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Written threat: Electrophysiological evidence for an attention bias to affective words in social anxiety disorder a
b
a
Pascal Wabnitz , Ulla Martens & Frank Neuner a
Department of Clinical Psychology and Psychotherapy, University of Bielefeld, Bielefeld, Germany b
Department of Cognitive Psychology, University of Osnabrück, Osnabrück, Germany Published online: 26 Mar 2015.
Click for updates To cite this article: Pascal Wabnitz, Ulla Martens & Frank Neuner (2015): Written threat: Electrophysiological evidence for an attention bias to affective words in social anxiety disorder, Cognition and Emotion, DOI: 10.1080/02699931.2015.1019837 To link to this article: http://dx.doi.org/10.1080/02699931.2015.1019837
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COGNITION AND EMOTION, 2015 http://dx.doi.org/10.1080/02699931.2015.1019837
Written threat: Electrophysiological evidence for an attention bias to affective words in social anxiety disorder Pascal Wabnitz1, Ulla Martens2, and Frank Neuner1 1
Department of Clinical Psychology and Psychotherapy, University of Bielefeld, Bielefeld, Germany Department of Cognitive Psychology, University of Osnabrück, Osnabrück, Germany
2
Downloaded by [University of Auckland Library] at 20:47 09 April 2015
(Received 3 February 2014; accepted 11 February 2015)
Social anxiety disorder (SAD) is associated with heightened sensitivity to threat cues, typically represented by emotional facial expressions. To examine if this bias can be transferred to a general hypersensitivity or whether it is specific to disorder relevant cues, we investigated electrophysiological correlates of emotional word processing (alpha activity and event-related potentials) in 20 healthy participants and 20 participants with SAD. The experimental task was a silent reading of neutral, positive, physically threatening and socially threatening words (the latter were abusive swear words) while responding to a randomly presented dot. Subsequently, all participants were asked to recall as many words as possible during an unexpected recall test. Participants with SAD showed blunted sensory processing followed by a rapid processing of emotional words during early stages (early posterior negativity – EPN). At later stages, all participants showed enhanced processing of negative (physically and socially threatening) compared to neutral and positive words (N400). Moreover, at later processing stages alpha activity was increased specifically for negative words in participants with SAD but not in healthy controls. Recall of emotional words for all subjects was best for socially threatening words, followed by negative and positive words irrespective of social anxiety. The present findings indicate that SAD is associated with abnormalities in emotional word processing characterised by early hypervigilance to emotional cues followed by cognitive avoidance at later processing stages. Most importantly, the specificity of these attentional biases seems to change as a function of time with a general emotional bias at early and a more specific bias at later processing stages. Keywords: Emotion; Word processing; Event-related potentials; Swear words; Social anxiety disorder.
Social anxiety disorder (SAD) is one of the most common psychiatric disorders (Kessler et al., 2005) and it is characterised by a persistent fear and avoidance of social situations (Buckner, Bernert, Cromer, Joiner, & Schmidt, 2008; Buckner,
Eggleston, & Schmidt, 2006). It is related to abnormalities in several cognitive processes (Amir, Elias, Klumpp, & Przeworski, 2003; Clark & Wells, 1995; Rapee & Heimberg, 1997), in particular in attention, memory and interpretation
Correspondence should be addressed to: Pascal Wabnitz, Department of Psychology, Bielefeld University, Postbox 100131, 33501 Bielefeld, Germany. E-mail: [email protected] © 2015 Taylor & Francis
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of ambiguous and threatening social information (for reviews see Heinrichs & Hofmann, 2001; Pishyar, Harris, & Menzies, 2004). A general hypervigilance towards potentially threatening information has been well-documented for participants with SAD (Bar-Haim, Lamy, Pergamin, Bakermans-Kranenburg, & van Ijzendoorn, 2007; Pishyar et al., 2004); however, the specificity of this effect is under debate. While a bias towards threat cues is a common characteristic of anxiety disorders, it is unclear whether this bias only occurs for stimuli that represent the core of the subjective anxiety (specificity), or whether it reflects a general state of hypervigilance to all incoming stimuli (general; Heinrichs & Hofmann, 2001). With respect to social anxiety features of this core are the fear of being exposed to an audience that might evaluate the person in a negative way (Rapee & Heimberg, 1997) as well as the fear of losing one’s social status or being rejected leading to avoidance behaviour (Clark & Wells, 1995). Following the schema congruency hypothesis (Beck, Emery, & Greenberg, 1985), Williams, Mathews, and MacLeod (1996) predicted differential biases in participants with anxiety disorders depending on the participants’ personal schemas (defined as cognitive, well-organised negative or positive representation of oneself or the environment for the rapid processing of incoming information) as well as systematics in diagnoses (see also Mathews & MacLeod, 1994). Tests of this assumption using a variety of experimental paradigms, including behavioural and physiological indicators, yielded mixed results with regard to the specificity of threat cues in SAD. Several studies have applied the Stroop task that determines an attentional bias to threat cues by observing the latencies in the identification of the colour of emotional words (MacLeod, 1991). Some studies found unspecific biases towards all emotional words regardless of the diagnosis (Asmundson & Stein, 1994), whilst other studies did confirm disorder-specific effects (Becker, Rinck, Margraf, & Roth, 2001; Hope, Rapee, Heimberg, & Dombeck, 1990; Mattia, Heimberg, & Hope, 1993). For instance, Becker et al. (2001)
