. Introduction
Social anxiety is commonly defined as feelings of uneasiness arising when an individual interacts with others and anticipates the possibility of being negatively evaluated. The criteria for a clinical form of social anxiety, social anxiety disorder (SAD), are met when anxiety related to social situations interferes significantly with the person’s normal life (American Psychiatric Association, 2013). The lifetime prevalence of SAD is estimated to be 7–13% (Furmark, 2002) and it typically emerges between early and late adolescence, the mean age of onset being between 10 and 16 years (Wittchen & Fehm, 2001). Cognitive-behavioral models of social anxiety suggest that negative self-appraisals in social situations are essential in the development and maintenance of social anxiety (Clark and Wells, 1995 and Rapee and Heimberg, 1997). It has been proposed that social anxiety is associated with approach–avoidance conflicts resulting, on one hand, from increased investment in peer relationships in adolescence and, on the other hand, from a fear of humiliation and embarrassment aroused by peer evaluation (Caouette & Guyer, 2014).
Eyes are considered to be the strongest fear-producing cue in situations containing social appraisal (Öhman, 1986). An eye contact is a prominent way to signal preparedness for social interaction. A direct gaze signals that one’s attention is directed towards the other person and an averted gaze suggests that one’s attention is directed to someplace else. Thus, a direct gaze may be a potential threat for people with social anxiety. A prominent clinical symptom of SAD is avoidance of eye contact as well as other safety behaviors in social situations (Greist, 1994).
Previous research has shown shortened viewing times of the eye region or reduced eye contact in participants with social anxiety in comparison to non-anxious participants (Daly, 1978 and Farabee et al., 1993; Garner, Mogg, & Bradley, 2006; Moukheiber et al., 2010). However, some studies have not found differences in gazing behavior between participants with and without social anxiety (Hofmann, Gerlach, Wender, & Roth, 1997), and even longer fixation times to the eye region by socially anxious females compared to non-anxious counterparts have been reported (Wieser, Pauli, Alpers, & Mühlberger, 2009). These discrepancies have been partly explained with a hypervigilance-avoidance hypothesis proposing that anxious individuals initially attend to but subsequently avoid threatening stimuli (Wieser, Pauli, Weyers, Alpers, & Mühlberger, 2009). It is also noteworthy, that only two of the studies cited above investigated clinically diagnosed socially anxious participants (Moukheiber et al., 2010 and Hofmann et al., 1997). Studies reporting physiological responses to eye contact in adults or adolescents with social anxiety are scarce. Wieser, Pauli, Alpers, et al. (2009) found more pronounced cardiac acceleration, an index of autonomic reactivity, in participants scoring high in social anxiety to direct vs. averted gaze, whereas this difference was reversed in the group with medium scores and it was non-existing in low socially anxious group. However, measurements of skin conductance responses, another measure of autonomic arousal shown to be sensitive to gaze direction in several studies (Helminen et al., 2011Helminen, Kaasinen, & Hietanen, 2011; Hietanen, Leppänen, Peltola, Linna-aho, & Ruuhiala, 2008; Nichols and Champness, 1971 and Pönkänen et al., 2011b; Myllyneva & Hietanen, 2015), did not indicate differences in responses to direct versus averted gaze in any of the groups.
