Gaze direction differentially affects avoidance tendencies to happy and angry faces in socially anxious individuals

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Abstract

Increasing evidence indicates that eye gaze direction affects the processing of emotional faces in anxious individuals. However, the effects of eye gaze direction on the behavioral responses elicited by emotional faces, such as avoidance behavior, remain largely unexplored. We administered an Approach-Avoidance Task (AAT) in high (HSA) and low socially anxious (LSA) individuals. All participants responded to photographs of angry, happy and neutral faces (presented with direct and averted gaze), by either pushing a joystick away from them (avoidance) or pulling it towards them (approach). Compared to LSA, HSA were faster in avoiding than approaching angry faces. Most crucially, this avoidance tendency was only present when the perceived anger was directed towards the subject (direct gaze) and not when the gaze of the face-stimulus was averted. In contrast, HSA individuals tended to avoid happy faces irrespectively of gaze direction. Neutral faces elicited no approach-avoidance tendencies. Thus avoidance of angry faces in social anxiety as measured by AA-tasks reflects avoidance of subject-directed anger and not of negative stimuli in general. In addition, although both anger and joy are considered to reflect approach-related emotions, gaze direction did not affect HSA's avoidance of happy faces, suggesting differential mechanisms affecting responses to happy and angry faces in social anxiety.

Introduction

Social anxiety is characterized by an extensive fear of being evaluated by others and leads socially anxious individuals to engage in so-called safety behaviors (e.g. Clark & Wells, 1995). Direct gaze is a clear signal of being attended to by someone else and hence a potential start of a social interaction. It may therefore constitute a critical threat stimulus for a socially anxious individual eliciting safety behaviors, such as social avoidance (Fox et al., 2007, Heuer et al., 2007, Horley et al., 2003, Marks, 1987, Roelofs, van Peer, et al., 2009). The present study aimed to test the effects of eye gaze direction on social avoidance tendencies elicited by emotional faces in socially anxious individuals.

There is increasing evidence that social threat cues, such as emotional faces accompanied by direct gaze, elicit avoidance tendencies in high socially anxious individuals (Heuer et al., 2007, Horley et al., 2003, Horley et al., 2004, Lange et al., 2008, Roelofs et al., 2005, Roelofs, van Peer, et al., 2009, Van Peer et al., 2007, Van Peer et al., 2009). For example, Heuer et al. (2007) applied a speeded Approach-Avoidance Task (AAT), where participants either pulled or pushed a joystick in response to visually presented emotional faces. The emotional faces gradually disappeared when participants pushed the joystick away from them and grew in size when participants pulled the joystick towards themselves. Comparison of high (HSA) versus low (LSA) socially anxious individuals demonstrated clear avoidance tendencies (faster pushing than pulling) in HSA, to both happy and angry facial expressions, but not to neutral faces or non-facial pictures. The fact that HSA not only avoided angry but also happy faces has been explained by the fact that both angry and happy facial expressions communicate emotions that are directed towards the subject (i.e. approach-related emotions, in contrast to sad and fearful faces communicating avoidance-related emotions; Adams and Kleck, 2003, Adams and Kleck, 2005, Heuer et al., 2007). Although this hypothesis has not been tested directly yet, this may indicate that it is the subject-directedness of the emotional faces, and not the content of the emotion per se, that elicits avoidance tendencies in high socially anxious individuals.

