اختلالات خاص در تشخیص حالت عاطفی چهره در بیماری پارکینسون

Abstract Studies investigating the ability to recognize emotional facial expressions in non-demented individuals with Parkinson's disease (PD) have yielded equivocal findings. A possible reason for this variability may lie in the confounding of emotion recognition with cognitive task requirements, a confound arising from the lack of a control condition using non-emotional stimuli. The present study examined emotional facial expression recognition abilities in 20 non-demented patients with PD and 23 control participants relative to their performance on a non-emotional landscape categorization test with comparable task requirements. We found that PD participants were normal on the control task but exhibited selective impairments in the recognition of facial emotion, specifically for anger (driven by those with right hemisphere pathology) and surprise (driven by those with left hemisphere pathology), even when controlling for depression level. Male but not female PD participants further displayed specific deficits in the recognition of fearful expressions. We suggest that the neural substrates that may subserve these impairments include the ventral striatum, amygdala, and prefrontal cortices. Finally, we observed that in PD participants, deficiencies in facial emotion recognition correlated with higher levels of interpersonal distress, which calls attention to the significant psychosocial impact that facial emotion recognition impairments may have on individuals with PD.

Introduction One of the most basic elements of emotional functioning, and one of the components most critical to social behavior, is the recognition of the emotional states of others (Darwin, 1872/1965). In Parkinson's disease (PD), facial emotion identification deficits have been reported in several studies (Dujardin et al., 2004; Jacobs, Shuren, Bowers, & Heilman, 1995; Kan, Kawamura, Hasegawa, Mochizuki, & Nakamura, 2002; Lawrence, Goerendt, & Brooks, 2007; Sprengelmeyer et al., 2003), though not in all (Adolphs, Schul, & Tranel, 1998; Pell & Leonard, 2005). Where deficits are found, there is as yet little consensus as to whether or not they apply to the recognition of specific emotions. Kan et al. (2002) noted deficits in the recognition of fear and disgust in medicated PD participants. Sprengelmeyer et al. (2003) found that the recognition of anger and fear was disrupted in medicated PD participants, and that the recognition of fear, sadness, disgust, and anger was impaired in unmedicated PD patients. Dujardin et al. (2004) observed that unmedicated PD participants were less accurate than healthy participants in perceiving facial expressions of anger, sadness, and disgust. More recently, Lawrence et al. (2007) reported that the recognition of anger was impaired in PD patients who had been temporarily removed from dopamine replacement therapy. It is generally argued that abnormalities in facial emotion recognition in PD arise from losses of dopaminergic neurons resulting in dysfunction of fronto-subcortical systems (e.g., Dujardin et al., 2004, Lawrence et al., 2007 and Sprengelmeyer et al., 2003). With growing evidence that dissociable neural substrates are involved in the recognition of different emotions (Adolphs, 2002; Posamentier & Abdi, 2003), gaining greater clarity on emotion recognition impairments in PD would help in ascertaining which neural substrates may underlie the disruption of emotion recognition. The inconsistency in the literature may be related to the variability in medication status of PD patients across studies; however, medication status may not explain these inconsistencies entirely. Notably, it has been suggested that the typical methods of investigating emotion recognition, particularly in neurologic patient populations, may result in artifactual findings that are related to task difficulty factors rather than to impairments in emotion recognition abilities arising from disruption of specific neuroanatomical structures (Rapcsak et al., 2000). Inconsistent findings in the PD literature may reflect differences in difficulty levels across emotions within a study. This effect may be compounded by the differences in the difficulty level of stimuli presented (within each category of emotion), which likely vary among studies. A second source of inconsistency may come from the confounding of emotion recognition abilities with unrelated task requirements. Executive function impairments, a hallmark of frontal dysfunction, are commonly noted in non-demented PD patients (e.g., Zgaljardic, Borod, Foldi, & Mattis, 2003). Frontally mediated