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reported a distinct bias to speech-related words (e.g., talk, stutter, blush) in participants with SAD. The dot-probe task is a different and potentially more valid paradigm for the assessment of attentional biases (MacLeod, Mathews, & Tata, 1986). In this task, an attentional bias to threat stimuli is identified through faster reaction times to probes replacing a threat-related cue (emotional facial expression or emotional word) than to probes replacing a neutral cue (Cisler, Olatunji, & Lohr, 2009; Mogg & Bradley, 1998). Especially in SAD, attention biases to emotional stimuli (angry facial expressions) have been confirmed in various studies using the dot-probe task (Bradley, Mogg, Falla, & Hamilton, 1998; Bradley, Mogg, & Millar, 2000; Mogg & Bradley, 2002). However, there are mixed results regarding the specificity of this effect, as some studies have found an unspecific bias to all types of emotional faces regardless of the specific emotion (Mogg, Garner, & Bradley, 2007; Wilson & MacLeod, 2003), while others have identified more specific biases of SAD towards (social) threat words (Asmundson & Stein, 1994) or disgust/judgmental facial expressions (Pishyar et al., 2004). Summing up, different paradigms have been applied to study attention biases in recent years (see Cisler, Bacon, & Williams, 2009, for an overview), all tapping in discrete cognitive processes and do not inevitably intercorrelate (Cisler, Bacon, et al., 2009). The present study aimed at disentangling the specificity of attention biases in SAD compared to healthy controls (i.e., subjects without a psychiatric disorder) using four different sources of information [event-related potentials (ERP), oscillatory brain activity, behavioural measures and memory performance]. For this purpose we relied on a new paradigm evaluated in one of our previous studies (Wabnitz, Martens, & Neuner, 2012) that does not specifically guide subjects’ attention to a certain artificial task (i.e., emotional Stroop or dot-probe task) but leaves the guidance of attention to the subjects’ motivation. This refers to the notion that social anxious subjects direct their attention to signals of social disapproval or rejection whenever they anticipate negative evaluations (Rapee & Heimberg, 1997). Thus, social anxious
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subjects instantly have a motivation to detect social threatening cues to avoid social humiliation or rejection. This hypervigilance is assumed to be followed by avoidance of threat cues (Clark, 2001), but is far from understood (Heinrichs & Hofmann, 2001). More importantly, in our view previous paradigms hold a low ecological validity, since their results not only illustrate pure attention processes but effects of certain, sometimes artificial, tasks (i.e., emotional Stroop). In fact, current research points to problems regarding the validity and reliability of posttraumatic stress disorder (PTSD) dot probe (Schmukle, 2005) and the emotional Stroop task (Cisler, Bacon, et al., 2009). Specificity of attention biases may exist across various anxiety disorders, but this cannot be answered within the present study.
ERP components associated with emotional processing While the dot-probe and the Stroop task rely on behavioural responses for measuring attention (biases), other measures are thought to directly tap into stimulus processing via measuring electrocortical responses to the presentation of a stimulus. For instance, ERPs associated with various stages of visual stimulus processing have been associated with anxiety. The amplitude of a positive-going voltage fluctuation approximately 100 ms after stimulus onset (P100) increases with the amount of attention allocated to the stimulus (e.g., Luck, Woodman, & Vogel, 2000). Studies that simultaneously presented neutral and emotional face pairs that were followed by a horizontal or vertical bar flashed to either left or right side of the screen replacing one of the face pairs reported larger P100 amplitudes when the bar replaced a fearful face than when it replaced a neutral face (e.g., Pourtois, Den, Grandjean, Sander, & Vuillemier, 2005) indicating that the P100 may be sensitive to the emotional salience of the stimulus. Hence, enlarged P100 amplitudes in social phobics may indicate vigilance for emotional words. However, whether this hypervigilance is evident for all words or only for those who
transport a socially threatening connotation is subject to the present study. Following the P100, a negative deflection that occurs at posterior sites around 200 ms after stimulus onset (early posterior negativity – EPN) differentiates between neutral and emotional stimuli (e.g., Schupp, Flaisch, Stockburger, & Junghöfer, 2006). The EPN is linked to increased emotional processing (Schupp, Junghöfer, Weike, & Hamm, 2003a, 2003b, 2004) and arises independent from instructed attention (Kissler, Herbert, Winkler, & Junghöfer, 2009). While the P100 has been suggested to be associated with general vigilance, enhanced EPN amplitudes to emotional stimuli reflects spontaneous selective processing of the emotional significance of the stimulus (Kissler et al., 2009). Somewhat later in the processing stream, after about 400 ms, a negative potential (N400) that has been associated with semantic integration based on subjects’ expectations or the context and structure of a sentence (Kutas & Federmeier, 2000) can also be modulated by the emotional content of a stimulus. Herbert, Junghofer, and Kissler (2008) reported attenuated N400 amplitudes by pleasant words, possibly indicating facilitated semantic integration of pleasant in contrast to unpleasant words. Thus, while sensory (P100) and automatic but selective processing (EPN) appears even without conscious processing, enhanced N400 amplitudes to emotional stimuli reflect somehow more elaborated processing (i.e., semantic or mood-dependent integration of the stimulus). Taken together, measuring ERPs allows a fine analysis of electrophysiological correlates of attention biases in a temporal sequence, due to its excellent temporal resolution. Assessing different components offers an insight in functional different levels of processing emotional stimuli. Applying these measures to the study of social anxiety sheds further light on the processing of emotional stimuli. In a series of studies, Kolassa, Musial, and Miltner (2007) reported generally increased visual P1 amplitudes in SAD participants to face stimuli (happy, sad, angry, neutral) compared to healthy participants and spider phobics. In line with this COGNITION AND EMOTION, 2015
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finding, Mühlberger, Wieser, Herrmann, Weyers, Tröger, and Pauli (2009) found that while socially anxious participants showed enhanced P1 amplitudes in response to all faces, the emotional modulation of the EPN may be specific for emotional faces only. However, Mühlberger et al. (2009) used artificial faces, thus limiting the generalisability of theirs results.
