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ORIGINAL ARTICLE
Attentional biases in irritable bowel syndrome patients夽 Mladenka Tkalcic a, Drazen Domijan a, Sanda Pletikosic a, Mia Setic a, Goran Hauser b,∗ a
Department of Psychology, Faculty of Humanities and Social Sciences, University of Rijeka, Sveucilisna avenija 4, 51000 Rijeka, Croatia b Department of Internal Medicine, Division of Gastroenterology, Clinical Hospital Centre Rijeka, Kresimirova 42, 51000 Rijeka, Croatia
Summary Background and objective: According to the cognitive behavioural model of irritable bowel syndrome (IBS) selective attention to visceral stimuli is one of the pathophysiological mechanisms in IBS. We aimed to investigate attentional biases in patients with IBS and to explore the relationship between neuroticism, trait anxiety, visceral anxiety and indices of attentional biases. Methods: Twenty-seven patients completed the global/local task and the modified Stroop task (using 4 word categories: neutral, symptom-related, emotionally and situationally relevant) while 28 healthy persons completed the Stroop task only. Both groups also filled out a set of psychological questionnaires. Results: The results show two distinct attentional biases in patients with irritable bowel syndrome. The index of global precedence was negatively correlated with neuroticism (r = −.41, P < .05) while there was no correlation of global precedence with trait and visceral anxiety. We found Stroop facilitation (F[3,81] = 3.98, P < .02) specifically for situational threat words. Also, there were positive correlations between trait anxiety, visceral anxiety and the Stroop facilitation index for situational threat words (r = .43 and r = .47, P < .05). In the control group, we found neither Stroop facilitation nor interference. But, facilitation index of emotional words was positively correlated with neuroticism (r = .40, P < .05), which is in line with the ‘‘emotion congruent attentional bias’’ in the general population. Conclusions: Neuroticism was associated with the reduction in global precedence observed in the global/local task. Trait anxiety and visceral anxiety were associated with Stroop facilitation elicited by situational threat words, which are of particular concern for patients with irritable bowel syndrome. These specific situations do not elicit an attentional bias in healthy participants, which might indicate that the observed facilitation to situational threat words is unique for IBS patients. © 2014 Elsevier Masson SAS. All rights reserved. 夽
The work was conducted at Clinical Hospital Centre, Rijeka, Department of Gastroenterology. Corresponding author. Tel.: +385 51 658 826. E-mail address: [email protected] (G. Hauser). 2210-7401/$ – see front matter © 2014 Elsevier Masson SAS. All rights reserved. http://dx.doi.org/10.1016/j.clinre.2014.02.002 ∗
Please cite this article in press as: Tkalcic M, et al. Attentional biases in irritable bowel syndrome patients. Clin Res Hepatol Gastroenterol (2014), http://dx.doi.org/10.1016/j.clinre.2014.02.002
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Introduction Irritable bowel syndrome (IBS) is the most common chronic functional gastrointestinal disorder. The IBS symptom profile includes chronic abdominal pain or discomfort and alterations in bowel habits [1,2]. Most patients with IBS believe in a psychological dimension of their symptoms and agree that symptoms have a great impact on their quality of life [3]. Based on a biopsychosocial model [4,5] and a specific cognitive behavioural model of IBS [6] we emphasize the importance of understanding the mechanisms of symptoms generation in the absence of physical pathology. Enhanced perception and selective attention to visceral stimuli could be considered as a possible pathophysiological mechanism in IBS suggesting an important role of cognition in this disease [7—9]. Dysfunction of the digestive system may result in an altered perception of abdominal symptoms [8,9] as well as aberrant cerebral function [10]. Research shows that patients with functional intestinal disorders express attention-dependent alterations of central nervous system processing as well as a generally negative emotional tendency in their cognitive processing strategies [11,12]. Suggested interactions between attention and emotion are important especially within the context of generation and maintenance of GI symptoms in IBS. Several theories of attention to emotional material were proposed [13]. Mogg and Bradley’s [14] model of cognitive motivational analysis and Mathews and Mackintosh’s [15] model of a competitive activation network, pointed out that a valence or threat-evaluation system enhances the activation of any items identified as potentially threatening thereby increasing automatic selective attention to such items. The first model [14] proposed two cognitive structures mediating attention—emotion interaction: • valence evaluation system (VES) which automatically evaluates threat posed by the stimulus; • goal engagement system (GES), which controls current processing according to goals set by the individual. When VES is activated by the presence of a threatening stimulus it sends a signal to the GES, which interrupts current processing and orients attentional resources to the material signalled by the VES. Similarly, Mathews and Mackintosh’s [15] model proposed that the threat-evaluation system enhances the representation of threatening stimuli in the competition for attentional resources. The attentional models point to individual differences in attentional biases toward the threatening stimuli [6,16]. Motivated by the findings of previous research, we were interested in the way that patients with IBS process both non-affective and affective information. We used Navon’s classic global-local paradigm [17] to study hierarchical visual attention (non-affective information), and the emotional Stroop task to study attentional bias to emotionally relevant words (affective information) [13]. The big and small letters, used as stimuli in the globallocal paradigm, constitute two different levels in the hierarchy of perceptual organization. The larger letter
represents the global level, whereas the small letters represent the local level. Participants identify the letters more rapidly when the global rather than the local level is relevant. This is the global advantage effect [17]. It has been suggested that individuals with obsessive-compulsive personalities [18] and anxious persons [19] tend to focus on small local details in their surroundings. IBS patients are characterised by a wide range of affective disturbances, including symptoms of depression and anxiety [20]. We hypothesise that patients with IBS will show a similar effect of local precedence where response to a target letter is faster when it is presented at the local level, compared to the global level. Such a reverse pattern might arise due to anxiety symptoms, which can turn the attention set to the local level. Neuroticism is also higher in patients with IBS and it is associated with increased negative affect and anxiety [21—23]. It is assumed that neuroticism is a risk factor for chronic pain, one of the main symptoms of IBS [21]. Neuroticism is defined as a broad dimension of individual differences in the tendency to experience negative emotions and the expression of associated behavioural and cognitive traits [24]. It is reasonable to assume that patients with IBS will be more inconsistent in their performance on global/local task like individuals high in neuroticism [22]. The observed instability of cognitive operations could be related to their current worries, negative mood or somatosensory input [22,24] related to their GI symptoms. Labus et al. [25] have introduced the concept of anxiety about specific gastrointestinal sensations, which possibly plays a role in the maintenance and occurrence of IBS symptoms and is related to neuroticism and trait anxiety. Gastrointestinal (GI)-specific or visceral anxiety can be defined as the cognitive, affective, and behavioural responses arising from fear of GI sensations and symptoms, and the context in which these visceral sensations and symptoms occur [25,26]. We hypothesise that GI-specific anxiety, along with neuroticism and trait anxiety, could maintain IBS symptoms through biased attention to GI-related symptoms. Using the ‘‘emotional word recall paradigm’’, Posserud et al. [27] showed that IBS patients recall a greater proportion of GI sensation words. These findings indicate an attentional bias to GI stimuli and a hypervigilance to GI sensations in IBS patients. Hence, we decided to introduce the modified emotional Stroop task, to test the hypothesis that IBS patients show an attentional bias to GI symptom-related words, as well as emotionally relevant and situational threat words [28]. The emotional Stroop task has been used to demonstrate selective processing of threat-related cues in anxious individuals [9,29]. The main assumption is that greater attention should be paid to the content of particular emotional words, resulting in greater impairment of colour naming of these words [13]. Afzal et al. [7] showed that IBS patients selectively process gastrointestinal symptom-related words compared with neutral words, but only when they are presented subliminally. Using a modified exogenous cueing task, Martin and Chapman [29,30] showed altered attentional processing of social threat and pain words relative to neutral words in IBS patients. Contrary to the usual results obtained in studies using the emotional Stroop task, the authors showed that IBS patients have a faster orientation response to social
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threat and pain words than to neutral stimuli, supporting the hypothesis of an important role for the hypervigilance for GI symptoms, and contextual social stimuli [31,32]. Based on the biopsychosocial model of IBS [4,5], we focused on the role of cognitive processes in IBS symptom perpetuation, especially the relation between attention and emotion [13]. We assumed that IBS patients might perceive GI symptoms faster compared to neutral stimuli. Additionally, they may selectively pay attention to certain social situations they find potentially threatening and/or of particular concern for them (e.g. social events, travelling, etc.). This assumption is based on Mathews and Mackintosh’s [15] hypothesis that the threat-evaluation system activates automatic selective attention to any item identified as potentially threatening. This can primarily be applied to those IBS patients with high levels of neuroticism and anxiety. Taking all into consideration, the first aim of this study was to determine whether patients with IBS show any deviation from normal deployment of visual attention using the global-local task. The second aim was to investigate whether patients with IBS show an attentional bias to emotionally relevant words in the modified Stroop task. The third aim was to investigate the relationship between neuroticism, trait anxiety, GI-specific anxiety and indices of attentional bias.
