This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy Neuropsychologia 50 (2012) 1936–1945 Contents lists available at SciVerse ScienceDirect Neuropsychologia journal homepage: www.elsevier.com/locate/neuropsychologia Hemispheric asymmetries and prosodic emotion recognition deficits in Parkinson’s disease Maria I. Ventura a,b, Kathleen Baynes c,d, Karen A. Sigvardt a,c,e, April M. Unruh a, Sarah S. Acklin b, Heidi E. Kirsch f,g, Elizabeth A. Disbrow a,c,e,g,n a Center for Neuroscience, University of California, Davis, CA, United States Department of Psychology, University of California, Davis, CA, United States c Department of Neurology, University of California, Davis, CA, United States d Center for Mind and Brain, University of California, Davis, CA, United States e VA Northern California Health Care System, Martinez, CA, United States f Department of Neurology, University of California, San Francisco, CA, United States g Department of Radiology and Biomedical Imaging, University of California, San Francisco, United States b a r t i c l e i n f o a b s t r a c t Article history: Received 22 August 2011 Received in revised form 30 March 2012 Accepted 20 April 2012 Available online 1 May 2012 While Parkinson’s disease (PD) has traditionally been described as a movement disorder, there is growing evidence of cognitive and social deficits associated with the disease. However, few studies have looked at multi-modal social cognitive deficits in patients with PD. We studied lateralization of both prosodic and facial emotion recognition (the ability to recognize emotional valence from either tone of voice or from facial expressions) in PD. The Comprehensive Affect Testing System (CATS) is a well-validated test of human emotion processing that has been used to study emotion recognition in several major clinical populations, but never before in PD. We administered an abbreviated version of CATS (CATS-A) to 24 medicated PD participants and 12 age-matched controls. PD participants were divided into two groups, based on side of symptom onset and unilateral motor symptom severity: leftaffected (N¼ 12) or right-affected PD participants (N ¼ 12). CATS-A is a computer-based button press task with eight subtests relevant to prosodic and facial emotion recognition. Left-affected PD participants with inferred predominant right-hemisphere pathology were expected to have difficulty with prosodic emotion recognition since there is evidence that the processing of prosodic information is right-hemisphere dominant. We found that facial emotion recognition was preserved in the PD group, however, left-affected PD participants had specific impairment in prosodic emotion recognition, especially for sadness. Selective deficits in prosodic emotion recognition suggests that (1) hemispheric effects in emotion recognition may contribute to the impairment of emotional communication in a subset of people with PD and (2) the coordination of neural networks needed to decipher temporally complex social cues may be specifically disrupted in PD. & 2012 Elsevier Ltd. All rights reserved. Keywords: Parkinson’s disease Emotion processing Social cognition Prosody lateralization 1. Introduction Social communication and the ability to respond to emotional signals are essential for meaningful interpersonal interactions. While Parkinson’s disease (PD) has traditionally been defined as a movement disorder, there is growing evidence of cognitive and social deficits associated with this disease. Non-motor symptoms, including disruptions in emotional information processing (Dujardin et al., 2004), have been found in over 50% of newly diagnosed PD patients (Janvin, Aarsland, Larsen, & Hugdahl, 2003) and can appear in any n Corresponding author at: Department of Neurology, University of California, Davis, CA, United States. E-mail address: eadisbrow@ucdavis.edu (E.A. Disbrow). 0028-3932/$ - see front matter & 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.neuropsychologia.2012.04.018 stage of disease progression (Park & Stacy, 2009). Interestingly, social cognitive dysfunction has been found before the appearance of motor disturbances in PD (Kawamura & Koyama, 2007). Social cognition critically depends on interpersonal sensitivity, or the ability to perceive accurately and respond appropriately to one’s social environment (Hall & Bernieri, 2001). Interpersonal sensitivity encompasses a wide range of subprocesses, including the perception of others’ emotional signals conveyed in tone of voice and facial expressions, interpretation of these signals, and the generation of an appropriate behavior or response (Adolphs, 2002). People with PD have been perceived as emotionally ‘‘flat’’ (Jaywant & Pell, 2010) and may show other signs of social cognitive dysfunction. There are