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Perception bias of disgust in ambiguous facial expressions in obsessive–compulsive disorder
Psychiatry Research 178 (2010) 126–131
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Psychiatry Research j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p s yc h r e s
Perception bias of disgust in ambiguous facial expressions in obsessive–compulsive disorder Kyungun Jhung a, Kee Namkoong a, Jee In Kang a,b, Ra Yeon Ha a, Suk Kyoon An a, Chan-Hyung Kim a, Se Joo Kim a,⁎ a b
Department of Psychiatry and Institute of Behavioral Science in Medicine, Yonsei University, College of Medicine, 250 Seongsan-no, Seodamun-gu, Seoul, South Korea Department of Psychiatry, Ilsan Hospital, National Health Insurance Corporation, Goyang, Gyeonggi-do, South Korea
a r t i c l e
i n f o
Article history: Received 8 December 2008 Received in revised form 20 November 2009 Accepted 21 November 2009 Keywords: Disgust Facial expressions Ambiguous stimuli OCD Symptom dimensions Disgust Scale
a b s t r a c t Impaired recognition of facial expressions of disgust has been suggested for patients with obsessive– compulsive disorder (OCD). This study aimed to compare the perception of negative emotions by OCD patients and controls using both non-ambiguous and ambiguous facial expressions. Forty-one OCD patients and thirtyseven controls performed the computerised emotion perception task. There were no differences between OCD patients and controls in the frequency of correct identification of non-ambiguous facial expressions. However, OCD patients were more likely to perceive disgust and less likely to perceive anger in response to ambiguous facial expressions when controlling for covariates. In OCD patients, a higher cleaning dimension was associated with a lower perception of anger and a higher perception of disgust when presented with ambiguous facial expressions. The domains of core disgust and contamination-based disgust domains of disgust sensitivity were positively correlated with the perception of ambiguous facial expressions as disgust, as well as cleaning symptom dimension scores. Our findings suggest that OCD patients, particularly those with higher washing/ contamination symptoms, are more likely to perceive disgust in ambiguous facial expressions. © 2009 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Disgust is thought to underlie various psychiatric illnesses. Initially defined as a revulsion response to distasteful foods (Darwin and Ekman, 1998), the current concept of disgust now also includes responses to a wide range of stimuli, such as poor hygiene, potential for disease and violations of the normal body envelope (Rozin and Fallon, 1987). At its core, disgust functions to prevent contamination and disease (Darwin and Ekman, 1998) by the characteristic behavioural dimension of avoidance (Rozin and Fallon, 1987). Disgust also has specific physiological manifestations, such as nausea and a distinct facial expression of narrowed nostrils, wrinkling of the brow and raising of the upper lip (Phillips et al., 1998; Rozin et al., 1994). From a developmental perspective, perception of disgust is thought to be absent at birth and to develop during childhood (Rozin and Fallon, 1987). The learning process is thought to occur through experience with other peoples' disgust, and to involve the identification of disgust-eliciting stimuli, the recognition of other peoples' facial expressions of disgust, and the correlation between the two (Sprengelmeyer et al., 1996). If there is a dysfunction in this appraisal process, the stimuli that elicit disgust in those with a dysfunction may
⁎ Corresponding author. Tel.: + 82 2 2228 1620; fax: + 82 2 313 0891. E-mail address: [email protected] (S.J. Kim). 0165-1781/$ – see front matter © 2009 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.psychres.2009.11.023
be dissimilar from the stimuli that elicit disgust in others (Sprengelmeyer et al., 1996). Impairment in this disgust appraisal process has been suggested to be closely related to obsessive–compulsive disorder (OCD). OCD is a relatively common disorder, characterised by persistent and unwanted thoughts and ritualistic behaviour. Among the heterogeneous symptoms of OCD, concerns with contamination are commonly involved. OCD patients often exhibit heightened appraisals of vulnerability to infection and spread of contamination in response to offensive objects, which elicit washing compulsions (Olatunji and McKay, 2007). Because the situations in which OCD patients experience disgust are different from those in which normal individuals experience disgust, it has been hypothesised that the learned association between the emotion of disgust and the facial expressions of disgust may have failed to develop (Sprengelmeyer et al., 1997). Experimental support for this theory of disgust perception in OCD, however, has been mixed. Sprengelmeyer et al. (1997) reported that all OCD patients examined showed a distinct and significant impairment in recognising facial expressions of disgust. However, subsequent studies have not revealed a clear association between OCD and the failure to recognise facial expressions of disgust. Parker et al. (2004) and Buhlmann et al. (2004) both reported no significant differences between OCD patients and normal controls with respect to facial expression recognition. In a more recent study, the results of Sprengelmeyer et al. (1997) were replicated, but the magnitude of the
K. Jhung et al. / Psychiatry Research 178 (2010) 126–131
effect was much smaller — only about a third of OCD subjects showed the impairment (Corcoran et al., 2008). These previous studies used non-ambiguous facial expressions to assess the responses of OCD patients, which could result in other important aspects of disgust perception being missed. Ambiguous facial expressions may further our understanding of emotion perception (Kee et al., 2006; Pollak and Kistler, 2002). Whereas non-ambiguous facial expressions are helpful in assessing facial emotion recognition, ambiguous facial expressions reveal whether individuals have a perception bias towards a certain emotion. Furthermore, due to the heterogeneity of OCD, some researchers have hypothesised that only a subset of OCD patients may have altered disgust perception, particularly those with contamination/ washing symptoms (Power and Dalgleish, 2008). Several studies have reported an association between contamination fear and disgust sensitivity (Mancini et al., 2001; Olatunji et al., 2004; Woody and Tolin, 2002), but the association between contamination fear and disgust perception has not been previously investigated. In the present study, we recruited OCD patients and healthy controls for the following purposes: (1) to compare their emotion recognition of non-ambiguous facial expressions, (2) to test if there are any perception biases in the classification of ambiguous facial expressions, especially the emotion of disgust, (3) to determine if the particular OCD symptom dimension of cleaning is associated with disgust perception and (4) to evaluate the domains of disgust sensitivity associated with disgust perception and the cleaning dimension of OCD. 2. Materials and methods 2.1. Participants Forty-one primary OCD patients were recruited from the psychiatric outpatient clinic of Severance Hospital, Yonsei University Medical Center. Patients were interviewed and diagnosed by experienced psychiatrists on the basis of the structured clinical interview for Diagnostic and Statistical Manual of Mental Disorders, fourth edition Diagnostic and Statistical Manual of Mental Disorders, fourth edition (DSM-IV) (SCID-CV) (First et al., 1997). Those with co-morbid diagnoses were included under the condition that OCD was the main reason for their visit. Exclusion criteria were substance abuse, psychosis or any neurological or medical condition that could affect the subject's performance. Thirty-seven normal controls were selected to match the OCD group for sex, age, and education level. SCID-CV was used to ensure that the normal controls had no history or current symptoms of neurological or psychiatric disorders and were not on any medication. 2.2. Measures For the OCD subjects, the Yale-Brown Obsessive-Compulsive Scale (Y-BOCS) and Y-BOCS Symptom Checklist (Goodman et al., 1989) was used to assess the severity and types of OC symptoms. A score of 0, 1 or 2 was assigned to each of the symptom categories of the Y-BOCS Symptom Checklist as follows: 0 if the patient did not have any of the symptoms under the category; 1 if the patient had at least one symptom, but not the principal symptom, under the category; or 2 if the principal symptom was under the symptom category. Using the four dimensional factors (symmetry, forbidden thoughts, cleaning and hoarding) identified by Bloch et al. (2008) in their meta-analysis, the sum of the scores for the symptom categories under each
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dimensional factor was the score for that dimension. Psychiatrists administered the Y-BOCS on the day the emotion perception task was performed. In both OCD and control groups, the severity of depressive symptoms was measured using the Montgomery–Asberg Depression Rating Scale (MADRS) (Davidson et al., 1986). To measure disgust sensitivity, all participants completed the Disgust Scale (Haidt et al., 1994), which includes seven domains of disgust elicitors i.e., food, animals, body products, body envelope violations, death, sex and hygiene) and sympathetic magic. In this study, a recently proposed model (Olatunji et al., 2007) consisting of the following three factors was used: contamination-based disgust (the disgust reaction based on the threat of transmission of contagion), core disgust (based on a sense of offensiveness and the threat of disease) and animal reminder disgust (stimuli that serve as reminder of animal origins of humans). All tests were in Korean, and the validity and reliability of these tests have been confirmed (Ahn et al., 2005; Chung et al., 2000; Kang et al., 2008.