Patients and methods Participants The sample consisted of 27 IBS patients recruited at the Gastroenterology Department of the Clinical Hospital Centre Rijeka. IBS was diagnosed based on Rome III criteria. Patients with severe chronic diseases of the gastrointestinal tract, severe psychiatric disorders (schizophrenia and other psychotic disorders, major depressive disorder and bipolar disorder) and malignancies were excluded from the study. Mean age of patients was 46.11 with an age range from 18 to 69 years (83% female). Most of the participants had a high school education (67%) or a university degree (24%). The majority of participants (70%) were married or living with a partner. Their duration of symptoms varied from 1 to 38 years (M = 7.97; SD = 8.19). No patients were taking anxiolytics or antidepressants, while less than half of the patients (39%) were taking medication for the treatment of gastrointestinal symptoms (Colospa retard, Controloc, Espumisan).
Table 1
The control group consisted of 28 persons with no history of IBS, matching IBS patients in age (M = 44.14), gender (85% female), educational level (54% high school education level) and marriage status (71.4%).
Questionnaires The questionnaires used in the study have previously been validated in Croatian. State-Trait Anxiety Inventory (STAIT) [33] was used to measure trait anxiety. It consists of 20 items, which are rated on a 5 point Likert Scale ranging from 0 (never) to 4 (always). The Big Five Inventory (BFI) [34] was used to measure personality traits included in the big five model: neuroticism, extraversion, openness, conscientiousness and agreeableness. The BFI consists of 44 items, each of which is rated on a 5 point scale ranging from 1 (strongly disagree) to 5 (strongly agree). For the purpose of this study, we used only neuroticism, an 8 item subscale, which refers to negative emotionality, such as feeling anxious, nervous, sad, worried and tense. For the measurement of anxiety related to GI sensations, symptoms or the contexts in which these may occur, we used the Visceral Sensitivity Index (VSI) [25], consisting of 15 items which are rated on a 5 point scale ranging from 0 (strongly disagree) to 4 (strongly agree). Table 1 shows the possible range for each questionnaire as well as means, standard deviations and Cronbach alphas obtained on these samples.
Apparatus and stimuli Stimulus presentation was controlled and response latency and accuracy were collected using a Pentium computer with a 17-inch CRT monitor. Global/local task [17] Each stimulus consisted of a large letter composed of small letters. There were four possible letters: A, H, L, and T. Letters A and H were targets. In the global condition, large letters A or H were composed of small letters, l or t. In the local condition, large letters L or T were composed of small letters, a or h. In each trial, either A or H is present but not both. The target letter appeared either on the global or the local level but never on both levels simultaneously.
Descriptive statistics for trait anxiety, neuroticism and visceral anxiety. SD
Cronbach ␣
Questionnaires
Participants
Possible range
M
Neuroticism (BFI)
IBS Control
8—40
24.89 20.59
4.73 6.12
.69 .86
STAI-T
IBS Control
0—80
37.61 27.54
11.05 11.32
.92 .91
VSI
IBS Control
0—60
30.43 5.04
14.64 4.59
.93 .77
BFI: Big Five Inventory; STAI-T: State-Trait Anxiety Inventory (trait anxiety); VSI: Visceral Sensitivity Index; IBS: irritable bowel syndrome.
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Emotional Stroop task The emotional Stroop task is a modified version of the classical Stroop task where emotionally relevant words are used instead of colour words [13]. The stimulus words selected for this task were presented either in red or orange colour, Arial font (lower case; size 28). We selected red and orange because they are similar enough to make the colour discrimination task difficult. This modified Stroop task was designed specifically for this study, therefore we are providing a detailed overview of the word selection procedure. A list of 65 words was given to 58 graduate students of the University of Rijeka. They rated the valence of each word (positive, neutral, negative) on a 7-point semantic differential scale (−3 to +3). The scores were recoded to a scale from 1 to 7 and average pleasantness of each word was calculated. Based on the concordance of the pleasantness ratings, 40 words were selected, 10 words for each of the categories: • GI symptom-related words — the most common IBS symptoms (e.g. pain, nausea, cramps); • emotionally relevant words — words denoting negative affectivity (e.g. worry, anxiety, shame); • situational threat words — words referring to places or situations which might be threatening to IBS patients (e.g. food, travel, toilette); • neutral words (e.g. flower, book, clock). Since pleasantness was rated by students almost all words from the third category were rated pleasant. But we assumed that these words might be unpleasant and threatening for IBS patients, thus the third word category was named situational threat words. Word frequency and pleasantness ratings for the selected words were compared across categories. There was no difference in word frequency across categories, F(3,36) = 2.50, P > .05. One-way ANOVA with word category as a betweenword factor showed a statistically significant main effect of word category, F(3,36) = 43.98, P < .001. There was no difference in pleasantness between GI symptom-related (M = 2.45) and emotionally relevant (M = 2.24) words, P > .10. There was no difference between situational threat (M = 5.28) and neutral words (M = 5.18), P > .10, suggesting that situational threat words were not perceived as unpleasant by the general population. Situational threat words were rated as more pleasant compared to GI symptom-related and emotionally relevant words (both Ps < .001) and neutral words were rated as more pleasant compared to GI symptom-related and emotionally relevant words (both Ps < .001).
