Neurophysiological correlates of attentional bias for emotional faces in socially anxious individuals – Evidence from a visual search task and N2pc
Introduction
Cognitive models of social anxiety disorder (SAD) propose that biases in the processing of social information constitute important factors in the etiology and maintenance of this disorder (Beck, Emery, & Greenberg, 1985; Bögels & Mansell, 2004; Cisler & Koster, 2010; Clark & Wells, 1995; Schultz & Heimberg, 2008; Wong, Gordon, & Heimberg, 2014). Particularly, an early attentional bias to threatening information has been proposed as a major factor which contributes to the etiology, maintenance, or exacerbation of anxiety in general (Bar-Haim, Lamy, Pergamin, Bakermans-Kranenburg, & van Ijzendoorn, 2007; Okon-Singer, Hendler, Pessoa, & Shackman, 2015) and social anxiety in particular (e.g., Miskovic & Schmidt, 2012).
In social anxiety, an attentional bias is mostly observed for social threat cues such as faces expressing disgust or anger, both on a behavioral and on neurophysiological level (e.g., Gilboa-Schechtman & Shachar-Lavie, 2013; Mogg, Philippot, & Bradley, 2004; Peschard and Philippot, 2016; Wieser, McTeague, & Keil, 2011, 2012; Wieser, Pauli, Weyers, Alpers, & Mühlberger, 2009). Summarizing the empirical evidence from the most frequently used paradigm – the emotional dot-probe task – it has recently been concluded that socially anxious individuals preferentially allocate their attention towards threat faces compared to non-anxious controls, but this bias seems to depend on several critical experimental parameters such as the type of reference stimulus, the stimulus duration, and severity of social anxiety (Bantin, Stevens, Gerlach, & Hermann, 2016).
Besides the aforementioned dot-probe task, one paradigm commonly used to investigate the attentional bias to threat is the visual search task, in which participants are asked to find a (potentially threatening) target (e.g., angry face) amongst neutral distracters and vice versa (Frischen, Eastwood, & Smilek, 2008; Hansen & Hansen, 1988). Using faces as stimuli, an “anger superiority effect” i.e. the faster detection of angry compared to friendly facial expressions in a crowd of distractor faces has been demonstrated using either schematic faces (Calvo, Avero, & Lundqvist, 2006; Fox et al., 2000; Juth, Lundqvist, Karlsson, & Öhman, 2005; Öhman et al., 2001; Tipples, Atkinson, & Young, 2002; Weymar, Löw, Öhman, & Hamm, 2011) or real faces (Fox & Damjanovic, 2006; Gilboa Schechtman, Foa, & Amir, 1999; Horstmann & Bauland, 2006; Pinkham, Griffin, Baron, Sasson, & Gur, 2010). Within the context of social anxiety, Juth et al. (2005) found in a series of experiments that both high and low socially anxious individuals were faster to detect happy faces in neutral crowds than angry or fearful faces in neutral crowds (see also Rinck, Becker, Kellermann, & Roth, 2003). In contrast, several studies report that participants suffering from clinical social phobia detected angry faces faster than happy faces when presented in neutral crowds, suggesting an attentional bias toward angry faces (Eastwood and Smilek, 2005; Gilboa Schechtman et al., 1999). Gilboa Schechtman et al. (1999) also report that SAD patients were more distracted by angry crowds compared to neutral crowds if the target was absent, suggesting that these individuals have difficulties disengaging attention away from threat. Similar effects were found in two other studies (Banos, Quero, & Botella, 2008).
Event-related brain potentials (ERPs) are particularly suited for examining attentional biases, as they can provide a temporally precise, direct measure of covert attention and may detect biases not evident in behavioral data (Kappenman, Farrens, Luck, & Proudfit, 2014; Reutter, Hewig, Wieser, & Osinsky, 2017). A good electrophysiological index of enhanced engagement of attention towards threat is the N2pc component as an electrophysiological marker of spatial selective attention (Hickey, Di Lollo, & McDonald, 2009; Kiss, Van Velzen, & Eimer, 2008; Luck and Hillyard, 1994). The N2pc is a negative component emerging around 200 ms after stimulus onset, which is enhanced at electrode sites contralateral to an attended location (e.g., Hickey, McDonald, & Theeuwes, 2006; Kappenman et al., 2014; Kiss et al., 2008; Luck & Hillyard, 1994; Woodman and Luck, 2003). It is named for its polarity (negative), latency (approximately 200 ms poststimulus), and topography (posterior/contralateral), and is defined as the difference between the brain wave elicited at target-ipsilateral sites and target-contralateral sites. It has been proposed that the N2pc reflects the deployment of attention to minimize the interference from (or “filter out”) task-irrelevant stimuli presented concurrently with task-relevant targets (for a review, see Luck, 2012).