2.3. Stimuli and procedure 2.3.1. Stimuli Pictures from the Facial Expressions of Emotion: Stimuli and Tests (FEEST) (Young et al., 2002) were used. Each picture is a morphed image of one prototypical facial expression with another from the Ekman and Friesen (1976) series. Morphed continua of only the negative emotions (anger, disgust, fear and sadness) were selected in 20% steps (e.g., 10% anger−90% fear, 30% anger−70% fear 50% anger−50% fear, 70% anger −30% fear and 90% anger−10% fear) (Figs. 1 and 2). Given that happiness and surprise are rarely confused with disgust (Corcoran et al., 2008), they were not selected to increase the difficulty of the task. Two models, one male and one female, were used, resulting in a total of 60 facial expressions (6 continua × 5 steps × 2 models). Although presented together, facial expressions with more than 70% morphed emotion were categorised as non-ambiguous, whereas 50% morphed facial expressions were considered to be ambiguous, and the two kinds of stimuli were analysed separately.
2.3.2. Procedure All participants completed a computerised emotion perception task. Participants were asked to choose which emotion the facial expressions most resembled among the four negative emotions. With 60 facial expressions repeated for six blocks, a total of 360 stimuli were shown (288 non-ambiguous and 72 ambiguous), in random order. For nonambiguous stimuli, there were 72 stimuli for each emotion. For ambiguous stimuli, there were no correct answers because no dominant emotion is present in 50% morphed emotions. Emotion word choices were counterbalanced across trials and presented below the pictures on the screen. Only when a response was made, the next picture appeared. All participants were asked the meaning of the emotion words before performing the task to test for comprehension. The entire task took approximately 30 minutes.
2.4. Statistical analyses All statistical analyses were performed using the Statistical Package for the Social Sciences (SPSS) version 12.0 for Windows (SPSS Inc., Chicago, IL, USA). Demographics and clinical variables for OCD patients and controls were compared using t-tests or the chi-square test. Multivariate analysis of covariance (MANCOVA) was used to compare the perception of each of the four emotions for non-ambiguous and ambiguous facial expressions between OCD patients and controls. All MANOVAs were performed both with and without controlling for age, sex and depression severity. The influence of the four symptom dimensions on the perception of facial expressions was tested using a multiple regression model (stepwise method). In addition, an enter method, in which the test is repeated by entering the covariates of age, sex and depression severity in the model first, was used. Pearson correlation analyses were conducted to explore the relationship between disgust sensitivity, the perception of facial expressions, and the cleaning dimension.
Fig. 1. Non-ambiguous facial expressions of anger, disgust, fear and sadness (more than 70% morphed).
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Fig. 2. Ambiguous facial expressions of anger, disgust, fear and sadness (50% morphed).
3. Results 3.1. Demographics and clinical variables No significant differences in demographic variables were found between groups. OCD patients scored higher on scales measuring disgust sensitivity and depression than the controls (Table 1). 3.2. Types of OCD symptoms As is typically the case, the majority of OCD patients had more than one type of OC symptom. The frequencies (%) of symptom dimensions, using the factor-analysed symptom dimensions identified by Bloch et al. (2008), were symmetry = 32 (78.0%), forbidden thoughts = 31 (75.6%), cleaning = 26 (63.4%) and hoarding = 18 (43.9%). 3.3. Perception of facial expressions 3.3.1. Effects of covariates There was a significant correlation between age and perception of non-ambiguous stimuli as disgust (r = 0.23, P = 0.04). MADRS scores were significantly correlated with the perception of sadness in nonambiguous stimuli (r = −0.31, P = 0.01). Females had significantly higher scores for recognition of disgust in non-ambiguous stimuli (t = − 2.18, P = 0.03). Although it did not reach statistical significance, age showed a trend in correlations with perception of non-ambiguous anger and sadness (r = 0.21, P = 0.06; r = 0.19, P = 0.09, respectively) and with the perception of sadness in ambiguous facial expressions (t = 0.21, P = 0.07), while the MADRS scores tended to correlate with non-ambiguous anger and disgust (r = −0.2, P = 0.08; r = −0.21, Table 1 Demographics and clinical characteristics of the enrolled subjects.
Sex (%)
Male Female
Age (years) Years of education IQ Age of onset of OCD (years) Duration of OCD (years) Y-BOCS total Y-BOCS obsessions Y-BOCS compulsions MADRS Disgust Scale
OCD (n = 41)
Normal control (n = 37)
P
32 (78.0%) 9 (22.0%) 24.85 (5.34) 13.89 (2.45) 108.92 (14.41) 16.0 (5.40) 9.7 (5.80) 20.62 (7.46) 10.71 (3.65) 10.07 (3.94) 13.68 (7.23) 54.35 (17.50)
28 (75.7%) 9 (24.3%) 25.95 (5.97) 14.24 (2.01) 114.47 (10.50) − − − − − 1.46 (2.74) 44.91 (13.74)
0.81a 0.40 0.51 0.07 − − − − − b 0.001 0.01
The mean values with the standard deviation in parenthesis are presented for all variables except sex. OCD; obsessive–compulsive disorder. Y-BOCS; Yale–Brown Obsessive–Compulsive Scale. MADRS; Montgomery–Asberg depression rating scale. a Compared using the χ2 test. All other comparisons were analysed by t-tests.
