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Self-reported and experimentally induced self-disgust is heightened in Parkinson’s disease: Contribution of behavioural symptoms


Authors: Marianna Tsatali aff001;  Paul G. Overton aff002;  Ana B. Vivas aff003
Authors place of work: South East European Research Center, SEERC, Thessaloniki, Greece aff001;  Psychology Department, University of Sheffield, Sheffield, United Kingdom aff002;  Psychology Department, The University of Sheffield International Faculty, City College, Thessaloniki, Greece aff003
Published in the journal: PLoS ONE 14(10)
Category: Research Article
doi: https://doi.org/10.1371/journal.pone.0223663

Summary

Parkinson’s disease (PD) is associated with deficits in the recognition and expression of basic emotions, although self-reported levels of the self-conscious emotions shame and embarrassment are higher. However, one self-conscious emotion—self-disgust–which has been shown to have a negative impact on psychological wellbeing, has not been investigated in PD before. Here we employed self-report measures of self-conscious emotions, and an emotion induction paradigm involving images of the self, and narrated personal vignettes of instances when patients with PD (and controls) found themselves disgusting. We found that self-reported and induced levels of self-disgust were higher in PD patients than in matched controls, and that trait self-disgust was specifically related to disorders of impulse control in PD patients. Given the link between self-disgust and impaired psychological wellbeing, and the prevalence of anxiety and depression in PD, self-disgust might make a useful therapeutic target for psychological interventions in the condition.

Keywords:

Patients – Cognitive impairment – emotions – anxiety – Face recognition – depression – Impulsivity – Parkinson disease

Introduction

Parkinson’s disease (PD) is a neurodegenerative condition involving the dopaminergic neurons of the substantia nigra, classically characterised by motor symptoms [12]. However, a number of non-motor symptoms, such as depression, anxiety, sleep problems, and Impulse Control Disorders (ICDs), are now also recognised to be part of the condition [3]. In addition, over the last two decades there has been growing interest in emotional processes in PD, as a number of studies have reported emotional disturbances in the disorder [46]. Emotional disturbances in PD may not be too surprising given the looped architecture of the basal ganglia within which the substantia nigra pars compacta operates, and the clear identification of a limbic (emotional) loop within that architecture [7].

In relation to the basic emotions, changes in PD have been identified in the recognition of emotional stimuli. There is consistency across studies that PD patients are less able to decode emotional features delivered through prosodic elements of the human voice [810]. Parkinson’s patients are also impaired at recognising emotions in facial expressions [89, 1114]. The deficits in emotion recognition, both in terms of prosody and facial expressions, appear to be worse for negative emotions [89, 15], and importantly are unrelated to depression [9, 4] and medication status [4].

In addition to changes in the recognition of emotional stimuli, changes have also been reported in vocal and facial expressions of emotion. Parkinson’s patients exhibit a reduced pitch and loudness range (‘dysprosody’) when producing emotional speech [1619], and are impaired when it comes to making spontaneous and posed facial expressions [17, 2023]. Again, changes in emotional expression, at least in terms of the face, are independent of depression [21,23] and seem to be worse for negative emotions [2123]. The impairments in vocal expression on the other hand may be broader, involving both sad and happy prosody [19].

In contrast to the widely reported impairments in emotion recognition and emotional expression in PD, experience of the basic emotions seems to be relatively unimpaired, whether that be the subjectively reported valence of emotions induced by images [2425], or subjective emotional reactions (including amusement) induced by video clips [23,26], although arousal levels appear to be lower in PD patients [2425,27]. However, the picture is somewhat different when it comes to self-conscious emotions rather than basic emotions. Self-conscious emotions are emotions that relate to our sense of self and our awareness of others’ reactions to us [28]. Although these emotions have been considered far less in relation to PD than the basic emotions, and have not been examined before in explicit emotion induction paradigms (unlike the basic emotions–see above), PD patients report increased levels of shame [2930] and embarrassment [3135], related to speech and language difficulties and the visibility of their condition. However, one potentially significant self-conscious emotion that has thus far received no attention in PD is self-disgust. Self-disgust is an aversive self-conscious affective state, independent of other self-conscious emotions like shame [36], that reflects disgust directed towards the self [37] and encompasses two dimensions: disgust directed towards one’s physical characteristics (physical self-disgust), and disgust directed towards one’s actions (behavioural self-disgust). Self-disgust has been operationalised as an “emotion schema”, which involves a lasting appraisal of aspect(s) of the self as disgusting [36], and growing evidence suggests that self-disgust is a causative factor in poor psychological wellbeing beyond shame and guilt [36,38].

In relation to PD, self-disgust may be particularly pertinent. Firstly, research has shown elevated levels of self-disgust (linked to poor psychological wellbeing) in other chronic illnesses, both physical [39] and psychological [4042]. Secondly, we have argued that the self-disgust schema is constructed at least in part from the reading and decoding of emotional reactions in others to enduring characteristics of one’s self and one’s behaviour [36]. As consequence, given that PD is a disorder with a highly visible behavioural syndrome of the classical motor symptoms [1], drug-induced dyskinesias [43], emotional expressivity problems [1617], and non-motor symptoms like ICDs [44]—all of which break sociocultural rules for ‘normality’–reactions by others to the disorder are likely to be prominent and frequently encountered. We suggest that these reactions are likely to be intense enough to break through any emotional recognition difficulties the patients may have. Indeed, the increased levels of shame and embarrassment in PD [29,31] suggest that patients are very sensitive to their symptoms.

With this in mind, in the present study we have assessed self-reported levels of self-disgust in a group of PD patients (relative to matched controls), and examined a range of potential predictors of self-disgust in this population. Included amongst these are impulsivity, ICDs and the dopamine replacement therapies which appear to play a role in their induction [44], all of which contribute to behaviours which could be causative in establishing a self-disgust schema. In addition, we have evaluated the possibility of inducing self-disgust in PD patients in an experimental context.

We hypothesize that baseline levels of self-disgust will be higher in patients and, given the evidence above that shame and embarrassment can be induced in PD patients (by the visibility of their symptoms to others), we expect it will be possible to similarly induce self-disgust in PD patients and that the extent of that induction will exceed that in controls. Assessing self-disgust and factors that predict it in this population could be the first step in tacking an important causative element in the well-documented poor psychological wellbeing in PD [45]. Also, given the well understood pathological process in PD, alterations in self-disgust might give clues to the neural substrate for the emotion, which as yet remains elusive, except for evidence of amygdala involvement, although in women with borderline personality disorder [46].

Materials and methods

Participants

Forty-five patients diagnosed with PD and 45 healthy participants matched on age (in years), gender and education (in years) took part in the study (see Table 1). Patients were recruited from the Outpatients Clinic of the Neurology Department of Papageorgiou and AXEPA Hospitals in Thessaloniki, Greece and the Parkinson Care Association ‘EPICOUROS’ in Athens, Greece. Healthy control participants were recruited from Senior Day Care centers in Thessaloniki and from a research volunteers’ data base from previous studies.

