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Disassociation of cognitive and affective aspects of theory of mind in obsessive-compulsive disorder
Author’s Accepted Manuscript Disassociation of cognitive and affective aspects of theory of mind in obsessive-compulsive disorder Wanting Liu, Jie Fan, Jun Gan, Hui Lei, Chaoyang Niu, Raymond C.K. Chan, Xiongzhao Zhu www.elsevier.com/locate/psychres
PII: DOI: Reference:
S0165-1781(16)31952-7 http://dx.doi.org/10.1016/j.psychres.2017.06.058 PSY10605
To appear in: Psychiatry Research Received date: 20 November 2016 Revised date: 7 March 2017 Accepted date: 16 June 2017 Cite this article as: Wanting Liu, Jie Fan, Jun Gan, Hui Lei, Chaoyang Niu, Raymond C.K. Chan and Xiongzhao Zhu, Disassociation of cognitive and affective aspects of theory of mind in obsessive-compulsive disorder, Psychiatry Research, http://dx.doi.org/10.1016/j.psychres.2017.06.058 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Disassociation of cognitive and affective aspects of theory of mind in obsessive-compulsive disorder
Wanting Liua, Jie Fana, Jun Gana, Hui Leib, Chaoyang Niua, Raymond C. K. Chanc,d，Xiongzhao Zhua,*
a
Medical Psychological Center, The Second Xiangya Hospital, Central South
University, Changsha, Hunan 410011, China b
c
College of Education, Hunan Agriculture University, Changsha 410128, P.R. China
Neuropsychology and Applied Cognitive Neuroscience Laboratory, CAS Key
Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, China d
Department of Psychology, University of Chinese Academy of Sciences, Beijing,
China
*
Corresponding author at: Medical Psychological Institute of the Second Xiangya
Hospital, Central South University, Renmin Road 139, Changsha, Hunan, PR China 410011. Tel: +86 731 85292126; Fax: +86 731 85361328; Email address: [email protected].
Abstract Impairment in social functioning has been widely described in obsessive-compulsive disorder (OCD). However, several aspects of social cognition, such as theory of mind (ToM), have not been substantially investigated in this context. This study examined cognitive and affective ToM in 40 OCD patients and 38 age-, sex-, and education-matched healthy controls (HCs) with the computerized Yoni task and a battery of neurocognitive tests. OCD symptom severity was assessed with the Yale-Brown Obsessive-Compulsive Scale (Y-BOCS). Depressive and anxiety symptoms were also assessed. Compared to HCs, OCD patients performed worse on second-order affective condition trials, but not cognitive or physical condition trials, of the Yoni task; there were not group differences in any of the first-order condition domains. Second-order ToM performance of OCD patients was associated with estimated intelligence and working memory performance. After controlling for neurocognitive variables, the group difference in second-order affective condition performance remained significant. These findings indicate that the affective component of ToM may be selectively impaired in OCD patients and that the observed deficit is largely independent of other neurocognitive impairments and clinical characteristics. Key words Obsessive-compulsive disorder; social cognition; theory of mind; metalizing; executive function
1. Introduction Obsessive-compulsive disorder (OCD) is a relatively common neuropsychiatric disorder characterized by intrusive and recurrent thoughts or images (obsessions) and/or repetitive and ritualistic acts or behaviors (compulsions) that the patients feel driven to perform to neutralize anxiety or distress induced by obsessions (American Psychiatric Association, 2013). Neurocognitive dysfunction, particularly in the areas of executive function (EF) and memory, have long been recognized (Abramovitch et al., 2013; Kuelz et al., 2004). It has been suggested that deficits in social cognition may be common to patients with basal ganglia abnormalities, including those with Huntington disease, Parkinson disease, and perhaps also OCD (Bodden et al., 2010). Unlike most neurocognitive functions described in the literature, which refer to functions that are associated with a particular brain area, pathway, or network, social cognition encompasses a mixture of cognitive processes that contribute to social interactions. Social cognition integrates a variety of socio-emotional abilities and experiences that influence one’s relationships with others and enable one to interpret others’ behaviors; in human psychology, social cognition is described as including several subdomains, namely social cue interpretation, emotion recognition, empathy, and theory of mind (ToM)(Adolphs, 2001). ToM is the capacity to make inferences about others’ mental states in terms of feelings, intentions, desires, and beliefs, which enables one to understand and predict other people’s behavior (Call and Tomasello, 2008), and thus is considered to be an essential prerequisite for successful social interaction (Brüne and Brüne-Cohrs, 2006). Some researchers have begun to break
down the complex notion of ToM into components. Apart from simply differentiating ToM with respect to task complexity into first- and second-order levels (Baron-Cohen, 1995), recent research suggests that cognitive ToM, that is, understanding and making inferences about others’ beliefs and motivations, should be distinguished from affective ToM, which is defined as inferring others’ feelings and emotions (Kalbe et al., 2007). Although social functioning impairments are often seen in OCD (Bystritsky et al., 2001), relative to other neurodevelopmental and psychiatric disorders such as autism (Baron-Cohen, 2000), schizophrenia (Brüne, 2005), bipolar affective disorder (Kerr et al., 2003), and depression (Inoue et al., 2006), ToM has received very little attention in OCD research. To the best of our knowledge, only two studies have examined ToM in OCD patients. Sayın et al. (2010) administered various ToM tasks including the Hinting task, double-bluff task, and first- and second-order false belief tasks, as well as some tests for memory and EF to 30 OCD patients and 30 age-, sex- and education-matched healthy controls (HCs). They found that OCD patients only performed significantly worse than HCs on the double-bluff task, and that their performance on that task correlated with memory capacity, suggesting that OCD patients were impaired in advanced ToM abilities, but had preserved basic ToM abilities (Sayın et al., 2010). More recently, Mavrogiorgou et al. (2016) administered the Hinting Task and the faux pas test to 20 OCD patients and 20 age-, sex- and education-matched HCs. They found that OCD patients did not differ from HCs with regard to performance in either task, leading them to concur that basic-level ToM was
normal in OCD patients. Historically, ToM in OCD research has been considered to be a hierarchical construct without differentiation between cognitive and affective aspects. Hence, it remains unclear whether OCD patients have impaired cognitive and/or affective ToM. In addition, previous ToM studies in other psychiatric populations have, usually, conducted two separate tasks to assess the cognitive and affective components of ToM independently (Russell et al., 2009; Santangelo et al., 2013). However, adequate control conditions for these ToM tasks have not been applied consistently. Moreover, the assessments of cognitive versus affective ToM tasks may be tapping into different cognitive demands, which may confound the cognitive-affective differentiation of ToM. Ideally, both the cognitive and affective components of ToM should be assessed in the same task with adequate control conditions. A novel cartoon-based ToM paradigm called the Yoni Task (Shamay-Tsoory and Aharon-Peretz, 2007) appears to be a promising paradigm with which to assess ToM abilities in OCD patients because it has three highly comparable conditions
(cognitive, affective, and physical) that
each contain first- and second-order items. The first aim of the present study was to further assess cognitive and affective components in OCD patients with the Yoni Task. Secondly, we examined how performance on this task may be related to clinical characteristics of OCD and other aspects of neurocognitive functioning.