P = 0.07, respectively). Many previous studies have suggested that age (Calder et al., 2003; Sullivan and Ruffman, 2004), sex (Rotter and Rotter, 1988; Thayer and Johnsen, 2000) and depression severity (Mikhailova et al., 1996; Rubinow and Post, 1992) affect facial expression perception. Therefore, the subsequent analyses were performed both with and without controlling for age, sex and depression severity. 3.3.2. Facial expression recognition of non-ambiguous stimuli Frequencies of correct recognition of non-ambiguous facial expressions for each of the four emotions showed a normal distribution in both OCD patients and controls. Levene's test for homogeneity of variance showed approximately equal variances for both groups. There were no significant differences between OCD patients and controls in the frequencies of correct recognition of non-ambiguous facial expressions before adjusting for age, sex and depression severity (F(4,73) = 1.15, P = 0.34). This result was unchanged after controlling for the possible effects of covariates (F(4,70) = 1.12, P = 0.36) (Table 2). 3.3.3. Facial expression perception of ambiguous stimuli Both the OCD and the control group showed a normal distribution and approximately equal variances for Levene's test for homogeneity of variance. Before adjusting for age, sex and depression severity, no significant differences were found between groups in terms of their perception of ambiguous facial expressions (F(3,74) = 2.09, P = 0.11). After adjusting for these covariates, however, OCD patients were significantly more likely to perceive ambiguous facial expressions as disgust (F = 8.27, df = 1, P = 0.005) and less likely to perceive them as anger (F = 7.50, df = 1, P = 0.008), relative to the controls (Table 3). 3.4. Symptom dimensions and perception of facial expressions 3.4.1. Symptom dimensions and recognition of non-ambiguous stimuli In OCD subjects, a higher hoarding dimension score was a predictor of lower correct recognition of disgust (β = −0.31, t =−2.04, P = 0.049). However, the results were not statistically significant when controlling for age, sex, and MADRS scores (β = −0.28, t = −1.82, P = 0.08). Table 2 Mean frequency and standard deviation of correct recognition of non-ambiguous facial expressions for each emotion. Expression
OCD (n = 41)
Normal (n = 37)
Before controlling for sex, age, and MADRS
After controlling for sex, age, and MADRS
Anger Disgust Fear Sadness
53.47 52.02 50.51 56.88
58.00 55.70 54.51 57.27
Pillai's trace; F(4,73) = 1.15, P = 0.34
Pillai's trace; F(4,70) = 1.12, P = 0.36
(12.88) (16.49) (14.37) (3.91)
(10.18) (14.1) (10.99) (3.25)
The mean values with the standard deviation in parenthesis are presented. The maximum score for each emotion was 72. OCD; obsessive–compulsive disorder. MADRS; Montgomery–Asberg depression rating scale.
K. Jhung et al. / Psychiatry Research 178 (2010) 126–131 Table 3 Mean frequency and standard deviation of responses to perception of ambiguous facial expressions. Response
Anger Disgust Fear Sadness
OCD (n = 41)
14.43 19.80 17.17 20.60
(7.70) (7.20) (6.73) (7.97)
Normal (n = 37)
17.14 16.05 17.11 21.70
(6.14) (5.46) (4.78) (7.49)
Before controlling for sex, age and MADRS
After controlling for sex, age and MADRS
Pillai's trace; F(3,74) = 2.09, P = 0.11
Pillai's trace; F(3,71) = 4.00, P = 0.01
F
df
P
F
df
P
2.91 6.03 0.08 0.40
1 1 1 1
0.09 0.02 0.96 0.53
7.50 8.27 1.03 0.50
1 1 1 1
0.008 0.005 0.31 0.50
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Table 5 Correlation between the cleaning dimension and the domains of the Disgust Scale in OCD patients (n = 41) without controlling for the effects of sex, age and MADRS scores. Disgust Scale
Cleaning dimension
Core Disgust
Animal Reminder Disgust
Contamination-disgustased Disgust
Disgust total
r = 0.32 P = 0.04
0.02 0.90
0.46 0.002
0.30 0.06
R values and P values are presented in order for each correlation.
The mean values with the standard deviation in parenthesis are presented. Each participant evaluated 72 ambiguous pictures in total. OCD; obsessive–compulsive disorder. MADRS; Montgomery–Asberg depression rating scale.
No dimension score was a predictor of correct identification of anger, fear or sadness facial expressions either before or after controlling for covariates.
3.4.2. Symptom dimensions and perception of ambiguous stimuli In OCD subjects, a higher cleaning dimension score was a predictor of lower perception of anger in ambiguous facial expressions (β = −0.39, t = −2.63, P = 0.01). Furthermore, a higher cleaning dimension score was a predictor of greater perception of disgust in ambiguous facial expressions disgust (β = 0.45, t = 3.16, P = 0.003). The results remained unchanged after controlling for age, sex and MADRS scores (β = −0.41, t = −2.63, P = 0.03; β = − 0.53, t = 2.98, P = 0.005, respectively). None of the dimension scores were a predictor of perception of fear or sadness in ambiguous facial expressions either before or after controlling for covariates.
3.5. Disgust sensitivity 3.5.1. Disgust sensitivity and perception of facial expressions Within OCD subjects, none of the disgust sensitivity domains were correlated with any of the emotions in non-ambiguous facial expressions. For ambiguous facial expressions, however, the domains of core disgust and contamination-based disgust were positively correlated with the perception of disgust in ambiguous facial expressions (r = 0.34, P = 0.03; r = 0.40, P = 0.01, respectively). No other disgust domains were correlated with any of the other facial emotions (Table 4). Results remained unchanged when controlling for the effects of age, sex and MADRS scores.
3.5.2. Cleaning dimension and disgust sensitivity Cleaning dimension scores were positively correlated with core disgust scores (r = 0.32, P = 0.04) and contamination-based disgust scores (r = 0.46, P = 0.002). Animal reminder disgust did not correlate with the cleaning dimension scores (r = 0.02, P = 0.90) (Table 5). Results remained unchanged after controlling for covariates. 4. Discussion In this study, we examined whether OCD patients show a bias in perceiving ambiguous facial expressions as expressions of disgust relative to healthy controls, especially in relation to contamination/ washing symptoms. One of the interesting findings in this study is that OCD subjects were significantly more likely to perceive disgust and less likely to perceive anger in ambiguous facial expressions when adjusting for sex, age and depression severity, but no differences were found in non-ambiguous emotion recognition. Facial expressions are usually ambiguous by nature, and emotion appraisals involve the processing of complex and ambiguous stimuli (Motley and Camden, 1988). Thus, ambiguous stimuli may be more representative of the actual social contexts in which erroneous disgust appraisals by individuals with OCD occur. In a recent study, borderline personality disorder patients were more likely to perceive anger in ambiguous facial expressions, while no significant differences were found in recognition of nonambiguous facial expressions (Domes et al., 2008), implicating a biased perception of social information in these patients. Several other studies have also used ambiguous stimuli to more accurately represent the type of stimuli seen in social contexts (Gilboa-Schechtman et al., 2005; Nomura et al., 2003; Simmons et al., 2006). Furthermore, it has been hypothesised, though not directly tested until the present study, that individuals with OCD might not only be impervious to others' expressions of disgust, but also be highly sensitive to them. If the learned association of disgust with its distinct facial expressions fails to develop in people with OCD, both not being able to recognise what others see as disgust and overidentifying a non-disgust expression as disgust may be possible (Berle and Phillips,
Table 4 Correlation between emotion perception of non-ambiguous/ambiguous facial expressions and the domains of the Disgust Scale in OCD patients (n = 41) without controlling for the effects of sex, age and MADRS scores. Non-ambiguous stimuli
Core Disgust Animal Reminder Disgust Contamination-Based Disgust Disgust total
Ambiguous stimuli
Anger
Disgust
Fear
Sadness
Anger
Disgust
Fear
Sadness
r = − 0.01 P = 0.97 0.15 0.34 − 0.26 0.10 − 0.02 0.90
0.18 0.27 0.16 0.31 − 0.14 0.38 0.11 0.49
− 0.12 0.47 0.03 0.83 − 0.12 0.46 − 0.08 0.62
0.12 0.46 0.15 0.34 − 0.16 0.31 0.07 0.65
− 0.10 0.54 0.03 0.87 − 0.29 0.06 − 0.12 0.45
0.34 0.03 0.05 0.78 0.40 0.01 0.30 0.06
− 0.23 0.14 − 0.16 0.33 − 0.02 0.92 − 0.18 0.26
− 0.03 0.85 0.06 0.70 − 0.09 0.57 − 0.02 0.91
R values and P values are presented in order for each correlation.