Tab. 1. Demographic and clinical characteristics of the patients with Parkinson disease (PD) and healthy controls at the time of assessment.
Demographic and clinical characteristics of the patients with Parkinson disease (PD) and healthy controls at the time of assessment.

The inclusion criteria for the patients were: i) diagnosis by a neurologist according to the UK Parkinson’s Disease Society Brain Bank Clinical Diagnostic Criteria [47], ii) to be at the mild or moderate stage of the disease according to The Unified Parkinson’s Disease Rating Scale–UPDRS- [4849] or/and the Hoehn &Yahr scale [50], iii) a score on the Mini-Mental State Examination–MMSE- [51] equal to or above 24 [52], iv) no evidence of other types of neurological or psychiatric diseases (except for anxiety and depression), such as atypical parkinsonism, idiopathic tremor, parkinsonism syndromes or vascular parkinsonism; and v) no evidence of a history of alcohol and other drugs abuse. The inclusion criteria for the control group were: i) a score on the MMSE equal to or above 24; ii) no history of self-reported neurological or psychiatric disease, of alcohol and/or other drug abuse.

The study, including the validation of the SDS-Greek (the see S1 Appendix. Validation study of the SDS-Greek), was approved by the University of Sheffield Ethics Committee, and informed written consent was obtained from all the participants. Patients included in the study were selected together with the clinician on the basis of being able to understand the requirements of the study. Thus, they were judged competent to provide informed consent. Almost all patients (42) were under medication (combinations of levodopa, inhibitors of dopamine catabolism and dopamine receptor agonists) at the time of the study. The levodopa equivalent daily dose (LEDD) was calculated using the formula proposed by [53].

Measurements and procedure

Self-report measures

The Hospital Anxiety and Depression Scale–HADS- [5455] was employed to measure depressive and anxious symptomatology, which has been consistently correlated with self-disgust scores [3738]. The HADS includes 14 items, with a scale ranging from 0 (not at all) to 3 (most of the time). The maximum score in the anxiety and depression sub-scales is 21.

The Questionnaire for Impulsive-Compulsive Disorders in Parkinson’s—Disease Rating Scale -QUIP-RS- [44] uses a 5-point scale, from 0 to 4, to measure frequency of compulsive thoughts and impulsive behaviours in connection with the targeted category (gambling, sex, buying, hobbyism and punding). The total combined score for QUIP-RS ranges from 0 to 112. The scale was translated and back-translated by two bilingual Greek-English neuropsychologists for the purpose of this study.

The Barratt Impulsiveness Scale -BIS-11- [5657] was employed to measure behavioral and trait of impulsiveness. The tool consists of 30 items, and the participant is required to answer each item on a 4-point scale from 1(Rarely/Never) to 4 (Almost Always/Always). The overall scale consists of 3 subscales; Motor Impulsiveness, Attentional Impulsiveness, and Non-planning Impulsiveness.

The Self-Conscious Affect questionnaire–TOSCA- [5859] was employed to measure shame and guilt. The scale consists of 16 scenarios, and participants self-report their potential reactions using a 5-point scale. TOSCA-3 includes six subscales, shame-proneness, guilt-proneness, externalization, detachment/unconcern, A-pride and B-pride. In this study we analysed only the shame and guilt subscales.

The Self-Disgust Scale (SDS) was developed by [37] to measure disgust directed towards the Self. This scale has not been used before in the Greek population, so we developed a Greek version of the scale (SDS-Greek, or SDS-G) and conducted a validation study (see S1 Appendix. Validation study of the SDS-Greek).

Emotion induction experiments

To our knowledge, there are no previous studies concerning the experimental induction of self-disgust, since self-disgust is a relatively new construct. Thus, we designed two experiments to induce disgust (and other emotions) toward the self.

Narration-induction experiment. This experiment was based on the paradigm to induce self-conscious emotions developed by Dickerson and colleagues [60], in which participants were asked to write down an experience that made them feel a certain way. Participants sat comfortably in a chair, and were instructed to narrate orally instead of writing (on the assumption that the PD patients would find oral narration less taxing) experiences that made them feel ashamed, guilty or self-disgusted. Also they were asked to narrate a neutral experience, something they did the day before. There was no time limit and narrations were recorded using Audacity software.

The guidelines for the narrations’ induction paradigm were similar to those of Dickerson et al. [60]. However, in Dickerson et al. [60] participants were asked to write about one traumatic and upsetting experience that made the individual feel bad about him/her-self or blame his/her-self, whereas in our study, participants narrated three separate traumatic and upsetting experiences in which they felt self-disgust, shame and guilt. Specifically the instructions for self-disgust were as follow ‘I want you to narrate one of the most traumatic and upsetting experiences of your life; please focus on an experience that you felt disgust towards the self. It could be an experience which made you feel negatively about yourself or a past experience when you did not like yourself. The important thing is that you tell about your deepest thoughts and feelings. Ideally, whatever you speak about should deal with an event or experience that you have not talked with others about in detail’. The same instructions were given for guilt and shame but changing the wording so that participants were encouraged to narrate an incident which made them feel guilty and ashamed, respectively. The instructions for the neutral condition were again similar to those employed in Dickerson et al. [60], ‘I want you to tell about what you did during the past 24 hours. You should describe your activities and schedule in detail, discussing the facts and circumstances as objectively as possible. You might describe what you had for dinner last night, what time you got up this morning, and so forth. The important thing is you discuss the facts and try to remain objective about your activities’.

After each narration, participants were asked to self-report how they felt using a Visual Analogue Scale (VAS) from 0 (Not at all) to 100 (Extremely). Specifically, they were asked to self-rate the target emotion in the narration (self-disgust, shame or guilt), other non-target emotions (anger, sadness and happiness), and level of arousal (from 0 -I feel completely calm- to 100 -I feel completely excited-).

Photo-induction of self-disgust. Participants were presented either with a full body picture of themselves or with a neutral picture. On arrival at the experimental setting, and after obtaining informed consent, the participants were asked to sit and pose with a neutral posture while the researcher took a photograph. In the paradigm, this was contrasted with a neutral photo selected from the International Affective Picture System, which had neutral scores in pleasantness and arousal, depicting hanging clothes (n.7217). Each photo was presented for 3 s, and the order of the photos was counterbalanced across participants. Participants were asked to view the photos passively, and were instructed as follows, “You will be presented with two consecutive photos. Please look at each photo carefully. After each photo you will be asked to rate how you feel”.

After each photo, participants were asked to self-report the target emotion (self-disgust), other non-target emotions (anger and sadness), and arousal levels using Visual Analogue Scales (VASs).

Procedure

Data collection lasted three hours approximately, and took place into two sessions. The first session included demographic data and the medical history of the participant, and all the self-report measures. The second session consisted of the emotion induction experiments. Testing took place in a quiet room in the health centers, the Senior Day Care centers, or at the University of Sheffield International Faculty. The picture-induction and the narration-induction procedures took place in a counterbalanced order across participants, and with a break in between.