2. Methods
2.1 Participants Forty outpatients (18 males, 22 females; mean age 24.60 ± 4.12 years, range 18–31 years) who were diagnosed with OCD according to the Structure Clinical Interview for DSM-IV Axis I Disorders (SCID-I) were recruited from the Psychological Clinic at Second Xiangya Hospital of Central South University of Hunan Province, China between September 2014 and October 2015. The exclusion criteria were: (1) comorbid psychiatric disorders (Axis I or Axis II); (2) history of specific medical or neurological problems, such as hyperactivity, organic mental disease, mental retardation, history of psychosurgery, or history of epilepsy; (3) history of taking psychoactive medication in the past 3 months; and (4) severe alcohol or substance abuse. Thirty-eight HCs (16 males, 22 females; mean age 23.32 ± 2.68 years, range 18–30 years) were recruited from the community and Central South University by poster advertisements. All HC subjects were screened with the Structured Clinical Interview for the DSM-Non-Patient edition (SCID-NP) to confirm a lifetime absence of psychiatric and neurologic illness. This study was approved by the Ethics Committee of the Second Xiangya Hospital of Central South University. All participants provided written informed consent prior to their inclusion in the study.
2.2 Clinical and neurocognitive assessments Severity of obsessive-compulsive symptoms in the OCD patients was measured with the Yale-Brown Obsessive-Compulsive Scale (Y-BOCS; Goodman et al., 1989a,
1989b). The Chinese version of this instrument (Xu and Zhang, 2006), which was used in the present study, has been demonstrated to have good reliability and validity, good internal consistency for the total score (Cronbach's α = 0.87), and acceptable interrater agreement [intraclass correlation coefficients (ICCs) > 0.75 for total score and items]. Beck’s Depression Inventory (BDI; Beck, et al., 1961) and the State-Trait Anxiety Inventory (STAI; Spielberger et al., 1983) were used to assess the severity of depressive and anxiety symptoms experienced by each participant, respectively. The Chinese versions of the BDI and STAI, which were used in the present study, have been shown to have satisfactory psychometric properties (Shek, 1988; 1990). A battery of background neurocognitive tests was administered to measure various aspects of cognition in both the OCD patients and the HCs. Estimated IQ was assessed using the information, arithmetic, similarity, and digit span subscales of the Chinese version of the Wechsler Adult Intelligence Scale-Revised (WAIS-R; Gong, 1992). Verbal and visual memory (-immediate and -delay) ability were assessed with the logical memory and visual reproduction subtests of the Chinese version of the Wechsler Memory Scale-Revised (WMS-R; Gong et al., 1989). For the logical memory subtest of the WMS-R, a short story consisting of 23 units was read aloud to the participants at a consistent pace. The subjects were then asked to recall the story immediately and 30 min after the reading. For the visual reproduction subtest of the WMS-R, the participants were shown two composite figures, one at a time for 10 s each, and then they were asked to reproduce those figures immediately and 30 min later. The Letter-Number Span Test (LNST; Chan et al., 2008) was conducted to
assess working memory. In this test, the participants were asked to sort numbers from letters within a row of alternating numbers and letters that was read to them, and to recall the numbers and letters separately in successive order. For example, the answer for the prompt “B2E63” would be “236BE.” The number of correct recalls for all trials with increasing difficulty (from two to seven items) was calculated. Finally, the 1-min verbal fluency test (Wang et al., 2008) was performed to assess EF. This test requires the participants to verbalize as many names of things in a category (i.e. animals in this study) as they can within 1 min. The number of reported animals was calculated (replicates excluded).
2.3 Assessment of cognitive and affective ToM The Chinese version of the computerized Yoni task (programmed with E-prime 2.0; Gu, et al., 2012) was used to assess both the cognitive (i.e. understanding and making inferences about others’ beliefs and motivations) and affective (i.e. inferring others’ feelings and emotions) components of ToM. The task was comprised of 98 trials, which were divided into three conditions: cognitive (36 trials), affective (48 trials), and physical (14 trials). Each condition included first- and second-order trials, with 12, 8, and 8 first-order trails for the cognitive (Cog1), affective (Aff1), and physical (Phy1) conditions, respectively, and 24, 36, and 6 second-order trails for the cognitive (Cog2), affective (Aff2) and physical (Phy2) conditions, respectively. In each Yoni task trial (Figure 1), a cartoon face named Yoni was presented in the middle of the screen with four colored pictures showing either a cartoon face or an
example of a single semantic category (e.g., fruits, animals, etc.) in each corner of the screen. Participants were asked to identify which picture Yoni was referring to based on an incomplete sentence shown at the top of the screen and available cues, such as Yoni’s eye gaze and facial expression or the eye gaze and facial expression of the image to which Yoni was referring. Answers in the physical condition required only a basic analysis of physical attributes relative to the character (e.g.,“Yoni is close to...”), whereas answering the cognitive and affective ToM trials required the subject to make an inference regarding Yoni’s mental state with respect to one of the four images in the corners (e.g., “Yoni is thinking of...“ or “Yoni loves...”). In half of the items, Yoni stares at one of the four stimuli (the correct answer); in the other half, he looks straight ahead. Participants were asked to choose the correct answer by clicking it with the computer mouse. The physical condition trials were used to check participants’ understanding of the task. Those with less than 50% success in the physical condition trials were excluded from the final analysis. For all items, accuracy was recorded.