impairments – mainly in decision-making and categorization abilities – may have an impact on PD patients’ performance on measures of facial emotion recognition. PD patients have shown impairments on tasks of explicit decision making ability (e.g., the Game of Dice task), which correlated with decreases in executive functioning abilities (Brand et al., 2004), and on tests of implicit decision making (e.g., Iowa Gambling Task), in which PET imaging revealed decreased activation in the orbitofrontal cortex (Thiel et al., 2003). Several studies have indicated that the ability to learn categorization rules is impaired in PD (e.g., Ashby, Noble, Filoteo, Waldron, & Ell, 2003; Knowlton, Mangels, & Squire, 1996; Maddox, Aparicio, Marchant, & Ivry, 2005; Maddox & Filoteo, 2001; Price, 2006). Most recently, Filoteo et al. (2007) suggested that the presence of extraneous stimuli features may impair PD patients’ performance on categorization tasks due to increased demands on selective attention processes. Taken together, these findings are highly relevant to studies of emotion identification that require participants to categorize facial expressions. The methods most often used to assess emotion recognition abilities require that the participant call upon several skills known to be disrupted in PD. Without employing a suitable control task to studies of facial emotion perception, it is difficult to ascertain whether PD participants’ poor performance on tasks of emotion recognition is due to an inability to identify emotions, or whether their difficulties arise from deficits in decision making, categorization skills, or the ability to identify the most salient features demarcating category boundaries. Impairments in the recognition of specific emotions may be related to the latter three possibilities, as any could result in increased error rates. To help resolve these issues, the present study examined the facial emotion recognition abilities of PD and healthy normal control participants relative to performance on a non-emotional categorization test with comparable task requirements. Landscapes were chosen because they provided a sufficient number of image categories, and, like faces, they are mono-oriented and are composed of several smaller elements that can be individually assessed and integrated when categorizing the image. A further aim of this study was to examine the relation between emotion recognition and body side of motor onset in PD. Motor symptoms in PD usually have a unilateral onset, and this pattern generally persists throughout the progression of the disease (Lee et al., 1995). There is evidence to suggest that this asymmetry is associated with reduced dopamine levels and abnormalities in the dopamine receptors of the contralateral hemisphere (Innis et al., 1993; Kempster, Gibb, Stern, & Lees, 1989), which persist even after motor symptoms have progressed to a more bilateral presentation (Antonini et al., 1995). Because differences in side of motor onset are associated with dysfunction of hemisphere-specific cognitive abilities in PD (e.g., Amick, Grace, & Chou, 2006; Amick, Schendan, Ganis, & Cronin-Golomb, 2006), in addition to the fact that the right hemisphere is thought to be more active than the left in processing emotional material, we examined the performance of PD participants with right and left motor symptom onset separately. We also examined whether men and women with PD display differences in emotion recognition, as men and women with PD may experience different disease effects (e.g., Haaxma et al., 2007 and Shulman, 2007), and numerous studies have shown male–female differences in emotion recognition abilities (e.g., Hall, Carter, Horgan, & Fischer, 2000; Hall & Matsumoto, 2004; Thayer & Johnsen, 2000). A final aim was to assess whether impairments in emotion recognition, if identified, are associated with increased difficulties in interpersonal relationships. Research in other neuropsychiatric patient populations suggests that abnormalities in facial emotion recognition correlate with declines in interpersonal interactions (Kornreich et al., 2002 and Shimokawa et al., 2001). We hypothesized that similar reductions in social interaction may occur in PD patients. Based on reports that female PD patients, compared to male PD patients, tend to endorse more difficulties on overall quality of life measures, which also address social functioning (Behari, Srivastava, & Pandey, 2005; Kuopio, Marttila, Helenius, Toivonen, & Rinne, 2000; Shulman, 2007), we hypothesized that female PD patients in our group would report more interpersonal difficulties than male PD patients.