Statistical analysis

Statistical analyses were carried out using IBM SPSS Statistics (Version 24). Comparisons between participants with and without PD on self-report measures and VAS measures of self-conscious emotions were carried out using Multivariate Analyses of Variance/Analyses of Variance. We further include as co-variate in the analyses those key confound variable that differed significantly between the groups. Pearson’s correlations were undertaken to investigate the relationship between demographic, clinical, psychological predictor variables and self-conscious emotion outcome variables. Regression analyses were conducted to investigate the relationship between predictor variables and the SDS-G outcome measure. Given the high number of correlations between the variables, only those that were significant at p < .01 were entered into the regression analyses [61]. The assumptions for linear regression analyses were examined and found satisfactory. In particular, standardized residual scatterplots followed the normal distribution with no obvious outliers. Therefore, analyses proceeded as planned.

Results and discussion

Five patients declined to participate in the emotion induction experiments. Consequently, 40 PD patients and 40 matched HC were included in the VAS analyses. From these 80 participants; five (3 HC and 2 PD) could not recall an experience were they felt disgust towards the self, eight (4 HC and 4 PD) could not recall an experience were they felt ashamed, and three patients could not recall an experience were they felt guilty. Thus, data from 80, 75, 72 and 77 participants were included in the Photo, Self-disgust narration, Shame narration and Guilt narration analyses, respectively. As shown in Table 1, PD patients and HC did not differ significantly on any of the demographic variables (age, gender and education). However, PD patients had significantly higher scores in anxiety and depression than HC participants.

Analysis of self-reported self-conscious emotions

The mean scores for the self-conscious emotion self-report questionnaires were submitted to a one-way MANOVA with group (PD and healthy control, HC) as the between subject factor and scores from the SDS-G, and the subscales of Shame and Guilt (TOSCA) as dependent variables. According to Pillai’s Trace there was a significant main effect of group on self-conscious emotions, [V = .164, F(3, 85) = 5.568, p = .002, ηp2 = .164]. Univariate analyses showed that the PD (MeanSDS = 31.36 and MeanShame = 47.55) group had significantly higher scores than the group of HC (MeanSDS = 23.04 and MeanShame = 42.69) on Self-disgust and Shame, F(1, 87) = 5.568,p = .001,ηp2 = .117] and [F(1, 87) = 4.079, p = .047, ηp2 = .645], respectively. There were no significant differences between the groups (MeanPD = 64.52 and MeanHC = 64.15) on Guilt scores, [F(1, 87) = .039, p = .843, ηp2<.0001].

Since PD patients and HC significantly differed on depression and anxiety scores, and depressive symptoms scores significantly correlated with Self-disgust and Shame scores, and anxiety symptoms with Shame scores, we conducted a further MANCOVA with Group as the between subject factor and depression (HADS-D) scores as a co-variate. According to Pillai’s Trace, the main effect of group on self-conscious emotion did not reach statistical significance, [V = .073, F(3, 84) = 2.198, p = .094]. However, the univariate analyses showed that the main effect of group on Self-disgust scores continued to be significant after including depression symptoms as a co-variate, [F(1, 86) = 4.457, p = .038, ηp2 = .049]. A further MACOVA with anxiety scores as a co-variate (HADS-A), showed a significant main effect of diagnosis on self-conscious emotions according to Pillai’s trace [V = .118, F(3, 84) = 3.74, p = .014, ηp2 = .118]. Univariate analyses showed that the main effect of group on Shame scores was no longer significant, although the main effect of Group on Self-disgust scores remained significant [F(1, 86) = 7.38, p = .008, ηp2 = .079].

VAS analyses for the Photo-induction experiment

The MANOVA (see Table 2) with the VAS scores from the Photo emotion-induction experiment showed a significant main effect of Condition (self-photo vs neutral photo), according to Pillai’s Trace [V = .072, F(4, 75) = 47.61, p <.0001], and a significant Group by Condition interaction, [V = .131, F(4, 75) = 2.82, p = .031]. Further, 2x2 ANOVAs on each VAS emotion showed that for self-disgust, the main effects of Group and Condition, and their interaction were statistically significant, [F(1, 78) = 4.35, p = .040, ηp2 = .053], [F(1, 74) = 74.95, p<.0001, ηp2 = .490], and [F(1, 78) = 3.98, p = .050, ηp2 = 0.049], respectively. PD participants had significantly higher self-disgust VAS scores than HC participants but only in the self-photo condition. For the anger VAS scores, results showed significant main effects of Group, Condition, and their interaction, [F(1, 79) = 5.96, p = .017,ηp2 = .071],[F(1, 78) = 11.65, p = .001, ηp2 = .130], and [F(1, 78) = 8.79, p = .004,ηp2 = .101], respectively. The analysis of the interaction showed that PD participants had significantly higher anger VAS scores than the HC participants but only in the self-photo condition. For the sadness VAS scores, results showed significant main effects of Group and Condition, F(1, 78) = 5.10, p = .027, ηp2 = .061] and [F(1, 79) = 48.24, p < .0001,ηp2 = .382] respectively. That is, PD patients had overall higher sadness VAS scores than HC participants, and scores were also higher for the self-photo condition than for the neutral photo condition. Finally, for the Happiness VAS scores, results showed only a significant main effect of Condition [F(1, 79) = 30.53, p <.0001, ηp2 = .281].

Tab. 2. Mean VAS scores and SD as a function of Group and Condition for the photo emotion induction experiment.
Mean VAS scores and SD as a function of Group and Condition for the photo emotion induction experiment.

VAS analyses of the Narration-induction experiment

The 3 separate MANOVAs with VAS scores from the narration emotion induction experiment showed the following results (see Table 3). For the self-disgust narration induction, there were significant main effects of Group and Condition (self-disgust narration vs neutral narration) and their interaction, [V = .180, F(4, 69) = 3.77, p = .008], [V = .862, F(4, 69) = 108.14, p <.0001] and [V = .172, F(4, 69) = 3.59, p = .010], respectively. We then conducted 4 separate 2x2 ANOVAs for each VAS emotion. For the self-disgust VAS scores, results showed significant main effects of Group, Condition, and their interaction, [F(1, 72) = 13.38, p <.0001, ηp2 = .157], [F(1, 72) = 314.36, p <.0001, ηp2 = .814] and [F(1, 72) = 13.66, p <.0001, ηp2 = .160], respectively. The analysis of the interaction showed that PD patients had higher self-disgust VAS scores than HC participants only in the self-disgust narration condition. For the anger VAS scores, results showed significant main effects of Group and Condition, [F(1, 72) = 4.86, p = .031, ηp2 = .063] and [F(1, 72) = 93.79, p <.0001, ηp2 = .566], respectively. That is, PD participants had overall higher anger VAS scores than HC participants, and the anger VAS scores were also higher in the self-disgust narration relative to the neutral narration. For the sadness VAS scores, results showed significant main effects of Group, Condition and their interaction, [F(1, 72) = 5.90, p = .018, ηp2 = .076], [F(1, 72) = 119.63, p <.0001, ηp2 = .624] and [F(1, 72) = 4.97, p = .029, ηp2 = .065], respectively. The analysis of the interaction showed that PD participants had significantly higher sadness VAS scores than HC participants only in the self-disgust narration condition. For the happiness VAS scores, results showed a significant main effect of condition.