2.4 Data analyses All statistical analyses were carried out with the Statistical Package for the Social Sciences version 18.0 for Windows. Before examining group differences in demographic,
clinical,
and
neurocognitive
variables,
one-sample
Kolmogorov-Sminov tests were applied to evaluate the normalcy of the distribution of each continuous variable. For normally distributed data, parametric methods were
used (t-test, Pearson correlations). In the remaining cases, non-parametric methods were used (Mann-Whitney U test, Spearman’s rank correlations). Differences in gender distribution (categorical data) were detected with the chi-squared test. Participants’ performance in the Yoni task was assessed with repeated measures (rm) analysis of variance (ANOVA)
for first- and second-order respectively, with group
(OCD patients and HCs) as the between-subjects factor, and ToM conditions (cognitive, affective, and physical) as the within-subjects factor. Multivariate ANOVAs (MANOVAs) were conducted to further identify between-group differences within a particular ToM condition. To investigate the impact of other neurocognitive functions on ToM, multivariate analysis of covariance (MANCOVA) was conducted to detect group differences in ToM performance, with neurocognitive variables that differed significantly between the groups as well as those that were related significantly to any of the ToM conditions in the OCD group being treated as covariates. A two-sided α-level of 0.05 was set as the significance cut-off for all tests performed.
3. Results 3.1 Demographic data and background clinical and neurocognitive assessment The data obtained for all variables were confirmed to be normally distributed (p > 0.05). The participants’ demographic data are shown in Table 1. Notably, the two groups of participants did not differ significantly in age, gender ratio, years of education, or estimated IQ (all ps > 0.05). For the clinical variables, OCD patients
scored higher than HCs on the BDI and STAI-T (both ps < 0.01). With the exception of the logical memory subtest of the WMS-R and 1-min verbal fluency test (both ps < 0.05), there were no other significant differences between OCD patients and HCs in any neurocognitive tests.
3.2 Participants’ performance in the Yoni task For the first-order ToM data, a rmANOVA revealed neither a main effect of ToM condition (Hotelling’s Trace; F2,75 = 0.047, p = 0.955), nor a main effect of group (F1,76 = 0.849, p = 0.360). There is not a significant group × condition interaction (F2,75 = 1.056, p = 0.353). For the second-order ToM data, a rmANOVA demonstrated a main effect of ToM condition (F2,75 = 15.920, p < 0.001) as well as a main effect of group (F1,76 = 5.463, p = 0.022), with OCD patients scoring lower than HCs in the Yoni task. Post-hoc pairwise comparisons found that, across the two groups, accuracy in the Phy2 condition was significantly higher than that in the Cog2 and Aff2 conditions (ps < 0.001), while accuracy in the Aff2 condition did not differ significantly from that in the Cog2 condition (p = 0.209). We did not find a significant group × condition interaction in the second-order ToM data (F2,75 = 1.825, p = 0.168). MANOVA results showed that OCD patients scored significantly lower than HCs in the Aff2 condition (OCD: 73.9% ± 0.15, HC: 84.4% ± 0.13, p = 0.002); no group differences in performance were detected in the Cog2 condition (OCD: 73.3% ± 0.22, HC: 81.3% ± 0.17, p = 0.077) or the Phy2 condition (OCD: 88.3% ± 0.22, HC: 91.2% ± 0.17, p =
0.431).
3.3 ToM relationships with clinical characteristics and other neurocognitive functions As shown in Table 2, in OCD patients, Spearman ’s correlational analyses showed that participants’ second-order ToM performance scores correlated with estimated IQ (Aff2: r = 0.608, p < 0.001; Cog2: r = 0.475, p = 0.002; Phy2: r = 0.433, p = 0.005) and LNST correct span score (Aff2: r = 0.314, p = 0.048; Cog2: r = 0.444, p = 0.001; Phy2: r = 0.463, p = 0.003), but not with other neurocognitive functions (all ps > 0.05). When WMS-R logical memory subscore, 1-min verbal fluency score, estimated IQ, and LNST correct span score were treated as covariates in a MANCOVA, significant group differences remained in the Aff2 condition (F1,71 = 5.433, p = 0.023), but not in the Cog2 condition (F1,71 = 0.322, p = 0.572) or the Phy2 condition ( F1,71 = 0.009, p = 0.927).
4. Discussion This is the first study to our knowledge to examine both the cognitive and affective components of ToM in OCD patients. The first main finding of the present study was that OCD patients exhibited preserved first-order ToM, but displayed selective difficulties in inferring and attributing second-order affective mental states. The second main finding of this study was that the ToM deficits observed in our OCD group could not be attributed to other neurocognitive dysfunctions because when
other neurocognitive dysfunctions were taken into account, the OCD patients still performed worse than HCs in the second-order affective ToM condition. Consistent with the findings of previous studies (Mavrogiorgou et al., 2016; Sayın et al., 2010) suggesting that the basic ToM is generally intact in OCD patients, our patients with OCD did not perform significant worse than HCs in the first-order ToM condition. These findings are consistent with the notion that ToM impairments in OCD patients may be confined to complex, higher-order ToM tasks. Conversely, our finding of a selective second-order affective ToM impairment in OCD patients conflicts with prior studies not finding second-order ToM impairment in OCD patients (Carluer et al., 2015; Laisney et al., 2013). We think this discrepancy may be due to the ToM tests used in the previous studies (i.e., second-order false belief tasks) assessing the cognitive component of ToM selectively. The Yoni task has the putative advantage of enabling detection of affective ToM. Additionally, the Yoni task provides a visual measure of ToM based on verbal cues, eye gaze, and facial expression, which is likely to reduce the languages, attention, and memory demands of the task, relative to a verbally-based task. The possibility that ToM impairments might be attributable to other cognitive dysfunctions has been a recurring issue. To address this issue, we explored the relationship between ToM and other nuerocognitive functions. Our results do not provide evidence of any other neurocognitive dysfunction underlying impaired affective ToM in OCD patients. Notably, ToM has been predicted to correlate with other neurocognitive functions, with EF in particular being posited as being linked to
ToM (Pellicano, 2007; Saltzman et al., 2000). However, some researchers have described dissociations between ToM and EF (Channon et al., 2004; Fine et al., 2001). Although EF was significantly impaired in our OCD patients, as evidenced by their reduced 1-min verbal fluency performance, it did not correlate with their ToM performance. Our results are consistent with the findings of Sayın et al. (2010) in supporting the notion that any ToM abnormality in individuals with OCD is independent of EF abilities. Meanwhile, after controlling for EF, intelligence and memory in a MANCOVA, the group difference in second-order affective condition performance remained significant. Our results further demonstrated that affective ToM abnormality in OCD patients could not be attributed to abnormalities in intelligence or memory. Our findings that OCD patients reported experiencing more depressive and anxiety symptoms than HCs are consistent with previous studies (Vivan et al., 2013; Whiteside et al., 2006). However, we did not find any evidence of an association between an affective ToM deficit and OCD symptom severity, OCD duration, or depressive and anxiety symptoms in OCD patients. The present results suggest that the affective ToM deficit observed in OCD patients is related to OCD per se and cannot be ascribed to any other clinical impairment. This study has several limitations. First, we used a convenience sampling technique to recruit participants, due to limited time and resources, which limits the generalizability of our results. Second, our study sample was relatively small. Consequently, our study should be regarded as exploratory. ToM subcomponent
assessments should be repeated with larger numbers of OCD patients. Third, our cross-sectional design does not provide information about how ToM impairments evolve with OCD progression, treatment resistance, or changes in OCD symptomatology. Longitudinal studies of how ToM might differ between patients with active illness and those with recovered OCD should be pursued. In conclusion, affective ToM was selectively impaired in OCD patients. That impairment could not be attributed to other neurocognitive deficits or clinical characteristics. Notwithstanding the aforementioned limitations, our study adds to the extremely limited literature on social cognition in OCD. From a clinical perspective, effective interventions for affective ToM may benefit patients with OCD.
