Epilepsy & Behavior 32 (2014) 108–113
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Cognitive deficits and emotion regulation strategies in patients with psychogenic nonepileptic seizures: A task-switching study Amara Gul ⁎, Hira Ahmad Department of Applied Psychology, The Islamia University of Bahawalpur, Pakistan
a r t i c l e
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Article history: Received 6 December 2013 Revised 1 January 2014 Accepted 20 January 2014 Available online 13 February 2014 Keywords: Cognitive impairment Attention Psychogenic nonepileptic seizures Emotion suppression Cognitive reappraisal
a b s t r a c t This study examined the task-switching ability and emotion regulation strategies in 72 patients with psychogenic nonepileptic seizures (PNES) and 72 healthy individuals, where participants categorized emotion and age dimensions among faces. Results demonstrated cognitive impairment in terms of the interrupted ability to switch between emotion and nonemotion face categorizations in patients with PNES. In contrast, healthy individuals exhibited efficient switching between these face categorizations. In patients with PNES, there was an asymmetric relationship between emotion and age tasks, while this asymmetry was absent in the healthy group. The results demonstrated that patients with PNES used expressive suppression to regulate their emotions more frequently than the control group. On the other hand, patients with PNES less frequently reappraised their cognitions than healthy individuals. Switching deficits in patients with PNES were positively correlated with expressive suppression but were negatively correlated with cognitive reappraisal. This is the first study demonstrating the presence of switching deficits in terms of inferior cognitive control of emotion in patients with PNES as compared to healthy individuals. The switching deficits are associated with emotion regulation strategies. These findings suggest that emotion regulation strategies are significant markers of switching deficits in patients with PNES. © 2014 Elsevier Inc. All rights reserved.
1. Introduction Psychogenic nonepileptic seizures (PNES) can be defined as involuntary behaviors due to psychological and emotional disturbances. They are very similar to epileptic seizures, but whereas the causes of. The causes of psychogenic nonepileptic seizures are psychological and emotional disturbances, epileptic seizures have a neurologic origin [1]. Psychogenic nonepileptic seizures are not characterized by electrical discharge associated with epileptic seizures and are known as nonepileptic attack disorders. Certain features are usual in PNES but are uncommon in epileptic seizures: (i) tongue biting usually at the tip of the tongue, (ii) seizure duration of more than 2 min with a gradual onset, (iii) closed eyes during the seizure, and (iv) side-to-side head movements. Rare features in PNES include incontinence, severe tongue biting, and automatic complex movements [2,3]. Patients with PNES suffer from impairment in brain areas which are responsible for emotion regulation, executive control process, and movement, such as the prefrontal cortex, insula, inferior frontal gyrus, parietal cortex, and central sulcus. As a result, patients have unstable cognitive, emotional, and attentional systems [4]. Patients with PNES process emotional information on a preconscious level. Neurocognitive data revealed that patients with PNES suffer from impairment in working memory and attentional deficit. In a masked emotion Stroop task, ⁎ Corresponding author. E-mail addresses: [email protected] (A. Gul), [email protected] (H. Ahmad). 1525-5050/$ – see front matter © 2014 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.yebeh.2014.01.015
color-naming latencies for backwardly masked faces were measured. Patients with PNES displayed a positive attentional bias (i.e., slower color naming) to angry faces. In contrast, healthy individuals responded faster to angry faces. This result showed vigilance to expressions of emotions in patients with PNES [5]. Similarly, patients with PNES reported more emotional intensity to standard affective pictures and showed general emotion regulation difficulties. This result demonstrated that patients with PNES experienced intense emotions and negative emotional behavior [6]. Patients with PNES displayed lower global cognitive performance and higher dissociation scores than healthy individuals. The resting state fMRI showed a strong connectivity between areas associated with emotion regulation (i.e., insula), executive functions (i.e., inferior frontal gyrus and parietal cortex), and movement, such as the precentral sulcus, in patients with PNES. The strong functional connectivity between brain areas which monitor emotion, executive control, and movement was associated with the tendency to dissociate. Such an abnormal connectivity forms the basis for a neurophysiological correlate for underlying dissociation in patients with PNES, where emotion interferes with executive control. As a result, an altered motor activity appears which resembles an epileptic seizure [7]. Patients with PNES showed impaired neuropsychological performance on measures of attention, concentration, memory, verbal abilities, abstract reasoning, concept formation, etc. because of dysfunctions in the frontal lobe, a brain area which is primarily responsible for executive functions [8]. Patients with PNES demonstrated deficiency across a broad range of neuropsychological domains, specifically in attention and working memory.
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Attentional deficits were influenced by emotional distress in patients with PNES [9]. The modern concept of stress and health was influenced by Freud who stated that unresolved emotional distress causes somatic symptoms. Psychogenic nonepileptic seizure is one of those somatic symptoms [10]. Research suggests that patients with PNES lack coping strategies to deal with their emotional impairment, which may lead to suicidal ideation, irritated behavior, embarrassment, feelings of dependence [11], high expression of anger [12], emotion dysregulation [13], and external locus of control [14]. Emotion regulation is essential for mental health. People use different strategies to regulate emotion. Cognitive reappraisal and emotion suppression are common strategies used to control/maintain the emotion. Cognitive reappraisal means how a person perceives the situation in a way that he/she alters the emotional impact of the situation. Expressive suppression means to hide the external signs of internal feelings. The deliberate hiding of expression, an escape from sentiments, feelings, recollections, and other personal disturbing affairs, leads to different psychological and behavioral impairments [15]. Individuals who frequently hide their feelings and emotions suffer from decreased memory functioning and use less problem-solving strategies [16]. Suppression decreases social interaction and interpersonal communication and also has a negative correlation with human well-being [17]. Inhibiting positive and negative emotions increases sympathetic activations of the cardiovascular system and reduces cognitive performance [18]. Cognitive reappraisal strategy involves two parts: (i) awareness of the person's negative response and (ii) understanding of the situation as a way to decrease the intensity of negative response [19]. Functional magnetic resonance imaging (fMRI) data suggest that gray matter volume in different brain areas is involved in emotion regulation strategies. Cognitive reappraisal is associated with gray matter volume in the left amygdala. On the other hand, expressive suppression is related with gray matter volume in the paracingulate cortex and medial prefrontal cortex (PFC). Thus, larger volumes of the medial PFC and paracingulate cortex are involved in the regulation of emotion-expressive behavior, and the amygdala plays an important role in cognitive reappraisal [20]. Emotion regulation strategies decrease the experience and behavior related with negative emotion. In an emotion-generative process, reappraisal comes first and results in an early response of the PFC and a decrease in amygdala and insular response. On the other hand, suppression produces late PFC response but an increased amygdala and insular response [21]. Psychogenic nonepileptic seizures are characterized by MRI abnormalities, epileptiform EEG changes, and neuropsychological deficits [22]. The pathophysiological model suggests that the brain areas of patients with PNES involved in emotion regulation and sensorimotor and cognitive processes have an altered connection and that PNES are supported by an unbalanced cognitive– emotional attention system [23]. There is a possibility that patients with PNES deploy emotion regulation strategies in a modified pattern compared to healthy individuals. A differential usage of emotion regulation strategies could strengthen cognitive deficits in patients with PNES. Here, we were interested to examine whether emotion suppression and cognitive reappraisal facilitate cognitive inflexibility in patients with PNES.