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Alpha desynchronisation in anxious individuals Another form of analysing electrophysiological responses to threat cues is the stimulus-dependent modulation of the oscillatory brain activity that is known to play are role in human cognition with varying behavioural correlates (e.g., Kahana, 2006). In particular, alpha-frequency activations are directly associated with distinct cognitive processes (i.e., inhibition). Cognitive inhibition can be mapped to distinct regions of the prefrontal cortex (PFC; Aron, Robbins, & Poldrack, 2004), a region that is thought to exert its inhibitory control on subcortical regions to implement executive control (Aron et al., 2004). This functional localisation seems to be limited to the right PFC and is thought to be associated with frontal alpha oscillations in the human EEG. However, current conceptualisations propose that high alpha-oscillatory activity may reflect the inhibition and disengagement of task-irrelevant cortical areas, while reduced alpha activity reflects active neuronal processing (see Palva & Palva, 2007). The asymmetry of frontal alpha activity has also been hypothesised to reflect a model of different emotional involvement during stimulus processing (Davidson, Marshall, Tomarken, & Henriques, 2000). In particular, while alpha desynchronisation over left regions of the PFC reflects approachrelated behaviour tendencies, right-sided alpha desynchronisation is associated with withdrawalrelated behaviour and emotions (Davidson et al., 2000; Heller, Nitschke, Etienne, & Miller, 1997). In fact, right-sided PFC activity (alpha desynchronisation) not only increased in anxious participants while listening to fearful and sad narratives compared to non-anxious participants (Heller
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et al., 1997), but also the triggering of anxiety was reported to account for a substantial proportion of variance of right-sided PFC activity (Davidson et al., 2000). Research assessing oscillations in frontal regions of the brain typically measured alpha desynchronisation while participants anticipated a public speech (Davidson et al., 2000), reading anxious and sad narratives (Heller et al., 1997) or during resting periods (Heller et al., 1997; Shackman, McMenamin, Maxwell, Greischar, & Davidson, 2009). In general, eventrelated desynchronisation in alpha power is augmented in anxious participants (e.g., Knyazev, Savostyanov, & Levin, 2006). The impact of emotion on cognitive systems has also been linked to incidental memory performance. In order to assess whether emotional content has a lasting impact on memory, Herbert et al. (2008) and Kissler, Herbert, Peyk, & Junghöfer (2007); Kissler et al. (2009) repeatedly assessed individuals’ incidental memory performance via a free recall test and found differences in recall depending on emotional content. In general, emotional words were recalled more often than neutral words. As memory performance benefits from increased semantic processing (Chwilla, Brown, & Hagoort, 1995), better memory performance for emotional stimuli might reflect better semantic processing. Previous studies with healthy participants reported differential effect of memory encoding of emotional stimuli (e.g., Dolcos & Cabeza, 2002; Kissler et al., 2009), showing that attention biases might also be traced by a behavioural measures. In a study by Jay, Caldwell-Harris, and King (2008), subjects had to recall neutral, emotional (e.g., cuddle, love, sick, kill) and taboo words (e.g., nigger, pussy, slut, anus) under conditions of shallow and deep encoding. They found superior recall for taboo words compared to neutral and emotional words regardless of the type of encoding. Moreover, compared to neutral words, emotional and taboo words did not benefit from deep processing. The authors concluded that the arousing nature of taboo words accounts for the superior memory performance regardless of task instructions, indicating that for arousing words, deep encoding is not
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necessary for facilitating the storage of information (Jay, Caldwell-Harris, and King, 2008). As emotional content of words has been shown to modulate ERP components (e.g., Kissler et al., 2009) and taboo words in the study by Jay and colleagues (2008) resemble social-negative words in the present study, we thought to extend previous research. To date, the impact of anxiety on memory performance yielded mixed results (Heinrichs & Hofmann, 2001). In our view, the absence of a clear memory effect for emotional words in social anxiety might be due to a failure of matching stimuli to the core anxiety. Therefore, we included a free recall task to (1) assess whether emotional content of words modulates incidental memory performance and (2) whether this modulation is associated with social anxiety when socially threatening stimuli are presented. To our knowledge, no study has assessed eventrelated alpha activity in social phobia to date. Therefore, we aimed at disentangling early and later effects of emotion processing in SAD via measuring both ERPs and oscillatory activity, which selectively reflect cortical hypervigilance (e.g., Kolassa et al., 2009; Mueller et al. 2009) and avoidance. To date, behavioural results indicate more specific biases towards stimuli with social threat-related emotional connotations. ERP studies have proposed that very early unspecific hyperarousal is followed by more specific biases in the subsequent processing stages. The goal of this study was to test this assumption by analysing ERPs and alpha oscillations in response to emotional words. Given that most humans are socialised via verbal learning processes, words should equally serve as motivationally relevant stimuli. Although there is considerable evidence that emotional words modulate ERPs (Kissler, Assadollahi, & Herbert, 2006; Schacht & Sommer, 2009), they have not yet been used in SAD. The main advantage of word stimuli is that they may allow a finely graduated semantic differentiation than faces, which is relevant when testing the specificity hypothesis. We used four types of emotional words, i.e., positive, neutral, physically and socially threatening words. Socially threatening words were represented by swear words.
Swear words have a strong self-reference and social connotation (Wabnitz et al., 2012). These aspects make them useful to study social threat processing, as it can be assumed that they act as cues for an endangered social integrity (i.e., rank or group affiliation). An endangered social integrity may in turn lead to social exclusion (Leary, 1990; Williams, 2001) that constitutes a main concern for healthy individuals but in particular for social phobics. In a previous study we found that responses to swear words were associated with a specific pattern of cortical activity as they captured more attentional resources than positive and physically threatening words in the P1 time window in healthy participants (Wabnitz et al., 2012). These findings suggest that socially threatening words are processed in a manner similar to other emotional words in healthy subjects. However, as healthy subjects were not thought to present an attention bias to a specific negative word class (social vs. physical threat), specific attention effects had to be studied in a sample that might be prone to a certain threat (e.g., social threat cue). Thus, the present study thought to extent these findings to socially anxious participants. We applied a passive reading paradigm, recently developed and evaluated in our laboratory (Wabnitz et al., 2012), to study attentional effects on evoked potentials as well as the alpha activity. As already mentioned, conflicting findings obtained with the dot-probe or the emotional Stroop task might be due to low ecological validity and task demands of these tasks. To assess whether this confusion might be due to a general lack of validity or task-specific attention processes, we abstained from a complex task demand (e.g., switching between colours and valence within the dot-probe task or switching attention between left and right or up and down within the dot-probe task) to obtain a “pure” measure of attention. Therefore, the current paradigm aims at tapping in pure attention processes within the individual and not within the task at hand. Given the findings that individuals with SAD are hypervigilant to threat cues at early stages of information processing and at the same time show avoidance of COGNITION AND EMOTION, 2015
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these cues at later stages (Bar-Haim et al., 2007), we hypothesised that (1) these individuals would show enhanced processing of social threat cues at a behavioural and cortical level; (2) the specificity of this hypervigilance would increase in consecutive ERP components from unspecific (P100) to increased specificity over consecutive stages (EPN and N400) represented by a higher level of cortical differentiation (i.e., different ERP amplitudes) between word classes; and (3) would be followed by cortical avoidance (illustrated by enhanced alpha activity) at later stages of word processing. With respect to memory performance, we hypothesised that social-negative words would show the highest recall rate regardless of anxiety.