Role of funding source This work was supported by the National Key Technology Research and Development Program of the Ministry of Science and Technology of China (Grant Nos. 2012BA136B01), the Beijing Training Project for the Leading Talents in S & T (Z151100000315020), and the Strategic Priority Research Program (B) of the Chinese Academy of Science (XDB02030002).
Contributors Zhu designed the study; Zhu, Liu, Fan, Gan, Lei, and Niu carried out experiments; Liu performed the data analyses and wrote the manuscript; and Fan and Chan contributed significantly to manuscript preparation.
Conflict of interest The authors declare that they have no conflicts of interest.
Acknowledgements The authors would like to thank all participants for their thoughtful contributions to the study.
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Table 1 Demographics, clinical characteristics, and neurocognitive functioning of OCD patients and HCs. OCD patients
HCs
Characteristic
t/2
df
p
(N = 40)
(N = 38)
24.60 (4.12)
23.32 (2.68)
1.638
76
0.106
18:22
16:22
0.066
1
0.797
15.85 (2.13)
16.29 (1.56)
-1.035
76
0.304
Estimated IQ a
113.73 (10.41)
117.42 (9.57)
-1.629
76
0.107
Illness Duration (months)
49.45 (49.35)
-
Y-BOCS-total
30.15 (6.93)
-
Y-BOCS-obsession
15.63 (3.90)
-
Y-BOCS-compulsion
12.88 (4.76)
-
BDI a
17.65 (11.60)
5.03 (5.35)
6.220
76
< 0.001
STAI-S a
43.70 (6.03)
43.53 (5.58)
0.132
76
0.895
STAI-T a
48.13 (6.75)
43.21 (5.47)
3.532
76
0.001
Logical Memory-immediate a
11.50 (4.11)
13.50 (3.63)
-2.274
76
0.026
Logical Memory-delay a
9.03 (3.65)
11.05 (4.12)
-2.304
76
0.024
Visual Memory-immediate a
19.43 (3.30)
20.29 (3.21)
-1.172
76
0.245
Visual Memory- delay a
19.13 (3.38)
19.95 (3.35)
-1.079
76
0.284
15.13 (3.44)
15.84 (3.36)
-0.932
76
0.354
20.58 (4.65)
22.87 (4.28)
-2.262
76
0.027
Age (years) a Gender (M:F) b Years of education (years) a
Episodic Memory
Working Memory LNST Correct span a Executive function Verbal Fluency a
Notes: F = Female, M = Male; df = degree of freedom; Y-BOCS = the Yale-Brown Obsessive-Compulsive Scale; BDI = the Beck’s Depression Inventory; STAI = the State-Trait Anxiety Inventory; LNST = Letter Number Span Test; a t-test; b Chi-squared test.
Table 2 Spearman’s correlation between ToM and clinical characteristics and other aspects of neurocognitive functioning in OCD patients. Parameter
Aff1
Cog1
Phy1
Aff2
Cog2
Phy2
Estimated IQ
0.305
0.182
0.131
0.608**
0.475**
0.433**
Illness Duration (months)
-0.187
-0.076
0.180
0.009
10.086
-0.198
YBOCS-total
0.038
-0.081
0.119
0.215
0.079
-0.026
Y-BOCS-obsession
0.032
-0.031
0.015
0.163
0.144
-0.052
Y-BOCS-compulsion
-0.063
-0.177
0.102
0.109
-0.092
-0.070
BDI
0.186
0.231
-0.130
0.290
0.149
-0.069
STAI-S
0.231
0.121
0.116
0.131
-0.063
-0.098
STAI-T
0.239
0.150
0.028
0.104
-0.037
-0.164
Logical Memory-immediate
0.227
0.263
0.007
0.210
0.259
0.032
Logical Memory-delay
0.133
0.183
-0.067
0.078
0.236
0.096
Visual Memory-immediate
0.066
0.048
-0.091
0.280
0.292
0.158
Visual Memory- delay
0.121
0.114
-0.188
0.219
0.310
0.239
LNST Correct span
0.202
0.042
0.105
0.314*
0.444**
0.419**
0.230
0.224
0.139
0.278
0.260
0.153
Memory
EF Verbal Fluency
Notes: Y-BOCS = Yale-Brown Obsessive-Compulsive Scale; BDI = Beck’s Depression Inventory; STAI = the State-Trait Anxiety Inventory; LNST = Letter Number Span Test; EF = executive function; *p < 0.05; ** p < 0.01
Highlights · The second-order affective ToM is selectively impaired in OCD patients. · ToM deficit in OCD is largely independent from other neurocognitive impairments. · ToM performance in OCD does not correlate with clinical characteristics.