Previous research has thus provided some evidence suggesting that seeing another person’s direct gaze may be an aversive and arousing stimulus for individuals suffering from social anxiety. In the present study, we aimed at providing further evidence for the aversive and arousing nature of direct gaze for socially anxious individuals and, more specifically, we aimed to investigate whether this is reflected in the psychophysiological measurements of cortical and autonomic nervous system activity. Electroencephalographic (EEG) studies have associated approach–avoidance–motivation to asymmetries in the frontal alpha activity (8–13 Hz). Stronger left-sided vs. right-sided frontal activity has been associated with activations of the approach–motivation system, whereas stronger right-sided vs. left sided activity has been associated with the activation of the avoidance–motivation system (Davidson, 2004, Harmon-Jones, 2003 and Van Honk and Schutter, 2006). Now there is experimental evidence showing that, in healthy adults, seeing a face with a direct vs. averted gaze results in more pronounced left-sided, approach-related frontal EEG activity in the perceiver’s brain (Hietanen et al., 2008 and Pönkänen et al., 2011b). Interestingly, stronger relative left-sided activity to direct vs. closed eyes has been observed also in typically developing children, but not in children with autism spectrum disorder (Kylliäinen et al., 2012). Although there are no previous studies measuring asymmetries in the frontal alpha activity of people suffering from social anxiety in response to perceiving a face with different gaze directions, individuals with social anxiety have been shown to exhibit elevations in right-sided, avoidance-related frontal EEG activity during resting state measurements under social stress (Davidson, Marshall, Tomarken, & Henriques, 2000). However, the findings concerning frontal alpha asymmetry in anxiety disorders are not totally consistent (for a review, see Thibodeau, Jorgensen, & Kim, 2006). One possible reason for these inconsistencies may be that passive resting state measurements are not optimal to capture state or trait relevant EEG-asymmetries and that emotionally and motivationally relevant situations should be employed instead (e.g., Coan, Allen, & McKnight, 2006; Wacker, Chavanon, & Stemmler, 2010).
In earlier studies from our laboratory, we have shown that viewing a face of a real live person, physically present in the experimental situation, elicits differential physiological and self-assessed responses compared to viewing a picture of a face (Hietanen et al., 2008 and Pönkänen et al., 2011b; Pönkänen, Alhoniemi, Leppänen, & Hietanen, 2011). For example, pronounced left-sided, approach-related frontal EEG activity and enhanced skin conductance responses to direct versus averted gaze were observed in response to live faces, but not when the faces of the same persons were shown in a pictorial format. The differences were suggested to be due to mentalizing processes, following from being looked at by another person (Hietanen et al., 2008, Myllyneva and Hietanen, 2015 and Pönkänen et al., 2011b). Being looked at by another individual is likely to elicit feelings of being evaluated. These feelings are, in turn, associated to public self-awareness (Buss, 1980). Our previous studies have shown, indeed, that self-assessed public self-awareness is higher when being looked at by a real person versus not being looked at (Hietanen et al., 2008 and Pönkänen et al., 2011b; Myllyneva & Hietanen, 2015). Cognitive theories of SAD postulate that heightened public self-awareness plays a central role in social anxiety (Clark and Wells, 1995 and Rapee and Heimberg, 1997) and this is supported by empirical evidence (Hope and Heimberg, 1988 and George and Stopa, 2008). Against these previous findings, we reasoned that the use of live social stimuli with a potential for interaction is especially important when investigating participants with social anxiety suffering from fear of negative evaluation and criticism from other people. Several other researchers working in the field of social cognition and social neuroscience have also raised similar concerns regarding the ecological validity of facial stimuli presented in pictorial or video format (Risko, Laidlaw, Freeth, Foulsham, & Kingstone, 2012; Schilbach et al., 2013 and Teufel et al., 2012). In the above mentioned studies investigating socially anxious individuals’ gazing of the eye region, only three had participants viewing real persons instead of pictures or videos (Daly, 1978, Farabee et al., 1993 and Hofmann et al., 1997), and yet the difference between using real persons vs. pictures or videos as stimuli can be considerable on gazing behavior (Laidlaw, Foulsham, Kuhn, & Kingstone, 2011).
In the present study, we investigated autonomic arousal and approach–avoidance related brain activity in response to a face with different gaze directions in adolescents with clinically diagnosed SAD vs. age and sex matched controls. We showed the participants a live face with either direct gaze, averted gaze, or closed eyes through a liquid crystal window, and simultaneously recorded skin conductance responses (SCR) and electroencephalographic (EEG) cortical activity. We hypothesized that all participants would show heightened sympathetic activity and, thus, larger SCRs to direct gaze compared to averted gaze or closed eyes. Because anxiety and fear are related to heightened autonomic activation (Kreibig, 2010), we expected that this pronounced sympathetic activation to direct gaze would be more salient in the SAD group than in the control group. Secondly, we hypothesized that participants in the SAD group would show less relative left-sided frontal cortical activity specifically when observing a face with a direct gaze compared to participants in the control group. In the second part of the experiment, the participants controlled the presentation of the stimuli (a face with a direct or averted gaze) themselves, and in addition to the psychophysiological responses, we measured the viewing time of the facial stimuli. We expected shorter self-controlled viewing times for direct gaze in the SAD group than in the control group. Finally, the participants were also asked to assess their subjective arousal, valence, and situational self-awareness when viewing a face with a direct or averted gaze. We expected that participants in the SAD group would show higher ratings of self-assessed arousal, lower ratings of affective valence (pleasantness), and higher levels of self-assessed public self-awareness for direct gaze compared to participants in the control group.