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2006). To the best of our knowledge, the current study is the first to use ambiguous stimuli to test this hypothesis. If OCD patients come across ambiguous external stimuli and perceive them as disgust, it may lead to cognitive and behavioural responses, such as contamination obsessions and washing rituals. In our study, OCD subjects with higher cleaning dimension scores were more likely to perceive ambiguous facial expressions as disgust. Results from neuroimaging studies also support the association of disgust perception with contamination symptoms. Regions involved with the perception of disgust facial expressions, such as the orbitofrontal cortex (Sprengelmeyer et al., 1998) the putamen (Phillips et al., 1997; Sprengelmeyer et al., 1998) and the anterior insula (Phillips et al., 1997) have been identified as regions of interest in OCD patients (Whiteside et al., 2004). Similar regions have also been associated with disgust-inducing visual stimuli (Schienle et al., 2002). More recently, Lawrence et al. (2007) reported that OCD patients with higher washing symptoms showed increased responses to disgust facial expressions in the left ventrolateral prefrontal cortex, a region associated with responses to disgusting visual stimuli. Because OCD is a clinically heterogeneous condition, such that two patients with OCD can display completely distinct symptom patterns, these results imply that different syndromes within OCD, particularly those involving the cleaning dimension, may have distinct etiological mechanisms. In contrast to disgust perception, OCD patients were less likely to perceive anger in ambiguous facial expressions. This result is interesting in that anger is the emotion known to be most easily confused with disgust in facial emotion perception (Ekman and Friesen, 1976; Rozin et al., 2005). Because these two emotions are easily confused, it is possible that ambiguous facial expressions with a component of anger might have been more easily perceived as disgust. Thus, the overidentification of disgust in OCD patients may have led to the underidentification of anger. Another possibility is the effect of anger itself in OCD. Facial expressions of anger are often used and perceived as threatening stimuli that induce avoidance-related behaviour (Marsh et al., 2005). OCD patients exhibit high harm avoidance (Alonso et al., 2008; Ettelt et al., 2008), and this trait may lead to increased avoidance of threatening stimuli. Attention bias away from threatening faces expressing anger and reduced sensitivity to anger recognition have been reported in other psychiatric conditions, such as social anxiety disorders (Chen et al., 2002; Mogg et al., 2004; Montagne et al., 2006), but further studies are warranted in OCD patients. In our study, there were no differences between OCD patients and the normal controls with regard to the recognition of non-ambiguous facial expressions. This is in contrast with Sprengelmeyer et al. (1997) and Corcoran et al. (2008) who reported that non-ambiguous facial recognition of disgust in OCD patients was impaired. However, the results of other studies also contradict the results of Sprengelmeyer et al. (1997) and Corcoran et al. (2008) (Buhlmann et al., 2004; Parker et al., 2004), and it is likely that more studies yielded negative results but were not reported given the difficulties of reporting negative studies. Furthermore, Sprengelmeyer et al. (1997) evaluated only 12 OCD subjects from two different counties. The number of OCD subjects in the study by Corcoran et al. (2008) was relatively large (n = 40), but their sample consisted of individuals from different ethnic groups. Moreover, there was a significant difference in ethnic distribution between the OCD group and the control group (Corcoran et al., 2008). It is well known that cultural differences can affect facial expression recognition (Shioiri et al., 1999), and the possible effects of cultural differences on the results cannot be excluded. In our study, we evaluated a large number of subjects (OCD, n = 41 and controls, n = 37) from the same cultural background (same ethnicity, language and area). However, because of the differences in the cultural backgrounds of our subjects and those evaluated in previous studies, we cannot directly compare our results to those of previous studies.
In the present study, the domains of core disgust and contamination-based disgust were positively correlated with both the perception of ambiguous facial expressions as disgust and cleaning dimension scores. These results are in agreement with the findings of Olatunji et al. (2007); these authors reported that OCD patients with washing symptoms scored significantly higher than OCD patients without washing symptoms or normal controls with regard to core disgust and contamination-based disgust, but not with regard to animal reminder disgust. Our results support the multidimensional use of the Disgust Scale and imply that distinct disgust sensitivity factors may play a role in the mechanisms of OCD symptomatology. Moreover, these results support and extend our initial hypothesis by demonstrating that disgust perception is indeed related to trait sensitivity to disgust, which could lead to behavioural symptoms of washing in OCD patients. This study has some limitations. One limitation is that participants may have been able to perceive two emotional expressions simultaneously but were forced to respond according to what they thought was the dominant emotion. In this case, participants may not have had a bias in perception of facial expressions, but instead, a preference for selecting one emotion over another. A different paradigm that can assess this possibility may help clarify if this could account for our findings. Furthermore, we did not exclude patients with co-morbid diagnoses if OCD was the main reason for their hospital visit. It is possible that co-morbidities may have affected the results, as different psychiatric conditions are known to affect facial emotion perception. Further studies with OCD subjects without co-morbid diagnoses are needed. In addition, it remains to be explored whether disgust perception in OCD patients is indicative of any causal role. Disgust may play a role in the pathophysiology of OCD, but it is also possible that OC symptoms may trigger subsequent responses that somehow lead to the current findings regarding disgust perception in patients with OCD. Further experimental studies can help clarify if there is a causal relationship. In conclusion, OCD patients were significantly more likely to perceive ambiguous facial expressions as disgust, whereas there were no significant differences between OCD patients and normal controls in the recognition of non-ambiguous facial expressions. Among OCD symptoms, this perception bias of disgust in OCD patients was associated with the cleaning dimension. These findings suggest that OCD patients, particularly those with higher washing/contamination symptoms, have perceptual biases towards facial expressions of disgust. References Ahn, Y.M., Lee, K.Y., Yi, J.S., Kang, M.H., Kim, D.-H., Kim, J.-L., Shin, J., Shin, H.-K., Yeon, B.K., Lee, J.H., Chung, S.-K., Cho, I.H., Pyo, K.-S., Han, S.H., Kim, Y.S., 2005. A Validation Study of the Korean-Version of the Montgomery–Asberg Depression Rating Scale. Journal of Korean Neuropsychiatric Association 44, 466–476. Alonso, P., Menchon, J.M., Jimenez, S., Segalas, J., Mataix-Cols, D., Jaurrieta, N., Labad, J., Vallejo, J., Cardoner, N., Pujol, J., 2008. Personality dimensions in obsessive– compulsive disorder: relation to clinical variables. Psychiatry Research 157, 159–168. Berle, D., Phillips, E.S., 2006. Disgust and obsessive–compulsive disorder: an update. Psychiatry 69, 228–238. Bloch, M.H., Landeros-Weisenberger, A., Rosario, M.C., Pittenger, C., Leckman, J.F., 2008. Meta-analysis of the symptom structure of obsessive–compulsive disorder. American Journal of Psychiatry 165, 1532–1542. Buhlmann, U., McNally, R.J., Etcoff, N.L., Tuschen-Caffier, B., Wilhelm, S., 2004. Emotion recognition deficits in body dysmorphic disorder. Journal of Psychiatric Research 38, 201–206. Calder, A.J., Keane, J., Manly, T., Sprengelmeyer, R., Scott, S., Nimmo-Smith, I., Young, A.W., 2003. Facial expression recognition across the adult life span. Neuropsychologia 41, 195–202. Chen, Y.P., Ehlers, A., Clark, D.M., Mansell, W., 2002. Patients with generalized social phobia direct their attention away from faces. Behaviour Research and Therapy 40, 677–687. Chung, S.-J., Lee, J.-S., Kang, Y.-H., Cho, S.-J., Suh, D.-H., Hong, K.-E.M., 2000. Development of Korean Form of Children's Yale–Brown Obsessive–Compulsive Scale (CY-BOCS): a reliability and validity study. Korean Journal of Child and Adolescent Psychiatry 11, 60–69.