1.1. The present study Epidemiological studies [24] stated that PNES had a high prevalence rate all over the world. Numerous studies which suggest that PNES are characterized by cognitive impairment [25]. However, none of these studies has yet addressed cognitive dysfunctions, specifically switching deficits in relation to emotion regulation, in patients with PNES. The present research was a preliminary attempt to compare the switching ability of patients with PNES to that of healthy individuals with particular reference to face categorization tasks.
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The following hypotheses were tested in the study: 1. Patients with PNES would show asymmetric switch costs (i.e., larger for the age task than the emotion task) between face categorization tasks. In contrast, healthy controls would exhibit a symmetric cost for emotion and age dimensions of faces. 2. Switch costs would have a positive relationship with expressive suppression in patients with PNES. 3. Switch costs would have a negative relationship with cognitive reappraisal in patients with PNES. 2. Methods 2.1. Participants From March 2013 until September 2013, 72 patients with PNES who were contacted from Services and Jinnah Hospital volunteered for the study. The inclusion criteria for the group with seizures were as follows: patients should (a) be aged 18 to 35 years; (b) have a diagnosis of PNES according to DSM-IV [26], whether the diagnosis was achieved on the basis of clinical observation or seizure history; (c) have a frequency of at least 2 seizures before their participation in the study; and (d) do not have any type of epileptic seizures. Seventy-two healthy individuals (controls) were contacted with the help of an advertisement through brochures distributed in the University of Punjab. The inclusion criteria for the healthy control group were as follows: individuals should (a) be aged 18 to 35 years, (b) have no signs or symptoms of psychological and mental disorders, (c) have no signs of any neurological disease, and (d) not be using any medication. Patients and controls were matched on the basis of age, gender, education, and economic status. 2.2. Measures 2.2.1. Depression Anxiety and Stress Scale [27] The Depression Anxiety and Stress Scale (DASS-42) was originally developed by Lovibond and Lovibond in 1995 [27]. It can be scored on a 4-point Likert scale of 0–3; 0 indicates “not apply to me”, and 3 indicates “completely apply”. Each subscale – depression, anxiety, and stress – consists of 14 items and can be scored by adding the score of those items which are relevant to that specific scale. The score of these three scales can be further categorized into normal, mild, moderate, and severe levels. The Depression Scale measures gloominess and cognitive problems. The Anxiety Scale evaluates the individual's experience of nervousness and impact of anxiety on the body. The Stress Scale measures the extent of relaxation and anxious arousal. Scores on depression are categorized as normal = 0–9, mild = 10–13, moderate = 14–20, and severe = 21–27, while anxiety scores are categorized as normal = 0–7, mild = 8–9, moderate = 10–14, and severe = 15–19. Stress scores are also divided into normal = 0–14, mild = 15–18, moderate = 19–25, and severe = 26–33. The Depression Anxiety and Stress Scale is strongly correlated with the Beck Anxiety Inventory (0.81) and Beck Depression Inventory (0.74). Cronbach's alpha is 0.96, 0.89, and 0.93 for depression, anxiety, and stress, respectively [28]. 2.2.2. Emotion Regulation Questionnaire [29] The Emotion Regulation Questionnaire measures an individual's capacity to assess how the individual regulates his/her emotions in stressful situations and daily life. This scale can be categorized into two subscales: (a) cognitive reappraisal and (b) emotion suppression. Cognitive reappraisal is the subcategory of the emotion regulation scale which measures how a person positively regulates or expresses his/her emotions to reduce psychological impact of the current situation. The scale consists of 6 items (1,3,5,7,8,10). Emotion suppression means to consciously hide or conceal uncomfortable feelings or thoughts in a more adaptable way. The scale consists of 4 items (2,4,6,9). The Emotion
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Regulation Questionnaire consists of 10 items which can be scored on a 7-point Likert scale: 7 (strongly agree) to 1 (strongly disagree). It is a valid and reliable test and has appropriate psychometric properties. The alpha reliabilities of reappraisal and suppression are .79 and .73, respectively. Both scales have a test–retest reliability of .69, with an internal consistency of α = .79 for cognitive reappraisal and α = .73 for emotion suppression [29].
2.2.3. Task-switching experiment The task-switching paradigm examines cognitive flexibility in performing various tasks. Switching between tasks requires updating of the task set in working memory each time the task switches. The inefficiency of the working memory to adopt a new task set is reflected in switch costs. The experiment in the present study involved switching between face categorization tasks. A total of 32 facial photographs were used in the experiment. Sixteen photographs showed young faces, and the other half depicted old faces. Among the 16 young faces, 8 faces showed a happy expression, and the remaining eight depicted an angry expression. Half of the young faces were female. Similarly, 8 of the 16 old faces showed a happy facial expression and the other eight depicted an angry expression. Among the sixteen old faces, 8 were of women. All the photographs were matched on size (325 × 325 pixels) and luminance. The alternating run [30] of the task-switching paradigms was used to design the experiment in E-prime software [31]. The experiment was presented on the screen of a 16-inch laptop. A pilot study showed that patients with PNES and controls can recognize the expression among the faces. Each trial comprised a fixation cross (+) displayed in the center of the screen for 1000 milliseconds (ms) followed by a blank screen for 1000 ms, and then by the appearance of the face. For each appearance, the face was displayed in the center of the screen on a colored background which indicated the task on hand. For instance, a black background indicated the age task. The tasks were counterbalanced with half of the participants performing the emotion task first and the remaining half performing the age task first. Participants made manual response to faces by pressing fixed keys on the keyboard. They were given instruction to press 3 to indicate happy, 2 to indicate angry, 1 to indicate young and 2 to indicate old faces. The face stayed on the screen until the time a response was completed. In total, the experiment had 225 trials. The first trial in the switching experiment never had a switch, so the data for the first trial were discarded from the analysis. Of the 112 trials in each task, 56 were switch trials, and the other fifty-six were repeat trials (Fig. 1).
Emotion Categorization
Age Categorization
+
Self-paced
1000ms 1000ms
+
Fig. 1. Example of the stimuli and displays for the emotion and age tasks.