Tab. 3. Mean VAS scores and SD as a function of Group and Condition for the Self-disgust narration induction.
Mean VAS scores and SD as a function of Group and Condition for the Self-disgust narration induction.

For the shame narration induction, there was a significant main effect of Condition [V = .846, F(4, 67) = 92.06, p < .001]. That is, overall VAS scores were higher for the shame narration induction condition relative to the neutral narration condition for all the VAS scores: shame, [F(1, 70) = 309.66, p <.0001, ηp2 = .816], anger [F(1, 70) = 79.85, p <.0001, ηp2 = .533], sadness [F(1, 70) = 101.48, p <.0001, ηp2 = .533], and happiness, [F(1, 70) = 87.83, p <.0001, ηp2 = .556]. However, only for shame VAS scores, the Group by Condition interaction was also statistically significant, [F(1, 70) = 5.66, p = .020, ηp2 = .075]. The analysis of the interaction showed that PD patients had higher shame VAS scores than HC but only in the shame narration condition.

For the guilt narration induction, the MANOVA yielded only a significant main effect of Condition [V = .864, F(4, 72) = 114.79, p <.0001]. Overall, VAS scores were higher for the guilt narration condition relative to the neutral condition: guilt, [F(1, 75) = 417.59, p <.0001, ηp2 = .848], anger, [F(1, 75) = 119.11, p <.0001, ηp2 = .614], sadness [F(1, 75) = 138.44, p <.0001, ηp2 = .649], and happiness [F(1, 75) = 106.17, p <.0001, ηp2 = .556]. However, only for the guilt VAS scores, the Group by condition interaction reached also statistical significance, [F(1, 75) = 5.83, p = .018, ηp2 = .072]. The analysis of the interaction showed that PD patients had higher guilt VAS scores than HC participants only in the guilt narration condition.

Since only the depression scores significantly correlated with VAS scores both in the photo and the narration emotion induction experiments, we conducted further 2x2 (4) MANCOVAs with depression scores as a co-variate. In the photo-induction, only the main effect of Condition for the Self-disgust VAS scores and the Happiness VAS remained significant after adjusting for the effect of depression, [F(1, 77) = 3.89, p = .05, ηp2 = .048] and [F(1, 77) = 12.68, p = .001, ηp2 = .141]. In the narration induction, for the Shame narration induction, and the Guilt narration induction analyses, only the main effect of Condition remained statistically significant after controlling for depression scores. However, in the Self-disgust narration induction, the group by condition interaction remained significant for the Self-disgust VAS scores after adjusting for the effect of depression, [F(1, 71) = 5.275, p = .025, ηp2 = .069]. That is, PD participants (adjusted Mean = 64.88) had significantly higher Self-disgust VAS scores than HC participants (adjusted Mean = 47.41) in the Self-disgust narration condition; whereas there were no differences between the groups in the neutral narration condition (adjusted MeanPD = 2.88 and adjusted MeanHC = 1.17).

Regression analyses in the PD group

In the PD group (see Table 4), SDS-G scores had significant positive correlations with LEDD [r = .448, N = 45, p = .002], BIS-Attentional [r = .420, N = 45, p = .004], BIS-Motor [r = .440, N = 45, p = .002] and QUIP-RS scores [r = .624, N = 45, p = .0001], and significant negative correlations with age [r = -.306, p = .041], TOSCA-Guilt [r = -.324, N = 45, p = .007], and TOSCA-Shame [r = -.304, N = 45, p = .045]. TOSCA-Shame scores also had a significant positive correlation with TOSCA-Guilt [r = .567, N = 45, p <.001], and a negative correlation with BIS-Attentional [r = -.305, p = .044], while TOSCA-Guilt was also positively correlated with MMSE scores [r = .401, N = 45, p = .007].

Tab. 4. Correlations between demographic, clinical, psychological predictor variables and self-conscious emotion outcome variables in the group of PD patients.
Correlations between demographic, clinical, psychological predictor variables and self-conscious emotion outcome variables in the group of PD patients.

In order to test the hypothesis that symptoms associated with PD may account for (predict) the self-disgust observed in this group, we introduced the significant correlations (p < .01) between SDS-G scores and LEDD, BIS-Attentional, BIS-Motor, and QUIP-RS into a regression model. Scores from the SDS-G were entered as the outcome variable, with higher scores representing higher levels of self-disgust. The regression analysis resulted in a statistically significant model that explained AR2 = 38% (R2 = .433, p <.0001) of the variance in Self-disgust scores, with QUIP-RS being the only statistically significant independent predictor (β = .552, p = .021).

Impairments in emotion recognition and emotional expression in relation to the basic emotions are widely reported in PD [8,22], although experience of the basic emotions seems to be relatively unimpaired [26]. However, the picture is rather different for self-conscious emotions, where PD patients report increased levels of shame [29] and embarrassment [31]. Here, we sought to investigate for the first time in PD another negative self-conscious emotion–self-disgust–a self-conscious emotion that has been previously demonstrated to play a causative role in depression [62]. In the present study we assessed self-reported levels of self-disgust in a group of medicated PD patients (relative to matched controls), and evaluated the possibility of inducing self-disgust in PD patients in an experimental context. The main findings were that self-disgust levels were higher in PD patients than in controls, even when controlling for the effect of depressive and anxiety symptoms, and that self-disgust levels were significantly and selectively predicted by ICDs as measured by the QUIP-RS. In addition, self-disgust was more readily induced in PD patients than in controls.

Levels of shame were also higher in PD patients, consistent with the existing literature [2930]. Although, after controlling for depression and anxiety symptoms, levels of shame were no longer found to be higher in the PD group. In the PD group, self-disgust was found to correlate with two aspects of BIS, namely BIS-Attentional Impulsiveness and BIS-Motor Impulsiveness. Increased impulsivity in PD is well recognized. Parkinson’s disease patients exhibit impaired decision making, as well as greater risk taking [63]. In relation to motor impulsivity, PD patients make significantly more impulsive motor errors [64], and have impaired stop-signal inhibition [65]. However, in relation to self-disgust, rather than self-reported trait impulsivity (as measured by BIS), behavioural/clinical symptoms of impulsivity (as measured by the QUIP-RS) were the only significant predictor.