Procedure The study protocol was approved by the Hospital’s Ethical Committee and all participants signed an informed consent form. The research was carried out in accordance with the Helsinki Declaration. Data was collected during 2012. The patients were recruited by a gastroenterologist during their regular medical check-up at the Clinical Hospital Centre Rijeka, where they were later tested individually. The control participants were tested individually at the Laboratory for Experimental Psychology, University of
Rijeka. Both groups of participants completed a set of questionnaires (BFI, STAI, VSI, respectively), followed by the global/local task and the modified Stroop task in the IBS group, and the modified Stroop task alone in the control group. Both groups of participants were instructed to respond as quickly and accurately as possible. The distance between the participants and the computer screen was about 72 cm. Global/local task In the global/local task, the trial consisted of three events. First, a fixation cross-appeared in the centre of the screen for 500 ms. Next, the stimulus appeared to the left or to the right of the fixation cross. The position of the stimulus was randomly chosen for each trial but both positions appeared equally often. The participant’s task was to decide whether letter A or H was presented on the screen by pressing the corresponding key on the computer keyboard. The stimulus remained on the screen until a response was made. After responding, feedback was provided with the word CORRECT if the response was accurate or with the word INCORRECT if the response was inaccurate. Feedback remained on the screen for 500 ms after which a new trial began. The participants completed 16 practice trials followed by 64 experimental trials. In the Stroop task, each trial started with the presentation of a word in the centre of the screen. The participants’ task was to decide whether the word was presented in red or orange colour and to press the corresponding key on the computer keyboard (C for red and N for orange; corresponding to the first letters of the colour names in Croatian). The word remained on the screen until a response was made after which a new trial began. There were 16 practice trials involving words not used in the main experiment followed by a single block of 160 experimental trials. Each word appeared twice in red and twice in orange colour. Order of word presentation was randomised across participants. Statistical analyses In order to determine whether patients with IBS show altered attentional functioning on the global/local task and the Stroop task, we performed analyses of variance. Reaction time (RT). Error trials were removed from the RT analysis (0.81% of data in the global/local task and 1.00% of data in the Stroop task). For each participant, we computed the median of the RT in each experimental condition in order to reduce the effect of outliers. We verified that conditions are met to perform parametric statistical procedures. In the global/local task, median reaction times were subjected to a 2 × 2 ANOVA with Target position (2 levels: global, local) and Target letter (2 levels: a, h) as a withinparticipants factors. In the Stroop task, median reaction times were subjected to a 2 × 4 ANOVA with Colour (2 levels: red, orange) and Word category (4 levels: GI symptomrelated, emotionally relevant, situational threat, neutral) as a within-participants factors. For data collected from IBS patients, as well as data from control participants, Mauchley’s test showed that there was no statistically significant deviation from the sphericity assumption for Word Category or for Word Category × Colour interaction (all Ws < 1, P > .10) indicating that there was no need for P-value adjustments.
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Accuracy. The same analyses were performed on arcsinetransformed accuracy rates in order to check for the presence of speed-accuracy trade off. Arcsine transformation was used because it normalizes the distribution of accuracy rates. For the Stroop task data from both of the groups, Mauchley’s test showed that there was no need for P-values adjustments for Word Category or for Word Category × Colour interaction (all Ws < 1, P > .10). Finally, in order to investigate the relationship between psychological measures and indices of attentional bias we performed Pearson’s correlations.
Results Global/local task Two-way ANOVA revealed a statistically significant main effect of Target position, F(1,26) = 20.56, P < .001 showing faster response when the target was positioned on the global (M = 829.32 ms, SE = 42.10) compared to the local level (M = 901.43 ms, SE = 42.37) indicating global advantage. There was a significant main effect of Target letter, F(1,26) = 5.64, P < .05, showing faster response to the letter A (M = 844.05 ms, SE = 37.16) compared to the letter H (M = 886.69 ms, SE = 47.50). This effect was of no theoretical importance so we will not discuss it further. There was no significant Target position × Target letter interaction, F(1,26) = 1.08, P > .10. Analysis of arcsine-transformed accuracy data revealed that there were no significant main effects of Target position, Target letter or their interaction (all Fs < 1, all Ps > .10). In order to investigate a relationship between performance on the global/local task and measures of individual differences in neuroticism, anxiety, and GI-specific anxiety, we computed a global precedence index by subtracting response latency to the global target from latency to the local target. Higher values of this index indicate greater global advantage. Descriptive data for all attentional indices are given in Table 2. The global precedence index was negatively correlated with neuroticism (r = −.41, P < .05) Table 2
suggesting that IBS patients with a higher level of neuroticism exhibit weaker global precedence. There was no significant correlation between the global precedence index with trait anxiety and GI-specific anxiety as shown in Table 2.
Stroop task Two-way ANOVA performed on the IBS patients’ data revealed a statistically significant main effect of Word Category, F(3,81) = 3.98, P < .02. Duncan’s post-hoc test showed that patients responded faster to situational threat words compared to neutral words (P < .02) suggesting a response facilitation by emotion congruent words. Responses to situational threat words were also faster compared to GI symptom-related (P < .02) and emotionally relevant words (P < .01). There was no difference in latency between emotionally relevant, GI symptom-related and neutral words (all Ps > .10). Post-hoc analysis revealed that there was no evidence for a Stroop-like interference in any of the three categories of relevant words. Rather, facilitation is observed specifically in response to words related to situations of major concern for the patients. There was no significant main effect of Colour (F < 1), and there was no Colour × Word Category interaction, F(3,81) = 1.42, P > .10. Two-way ANOVA with Word Category and Colour as withinparticipants factors revealed a significant main effect of Word Category, F(3,81) = 3.30; P < .05. That implies there was no speed-accuracy trade off because faster response times for situational threat words were accompanied with a greater accuracy level. As in the RT analysis, there was no significant main effect of Colour (F < 1), and there was no Colour × Word Category interaction (F < 1). In the same manner as in the global/local task, we computed a Stroop Facilitation Index by subtracting the response latency to symptom-related, emotionally relevant and situational threat words from the latency of neutral words. More positive values of this index are associated with a greater amount of facilitation. Conversely, more negative values are associated with a greater Stroop interference. The facilitation index of situational
Attention indices and self-report measures for IBS patients: correlations, means and standard deviations. 1.
2.
3.
4.
5a
5b
5c
1. Neuroticism (BFI) 2. STAI-T
.66b
3. VSI
.22
.34
4. Global Precedence Index
−.41a
−.14
.30
5. Stroop Facilitation Index for: a) Symptom-related words b) Emotional words c) Situational threat words
−.27 .09 .26
−.04 .33 .43a
.31 .30 .47a
Mean
24.89
37.61
30.43
72.11
−0.64
−5.69
19.12
SD
4.73
11.05
14.64
82.64
41.94
35.81
39.39
BFI: Big Five Inventory; STAI-T: State-Trait Anxiety Inventory (trait anxiety); VSI: Visceral Sensitivity Index; IBS: irritable bowel syndrome. a P < .05. b P < .01.
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threat words was positively correlated with trait anxiety (r = .43, P < .05) and with GI-specific anxiety (r = .47, P < .05). There was no statistically significant correlation between Stroop facilitation of situational threat words and neuroticism (r = .26, P > .05). The Stroop facilitation indexes of GI symptom-related and emotionally relevant words were not correlated with trait anxiety, neuroticism or GI-specific anxiety, as shown in Table 2. In order to test whether the observed Stroop facilitation and its relation to anxiety measures is specific for IBS patients, we performed the same analyses on the control group data. As expected, the control group had a significantly (P < 01) lower level of neuroticism (Mc = 20.59, SDc = 6.12) compared to IBS patients (Mibs = 24.89, SDibs = 4.73), as well as lower levels of trait anxiety (Mc = 27.54, SDc = 11.32; Mibs = 37.61, SDibs = 11.05), and lower levels of GI-specific anxiety (Mc = 5.04, SDc = 4.59; Mibs = 30.43, SDibs = 14.64), respectively. Although the control group expressed a lower mean result on neuroticism and trait anxiety than IBS patients, anxiety scores of both healthy and IBS participants vary similarly (SD ∼ 11). The two-way ANOVAs were performed on the control group data in the same manner as on the IBS data. There were no main effects of Word Category or Colour (all Fs < 1, Ps > .10) for RT or accuracy. There was no significant interaction for RT (F = 2.21, P < .10) or accuracy data (F = 1.97, P < .10). The facilitation index of emotionally relevant words was positively correlated with neuroticism (r = .40, P < .05) but there were no statistically significant correlations between the facilitation index of emotional words and trait anxiety (r = .28, P > .05) and GI-specific anxiety (r = .09, P > .05). The Stroop facilitation indexes of GI symptom-related and situational threat words were not correlated with anxiety, neuroticism or GI-specific anxiety.