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Psychiatry Research j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p s yc h r e s
Perception bias of disgust in ambiguous facial expressions in obsessive–compulsive disorder Kyungun Jhung a, Kee Namkoong a, Jee In Kang a,b, Ra Yeon Ha a, Suk Kyoon An a, Chan-Hyung Kim a, Se Joo Kim a,⁎ a b
Department of Psychiatry and Institute of Behavioral Science in Medicine, Yonsei University, College of Medicine, 250 Seongsan-no, Seodamun-gu, Seoul, South Korea Department of Psychiatry, Ilsan Hospital, National Health Insurance Corporation, Goyang, Gyeonggi-do, South Korea
a r t i c l e
i n f o
Article history: Received 8 December 2008 Received in revised form 20 November 2009 Accepted 21 November 2009 Keywords: Disgust Facial expressions Ambiguous stimuli OCD Symptom dimensions Disgust Scale
a b s t r a c t Impaired recognition of facial expressions of disgust has been suggested for patients with obsessive– compulsive disorder (OCD). This study aimed to compare the perception of negative emotions by OCD patients and controls using both non-ambiguous and ambiguous facial expressions. Forty-one OCD patients and thirtyseven controls performed the computerised emotion perception task. There were no differences between OCD patients and controls in the frequency of correct identification of non-ambiguous facial expressions. However, OCD patients were more likely to perceive disgust and less likely to perceive anger in response to ambiguous facial expressions when controlling for covariates. In OCD patients, a higher cleaning dimension was associated with a lower perception of anger and a higher perception of disgust when presented with ambiguous facial expressions. The domains of core disgust and contamination-based disgust domains of disgust sensitivity were positively correlated with the perception of ambiguous facial expressions as disgust, as well as cleaning symptom dimension scores. Our findings suggest that OCD patients, particularly those with higher washing/ contamination symptoms, are more likely to perceive disgust in ambiguous facial expressions. © 2009 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Disgust is thought to underlie various psychiatric illnesses. Initially defined as a revulsion response to distasteful foods (Darwin and Ekman, 1998), the current concept of disgust now also includes responses to a wide range of stimuli, such as poor hygiene, potential for disease and violations of the normal body envelope (Rozin and Fallon, 1987). At its core, disgust functions to prevent contamination and disease (Darwin and Ekman, 1998) by the characteristic behavioural dimension of avoidance (Rozin and Fallon, 1987). Disgust also has specific physiological manifestations, such as nausea and a distinct facial expression of narrowed nostrils, wrinkling of the brow and raising of the upper lip (Phillips et al., 1998; Rozin et al., 1994). From a developmental perspective, perception of disgust is thought to be absent at birth and to develop during childhood (Rozin and Fallon, 1987). The learning process is thought to occur through experience with other peoples' disgust, and to involve the identification of disgust-eliciting stimuli, the recognition of other peoples' facial expressions of disgust, and the correlation between the two (Sprengelmeyer et al., 1996). If there is a dysfunction in this appraisal process, the stimuli that elicit disgust in those with a dysfunction may
⁎ Corresponding author. Tel.: + 82 2 2228 1620; fax: + 82 2 313 0891. E-mail address: [email protected] (S.J. Kim). 0165-1781/$ – see front matter © 2009 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.psychres.2009.11.023
be dissimilar from the stimuli that elicit disgust in others (Sprengelmeyer et al., 1996). Impairment in this disgust appraisal process has been suggested to be closely related to obsessive–compulsive disorder (OCD). OCD is a relatively common disorder, characterised by persistent and unwanted thoughts and ritualistic behaviour. Among the heterogeneous symptoms of OCD, concerns with contamination are commonly involved. OCD patients often exhibit heightened appraisals of vulnerability to infection and spread of contamination in response to offensive objects, which elicit washing compulsions (Olatunji and McKay, 2007). Because the situations in which OCD patients experience disgust are different from those in which normal individuals experience disgust, it has been hypothesised that the learned association between the emotion of disgust and the facial expressions of disgust may have failed to develop (Sprengelmeyer et al., 1997). Experimental support for this theory of disgust perception in OCD, however, has been mixed. Sprengelmeyer et al. (1997) reported that all OCD patients examined showed a distinct and significant impairment in recognising facial expressions of disgust. However, subsequent studies have not revealed a clear association between OCD and the failure to recognise facial expressions of disgust. Parker et al. (2004) and Buhlmann et al. (2004) both reported no significant differences between OCD patients and normal controls with respect to facial expression recognition. In a more recent study, the results of Sprengelmeyer et al. (1997) were replicated, but the magnitude of the
K. Jhung et al. / Psychiatry Research 178 (2010) 126–131
effect was much smaller — only about a third of OCD subjects showed the impairment (Corcoran et al., 2008). These previous studies used non-ambiguous facial expressions to assess the responses of OCD patients, which could result in other important aspects of disgust perception being missed. Ambiguous facial expressions may further our understanding of emotion perception (Kee et al., 2006; Pollak and Kistler, 2002). Whereas non-ambiguous facial expressions are helpful in assessing facial emotion recognition, ambiguous facial expressions reveal whether individuals have a perception bias towards a certain emotion. Furthermore, due to the heterogeneity of OCD, some researchers have hypothesised that only a subset of OCD patients may have altered disgust perception, particularly those with contamination/ washing symptoms (Power and Dalgleish, 2008). Several studies have reported an association between contamination fear and disgust sensitivity (Mancini et al., 2001; Olatunji et al., 2004; Woody and Tolin, 2002), but the association between contamination fear and disgust perception has not been previously investigated. In the present study, we recruited OCD patients and healthy controls for the following purposes: (1) to compare their emotion recognition of non-ambiguous facial expressions, (2) to test if there are any perception biases in the classification of ambiguous facial expressions, especially the emotion of disgust, (3) to determine if the particular OCD symptom dimension of cleaning is associated with disgust perception and (4) to evaluate the domains of disgust sensitivity associated with disgust perception and the cleaning dimension of OCD. 2. Materials and methods 2.1. Participants Forty-one primary OCD patients were recruited from the psychiatric outpatient clinic of Severance Hospital, Yonsei University Medical Center. Patients were interviewed and diagnosed by experienced psychiatrists on the basis of the structured clinical interview for Diagnostic and Statistical Manual of Mental Disorders, fourth edition Diagnostic and Statistical Manual of Mental Disorders, fourth edition (DSM-IV) (SCID-CV) (First et al., 1997). Those with co-morbid diagnoses were included under the condition that OCD was the main reason for their visit. Exclusion criteria were substance abuse, psychosis or any neurological or medical condition that could affect the subject's performance. Thirty-seven normal controls were selected to match the OCD group for sex, age, and education level. SCID-CV was used to ensure that the normal controls had no history or current symptoms of neurological or psychiatric disorders and were not on any medication. 2.2. Measures For the OCD subjects, the Yale-Brown Obsessive-Compulsive Scale (Y-BOCS) and Y-BOCS Symptom Checklist (Goodman et al., 1989) was used to assess the severity and types of OC symptoms. A score of 0, 1 or 2 was assigned to each of the symptom categories of the Y-BOCS Symptom Checklist as follows: 0 if the patient did not have any of the symptoms under the category; 1 if the patient had at least one symptom, but not the principal symptom, under the category; or 2 if the principal symptom was under the symptom category. Using the four dimensional factors (symmetry, forbidden thoughts, cleaning and hoarding) identified by Bloch et al. (2008) in their meta-analysis, the sum of the scores for the symptom categories under each
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dimensional factor was the score for that dimension. Psychiatrists administered the Y-BOCS on the day the emotion perception task was performed. In both OCD and control groups, the severity of depressive symptoms was measured using the Montgomery–Asberg Depression Rating Scale (MADRS) (Davidson et al., 1986). To measure disgust sensitivity, all participants completed the Disgust Scale (Haidt et al., 1994), which includes seven domains of disgust elicitors i.e., food, animals, body products, body envelope violations, death, sex and hygiene) and sympathetic magic. In this study, a recently proposed model (Olatunji et al., 2007) consisting of the following three factors was used: contamination-based disgust (the disgust reaction based on the threat of transmission of contagion), core disgust (based on a sense of offensiveness and the threat of disease) and animal reminder disgust (stimuli that serve as reminder of animal origins of humans). All tests were in Korean, and the validity and reliability of these tests have been confirmed (Ahn et al., 2005; Chung et al., 2000; Kang et al., 2008.
