Attentional processes during emotional face perception in social anxiety disorder: A systematic review and meta-analysis of eye-tracking findings

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Highlights

  • Studies on attention to emotion faces in clinical social anxiety are reviewed.

  • Eye-tracking research administering single or pairs of faces is analyzed.

  • Eye contact to emotional faces is avoided in social anxiety disorder.

  • A small early attention bias toward angry faces is found in social anxiety disorder.

  • Face scanning during single face viewing is increased in social anxiety disorder.

Abstract

Background

In recent years, a growing body of eye-tracking research has investigated gaze behavior in individuals with social anxiety during the visual perception of emotional stimuli. The aim of this article was to review and synthesize studies examining attention orientation in patients with clinical social anxiety by means of eye-tracking methodology.

Methods

Through a systematic search, 30 articles were identified, including 11 studies in which single emotional faces were used as stimuli and seven eligible studies in which threatening faces were paired with neutral stimuli. Meta-analyses were conducted to compare prolonged eye-contact behavior and early attentional biases to threats in individuals with social anxiety disorder (SAD) and healthy controls.

Results

Moderate group differences were revealed for single face viewing studies, with SAD patients showing significantly reduced eye contact with negative (Hedges' g = −0.67) and positive emotional faces (g = −0.49) compared to that of healthy participants. Type of task and duration of stimulus presentation were (marginally) significant moderators of between-study variance in effect size. Small but significant group differences were found for early attentional biases toward angry faces versus neutral stimuli (g = 0.21) but not toward happy faces versus neutral stimuli (g = 0.05). Preliminary evidence for a hyperscanning strategy in SAD patients relative to healthy controls emerged (g = 0.42).

Limitations

The number of included studies with face pairings was low, and two studies were excluded due to unavailable data.

Conclusions

Our results suggest that eye contact avoidance with emotional faces is a prominent feature in SAD patients. Patients might benefit from guidance to learn to make adequate eye contact during therapeutic interventions, such as exposure therapy. SAD patients demonstrated slightly heightened attention allocation toward angry faces relative to that of healthy participants during early processing stages. Threat biases can be potential targets for attention modification training as an adjuvant to other treatments. Future research on early attentional processes may benefit from improved arrangements of paired stimuli to increase the psychometric properties of initial attention indices.

Introduction

Social anxiety is characterized by exaggerated fears of being rejected or negatively judged by others (Leary and Kowalski, 1995). This fear is often accompanied by dysfunctional assumptions about people's high social standards for performance and people's overcritical attitude (Rapee and Heimberg, 1997). Patients with social anxiety disorder (SAD, or social phobia) report intense feelings of distress in anticipated or actual social situations and tend to manifest maladaptive avoidant behaviors. Affected individuals suffer from significant functional impairments in daily life (American Psychiatric Association, 2013), and if left untreated, the disorder typically follows a chronic course (Beard et al., 2010). With a lifetime prevalence of 11–12%, SAD is a relatively common psychiatric disorder (Kessler et al., 2012) and has a significant impact on health economics (Wittchen and Jacobi, 2001). A large body of research has tried to elucidate the patterns of information processing that may contribute to the occurrence and persistence of symptoms. Cognitive models emphasize the importance of attentional biases and altered threat perception for the etiology and maintenance of anxiety (Beck and Clark, 1997; Rapee and Heimberg, 1997). It has been postulated that individuals with social anxiety preferentially allocate their attention to potential social threats in the environment, i.e., indicators of negative evaluation or rejection (Rapee and Heimberg, 1997). The facilitated detection of a threat is assumed to occur at an early stage of information processing (Rapee and Heimberg, 1997); this stage of information processing occurs at an automatic level and involves the nonconscious, rapid, and involuntary recognition of stimuli (Beck and Clark, 1997). Theoretical models suggest that anxious individuals are characterized not only by an overreactive threat detection system but also by an impaired ability to disengage attention from detected threats (Fox et al., 2001; Cisler and Koster, 2010). Thus, anxious individuals are thought to manifest initial hypervigilance to potential dangers and a maintenance bias to stimuli perceived as threatening.

Additionally, later strategic avoidance of threatening information has been discussed as an attempt to regulate emotional distress (Mogg et al., 2004a; Koster et al., 2005). Avoidance has been described as a safety behavior to prevent feared social encounters and negative evaluations (Clark and Wells, 1995). In addition to complete withdrawal from social situations as an extensive form of avoidance, limited eye contact has been described as a subtle but typical avoidance behavior in SAD patients (American Psychiatric Association, 2013). Whereas avoidance strategies are considered voluntary, initial attention orientation toward threats (vigilance) and delayed disengagement (maintenance biases) appear to be rather automatic (e.g., Beck and Clark, 1997; Cisler and Koster, 2010).