Clinically diagnosed ICDs have a prevalence rate of around 14% in PD [6667], which rises to 59% when undiagnosed ICDs are also accounted for via the QUIP-RS [68]. Specifically, ICDs are behavioral disturbances characterized by impulsivity, in which patients are unable to control their impulses to act out in ways that compromise social rules [69]. Impulse Control Disorders identified in PD involve a variety of behaviors such as compulsive gambling, shopping, excessive hobbyism, compulsive sexual behavior and binge-eating [68,70]. These disturbances can cause serious problems in patients’ lives [71]. Although, (perhaps not surprisingly given the proposed causal role of dopamine replacement therapies in ICDs in PD [67]) medication (l-DOPA equivalent dose) was correlated with QUIP-RS scores in the present study, its role as an independent predictor of self-disgust was not significant alongside QUIP-RS scores themselves.

Since the predictive relationship between QUIP-RS scores and self-disgust in the present study was based on cross-sectional data, the directionality of the relationship cannot be inferred from the data alone. However, theory would most likely suggest that ICDs (at some level) cause self-disgust rather than the other way round. Self-conscious emotions include the ability to evaluate the self in comparison to others [72], and so they require evaluation of the self and others [28]. Unlike the six basic emotions, self-conscious emotions rely on more complex functions, which are more cognition-dependent. Hence, self-conscious emotions arise in the context of social networks [73], where the sense of the self is depicted in relation to others and with respect to the social norms [74]. As a consequence, being impelled to behave in certain ways by the compulsions that underlie ICDs could be seen as likely to lead to the violation of social norms and thus to provide disgust-related evidence pertaining to the self that gets added to an evolving self-disgust schema [38], leading to heightened levels of trait self-disgust in PD patients. The converse, where self-disgust leads to ICDs, is much more difficult to defend conceptually, especially given that self-disgust tends to lead to social avoidance [38].

In addition to trait self-disgust in PD patients, we also investigated to what extent state self-disgust might be inducible in PD patients (as has been shown for shame and embarrassment–see Introduction)–i.e. how malleable state self-disgust was, a question we approached with two experimental emotion induction paradigms. The findings agree with those of self-reported trait levels of SD. That is, PD patients reported higher levels of state self-disgust than healthy controls in experimental conditions where we used an emotional elicitor (self-photo or instruction to narrate an emotional experience), but no differences when the elicitor was neutral. Since we used different scales to measure trait and state self-conscious emotions, we cannot directly compare the results to conclude on the typically reported intensity or impact bias (whether trait or state levels are higher) [75]. Previous studies have supported a discrepancy between the mean-level self-reported trait and state scores on emotion, which has been explained in terms of differential cognitive processes and contextual information contributing to the corresponding assessment method [7576]. Despite the potential differences between our assessment methods, evidence from both methods in the current study converges to increased self-disgust in PD patients.

The use of visual or auditory stimuli such as film and pictures to elicit basic emotions is widespread in the literature [7779], but to our knowledge our study is the first to use a visual stimulus—a self-photo—to elicit self-disgust. Our study shows that this paradigm, and a paradigm using the reproduction of past emotional experiences (previously used to induce shame in a healthy population) [60] are effective at eliciting self-disgust in PD patients and healthy controls. In both paradigms, participants also reported overall higher levels of non-target negative emotions (anger and sadness) in the experimental condition relative to the neutral condition. This is not an unexpected result, since research has shown that negative emotions tend to co-exist [80], specifically it has been shown that self-disgust and sadness are closely related [62,81]. In addition, the intensity of the state emotion reported using VAS in the self-photo and the self-disgust narration conditions were significantly correlated (r = .349, N = 75, p = .002), which supports the conclusion of both paradigms being effective in eliciting the target emotion.

While the current report represents a useful addition to understanding self-conscious emotions in PD, there are limitations worth noting. The first limitation is that the present research relies entirely on self-report measures. However, self-report measures have been extensively used in research on disgust as they are inexpensive, easy to administer (in comparison to physiological and neurological measures), and are particularly useful in studies (such as this) that are concerned with the simultaneous assessment of multiple emotional states [82]. Furthermore, emotions were measured in two different ways, with questionnaires and VASs, both of which produced conclusions that pointed in the same direction.

The second limitation is that the Greek version of the SDS was validated in a young population rather than older participants (to age match the participants in the main study). This was to allow us to compare the findings to the original English validation. However, scores on the SDS-G (see S1 Appendix. Validation study of the SDS-Greek), did not differ markedly between the validation sample and the older HC group (MeanValidation = 28.0, SD 10.7, and MeanHC = M 23.0, SD 9.1). The small difference agrees with the general finding that self-disgust levels tend to decrease a little with age (see the negative correlation in Table 4).

Another limitation is that although we excluded participants with a potential diagnosis of dementia (based on MMSE cut off scores), we cannot rule out that some of our participants may have fulfilled the criteria for the more recent clinical construct of Mild Cognitive Impairment [83]. Mild Cognitive Impairment is an intermediate stage between healthy aging and dementia, which is predominantly characterized by memory impairments [83], and consequently it might have affected the experiencing and expression of emotions in our participants. However, both PD and HC would have been equally affected, and research suggests that self-reported affect, and memory for emotional scenes are relatively intact in MCI [8485]. In terms of medical status though, one thing that would have selectively affected the PD group is that the majority of the patients were under medication at the period of testing, and thus we cannot exclude the possibility that the observed results may be due to medication. However, it is important to point out that although LEDD did indeed significantly correlate with self-disgust scores, it was not an independent predictor in the regression model. Thus, the regression model suggests that impulsive behavior was the main factor accounting for the variance in self-disgust scores. Future studies may though seek to replicate the study in patients off medication.

A final limitation is that that the study had a cross-sectional design. However, longitudinal studies are very difficult to conduct and interpret in people with PD, who have a chronic progressive illness. Furthermore, we have found the attrition rate (particularly with negatively-valenced studies like our own) to be high in such groups.

Conclusions

This is the first study to investigate self-disgust in PD patients. We found that PD patients exhibited higher levels of self-reported, and experimentally induced, self-disgust relative to matched control participants. Additionally, trait self-disgust levels were significantly and selectively predicted by disorders of impulse control in the group of patients. The high levels of self-disgust in PD may represent a useful therapeutic target for psychological interventions. Recently, Acceptance and Commitment Therapy (ACT) has been proposed as a useful approach for psychological distress in chronic illness [86]. Our findings here which stress the importance of emotional factors in PD adds further weight to this suggestion, given ACT’s focus on emotional acceptance. Indeed, ACT has already been found to be effective in treating wearing off anxiety in PD [87].

Supporting information

S1 Appendix [docx]
Validation study of the SDS-Greek.


Zdroje

1. Stern MB. The clinical characteristics of Parkinson’s disease and parkinsonian syndromes: diagnosis and assessment. In: Stern MB, Hurtig HI, editors. The comprehensive management of Parkinson’s disease. New York: PMA Publishing Company; 1988. pp. 3–50.