Discussion The present study examined attention and its relationship with personality characteristics in patients with IBS. Apart from a few studies [7,29,30], cognitive and attentional processing in patients with IBS has not been thoroughly studied. We used Navon’s global/local task and the emotional Stroop task as measures of attentional processing and correlated them with self-reported neuroticism, trait anxiety and GIspecific anxiety. The findings of the present study should be interpreted with caution. As it is often the case when a clinical population is involved, the present study employed a small heterogeneous sample resulting in lower statistical power. Furthermore, testing was done in a hospital setting and not in the laboratory, which might induce additional anxiety that might bias the results. Additionally, when the natural group design is used, it is often difficult to assure that groups are comparable and it is possible to object that differences among groups might arise from some other uncontrollable factor. Also, the sample was predominantly female which limits the generalizability of our results. However, a high female predominance is one of the main features of IBS.
The main finding in the global-local paradigm is that participants responded faster to global compared to local targets, i.e. they showed processing preference for the global configuration over local parts [17,35]. We hypothesised that increased neuroticism could be associated with increased noise in dividing attentional resources between the global and the local level. Neurotic individuals might sometimes focus their attention to the global level first, but might prefer the local level at other times. Such a concurrent speed-up at the global and local level could lead to a reduction in global advantage. Consistent with the proposed hypothesis, we found that neuroticism is negatively correlated with the global precedence index suggesting that a higher level of neuroticism is associated with reduced global precedence. The lack of correlation of trait anxiety or GIspecific anxiety with the global precedence index indicates that heightened anxiety does not contribute to the performance in this task. This is consistent with the conclusion that anxiety specifically leads to attention bias toward threatening stimuli and it does not affect performance on stimuli without emotional valence [14,15]. Afzal et al. [7] used the emotional Stroop task to demonstrate interference from symptom-related words in patients with IBS. However, they used a block design where presentation of emotional and neutral words was grouped into separate blocks of trials. In this case, Stroop interference can arise merely as a consequence of cumulative exposure to stimuli of the same valence, which attract attention [36]. In order to avoid blocking, we mixed all of the words from the four categories into a single block. Instead of interference, we found evidence for Stroop facilitation to situational threat words only. The facilitation index is positively associated with trait anxiety and GI-specific anxiety. Increased anxiety and worries about visceral symptoms lead to a faster attentional engagement to situational threat words. Stroop facilitation is consistent with the findings of Chapman and Martin [30] who showed faster attentional engagement in the exogenous cueing task. Our results showed that patients were not concerned with symptoms or social threat per se, but rather with the social consequences of their illness (inability to go to a banquet or a social gathering), which seriously diminish the quality of their everyday life. Such concerns might lead to an increased sensitivity to visceral symptoms. On the other hand, these specific situations do not elicit an attentional bias in healthy participants, which might indicate that the observed facilitation to situational threat words is unique for IBS patients. However, healthy participants with heightened neuroticism have a tendency towards negative emotions, hence they react faster to negative emotional words compared to neutral words. This is in line with the commonly observed ‘‘emotion congruent attentional bias’’ in the general population [16]. Several theories were put forward to explain how emotions can guide attention. [13] As already described, two theoretical models, Mogg and Bradley’s [14], and Mathews and Mackintosh’s [15], can be used to explain the empirical findings of this study. Individual differences in the reactivity of the valence evaluation system (VES) can explain why anxious individuals might orient more toward threatening stimuli. Similarly, according to the second model [15], when the threat-evaluation system is overactive as in individuals
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Attentional biases in IBS with anxiety it will constantly bias attention toward threatening stimuli. It is interesting to note that although the correlation between neuroticism and trait anxiety was high (r = .66, P < .05) they showed different patterns of relationships with global precedence and Stroop facilitation, suggesting that they capture different components of the attentional system in IBS patients. In the context of Mogg and Bradley’s theory [14], we can speculate that the emotional Stroop task activates VES, which signals the presence of a threat to goal engagement system (GES). Heightened anxiety in patients with IBS might result in oversensitivity of VES specifically to situations, which they find threatening. Increased sensitivity leads to faster attentional engagement resulting in Stroop facilitation. On the other hand, we assume that performance in the global-local task is under the control of GES. Switching attention between global and local levels of analysis requires some form of mental control. Increased neuroticism might result in a poorer performance of the GES, and consequently with a poorer control over how to divide attention between the global structure and local details. This preliminary data may suggest an important role of attention in generating abdominal symptoms and could be used as a strategy to create a novel approach to the treatment of IBS. If these results would be replicated in future research, we may presume that various kinds of attention exercises could help patients to re-focus their attention from abdominal symptoms to other sources and to alleviate the symptoms of the disease [37]. This assumption is based on the core premise of the CBT approach that physiological, cognitive/affective and behavioural responses are interdependent and responsible for maintaining the disorder [38]. For this reason, changing cognitions, behaviour or both may indirectly reduce anxiety and lead to an improvement in symptoms. It is well known that relaxation and mindfulness techniques, as a part of the cognitive behavioural therapy approach, also include changes on the physiological, affective and attention levels and already serve as a useful approach in the treatment of IBS symptoms [39]. Despite the existing limitations, this study revealed interesting results, which deserve further research. In order to determine which characteristics of the disorder contribute to the observed attentional biases in IBS patients, it is necessary to examine whether similar patterns of attention exist in patients with other medical conditions, such as inflammatory bowel disease or celiac disease. These diseases are characterized by similar symptoms as IBS but their origins are different. Data obtained on these groups of patients could improve the understanding of the particular role of anxiety in maintaining IBS symptoms through biased attention as well as help in creating more successful treatment protocols. In conclusion, this study offers novel insights into the pattern of attentional biases in patients with IBS. Neuroticism was associated with the reduction in global precedence observed in the global/local task. Trait anxiety and visceral anxiety were associated with Stroop facilitation elicited by situational threat words, which are of particular concern for patients with irritable bowel syndrome. These specific situations do not elicit an attentional bias in healthy participants, which might indicate that the observed
7 facilitation to situational threat words is unique for IBS patients.
Disclosure of interest The authors declare that they have no conflicts of interest concerning this article.
Acknowledgements This study was funded by the Ministry of Science, Education and Sport, Republic of Croatia, Grant number 009-00926602655 and 009-0362214-0818 and by the Croatian Science Foundation grant 02.05/06.