A growing body of evidence from neurophysiological and imaging studies on face processing suggests that direct eye gaze, as compared to averted eye gaze, induces enhanced visual processing of facial information (e.g. Conty et al., 2007, George et al., 2001, Pelphrey et al., 2004). Direct gaze elicits enhanced activation not only in visual brain areas (e.g., Wicker et al., 1998, Wicker et al., 2003), but also in the amygdala (George et al., 2001, Kawashima et al., 1999). Although the evidence for angry face stimuli is less conclusive (Adams et al., 2003, Sato et al., 2004), such enhanced processing associated with direct gaze may particularly occur when the faces communicate approach-driven emotions, such as anger and joy (Adams and Kleck, 2003, Adams and Kleck, 2005). In a speeded emotion detection study, Adams and Kleck (2003) found that emotion detection of faces expressing approach oriented emotions (e.g. anger and joy) was faster when the faces presented with direct gaze. In contrast, faces expressing avoidance oriented emotions (e.g. fear and sadness) were labeled faster in combination with averted gaze. These findings suggest that gaze direction influences both the processing speed and the perceptual interpretation of facial cues. In 2005, Adams Jr. and Kleck replicated these findings and in addition showed that gaze direction influenced subjective intensity ratings of facial expressions. In addition, Hietanen et al. (2008) explored whether eye gaze direction may activate lateralized neural approach-avoidance systems and tested whether seeing another person's direct versus averted gaze influenced the hemispheric asymmetry in the frontal electroencephalographic (EEG) activity. Direct gaze indeed elicited a relative left-sided frontal EEG activation (taken as indicative of a tendency to approach), whereas averted gaze activated right-sided asymmetry (taken as indicative of avoidance). Moreover, direct gaze was associated with more intense autonomic activation and higher subjective ratings of emotional arousal and valence, supporting previous findings that direct gaze induces higher cardiac acceleration in healthy (for review see Kleinke, 1986) as well as in socially anxious individuals (Wieser et al., 2009).

In sum, studies in healthy participants suggest that eye gaze direction affects the processing of faces, both by itself and in interaction with the emotional expression of the faces (see also Fox et al., 2007, Holmes et al., 2006). However, to our knowledge, no studies have directly tested the effects of eye gaze direction on social approach-avoidance tendencies. Given the significance of gaze direction in emotion detection studies, one might predict that the previously found avoidance tendencies elicited by angry faces on manual Approach-Avoidance Tasks (Heuer et al., 2007, Lange et al., 2008, Rotteveel and Phaf, 2004, Roelofs et al., 2005, Roelofs, Minelli, et al., 2009, Roelofs, van Peer, et al., 2009, Van Peer et al., 2007, Van Peer et al., 2009) largely depend on the use of direct gaze.

The major aim of the present study was to test this hypothesis by manipulating gaze direction of emotional (happy, angry and neutral) faces on the AAT. Second, in addition to angry faces, happy facial expressions are also considered to communicate an approach-driven emotion. Although avoidance reactions to happy faces are less frequently observed, Heuer et al. (2007) and Lange et al. (2008) found HSA to avoid happy faces in addition to angry faces and suggested that direct gaze, even when accompanied by a positive expression may be threatening to a socially anxious individual as it may reflect an invitation to the feared social contact. Based on this hypothesis we predicted that happy faces would also elicit avoidance tendencies in HSA, but only when presented with direct gaze.

Section snippets

Participants

Twenty high (HSA) and twenty low (LSA) socially anxious individuals were selected from a sample of 480 students from Leiden University, based on their anxiety score on the Liebowitz Social Anxiety Scale (LSAS: Liebowitz, 1987), with LSAS-anxiety scores >27 for HSA and <13 for LSA (see Heuer et al., 2007). All HSA participants met the LSAS-total cutoff score of 30 for social anxiety disorder and 8 HSA participants met the LSAS-total cutoff of 60 for generalized social anxiety disorder –Rytwinski

Results

One LSA participant was excluded from analysis because of RTs deviating > 3 SD from the group mean. See Table 2 for mean RTs per cell. Error rates were low. HSA: 2.6% and LSA: 3.2%.

The 3-way (Group × Emotion × Gaze) ANOVA rm for the AAT effect-scores revealed a significant main effect for Emotion (F(2,36) = 5.66; p = 0.007; ηp2 = 0.24) and, most importantly, a significant 3-way interaction of Group × Emotion × Gaze (F(2,36) = 4.61; p = 0.017; ηp2 = 0.21). To explore the nature of this interaction, separate analyses

Discussion

Previous research using the zooming AAT (Heuer et al., 2007) indicated that HSA individuals show increased avoidance tendencies in response to both angry and happy facial expressions. In the present study we largely replicated these results and moreover extended these findings by showing that avoidance of angry faces depends on the eye gaze direction displayed by the face, whereas avoidance of happy faces does not.

The relative tendency to avoid angry faces in HSA subjects is in line with

Acknowledgements

K. Roelofs was supported by a VIDI Grant (#452-07-008) and P. Putman by a VENI Grant (#451-07-028) from the Netherlands Organization for Scientific Research (NWO).

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