2. Gelb DJ, Oliver E, Gilman S. Diagnostic criteria for Parkinson disease. Arch Neurol. 1999; 56(1): 33–39. doi: 10.1001/archneur.56.1.33 9923759

3. Gallagher DA, Lees AJ, Schrag A. What are the most important nonmotor symptoms in patients with Parkinson’s disease and are we missing them? Mov Disord. 2010;25(15): 2493–2500. doi: 10.1002/mds.23394 20922807

4. Gray HM, Tickle-Degnen L. A meta-analysis of performance on emotion recognition tasks in Parkinson’s disease. Neuropsychol. 2010;24(2): 176–91.

5. Péron J, Dondaine T, Le Jeune F, Grandjean D, Vérin M. Emotional processing in Parkinson’s disease: a systematic review. Mov Disord. 2012; 27(2): 186–199. doi: 10.1002/mds.24025 22162004

6. Sotgiu I, Rusconi ML. Investigating emotions in Parkinson’s disease: what we know and what we still don’t know. Front Psychol. 2013;4: 336. doi: 10.3389/fpsyg.2013.00336 23772218

7. Alexander GE, De Long MR, Strick PL. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci. 1986;9(1): 357–381.

8. Kan Y, Kawamura M, Hasegawa Y, Mochizuki S, Nakamura K. Recognition of emotion from facial, prosodic and written verbal stimuli in Parkinson’s disease. Cortex. 2002;38(4): 623–630. doi: 10.1016/s0010-9452(08)70026-1 12465672

9. Yip J, Lee T, Ho S, Tsang K, Li L. Emotion recognition in patients with idiopathic Parkinson’s disease. Mov Disord. 2003;18(10): 1115–1122. doi: 10.1002/mds.10497 14534914

10. Schröder C, Möbes J, Schütze M, Szymanowski F, Nager W, Bangert M, et al. Perception of emotional speech in Parkinson’s disease. Mov Disord. 2006;21(10):1774–1778. doi: 10.1002/mds.21038 16830324

11. Dujardin K, Blairy S, Defebvre L, Duhem S, Noël Y, Hess U, et al. Deficits in decoding emotional facial expressions in Parkinson’s disease. Neuropsychologia. 2004;42(2):239–250. doi: 10.1016/s0028-3932(03)00154-4 14644109

12. Suzuki A, Hoshino T, Shigemasu K, Kawamura M. Disgust-specific impairment of facial expression recognition in Parkinson’s disease. Brain. 2006;129(3):707–717.

13. Lawrence AD, Goerendt IK, Brooks DJ. Impaired recognition of facial expressions of anger in Parkinson’s disease patients acutely withdrawn from dopamine replacement therapy. Neuropsychologia. 2007;45(1):65–74. doi: 10.1016/j.neuropsychologia.2006.04.016 16780901

14. Clark US, Neargarder S, Cronin-Golomb A. Specific impairments in the recognition of emotional facial expressions in Parkinson’s disease. Neuropsychologia. 2008;46(9): 2300–2309. doi: 10.1016/j.neuropsychologia.2008.03.014 18485422

15. Sprengelmeyer R, Young AW, Mahn K, Schroeder U, Woitalla D, Büttner T, et al. Facial expression recognition in people with medicated and unmedicated Parkinson’s disease. Neuropsychologia. 2003;41(8): 1047–1057. doi: 10.1016/s0028-3932(02)00295-6 12667540

16. Blonder LX, Gur RE, Gur RC. The effects of right and left parkinsonism on prosody. Brain Lang. 1989;36(2):193–207. doi: 10.1016/0093-934x(89)90061-8 2920285

17. Borod JC, Welkowitz J, Alpert M, Brozgold AZ, Martin C, Peselow E, et al. Parameters of emotional processing in neuropsychiatric disorders: conceptual issues and a battery of tests. J Commun Disord. 1990;23(4–5): 247–271. 2246382

18. Caekebeke JF, Jennekens-Schinkel A, van der Linden ME, Buruma OJ, Roos RA. The interpretation of dysprosody in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry. 1991;54(2): 145–148. doi: 10.1136/jnnp.54.2.145 2019840

19. Möbes J, Joppich G, Stiebritz F, Dengler R, Schröder C. Emotional speech in Parkinson’s disease. Mov Disord. 2008;23(6): 824–829. doi: 10.1002/mds.21940 18307245

20. Madeley P, Ellis AW, Mindham RHS. Facial expression and Parkinson’s disease. Behav Neurol. 1995;8(2): 115–119. doi: 10.3233/BEN-1995-8207 24487429

21. Jacobs DH, Shuren J, Bowers D, Heilman KM. Emotional facial imagery, perception and expression in Parkinson’s disease. Neurology. 1995;45(9): 1696–1702. doi: 10.1212/wnl.45.9.1696 7675229

22. Simons G, Ellgring H, Pasqualini MCS. Disturbance of spontaneous and posed facial expressions in Parkinson’s disease. Cogn Emot. 2003;17(5): 759–778.

23. Simons G, Pasqualini MC, Reddy V, Wood J. Emotional and non emotional facial expressions in people with Parkinson’s disease. J Int Neuropsychol Soc. 2004;10(4): 521–555. doi: 10.1017/S135561770410413X 15327731

24. Bowers D, Miller K, Bosch W, Gokcay D, Pedraza O, Springer U, et al. Faces of emotion in Parkinsons disease: micro-expressivity and bradykinesia during voluntary facial expressions. J Int Neuropsychol Soc. 2006;12(6): 765–773. doi: 10.1017/S135561770606111X 17064440

25. Miller KM, Okun MS, Marsiske M, Fennell EB, Bowers D. Startle reflex hyporeactivity in Parkinson’s disease: an emotion-specific or arousal-modulated deficit? Neuropsychologia. 2009;47(8): 1917–1927.

26. Smith MC, Smith MK, Ellgring H. Spontaneous and posed facial expression in Parkinson’s disease. J Int Neuropsychol Soc. 1996;2(5): 383–391. 9375163

27. Wieser MJ, Mühlberger A, Alpers GW, Macht M, Ellgring H, Pauli P. Emotion processing in Parkinson’s disease: dissociation between early neuronal processing and explicit ratings. Clin Neurophysiol. 2006;117(1): 94–102. doi: 10.1016/j.clinph.2005.09.009 16330254

28. Tracy JL, Robins RW. Putting the self into self-conscious emotions: A theoretical model. Psychol Inq. 2004;15(2): 103–125.

29. Nijhof G. Parkinson’s disease as a problem of shame in public appearance. Sociol Health Illn. 1995;17(2): 193–205.

30. Abudi S, Bar‐Tal Y, Ziv L, Fish M. Parkinson’s disease symptoms—‘patients’ perceptions. J Adv Nurs. 1997;25(1): 54–59. doi: 10.1046/j.1365-2648.1997.1997025054.x 9004011

31. Metzer WS. Severe essential tremor compared with Parkinson’s disease in male veterans: diagnostic characteristics, treatment, and psychosocial compli-cations. Southern Med J. 1992;85(8): 825–828. doi: 10.1097/00007611-199208000-00008 1502624

32. Khlebtovsky A, Rigbi A, Melamed E, Ziv I, Steiner I, Gad A, et al. Patient and caregiver perceptions of the social impact of advanced Parkinson’s disease and dyskinesias. J Neural Transm. 2012;119(11): 1367–1371. doi: 10.1007/s00702-012-0796-9 22437202

33. Spurgeon L, Clarke CE, Sackley C. Subjective experiences of speech and language therapy in patients with Parkinson’s disease: a pilot study. Rehabil Res Pract. 2015;839–895.