2.3. Procedure The study was approved by the board of studies of The Islamia University of Bahawalpur. The participants completed the informed consent form, followed by their screening on depression and emotion regulation strategies. The comorbid psychopathology was assessed using the DSM-IV [26]. Those with no sign of comorbid disorder were invited to participate in the study, except for a few patients with PNES within sample who reported mild anxiety, stress and depression (see Table 1). After the screening, participants were given a detailed description of the experiment and its procedure. Participants viewed the laptop screen from a comfortable distance. They were told that their reaction time will be recorded and that they were required to categorize faces presented against a blue background according to the emotion expressed (happy or angry) by pressing the appropriate key on the keyboard. On the other hand, their task was to categorize the faces according to age (young or old) when the faces appeared on a black background. They were required to perform the tasks as quickly as possible, keeping the accuracy of the response intact. Upon completion of the 225 experimental trials, they were debriefed and were thanked for their participation. 3. Results 3.1. Task-switching and face categorization data The results of switching between face categorization tasks were shown in separate sections: (a) reaction times on emotion and age categorization tasks and (b) errors on categorizations of emotion and age. 3.1.1. Reaction time data Response times (RTs) were discarded when they were above 2.5 standard deviations from each participant's mean. Response times for the first trial were excluded because the task had no switch on the first trial. Following this, the switch costs for both tasks (mean RT switch minus repeat trials) were calculated, and then mean RTs were submitted to compute a repeated measures analysis of variance (ANOVA) with trial (switch vs. repeat) and task (emotion vs. age) as within-subjects factors and group (controls vs. patients) as between-subjects factors. The main effect of trial was significant (F (1, 142) = 419.54, p b 0.001, ηp2 = .74). Response times were slower on switch (M = 1970 ms) than on repeat (M = 751 ms) trials. There was a reliable main effect of task (F (1, 142) = 38.14, p b 0.001, ηp2 = .21). The RTs were faster on the emotion task than on the age task (M = 1311 vs. 1410 ms, respectively). There was a reliable effect of group (F (1, 142) = 1.32, p = .25, ηp2 = .00). Patients performed slower than controls (M = 1406 vs. 1316 ms, respectively). There was a reliable interaction between trial and task (F (1, 142) = 22.00, p b 0.001, ηp2 = .13). The switch cost for the age task was larger than that for the emotion task (t (143) = 4.42, p b 0.001 (M = 1286 vs. 1151 ms)). There was a significant higher order interaction between trial, task, and group (F (1, 142) = 17.43, p b 0.001, ηp2 = .10, Fig. 2). This interaction was further analyzed through separate repeated measure ANOVAs for patients and the control group with trial (switch vs. repeat) and task (emotion vs. age) as within-subjects factors. For patients, main effects were reliable [trial: F (1, 71) = 191.47, p b 0.001, ηp2 = .73; task: F (1, 71) = 34.17, p b 0.001, ηp2 = .32]. The switch trials were slower than the repeat trials, and the emotion task was faster than the age task. There was a reliable interaction between trial, task, and group (F (1, 71) = 38.00, p b 0.001, ηp2 = .34). The switch cost for the age task was larger than that for the emotion task (t (71) = 6.13, p b 0.001). For controls, the main effects of trial (F (1, 71) = 228.06, p b 0.001, ηp2 = .76) and task (F (1, 71) = 7.48, p b 0.01, ηp2 = .09) were reliable. Again, repeat trials were performed more efficiently than
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Table 1 Demographic and clinical characteristics of patients with PNES and healthy controls. Variables
Patients (N = 72)
Control (N = 72)
Statistics
M (SD)
Range (min–max)
M (SD)
Range (min–max)
Emotion suppression Cognitive reappraisal
16.95 (8.23) 23.56 (10.57)
(05–28) (09–42)
9.66 (2.47) 32.70 (3.29)
(04–15) (25–38)
Comorbidity psychopathology Somatization Depression Stress Anxiety Age
None 4 12 10 28.36 (3.93)
(18.00–34.00)
None None None None 23.93 (3.09)
(19.00–32.00)
Gender Female Male
37 35
40 32
Economic status Lower Middle Higher
65 7
69 3
Education Primary Secondary Higher
30 42
25 47
switch trials. The age task was performed slower than the emotion task. In contrast to the patient data, the interaction between trial and task failed to reach significance level (F (1, 71) = 0.13, p = .72, ηp2 = .00).
3.2. Error data Errors for the first trial were discarded because no task switch took place. Mean errors were submitted to a repeated measures analysis of variance (ANOVA) with trial (switch vs. repeat) and task (emotion vs.
Mean reaction time (ms)
a 2500
Patients
2000 Switch
1500
Repeat 1000
t (71) = 7.91, p b 0.001 t (71) = 7.25, p b 0.001
age) as within-subjects factors and group (controls vs. patients) as between-subjects factors. The main effect of trial was significant (F (1, 142) = 25.57, p = 0.26, MSE = .00, ηp2 = .01; M = 0.11 (switch) vs. M = 0.10 (repeat)). There was a reliable main effect of task (F (1, 142) =766.03, p b 0.001, MSE = .00, ηp2 = .84). Errors were larger in the emotion task than in the age task (M = 0.16 vs. 0.05, respectively). The effect of group was not reliable (F (1, 142) = 1.27, p = 0.26, MSE = .00, ηp2 = .00; M = 0.10 (patients) vs. M = 0.11 (control)). There was a significant interaction between task and group (F (1, 142) = 26.14, p b 0.001, MSE = 0.00, ηp2 = .15, Fig. 3). The interaction between trial and task was not reliable (F (1, 142) = 2.71, p = .10, MSE = 0.00, ηp2 = .01; emotion (switch: M = .16, repeat: M = .05), age (switch: M = .16, repeat: M = .04)). Similarly, the interaction between trial and group was not significant (F (1, 142) = 0.24, p = .62, MSE = 0.001, ηp2 = .00; patients (switch: M = .11, repeat: M = .10), control (switch: M = .11, repeat: M = .11)). The higher order interaction between trial, task, and group was not significant (F (1, 142) = 7.00, p b 0.001, MSE = 0.00, ηp2 =.04, Fig. 4). 3.3. Task-switching costs and emotion regulation strategies
500 Emotion
3000
Patients with PNES scored higher on emotion suppression than healthy controls. In contrast, patients with PNES scored lower on
Controls 0.19
2500
0.17
2000 Switch 1500
Repeat
1000
Mean error rate
Mean reaction times (ms)
b
Age
0.15 0.13 0.11 0.09
Patients
0.07
Controls
0.05 0.03
500 Emotion
Age
Fig. 2. a. Mean reaction times (ms) for patients on switch and repeat trials. Error bars represent standard errors. b. Mean reaction times (ms) for controls on switch and repeat trials. Error bars represent standard errors.
0.01 Emotion
Age
Task Fig. 3. Mean error rates of patients and controls on emotion and age tasks.
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a
0.2
Patients
Mean error rate
0.18 0.16 0.14 0.12
Emotion
0.1
Age
0.08 0.06 0.04 0.02 Emotion
b
0.2
age
Controls
Mean error rate
0.18 0.16 0.14 0.12
Emotion
0.1
Age
0.08 0.06 0.04 0.02 Emotion
age
Fig. 4. a. Mean error rates of patients on switch and repeat trials for emotion and age tasks. b. Mean error rates of controls on switch and repeat trials for emotion and age tasks.