Results The analyses that follow consist of mixed design ANOVAs, followed by post hoc analyses when appropriate, and Pearson correlations using a conservative alpha level of .01. For clarity, only those analyses revealing significant effects of interest are reported. 4.1. Facial emotion recognition 4.1.1. Comparisons of group performances on the facial emotion recognition and landscape categorization tasks Our primary aim was to compare the PD and HC groups’ ability to identify facial emotions to their ability to classify non-emotional images of equal difficulty level. We used paired samples t-tests to compare the HC group's accuracy scores on the matched facial and landscape image categories. Accuracy scores on matched categories were comparable, with the exception of accuracy scores for fearful images, which were lower than the accuracy scores for the matched landscape category for this expression (i.e., tropical) (t[22] = −3.23, p < .01) (see Table 2). We determined that town images were a better match for fearful images, as the HC group's accuracy scores did not differ significantly for these categories (t[22] = −.45, p = .66). Table 2. Percent recognition for the matched facial emotion and landscape image categories in 28 independent young observers, and in the healthy control group of the present study (10 images in each category; 70 images total) Emotion YO HC Landscape YO HC M S.D. M S.D. M S.D. M S.D. Anger 86.8 11.8 87.4 14.5 City 89.3 11.5 85.2 11.6 Disgust 65.4 16.6 79.1 15.0 Town 61.8 17.2 76.1 20.4 Fear 78.9 16.4 73.9 a 17.8 Tropical 82.5 6.4 90.0 a 16.2 Happy 99.6 1.1 98.7 3.4 Forest 97.9 1.8 100.0 0.0 Neutral 85.0 13.9 83.9 12.0 Mountain 79.6 14.9 90.4 7.7 Sad 84.6 10.1 80.9 19.3 Canyon 83.9 12.7 84.3 17.0 Surprise 89.6 6.8 90.9 10.0 Shore 81.4 16.8 86.1 11.2 All faces 84.3 15.1 84.97 7.0 All landscapes 82.3 15.9 87.45 4.6 Note: YO = young observers; HC = healthy control group of the present study. Within rows, means with the same alphabet are significantly different at p < .05. Table options Mixed design ANOVAs with factors of group (PD, HC) and stimuli (matched emotion and landscapes categories) were conducted to compare the PD and HC groups’ ability to correctly identify images from each category of facial expression to its matched landscape category. For angry faces and city landscapes, there was a significant interaction between group and stimuli (F[1, 41] = 4.54, p < .05). Post hoc tests indicated that PD participants were less accurate than HC participants at identifying anger (t[41] = −2.68, p < .05). For surprise and shore images, there was a significant group by stimuli interaction (F[1, 41] = 5.25, p < .05). Post hoc tests showed that PD participants were significantly less accurate than HC participants at identifying facial expressions of surprise (t[41] = −3.10, p < .01). The above findings were replicated when group performances on the emotion recognition task alone were analyzed using a more conventional method, by comparing their abilities to recognize emotions across all emotion types (see Fig. 2). Mean (+standard error of the mean) percentage of facial expression images that ... Fig. 2. Mean (+standard error of the mean) percentage of facial expression images that were correctly identified by each group. PD = Parkinson's disease; HC = healthy control. Asterisks indicate that the groups’ means are significantly different at the p < .05 level (*) or p < .01 level (**). Figure options To compare the two groups’ overall accuracy at identifying emotions versus landscapes, we conducted a mixed design ANOVA with factors of group (PD, HC) and stimuli (all emotions combined, all landscapes combined). The analysis showed a significant main effect of group (F[1, 41] = 4.91, p < .05). Post hoc tests revealed a trend for the PD participants to be less accurate than HC at identifying emotional expressions (t[41] = −1.96, p = .057). 