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[29] Martin M, Chapman SC. Cognitive processing in putative functional gastrointestinal disorder: rumination yields orientation to social threat not pain. Eur J Pain 2010;14: 207—13. [30] Chapman SC, Martin M. Attention to pain words in irritable bowel syndrome: increased orienting and speeded engagement. Br J Health Psychol 2011;16: 47—60. [31] Hirsch CR, MacLeod C, Mathews A, Sandher O, Siyani A, Hayes S. The contribution of attentional bias to worry: distinguishing the roles of selective engagement and disengagement. J Anxiety Disord 2011;25:272—7. [32] Vuilleumier P, Huang YM. Emotional attention: uncovering the mechanisms of affective biases in perception. Curr Dir Psychol Sci 2009;18:148—52. [33] Spielberger CD, Gorsuch RL, Lushene R, Vagg PR, Jacobs GA. Manual for the State-Trait Anxiety Inventory. Palo Alto: Consulting Psychologists Press; 1983. [34] Benet-Martínez V, John OP. Los Cinco Grandes across cultures and ethnic groups: multitrait method analyses of the big five in Spanish and English. J Pers Soc Psychol 1998;75:729—50. [35] Shulman GL, Wilson J. Spatial frequency and selective attention to local and global information. Percept 1987;16:89—101. [36] McKenna FP, Sharma D. Reversing the emotional stroop effect reveals that it is not what it seems: the role of fast and slow components. J Exp Psychol Learn Mem Cogn 2004;30:382—92. [37] Rowlands L. The effect of perceptual training on somatosensory distortion in physical symptom reporters. Doctoral thesis. Manchester: University of Manchester; 2011. [38] Kennedy TM, Chalder T, McCrone P, Darnley S, Knapp M, Jones RH, et al. Cognitive behavioural therapy in addition to antispasmodic therapy for irritable bowel syndrome in primary care: randomised controlled trial. Health Technol Assess 2006;10:1—67. [39] Fjorback LO. Mindfulness and bodily distress. Dan Med J 2012;59(11):B4547.
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ORIGINAL ARTICLE
Attentional biases in irritable bowel syndrome patients夽 Mladenka Tkalcic a, Drazen Domijan a, Sanda Pletikosic a, Mia Setic a, Goran Hauser b,∗ a
Department of Psychology, Faculty of Humanities and Social Sciences, University of Rijeka, Sveucilisna avenija 4, 51000 Rijeka, Croatia b Department of Internal Medicine, Division of Gastroenterology, Clinical Hospital Centre Rijeka, Kresimirova 42, 51000 Rijeka, Croatia
Summary Background and objective: According to the cognitive behavioural model of irritable bowel syndrome (IBS) selective attention to visceral stimuli is one of the pathophysiological mechanisms in IBS. We aimed to investigate attentional biases in patients with IBS and to explore the relationship between neuroticism, trait anxiety, visceral anxiety and indices of attentional biases. Methods: Twenty-seven patients completed the global/local task and the modified Stroop task (using 4 word categories: neutral, symptom-related, emotionally and situationally relevant) while 28 healthy persons completed the Stroop task only. Both groups also filled out a set of psychological questionnaires. Results: The results show two distinct attentional biases in patients with irritable bowel syndrome. The index of global precedence was negatively correlated with neuroticism (r = −.41, P < .05) while there was no correlation of global precedence with trait and visceral anxiety. We found Stroop facilitation (F[3,81] = 3.98, P < .02) specifically for situational threat words. Also, there were positive correlations between trait anxiety, visceral anxiety and the Stroop facilitation index for situational threat words (r = .43 and r = .47, P < .05). In the control group, we found neither Stroop facilitation nor interference. But, facilitation index of emotional words was positively correlated with neuroticism (r = .40, P < .05), which is in line with the ‘‘emotion congruent attentional bias’’ in the general population. Conclusions: Neuroticism was associated with the reduction in global precedence observed in the global/local task. Trait anxiety and visceral anxiety were associated with Stroop facilitation elicited by situational threat words, which are of particular concern for patients with irritable bowel syndrome. These specific situations do not elicit an attentional bias in healthy participants, which might indicate that the observed facilitation to situational threat words is unique for IBS patients. © 2014 Elsevier Masson SAS. All rights reserved. 夽
The work was conducted at Clinical Hospital Centre, Rijeka, Department of Gastroenterology. Corresponding author. Tel.: +385 51 658 826. E-mail address: [email protected] (G. Hauser). 2210-7401/$ – see front matter © 2014 Elsevier Masson SAS. All rights reserved. http://dx.doi.org/10.1016/j.clinre.2014.02.002 ∗
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Introduction Irritable bowel syndrome (IBS) is the most common chronic functional gastrointestinal disorder. The IBS symptom profile includes chronic abdominal pain or discomfort and alterations in bowel habits [1,2]. Most patients with IBS believe in a psychological dimension of their symptoms and agree that symptoms have a great impact on their quality of life [3]. Based on a biopsychosocial model [4,5] and a specific cognitive behavioural model of IBS [6] we emphasize the importance of understanding the mechanisms of symptoms generation in the absence of physical pathology. Enhanced perception and selective attention to visceral stimuli could be considered as a possible pathophysiological mechanism in IBS suggesting an important role of cognition in this disease [7—9]. Dysfunction of the digestive system may result in an altered perception of abdominal symptoms [8,9] as well as aberrant cerebral function [10]. Research shows that patients with functional intestinal disorders express attention-dependent alterations of central nervous system processing as well as a generally negative emotional tendency in their cognitive processing strategies [11,12]. Suggested interactions between attention and emotion are important especially within the context of generation and maintenance of GI symptoms in IBS. Several theories of attention to emotional material were proposed [13]. Mogg and Bradley’s [14] model of cognitive motivational analysis and Mathews and Mackintosh’s [15] model of a competitive activation network, pointed out that a valence or threat-evaluation system enhances the activation of any items identified as potentially threatening thereby increasing automatic selective attention to such items. The first model [14] proposed two cognitive structures mediating attention—emotion interaction: • valence evaluation system (VES) which automatically evaluates threat posed by the stimulus; • goal engagement system (GES), which controls current processing according to goals set by the individual. When VES is activated by the presence of a threatening stimulus it sends a signal to the GES, which interrupts current processing and orients attentional resources to the material signalled by the VES. Similarly, Mathews and Mackintosh’s [15] model proposed that the threat-evaluation system enhances the representation of threatening stimuli in the competition for attentional resources. The attentional models point to individual differences in attentional biases toward the threatening stimuli [6,16]. Motivated by the findings of previous research, we were interested in the way that patients with IBS process both non-affective and affective information. We used Navon’s classic global-local paradigm [17] to study hierarchical visual attention (non-affective information), and the emotional Stroop task to study attentional bias to emotionally relevant words (affective information) [13]. The big and small letters, used as stimuli in the globallocal paradigm, constitute two different levels in the hierarchy of perceptual organization. The larger letter
represents the global level, whereas the small letters represent the local level. Participants identify the letters more rapidly when the global rather than the local level is relevant. This is the global advantage effect [17]. It has been suggested that individuals with obsessive-compulsive personalities [18] and anxious persons [19] tend to focus on small local details in their surroundings. IBS patients are characterised by a wide range of affective disturbances, including symptoms of depression and anxiety [20]. We hypothesise that patients with IBS will show a similar effect of local precedence where response to a target letter is faster when it is presented at the local level, compared to the global level. Such a reverse pattern might arise due to anxiety symptoms, which can turn the attention set to the local level. Neuroticism is also higher in patients with IBS and it is associated with increased negative affect and anxiety [21—23]. It is assumed that neuroticism is a risk factor for chronic pain, one of the main symptoms of IBS [21]. Neuroticism is defined as a broad dimension of individual differences in the tendency to experience negative emotions and the expression of associated behavioural and cognitive traits [24]. It is reasonable to assume that patients with IBS will be more inconsistent in their performance on global/local task like individuals high in neuroticism [22]. The observed instability of cognitive operations could be related to their current worries, negative mood or somatosensory input [22,24] related