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Purpose: Psychogenic nonepileptic seizures (PNES) have long been considered as paroxysmal dissociative symptoms characterized by an alteration of attentional functions caused by severe stress or trauma. Although interpersonal trauma is common in PNES, the proposed relation between trauma and attentional functions remains under explored. We examined the attentional processing of social threat in PNES in relation to interpersonal trauma and acute psychological stress.
Methods: A masked emotional Stroop test, comparing color-naming latencies for backwardly masked angry, neutral, and happy faces, was administered to 19 unmedicated patients with PNES and 20 matched healthy controls, at baseline and in a stress condition. Stress was induced by means of the Trier Social Stress Test and physiologic stress parameters, such as heart rate variability (HRV) and cortisol, were measured throughout the experiment.
Results: No group differences related to the acute stress induction were found. Compared to controls, however, patients displayed a positive attentional bias for masked angry faces at baseline, which was correlated to self-reported sexual trauma. Moreover, patients showed lower HRV at baseline and during recovery.
Discussion: These findings are suggestive of a state of hypervigilance in patients with PNES. The relation with self-reported trauma, moreover, offers the first evidence linking psychological risk factors to altered information processing in PNES.
Psychogenic nonepileptic seizures (PNES) can be defined as paroxysmal involuntary behavioral patterns that mimic epileptic events but for which no organic cause can be identified. PNES lack ictal epileptiform activity in the brain and are thought to be mediated by psychological factors (World Health Organization, 1993; American Psychiatric Association, 1994). They are characterized by a sudden and time-limited alteration of consciousness and are associated with a disturbance in controlling motor, sensory, autonomic, cognitive, emotional, and/or behavioral functions (e.g., Kuyk et al., 1999).
PNES form one of the major manifestations of conversion disorder as described in the DSM-IV (American Psychiatric Association, 1994). In ICD-10 (World Health Organization, 1993) PNES are categorized under dissociative disorders, more specifically under dissociative convulsions. Both classification systems specify that the etiology of PNES is related to psychological stress factors.
Conversion/dissociative symptoms such as PNES have long been regarded as attention-related complaints caused by psychological stress factors (Janet, 1907; Ludwig, 1972; Brown, 2004). Pierre Janet (1907); for example, proposed that these symptoms result from an impairment of the attentional functions caused by severe stress or trauma. There is empirical evidence for altered attentional functioning in trauma-related disorders. For example, patients with posttraumatic stress disorder (PTSD) commonly allocate their attention toward trauma-related stimuli, as evidenced by studies using the emotional Stroop task (for reviews see McNally, 1996; Buckley et al., 2000). These studies demonstrated that patients with PTSD are slower in color-naming trauma-specific threat words, as compared to trauma-unrelated words indicating that attention is allocated automatically toward the threat-value of the word (Williams et al., 1996).
These findings may be relevant for our understanding of the theorized impairments of attentional functions in patients with PNES, although studies on stress and attentional functioning in patients with PNES are scarce. Compared to healthy control groups, patients with PNES show decreased attentional functioning in standard neuropsychologic test batteries (for a review see Cragar et al., 2002) There is, however, only one study in which the effects of stress on cognitive functions in PNES were examined. Bendefeldt et al. (1976) investigated attentional processing in 17 patients with conversion symptoms (10 had PNES) and found some evidence for worsened attentional processing (compared to a nonpsychotic patient control group) in both baseline and stress conditions, using a face-recognition task and a mental switch-task. Only the processing of neutral stimuli was, however, assessed. The processing of stimuli relevant to interpersonal trauma, such as trauma-related words or threatening faces, has not been examined. In addition, no studies have addressed the relationship between interpersonal trauma and attentional deficits in PNES.
With the present study we aimed to test the proposed relationship between attentional processing of social threat stimuli and psychological stress factors in a sample of PNES patients. We were specifically interested in testing the hypothesis that patients with PNES automatically allocate their attentional resources toward social threat stimuli. To test this hypothesis, patients and matched healthy controls were administered a masked emotional Stroop task, in which pictures of angry, happy, and neutral facial expressions were presented backwardly masked and participants were asked to color-name the masks (Van Honk et al., 1998, 2000; Putman et al., 2004; Hermans et al., 2006, 2008; Roelofs et al., 2007). The major outcome of emotional Stroop tasks is the attentional bias score, which is calculated by subtracting the color-naming latencies for neutral faces from the latencies needed to color-name emotional faces. A positive attentional bias score (i.e., color-naming latencies for emotional faces are larger than those for neutral faces) is taken to indicate vigilance, whereas a negative attentional bias score (i.e., color-naming latencies for emotional faces are shorter than those for neutral faces) is thought to indicate avoidance (e.g., Mathews & MacLeod, 1994; Van Honk et al., 1998, 2000; Putman et al., 2004). We used a masked version of the emotional Stroop task, in which the stimulus processing remains preconscious owing the short stimulus presentation (14 ms), making it unlikely that subjects exerted strategic effort to control possible attentional bias effects (e.g., MacLeod & Hagan, 1992; Van den Hout et al., 1995; Williams et al., 1996; Putman et al., 2004). Masked Stroop tasks have yielded more consistent results (Putman et al., 2004) and are more predictive than unmasked Stroop tasks of actual coping with stressful life-events (MacLeod & Hagan, 1992). On the basis of the previous findings in trauma-related disorders we expected that patients with PNES would show a positive attentional bias for angry faces.
