe et al, 2003)

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