4.1.2. Facial emotion recognition and side of motor onset The RPD, LPD, and HC groups’ performance on the emotion recognition task were compared against their performance on the landscape categorization task by performing mixed design ANOVAs followed by post hoc analyses when appropriate (see Fig. 3). Significant findings revealed that compared to the HC group, the LPD group displayed specific impairments in the recognition of both facial emotion (angry: F[2, 40] = 4.26, p < .05; post hoc, p < .05) and landscapes (forest: F[2, 40] = 3.65, p < .05; post hoc, p < .05). Compared to the HC and LPD groups, the RPD group displayed a specific impairment in the recognition of facial emotion only (surprise: F[2, 40] = 10.26, p < .001; post hoc, p < .01, p < .05, respectively). Mean (+standard error of the mean) percentage of matched angry and city images, ... Fig. 3. Mean (+standard error of the mean) percentage of matched angry and city images, and matched surprise and shore images that were correctly identified by each group. RPD = Right body side of motor onset Parkinson's disease; LPD = left body side of motor onset Parkinson's disease; HC = healthy control. Asterisks indicate that the groups’ means are significantly different at the p < .05 level (*) or p < .01 level (**). Figure options 4.1.3. Facial emotion recognition and gender differences We conducted mixed design ANOVAs with factors of group (PD, HC), gender (male, female), and stimuli (matched emotion and landscapes categories). Post hoc analyses conducted on the significant interaction effect between group and gender (F[1, 39] = 15.61, p < .001) revealed that men with PD were significantly less accurate at identifying fearful images than were women with PD (t[18] = −3.22, p < .01) and HC men (t[19] = −3.52, p < .01). By contrast, HC women were less accurate than HC men at identifying fearful expressions (t[21] = 2.22, p < .05) (see Fig. 4). Mean (+standard error of the mean) percentage of fearful facial expressions that ... Fig. 4. Mean (+standard error of the mean) percentage of fearful facial expressions that were correctly identified by each group, split by gender. PD = Parkinson's disease; HC = healthy control. Asterisks indicate that the groups’ means are significantly different at the p < .05 (*) and p < .01 (**) level. Figure options 4.1.4. Associations between facial emotion recognition performance and depression, anxiety, facial perception, prosodic emotion recognition, and demographic variables In the PD group, there was a significant negative correlation between BDI and BAI scores and recognition of sad expressions (r = −.68, p = .001; r = −.73, p < .001, respectively). BDI was also negatively correlated with emotion recognition across all facial expressions combined (r = −.592, p < .01). None of the correlations for BDI and BAI were significant in the HC group (all r's < .35, p's > .10). Two separate mixed design analyses of covariance were performed to examine whether participants’ depression and anxiety scores affected emotion recognition. Although a correlation existed between emotion recognition accuracy and BAI in the PD group, the covariate of BAI was not significant (p = .07). After controlling for depression ratings, the PD group was still less accurate at identifying angry expressions (F[1, 40] = 3.65, p < .05) (one-tailed), and expressions of surprise (F[1, 40] = 8.18, p < .01) (one-tailed). There was no significant correlation between facial emotion recognition ability and any of the following for either the PD or HC group: age, education, acuity, contrast sensitivity, facial recognition ability (Benton Test of Facial Recognition), or performance on the test of emotional prosody; nor additionally for PD in regard to motor symptom severity (Hoehn and Yahr stage) or disease duration (all r's < .33, p's > alpha of .01). 4.2. Prosodic emotion recognition Performance on the emotional prosody recognition test was assessed by conducting a mixed design ANOVA with factors of group (PD, HC) and prosodic emotions (angry, disgust, fear, happy, sad, pleasant surprise). Significant group differences were not observed (main effect of group: F[1, 41] = 1.13, p = .29; group by prosodic emotion interaction: F[5, 205] = .19, p = .97). Results of the ANOVA comparing RPD, LPD, and HC on this measure showed no group differences (main effect of group: F[2, 40] = 1.24, p = .30; group by emotion interaction: F[10, 200] = .99, p = .45). 