1st order
2nd order
Cognitive
Affective
Physical
Figure 1 Illustrations of the Chinese version of the Yoni task.
PII: DOI: Reference:
S0165-1781(16)31952-7 http://dx.doi.org/10.1016/j.psychres.2017.06.058 PSY10605
To appear in: Psychiatry Research Received date: 20 November 2016 Revised date: 7 March 2017 Accepted date: 16 June 2017 Cite this article as: Wanting Liu, Jie Fan, Jun Gan, Hui Lei, Chaoyang Niu, Raymond C.K. Chan and Xiongzhao Zhu, Disassociation of cognitive and affective aspects of theory of mind in obsessive-compulsive disorder, Psychiatry Research, http://dx.doi.org/10.1016/j.psychres.2017.06.058 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Disassociation of cognitive and affective aspects of theory of mind in obsessive-compulsive disorder
Wanting Liua, Jie Fana, Jun Gana, Hui Leib, Chaoyang Niua, Raymond C. K. Chanc,d，Xiongzhao Zhua,*
a
Medical Psychological Center, The Second Xiangya Hospital, Central South
University, Changsha, Hunan 410011, China b
c
College of Education, Hunan Agriculture University, Changsha 410128, P.R. China
Neuropsychology and Applied Cognitive Neuroscience Laboratory, CAS Key
Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, China d
Department of Psychology, University of Chinese Academy of Sciences, Beijing,
China
*
Corresponding author at: Medical Psychological Institute of the Second Xiangya
Hospital, Central South University, Renmin Road 139, Changsha, Hunan, PR China 410011. Tel: +86 731 85292126; Fax: +86 731 85361328; Email address: [email protected].
Abstract Impairment in social functioning has been widely described in obsessive-compulsive disorder (OCD). However, several aspects of social cognition, such as theory of mind (ToM), have not been substantially investigated in this context. This study examined cognitive and affective ToM in 40 OCD patients and 38 age-, sex-, and education-matched healthy controls (HCs) with the computerized Yoni task and a battery of neurocognitive tests. OCD symptom severity was assessed with the Yale-Brown Obsessive-Compulsive Scale (Y-BOCS). Depressive and anxiety symptoms were also assessed. Compared to HCs, OCD patients performed worse on second-order affective condition trials, but not cognitive or physical condition trials, of the Yoni task; there were not group differences in any of the first-order condition domains. Second-order ToM performance of OCD patients was associated with estimated intelligence and working memory performance. After controlling for neurocognitive variables, the group difference in second-order affective condition performance remained significant. These findings indicate that the affective component of ToM may be selectively impaired in OCD patients and that the observed deficit is largely independent of other neurocognitive impairments and clinical characteristics. Key words Obsessive-compulsive disorder; social cognition; theory of mind; metalizing; executive function
1. Introduction Obsessive-compulsive disorder (OCD) is a relatively common neuropsychiatric disorder characterized by intrusive and recurrent thoughts or images (obsessions) and/or repetitive and ritualistic acts or behaviors (compulsions) that the patients feel driven to perform to neutralize anxiety or distress induced by obsessions (American Psychiatric Association, 2013). Neurocognitive dysfunction, particularly in the areas of executive function (EF) and memory, have long been recognized (Abramovitch et al., 2013; Kuelz et al., 2004). It has been suggested that deficits in social cognition may be common to patients with basal ganglia abnormalities, including those with Huntington disease, Parkinson disease, and perhaps also OCD (Bodden et al., 2010). Unlike most neurocognitive functions described in the literature, which refer to functions that are associated with a particular brain area, pathway, or network, social cognition encompasses a mixture of cognitive processes that contribute to social interactions. Social cognition integrates a variety of socio-emotional abilities and experiences that influence one’s relationships with others and enable one to interpret others’ behaviors; in human psychology, social cognition is described as including several subdomains, namely social cue interpretation, emotion recognition, empathy, and theory of mind (ToM)(Adolphs, 2001). ToM is the capacity to make inferences about others’ mental states in terms of feelings, intentions, desires, and beliefs, which enables one to understand and predict other people’s behavior (Call and Tomasello, 2008), and thus is considered to be an essential prerequisite for successful social interaction (Brüne and Brüne-Cohrs, 2006). Some researchers have begun to break
down the complex notion of ToM into components. Apart from simply differentiating ToM with respect to task complexity into first- and second-order levels (Baron-Cohen, 1995), recent research suggests that cognitive ToM, that is, understanding and making inferences about others’ beliefs and motivations, should be distinguished from affective ToM, which is defined as inferring others’ feelings and emotions (Kalbe et al., 2007). Although social functioning impairments are often seen in OCD (Bystritsky et al., 2001), relative to other neurodevelopmental and psychiatric disorders such as autism (Baron-Cohen, 2000), schizophrenia (Brüne, 2005), bipolar affective disorder (Kerr et al., 2003), and depression (Inoue et al., 2006), ToM has received very little attention in OCD research. To the best of our knowledge, only two studies have examined ToM in OCD patients. Sayın et al. (2010) administered various ToM tasks including the Hinting task, double-bluff task, and first- and second-order false belief tasks, as well as some tests for memory and EF to 30 OCD patients and 30 age-, sex- and education-matched healthy controls (HCs). They found that OCD patients only performed significantly worse than HCs on the double-bluff task, and that their performance on that task correlated with memory capacity, suggesting that OCD patients were impaired in advanced ToM abilities, but had preserved basic ToM abilities (Sayın et al., 2010). More recently, Mavrogiorgou et al. (2016) administered the Hinting Task and the faux pas test to 20 OCD patients and 20 age-, sex- and education-matched HCs. They found that OCD patients did not differ from HCs with regard to performance in either task, leading them to concur that basic-level ToM was
normal in OCD patients. Historically, ToM in OCD research has been considered to be a hierarchical construct without differentiation between cognitive and affective aspects. Hence, it remains unclear whether OCD patients have impaired cognitive and/or affective ToM. In addition, previous ToM studies in other psychiatric populations have, usually, conducted two separate tasks to assess the cognitive and affective components of ToM independently (Russell et al., 2009; Santangelo et al., 2013). However, adequate control conditions for these ToM tasks have not been applied consistently. Moreover, the assessments of cognitive versus affective ToM tasks may be tapping into different cognitive demands, which may confound the cognitive-affective differentiation of ToM. Ideally, both the cognitive and affective components of ToM should be assessed in the same task with adequate control conditions. A novel cartoon-based ToM paradigm called the Yoni Task (Shamay-Tsoory and Aharon-Peretz, 2007) appears to be a promising paradigm with which to assess ToM abilities in OCD patients because it has three highly comparable conditions
(cognitive, affective, and physical) that
each contain first- and second-order items. The first aim of the present study was to further assess cognitive and affective components in OCD patients with the Yoni Task. Secondly, we examined how performance on this task may be related to clinical characteristics of OCD and other aspects of neurocognitive functioning.