to their GI symptoms. Labus et al. [25] have introduced the concept of anxiety about specific gastrointestinal sensations, which possibly plays a role in the maintenance and occurrence of IBS symptoms and is related to neuroticism and trait anxiety. Gastrointestinal (GI)-specific or visceral anxiety can be defined as the cognitive, affective, and behavioural responses arising from fear of GI sensations and symptoms, and the context in which these visceral sensations and symptoms occur [25,26]. We hypothesise that GI-specific anxiety, along with neuroticism and trait anxiety, could maintain IBS symptoms through biased attention to GI-related symptoms. Using the ‘‘emotional word recall paradigm’’, Posserud et al. [27] showed that IBS patients recall a greater proportion of GI sensation words. These findings indicate an attentional bias to GI stimuli and a hypervigilance to GI sensations in IBS patients. Hence, we decided to introduce the modified emotional Stroop task, to test the hypothesis that IBS patients show an attentional bias to GI symptom-related words, as well as emotionally relevant and situational threat words [28]. The emotional Stroop task has been used to demonstrate selective processing of threat-related cues in anxious individuals [9,29]. The main assumption is that greater attention should be paid to the content of particular emotional words, resulting in greater impairment of colour naming of these words [13]. Afzal et al. [7] showed that IBS patients selectively process gastrointestinal symptom-related words compared with neutral words, but only when they are presented subliminally. Using a modified exogenous cueing task, Martin and Chapman [29,30] showed altered attentional processing of social threat and pain words relative to neutral words in IBS patients. Contrary to the usual results obtained in studies using the emotional Stroop task, the authors showed that IBS patients have a faster orientation response to social
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threat and pain words than to neutral stimuli, supporting the hypothesis of an important role for the hypervigilance for GI symptoms, and contextual social stimuli [31,32]. Based on the biopsychosocial model of IBS [4,5], we focused on the role of cognitive processes in IBS symptom perpetuation, especially the relation between attention and emotion [13]. We assumed that IBS patients might perceive GI symptoms faster compared to neutral stimuli. Additionally, they may selectively pay attention to certain social situations they find potentially threatening and/or of particular concern for them (e.g. social events, travelling, etc.). This assumption is based on Mathews and Mackintosh’s [15] hypothesis that the threat-evaluation system activates automatic selective attention to any item identified as potentially threatening. This can primarily be applied to those IBS patients with high levels of neuroticism and anxiety. Taking all into consideration, the first aim of this study was to determine whether patients with IBS show any deviation from normal deployment of visual attention using the global-local task. The second aim was to investigate whether patients with IBS show an attentional bias to emotionally relevant words in the modified Stroop task. The third aim was to investigate the relationship between neuroticism, trait anxiety, GI-specific anxiety and indices of attentional bias.
Patients and methods Participants The sample consisted of 27 IBS patients recruited at the Gastroenterology Department of the Clinical Hospital Centre Rijeka. IBS was diagnosed based on Rome III criteria. Patients with severe chronic diseases of the gastrointestinal tract, severe psychiatric disorders (schizophrenia and other psychotic disorders, major depressive disorder and bipolar disorder) and malignancies were excluded from the study. Mean age of patients was 46.11 with an age range from 18 to 69 years (83% female). Most of the participants had a high school education (67%) or a university degree (24%). The majority of participants (70%) were married or living with a partner. Their duration of symptoms varied from 1 to 38 years (M = 7.97; SD = 8.19). No patients were taking anxiolytics or antidepressants, while less than half of the patients (39%) were taking medication for the treatment of gastrointestinal symptoms (Colospa retard, Controloc, Espumisan).
Table 1
The control group consisted of 28 persons with no history of IBS, matching IBS patients in age (M = 44.14), gender (85% female), educational level (54% high school education level) and marriage status (71.4%).
Questionnaires The questionnaires used in the study have previously been validated in Croatian. State-Trait Anxiety Inventory (STAIT) [33] was used to measure trait anxiety. It consists of 20 items, which are rated on a 5 point Likert Scale ranging from 0 (never) to 4 (always). The Big Five Inventory (BFI) [34] was used to measure personality traits included in the big five model: neuroticism, extraversion, openness, conscientiousness and agreeableness. The BFI consists of 44 items, each of which is rated on a 5 point scale ranging from 1 (strongly disagree) to 5 (strongly agree). For the purpose of this study, we used only neuroticism, an 8 item subscale, which refers to negative emotionality, such as feeling anxious, nervous, sad, worried and tense. For the measurement of anxiety related to GI sensations, symptoms or the contexts in which these may occur, we used the Visceral Sensitivity Index (VSI) [25], consisting of 15 items which are rated on a 5 point scale ranging from 0 (strongly disagree) to 4 (strongly agree). Table 1 shows the possible range for each questionnaire as well as means, standard deviations and Cronbach alphas obtained on these samples.
Apparatus and stimuli Stimulus presentation was controlled and response latency and accuracy were collected using a Pentium computer with a 17-inch CRT monitor. Global/local task [17] Each stimulus consisted of a large letter composed of small letters. There were four possible letters: A, H, L, and T. Letters A and H were targets. In the global condition, large letters A or H were composed of small letters, l or t. In the local condition, large letters L or T were composed of small letters, a or h. In each trial, either A or H is present but not both. The target letter appeared either on the global or the local level but never on both levels simultaneously.
Descriptive statistics for trait anxiety, neuroticism and visceral anxiety. SD
Cronbach ␣
Questionnaires
Participants
Possible range
M
Neuroticism (BFI)
IBS Control
8—40
24.89 20.59
4.73 6.12
.69 .86
STAI-T
IBS Control
0—80
37.61 27.54
11.05 11.32
.92 .91
VSI
IBS Control
0—60
30.43 5.04
14.64 4.59
.93 .77
BFI: Big Five Inventory; STAI-T: State-Trait Anxiety Inventory (trait anxiety); VSI: Visceral Sensitivity Index; IBS: irritable bowel syndrome.
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Emotional Stroop task The emotional Stroop task is a modified version of the classical Stroop task where emotionally relevant words are used instead of colour words [13]. The stimulus words selected for this task were presented either in red or orange colour, Arial font (lower case; size 28). We selected red and orange because they are similar enough to make the colour discrimination task difficult. This modified Stroop task was designed specifically for this study, therefore we are providing a detailed overview of the word selection procedure. A list of 65 words was given to 58 graduate students of the University of Rijeka. They rated the valence of each word (positive, neutral, negative) on a 7-point semantic differential scale (−3 to +3). The scores were recoded to a scale from 1 to 7 and average pleasantness of each word was calculated. Based on the concordance of the pleasantness ratings, 40 words were selected, 10 words for each of the categories: • GI symptom-related words — the most common IBS symptoms (e.g. pain, nausea, cramps); • emotionally relevant words — words denoting negative affectivity (e.g. worry, anxiety, shame); • situational threat words — words referring to places or situations which might be threatening to IBS patients (e.g. food, travel, toilette); • neutral words (e.g. flower, book, clock). Since pleasantness was rated by students almost all words from the third category were rated pleasant. But we assumed that these words might be unpleasant and threatening for IBS patients, thus the third word category was named situational threat words. Word frequency and pleasantness ratings for the selected words were compared across categories. There was no difference in word frequency across categories, F(3,36) = 2.50, P > .05. One-way ANOVA with word category as a betweenword factor showed a statistically significant main effect of word category, F(3,36) = 43.98, P < .001. There was no difference in pleasantness between GI symptom-related (M = 2.45) and emotionally relevant (M = 2.24) words, P > .10. There was no difference between situational threat (M = 5.28) and neutral words (M = 5.18), P > .10, suggesting that situational threat words were not perceived as unpleasant by the general population. Situational threat words were rated as more pleasant compared to GI symptom-related and emotionally relevant words (both Ps < .001) and neutral words were rated as more pleasant compared to GI symptom-related and emotionally relevant words (both Ps < .001).