In earlier meta-analyses across anxiety disorders and subclinical trait anxiety (e.g., Bar-Haim et al., 2007) that focused on reaction time tasks, an attentional bias to threats was identified. However, findings in SAD patients appear less consistent. Several studies used reaction time tasks and provided support for the presence of attentional biases (i.e., vigilance or maintenance biases) toward social threats in SAD patients (Amir et al., 2003; Mogg et al., 2004b for the brief stimulus exposure duration; Sposari and Rapee, 2007; Stevens et al., 2009 for the brief stimulus exposure condition); however, a substantial number of studies reported contradictory results (Chen et al., 2002; Gotlib et al., 2004; Mogg et al., 2004b and Stevens et al., 2009 for the longer stimulus exposure duration). A quantitative review investigated attentional biases as a function of clinical and subclinical social anxiety based on studies using the dot-probe task (Bantin et al., 2016). Group differences of medium effect size (g = 0.53) were revealed, suggesting heightened vigilance for negative faces in socially anxious individuals. Group comparisons yielded no evidence for attentional preferences for positive faces in individuals with social anxiety (g = 0.13). However, reaction time-based measures as indicators of attention allocation have been frequently criticized as generally unsuitable for differentiating components of attentional bias (Clarke et al., 2013). In addition to reports of poor reliability (Schmukle, 2005; Staugaard, 2009; Waechter et al., 2014), it has been argued that these tasks only provide a current snapshot of spatial attention (Bradley et al., 2000). These measures allow for inferences about attention focus at a single time point depending on stimulus presentation duration. Bradley et al. (2000) highlighted the importance of alternative indicators of attention, such as assessments of eye movement. Eye-tracking techniques allow researchers to directly examine eye movements as an indicator of attention allocation since gaze direction and attention focus are assumed to be tightly coupled (Wright and Ward, 2008). Early stages as well as later stages and changes in attention could be investigated over a longer time course (Sears et al., 2019). The location or probability of initial fixation, first fixation latency, and initial fixation durations were subsumed under early attention parameters. Armstrong and Olatunji (2012) argued that the first second of stimulus presentation is largely determined by the first orientation and first maintenance of gaze, leaving only limited time for viewing other parts of the stimuli. The authors explained that this phase of initial attention allocation is largely driven by exogenous characteristics of a stimulus. These exogenous effects are thought to persist beyond the initial orientation to the initial maintenance of gaze, whereas endogenous control processes follow and increase over time. Later attentional engagement is often indicated by the viewing pattern that follows the initial viewing epoch, including dwell time and fixation duration parameters. A meta-analysis based on eye-tracking research was performed by Armstrong and Olatunji (2012) to investigate attentional biases in anxiety and depression. The majority of the included studies examined subclinical levels of (social) anxiety or other types of clinical anxiety disorders aside from SAD. Until then, only a few eye-tracking studies have been conducted with individuals with clinical SAD. For free-viewing tasks with at least two competing stimuli, the results revealed medium effect sizes (g = 0.47) for initial attention allocation toward a threat in anxious individuals compared to that in nonanxious individuals. For social anxiety in particular, effect sizes were somewhat lower (g = 0.37), but mainly nonclinical studies (k = 7, vs. k = 2 clinical) were included in this analysis. Initial attention allocation to positive stimuli was not significantly related to anxious tendencies.

In contrast, a more recent meta-analysis on eye tracking in child and adolescent clinical and subclinical anxiety revealed no significant group effects for orientation biases to threats (Lisk et al., 2020). High- and low-anxiety individuals showed similar early viewing patterns for threatening versus neutral stimuli. The results indicated later avoidance tendencies for threatening stimuli in individuals with anxiety. However, this effect was primarily pronounced in samples with mixed anxiety issues (e.g., trait anxiety, generalized anxiety) and did not emerge in socially anxious youths. The authors concluded that late avoidance effects may be driven by anxiety symptoms rather than by social fears.

In 2017, a review was published by Chen and Clarke, summarizing findings from eye-tracking research in social anxiety.1 Here, findings for selective attention to competing stimuli, typically presented as pairs of emotional and neutral stimuli, and for attention patterns while viewing single faces were reported in a qualitative manner. Of note, no systematic search method was described, and studies dealing with the effects of clinical and subclinical social anxiety were included. For competing stimuli, the authors concluded that there is evidence for an initial preference for, as well as initial avoidance of, threatening information in social anxiety. Thus, research indicates the existence of attentional biases in social anxiety, but the direction in terms of vigilance or avoidance is not clear. Chen and Clarke (2017) recommended the identification of potential moderators to explain these heterogeneous findings. Moreover, the research findings pointed to avoidance of eye contact in socially anxious individuals.