METHOD Participants Participants were recruited through campus bulletin boards (healthy controls) and through the Bielefeld University Psychotherapy Outpatient Clinic (SAD subjects). According to measure and criteria specified by Oldfield (1971) all participants were right-handed. All participants underwent an extensive clinical assessment administered by an M.Sc. level-trained clinically psychologist. Current diagnoses of social phobia and co-morbid DSM-IV axis one disorders were assessed with the Mini-international Neuropsychiatric Interview (MINI; Sheehan et al., 1998). In total, of the 43 participants with normal or corrected-to-normal vision who were assessed for eligibility, 22 met the inclusion criterion for the clinical group and fulfilled the DSM-IV criteria for current “SAD”. The remaining 21 participants did not meet a principal DSM-IV lifetime diagnosis and were assigned to the healthy control group (“Controls”; exclusion criterion was a current DSM-IV diagnosis). Co-morbid DSM-IV diagnoses, based on assessment with the MINI, in the phobics group were depression (2), dysthymia (1) and panic disorder and agoraphobia (2). All subjects were unmedicated at the time of testing. In the clinical group, one participant reported
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prior in-patient, two participants reported prior outpatient treatment. In the control group no participant reported psychiatric or psychological treatment during lifetime. Exclusion criteria for both groups were: (1) suicidal intent or ideation; (2) current substance abuse or dependence; and (3) current or past schizophrenia, bipolar disorder, or mental disorder mainly due to a medical condition. No other inclusion or exclusion criteria were applied. Due to excessive artefacts in the EEG recordings, the data of two participants in the phobics group and one participant in the control group were excluded from further analyses, resulting in 20 participants per group. There were no significant differences between both groups with respect to age, sex, education or maternal status (Table 1). Regarding general psychopathology and social phobic symptoms, participants of the phobic group reported more depressive symptoms, aversive and potential traumatising life events and social phobic symptoms than the control group (see Table 1). These symptoms were assessed with the Social Phobia Scale/Social Interaction Anxiety Scale (SPS/SIAS; Heinrichs et al., 2002), the Childhood Trauma Questionnaire (CTQ; Wingenfeld et al., 2010), the Brief Symptom Inventory (BSI; Franke & Derogatis, 2000), the Fragebogen belastender Sozialerfahrungen (FBS; questionnaire of stressful social experiences; Sansen, Iffland, Catani, & Neuner, 2013), and the Beck Depression Inventory – II (BDI; Beck, Ward, & Mendelson, 1961). All scales were administered in German (Table 1). Internal consistency (Cronbachs α) for the German translations of these questionnaires in the present study were high (SIAS: α = 0.84; SPS: α = 0.95; BDI: α = 0.94; FBS: α = 0.89; BSI: α = 0.97; CTQ: all scales α ≥ 0.85). With respect to differences between both groups in general psychopathology and potential traumatising life events, correlation analyses were conducted to assess potential correlations between these variables and ERP components. No correlations reached statistical significance (all ps > .63). All participants signed the informed consent. The study protocol was approved by the local ethics committee.
AFFECTIVE WORDS AND SOCIAL PHOBIA
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Stimulus material Experimental stimuli consisted of 100 German words (only nouns) from four different categories (neutral, positive, physical-negative and socialnegative; Wabnitz, Martens, & Neuner, 2012). As social-negative words were represented by swear words (i.e., nouns) all remaining words had to be noun words as well in order to match word categories. Positive, neutral and physicalnegative words were chosen out of 200 nouns from the Berlin Affective Word List Reloaded (BAWL-R; Võ et al., 2009). As mentioned above, social-negative words were represented by swear words (e.g., Hurensohn, Arschloch, Missgeburt; the tentative English translation would be son of a bitch, asshole, freak). The physical-negative words (e.g., Schnitt, Kopfschuss, Verbrennung; translated with cut, shot to the head, burn) should elicit physical threat, whereas the swear words should elicit social threat. Positive words described a broad range of positive and eligible actions, places or conditions
(e.g., Sex, Glück, Urlaub; translated as sex, luck and holiday), and words that are less arousing and valent were chosen as neutral words (e.g., Lesesaal, Lampe; translated as reading room and lamp). All words were previously rated by 55 university students in return for course credits or financial bonus. Ratings were obtained on three dimensions (valence, arousal and dominance) by use of the German version of the Self-Assessment Manikin (SAM; Bradley & Lang, 1994) as well as a rating for perceived threat for physical and social integrity assessed on a 5-point Likert scale lasting from 1 (very low physical/social threatening) to 5 (very high physical/social threatening). The words differed significantly with respect to the categoryspecific valence ratings from each other, only the valence ratings of physical-negative and socialnegative words were similar to each other. There was no significant difference in arousal ratings between positive, physical-negative and socialnegative words. However, all three categories were significantly more arousing than neutral
Table 1. Demographic and clinical characteristics for phobics and control participants
Phobics (n = 20) Demographic data Sex (male) Age (years) Education (years) Marital status (married) Clinical data FBS events childhood FBS events adolescents BDI score SPS score SIAS score BSI score CTQ score Emotional abuse Emotional neglect Physical abuse Physical neglect Sexual abuse
Controls (n = 20)
pa
ESb
N (%) M (SD) M (SD) N (%)
9 27.84 14.75 1
(45.0) (9.14) (2.45) (5.0)
11 26.71 15.14 2
(52.38) (9.86) (2.54) (9.5)
0.53 0.71 0.62 0.48
0.04 0.12 0.16 0.14
M M M M M M M M M M M M
8.20 8.65 19.30 40.16 48.96 1.28 40.65 9.85 12.70 5.25 7.50 5.35
(4.03) (4.70) (10.80) (11.46) (11.66) (0.64) (11.25) (4.40) (5.12) (0.44) (2.69) (0.81)
3.38 4.05 4.47 12.09 19.85 0.33 30.86 6.57 7.71 5.33 5.95 5.28
(2.48) (2.82) (3.30) (9.84) (12.70) (0.28) (7.42) (2.84) (2.75) (0.97) (1.20) (1.30)
Cognition and Emotion Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/pcem20
Written threat: Electrophysiological evidence for an attention bias to affective words in social anxiety disorder a
b
a
Pascal Wabnitz , Ulla Martens & Frank Neuner a
Department of Clinical Psychology and Psychotherapy, University of Bielefeld, Bielefeld, Germany b
Department of Cognitive Psychology, University of Osnabrück, Osnabrück, Germany Published online: 26 Mar 2015.