Procedure The study protocol was approved by the Hospital’s Ethical Committee and all participants signed an informed consent form. The research was carried out in accordance with the Helsinki Declaration. Data was collected during 2012. The patients were recruited by a gastroenterologist during their regular medical check-up at the Clinical Hospital Centre Rijeka, where they were later tested individually. The control participants were tested individually at the Laboratory for Experimental Psychology, University of
Rijeka. Both groups of participants completed a set of questionnaires (BFI, STAI, VSI, respectively), followed by the global/local task and the modified Stroop task in the IBS group, and the modified Stroop task alone in the control group. Both groups of participants were instructed to respond as quickly and accurately as possible. The distance between the participants and the computer screen was about 72 cm. Global/local task In the global/local task, the trial consisted of three events. First, a fixation cross-appeared in the centre of the screen for 500 ms. Next, the stimulus appeared to the left or to the right of the fixation cross. The position of the stimulus was randomly chosen for each trial but both positions appeared equally often. The participant’s task was to decide whether letter A or H was presented on the screen by pressing the corresponding key on the computer keyboard. The stimulus remained on the screen until a response was made. After responding, feedback was provided with the word CORRECT if the response was accurate or with the word INCORRECT if the response was inaccurate. Feedback remained on the screen for 500 ms after which a new trial began. The participants completed 16 practice trials followed by 64 experimental trials. In the Stroop task, each trial started with the presentation of a word in the centre of the screen. The participants’ task was to decide whether the word was presented in red or orange colour and to press the corresponding key on the computer keyboard (C for red and N for orange; corresponding to the first letters of the colour names in Croatian). The word remained on the screen until a response was made after which a new trial began. There were 16 practice trials involving words not used in the main experiment followed by a single block of 160 experimental trials. Each word appeared twice in red and twice in orange colour. Order of word presentation was randomised across participants. Statistical analyses In order to determine whether patients with IBS show altered attentional functioning on the global/local task and the Stroop task, we performed analyses of variance. Reaction time (RT). Error trials were removed from the RT analysis (0.81% of data in the global/local task and 1.00% of data in the Stroop task). For each participant, we computed the median of the RT in each experimental condition in order to reduce the effect of outliers. We verified that conditions are met to perform parametric statistical procedures. In the global/local task, median reaction times were subjected to a 2 × 2 ANOVA with Target position (2 levels: global, local) and Target letter (2 levels: a, h) as a withinparticipants factors. In the Stroop task, median reaction times were subjected to a 2 × 4 ANOVA with Colour (2 levels: red, orange) and Word category (4 levels: GI symptomrelated, emotionally relevant, situational threat, neutral) as a within-participants factors. For data collected from IBS patients, as well as data from control participants, Mauchley’s test showed that there was no statistically significant deviation from the sphericity assumption for Word Category or for Word Category × Colour interaction (all Ws < 1, P > .10) indicating that there was no need for P-value adjustments.
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Accuracy. The same analyses were performed on arcsinetransformed accuracy rates in order to check for the presence of speed-accuracy trade off. Arcsine transformation was used because it normalizes the distribution of accuracy rates. For the Stroop task data from both of the groups, Mauchley’s test showed that there was no need for P-values adjustments for Word Category or for Word Category × Colour interaction (all Ws < 1, P > .10). Finally, in order to investigate the relationship between psychological measures and indices of attentional bias we performed Pearson’s correlations.
Results Global/local task Two-way ANOVA revealed a statistically significant main effect of Target position, F(1,26) = 20.56, P < .001 showing faster response when the target was positioned on the global (M = 829.32 ms, SE = 42.10) compared to the local level (M = 901.43 ms, SE = 42.37) indicating global advantage. There was a significant main effect of Target letter, F(1,26) = 5.64, P < .05, showing faster response to the letter A (M = 844.05 ms, SE = 37.16) compared to the letter H (M = 886.69 ms, SE = 47.50). This effect was of no theoretical importance so we will not discuss it further. There was no significant Target position × Target letter interaction, F(1,26) = 1.08, P > .10. Analysis of arcsine-transformed accuracy data revealed that there were no significant main effects of Target position, Target letter or their interaction (all Fs < 1, all Ps > .10). In order to investigate a relationship between performance on the global/local task and measures of individual differences in neuroticism, anxiety, and GI-specific anxiety, we computed a global precedence index by subtracting response latency to the global target from latency to the local target. Higher values of this index indicate greater global advantage. Descriptive data for all attentional indices are given in Table 2. The global precedence index was negatively correlated with neuroticism (r = −.41, P < .05) Table 2
suggesting that IBS patients with a higher level of neuroticism exhibit weaker global precedence. There was no significant correlation between the global precedence index with trait anxiety and GI-specific anxiety as shown in Table 2.
Stroop task Two-way ANOVA performed on the IBS patients’ data revealed a statistically significant main effect of Word Category, F(3,81) = 3.98, P < .02. Duncan’s post-hoc test showed that patients responded faster to situational threat words compared to neutral words (P < .02) suggesting a response facilitation by emotion congruent words. Responses to situational threat words were also faster compared to GI symptom-related (P < .02) and emotionally relevant words (P < .01). There was no difference in latency between emotionally relevant, GI symptom-related and neutral words (all Ps > .10). Post-hoc analysis revealed that there was no evidence for a Stroop-like interference in any of the three categories of relevant words. Rather, facilitation is observed specifically in response to words related to situations of major concern for the patients. There was no significant main effect of Colour (F < 1), and there was no Colour × Word Category interaction, F(3,81) = 1.42, P > .10. Two-way ANOVA with Word Category and Colour as withinparticipants factors revealed a significant main effect of Word Category, F(3,81) = 3.30; P < .05. That implies there was no speed-accuracy trade off because faster response times for situational threat words were accompanied with a greater accuracy level. As in the RT analysis, there was no significant main effect of Colour (F < 1), and there was no Colour × Word Category interaction (F < 1). In the same manner as in the global/local task, we computed a Stroop Facilitation Index by subtracting the response latency to symptom-related, emotionally relevant and situational threat words from the latency of neutral words. More positive values of this index are associated with a greater amount of facilitation. Conversely, more negative values are associated with a greater Stroop interference. The facilitation index of situational
Attention indices and self-report measures for IBS patients: correlations, means and standard deviations. 1.
2.
3.
4.
5a
5b
5c
1. Neuroticism (BFI) 2. STAI-T
.66b
3. VSI
.22
.34
4. Global Precedence Index
−.41a
−.14
.30
5. Stroop Facilitation Index for: a) Symptom-related words b) Emotional words c) Situational threat words
−.27 .09 .26
−.04 .33 .43a
.31 .30 .47a
Mean
24.89
37.61
30.43
72.11
−0.64
−5.69
19.12
SD
4.73
11.05
14.64
82.64
41.94
35.81
39.39
BFI: Big Five Inventory; STAI-T: State-Trait Anxiety Inventory (trait anxiety); VSI: Visceral Sensitivity Index; IBS: irritable bowel syndrome. a P < .05. b P < .01.