3. Results
3.1. Skin conductance response
For the computer-controlled presentations, a 3 × 2 ANOVA was conducted with gaze direction (direct, averted, eyes closed) as a within-subjects factor and group (clinical, control) as a between-subjects factor. A main effect of gaze direction was revealed(F(2,60) = 4.4, p = 0.026, View the MathML sourceηp2 = 0.129) indicating larger responses to direct gaze compared to averted gaze or closed eyes regardless of experimental group. Other effects remained non-significant. Mean SCRs for each gaze direction are presented in Fig. 1a.
Mean skin conductance responses to direct gaze, averted gaze and closed eyes (a) ...
Fig. 1.
Mean skin conductance responses to direct gaze, averted gaze and closed eyes (a) in computer-controlled viewing time condition and (b) in self-controlled viewing time condition
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For the self-controlled presentations, a 2 × 2 ANOVA was conducted with gaze direction (direct, averted) as a within-groups factor and group as a between-subjects factor. A main effect of gaze direction was marginally significant (F(1,31) = 3.5, p = 0.07, View the MathML sourceηp2 = 0.102). More importantly, however, there was an interaction between gaze direction and group (F(1,31) = 4.4, p = 0. 043, View the MathML sourceηp2 = 0.125). When comparing the responses to direct and averted gaze between groups, t-tests did not find any significant effects (all ps < 0.1). Further analysis revealed that interaction was due to differences in responses to direct and averted gaze within groups: t-tests indicated greater response to direct gaze than to averted gaze in the clinical group (t = 2.5, p = 0.023, df = 15, d = 0.63) but not in the control group (t = 0.18, p = 0.86, df = 16, d = 0.04). Mean SCRs for each gaze direction and for both groups are presented in Fig. 1b.
3.2. Frontal EEG asymmetry to facial stimuli
Fig. 2 presents mean frontal alpha-asymmetry scores for both experimental groups in the computer-controlled stimulus presentation condition. A 3 × 2 ANOVA revealed no main effects, but there was a marginally significant interaction between gaze direction and group (F(1,30) = 2.66, p = 0.078, View the MathML sourceηp2 = 0.08). A t-test for independent samples suggested that alpha-asymmetry scores for seeing a face with direct gaze was marginally more positive in the control group compared to the clinical group (t = 1.73, p = 0.094, df = 30, d = 0.53).
Mean frontal alpha-asymmetry scores to direct gaze, averted gaze and closed ...
Fig. 2.
Mean frontal alpha-asymmetry scores to direct gaze, averted gaze and closed eyes. A positive value indexes stronger relative left-sided frontal brain activity associated with approach–motivation and a negative value indexes stronger relative right-sided frontal brain activity associated with avoidance–motivation.
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3.3. Viewing time
Fig. 3 shows mean viewing times in the self-controlled presentation block for direct and averted gaze in both experimental groups. A 2 × 2 ANOVA revealed a main effect of gaze direction (F(1,31) = 5.5, p = 0.026, View the MathML sourceηp2 = 0.15) and an interaction between gaze direction and group (F(1,31) = 12.8, p = 0.001, View the MathML sourceηp2 = 0.29). For direct gaze, an independent-samples t-test indicated shorter viewing times in the clinical group compared to the control group (t = 2.27, p = 0.03, df = 31, d = 0.77). For averted gaze, there was no difference between the groups (t = 0.62, p = 0.54, df = 31, d = 0.21).