cognitive reappraisal than healthy controls (see Table 1). Further, Pearson correlations were conducted to assess the relationship between emotion regulation strategies and task-switching costs in patients with PNES. There was a reliable positive relationship between emotion suppression and switch costs (r = .47, p b 0.001) and a negative relationship between cognitive reappraisal and switch cost (r = −.31, p b 0.01). This result suggested that the inferior switching ability of patients with PNES was correlated with high emotion suppression and less frequent cognitive reappraisal. 4. Discussion The present study was designed to assess two important issues: (i) ease of switching between face categorizations in patients with PNES and (ii) relationship between switching ability and emotion regulation strategies in patients with PNES. 4.1. Task switching and face categorization There was an asymmetric relationship between emotion and age categorizations among faces; in contrast, there was an absence of asymmetry in healthy controls. This result supported the first hypothesis of the study. In patients with PNES, emotion categorization was easier than age categorization. Performance on the switch trials was slower than that on the repeat trials. There was a larger switch cost for the age categorization than for the emotion categorization. Patients with PNES showed more difficulty in switching attention from the emotion dimension of the faces than from the age dimension, thus a larger switch cost for the age dimension was exhibited. The performance for age decisions was slower than that for emotion decisions on the switch trials, which demonstrated that it was harder for patients with PNES to disengage attention from emotion which in turn produced cost on the computation of age dimension. It seems that their attentional system was biased towards different dimensions of faces. The results indicated
here that emotion categorization consumed more resources; therefore, the age categorization suffered. In patients with PNES, emotion categorization was faster than age categorization, and performance was less efficient on switch trials than on repeat trials. In contrast, in healthy controls, there was an absence of asymmetric relationship between emotion and age categorizations of faces. The absence of an asymmetry in healthy controls showed that the computation of emotion and age dimensions was performed with an equal speed. Thus, none of these two dimensions utilized more resources in their attentional system. The results are consistent with previous studies confirming the presence of bias in the attentional system of patients with PNES. In a masked emotion Stroop test, patients with PNES and healthy group showed similar response on neutral pictures while patients showed attentional biasness on angry stimuli [2] because functional connections are dysfunctional between brain areas such as the dorsolateral prefrontal cortex, anterior cingulate, and parietal cortex, which control emotion and sensorimotor and cognitive functioning [4,7]. Further, high levels of emotional dysregulation [32] and elevated cortisol levels [33] have been demonstrated in patients with PNES. 4.2. Task-switching and emotion regulation strategies The results of the current study showed that cognitive deficits in patients with PNES are linked with emotion regulation strategies. The group with PNES showed higher scores on emotion suppression than healthy controls. In contrast, patients with PNES employed less frequent reappraisal of cognitions than healthy individuals. Further, there were individual differences in emotion regulation strategies such as frequent use of emotion suppression, and less cognitive reappraisal produces higher switch cost(s). We can infer that strategies to regulate emotion modulate the ability to perceive faces. These results are consistent with those of previous studies suggesting that deliberately concealing emotions can have drastic physiological consequences such as stress and elevation of blood pressure [34]. Our results showed that inferior switching ability was associated with more frequent use of emotion suppression in patients with PNES. An attentional bias to expressions of emotions appeared which produced asymmetric switch costs during face categorizations. Suppression is basically a formal state of mind in which an individual consciously avoids the situation [35]. Suppression of emotions, thoughts, and feelings plays a major role in the development of psychopathology [36]. Conscious avoidance and expressive suppression are basically a part of attentional bias. Attentional bias can occur because of two reasons: (i) brain areas are not properly integrated and (ii) conscious avoidance or suppression of emotion. Stimulus recognition is a spontaneous mechanism, while expressive suppression or avoidance is a gradual process. When these two processes do not operate simultaneously, attentional bias occurs [37]. This result is in line with those of previous studies which demonstrated the maladaptive pattern of coping strategies in patients with PNES. Patients with psychogenic nonepileptic seizures adopt a more stressful lifestyle and repress their emotions and feelings compared with healthy individuals [38]. It has been shown that continuous suppression of distressing thoughts or avoidance of situations induces higher frequency of these thoughts [39]; thus, patients with PNES display an attentional bias towards facial emotion and suffer from a difficulty to disengage their attention from expressions of emotion. As a result, the nonemotion feature carries a greater switch cost. Our results demonstrated that cognitive reappraisal was another important strategy which influenced switching ability among patients with PNES. The less frequent use of cognitive reappraisal was associated with the inferior switching ability of patients with PNES. Cognitive reappraisal is the downregulation strategy that is used to reformulate an emotional experience in order to lessen the intensity of physiological arousal in response to an unpleasant emotional [23,40–42] and stressful [14,43] experience. Reappraisal induces changes in late positive potentials (as measured by event-related potentials) and improves salivary immunity gauged by secretory immunoglobulin
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which is associated with cognitive restructuring of negative emotions [44]. The less frequent usage of cognitive reappraisal in patients with PNES facilitates the concentration of attention on emotional stimuli; as a result, cognitive performance is interrupted. An altered activation in brain areas involved in emotion processing could be responsible for differential usage of emotion suppression and cognitive reappraisal in patients with PNES compared to healthy individuals. As observed here, the constant suppression of emotion and irregular reappraisal of cognitions facilitate cognitive inflexibility in patients with PNES. 4.3. Conclusion The data suggest that patients with PNES suffer from an attentional bias towards the categorization of facial attributes. Their attentional system consumes more resources when confronted with the emotion dimension of faces; therefore, a nonemotion task suffers as sufficient resources are not available for such categorizations. The cost that an attentional system bears is linked with a frequent use of emotion suppression and less frequent reappraisal of cognitions as emotion regulation strategies. The results of the current study have implications for psychotherapists, counselors, medical practitioners, and mental health practitioners and will help in understanding the mechanisms underlying face categorization, cognitive system, and emotion regulation. Future studies must examine whether the observed cognitive deficits in patients with PNES can be improved with training. Disclosure None of the authors has any conflict of interests to disclose. References [1] Brooks JL, Baker GA, Boon PA, Hendriksen JG, Mulder OG, Aldenkamn AP. Psychogenic non-epileptic seizures—definition, etiology, treatment and prognostic issues: a critical review. Seizure Eur J Epilepsy 2009;18:543–53. [2] Mellers JDC. The approach to patients with “non-epileptic seizures”. Postgrad Med J 2005;81(958):498–504. [3] Carreno M. Recognition of nonepileptic events. Semin Neurol 2008;28(3):297–304. [4] Baslet G. Psychogenic non-epileptic seizures: a model of their pathogenic mechanism. Seizure 2011;20:1–13. [5] Bakvis P, Roelofs K, Kuyk J, Edelbroek OM, Swinkels WAM, Spinhoven P, et al. Trauma, stress, and preconscious threat processing in patients with psychogenic nonepileptic seizures. Epilepsia 2009;50(5):1001–11. [6] Roberts NA, Burleson MH, Weber DJ, Larson A, Sergeant K, Devine MJ, et al. Emotion in psychogenic nonepileptic seizures: responses to affective pictures. Epilepsy Behav 2012;24:107–15. [7] Van der Kruijs SJ, Bodde NM, Vaessen MJ, Lazeron RH, Vonck K, Boon P. Functional connectivity of dissociation in patients with psychogenic non-epileptic seizures. J Neurol Neurosurg Psychiatry 2012;83(3):239–47. [8] Kalogjera-Sackellares D, Sackellares JC. Intellectual and neuropsychological features of patients with psychogenic pseudoseizures. Psychiatry Res 1999;86(1):73–84. [9] Strutt AM, Hill SW, Scott BM, Uber-Zak L, Fogel TG. A comprehensive neuropsychological profile of women with psychogenic nonepileptic seizures. Epilepsy Behav 2011;20:24–8. [10] Woolfolk RL, Allen LA, Tiu JE. New directions in the treatment of somatization. Psychiatr Clin N Am 2007;30(4):621–44. [11] Thompson R, Isaac CL, Rowse G, Tooth CL, Reuber M. What is it like to receive a diagnosis of nonepileptic? Epilepsy Behav 2009;14(3):508–15. [12] Mokleby K, Blomhoff S, Malt UF, Dahlstro MA, Tauboll E, Gjerstad L. Psychiatric comorbidity and hostility in patients with psychogenic nonepileptic seizures compared with somatoform disorders and healthy controls. Epilepsia 2002;43:193–8.