Another recent review assembled evidence, based on eye-tracking and observer ratings, to determine whether socially anxious individuals avoid looking into another's eyes during social interactions, performance, and face viewing (Chen et al., 2020). This qualitative summary was focused on prolonged eye contact and late attention parameters, such as total fixations or eye contact counts, over the whole trial. In line with Chen and Clarke (2017), the authors concluded that SAD is characterized by an avoidance of mutual gaze. However, the findings appeared more consistent for clinical subjects than for subclinical subjects across different experimental situations. Additionally, the results of Armstrong and Olatunji (2012) suggested that effect sizes for clinical samples are higher than those for nonclinical samples, emphasizing the importance of clarifying the effects of clinically relevant SAD on attentional processes.

There is a growing body of research examining gaze behavior in individuals with SAD during the perception of single emotional faces. To date, no meta-analyses on eye-contact behavior with emotional faces have been performed in clinical SAD patients. Against this background, it appears reasonable to present an updated synthesis of eye-tracking research in clinical SAD patients in a quantitative manner. Thus, the current systematic review and meta-analyses aimed to summarize findings based on eye-tracking methodology to expand our understanding of altered attentional processes during the perception of social-emotional stimuli in clinically relevant SAD. This review may help to further clarify attentional processes that contribute to the psychopathology of SAD and to disentangle previous heterogeneous findings. Treatment approaches that target maladaptive attentional processes, such as attentional bias modification (ABM) training programs, have become increasingly established (e.g., Heeren et al., 2015) and might benefit from further insights on attentional control in SAD patients.

The majority of eye-tracking studies in SAD patients utilized single face perception tasks to examine their eye-contact behavior. Other studies implemented free viewing and dot-probe paradigms where emotional faces were paired with neutral stimuli, subsequently referred to as face pairing paradigms.

Based on the available data, the impact of SAD on an individual's extended eye-contact behavior during single face viewing as well as on early attentional processes during the perception of competing stimuli can be quantitatively evaluated by means of meta-analyses.

The main objectives of our meta-analyses were as follows: first, whether SAD patients, compared to healthy controls, exhibit avoidance of eye contact, as indicated by decreased attention allocation to the eye regions of single emotional faces, was evaluated. Effect sizes were calculated separately for faces expressing positive and negative emotions. For exploratory purposes, effect sizes for neutral faces were additionally determined.

Second, whether SAD patients, compared to healthy controls, are characterized by an early attentional bias toward socially threatening stimuli when they are simultaneously presented with neutral stimuli was examined. For exploratory purposes, early attentional biases to positive stimuli were also explored as a function of SAD.

Several sample and task characteristics were taken into account as potential moderators of effects.

Section snippets

Selection criteria of articles

The criteria for the inclusion of studies were (1) utilization of eye-tracking methods (video-based infrared systems or electrooculography) to examine attention to emotional faces, (2) comparison of patients suffering from clinical SAD with healthy controls, and (3) English language articles. The exclusion criteria were as follows: (1) meta-analyses, review articles, case reports, letters to the editor, or commentaries; (2) studies that investigated eye movements in social anxiety with

Study selection

Fig. 1 illustrates the systematic search and study selection process. The initial search (including the additional search through other resources) yielded 750 hits, and 618 remained after duplicates were removed. Screening titles and abstracts resulted in 78 included articles for full-text screening. Forty-eight articles were excluded, resulting in 30 articles that were eligible for qualitative (n = 11) and partially quantitative (n = 19) synthesis.

Single face viewing

The present meta-analysis integrates 11

Eye contact behavior

The current overview aimed to summarize quantitatively and qualitatively existing eye-tracking investigations on attention to social-emotional stimuli in patients with clinical SAD. The majority of available studies employed free viewing tasks with single emotional faces as stimuli to examine eye contact over an extended duration. Our meta-analyses on mutual eye gaze with emotional faces included eleven studies and revealed moderate group differences, with SAD patients showing reduced eye

Conclusions

Our results confirm the notion that eye contact avoidance is a prominent feature in SAD. Additionally, we provide evidence for slightly heightened attention allocation toward angry faces during early processing stages in SAD patients relative to healthy controls. Interpersonal contact in SAD patients may be biased by their inappropriate avoidant behavior and dysfunctional perception of social threat signals. Patients might benefit from guidance to learn to employ adequate eye contact during

Role of funding source

Vivien Günther and Adam Kropidlowski were supported by the junior research grant of the Medical Faculty of the University of Leipzig.

Declaration of Competing Interest

The authors declare no conflicts of interest.

Acknowledgements

None.

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