few studies of multi-modal deficits in emotion processing in PD (i.e., both prosodic and facial emotion recognition). Author's personal copy 1937 M.I. Ventura et al. / Neuropsychologia 50 (2012) 1936–1945 Prosodic emotion recognition refers to the ability to recognize the emotional content in tone of voice (such as happiness, sadness, anger, and disgust). Facial emotion recognition processing is the ability to recognize and identify facial expressions. Existing data on emotion recognition in PD is sparse and contradictory. Some studies have shown that emotional prosody decoding is intact in PD (Mitchell & Boucas, 2009). Clark, Neargarder, & Cronin-Golomb (2008) found that people with PD could perform an emotional prosody recognition task and a non-emotional landscape categorization task; however, facial emotion recognition was impaired. In a follow-up study, Clark et al. (2010) suggested that impaired facial emotion recognition may be due to specific visual scanning disturbances in PD. Others (Ariatti, Benuzzi, & Nichelli, 2008) have also shown that emotion recognition from visual cues is impaired, especially in recognizing sad and fearful faces, leading to the suggestion that PD-related emotion recognition deficits selectively impair negative emotion perception (Dara, Monetta, & Pell, 2008; Peron et al., 2010; Tessitore et al., 2002). For example, it has been shown that both medicated and unmedicated people with PD may be selectively impaired in the recognition of facial expressions of disgust (Assogna et al., 2010; Sprengelmeyer et al., 2003; Suzuki, Hoshino, Shigemasu, & Kawamura, 2006). There is also some evidence that emotion prosody processing is disrupted in other disorders that impact basal ganglia functioning. Individuals with lesions within left basal ganglia may have selective impairments for processing fear and disgust prosody, suggesting dopaminergic involvement in the recognition of these negative emotions (Paulmann, Pell, & Kotz, 2008). However, there is some evidence that emotion recognition in PD is impaired for both positively and negatively valenced prosody (e.g., happy vs. sad; Schroder et al., 2006). Schroder et al. (2010) found diminished event-related potentials to both happy and sad emotional prosody during passive listening, suggesting impaired early preattentive processing for both positive and negative emotions. Thus, more work is needed to clarify the valence effects in both prosodic and facial emotion recognition deficits in PD. Traditional theories of emotional processing suggest righthemisphere specialization for the perception and recognition of social cues (for a review, see Kirsch, 2006). More recently, lateralization of emotion recognition has been debated. Evidence for the underlying cerebral mechanisms and the lateralization of prosodic emotion processing is inconclusive. For example, some studies show that patients with either left- or right hemisphere damage perform poorly in affective-prosodic identification tasks compared to controls (Pell & Baum, 1997; Van Lancker & Sidtis, 1992). Other studies show that language functions, including emotional prosodic processing, are mediated more by the right than the left hemisphere (Mitchell and Crow, 2005; Kotz, Meyer, & Paulmann, 2006; Bach et al., 2009). It has been suggested that facial emotion processing is primarily lateralized to the right hemisphere (for reviews, see Mandal & Ambady, 2004; Meletti et al., 2003). Neuroimaging studies of face perception in normal adults have shown bilateral activation. However, responses were of greater signal intensity in the right hemisphere (Ishai, Schmidt, & Boesiger, 2005; Killgore & Yurgelun-Todd, 2007; Barbeau et al., 2008). Studies have shown impaired facial emotion recognition in right mesial temporal lobe epilepsy patients, especially with facial cues of fear and sadness (Batut et al., 2006; Hlobil, Rathore, Alexander, Sarma, & Radhakrishman, 2008). Thus, although the left hemisphere may play a role in facial emotion recognition, these studies suggest that facial emotion recognition is mediated by a complex distributed cortical network with right hemisphere dominance. The impact of deficits in interpersonal sensitivity in people with PD is far reaching. Social relationships are fundamentally important to people’s health and well-being (Cacioppo et al., 2007). Having the ability to read others’ emotions and to react appropriately is an important component of interpersonal relationships. Disrupting these relationships can lead to frustration and feelings of social disconnection (Clark et al., 2008), and deficits in social cognition can have adverse effects on the quality of life for those diagnosed with PD (Gray & Tickle-Degnen, 2010). Here we used the Comprehensive Affect Testing System (CATS; Froming, Levy, Schaffer & Ekman, 2006), a psychometrically-validated test of human emotion processing that incorporates both prosodic and facial emotion recognition and has been used to study emotion recognition in several major clinical populations, but never before in PD. Our goals were to test the hypotheses that (1) these deficits may exhibit hemispheric asymmetry, (2) people with PD may have multi-modal deficits in emotion recognition, and (3) these deficits may impact quality of life. 2. Materials and methods 2.1. Participants Twenty-four right-handed individuals (13F, 11M) with Parkinson’s disease and twelve healthy, right-handed, education and age-matched controls (6F, 6M) participated in this study (Table 1). All PD participants were on dopamine replacement therapy, and were recruited from the University of California, Davis Medical Center movement disorders clinic and PD support groups. Participants of either sex between the ages of 50 and 80 with confirmed idiopathic PD and who responded to anti-Parkinsonian medication were included in the study group. 2.2. General inclusion and exclusion criteria Participants who were fluent in English and had normal or corrected to normal vision and normal hearing capabilities were included in this study. Participants with a history of stroke, significant head trauma, brain surgery, significant vision impairment, atypical PD (i.e., age of onset o50), depression severity (Geriatric Depression Scale score 410), and global cognitive deterioration (Mini Mental State Exam score o 25) were excluded from this study. The study was performed with the approval of the University of California, Davis Committee for Human Research and all participants provided written consent. 2.3. Experimental design and procedure The abbreviated Comprehensive Affect Testing System (CATS-A) is a computer-based task with eight subtests (Schaffer, Wisniewski, Dahdah, & Froming, 2009). CATS-A behavioral assessments were completed while participants were seated comfortably in a quiet testing environment with an IBM ThinkPad laptop positioned approximately 70 cm away from their face. Auditory stimuli were presented at 60 dB A-weighted sound pressure level. Facial stimuli were 4 cm by 2.5 cm and were of uniform size across all conditions. Table 1 Summary of demographic, clinical, and cognitive data. Average scores (Standard deviation) are reported: H & Y: Hoehn & Yahr; MMSE: mini-mental state exam [range of scores]; GDS: Geriatric depression scale. Left-affected PD participants Right-affected PD participants Age-matched controls a N Age (SD) Sex Years of education H&Y MMSE [range] GDS 12 12 12 71a (4.7) 66 (4.2) 64.2 (5.5) 4M, 8F 6M, 6F 6M, 6F 15.9 (3.6) 16.3 (1.4) 16.1 (3.4) 2 2 – 28 [25–30] 29 [25–30] 28 [25–30] 3.8 (3) 3.8 (4) 1.5 (1) Left-affected PD participants were significantly older (p o.05). Author's personal copy 1938 M.I. Ventura et al. / Neuropsychologia 50 (2012) 1936–1945 Participants were required to use their dominant hand, and all were righthanded. To perform the task, subjects used the mouse to select and click on the appropriate button at the bottom of the computer screen, clearly marked with a text label. Before test administration, all participants performed 3 practice trials of prosodic discrimination and 3 of facial discrimination. Participants could repeat stimuli no more than once before being required to give their response. All participants completed subtests 1–8 in order in approximately 45 min.   Subtest 1 (Non-emotional Prosody Discrimination): participants heard two        serially presented sentences spoken in non-emotional tones, either declarative or interrogatory, and determined if the sentences sounded the same or different. Participants selected one of two response buttons labeled ‘‘Same’’ or ‘‘Different.’’ Subtest 2 (Emotional Prosody Discrimination): participants heard two serially presented sentences spoken in emotional tones (happy, sad, angry, frightened or neutral) and determined if the sentences conveyed the same or different emotion. Participants selected one of two response buttons labeled ‘‘Same’’ or ‘‘Different.’’ Subtest 3 (Name Emotional Prosody): participants heard one sentence and identified the emotion conveyed in the tone (happy, sad, angry, frightened or neutral). Participants selected one of five response buttons. Subtest 4 (Identity Discrimination): participants saw simultaneously presented black and white photos of two faces (Ekman & Friesen, 1976) matched for emotional expression and determined if the photos they saw were the same or different person. Participants selected one of two response buttons. Subtest 5 (Affect Discrimination): participants saw simultaneously presented black and white photos of two faces expressing emotions (happy, sad, angry, frightened or neutral) and determined if the faces they saw were expressing the same or different emotion. Participants selected one of two response buttons. Subtest 6 (Name Affect): participants saw one photo and were asked to identify the facial emotion expressed by the person in the picture (happy, sad, angry, frightened, surprised, disgusted or neutral). Participants selected one of seven response buttons. Subtest 7 (Match Emotional Prosody and Face): participants heard one sentence spoken in an emotional tone (happy, sad, angry, frightened or neutral). They simultaneously viewed photos of 5 faces expressing these five emotions. Participants selected the face that expressed the emotion corresponding to the tone of voice. Participants used the mouse to select and click on the corresponding face. Subtest 8 (Conflicting Prosody and Meaning — attend to prosody): participants heard a single sentence spoken in an emotional tone (happy, sad or neutral). The sentence contained conflicting prosody and meaning (e.g., ‘‘The puppies were rescued’’ — positive content spoken in a sad tone). Participants were instructed to ignore what was being said (i.e., the content) and instead identify emotional prosody. Participants selected one of three response buttons (in this example, sad). Participants also completed a battery of standardized cognitive and behavioral tasks to establish degree of impairment in cognitive and motor performance. Cognitive and behavioral assessments were completed at a testing facility at the University of California, Davis Center for Neuroscience. Timed motor tasks and paper and pencil questionnaires were administered in a quiet location by a single researcher (SSA) trained in neuropsychological testing, and were completed by participants without assistance. Testing sessions lasted 2–3 h with frequent breaks as dictated by the participant. Tests included:  Timed Instrumental Activities of Daily Living Tasks (TIADL tasks; Owsley, Sloane,    McGwin, & Ball, 2002) — the TIADL consisted of five tasks that are important for independent daily living. Tasks are: (1) participant is required to find a number in the phone book, (2) participant is required to make change with a handful of coins, (3) participant is required to find the ingredients listed on a can of food and read the ingredients aloud, (4) participant is required to locate specific food items on a shelf, and (5) participant is required to read the directions on a medicine bottle out loud. Time to completion is recorded for each task. Completion time: approximately 20 min. North American Adult Reading Test (NAART; Blair & Spreen, 1989) — used to estimate verbal intellectual ability. Completion time: approximately 5 min. PDQ39 (Peto, Jenkinson, Fitzpatrick & Greenhall, 1995) — a paper and pencil self-report measure of 8 areas of quality of life (including mobility, activities of daily living, emotional well-being, stigma, social support, cognition, communication, and bodily discomfort). Completion time: approximately 5 min. Behavior Rating Inventory of Executive Function – Adult Version (BRIEF-A; Roth, Isquith & Gioia, 2005) – a paper and pencil standardized rating scale that indexes specific domains of executive functioning (including behavioral regulation and emotional control). Completion time: approximately 10 min. Assessments of disease severity included:  The Unified Parkinson’s Disease Rating Scale (UPDRS) — a clinical measure used to evaluate the severity of Parkinson’s disease. It contained 5 sections: (1) mentation, behavior and mood, (2) activities of daily living, (3) motor performance, (4) H&Y scale (see below), and (5) Schwab and England ADL scale. The UPDRS interview and clinical evaluation was administered by a single nurse practitioner trained in the use of the UPDRS. Completion time: approximately 30–40 min. Hoehn and Yahr (H & Y) scale — used to characterize stages associated with Parkinson’s disease; level of disability is staged from 0 to 5 (0 ¼ symptoms associated with the beginning stages of the disease and 5¼ symptoms associated with the latter stages of the disease). Completion time: approximately 5 min. Screening Instruments:  The Mini Mental State Examination (MMSE; Folstein, Folstein & McHugh, 1975)  — measured five areas of cognitive function: orientation, registration, attention and calculation, recall, and language using a short list of items that can be administered repeatedly. These measures of general cognitive function were used as covariates in the analysis. Completion time: approximately 15 min. Geriatric Depression Scale (GDS; Yesavage et al., 1983) — a 30 item self-report inventory composed of questions relating to seven common characteristics of depression later in life. These scales were: somatic concern, lowered affect, cognitive impairment, feelings