Click for updates To cite this article: Pascal Wabnitz, Ulla Martens & Frank Neuner (2015): Written threat: Electrophysiological evidence for an attention bias to affective words in social anxiety disorder, Cognition and Emotion, DOI: 10.1080/02699931.2015.1019837 To link to this article: http://dx.doi.org/10.1080/02699931.2015.1019837
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions
COGNITION AND EMOTION, 2015 http://dx.doi.org/10.1080/02699931.2015.1019837
Written threat: Electrophysiological evidence for an attention bias to affective words in social anxiety disorder Pascal Wabnitz1, Ulla Martens2, and Frank Neuner1 1
Department of Clinical Psychology and Psychotherapy, University of Bielefeld, Bielefeld, Germany Department of Cognitive Psychology, University of Osnabrück, Osnabrück, Germany
2
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(Received 3 February 2014; accepted 11 February 2015)
Social anxiety disorder (SAD) is associated with heightened sensitivity to threat cues, typically represented by emotional facial expressions. To examine if this bias can be transferred to a general hypersensitivity or whether it is specific to disorder relevant cues, we investigated electrophysiological correlates of emotional word processing (alpha activity and event-related potentials) in 20 healthy participants and 20 participants with SAD. The experimental task was a silent reading of neutral, positive, physically threatening and socially threatening words (the latter were abusive swear words) while responding to a randomly presented dot. Subsequently, all participants were asked to recall as many words as possible during an unexpected recall test. Participants with SAD showed blunted sensory processing followed by a rapid processing of emotional words during early stages (early posterior negativity – EPN). At later stages, all participants showed enhanced processing of negative (physically and socially threatening) compared to neutral and positive words (N400). Moreover, at later processing stages alpha activity was increased specifically for negative words in participants with SAD but not in healthy controls. Recall of emotional words for all subjects was best for socially threatening words, followed by negative and positive words irrespective of social anxiety. The present findings indicate that SAD is associated with abnormalities in emotional word processing characterised by early hypervigilance to emotional cues followed by cognitive avoidance at later processing stages. Most importantly, the specificity of these attentional biases seems to change as a function of time with a general emotional bias at early and a more specific bias at later processing stages. Keywords: Emotion; Word processing; Event-related potentials; Swear words; Social anxiety disorder.
Social anxiety disorder (SAD) is one of the most common psychiatric disorders (Kessler et al., 2005) and it is characterised by a persistent fear and avoidance of social situations (Buckner, Bernert, Cromer, Joiner, & Schmidt, 2008; Buckner,
Eggleston, & Schmidt, 2006). It is related to abnormalities in several cognitive processes (Amir, Elias, Klumpp, & Przeworski, 2003; Clark & Wells, 1995; Rapee & Heimberg, 1997), in particular in attention, memory and interpretation
Correspondence should be addressed to: Pascal Wabnitz, Department of Psychology, Bielefeld University, Postbox 100131, 33501 Bielefeld, Germany. E-mail: [email protected] © 2015 Taylor & Francis
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of ambiguous and threatening social information (for reviews see Heinrichs & Hofmann, 2001; Pishyar, Harris, & Menzies, 2004). A general hypervigilance towards potentially threatening information has been well-documented for participants with SAD (Bar-Haim, Lamy, Pergamin, Bakermans-Kranenburg, & van Ijzendoorn, 2007; Pishyar et al., 2004); however, the specificity of this effect is under debate. While a bias towards threat cues is a common characteristic of anxiety disorders, it is unclear whether this bias only occurs for stimuli that represent the core of the subjective anxiety (specificity), or whether it reflects a general state of hypervigilance to all incoming stimuli (general; Heinrichs & Hofmann, 2001). With respect to social anxiety features of this core are the fear of being exposed to an audience that might evaluate the person in a negative way (Rapee & Heimberg, 1997) as well as the fear of losing one’s social status or being rejected leading to avoidance behaviour (Clark & Wells, 1995). Following the schema congruency hypothesis (Beck, Emery, & Greenberg, 1985), Williams, Mathews, and MacLeod (1996) predicted differential biases in participants with anxiety disorders depending on the participants’ personal schemas (defined as cognitive, well-organised negative or positive representation of oneself or the environment for the rapid processing of incoming information) as well as systematics in diagnoses (see also Mathews & MacLeod, 1994). Tests of this assumption using a variety of experimental paradigms, including behavioural and physiological indicators, yielded mixed results with regard to the specificity of threat cues in SAD. Several studies have applied the Stroop task that determines an attentional bias to threat cues by observing the latencies in the identification of the colour of emotional words (MacLeod, 1991). Some studies found unspecific biases towards all emotional words regardless of the diagnosis (Asmundson & Stein, 1994), whilst other studies did confirm disorder-specific effects (Becker, Rinck, Margraf, & Roth, 2001; Hope, Rapee, Heimberg, & Dombeck, 1990; Mattia, Heimberg, & Hope, 1993). For instance, Becker et al. (2001)