2.3. Stimuli and procedure 2.3.1. Stimuli Pictures from the Facial Expressions of Emotion: Stimuli and Tests (FEEST) (Young et al., 2002) were used. Each picture is a morphed image of one prototypical facial expression with another from the Ekman and Friesen (1976) series. Morphed continua of only the negative emotions (anger, disgust, fear and sadness) were selected in 20% steps (e.g., 10% anger−90% fear, 30% anger−70% fear 50% anger−50% fear, 70% anger −30% fear and 90% anger−10% fear) (Figs. 1 and 2). Given that happiness and surprise are rarely confused with disgust (Corcoran et al., 2008), they were not selected to increase the difficulty of the task. Two models, one male and one female, were used, resulting in a total of 60 facial expressions (6 continua × 5 steps × 2 models). Although presented together, facial expressions with more than 70% morphed emotion were categorised as non-ambiguous, whereas 50% morphed facial expressions were considered to be ambiguous, and the two kinds of stimuli were analysed separately.
2.3.2. Procedure All participants completed a computerised emotion perception task. Participants were asked to choose which emotion the facial expressions most resembled among the four negative emotions. With 60 facial expressions repeated for six blocks, a total of 360 stimuli were shown (288 non-ambiguous and 72 ambiguous), in random order. For nonambiguous stimuli, there were 72 stimuli for each emotion. For ambiguous stimuli, there were no correct answers because no dominant emotion is present in 50% morphed emotions. Emotion word choices were counterbalanced across trials and presented below the pictures on the screen. Only when a response was made, the next picture appeared. All participants were asked the meaning of the emotion words before performing the task to test for comprehension. The entire task took approximately 30 minutes.
2.4. Statistical analyses All statistical analyses were performed using the Statistical Package for the Social Sciences (SPSS) version 12.0 for Windows (SPSS Inc., Chicago, IL, USA). Demographics and clinical variables for OCD patients and controls were compared using t-tests or the chi-square test. Multivariate analysis of covariance (MANCOVA) was used to compare the perception of each of the four emotions for non-ambiguous and ambiguous facial expressions between OCD patients and controls. All MANOVAs were performed both with and without controlling for age, sex and depression severity. The influence of the four symptom dimensions on the perception of facial expressions was tested using a multiple regression model (stepwise method). In addition, an enter method, in which the test is repeated by entering the covariates of age, sex and depression severity in the model first, was used. Pearson correlation analyses were conducted to explore the relationship between disgust sensitivity, the perception of facial expressions, and the cleaning dimension.
Fig. 1. Non-ambiguous facial expressions of anger, disgust, fear and sadness (more than 70% morphed).
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Fig. 2. Ambiguous facial expressions of anger, disgust, fear and sadness (50% morphed).
3. Results 3.1. Demographics and clinical variables No significant differences in demographic variables were found between groups. OCD patients scored higher on scales measuring disgust sensitivity and depression than the controls (Table 1). 3.2. Types of OCD symptoms As is typically the case, the majority of OCD patients had more than one type of OC symptom. The frequencies (%) of symptom dimensions, using the factor-analysed symptom dimensions identified by Bloch et al. (2008), were symmetry = 32 (78.0%), forbidden thoughts = 31 (75.6%), cleaning = 26 (63.4%) and hoarding = 18 (43.9%). 3.3. Perception of facial expressions 3.3.1. Effects of covariates There was a significant correlation between age and perception of non-ambiguous stimuli as disgust (r = 0.23, P = 0.04). MADRS scores were significantly correlated with the perception of sadness in nonambiguous stimuli (r = −0.31, P = 0.01). Females had significantly higher scores for recognition of disgust in non-ambiguous stimuli (t = − 2.18, P = 0.03). Although it did not reach statistical significance, age showed a trend in correlations with perception of non-ambiguous anger and sadness (r = 0.21, P = 0.06; r = 0.19, P = 0.09, respectively) and with the perception of sadness in ambiguous facial expressions (t = 0.21, P = 0.07), while the MADRS scores tended to correlate with non-ambiguous anger and disgust (r = −0.2, P = 0.08; r = −0.21, Table 1 Demographics and clinical characteristics of the enrolled subjects.
Sex (%)
Male Female
Age (years) Years of education IQ Age of onset of OCD (years) Duration of OCD (years) Y-BOCS total Y-BOCS obsessions Y-BOCS compulsions MADRS Disgust Scale
OCD (n = 41)
Normal control (n = 37)
P
32 (78.0%) 9 (22.0%) 24.85 (5.34) 13.89 (2.45) 108.92 (14.41) 16.0 (5.40) 9.7 (5.80) 20.62 (7.46) 10.71 (3.65) 10.07 (3.94) 13.68 (7.23) 54.35 (17.50)
28 (75.7%) 9 (24.3%) 25.95 (5.97) 14.24 (2.01) 114.47 (10.50) − − − − − 1.46 (2.74) 44.91 (13.74)
0.81a 0.40 0.51 0.07 − − − − − b 0.001 0.01
The mean values with the standard deviation in parenthesis are presented for all variables except sex. OCD; obsessive–compulsive disorder. Y-BOCS; Yale–Brown Obsessive–Compulsive Scale. MADRS; Montgomery–Asberg depression rating scale. a Compared using the χ2 test. All other comparisons were analysed by t-tests.
P = 0.07, respectively). Many previous studies have suggested that age (Calder et al., 2003; Sullivan and Ruffman, 2004), sex (Rotter and Rotter, 1988; Thayer and Johnsen, 2000) and depression severity (Mikhailova et al., 1996; Rubinow and Post, 1992) affect facial expression perception. Therefore, the subsequent analyses were performed both with and without controlling for age, sex and depression severity. 3.3.2. Facial expression recognition of non-ambiguous stimuli Frequencies of correct recognition of non-ambiguous facial expressions for each of the four emotions showed a normal distribution in both OCD patients and controls. Levene's test for homogeneity of variance showed approximately equal variances for both groups. There were no significant differences between OCD patients and controls in the frequencies of correct recognition of non-ambiguous facial expressions before adjusting for age, sex and depression severity (F(4,73) = 1.15, P = 0.34). This result was unchanged after controlling for the possible effects of covariates (F(4,70) = 1.12, P = 0.36) (Table 2). 3.3.3. Facial expression perception of ambiguous stimuli Both the OCD and the control group showed a normal distribution and approximately equal variances for Levene's test for homogeneity of variance. Before adjusting for age, sex and depression severity, no significant differences were found between groups in terms of their perception of ambiguous facial expressions (F(3,74) = 2.09, P = 0.11). After adjusting for these covariates, however, OCD patients were significantly more likely to perceive ambiguous facial expressions as disgust (F = 8.27, df = 1, P = 0.005) and less likely to perceive them as anger (F = 7.50, df = 1, P = 0.008), relative to the controls (Table 3). 3.4. Symptom dimensions and perception of facial expressions 3.4.1. Symptom dimensions and recognition of non-ambiguous stimuli In OCD subjects, a higher hoarding dimension score was a predictor of lower correct recognition of disgust (β = −0.31, t =−2.04, P = 0.049). However, the results were not statistically significant when controlling for age, sex, and MADRS scores (β = −0.28, t = −1.82, P = 0.08). Table 2 Mean frequency and standard deviation of correct recognition of non-ambiguous facial expressions for each emotion. Expression
OCD (n = 41)
Normal (n = 37)
Before controlling for sex, age, and MADRS
After controlling for sex, age, and MADRS
Anger Disgust Fear Sadness
53.47 52.02 50.51 56.88
58.00 55.70 54.51 57.27
Pillai's trace; F(4,73) = 1.15, P = 0.34
Pillai's trace; F(4,70) = 1.12, P = 0.36
(12.88) (16.49) (14.37) (3.91)
(10.18) (14.1) (10.99) (3.25)
The mean values with the standard deviation in parenthesis are presented. The maximum score for each emotion was 72. OCD; obsessive–compulsive disorder. MADRS; Montgomery–Asberg depression rating scale.