Mean preferred viewing times to direct gaze and averted gaze facial stimuli in ...
Fig. 3.
Mean preferred viewing times to direct gaze and averted gaze facial stimuli in self-controlled viewing time condition.
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3.4. Self-assessed arousal and valence
The subjective ratings of arousal and valence are shown in Table 1. A 3 × 2 ANOVA for self-ratings of arousal revealed a main effect of gaze direction (F(2,60) = 32.9, p < 0.001, View the MathML sourceηp2 = 0.523) and an interaction between gaze direction and group (F(2,60) = 4.7, p = 0.013, View the MathML sourceηp2 = 0.135). For direct gaze, a t-test showed higher arousal ratings in the clinical group compared to the control group (t = 2.52, p = 0.02, df = 30, d = 0.80), whereas the difference was not significant between the groups for averted gaze (t = 0.78, p = 0.44, df = 31, d = 0.25) or for closed eyes (t = 1.51, p = 0.14, df = 30, d = 0.52).
Table 1.
The self-assessed situational self-awareness scores (and standard deviations) to direct gaze and averted gaze facial stimuli, and the self-assessed ratings of valence and arousal. The scores of SSAS include three factors of self-awareness: public, private and surroundings. The scale-range in SSAS scores is 1–7 and valence and arousal scores 1–9.
Clinical group Control group
Direct gaze Averted gaze Closed eyes Direct gaze Averted gaze Closed eyes
Arousal 4.63 (2.03) 3.12 (1.69) 2.38 (1.20) 3.00 (1.59) 2.71 (1.45) 1.75 (1.13)
Valence 3.19 (1.94) 4.5 (1.67) 5.94 (1.43) 5.43 (1.59) 5.44 (1.31) 6.06 (1.34)
Public 4.74 (1.71) 3.68 (1.30) – 2.90 (1.71) 2.35 (1.40) –
Private 3.75 (1.38) 3.52 (1.23) – 3.47 (1.18) 3.47 (1.09) –
Surroundings 3.75 (1.20) 3.85 (0.98) – 4.65 (1.57) 4.37 (1.70) –
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A 3 × 2 ANOVA for valence ratings indicated significant main effects of gaze direction (F(2,60) = 16.9, p < 0.001, View the MathML sourceηp2 = 0.361) and group (F(1,30) = 7.2, p = 0.011, View the MathML sourceηp2 = 0.196). Overall, the pleasantness ratings were the lowest for direct gaze and the highest for closed eyes; participants in the control group gave higher pleasantness ratings than participants in the clinical group. Importantly, the interaction between gaze direction and group was significant (F(2,60) = 6.2, p = 0.004, View the MathML sourceηp2 = 0.170). When analyzing the responses to different gaze directions separately between the clinical and control groups, t-tests indicated lower pleasantness ratings in the clinical vs. control group to direct gaze (t = 3.81, p = 0.001, df = 31, d = 1.21), marginally significantly to an averted gaze (t = 1.76, p = 0.09, df = 30, d = 0.56), and no difference in ratings to closed eyes (t = 0.25, p = 0.80, df = 31, d = 0.33). Importantly, participants in the control group evaluated direct gaze as mildly pleasant (M = 5.43), whereas the participants with SAD evaluated direct gaze as unpleasant (M = 3.19).
3.5. Self-awareness
Situational self-awareness was analyzed separately for each of three components (public, private and awareness of surroundings). For public self-awareness, a 2 × 2 ANOVA with gaze direction (direct, averted) as a within-subjects factor and group (clinical, control) as a between subjects factor revealed main effects of gaze direction (F(1,31) = 15.9, p < 0.001, View the MathML sourceηp2 = 0.339) and group (F(1,31)= 10.3, p = 0.003, View the MathML sourceηp2 = 0.248The self-assessed public self-awareness was higher to direct vs. averted gaze and, overall, it was higher in the clinical than in the control group. No effects were found for private self-awareness or awareness of immediate surroundings (all ps > 0.1). Mean SSAS scores for both groups are shown in Table 1.