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reported a distinct bias to speech-related words (e.g., talk, stutter, blush) in participants with SAD. The dot-probe task is a different and potentially more valid paradigm for the assessment of attentional biases (MacLeod, Mathews, & Tata, 1986). In this task, an attentional bias to threat stimuli is identified through faster reaction times to probes replacing a threat-related cue (emotional facial expression or emotional word) than to probes replacing a neutral cue (Cisler, Olatunji, & Lohr, 2009; Mogg & Bradley, 1998). Especially in SAD, attention biases to emotional stimuli (angry facial expressions) have been confirmed in various studies using the dot-probe task (Bradley, Mogg, Falla, & Hamilton, 1998; Bradley, Mogg, & Millar, 2000; Mogg & Bradley, 2002). However, there are mixed results regarding the specificity of this effect, as some studies have found an unspecific bias to all types of emotional faces regardless of the specific emotion (Mogg, Garner, & Bradley, 2007; Wilson & MacLeod, 2003), while others have identified more specific biases of SAD towards (social) threat words (Asmundson & Stein, 1994) or disgust/judgmental facial expressions (Pishyar et al., 2004). Summing up, different paradigms have been applied to study attention biases in recent years (see Cisler, Bacon, & Williams, 2009, for an overview), all tapping in discrete cognitive processes and do not inevitably intercorrelate (Cisler, Bacon, et al., 2009). The present study aimed at disentangling the specificity of attention biases in SAD compared to healthy controls (i.e., subjects without a psychiatric disorder) using four different sources of information [event-related potentials (ERP), oscillatory brain activity, behavioural measures and memory performance]. For this purpose we relied on a new paradigm evaluated in one of our previous studies (Wabnitz, Martens, & Neuner, 2012) that does not specifically guide subjects’ attention to a certain artificial task (i.e., emotional Stroop or dot-probe task) but leaves the guidance of attention to the subjects’ motivation. This refers to the notion that social anxious subjects direct their attention to signals of social disapproval or rejection whenever they anticipate negative evaluations (Rapee & Heimberg, 1997). Thus, social anxious
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subjects instantly have a motivation to detect social threatening cues to avoid social humiliation or rejection. This hypervigilance is assumed to be followed by avoidance of threat cues (Clark, 2001), but is far from understood (Heinrichs & Hofmann, 2001). More importantly, in our view previous paradigms hold a low ecological validity, since their results not only illustrate pure attention processes but effects of certain, sometimes artificial, tasks (i.e., emotional Stroop). In fact, current research points to problems regarding the validity and reliability of posttraumatic stress disorder (PTSD) dot probe (Schmukle, 2005) and the emotional Stroop task (Cisler, Bacon, et al., 2009). Specificity of attention biases may exist across various anxiety disorders, but this cannot be answered within the present study.
ERP components associated with emotional processing While the dot-probe and the Stroop task rely on behavioural responses for measuring attention (biases), other measures are thought to directly tap into stimulus processing via measuring electrocortical responses to the presentation of a stimulus. For instance, ERPs associated with various stages of visual stimulus processing have been associated with anxiety. The amplitude of a positive-going voltage fluctuation approximately 100 ms after stimulus onset (P100) increases with the amount of attention allocated to the stimulus (e.g., Luck, Woodman, & Vogel, 2000). Studies that simultaneously presented neutral and emotional face pairs that were followed by a horizontal or vertical bar flashed to either left or right side of the screen replacing one of the face pairs reported larger P100 amplitudes when the bar replaced a fearful face than when it replaced a neutral face (e.g., Pourtois, Den, Grandjean, Sander, & Vuillemier, 2005) indicating that the P100 may be sensitive to the emotional salience of the stimulus. Hence, enlarged P100 amplitudes in social phobics may indicate vigilance for emotional words. However, whether this hypervigilance is evident for all words or only for those who
transport a socially threatening connotation is subject to the present study. Following the P100, a negative deflection that occurs at posterior sites around 200 ms after stimulus onset (early posterior negativity – EPN) differentiates between neutral and emotional stimuli (e.g., Schupp, Flaisch, Stockburger, & Junghöfer, 2006). The EPN is linked to increased emotional processing (Schupp, Junghöfer, Weike, & Hamm, 2003a, 2003b, 2004) and arises independent from instructed attention (Kissler, Herbert, Winkler, & Junghöfer, 2009). While the P100 has been suggested to be associated with general vigilance, enhanced EPN amplitudes to emotional stimuli reflects spontaneous selective processing of the emotional significance of the stimulus (Kissler et al., 2009). Somewhat later in the processing stream, after about 400 ms, a negative potential (N400) that has been associated with semantic integration based on subjects’ expectations or the context and structure of a sentence (Kutas & Federmeier, 2000) can also be modulated by the emotional content of a stimulus. Herbert, Junghofer, and Kissler (2008) reported attenuated N400 amplitudes by pleasant words, possibly indicating facilitated semantic integration of pleasant in contrast to unpleasant words. Thus, while sensory (P100) and automatic but selective processing (EPN) appears even without conscious processing, enhanced N400 amplitudes to emotional stimuli reflect somehow more elaborated processing (i.e., semantic or mood-dependent integration of the stimulus). Taken together, measuring ERPs allows a fine analysis of electrophysiological correlates of attention biases in a temporal sequence, due to its excellent temporal resolution. Assessing different components offers an insight in functional different levels of processing emotional stimuli. Applying these measures to the study of social anxiety sheds further light on the processing of emotional stimuli. In a series of studies, Kolassa, Musial, and Miltner (2007) reported generally increased visual P1 amplitudes in SAD participants to face stimuli (happy, sad, angry, neutral) compared to healthy participants and spider phobics. In line with this COGNITION AND EMOTION, 2015
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finding, Mühlberger, Wieser, Herrmann, Weyers, Tröger, and Pauli (2009) found that while socially anxious participants showed enhanced P1 amplitudes in response to all faces, the emotional modulation of the EPN may be specific for emotional faces only. However, Mühlberger et al. (2009) used artificial faces, thus limiting the generalisability of theirs results.