K. Jhung et al. / Psychiatry Research 178 (2010) 126–131 Table 3 Mean frequency and standard deviation of responses to perception of ambiguous facial expressions. Response
Anger Disgust Fear Sadness
OCD (n = 41)
14.43 19.80 17.17 20.60
(7.70) (7.20) (6.73) (7.97)
Normal (n = 37)
17.14 16.05 17.11 21.70
(6.14) (5.46) (4.78) (7.49)
Before controlling for sex, age and MADRS
After controlling for sex, age and MADRS
Pillai's trace; F(3,74) = 2.09, P = 0.11
Pillai's trace; F(3,71) = 4.00, P = 0.01
F
df
P
F
df
P
2.91 6.03 0.08 0.40
1 1 1 1
0.09 0.02 0.96 0.53
7.50 8.27 1.03 0.50
1 1 1 1
0.008 0.005 0.31 0.50
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Table 5 Correlation between the cleaning dimension and the domains of the Disgust Scale in OCD patients (n = 41) without controlling for the effects of sex, age and MADRS scores. Disgust Scale
Cleaning dimension
Core Disgust
Animal Reminder Disgust
Contamination-disgustased Disgust
Disgust total
r = 0.32 P = 0.04
0.02 0.90
0.46 0.002
0.30 0.06
R values and P values are presented in order for each correlation.
The mean values with the standard deviation in parenthesis are presented. Each participant evaluated 72 ambiguous pictures in total. OCD; obsessive–compulsive disorder. MADRS; Montgomery–Asberg depression rating scale.
No dimension score was a predictor of correct identification of anger, fear or sadness facial expressions either before or after controlling for covariates.
3.4.2. Symptom dimensions and perception of ambiguous stimuli In OCD subjects, a higher cleaning dimension score was a predictor of lower perception of anger in ambiguous facial expressions (β = −0.39, t = −2.63, P = 0.01). Furthermore, a higher cleaning dimension score was a predictor of greater perception of disgust in ambiguous facial expressions disgust (β = 0.45, t = 3.16, P = 0.003). The results remained unchanged after controlling for age, sex and MADRS scores (β = −0.41, t = −2.63, P = 0.03; β = − 0.53, t = 2.98, P = 0.005, respectively). None of the dimension scores were a predictor of perception of fear or sadness in ambiguous facial expressions either before or after controlling for covariates.
3.5. Disgust sensitivity 3.5.1. Disgust sensitivity and perception of facial expressions Within OCD subjects, none of the disgust sensitivity domains were correlated with any of the emotions in non-ambiguous facial expressions. For ambiguous facial expressions, however, the domains of core disgust and contamination-based disgust were positively correlated with the perception of disgust in ambiguous facial expressions (r = 0.34, P = 0.03; r = 0.40, P = 0.01, respectively). No other disgust domains were correlated with any of the other facial emotions (Table 4). Results remained unchanged when controlling for the effects of age, sex and MADRS scores.
3.5.2. Cleaning dimension and disgust sensitivity Cleaning dimension scores were positively correlated with core disgust scores (r = 0.32, P = 0.04) and contamination-based disgust scores (r = 0.46, P = 0.002). Animal reminder disgust did not correlate with the cleaning dimension scores (r = 0.02, P = 0.90) (Table 5). Results remained unchanged after controlling for covariates. 4. Discussion In this study, we examined whether OCD patients show a bias in perceiving ambiguous facial expressions as expressions of disgust relative to healthy controls, especially in relation to contamination/ washing symptoms. One of the interesting findings in this study is that OCD subjects were significantly more likely to perceive disgust and less likely to perceive anger in ambiguous facial expressions when adjusting for sex, age and depression severity, but no differences were found in non-ambiguous emotion recognition. Facial expressions are usually ambiguous by nature, and emotion appraisals involve the processing of complex and ambiguous stimuli (Motley and Camden, 1988). Thus, ambiguous stimuli may be more representative of the actual social contexts in which erroneous disgust appraisals by individuals with OCD occur. In a recent study, borderline personality disorder patients were more likely to perceive anger in ambiguous facial expressions, while no significant differences were found in recognition of nonambiguous facial expressions (Domes et al., 2008), implicating a biased perception of social information in these patients. Several other studies have also used ambiguous stimuli to more accurately represent the type of stimuli seen in social contexts (Gilboa-Schechtman et al., 2005; Nomura et al., 2003; Simmons et al., 2006). Furthermore, it has been hypothesised, though not directly tested until the present study, that individuals with OCD might not only be impervious to others' expressions of disgust, but also be highly sensitive to them. If the learned association of disgust with its distinct facial expressions fails to develop in people with OCD, both not being able to recognise what others see as disgust and overidentifying a non-disgust expression as disgust may be possible (Berle and Phillips,
Table 4 Correlation between emotion perception of non-ambiguous/ambiguous facial expressions and the domains of the Disgust Scale in OCD patients (n = 41) without controlling for the effects of sex, age and MADRS scores. Non-ambiguous stimuli
Core Disgust Animal Reminder Disgust Contamination-Based Disgust Disgust total
Ambiguous stimuli
Anger
Disgust
Fear
Sadness
Anger
Disgust
Fear
Sadness
r = − 0.01 P = 0.97 0.15 0.34 − 0.26 0.10 − 0.02 0.90
0.18 0.27 0.16 0.31 − 0.14 0.38 0.11 0.49
− 0.12 0.47 0.03 0.83 − 0.12 0.46 − 0.08 0.62
0.12 0.46 0.15 0.34 − 0.16 0.31 0.07 0.65
− 0.10 0.54 0.03 0.87 − 0.29 0.06 − 0.12 0.45
0.34 0.03 0.05 0.78 0.40 0.01 0.30 0.06
− 0.23 0.14 − 0.16 0.33 − 0.02 0.92 − 0.18 0.26
− 0.03 0.85 0.06 0.70 − 0.09 0.57 − 0.02 0.91
R values and P values are presented in order for each correlation.