2. Methods
2.1 Participants Forty outpatients (18 males, 22 females; mean age 24.60 ± 4.12 years, range 18–31 years) who were diagnosed with OCD according to the Structure Clinical Interview for DSM-IV Axis I Disorders (SCID-I) were recruited from the Psychological Clinic at Second Xiangya Hospital of Central South University of Hunan Province, China between September 2014 and October 2015. The exclusion criteria were: (1) comorbid psychiatric disorders (Axis I or Axis II); (2) history of specific medical or neurological problems, such as hyperactivity, organic mental disease, mental retardation, history of psychosurgery, or history of epilepsy; (3) history of taking psychoactive medication in the past 3 months; and (4) severe alcohol or substance abuse. Thirty-eight HCs (16 males, 22 females; mean age 23.32 ± 2.68 years, range 18–30 years) were recruited from the community and Central South University by poster advertisements. All HC subjects were screened with the Structured Clinical Interview for the DSM-Non-Patient edition (SCID-NP) to confirm a lifetime absence of psychiatric and neurologic illness. This study was approved by the Ethics Committee of the Second Xiangya Hospital of Central South University. All participants provided written informed consent prior to their inclusion in the study.
2.2 Clinical and neurocognitive assessments Severity of obsessive-compulsive symptoms in the OCD patients was measured with the Yale-Brown Obsessive-Compulsive Scale (Y-BOCS; Goodman et al., 1989a,
1989b). The Chinese version of this instrument (Xu and Zhang, 2006), which was used in the present study, has been demonstrated to have good reliability and validity, good internal consistency for the total score (Cronbach's α = 0.87), and acceptable interrater agreement [intraclass correlation coefficients (ICCs) > 0.75 for total score and items]. Beck’s Depression Inventory (BDI; Beck, et al., 1961) and the State-Trait Anxiety Inventory (STAI; Spielberger et al., 1983) were used to assess the severity of depressive and anxiety symptoms experienced by each participant, respectively. The Chinese versions of the BDI and STAI, which were used in the present study, have been shown to have satisfactory psychometric properties (Shek, 1988; 1990). A battery of background neurocognitive tests was administered to measure various aspects of cognition in both the OCD patients and the HCs. Estimated IQ was assessed using the information, arithmetic, similarity, and digit span subscales of the Chinese version of the Wechsler Adult Intelligence Scale-Revised (WAIS-R; Gong, 1992). Verbal and visual memory (-immediate and -delay) ability were assessed with the logical memory and visual reproduction subtests of the Chinese version of the Wechsler Memory Scale-Revised (WMS-R; Gong et al., 1989). For the logical memory subtest of the WMS-R, a short story consisting of 23 units was read aloud to the participants at a consistent pace. The subjects were then asked to recall the story immediately and 30 min after the reading. For the visual reproduction subtest of the WMS-R, the participants were shown two composite figures, one at a time for 10 s each, and then they were asked to reproduce those figures immediately and 30 min later. The Letter-Number Span Test (LNST; Chan et al., 2008) was conducted to
assess working memory. In this test, the participants were asked to sort numbers from letters within a row of alternating numbers and letters that was read to them, and to recall the numbers and letters separately in successive order. For example, the answer for the prompt “B2E63” would be “236BE.” The number of correct recalls for all trials with increasing difficulty (from two to seven items) was calculated. Finally, the 1-min verbal fluency test (Wang et al., 2008) was performed to assess EF. This test requires the participants to verbalize as many names of things in a category (i.e. animals in this study) as they can within 1 min. The number of reported animals was calculated (replicates excluded).
2.3 Assessment of cognitive and affective ToM The Chinese version of the computerized Yoni task (programmed with E-prime 2.0; Gu, et al., 2012) was used to assess both the cognitive (i.e. understanding and making inferences about others’ beliefs and motivations) and affective (i.e. inferring others’ feelings and emotions) components of ToM. The task was comprised of 98 trials, which were divided into three conditions: cognitive (36 trials), affective (48 trials), and physical (14 trials). Each condition included first- and second-order trials, with 12, 8, and 8 first-order trails for the cognitive (Cog1), affective (Aff1), and physical (Phy1) conditions, respectively, and 24, 36, and 6 second-order trails for the cognitive (Cog2), affective (Aff2) and physical (Phy2) conditions, respectively. In each Yoni task trial (Figure 1), a cartoon face named Yoni was presented in the middle of the screen with four colored pictures showing either a cartoon face or an
example of a single semantic category (e.g., fruits, animals, etc.) in each corner of the screen. Participants were asked to identify which picture Yoni was referring to based on an incomplete sentence shown at the top of the screen and available cues, such as Yoni’s eye gaze and facial expression or the eye gaze and facial expression of the image to which Yoni was referring. Answers in the physical condition required only a basic analysis of physical attributes relative to the character (e.g.,“Yoni is close to...”), whereas answering the cognitive and affective ToM trials required the subject to make an inference regarding Yoni’s mental state with respect to one of the four images in the corners (e.g., “Yoni is thinking of...“ or “Yoni loves...”). In half of the items, Yoni stares at one of the four stimuli (the correct answer); in the other half, he looks straight ahead. Participants were asked to choose the correct answer by clicking it with the computer mouse. The physical condition trials were used to check participants’ understanding of the task. Those with less than 50% success in the physical condition trials were excluded from the final analysis. For all items, accuracy was recorded.