of discrimination, impaired motivation, lack of future, orientation, lack of self-esteem. Scores were used as exclusion criteria and as covariates in the analysis. Completion time: approximately 10 min. 2.4. Analysis PD participants were divided into two groups, based on side of symptom onset and unilateral motor symptom severity: left-affected (N ¼12) or right-affected PD participants (N ¼ 12). Side of symptom onset was obtained from self-report, and current affected side was determined by the UPDRS and self-report. In all cases, side of symptom onset and current lateralization corresponded. From the 8 CATS subtests we defined 5 categories. Following analysis methods described by Schaffer et al. (2009), we averaged performance on Emotional Prosody Discrimination (subtest 2), Name Emotional Prosody (subtest 3), and Conflicting Prosody and Meaning (subtest 8), and referred to these combined subtests as the Composite Prosody Scale. We also averaged performance on Affect Discrimination (subtest 5) and Name Affect (subtest 6), and referred to these combined subtests as the Composite Facial Scale. Schaffer et al. (2009) found significant intercorrelation within these two groups of subtests in their investigation of test reliability. Non-emotional Prosody (subtest 1), Identity Discrimination (subtest 4), and Match Emotional Prosody and Face (subtest 7), were kept as separate subtests (Schaffer et al., 2009). Analysis of covariance (ANCOVA) was used to identify group differences in CATS performance, cognitive and motor scores and disease severity with age as a covariate. We also examined the correlation between CATS performance (reaction time) on prosodic emotion recognition tasks and neuropsychological measures of emotional control (BRIEF), activities of daily living (TIADL) and quality of life (PDQ39). 3. Results 3.1. Participant characteristics The three participant groups (left-affected PD, right-affected PD and control) were matched for years of education, cognitive performance and disease severity (Table 1). The mean age for the left-affected PD group was significantly older than right-affected PD and control groups. Therefore, an ANCOVA was used to compare MMSE and GDS scores for the three groups as well as H&Y scores for the two PD groups, controlling for age. Age was not found to be a significant covariate. The scores on the measures of disease severity and cognitive and motor performance did not show any significant differences across groups. There were no significant differences between groups for the MMSE (score range 25–30), F(2, 31)¼ .411, p ¼.67, the GDS, F(2, 31) ¼1.76, p ¼.19, or H&Y scores, F(1, 18)¼ .091, p ¼.77. 3.2. Emotion recognition CATS performance (mean percent correct and standard deviation) is reported on all eight subtests (Table 2). Emotion recognition ability was assessed across groups for percent correct Author's personal copy 1939 M.I. Ventura et al. / Neuropsychologia 50 (2012) 1936–1945 Table 2 Behavioral performance on all subtests of the Comprehensive Affect Testing System-abbreviated (CATS-A). Means and SD reported. CATS Subtests 12 LPD 12 RPD 12 Control 1. 2. 3. 4. 5. 6. 7. 8. 97.7 94.45 63.2n 93.93 81.44 76.04 52.65n 75.78n 98.1 96.2 74.6 93.55 79.16 77.6 67.04 84.63 99.6 98.48 71.59 98.4 83.33 82.29 61.74 86.19 Non-emotional prosody discrimination Emotional prosody discrimination Name emotional prosody Identity discrimination Affect discrimination Name affect Match emotional prosody & Face Conflicting prosody & meaning — attend to prosody (7.8) (6.9) (11.5) (9.4) (5.3) (13.0) (14.0) (14.5) (3.6) (3.8) (8.3) (6.6) (7.6) (9.0) (13.4) (9.3) (1.3) (2.9) (12.9) (2.9) (5.9) (13.2) (15.1) (9.2) Fig. 1. Behavioral performance on the Comprehensive Affect Testing System-abbreviated (CATS-A). Non-emotional Prosody (subtest 1), Identity Discrimination (subtest 4), the Composite Prosody Scale – average performance on Emotional Prosody Discrimination (subtest 2), Name Emotional Prosody (subtest 3), and Conflicting Prosody and Meaning (subtest 8), the Composite Facial Scale – average performance on Affect Discrimination (subtest 5) and Name Affect (subtest 6), and cross-modal Match Emotional Prosody and Face (subtest 7). (A) Percent correct: The left-affected PD group made significantly more errors than the right-affected PD group in the Composite Prosody Scale and in the cross-modal subtest (p o .05). (B) Reaction Time: The left-affected PD group was significantly faster than the right-affected PD group in the cross-modal subtest (p o .05). (Fig. 1(A) and reaction time (Fig. 1(B) based on the five categories of CATS subtests as described in Section 2 of Materials and Methods. A 3  5 mixed analysis of variance was performed using the 3 participant groups and the 5 CATS categories. GreenhouseGeisser