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Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Cognitive deficits and emotion regulation strategies in patients with psychogenic nonepileptic seizures: A task-switching study Amara Gul ⁎, Hira Ahmad Department of Applied Psychology, The Islamia University of Bahawalpur, Pakistan
a r t i c l e
i n f o
Article history: Received 6 December 2013 Revised 1 January 2014 Accepted 20 January 2014 Available online 13 February 2014 Keywords: Cognitive impairment Attention Psychogenic nonepileptic seizures Emotion suppression Cognitive reappraisal
a b s t r a c t This study examined the task-switching ability and emotion regulation strategies in 72 patients with psychogenic nonepileptic seizures (PNES) and 72 healthy individuals, where participants categorized emotion and age dimensions among faces. Results demonstrated cognitive impairment in terms of the interrupted ability to switch between emotion and nonemotion face categorizations in patients with PNES. In contrast, healthy individuals exhibited efficient switching between these face categorizations. In patients with PNES, there was an asymmetric relationship between emotion and age tasks, while this asymmetry was absent in the healthy group. The results demonstrated that patients with PNES used expressive suppression to regulate their emotions more frequently than the control group. On the other hand, patients with PNES less frequently reappraised their cognitions than healthy individuals. Switching deficits in patients with PNES were positively correlated with expressive suppression but were negatively correlated with cognitive reappraisal. This is the first study demonstrating the presence of switching deficits in terms of inferior cognitive control of emotion in patients with PNES as compared to healthy individuals. The switching deficits are associated with emotion regulation strategies. These findings suggest that emotion regulation strategies are significant markers of switching deficits in patients with PNES. © 2014 Elsevier Inc. All rights reserved.
1. Introduction Psychogenic nonepileptic seizures (PNES) can be defined as involuntary behaviors due to psychological and emotional disturbances. They are very similar to epileptic seizures, but whereas the causes of. The causes of psychogenic nonepileptic seizures are psychological and emotional disturbances, epileptic seizures have a neurologic origin [1]. Psychogenic nonepileptic seizures are not characterized by electrical discharge associated with epileptic seizures and are known as nonepileptic attack disorders. Certain features are usual in PNES but are uncommon in epileptic seizures: (i) tongue biting usually at the tip of the tongue, (ii) seizure duration of more than 2 min with a gradual onset, (iii) closed eyes during the seizure, and (iv) side-to-side head movements. Rare features in PNES include incontinence, severe tongue biting, and automatic complex movements [2,3]. Patients with PNES suffer from impairment in brain areas which are responsible for emotion regulation, executive control process, and movement, such as the prefrontal cortex, insula, inferior frontal gyrus, parietal cortex, and central sulcus. As a result, patients have unstable cognitive, emotional, and attentional systems [4]. Patients with PNES process emotional information on a preconscious level. Neurocognitive data revealed that patients with PNES suffer from impairment in working memory and attentional deficit. In a masked emotion Stroop task, ⁎ Corresponding author. E-mail addresses: [email protected] (A. Gul), [email protected] (H. Ahmad). 1525-5050/$ – see front matter © 2014 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.yebeh.2014.01.015
color-naming latencies for backwardly masked faces were measured. Patients with PNES displayed a positive attentional bias (i.e., slower color naming) to angry faces. In contrast, healthy individuals responded faster to angry faces. This result showed vigilance to expressions of emotions in patients with PNES [5]. Similarly, patients with PNES reported more emotional intensity to standard affective pictures and showed general emotion regulation difficulties. This result demonstrated that patients with PNES experienced intense emotions and negative emotional behavior [6]. Patients with PNES displayed lower global cognitive performance and higher dissociation scores than healthy individuals. The resting state fMRI showed a strong connectivity between areas associated with emotion regulation (i.e., insula), executive functions (i.e., inferior frontal gyrus and parietal cortex), and movement, such as the precentral sulcus, in patients with PNES. The strong functional connectivity between brain areas which monitor emotion, executive control, and movement was associated with the tendency to dissociate. Such an abnormal connectivity forms the basis for a neurophysiological correlate for underlying dissociation in patients with PNES, where emotion interferes with executive control. As a result, an altered motor activity appears which resembles an epileptic seizure [7]. Patients with PNES showed impaired neuropsychological performance on measures of attention, concentration, memory, verbal abilities, abstract reasoning, concept formation, etc. because of dysfunctions in the frontal lobe, a brain area which is primarily responsible for executive functions [8]. Patients with PNES demonstrated deficiency across a broad range of neuropsychological domains, specifically in attention and working memory.
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Attentional deficits were influenced by emotional distress in patients with PNES [9]. The modern concept of stress and health was influenced by Freud who stated that unresolved emotional distress causes somatic symptoms. Psychogenic nonepileptic seizure is one of those somatic symptoms [10]. Research suggests that patients with PNES lack coping strategies to deal with their emotional impairment, which may lead to suicidal ideation, irritated behavior, embarrassment, feelings of dependence [11], high expression of anger [12], emotion dysregulation [13], and external locus of control [14]. Emotion regulation is essential for mental health. People use different strategies to regulate emotion. Cognitive reappraisal and emotion suppression are common strategies used to control/maintain the emotion. Cognitive reappraisal means how a person perceives the situation in a way that he/she alters the emotional impact of the situation. Expressive suppression means to hide the external signs of internal feelings. The deliberate hiding of expression, an escape from sentiments, feelings, recollections, and other personal disturbing affairs, leads to different psychological and behavioral impairments [15]. Individuals who frequently hide their feelings and emotions suffer from decreased memory functioning and use less problem-solving strategies [16]. Suppression decreases social interaction and interpersonal communication and also has a negative correlation with human well-being [17]. Inhibiting positive and negative emotions increases sympathetic activations of the cardiovascular system and reduces cognitive performance [18]. Cognitive reappraisal strategy involves two parts: (i) awareness of the person's negative response and (ii) understanding of the situation as a way to decrease the intensity of negative response [19]. Functional magnetic resonance imaging (fMRI) data suggest that gray matter volume in different brain areas is involved in emotion regulation strategies. Cognitive reappraisal is associated with gray matter volume in the left amygdala. On the other hand, expressive suppression is related with gray matter volume in the paracingulate cortex and medial prefrontal cortex (PFC). Thus, larger volumes of the medial PFC and paracingulate cortex are involved in the regulation of emotion-expressive behavior, and the amygdala plays an important role in cognitive reappraisal [20]. Emotion regulation strategies decrease the experience and behavior related with negative emotion. In an emotion-generative process, reappraisal comes first and results in an early response of the PFC and a decrease in amygdala and insular response. On the other hand, suppression produces late PFC response but an increased amygdala and insular response [21]. Psychogenic nonepileptic seizures are characterized by MRI abnormalities, epileptiform EEG changes, and neuropsychological deficits [22]. The pathophysiological model suggests that the brain areas of patients with PNES involved in emotion regulation and sensorimotor and cognitive processes have an altered connection and that PNES are supported by an unbalanced cognitive– emotional attention system [23]. There is a possibility that patients with PNES deploy emotion regulation strategies in a modified pattern compared to healthy individuals. A differential usage of emotion regulation strategies could strengthen cognitive deficits in patients with PNES. Here, we were interested to examine whether emotion suppression and cognitive reappraisal facilitate cognitive inflexibility in patients with PNES.