2.4 Data analyses All statistical analyses were carried out with the Statistical Package for the Social Sciences version 18.0 for Windows. Before examining group differences in demographic,
clinical,
and
neurocognitive
variables,
one-sample
Kolmogorov-Sminov tests were applied to evaluate the normalcy of the distribution of each continuous variable. For normally distributed data, parametric methods were
used (t-test, Pearson correlations). In the remaining cases, non-parametric methods were used (Mann-Whitney U test, Spearman’s rank correlations). Differences in gender distribution (categorical data) were detected with the chi-squared test. Participants’ performance in the Yoni task was assessed with repeated measures (rm) analysis of variance (ANOVA)
for first- and second-order respectively, with group
(OCD patients and HCs) as the between-subjects factor, and ToM conditions (cognitive, affective, and physical) as the within-subjects factor. Multivariate ANOVAs (MANOVAs) were conducted to further identify between-group differences within a particular ToM condition. To investigate the impact of other neurocognitive functions on ToM, multivariate analysis of covariance (MANCOVA) was conducted to detect group differences in ToM performance, with neurocognitive variables that differed significantly between the groups as well as those that were related significantly to any of the ToM conditions in the OCD group being treated as covariates. A two-sided α-level of 0.05 was set as the significance cut-off for all tests performed.
3. Results 3.1 Demographic data and background clinical and neurocognitive assessment The data obtained for all variables were confirmed to be normally distributed (p > 0.05). The participants’ demographic data are shown in Table 1. Notably, the two groups of participants did not differ significantly in age, gender ratio, years of education, or estimated IQ (all ps > 0.05). For the clinical variables, OCD patients
scored higher than HCs on the BDI and STAI-T (both ps < 0.01). With the exception of the logical memory subtest of the WMS-R and 1-min verbal fluency test (both ps < 0.05), there were no other significant differences between OCD patients and HCs in any neurocognitive tests.
3.2 Participants’ performance in the Yoni task For the first-order ToM data, a rmANOVA revealed neither a main effect of ToM condition (Hotelling’s Trace; F2,75 = 0.047, p = 0.955), nor a main effect of group (F1,76 = 0.849, p = 0.360). There is not a significant group × condition interaction (F2,75 = 1.056, p = 0.353). For the second-order ToM data, a rmANOVA demonstrated a main effect of ToM condition (F2,75 = 15.920, p < 0.001) as well as a main effect of group (F1,76 = 5.463, p = 0.022), with OCD patients scoring lower than HCs in the Yoni task. Post-hoc pairwise comparisons found that, across the two groups, accuracy in the Phy2 condition was significantly higher than that in the Cog2 and Aff2 conditions (ps < 0.001), while accuracy in the Aff2 condition did not differ significantly from that in the Cog2 condition (p = 0.209). We did not find a significant group × condition interaction in the second-order ToM data (F2,75 = 1.825, p = 0.168). MANOVA results showed that OCD patients scored significantly lower than HCs in the Aff2 condition (OCD: 73.9% ± 0.15, HC: 84.4% ± 0.13, p = 0.002); no group differences in performance were detected in the Cog2 condition (OCD: 73.3% ± 0.22, HC: 81.3% ± 0.17, p = 0.077) or the Phy2 condition (OCD: 88.3% ± 0.22, HC: 91.2% ± 0.17, p =
0.431).
3.3 ToM relationships with clinical characteristics and other neurocognitive functions As shown in Table 2, in OCD patients, Spearman ’s correlational analyses showed that participants’ second-order ToM performance scores correlated with estimated IQ (Aff2: r = 0.608, p < 0.001; Cog2: r = 0.475, p = 0.002; Phy2: r = 0.433, p = 0.005) and LNST correct span score (Aff2: r = 0.314, p = 0.048; Cog2: r = 0.444, p = 0.001; Phy2: r = 0.463, p = 0.003), but not with other neurocognitive functions (all ps > 0.05). When WMS-R logical memory subscore, 1-min verbal fluency score, estimated IQ, and LNST correct span score were treated as covariates in a MANCOVA, significant group differences remained in the Aff2 condition (F1,71 = 5.433, p = 0.023), but not in the Cog2 condition (F1,71 = 0.322, p = 0.572) or the Phy2 condition ( F1,71 = 0.009, p = 0.927).
4. Discussion This is the first study to our knowledge to examine both the cognitive and affective components of ToM in OCD patients. The first main finding of the present study was that OCD patients exhibited preserved first-order ToM, but displayed selective difficulties in inferring and attributing second-order affective mental states. The second main finding of this study was that the ToM deficits observed in our OCD group could not be attributed to other neurocognitive dysfunctions because when
other neurocognitive dysfunctions were taken into account, the OCD patients still performed worse than HCs in the second-order affective ToM condition. Consistent with the findings of previous studies (Mavrogiorgou et al., 2016; Sayın et al., 2010) suggesting that the basic ToM is generally intact in OCD patients, our patients with OCD did not perform significant worse than HCs in the first-order ToM condition. These findings are consistent with the notion that ToM impairments in OCD patients may be confined to complex, higher-order ToM tasks. Conversely, our finding of a selective second-order affective ToM impairment in OCD patients conflicts with prior studies not finding second-order ToM impairment in OCD patients (Carluer et al., 2015; Laisney et al., 2013). We think this discrepancy may be due to the ToM tests used in the previous studies (i.e., second-order false belief tasks) assessing the cognitive component of ToM selectively. The Yoni task has the putative advantage of enabling detection of affective ToM. Additionally, the Yoni task provides a visual measure of ToM based on verbal cues, eye gaze, and facial expression, which is likely to reduce the languages, attention, and memory demands of the task, relative to a verbally-based task. The possibility that ToM impairments might be attributable to other cognitive dysfunctions has been a recurring issue. To address this issue, we explored the relationship between ToM and other nuerocognitive functions. Our results do not provide evidence of any other neurocognitive dysfunction underlying impaired affective ToM in OCD patients. Notably, ToM has been predicted to correlate with other neurocognitive functions, with EF in particular being posited as being linked to
ToM (Pellicano, 2007; Saltzman et al., 2000). However, some researchers have described dissociations between ToM and EF (Channon et al., 2004; Fine et al., 2001). Although EF was significantly impaired in our OCD patients, as evidenced by their reduced 1-min verbal fluency performance, it did not correlate with their ToM performance. Our results are consistent with the findings of Sayın et al. (2010) in supporting the notion that any ToM abnormality in individuals with OCD is independent of EF abilities. Meanwhile, after controlling for EF, intelligence and memory in a MANCOVA, the group difference in second-order affective condition performance remained significant. Our results further demonstrated that affective ToM abnormality in OCD patients could not be attributed to abnormalities in intelligence or memory. Our findings that OCD patients reported experiencing more depressive and anxiety symptoms than HCs are consistent with previous studies (Vivan et al., 2013; Whiteside et al., 2006). However, we did not find any evidence of an association between an affective ToM deficit and OCD symptom severity, OCD duration, or depressive and anxiety symptoms in OCD patients. The present results suggest that the affective ToM deficit observed in OCD patients is related to OCD per se and cannot be ascribed to any other clinical impairment. This study has several limitations. First, we used a convenience sampling technique to recruit participants, due to limited time and resources, which limits the generalizability of our results. Second, our study sample was relatively small. Consequently, our study should be regarded as exploratory. ToM subcomponent
assessments should be repeated with larger numbers of OCD patients. Third, our cross-sectional design does not provide information about how ToM impairments evolve with OCD progression, treatment resistance, or changes in OCD symptomatology. Longitudinal studies of how ToM might differ between patients with active illness and those with recovered OCD should be pursued. In conclusion, affective ToM was selectively impaired in OCD patients. That impairment could not be attributed to other neurocognitive deficits or clinical characteristics. Notwithstanding the aforementioned limitations, our study adds to the extremely limited literature on social cognition in OCD. From a clinical perspective, effective interventions for affective ToM may benefit patients with OCD.