34. Balash Y, Korczyn AD, Knaani J, Migirov AA, Gurevich T. Quality‐of‐life perception by Parkinson’s disease patients and caregivers. Acta Neurol Scand. 2017;136(2): 151–154. doi: 10.1111/ane.12726 28083960

35. Schalling E, Johansson K, Hartelius L. Speech and communication changes reported by people with Parkinson’s disease. Folia Phoniatr Logop. 2017;69(3): 131–141. doi: 10.1159/000479927 29346787

36. Powell PA, Simpson J, Overton PG. Self-affirming trait kindness regulates disgust toward one’s physical appearance. Body Image. 2015;12:98–107. doi: 10.1016/j.bodyim.2014.10.006 25462888

37. Overton PG, Markland FE, Taggart HS, Bagshaw GL, Simpson J. Self-disgust mediates the relationship between dysfunctional cognitions and depressive symptomatology. Emotion. 2008;8(3): 379–385. doi: 10.1037/1528-3542.8.3.379 18540753

38. Powell PA, Simpson J, Overton PG.When disgust leads to dysphoria: three-wave longitudinal study assessing the temporal relationship between self-disgust and depressive symptoms. Cogn Emot. 2013;27(5): 900–913. doi: 10.1080/02699931.2013.767223 23410007

39. Azlan HA, Overton PG, Simpson J, Powell PA. Effect of partners’ disgust responses on psychological wellbeing in cancer patients. J Clin Psychol Med Settings. 2017;24(3–4): 355–364. doi: 10.1007/s10880-017-9521-z 29164511

40. Fox JR, Froom K. Eating disorders: A basic emotion perspective. Clin Psychol Psychother. 2009;16(4):328–35. doi: 10.1002/cpp.622 19639651

41. Olatunji BO, Cox R, Kim EH. Self-disgust mediates the associations between shame and symptoms of bulimia and obsessive-compulsive disorder. J Soc Clin Psychol. 2015;34(3): 239–258.

42. Ille R, Schöggl H, Kapfhammer HP, Arendasy M, Sommer M, Schienle A. Self-disgust in mental disorders—symptom-related or disorder-specific? Compr Psychiatry. 2014;55(4): 938–943. doi: 10.1016/j.comppsych.2013.12.020 24480418

43. Schrag A, Quinn N. Dyskinesias and motor fluctuations in Parkinson’s disease: A community-based study. Brain. 2000;123(11): 2297–2305.

44. Weintraub D, Mamikonyan E, Papay K, Shea JA, Xie SX, Siderowf A. Questionnaire for impulsive—compulsive disorders in Parkinson’s Disease–Rating Scale. Mov Disord. 2012;27(2): 242–247. doi: 10.1002/mds.24023 22134954

45. Timmer MHM, van Beek MHCT, Bloem BR, Esselink RAJ. What a neurologist should know about depression in Parkinson’s disease. Pract Neurol. 2017;17(5): 359–368. doi: 10.1136/practneurol-2017-001650 28739866

46. Schienle A, Wabnegger A, Schöngassner F, Leutgeb V. Effects of personal space intrusion in affective contexts: an fMRI investigation with women suffering from borderline personality disorder. Soc Cogn Affect Neurosci. 2015;10(10): 1424–1428. doi: 10.1093/scan/nsv034 25809402

47. Hughes AJ, Daniel SE, Kilford L, Lees AJ. Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry. 1992, 55(3), 181–184. doi: 10.1136/jnnp.55.3.181 1564476

48. Goetz CG, Fahn S, Martinez-Martin P, Poewe W, Sampaio C, Stebbins GT, et al. Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): Process, format, and clinimetric testing plan. Mov Disord. 2007;22(1): 41–47. doi: 10.1002/mds.21198 17115387

49. Goetz CG, Poewe W, Rascol O, Sampaio C, Stebbins GT, Counsell C, et al. Movement Disorder Society Task Force report on the Hoehn and Yahr staging scale: status and recommendations the Movement Disorder Society Task Force on rating scales for Parkinson’s disease. Mov Disord. 2004;19(9): 1020–1028.

50. Hoehn MM, Yahr MD. Parkinsonism: onset, progression and mortality. Neurology. 1967;17(5): 427–442. doi: 10.1212/wnl.17.5.427 6067254

51. Folstein MF, Folstein SE, McHugh PR. Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12(3): 189–98. doi: 10.1016/0022-3956(75)90026-6 1202204

52. Fountoulakis K. N., Tsolaki M., Chantzi H., & Kazis A. (2000). Mini mental state examination (MMSE): a validation study in Greece. Am J Alzheimers Dis Other Demen. 2000, 15(6), 342–345.

53. Bliwise DL, Trotti LM, Wilson AG, Greer SA, Wood‐Siverio C, Juncos JJ, et al. Daytime alertness in Parkinson’s disease: potentially dose‐dependent, divergent effects by drug class. Mov Disord. 2012;27(9): 1118–1124. doi: 10.1002/mds.25082 22753297

54. Zigmond AS, Snaith RP. The hospital anxiety and depression scale. Acta Psychiatr. Scand. 1983;67(6): 361–370. doi: 10.1111/j.1600-0447.1983.tb09716.x 6880820

55. Michopoulos I, Douzenis A, Kalkavoura C, Christodoulou C, Michalopoulou P, Kalemi G, et al. Hospital Anxiety and Depression Scale (HADS): validation in a Greek general hospital sample. Ann Gen Psychiatry. 2008;7(1): 1–5.

56. Patton JH, Stanford MS, Barratt ES. Factor structure of the Barratt Impulsiveness Scale. J. Clin. Psychol. 1995;51(6): 768–774. doi: 10.1002/1097-4679(199511)51:6<768::aid-jclp2270510607>3.0.co;2-1 8778124

57. Giotakos O, Markianos M, Vaidakis N, Christodoulou GN. Aggression, impulsivity, plasma sex hormones, and biogenic amine turnover in a forensic population of rapists. J Sex Marital Ther. 2003;29(3): 215–25. doi: 10.1080/00926230390155113 12851126

58. Tangney JP, Dearing RL, Wagner PE, Gramzow R. The Test of Self-Conscious Affect-3 (TOSCA-3). George Mason University: Fairfax; 2000.

59. Gouva M, Kaltsouda A, Paschou A. Psychometric Evaluation of the Greek version of TOSCA-3 to measure Shame and Guilt. Interscientific Health Care. 2012;4(3): 105–113.