1.1. The present study Epidemiological studies [24] stated that PNES had a high prevalence rate all over the world. Numerous studies which suggest that PNES are characterized by cognitive impairment [25]. However, none of these studies has yet addressed cognitive dysfunctions, specifically switching deficits in relation to emotion regulation, in patients with PNES. The present research was a preliminary attempt to compare the switching ability of patients with PNES to that of healthy individuals with particular reference to face categorization tasks.
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The following hypotheses were tested in the study: 1. Patients with PNES would show asymmetric switch costs (i.e., larger for the age task than the emotion task) between face categorization tasks. In contrast, healthy controls would exhibit a symmetric cost for emotion and age dimensions of faces. 2. Switch costs would have a positive relationship with expressive suppression in patients with PNES. 3. Switch costs would have a negative relationship with cognitive reappraisal in patients with PNES. 2. Methods 2.1. Participants From March 2013 until September 2013, 72 patients with PNES who were contacted from Services and Jinnah Hospital volunteered for the study. The inclusion criteria for the group with seizures were as follows: patients should (a) be aged 18 to 35 years; (b) have a diagnosis of PNES according to DSM-IV [26], whether the diagnosis was achieved on the basis of clinical observation or seizure history; (c) have a frequency of at least 2 seizures before their participation in the study; and (d) do not have any type of epileptic seizures. Seventy-two healthy individuals (controls) were contacted with the help of an advertisement through brochures distributed in the University of Punjab. The inclusion criteria for the healthy control group were as follows: individuals should (a) be aged 18 to 35 years, (b) have no signs or symptoms of psychological and mental disorders, (c) have no signs of any neurological disease, and (d) not be using any medication. Patients and controls were matched on the basis of age, gender, education, and economic status. 2.2. Measures 2.2.1. Depression Anxiety and Stress Scale [27] The Depression Anxiety and Stress Scale (DASS-42) was originally developed by Lovibond and Lovibond in 1995 [27]. It can be scored on a 4-point Likert scale of 0–3; 0 indicates “not apply to me”, and 3 indicates “completely apply”. Each subscale – depression, anxiety, and stress – consists of 14 items and can be scored by adding the score of those items which are relevant to that specific scale. The score of these three scales can be further categorized into normal, mild, moderate, and severe levels. The Depression Scale measures gloominess and cognitive problems. The Anxiety Scale evaluates the individual's experience of nervousness and impact of anxiety on the body. The Stress Scale measures the extent of relaxation and anxious arousal. Scores on depression are categorized as normal = 0–9, mild = 10–13, moderate = 14–20, and severe = 21–27, while anxiety scores are categorized as normal = 0–7, mild = 8–9, moderate = 10–14, and severe = 15–19. Stress scores are also divided into normal = 0–14, mild = 15–18, moderate = 19–25, and severe = 26–33. The Depression Anxiety and Stress Scale is strongly correlated with the Beck Anxiety Inventory (0.81) and Beck Depression Inventory (0.74). Cronbach's alpha is 0.96, 0.89, and 0.93 for depression, anxiety, and stress, respectively [28]. 2.2.2. Emotion Regulation Questionnaire [29] The Emotion Regulation Questionnaire measures an individual's capacity to assess how the individual regulates his/her emotions in stressful situations and daily life. This scale can be categorized into two subscales: (a) cognitive reappraisal and (b) emotion suppression. Cognitive reappraisal is the subcategory of the emotion regulation scale which measures how a person positively regulates or expresses his/her emotions to reduce psychological impact of the current situation. The scale consists of 6 items (1,3,5,7,8,10). Emotion suppression means to consciously hide or conceal uncomfortable feelings or thoughts in a more adaptable way. The scale consists of 4 items (2,4,6,9). The Emotion
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Regulation Questionnaire consists of 10 items which can be scored on a 7-point Likert scale: 7 (strongly agree) to 1 (strongly disagree). It is a valid and reliable test and has appropriate psychometric properties. The alpha reliabilities of reappraisal and suppression are .79 and .73, respectively. Both scales have a test–retest reliability of .69, with an internal consistency of α = .79 for cognitive reappraisal and α = .73 for emotion suppression [29].
2.2.3. Task-switching experiment The task-switching paradigm examines cognitive flexibility in performing various tasks. Switching between tasks requires updating of the task set in working memory each time the task switches. The inefficiency of the working memory to adopt a new task set is reflected in switch costs. The experiment in the present study involved switching between face categorization tasks. A total of 32 facial photographs were used in the experiment. Sixteen photographs showed young faces, and the other half depicted old faces. Among the 16 young faces, 8 faces showed a happy expression, and the remaining eight depicted an angry expression. Half of the young faces were female. Similarly, 8 of the 16 old faces showed a happy facial expression and the other eight depicted an angry expression. Among the sixteen old faces, 8 were of women. All the photographs were matched on size (325 × 325 pixels) and luminance. The alternating run [30] of the task-switching paradigms was used to design the experiment in E-prime software [31]. The experiment was presented on the screen of a 16-inch laptop. A pilot study showed that patients with PNES and controls can recognize the expression among the faces. Each trial comprised a fixation cross (+) displayed in the center of the screen for 1000 milliseconds (ms) followed by a blank screen for 1000 ms, and then by the appearance of the face. For each appearance, the face was displayed in the center of the screen on a colored background which indicated the task on hand. For instance, a black background indicated the age task. The tasks were counterbalanced with half of the participants performing the emotion task first and the remaining half performing the age task first. Participants made manual response to faces by pressing fixed keys on the keyboard. They were given instruction to press 3 to indicate happy, 2 to indicate angry, 1 to indicate young and 2 to indicate old faces. The face stayed on the screen until the time a response was completed. In total, the experiment had 225 trials. The first trial in the switching experiment never had a switch, so the data for the first trial were discarded from the analysis. Of the 112 trials in each task, 56 were switch trials, and the other fifty-six were repeat trials (Fig. 1).
Emotion Categorization
Age Categorization
+
Self-paced
1000ms 1000ms
+
Fig. 1. Example of the stimuli and displays for the emotion and age tasks.