Role of funding source This work was supported by the National Key Technology Research and Development Program of the Ministry of Science and Technology of China (Grant Nos. 2012BA136B01), the Beijing Training Project for the Leading Talents in S & T (Z151100000315020), and the Strategic Priority Research Program (B) of the Chinese Academy of Science (XDB02030002).
Contributors Zhu designed the study; Zhu, Liu, Fan, Gan, Lei, and Niu carried out experiments; Liu performed the data analyses and wrote the manuscript; and Fan and Chan contributed significantly to manuscript preparation.
Conflict of interest The authors declare that they have no conflicts of interest.
Acknowledgements The authors would like to thank all participants for their thoughtful contributions to the study.
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Table 1 Demographics, clinical characteristics, and neurocognitive functioning of OCD patients and HCs. OCD patients
HCs
Characteristic
t/2
df
p
(N = 40)
(N = 38)
24.60 (4.12)
23.32 (2.68)
1.638
76
0.106
18:22
16:22
0.066
1
0.797
15.85 (2.13)
16.29 (1.56)
-1.035
76
0.304
Estimated IQ a
113.73 (10.41)
117.42 (9.57)
-1.629
76
0.107
Illness Duration (months)
49.45 (49.35)
-
Y-BOCS-total
30.15 (6.93)
-
Y-BOCS-obsession
15.63 (3.90)
-
Y-BOCS-compulsion
12.88 (4.76)
-
BDI a
17.65 (11.60)
5.03 (5.35)
6.220
76
< 0.001
STAI-S a
43.70 (6.03)
43.53 (5.58)
0.132
76
0.895
STAI-T a
48.13 (6.75)
43.21 (5.47)
3.532
76
0.001
Logical Memory-immediate a
11.50 (4.11)
13.50 (3.63)
-2.274
76
0.026
Logical Memory-delay a
9.03 (3.65)
11.05 (4.12)
-2.304
76
0.024
Visual Memory-immediate a
19.43 (3.30)
20.29 (3.21)
-1.172
76
0.245
Visual Memory- delay a
19.13 (3.38)
19.95 (3.35)
-1.079
76
0.284
15.13 (3.44)
15.84 (3.36)
-0.932
76
0.354
20.58 (4.65)
22.87 (4.28)
-2.262
76
0.027
Age (years) a Gender (M:F) b Years of education (years) a
Episodic Memory
Working Memory LNST Correct span a Executive function Verbal Fluency a
Notes: F = Female, M = Male; df = degree of freedom; Y-BOCS = the Yale-Brown Obsessive-Compulsive Scale; BDI = the Beck’s Depression Inventory; STAI = the State-Trait Anxiety Inventory; LNST = Letter Number Span Test; a t-test; b Chi-squared test.
Table 2 Spearman’s correlation between ToM and clinical characteristics and other aspects of neurocognitive functioning in OCD patients. Parameter
Aff1
Cog1
Phy1
Aff2
Cog2
Phy2
Estimated IQ
0.305
0.182
0.131
0.608**
0.475**
0.433**
Illness Duration (months)
-0.187
-0.076
0.180
0.009
10.086
-0.198
YBOCS-total
0.038
-0.081
0.119
0.215
0.079
-0.026
Y-BOCS-obsession
0.032
-0.031
0.015
0.163
0.144
-0.052
Y-BOCS-compulsion
-0.063
-0.177
0.102
0.109
-0.092
-0.070
BDI
0.186
0.231
-0.130
0.290
0.149
-0.069
STAI-S
0.231
0.121
0.116
0.131
-0.063
-0.098
STAI-T
0.239
0.150
0.028
0.104
-0.037
-0.164
Logical Memory-immediate
0.227
0.263
0.007
0.210
0.259
0.032
Logical Memory-delay
0.133
0.183
-0.067
0.078
0.236
0.096
Visual Memory-immediate
0.066
0.048
-0.091
0.280
0.292
0.158
Visual Memory- delay
0.121
0.114
-0.188
0.219
0.310
0.239
LNST Correct span
0.202
0.042
0.105
0.314*
0.444**
0.419**
0.230
0.224
0.139
0.278
0.260
0.153
Memory
EF Verbal Fluency
Notes: Y-BOCS = Yale-Brown Obsessive-Compulsive Scale; BDI = Beck’s Depression Inventory; STAI = the State-Trait Anxiety Inventory; LNST = Letter Number Span Test; EF = executive function; *p < 0.05; ** p < 0.01
Highlights · The second-order affective ToM is selectively impaired in OCD patients. · ToM deficit in OCD is largely independent from other neurocognitive impairments. · ToM performance in OCD does not correlate with clinical characteristics.
1st order
2nd order
Cognitive
Affective
Physical
Figure 1 Illustrations of the Chinese version of the Yoni task.