corrections were used to adjust degrees of freedom. A significant subtest x group interaction was identified for percent correct (F(4.6, 71.42)¼2.99, p¼.019) and reaction time (F(4.25, 70.12)¼ 2.51, p¼.046). Results revealed no significant differences in percent correct or reaction time among the groups in control subtests Non-emotional Prosody Discrimination (subtest 1) and Identity Discrimination (subtest 4). In the Composite Prosody Scale (subtests 2, 3 and 8), post-hoc analysis on the interactions identified in the ANOVA was performed using the Sidak correction (Sidak, 1967) to control for alpha inflation. Results indicated that the left-affected PD group had fewer correct responses (79710%, Fig. 1(A) than the right-affected Author's personal copy 1940 M.I. Ventura et al. / Neuropsychologia 50 (2012) 1936–1945 PD group (8575%; po.05). However, no significant differences in reaction time were found between groups in the Composite Prosody Scale. Results revealed no significant differences in percent correct or reaction time among the groups in the Composite Facial Scale (subtests 5 and 6). In the cross-modal subtest (subtest 7, Match Emotional Prosody and Face), the left-affected PD group had fewer correct responses (52.5714%) than the right-affected PD group (67.3713%; po.05). The left-affected PD group also had significantly faster reaction time (5.472.2 seconds) than rightaffected PD group (7.571.9 seconds; po.05) in cross-modal subtest 7 (Fig. 1(B). One-way analyses of variance (ANOVAs) were performed for population variables years of education and gender. The three participant groups did not differ in years of education. Gender differences in PD have been previously identified (Miller & CroninGolomb, 2010). Specifically, women with PD have reported lower levels of quality of life and tend to be more depressed than men. However, we did not find any significant differences in performance on the CATS subtests between male and female participants, nor did we find differences in our measure of quality of life (PDQ39) or depression severity (GDS) between male and female PD participants. However, our analysis was underpowered with only 4 male and 8 female participants in the LPD group, and 6 males and 6 females in the RPD and control groups. 3.3. Emotion recognition: Separate emotions CATS performance (percent correct and reaction time) for separate emotions was also evaluated in each modality (prosodic/auditory and facial/visual) to determine if the ability to recognize specific emotions was disrupted in PD. We first evaluated prosodic emotion recognition in subtest 3 (Name Emotional Prosody) for each individual emotion. One-way ANCOVAs were used to compare percent correct and reaction time across the three participant groups (left-affected PD, right-affected PD and control) on separate prosodic expressions of emotion (happy, sad, angry and fear) controlling for age. Age was not a significant covariate. Results revealed no differences among the groups on prosodic cues of happiness F(2, 32)¼.002, p¼ .998, anger F(2, 32)¼.126, p¼.882 or fear F(2, 32)¼.772, p¼.494. However, a significant difference was found among groups for recognition of prosodic cues of sadness F(2, 32)¼3.579, p¼ .040. Sidak post-hoc tests revealed that left-affected PD (mean 66721%) had fewer correct responses in recognizing prosodic cues of sadness than right-affected PD (mean 8677%; Fig. 2(A)) and were slower (mean 8.775) to recognize prosodic cues of sadness compared to controls (mean 6.573.4; Fig. 2(B)). We were also interested to see if emotion recognition ability for specific emotions was disrupted in the facial/visual modality and evaluated facial emotion recognition in subtest 6 (Name Affect; Table 3). One-way ANCOVAs were used to compare percent correct and reaction time across the three participant groups on separate facial expressions of emotion (happy, sad, anger, fear, surprise, disgust and neutral) controlling for age. Age was not a significant covariate for any of the separate facial expressions of emotion except for the neutral facial condition F(1, 32)¼5.08, p ¼.031. Results revealed no differences in percent correct or reaction time among the groups on the facial cues of happiness, anger, fear, surprise, disgust or neutral. Fig. 2. Performance for separate emotions in Name Emotional Prosody (subtest 3). (A) Percent correct: Left-affected PD participants (inferred right-hemisphere pathology) performed significantly more errors in recognizing prosodic cues of sadness compared to right-affected PD participants (p o .05). (B) Reaction time: Left-affected PD participants were slower to recognize prosodic cues of sadness compared to controls (p o .05). Author's personal copy 1941 M.I. Ventura et al. / Neuropsychologia 50 (2012) 1936–1945 Table 3 