2.3. Procedure The study was approved by the board of studies of The Islamia University of Bahawalpur. The participants completed the informed consent form, followed by their screening on depression and emotion regulation strategies. The comorbid psychopathology was assessed using the DSM-IV [26]. Those with no sign of comorbid disorder were invited to participate in the study, except for a few patients with PNES within sample who reported mild anxiety, stress and depression (see Table 1). After the screening, participants were given a detailed description of the experiment and its procedure. Participants viewed the laptop screen from a comfortable distance. They were told that their reaction time will be recorded and that they were required to categorize faces presented against a blue background according to the emotion expressed (happy or angry) by pressing the appropriate key on the keyboard. On the other hand, their task was to categorize the faces according to age (young or old) when the faces appeared on a black background. They were required to perform the tasks as quickly as possible, keeping the accuracy of the response intact. Upon completion of the 225 experimental trials, they were debriefed and were thanked for their participation. 3. Results 3.1. Task-switching and face categorization data The results of switching between face categorization tasks were shown in separate sections: (a) reaction times on emotion and age categorization tasks and (b) errors on categorizations of emotion and age. 3.1.1. Reaction time data Response times (RTs) were discarded when they were above 2.5 standard deviations from each participant's mean. Response times for the first trial were excluded because the task had no switch on the first trial. Following this, the switch costs for both tasks (mean RT switch minus repeat trials) were calculated, and then mean RTs were submitted to compute a repeated measures analysis of variance (ANOVA) with trial (switch vs. repeat) and task (emotion vs. age) as within-subjects factors and group (controls vs. patients) as between-subjects factors. The main effect of trial was significant (F (1, 142) = 419.54, p b 0.001, ηp2 = .74). Response times were slower on switch (M = 1970 ms) than on repeat (M = 751 ms) trials. There was a reliable main effect of task (F (1, 142) = 38.14, p b 0.001, ηp2 = .21). The RTs were faster on the emotion task than on the age task (M = 1311 vs. 1410 ms, respectively). There was a reliable effect of group (F (1, 142) = 1.32, p = .25, ηp2 = .00). Patients performed slower than controls (M = 1406 vs. 1316 ms, respectively). There was a reliable interaction between trial and task (F (1, 142) = 22.00, p b 0.001, ηp2 = .13). The switch cost for the age task was larger than that for the emotion task (t (143) = 4.42, p b 0.001 (M = 1286 vs. 1151 ms)). There was a significant higher order interaction between trial, task, and group (F (1, 142) = 17.43, p b 0.001, ηp2 = .10, Fig. 2). This interaction was further analyzed through separate repeated measure ANOVAs for patients and the control group with trial (switch vs. repeat) and task (emotion vs. age) as within-subjects factors. For patients, main effects were reliable [trial: F (1, 71) = 191.47, p b 0.001, ηp2 = .73; task: F (1, 71) = 34.17, p b 0.001, ηp2 = .32]. The switch trials were slower than the repeat trials, and the emotion task was faster than the age task. There was a reliable interaction between trial, task, and group (F (1, 71) = 38.00, p b 0.001, ηp2 = .34). The switch cost for the age task was larger than that for the emotion task (t (71) = 6.13, p b 0.001). For controls, the main effects of trial (F (1, 71) = 228.06, p b 0.001, ηp2 = .76) and task (F (1, 71) = 7.48, p b 0.01, ηp2 = .09) were reliable. Again, repeat trials were performed more efficiently than
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Table 1 Demographic and clinical characteristics of patients with PNES and healthy controls. Variables
Patients (N = 72)
Control (N = 72)
Statistics
M (SD)
Range (min–max)
M (SD)
Range (min–max)
Emotion suppression Cognitive reappraisal
16.95 (8.23) 23.56 (10.57)
(05–28) (09–42)
9.66 (2.47) 32.70 (3.29)
(04–15) (25–38)
Comorbidity psychopathology Somatization Depression Stress Anxiety Age
None 4 12 10 28.36 (3.93)
(18.00–34.00)
None None None None 23.93 (3.09)
(19.00–32.00)
Gender Female Male
37 35
40 32
Economic status Lower Middle Higher
65 7
69 3
Education Primary Secondary Higher
30 42
25 47
switch trials. The age task was performed slower than the emotion task. In contrast to the patient data, the interaction between trial and task failed to reach significance level (F (1, 71) = 0.13, p = .72, ηp2 = .00).
3.2. Error data Errors for the first trial were discarded because no task switch took place. Mean errors were submitted to a repeated measures analysis of variance (ANOVA) with trial (switch vs. repeat) and task (emotion vs.
Mean reaction time (ms)
a 2500
Patients
2000 Switch
1500
Repeat 1000
t (71) = 7.91, p b 0.001 t (71) = 7.25, p b 0.001
age) as within-subjects factors and group (controls vs. patients) as between-subjects factors. The main effect of trial was significant (F (1, 142) = 25.57, p = 0.26, MSE = .00, ηp2 = .01; M = 0.11 (switch) vs. M = 0.10 (repeat)). There was a reliable main effect of task (F (1, 142) =766.03, p b 0.001, MSE = .00, ηp2 = .84). Errors were larger in the emotion task than in the age task (M = 0.16 vs. 0.05, respectively). The effect of group was not reliable (F (1, 142) = 1.27, p = 0.26, MSE = .00, ηp2 = .00; M = 0.10 (patients) vs. M = 0.11 (control)). There was a significant interaction between task and group (F (1, 142) = 26.14, p b 0.001, MSE = 0.00, ηp2 = .15, Fig. 3). The interaction between trial and task was not reliable (F (1, 142) = 2.71, p = .10, MSE = 0.00, ηp2 = .01; emotion (switch: M = .16, repeat: M = .05), age (switch: M = .16, repeat: M = .04)). Similarly, the interaction between trial and group was not significant (F (1, 142) = 0.24, p = .62, MSE = 0.001, ηp2 = .00; patients (switch: M = .11, repeat: M = .10), control (switch: M = .11, repeat: M = .11)). The higher order interaction between trial, task, and group was not significant (F (1, 142) = 7.00, p b 0.001, MSE = 0.00, ηp2 =.04, Fig. 4). 3.3. Task-switching costs and emotion regulation strategies
500 Emotion
3000
Patients with PNES scored higher on emotion suppression than healthy controls. In contrast, patients with PNES scored lower on
Controls 0.19
2500
0.17
2000 Switch 1500
Repeat
1000
Mean error rate
Mean reaction times (ms)
b
Age
0.15 0.13 0.11 0.09
Patients
0.07
Controls
0.05 0.03
500 Emotion
Age
Fig. 2. a. Mean reaction times (ms) for patients on switch and repeat trials. Error bars represent standard errors. b. Mean reaction times (ms) for controls on switch and repeat trials. Error bars represent standard errors.
0.01 Emotion
Age
Task Fig. 3. Mean error rates of patients and controls on emotion and age tasks.
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a
0.2
Patients
Mean error rate
0.18 0.16 0.14 0.12
Emotion
0.1
Age
0.08 0.06 0.04 0.02 Emotion
b
0.2
age
Controls
Mean error rate
0.18 0.16 0.14 0.12
Emotion
0.1
Age
0.08 0.06 0.04 0.02 Emotion
age
Fig. 4. a. Mean error rates of patients on switch and repeat trials for emotion and age tasks. b. Mean error rates of controls on switch and repeat trials for emotion and age tasks.