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Alpha desynchronisation in anxious individuals Another form of analysing electrophysiological responses to threat cues is the stimulus-dependent modulation of the oscillatory brain activity that is known to play are role in human cognition with varying behavioural correlates (e.g., Kahana, 2006). In particular, alpha-frequency activations are directly associated with distinct cognitive processes (i.e., inhibition). Cognitive inhibition can be mapped to distinct regions of the prefrontal cortex (PFC; Aron, Robbins, & Poldrack, 2004), a region that is thought to exert its inhibitory control on subcortical regions to implement executive control (Aron et al., 2004). This functional localisation seems to be limited to the right PFC and is thought to be associated with frontal alpha oscillations in the human EEG. However, current conceptualisations propose that high alpha-oscillatory activity may reflect the inhibition and disengagement of task-irrelevant cortical areas, while reduced alpha activity reflects active neuronal processing (see Palva & Palva, 2007). The asymmetry of frontal alpha activity has also been hypothesised to reflect a model of different emotional involvement during stimulus processing (Davidson, Marshall, Tomarken, & Henriques, 2000). In particular, while alpha desynchronisation over left regions of the PFC reflects approachrelated behaviour tendencies, right-sided alpha desynchronisation is associated with withdrawalrelated behaviour and emotions (Davidson et al., 2000; Heller, Nitschke, Etienne, & Miller, 1997). In fact, right-sided PFC activity (alpha desynchronisation) not only increased in anxious participants while listening to fearful and sad narratives compared to non-anxious participants (Heller
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et al., 1997), but also the triggering of anxiety was reported to account for a substantial proportion of variance of right-sided PFC activity (Davidson et al., 2000). Research assessing oscillations in frontal regions of the brain typically measured alpha desynchronisation while participants anticipated a public speech (Davidson et al., 2000), reading anxious and sad narratives (Heller et al., 1997) or during resting periods (Heller et al., 1997; Shackman, McMenamin, Maxwell, Greischar, & Davidson, 2009). In general, eventrelated desynchronisation in alpha power is augmented in anxious participants (e.g., Knyazev, Savostyanov, & Levin, 2006). The impact of emotion on cognitive systems has also been linked to incidental memory performance. In order to assess whether emotional content has a lasting impact on memory, Herbert et al. (2008) and Kissler, Herbert, Peyk, & Junghöfer (2007); Kissler et al. (2009) repeatedly assessed individuals’ incidental memory performance via a free recall test and found differences in recall depending on emotional content. In general, emotional words were recalled more often than neutral words. As memory performance benefits from increased semantic processing (Chwilla, Brown, & Hagoort, 1995), better memory performance for emotional stimuli might reflect better semantic processing. Previous studies with healthy participants reported differential effect of memory encoding of emotional stimuli (e.g., Dolcos & Cabeza, 2002; Kissler et al., 2009), showing that attention biases might also be traced by a behavioural measures. In a study by Jay, Caldwell-Harris, and King (2008), subjects had to recall neutral, emotional (e.g., cuddle, love, sick, kill) and taboo words (e.g., nigger, pussy, slut, anus) under conditions of shallow and deep encoding. They found superior recall for taboo words compared to neutral and emotional words regardless of the type of encoding. Moreover, compared to neutral words, emotional and taboo words did not benefit from deep processing. The authors concluded that the arousing nature of taboo words accounts for the superior memory performance regardless of task instructions, indicating that for arousing words, deep encoding is not
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necessary for facilitating the storage of information (Jay, Caldwell-Harris, and King, 2008). As emotional content of words has been shown to modulate ERP components (e.g., Kissler et al., 2009) and taboo words in the study by Jay and colleagues (2008) resemble social-negative words in the present study, we thought to extend previous research. To date, the impact of anxiety on memory performance yielded mixed results (Heinrichs & Hofmann, 2001). In our view, the absence of a clear memory effect for emotional words in social anxiety might be due to a failure of matching stimuli to the core anxiety. Therefore, we included a free recall task to (1) assess whether emotional content of words modulates incidental memory performance and (2) whether this modulation is associated with social anxiety when socially threatening stimuli are presented. To our knowledge, no study has assessed eventrelated alpha activity in social phobia to date. Therefore, we aimed at disentangling early and later effects of emotion processing in SAD via measuring both ERPs and oscillatory activity, which selectively reflect cortical hypervigilance (e.g., Kolassa et al., 2009; Mueller et al. 2009) and avoidance. To date, behavioural results indicate more specific biases towards stimuli with social threat-related emotional connotations. ERP studies have proposed that very early unspecific hyperarousal is followed by more specific biases in the subsequent processing stages. The goal of this study was to test this assumption by analysing ERPs and alpha oscillations in response to emotional words. Given that most humans are socialised via verbal learning processes, words should equally serve as motivationally relevant stimuli. Although there is considerable evidence that emotional words modulate ERPs (Kissler, Assadollahi, & Herbert, 2006; Schacht & Sommer, 2009), they have not yet been used in SAD. The main advantage of word stimuli is that they may allow a finely graduated semantic differentiation than faces, which is relevant when testing the specificity hypothesis. We used four types of emotional words, i.e., positive, neutral, physically and socially threatening words. Socially threatening words were represented by swear words.
Swear words have a strong self-reference and social connotation (Wabnitz et al., 2012). These aspects make them useful to study social threat processing, as it can be assumed that they act as cues for an endangered social integrity (i.e., rank or group affiliation). An endangered social integrity may in turn lead to social exclusion (Leary, 1990; Williams, 2001) that constitutes a main concern for healthy individuals but in particular for social phobics. In a previous study we found that responses to swear words were associated with a specific pattern of cortical activity as they captured more attentional resources than positive and physically threatening words in the P1 time window in healthy participants (Wabnitz et al., 2012). These findings suggest that socially threatening words are processed in a manner similar to other emotional words in healthy subjects. However, as healthy subjects were not thought to present an attention bias to a specific negative word class (social vs. physical threat), specific attention effects had to be studied in a sample that might be prone to a certain threat (e.g., social threat cue). Thus, the present study thought to extent these findings to socially anxious participants. We applied a passive reading paradigm, recently developed and evaluated in our laboratory (Wabnitz et al., 2012), to study attentional effects on evoked potentials as well as the alpha activity. As already mentioned, conflicting findings obtained with the dot-probe or the emotional Stroop task might be due to low ecological validity and task demands of these tasks. To assess whether this confusion might be due to a general lack of validity or task-specific attention processes, we abstained from a complex task demand (e.g., switching between colours and valence within the dot-probe task or switching attention between left and right or up and down within the dot-probe task) to obtain a “pure” measure of attention. Therefore, the current paradigm aims at tapping in pure attention processes within the individual and not within the task at hand. Given the findings that individuals with SAD are hypervigilant to threat cues at early stages of information processing and at the same time show avoidance of COGNITION AND EMOTION, 2015
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these cues at later stages (Bar-Haim et al., 2007), we hypothesised that (1) these individuals would show enhanced processing of social threat cues at a behavioural and cortical level; (2) the specificity of this hypervigilance would increase in consecutive ERP components from unspecific (P100) to increased specificity over consecutive stages (EPN and N400) represented by a higher level of cortical differentiation (i.e., different ERP amplitudes) between word classes; and (3) would be followed by cortical avoidance (illustrated by enhanced alpha activity) at later stages of word processing. With respect to memory performance, we hypothesised that social-negative words would show the highest recall rate regardless of anxiety.