Secondly, we tested whether such positive attentional bias would be related to interpersonal trauma reports in patients with PNES. Finally, we tested whether acute psychological stress affects the attentional bias toward interpersonal threat cues in patients with PNES. Therefore, we administered the Stroop task in a baseline and a social stress condition. Physiologic and subjective stress markers (cortisol, heart rate, blood pressure, and subjective anxiety) were assessed throughout the experiment.
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In this study, patients with PNES and matched controls did not differ in their performance on a neutral (and unmasked) Stroop task, but they showed significant differences in the processing of emotional stimuli on a masked pictorial Stroop task. Whereas the healthy controls displayed a negative attentional bias (AB) for angry faces, patients showed a positive AB for these social threatening stimuli, indicating that on a preconscious level of processing, patients were vigilant for social threat stimuli. In addition, this increased threat vigilance was related to self-reported trauma in patients with PNES. We describe these results in detail and discuss their implications.
The finding that patients with PNES reported more traumatic events than controls fits with the generally found high trauma rates in patients with PNES (e.g., Betts & Boden, 1992; Bowman, 1993; Moore & Baker, 1997; Kuyk et al., 1999; Fiszman et al., 2004; Sharpe & Faye, 2006) and conversion disorder in general (Roelofs et al., 2002). Most importantly, self-reported sexual trauma was related to the positive AB for angry faces in the patient group but not in controls. This relationship between threat vigilance and trauma reports shows an interesting parallel with findings in patients with PTSD to trauma-specific threat stimuli (for a review see McNally, 1998; Buckley et al., 2000). In patients with PTSD, such vigilance for trauma-related stimuli is considered as a tendency constantly to scan the environment for any signs of potential threat (Buckley et al., 2000), or it could reflect an impaired suppression of trauma information once it is activated (McNally, 1998). A similar positive AB for preconsciously presented angry faces, using the same masked pictorial Stroop task, was found in traumatized subjects with Dissociative Identity Disorder (Hermans et al., 2006), which was interpreted as indicating a state of hypervigilance. The finding of increased allocation of attentional resources to social threat in the current study may similarly reflect a state of hypervigilance, an interpretation that is supported by the finding that patients with PNES showed decreased HRV throughout the experiment. Decreased HRV is associated with increased arousal and anxiety and was previously found in patients with anxiety disorders, such as panic disorder (Friedman & Thayer, 1998), generalized anxiety disorder (Thayer et al., 1996), and PTSD (Cohen et al., 1999), and has been suggested as being associated with poor emotion regulation (Ruiz-Padial et al., 2003) and a negativity bias (Thayer & Brosschot, 2005). It is interesting to relate these findings to previous findings of repressive coping styles in PNES (e.g. Frances et al., 1999; Goldstein et al., 2000). Cognitive vigilance and avoidance are considered as ways of coping in the face of threat (e.g., Calvo & Eysenck, 2000; Hock & Krohne, 2004), and so-called repressors are characterized by an initial disproportionate engaging in threat processing, followed by an avoidance of threat processing and high physiologic arousal (Calvo & Eysenck, 2000). Future studies should investigate whether the threat-vigilance identified in the present study may be associated by subsequent avoidance, for example by using a modified dot-probe paradigm (see Mogg et al., 1997; Bögels & Mansell, 2004). Such investigation is particularly relevant because seizure reduction or cessation is generally associated with more active coping strategies in patients with PNES (Bodde et al., 2007; Kuyk et al., 2008), and it may contribute to fine tuning of psychological treatment of PNES. In contrast, the (early) avoidant coping style exhibited by our healthy controls in the face of threat, is considered as an adequate manner to avoid injury and unnecessary energy loss (Sapolsky, 1990; Van Honk et al., 2000).