60. Dickerson SS, Kemeny ME, Aziz N, Kim KH, Fahey JL. Immunological effects of induced shame and guilt. Psychosom Med. 2004;66(1): 124–131. doi: 10.1097/01.psy.0000097338.75454.29 14747646

61. Edgar KA, Skinner TC. Illness representations and coping as predictors of emotional well-being in adolescents with type 1 diabetes. J Pediatr Psychol. 2003;28(7): 485–493. doi: 10.1093/jpepsy/jsg039 12968040

62. Powell PA, Overton PG, Simpson J. The revolting self: Perspectives on the psychological, social, and clinical implications of self-directed disgust. London: Karnac books; 2014.

63. Kobayakawa M, Koyama S, Mimura M, Kawamura M. Decision making in Parkinson’s disease: Analysis of behavioral and physiological patterns in the Iowa gambling task. Mov Disord. 2008;23(4): 547–552. doi: 10.1002/mds.21865 18069681

64. Wylie SA, van den Wildenberg W, Ridderinkhof KR, Claassen DO, Wooten GF, Manning CA. Differential susceptibility to motor impulsivity among functional subtypes of Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2012;83(12): 1149–1154. doi: 10.1136/jnnp-2012-303056 22917670

65. Obeso I, Wilkinson L, Casabona E, Bringas ML, Alvarez M, Alvarez L, et al. Deficits in inhibitory control and conflict resolution on cognitive and motor tasks in Parkinson’s disease. Exp Brain Res. 2011;212(3): 371–384. doi: 10.1007/s00221-011-2736-6 21643718

66. Giladi N, Weitzman N, Schreiber S, Shabtai H, Peretz C. New onset heightened interest or drive for gambling, shopping, eating or sexual activity in patients with Parkinson’s disease: The role of dopamine agonist treatment and age at motor symptom onset. J Psychopharmacol. 2007;21(5): 501–506. doi: 10.1177/0269881106073109 17446202

67. Weintraub D, Koester J, Potenza MN, Siderowf AD, Stacy M, Voon V, et al. Impulse control disorders in Parkinson’s disease: a cross-sectional study of 3,090 patients. Arch Neurol. 2010;67(5): 589–595. doi: 10.1001/archneurol.2010.65 20457959

68. Garlovsky JK, Simpson J, Grünewald RA, Overton PG. Impulse control disorders in Parkinson’s disease: Predominant role of psychological determinants. Psychol Health. 2016;31(12): 1391–1414. doi: 10.1080/08870446.2016.1218879 27473645

69. Grant JE, Levine L, Kim D, Potenza MN. Impulse control disorders in adult psychiatric inpatients. Am J Psychiatr. 2005;162(11): 2184–2188. doi: 10.1176/appi.ajp.162.11.2184 16263865

70. Evans AH, Strafella AP, Weintraub D, Stacy M. Impulsive and compulsive behaviors in Parkinson’s disease. Mov Disord. 2009;24(11): 1561–1570. doi: 10.1002/mds.22505 19526584

71. Pontone G, Williams JR, Bassett SS, Marsh L. Clinical features associated with impulse control disorders in Parkinson disease. Neurology. 2006;67(7): 1258–1261. doi: 10.1212/01.wnl.0000238401.76928.45 17030761

72. Sturm VE, Ascher EA, Miller BL, Levenson RW. Diminished self-conscious emotional responding in frontotemporal lobar degeneration patients. Emotion. 2008;8(6): 861–869. doi: 10.1037/a0013765 19102597

73. Parker ST. A social selection model for the evolution and adaptive significance of self-conscious emotions. In: Ferrari M, Sternberg RJ, editors. Self-awareness: Its nature and development. New York: Guilford Press; 1998. pp. 108–34.

74. Keltner D, Anderson C. Saving face for Darwin: The functions and uses of embarrassment. Curr Dir Psychol Sci. 2000;9(6): 187–192.

75. Robinson MD, Clore GL. Belief and feeling: evidence for an accessibility model of emotional self-report. Psychol Bull. 2002;128(6): 934. doi: 10.1037/0033-2909.128.6.934 12405138

76. Bieg M, Goetz T, Lipnevich AA. What students think they feel differs from what they really feel–academic self-concept moderates the discrepancy between students’ trait and state emotional self-reports. PLoS One. 2014;9(3): e92563. doi: 10.1371/journal.pone.0092563 24647760

77. Aftanas LI, Lotova NV, Koshkarov VI, Pokrovskaja VL, Popov SA, Makhnev VP. Non-linear analysis of emotion EEG: calculation of Kolmogorov entropy and the principal Lyapunov exponent. Neurosci Lett. 1997;226(1): 13–16. doi: 10.1016/s0304-3940(97)00232-2 9153630

78. Codispoti M, Ferrari V, Bradley MM. Repetitive picture processing: autonomic and cortical correlates. Brain Res. 2006;1068(1): 213–220. doi: 10.1016/j.brainres.2005.11.009 16403475

79. Lobbestael J, Arntz A, Wiers RW. How to push someone’s buttons: A comparison of four anger-induction methods. Cogn Emot. 2008;22(2): 353–373.

80. Tangney JP, Wagner P, Fletcher C, Gramzow R. Shamed into anger? The relation of shame and guilt to anger and self-reported aggression. J Pers Soc Psychol. 1992;62(4): 669–675. doi: 10.1037//0022-3514.62.4.669 1583590

81. Power MJ, Dalgleish T. Cognition and Emotion: From Order to Disorder (2nded.). East Sussex, England: Psychology Press; 2008.

82. Simpson J, Carter S, Anthony SH, Overton PG. Is disgust a homogeneous emotion? Motiv Emot. 2006;30(1): 31–41.

83. Petersen RC, Smith GE, Waring SC, Ivnik RJ, Tangalos EG, Kokmen E. Mild cognitive impairment: clinical characterization and outcome. Arch Neurol. 1999;56: 303. doi: 10.1001/archneur.56.3.303 10190820

84. Ready RE, Carvalho JO, Green RC, Gavett BE, Stern RA. The structure and validity of self-reported affect in mild cognitive impairment and mild Alzheimer’s disease. Int Psychogeriatr. 2011;23(6):887–98. doi: 10.1017/S104161021100041X 21429280

85. Waring JD, Dimsdale-Zucker HR, Flannery S, Budson AE, Kensinger EA. Effects of mild cognitive impairment on emotional scene memory. Neuropsychologia. 2017;96:240–8. doi: 10.1016/j.neuropsychologia.2017.01.011 28089697

86. Angiola JE, Bowen AM. Quality of life in advanced cancer: An acceptance and commitment therapy view. Couns Psychol. 2013;41(2): 313–335.

87. Ghielen I, van Wegen EE, Rutten S, de Goede CJ, Houniet-de Gier M, Collette E H, et al. Body awareness training in the treatment of wearing-off related anxiety in patients with Parkinson’s disease: Results from a pilot randomized controlled trial. J Psychosom Res. 2017;103: 1–8. doi: 10.1016/j.jpsychores.2017.09.008 29167034


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