METHOD Participants Participants were recruited through campus bulletin boards (healthy controls) and through the Bielefeld University Psychotherapy Outpatient Clinic (SAD subjects). According to measure and criteria specified by Oldfield (1971) all participants were right-handed. All participants underwent an extensive clinical assessment administered by an M.Sc. level-trained clinically psychologist. Current diagnoses of social phobia and co-morbid DSM-IV axis one disorders were assessed with the Mini-international Neuropsychiatric Interview (MINI; Sheehan et al., 1998). In total, of the 43 participants with normal or corrected-to-normal vision who were assessed for eligibility, 22 met the inclusion criterion for the clinical group and fulfilled the DSM-IV criteria for current “SAD”. The remaining 21 participants did not meet a principal DSM-IV lifetime diagnosis and were assigned to the healthy control group (“Controls”; exclusion criterion was a current DSM-IV diagnosis). Co-morbid DSM-IV diagnoses, based on assessment with the MINI, in the phobics group were depression (2), dysthymia (1) and panic disorder and agoraphobia (2). All subjects were unmedicated at the time of testing. In the clinical group, one participant reported
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prior in-patient, two participants reported prior outpatient treatment. In the control group no participant reported psychiatric or psychological treatment during lifetime. Exclusion criteria for both groups were: (1) suicidal intent or ideation; (2) current substance abuse or dependence; and (3) current or past schizophrenia, bipolar disorder, or mental disorder mainly due to a medical condition. No other inclusion or exclusion criteria were applied. Due to excessive artefacts in the EEG recordings, the data of two participants in the phobics group and one participant in the control group were excluded from further analyses, resulting in 20 participants per group. There were no significant differences between both groups with respect to age, sex, education or maternal status (Table 1). Regarding general psychopathology and social phobic symptoms, participants of the phobic group reported more depressive symptoms, aversive and potential traumatising life events and social phobic symptoms than the control group (see Table 1). These symptoms were assessed with the Social Phobia Scale/Social Interaction Anxiety Scale (SPS/SIAS; Heinrichs et al., 2002), the Childhood Trauma Questionnaire (CTQ; Wingenfeld et al., 2010), the Brief Symptom Inventory (BSI; Franke & Derogatis, 2000), the Fragebogen belastender Sozialerfahrungen (FBS; questionnaire of stressful social experiences; Sansen, Iffland, Catani, & Neuner, 2013), and the Beck Depression Inventory – II (BDI; Beck, Ward, & Mendelson, 1961). All scales were administered in German (Table 1). Internal consistency (Cronbachs α) for the German translations of these questionnaires in the present study were high (SIAS: α = 0.84; SPS: α = 0.95; BDI: α = 0.94; FBS: α = 0.89; BSI: α = 0.97; CTQ: all scales α ≥ 0.85). With respect to differences between both groups in general psychopathology and potential traumatising life events, correlation analyses were conducted to assess potential correlations between these variables and ERP components. No correlations reached statistical significance (all ps > .63). All participants signed the informed consent. The study protocol was approved by the local ethics committee.
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Stimulus material Experimental stimuli consisted of 100 German words (only nouns) from four different categories (neutral, positive, physical-negative and socialnegative; Wabnitz, Martens, & Neuner, 2012). As social-negative words were represented by swear words (i.e., nouns) all remaining words had to be noun words as well in order to match word categories. Positive, neutral and physicalnegative words were chosen out of 200 nouns from the Berlin Affective Word List Reloaded (BAWL-R; Võ et al., 2009). As mentioned above, social-negative words were represented by swear words (e.g., Hurensohn, Arschloch, Missgeburt; the tentative English translation would be son of a bitch, asshole, freak). The physical-negative words (e.g., Schnitt, Kopfschuss, Verbrennung; translated with cut, shot to the head, burn) should elicit physical threat, whereas the swear words should elicit social threat. Positive words described a broad range of positive and eligible actions, places or conditions
(e.g., Sex, Glück, Urlaub; translated as sex, luck and holiday), and words that are less arousing and valent were chosen as neutral words (e.g., Lesesaal, Lampe; translated as reading room and lamp). All words were previously rated by 55 university students in return for course credits or financial bonus. Ratings were obtained on three dimensions (valence, arousal and dominance) by use of the German version of the Self-Assessment Manikin (SAM; Bradley & Lang, 1994) as well as a rating for perceived threat for physical and social integrity assessed on a 5-point Likert scale lasting from 1 (very low physical/social threatening) to 5 (very high physical/social threatening). The words differed significantly with respect to the categoryspecific valence ratings from each other, only the valence ratings of physical-negative and socialnegative words were similar to each other. There was no significant difference in arousal ratings between positive, physical-negative and socialnegative words. However, all three categories were significantly more arousing than neutral
Table 1. Demographic and clinical characteristics for phobics and control participants
Phobics (n = 20) Demographic data Sex (male) Age (years) Education (years) Marital status (married) Clinical data FBS events childhood FBS events adolescents BDI score SPS score SIAS score BSI score CTQ score Emotional abuse Emotional neglect Physical abuse Physical neglect Sexual abuse
Controls (n = 20)
pa
ESb
N (%) M (SD) M (SD) N (%)
9 27.84 14.75 1
(45.0) (9.14) (2.45) (5.0)
11 26.71 15.14 2
(52.38) (9.86) (2.54) (9.5)
0.53 0.71 0.62 0.48
0.04 0.12 0.16 0.14
M M M M M M M M M M M M
8.20 8.65 19.30 40.16 48.96 1.28 40.65 9.85 12.70 5.25 7.50 5.35
(4.03) (4.70) (10.80) (11.46) (11.66) (0.64) (11.25) (4.40) (5.12) (0.44) (2.69) (0.81)
3.38 4.05 4.47 12.09 19.85 0.33 30.86 6.57 7.71 5.33 5.95 5.28
(2.48) (2.82) (3.30) (9.84) (12.70) (0.28) (7.42) (2.84) (2.75) (0.97) (1.20) (1.30)