Recent ERP studies demonstrated that highly salient threat cues (such as facial expressions) modulate the N2pc: For instance, larger N2pc amplitudes were found in response to fearful or angry faces, relative to neutral or happy faces in the dot-probe task (Grimshaw, Foster, & Corballis, 2014; Holmes, Bradley, Nielsen, & Mogg, 2009; Holmes, Mogg, de Fockert, Nielsen, & Bradley, 2014; Osinsky, Wilisz, Kim, Karl, & Hewig, 2014) and other tasks tapping into visual attention allocation such as visual search tasks (Eimer & Kiss, 2007; Feldmann-Wustefeld, Schmidt-Daffy, & Schubo, 2011; Ikeda, Sugiura, & Hasegawa, 2013; Weymar et al., 2011). Together with findings showing that the N2pc is also modulated when salient faces are task-irrelevant (e.g., Eimer and Kiss, 2007), current electrophysiological data suggest rapid prioritized spatial attention to facial threat.
Several experiments also showed that anxiety modulates the N2pc for threat stimuli. For example, trait anxious individuals showed a greater N2pc for angry faces compared to healthy individuals in a modified visual-probe task (Fox, Derakshan, & Shoker, 2008), which again suggests that anxious individuals have increased engagement with threat. The N2pc is also modulated by specific fear, as phobic individuals (such as individuals with blood phobia or spider phobia) have a greater N2pc for stimuli related to their phobia than for other threatening stimuli (Buodo, Sarlo, & Munafò, 2010; Weymar, Gerdes, Löw, Alpers, & Hamm, 2013). Compared to non-fearful participants, spider fearful individuals showed a more enhanced posterior N2pc to spider (vs. butterfly) targets in an array of flowers. Furthermore, spider fearful participants showed enhanced hypervigilance for all presented stimuli compared to controls as reflected by enhanced C1 (40–60 ms; Weymar, Keil, & Hamm, 2014) and N1 amplitudes (160–200 ms; Weymar et al., 2013). These findings provide neural evidence not only for a general hypervigilance in potentially dangerous contexts in phobic individuals but also for selective (spatial) attention (e.g., N2pc) to fear-relevant stimuli.
In the present study, we used aforementioned visual search paradigm to investigate spatial attention to fear-relevant and fear-irrelevant stimuli (facial expressions) in socially anxious participants and non-anxious controls. In addition to behavioral measures, we included electrophysiological measures of attention selection. Moreover, to improve ecological validity we used pictures of “real” faces instead of schematic ones (Weymar et al., 2011) in the visual search arrays. In line with previous behavioral studies (Öhman et al., 2001; Soares, Esteves, Lundqvist, & Öhman, 2009b), we expected increased spatial attention towards fear-specific targets (threatening faces) in high socially anxious compared to low socially anxious individuals. Furthermore, in line with our recent electrophysiological studies (Weymar et al., 2013; Weymar et al., 2011) we also expected larger N2pc amplitudes in response to threat-relevant faces in HSA compared to LSA individuals. Potentially, attention to the task-relevant items is distracted in displays with threat-relevant distractors, which would result in slower response times in HSA participants (Gerdes, Alpers, & Pauli, 2008) due to delayed disengagement (Fox, Russo, Bowles, & Dutton, 2001). Thus, we expected the N2pc to be reduced or even absent due to enhanced attention capture by the fear-relevant background objects. As some evidence exists for a left visual field/right brain hemisphere advantage both in sustained attention (e.g., Verleger et al., 2009), face (e.g., Kanwisher, McDermott, & Chun, 1997) and emotion processing (e.g., Borod et al., 1998; Kanwisher et al., 1997), we also looked for differences between targets being present in the left versus in the right visual hemifield.
Section snippets
Participants
All participants were female undergraduate students at the University of Würzburg without any past or present psychiatric diagnosis (self-report), who were paid or received course credit for participation. More than 1000 students filled in a pre-screening questionnaire consisting of five items (Ahrens, Mühlberger, Pauli, & Wieser, 2014) based on the DSM-IV criteria for social phobia (American Psychiatric Association, 2013), on a 5-point Likert scale (0 = “Strongly disagree” to 4 = “Strongly
N2pc in response to emotional targets (angry and happy faces amongst neutral distractors)
No general N2pc was observed, F(1,40) = 2.35, p = .133, ηp2 = 0.06. However, a reliable N2pc was present in the HSA group, as indicated by a significant interaction of contralaterality x group, F(1,40) = 4.21, p = .047, ηp2 = 0.10. Separate analyses per group confirmed that a N2pc to face targets (both happy and threatening) was only detectable in HSA, F(1,20) = 4.47, p = .047, ηp2 = 0.18, whereas LSA showed no reliable N2pc, F(1,20) = 0.24, p = .630, ηp2 = 0.01 (see Table 2 and Fig. 2). No
Discussion
Using a visual search paradigm, we investigated if and how individuals with high social anxiety show enhanced attentional capture by threatening faces. In behavior, HSA indeed showed more accurate but not faster responses to angry faces targets. In the N2pc component of the visual ERP elicited by face targets, we found further evidence for an enhanced attention allocation and engagement in HSA for emotional target faces per se: HSA exhibited enhanced spatial attention to emotional (angry and
Author notes
This work was supported by the German Research Foundation (SFB/TRR-58, project B05).
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