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K. Jhung et al. / Psychiatry Research 178 (2010) 126–131
2006). To the best of our knowledge, the current study is the first to use ambiguous stimuli to test this hypothesis. If OCD patients come across ambiguous external stimuli and perceive them as disgust, it may lead to cognitive and behavioural responses, such as contamination obsessions and washing rituals. In our study, OCD subjects with higher cleaning dimension scores were more likely to perceive ambiguous facial expressions as disgust. Results from neuroimaging studies also support the association of disgust perception with contamination symptoms. Regions involved with the perception of disgust facial expressions, such as the orbitofrontal cortex (Sprengelmeyer et al., 1998) the putamen (Phillips et al., 1997; Sprengelmeyer et al., 1998) and the anterior insula (Phillips et al., 1997) have been identified as regions of interest in OCD patients (Whiteside et al., 2004). Similar regions have also been associated with disgust-inducing visual stimuli (Schienle et al., 2002). More recently, Lawrence et al. (2007) reported that OCD patients with higher washing symptoms showed increased responses to disgust facial expressions in the left ventrolateral prefrontal cortex, a region associated with responses to disgusting visual stimuli. Because OCD is a clinically heterogeneous condition, such that two patients with OCD can display completely distinct symptom patterns, these results imply that different syndromes within OCD, particularly those involving the cleaning dimension, may have distinct etiological mechanisms. In contrast to disgust perception, OCD patients were less likely to perceive anger in ambiguous facial expressions. This result is interesting in that anger is the emotion known to be most easily confused with disgust in facial emotion perception (Ekman and Friesen, 1976; Rozin et al., 2005). Because these two emotions are easily confused, it is possible that ambiguous facial expressions with a component of anger might have been more easily perceived as disgust. Thus, the overidentification of disgust in OCD patients may have led to the underidentification of anger. Another possibility is the effect of anger itself in OCD. Facial expressions of anger are often used and perceived as threatening stimuli that induce avoidance-related behaviour (Marsh et al., 2005). OCD patients exhibit high harm avoidance (Alonso et al., 2008; Ettelt et al., 2008), and this trait may lead to increased avoidance of threatening stimuli. Attention bias away from threatening faces expressing anger and reduced sensitivity to anger recognition have been reported in other psychiatric conditions, such as social anxiety disorders (Chen et al., 2002; Mogg et al., 2004; Montagne et al., 2006), but further studies are warranted in OCD patients. In our study, there were no differences between OCD patients and the normal controls with regard to the recognition of non-ambiguous facial expressions. This is in contrast with Sprengelmeyer et al. (1997) and Corcoran et al. (2008) who reported that non-ambiguous facial recognition of disgust in OCD patients was impaired. However, the results of other studies also contradict the results of Sprengelmeyer et al. (1997) and Corcoran et al. (2008) (Buhlmann et al., 2004; Parker et al., 2004), and it is likely that more studies yielded negative results but were not reported given the difficulties of reporting negative studies. Furthermore, Sprengelmeyer et al. (1997) evaluated only 12 OCD subjects from two different counties. The number of OCD subjects in the study by Corcoran et al. (2008) was relatively large (n = 40), but their sample consisted of individuals from different ethnic groups. Moreover, there was a significant difference in ethnic distribution between the OCD group and the control group (Corcoran et al., 2008). It is well known that cultural differences can affect facial expression recognition (Shioiri et al., 1999), and the possible effects of cultural differences on the results cannot be excluded. In our study, we evaluated a large number of subjects (OCD, n = 41 and controls, n = 37) from the same cultural background (same ethnicity, language and area). However, because of the differences in the cultural backgrounds of our subjects and those evaluated in previous studies, we cannot directly compare our results to those of previous studies.
In the present study, the domains of core disgust and contamination-based disgust were positively correlated with both the perception of ambiguous facial expressions as disgust and cleaning dimension scores. These results are in agreement with the findings of Olatunji et al. (2007); these authors reported that OCD patients with washing symptoms scored significantly higher than OCD patients without washing symptoms or normal controls with regard to core disgust and contamination-based disgust, but not with regard to animal reminder disgust. Our results support the multidimensional use of the Disgust Scale and imply that distinct disgust sensitivity factors may play a role in the mechanisms of OCD symptomatology. Moreover, these results support and extend our initial hypothesis by demonstrating that disgust perception is indeed related to trait sensitivity to disgust, which could lead to behavioural symptoms of washing in OCD patients. This study has some limitations. One limitation is that participants may have been able to perceive two emotional expressions simultaneously but were forced to respond according to what they thought was the dominant emotion. In this case, participants may not have had a bias in perception of facial expressions, but instead, a preference for selecting one emotion over another. A different paradigm that can assess this possibility may help clarify if this could account for our findings. Furthermore, we did not exclude patients with co-morbid diagnoses if OCD was the main reason for their hospital visit. It is possible that co-morbidities may have affected the results, as different psychiatric conditions are known to affect facial emotion perception. Further studies with OCD subjects without co-morbid diagnoses are needed. In addition, it remains to be explored whether disgust perception in OCD patients is indicative of any causal role. Disgust may play a role in the pathophysiology of OCD, but it is also possible that OC symptoms may trigger subsequent responses that somehow lead to the current findings regarding disgust perception in patients with OCD. Further experimental studies can help clarify if there is a causal relationship. In conclusion, OCD patients were significantly more likely to perceive ambiguous facial expressions as disgust, whereas there were no significant differences between OCD patients and normal controls in the recognition of non-ambiguous facial expressions. Among OCD symptoms, this perception bias of disgust in OCD patients was associated with the cleaning dimension. These findings suggest that OCD patients, particularly those with higher washing/contamination symptoms, have perceptual biases towards facial expressions of disgust. References Ahn, Y.M., Lee, K.Y., Yi, J.S., Kang, M.H., Kim, D.-H., Kim, J.-L., Shin, J., Shin, H.-K., Yeon, B.K., Lee, J.H., Chung, S.-K., Cho, I.H., Pyo, K.-S., Han, S.H., Kim, Y.S., 2005. A Validation Study of the Korean-Version of the Montgomery–Asberg Depression Rating Scale. Journal of Korean Neuropsychiatric Association 44, 466–476. Alonso, P., Menchon, J.M., Jimenez, S., Segalas, J., Mataix-Cols, D., Jaurrieta, N., Labad, J., Vallejo, J., Cardoner, N., Pujol, J., 2008. Personality dimensions in obsessive– compulsive disorder: relation to clinical variables. Psychiatry Research 157, 159–168. Berle, D., Phillips, E.S., 2006. Disgust and obsessive–compulsive disorder: an update. Psychiatry 69, 228–238. Bloch, M.H., Landeros-Weisenberger, A., Rosario, M.C., Pittenger, C., Leckman, J.F., 2008. Meta-analysis of the symptom structure of obsessive–compulsive disorder. American Journal of Psychiatry 165, 1532–1542. Buhlmann, U., McNally, R.J., Etcoff, N.L., Tuschen-Caffier, B., Wilhelm, S., 2004. Emotion recognition deficits in body dysmorphic disorder. Journal of Psychiatric Research 38, 201–206. Calder, A.J., Keane, J., Manly, T., Sprengelmeyer, R., Scott, S., Nimmo-Smith, I., Young, A.W., 2003. Facial expression recognition across the adult life span. Neuropsychologia 41, 195–202. Chen, Y.P., Ehlers, A., Clark, D.M., Mansell, W., 2002. Patients with generalized social phobia direct their attention away from faces. Behaviour Research and Therapy 40, 677–687. Chung, S.-J., Lee, J.-S., Kang, Y.-H., Cho, S.-J., Suh, D.-H., Hong, K.-E.M., 2000. Development of Korean Form of Children's Yale–Brown Obsessive–Compulsive Scale (CY-BOCS): a reliability and validity study. Korean Journal of Child and Adolescent Psychiatry 11, 60–69.
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