cognitive reappraisal than healthy controls (see Table 1). Further, Pearson correlations were conducted to assess the relationship between emotion regulation strategies and task-switching costs in patients with PNES. There was a reliable positive relationship between emotion suppression and switch costs (r = .47, p b 0.001) and a negative relationship between cognitive reappraisal and switch cost (r = −.31, p b 0.01). This result suggested that the inferior switching ability of patients with PNES was correlated with high emotion suppression and less frequent cognitive reappraisal. 4. Discussion The present study was designed to assess two important issues: (i) ease of switching between face categorizations in patients with PNES and (ii) relationship between switching ability and emotion regulation strategies in patients with PNES. 4.1. Task switching and face categorization There was an asymmetric relationship between emotion and age categorizations among faces; in contrast, there was an absence of asymmetry in healthy controls. This result supported the first hypothesis of the study. In patients with PNES, emotion categorization was easier than age categorization. Performance on the switch trials was slower than that on the repeat trials. There was a larger switch cost for the age categorization than for the emotion categorization. Patients with PNES showed more difficulty in switching attention from the emotion dimension of the faces than from the age dimension, thus a larger switch cost for the age dimension was exhibited. The performance for age decisions was slower than that for emotion decisions on the switch trials, which demonstrated that it was harder for patients with PNES to disengage attention from emotion which in turn produced cost on the computation of age dimension. It seems that their attentional system was biased towards different dimensions of faces. The results indicated
here that emotion categorization consumed more resources; therefore, the age categorization suffered. In patients with PNES, emotion categorization was faster than age categorization, and performance was less efficient on switch trials than on repeat trials. In contrast, in healthy controls, there was an absence of asymmetric relationship between emotion and age categorizations of faces. The absence of an asymmetry in healthy controls showed that the computation of emotion and age dimensions was performed with an equal speed. Thus, none of these two dimensions utilized more resources in their attentional system. The results are consistent with previous studies confirming the presence of bias in the attentional system of patients with PNES. In a masked emotion Stroop test, patients with PNES and healthy group showed similar response on neutral pictures while patients showed attentional biasness on angry stimuli [2] because functional connections are dysfunctional between brain areas such as the dorsolateral prefrontal cortex, anterior cingulate, and parietal cortex, which control emotion and sensorimotor and cognitive functioning [4,7]. Further, high levels of emotional dysregulation [32] and elevated cortisol levels [33] have been demonstrated in patients with PNES. 4.2. Task-switching and emotion regulation strategies The results of the current study showed that cognitive deficits in patients with PNES are linked with emotion regulation strategies. The group with PNES showed higher scores on emotion suppression than healthy controls. In contrast, patients with PNES employed less frequent reappraisal of cognitions than healthy individuals. Further, there were individual differences in emotion regulation strategies such as frequent use of emotion suppression, and less cognitive reappraisal produces higher switch cost(s). We can infer that strategies to regulate emotion modulate the ability to perceive faces. These results are consistent with those of previous studies suggesting that deliberately concealing emotions can have drastic physiological consequences such as stress and elevation of blood pressure [34]. Our results showed that inferior switching ability was associated with more frequent use of emotion suppression in patients with PNES. An attentional bias to expressions of emotions appeared which produced asymmetric switch costs during face categorizations. Suppression is basically a formal state of mind in which an individual consciously avoids the situation [35]. Suppression of emotions, thoughts, and feelings plays a major role in the development of psychopathology [36]. Conscious avoidance and expressive suppression are basically a part of attentional bias. Attentional bias can occur because of two reasons: (i) brain areas are not properly integrated and (ii) conscious avoidance or suppression of emotion. Stimulus recognition is a spontaneous mechanism, while expressive suppression or avoidance is a gradual process. When these two processes do not operate simultaneously, attentional bias occurs [37]. This result is in line with those of previous studies which demonstrated the maladaptive pattern of coping strategies in patients with PNES. Patients with psychogenic nonepileptic seizures adopt a more stressful lifestyle and repress their emotions and feelings compared with healthy individuals [38]. It has been shown that continuous suppression of distressing thoughts or avoidance of situations induces higher frequency of these thoughts [39]; thus, patients with PNES display an attentional bias towards facial emotion and suffer from a difficulty to disengage their attention from expressions of emotion. As a result, the nonemotion feature carries a greater switch cost. Our results demonstrated that cognitive reappraisal was another important strategy which influenced switching ability among patients with PNES. The less frequent use of cognitive reappraisal was associated with the inferior switching ability of patients with PNES. Cognitive reappraisal is the downregulation strategy that is used to reformulate an emotional experience in order to lessen the intensity of physiological arousal in response to an unpleasant emotional [23,40–42] and stressful [14,43] experience. Reappraisal induces changes in late positive potentials (as measured by event-related potentials) and improves salivary immunity gauged by secretory immunoglobulin
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which is associated with cognitive restructuring of negative emotions [44]. The less frequent usage of cognitive reappraisal in patients with PNES facilitates the concentration of attention on emotional stimuli; as a result, cognitive performance is interrupted. An altered activation in brain areas involved in emotion processing could be responsible for differential usage of emotion suppression and cognitive reappraisal in patients with PNES compared to healthy individuals. As observed here, the constant suppression of emotion and irregular reappraisal of cognitions facilitate cognitive inflexibility in patients with PNES. 4.3. Conclusion The data suggest that patients with PNES suffer from an attentional bias towards the categorization of facial attributes. Their attentional system consumes more resources when confronted with the emotion dimension of faces; therefore, a nonemotion task suffers as sufficient resources are not available for such categorizations. The cost that an attentional system bears is linked with a frequent use of emotion suppression and less frequent reappraisal of cognitions as emotion regulation strategies. The results of the current study have implications for psychotherapists, counselors, medical practitioners, and mental health practitioners and will help in understanding the mechanisms underlying face categorization, cognitive system, and emotion regulation. Future studies must examine whether the observed cognitive deficits in patients with PNES can be improved with training. Disclosure None of the authors has any conflict of interests to disclose. References [1] Brooks JL, Baker GA, Boon PA, Hendriksen JG, Mulder OG, Aldenkamn AP. Psychogenic non-epileptic seizures—definition, etiology, treatment and prognostic issues: a critical review. Seizure Eur J Epilepsy 2009;18:543–53. [2] Mellers JDC. The approach to patients with “non-epileptic seizures”. Postgrad Med J 2005;81(958):498–504. [3] Carreno M. Recognition of nonepileptic events. Semin Neurol 2008;28(3):297–304. [4] Baslet G. Psychogenic non-epileptic seizures: a model of their pathogenic mechanism. Seizure 2011;20:1–13. [5] Bakvis P, Roelofs K, Kuyk J, Edelbroek OM, Swinkels WAM, Spinhoven P, et al. Trauma, stress, and preconscious threat processing in patients with psychogenic nonepileptic seizures. Epilepsia 2009;50(5):1001–11. [6] Roberts NA, Burleson MH, Weber DJ, Larson A, Sergeant K, Devine MJ, et al. Emotion in psychogenic nonepileptic seizures: responses to affective pictures. Epilepsy Behav 2012;24:107–15. [7] Van der Kruijs SJ, Bodde NM, Vaessen MJ, Lazeron RH, Vonck K, Boon P. Functional connectivity of dissociation in patients with psychogenic non-epileptic seizures. J Neurol Neurosurg Psychiatry 2012;83(3):239–47. [8] Kalogjera-Sackellares D, Sackellares JC. Intellectual and neuropsychological features of patients with psychogenic pseudoseizures. Psychiatry Res 1999;86(1):73–84. [9] Strutt AM, Hill SW, Scott BM, Uber-Zak L, Fogel TG. A comprehensive neuropsychological profile of women with psychogenic nonepileptic seizures. Epilepsy Behav 2011;20:24–8. [10] Woolfolk RL, Allen LA, Tiu JE. New directions in the treatment of somatization. Psychiatr Clin N Am 2007;30(4):621–44. [11] Thompson R, Isaac CL, Rowse G, Tooth CL, Reuber M. What is it like to receive a diagnosis of nonepileptic? Epilepsy Behav 2009;14(3):508–15. [12] Mokleby K, Blomhoff S, Malt UF, Dahlstro MA, Tauboll E, Gjerstad L. Psychiatric comorbidity and hostility in patients with psychogenic nonepileptic seizures compared with somatoform disorders and healthy controls. Epilepsia 2002;43:193–8.
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