In the present study, an increase of subjective and physiologic stress parameters during stress in both patients and controls suggested that the stress induction by means of the Trier Social Stress Test was successful. The group difference in attentional processing of social threat stimuli reported for the baseline condition was no longer present when subjects were tested in the context of social stress. Although this finding was in contrast to our predictions derived from Bendefeldt et al. (1976), this result is in agreement with earlier studies in patients with PTSD (Constans et al., 2004) and social phobia (Amir et al., 1996) in which patients exhibited a positive AB for threat words in a emotional Stroop task at baseline, which was suppressed in anticipation of a stressor. Because a positive AB for angry faces is often taken as indicating hypervigilance for signs of social threat, the fact that this effect disappeared during stress may be related to the unambiguousness of the social stress context, which makes an AB toward social threat stimuli in the emotional Stroop task simply redundant. Such interpretation is supported by Pessoa et al. (2002), who found that processing of emotional stimuli in a highly demanding environment did not lead to an activation of the amygdala. It was previously argued that in a highly demanding environment, all available attentional resources are focused on the environment, not on the cognitive task, resulting in reaction patterns that are independent of the emotional valence of the emotional stimuli (Lavie, 1995). In our study, the disappearance of the patients’ positive AB to angry faces in the social stress condition may reflect an allocation of all attentional resources towards the socioevaluative threat of the audience in this condition. Alternatively, it is possible that patients put more effort into complying with the task demand, in the context of social stress, resulting in a suppression of the AB for angry faces. The fact that patients made fewer errors in both Stroop tasks during stress, as compared to baseline, supports this notion, although this latter finding could also reflect a possible learning effect.
Patients and controls did not differ with respect to their basal and stress-induced cortisol levels. Although these findings are suggestive of a normal stress-reactivity of the HPA-axis in PNES, it should be noted that the currently used stressor was not specific for this disorder. In the context of trauma-related disorders, the use of personalized trauma scripts may constitute a more relevant or specific stressor, yielding different results (e.g., Elzinga et al., 2003).
When evaluating these results some strengths and limitations of the present study should be considered. A strong point is that all participating patients were diagnosed using the golden standard: an ictal video-EEG registration of a typical seizure in order to confirm the absence of epileptiform activity during a seizure (Reuber & Elger, 2003), making the diagnosis of PNES maximally reliable. Secondly, the fact that all participating patients were unmedicated rules out the possibility that the altered cognitive processing in our patients was the result of medication effects. As a consequence, however, we cannot automatically generalize these results to patients with PNES patient who are on medication. Thirdly, previous studies on neuropsychological functioning in patients with PNES were focused solely on the cognitive processing of nonemotional information (see Cragar et al., 2002 for a review). This is the first study investigating the cognitive processing of emotional stimuli in PNES. Facial expressions constitute important signals of threat or appeasement in the social environment (Öhman, 1986). Several neuroimaging studies have shown that viewing angry faces activates limbic structures, the amygdala in particular (for an overview see Adolphs et al., 2002; McClure et al., 2004; Strauss et al., 2005b), supporting the relevance of these stimuli in the study of stress-related disorders and the role of interpersonal trauma, in particular. Finally, the use of a masked Stroop task has the advantage that the subjects do not consciously perceive the stimuli, which was confirmed by the results from our awareness-check. This makes it unlikely that subjects exerted strategic effort to control AB effects (e.g., MacLeod & Hagan, 1992; Van den Hout et al., 1995; Williams et al., 1996; Putman et al., 2004) and makes the findings less vulnerable to uncontrollable subject factors.
A limitation of the present study is the lack of a clinical control group, making it difficult to state the specificity of the effects for the group with PNES and to exclude the possibility that the altered AB was mediated by comorbid psychopathology. However, in this respect it is relevant to mention that application of exactly the same masked emotional Stroop task in patients with social phobia resulted in opposite results; these patients allocated their attention away from the social threatening stimuli (E. Hermans, unpublished data). Despite this limitation, our data provide the first evidence linking interpersonal trauma with altered emotional processing in patients with PNES and give rise to several interesting questions for future research exploring the possible psychiatric mechanisms associated with PNES. For example, although we found clear results on the processing of masked emotional Stroop stimuli in our patient group, it remains to be tested whether the same findings hold for unmasked threat stimuli. Secondly, as stated earlier, it would be very interesting to replicate the present study by inducing stress using a more relevant/specific stressor, namely personalized trauma scripts or a physiologic stressor. Thirdly, considering that PNES is a rather heterogeneous group with respect to PNES characteristics, it would be interesting to investigate the effects of, besides psychotrauma, different PNES presentations (see e.g. Selwa et al., 2000) and comorbid psychopathology on the attentional processing of threatening stimuli. This is particularly relevant to gain insight into the possible different underlying mechanisms in the diverse semiology of PNES. Lastly, neuroimaging studies in PNES are needed to investigate which brain structures are involved in the processing of altered emotional information in neutral and stress conditions.
In conclusion, the present study showed impaired emotional information processing in patients with PNES. Compared to healthy controls, patients showed increased vigilance for masked angry faces. This preconscious AB for angry faces was significantly correlated to self-reported sexual trauma rates and probably reflects a state of hypervigilance. This interpretation is further supported by the finding of decreased HRV in patients with PNES, which was previously related to increased arousal/anxiety and poor emotion regulation. Given these results, further experimental research, investigating the relationship between attention, trauma, stress, and coping in patients with PNES seems promising to gain additional insight in possible neuropsychiatric mechanisms underlying this disorder with the ultimate purpose of improving (psychological) care for and treatment of this invalidating disorder.