4.3. Interpersonal problems 4.3.1. Interpersonal problems questionnaire We hypothesized that PD participants would report higher rates of interpersonal difficulties than HC participants and that female PD participants would report higher rates of interpersonal distress than male PD participants. We conducted a mixed design ANOVA with factors of group (PD, HC), gender (male, female), and IIP scale. Results revealed a significant group by scale by gender interaction (F[3.2, 124.4] = 3.22, p < .05). Individual two-way ANOVAs, with group and gender as between subjects factors, identified a significant main effect of group (F[1, 39] = 4.34, p < .05, one-tailed) and significant group by gender interaction (F[1, 39] = 3.2, p < .05, one-tailed) for scale 5 (difficulties with self-assertion) as well as a significant group by gender interaction for scale 6 (over-accommodating behavior; F[1, 39] = 3.34, p < .05, one-tailed). Because men and women are known to report different levels of difficulty on the IIP ( Horowitz et al., 2000), we compared male PD and HC participants separately from female PD and HC participants in post hoc comparisons using independent groups t-tests. On scale 5 we found that, compared to HC, PD participants reported higher rates of distress (t[41] = 2.06, p < .05), which appeared to be driven by women with PD who reported higher rates of distress than HC women (t[20] = 2.47, p < .05). Significant findings revealed that for scale 6, women with PD reported significantly higher rates of distress than did HC women (t[20] = 2.47, p < .05; t[20] = 2.16, p < .05, respectively). Mean group ratings on the IIP scales are presented in Table 3. Table 3. Mean (+standard deviations) group scores on the eight the IIP scales (maximum score = 32) IIP scales PD HC Male PD Male HC Female PD Female HC M S.D. M S.D. M S.D. M S.D. M S.D. M S.D. 1. Controlling 5.3 4.5 4.0 3.7 5.7 5.7 4.1 3.4 4.8 3.0 3.8 4.1 2. Vindictive/angry 3.5 5.1 3.7 4.1 5.4 6.7 3.6 4.1 1.5 1.1 3.8 4.3 3. Distant 4.4 5.1 4.7 5.1 5.8 6.7 5.3 6.5 2.9 2.2 4.3 3.7 4. Socially avoidant 7.3 4.8 6.0 5.6 8.0 5.1 7.2 6.4 6.5 4.6 4.9 4.7 5. Non-assertive 12.4 a 8.6 7.7 a 6.4 9.3 5.1 8.6 7.1 15.4 b 10.4 6.8 b 5.8 6. Exploitable/overly accommodating 10.2 5.4 8.0 6.3 8.5 4.8 9.6 6.7 11.9 c 5.8 6.5 c 5.9 7. Self-sacrificing 10.5 4.2 8.5 6.8 9.3 4.5 9.8 8.2 11.6 3.7 7.3 5.2 8. Needy 5.7 3.5 4.2 3.3 5.7 3.4 3.5 3.3 5.7 3.7 4.8 3.3 Note: PD = Parkinson's disease; HC = healthy control; M = mean, S.D. = standard deviation. Within rows, means with the same alphabet are significantly different at p < .05. Table options 4.3.2. Relation between facial emotion recognition abilities and interpersonal difficulties Correlations were computed to investigate the association between reports of interpersonal problems with facial emotion recognition abilities in the PD and HC groups. In HC, emotion recognition abilities were not significantly correlated with reports of interpersonal problems (p > .05 for all correlations). In PD participants, recognition of fearful faces was negatively correlated with ratings of anger and frustration in social relationships (scale 2, r = −.685, p < .01) and ratings of difficulties with social connectedness (scale 3, r = −.603, p < .01). PD participants’ ability to recognize sad faces was negatively correlated with levels of controlling behaviors (scale 1, r = −.593, p ≤ .01), difficulties related to social connections with others (scale 3, r = −.594, p ≤ .01), and ratings of the desire to engage or connect with others (scale 8, r = −.624, p < .01). PD participants’ ability to recognize emotions in general (i.e., their overall performance on the emotion recognition task across all emotions) was negatively correlated with rates of frustration in interpersonal relationships (scale 2, r = −.579, p < .01) and difficulties related to social connections with others (scale 3, r = −.725, p < .01). In HC men, emotion recognition abilities did not correlate significantly with reports of interpersonal problems. In men with PD, the ability to recognize fearful faces was negatively correlated with rates of discomfort in social situations (scale 4, r = −.801, p < .01). In women with PD, the ability to recognize sad expressions was negatively correlated with ratings of difficulties with social connections (scale 3, r = −.829, p < .01). Recognition of sad expressions was also negatively correlated with ratings of the desire to engage or connect with others (scale 8, r = −.747, p ≤ .01). The ability to recognize emotional faces, across all facial expressions combined, was negatively correlated with rates of frustration in interpersonal relationships (scale 2, r = −.810, p < .01).