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threat words was positively correlated with trait anxiety (r = .43, P < .05) and with GI-specific anxiety (r = .47, P < .05). There was no statistically significant correlation between Stroop facilitation of situational threat words and neuroticism (r = .26, P > .05). The Stroop facilitation indexes of GI symptom-related and emotionally relevant words were not correlated with trait anxiety, neuroticism or GI-specific anxiety, as shown in Table 2. In order to test whether the observed Stroop facilitation and its relation to anxiety measures is specific for IBS patients, we performed the same analyses on the control group data. As expected, the control group had a significantly (P < 01) lower level of neuroticism (Mc = 20.59, SDc = 6.12) compared to IBS patients (Mibs = 24.89, SDibs = 4.73), as well as lower levels of trait anxiety (Mc = 27.54, SDc = 11.32; Mibs = 37.61, SDibs = 11.05), and lower levels of GI-specific anxiety (Mc = 5.04, SDc = 4.59; Mibs = 30.43, SDibs = 14.64), respectively. Although the control group expressed a lower mean result on neuroticism and trait anxiety than IBS patients, anxiety scores of both healthy and IBS participants vary similarly (SD ∼ 11). The two-way ANOVAs were performed on the control group data in the same manner as on the IBS data. There were no main effects of Word Category or Colour (all Fs < 1, Ps > .10) for RT or accuracy. There was no significant interaction for RT (F = 2.21, P < .10) or accuracy data (F = 1.97, P < .10). The facilitation index of emotionally relevant words was positively correlated with neuroticism (r = .40, P < .05) but there were no statistically significant correlations between the facilitation index of emotional words and trait anxiety (r = .28, P > .05) and GI-specific anxiety (r = .09, P > .05). The Stroop facilitation indexes of GI symptom-related and situational threat words were not correlated with anxiety, neuroticism or GI-specific anxiety.
Discussion The present study examined attention and its relationship with personality characteristics in patients with IBS. Apart from a few studies [7,29,30], cognitive and attentional processing in patients with IBS has not been thoroughly studied. We used Navon’s global/local task and the emotional Stroop task as measures of attentional processing and correlated them with self-reported neuroticism, trait anxiety and GIspecific anxiety. The findings of the present study should be interpreted with caution. As it is often the case when a clinical population is involved, the present study employed a small heterogeneous sample resulting in lower statistical power. Furthermore, testing was done in a hospital setting and not in the laboratory, which might induce additional anxiety that might bias the results. Additionally, when the natural group design is used, it is often difficult to assure that groups are comparable and it is possible to object that differences among groups might arise from some other uncontrollable factor. Also, the sample was predominantly female which limits the generalizability of our results. However, a high female predominance is one of the main features of IBS.
The main finding in the global-local paradigm is that participants responded faster to global compared to local targets, i.e. they showed processing preference for the global configuration over local parts [17,35]. We hypothesised that increased neuroticism could be associated with increased noise in dividing attentional resources between the global and the local level. Neurotic individuals might sometimes focus their attention to the global level first, but might prefer the local level at other times. Such a concurrent speed-up at the global and local level could lead to a reduction in global advantage. Consistent with the proposed hypothesis, we found that neuroticism is negatively correlated with the global precedence index suggesting that a higher level of neuroticism is associated with reduced global precedence. The lack of correlation of trait anxiety or GIspecific anxiety with the global precedence index indicates that heightened anxiety does not contribute to the performance in this task. This is consistent with the conclusion that anxiety specifically leads to attention bias toward threatening stimuli and it does not affect performance on stimuli without emotional valence [14,15]. Afzal et al. [7] used the emotional Stroop task to demonstrate interference from symptom-related words in patients with IBS. However, they used a block design where presentation of emotional and neutral words was grouped into separate blocks of trials. In this case, Stroop interference can arise merely as a consequence of cumulative exposure to stimuli of the same valence, which attract attention [36]. In order to avoid blocking, we mixed all of the words from the four categories into a single block. Instead of interference, we found evidence for Stroop facilitation to situational threat words only. The facilitation index is positively associated with trait anxiety and GI-specific anxiety. Increased anxiety and worries about visceral symptoms lead to a faster attentional engagement to situational threat words. Stroop facilitation is consistent with the findings of Chapman and Martin [30] who showed faster attentional engagement in the exogenous cueing task. Our results showed that patients were not concerned with symptoms or social threat per se, but rather with the social consequences of their illness (inability to go to a banquet or a social gathering), which seriously diminish the quality of their everyday life. Such concerns might lead to an increased sensitivity to visceral symptoms. On the other hand, these specific situations do not elicit an attentional bias in healthy participants, which might indicate that the observed facilitation to situational threat words is unique for IBS patients. However, healthy participants with heightened neuroticism have a tendency towards negative emotions, hence they react faster to negative emotional words compared to neutral words. This is in line with the commonly observed ‘‘emotion congruent attentional bias’’ in the general population [16]. Several theories were put forward to explain how emotions can guide attention. [13] As already described, two theoretical models, Mogg and Bradley’s [14], and Mathews and Mackintosh’s [15], can be used to explain the empirical findings of this study. Individual differences in the reactivity of the valence evaluation system (VES) can explain why anxious individuals might orient more toward threatening stimuli. Similarly, according to the second model [15], when the threat-evaluation system is overactive as in individuals
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Attentional biases in IBS with anxiety it will constantly bias attention toward threatening stimuli. It is interesting to note that although the correlation between neuroticism and trait anxiety was high (r = .66, P < .05) they showed different patterns of relationships with global precedence and Stroop facilitation, suggesting that they capture different components of the attentional system in IBS patients. In the context of Mogg and Bradley’s theory [14], we can speculate that the emotional Stroop task activates VES, which signals the presence of a threat to goal engagement system (GES). Heightened anxiety in patients with IBS might result in oversensitivity of VES specifically to situations, which they find threatening. Increased sensitivity leads to faster attentional engagement resulting in Stroop facilitation. On the other hand, we assume that performance in the global-local task is under the control of GES. Switching attention between global and local levels of analysis requires some form of mental control. Increased neuroticism might result in a poorer performance of the GES, and consequently with a poorer control over how to divide attention between the global structure and local details. This preliminary data may suggest an important role of attention in generating abdominal symptoms and could be used as a strategy to create a novel approach to the treatment of IBS. If these results would be replicated in future research, we may presume that various kinds of attention exercises could help patients to re-focus their attention from abdominal symptoms to other sources and to alleviate the symptoms of the disease [37]. This assumption is based on the core premise of the CBT approach that physiological, cognitive/affective and behavioural responses are interdependent and responsible for maintaining the disorder [38]. For this reason, changing cognitions, behaviour or both may indirectly reduce anxiety and lead to an improvement in symptoms. It is well known that relaxation and mindfulness techniques, as a part of the cognitive behavioural therapy approach, also include changes on the physiological, affective and attention levels and already serve as a useful approach in the treatment of IBS symptoms [39]. Despite the existing limitations, this study revealed interesting results, which deserve further research. In order to determine which characteristics of the disorder contribute to the observed attentional biases in IBS patients, it is necessary to examine whether similar patterns of attention exist in patients with other medical conditions, such as inflammatory bowel disease or celiac disease. These diseases are characterized by similar symptoms as IBS but their origins are different. Data obtained on these groups of patients could improve the understanding of the particular role of anxiety in maintaining IBS symptoms through biased attention as well as help in creating more successful treatment protocols. In conclusion, this study offers novel insights into the pattern of attentional biases in patients with IBS. Neuroticism was associated with the reduction in global precedence observed in the global/local task. Trait anxiety and visceral anxiety were associated with Stroop facilitation elicited by situational threat words, which are of particular concern for patients with irritable bowel syndrome. These specific situations do not elicit an attentional bias in healthy participants, which might indicate that the observed
7 facilitation to situational threat words is unique for IBS patients.
Disclosure of interest The authors declare that they have no conflicts of interest concerning this article.
Acknowledgements This study was funded by the Ministry of Science, Education and Sport, Republic of Croatia, Grant number 009-00926602655 and 009-0362214-0818 and by the Croatian Science Foundation grant 02.05/06.
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