Performance for separate emotions in Name Affect (subtest 6). Means and SD reported for percent correct and reaction times. There were no significant differences in recognizing facial cues of emotion across groups. Facial emotions 12 LPD % Correct 12 LPD RT 12 RPD % correct 12 RPD RT 12 Controls % correct 12 controls RT Happy Sad Angry Frightened Surprised Disgusted Neutral 100 66.66 75 54.1 70.8 70.8 85.4 4.4 12.5 8.2 5.9 7.2 7.0 6.9 100 75 62.5 58.3 87.5 66.66 85.4 4.9 11.2 8.9 6.4 6.5 5.7 7.1 100 62.5 83.33 54.1 87.5 79.1 95.8 4.5 10.2 7.4 7 5.1 6.3 5.6 (0) (32) (33) (45) (45) (33) (16) (1.6) (10.3) (5.1) (2.5) (4.7) (4.4 ) (5.7) (0) (33) (37) (41) (22) (44) (19) (2) (7.2) (6.7) (2.7) (3.8) (2.9) (4.2) (0) (37) (24) (45) (31) (25) (14) (1.1) (7.1) (3.9) (3.4) (1.6) (3.8) (3.9) Fig. 3. Correlating emotion recognition deficits with neuropsychological measures. (A) Left-affected PD participants with slower reaction times in recognizing prosodic cues of sadness in Name Emotional Prosody (subtest 3) had higher BRIEF Emotional Control T scores, reflecting greater difficulties in emotional control. (B) Left-affected PD participants with slower reaction times in recognizing prosodic cues of sadness had longer completion times in the TIADL, reflecting greater difficulty in completing tasks of daily living. 3.4. Correlating emotion recognition deficits with cognitive measures For subtest 3 (Name Emotional Prosody), we found a relationship between reaction time for prosodic recognition of sadness and the BRIEF Emotional Control T score in left-affected PD participants (Fig. 3(A)). Left-affected PD participants had slower reaction times for recognition of prosodic cues of sadness, which were positively correlated with higher BRIEF Emotional Control T scores (r ¼.67, p ¼.016). Thus, slower reaction time for recognition of sadness was correlated with decreased emotional control, or decreased ability to maintain appropriate regulatory control of one’s own behavior and emotional responses. We also found a significant relationship between reaction time for prosodic recognition of sadness and TIADL score in leftaffected PD participants (Fig. 3(B)). Left-affected PD participants had slower reaction times for recognition of prosodic cues of Table 4 Scores on PDQ-Emotion, PDQ-Communication, and overall PDQ-39. Means and SD reported. There were no significant differences in self-report quality of life between left-affected and right-affected PD. PDQ39 Emotion subscore LPD 2.6 (2) RPD 3.5 (3) PDQ39 Communication subscore PDQ39 Overall score 1.8 (1) 1.75 (2) 24.8 (15) 23.7 (19) sadness, which were positively correlated with completion time of the TIADL (r ¼.69, p ¼.019). Thus, slower reaction time for recognition of sadness was correlated with longer time to complete instrumental activities of daily living. Finally, behavioral performance on CATS (percent correct and reaction time) did not correlate with PDQ39 subscores Emotion and Communication (Table 4). However, we found a trend for the Author's personal copy 1942 M.I. Ventura et al. / Neuropsychologia 50 (2012) 1936–1945 correlation between reaction time for prosodic recognition of sadness and overall PDQ39 in left-affected PD participants. Leftaffected PD participants had slower reaction times for recognition of prosodic cues of sadness, which approached significance and were positively correlated with higher overall scores on the PDQ39 (r ¼.53, p ¼.07), a self-report measure of quality of life. Thus, slower reaction time for recognition of sadness tended to be correlated with impairment in activities of daily living and decreased quality of life. 4. Discussion 4.1. Left versus right lateralization We found that PD participants with greater symptom severity on the left side of the body (inferred right-hemisphere pathology) were specifically impaired in prosodic emotion recognition. These results are consistent with Ross & Monnot (2008), who found that although prosodic deficits may occur after either left- or rightbrain damage, focal injury to temporal operculum, particularly in the right hemisphere, resulted in significantly poorer comprehension and production of affective prosody. Furthermore, the right temporal lobe is thought to be involved in social awareness (Rankin, Baldwin, Pace-Savitsky, Kramer, & Miller, 2005) and in the perception of salient social cues (Bechara, Damasio, Damasio, & Anderson, 1994). Previous studies have shown deficits in the perception of emotional speech in PD (Dara et al., 2008; Schroder, Nikolova, & Dengler, 2010). However, our findings provide further evidence that prosodic emotion recognition ability may be specifically affected by right hemisphere pathology. It is important to distinguish affected side and contrast behavioral performance of PD participants based on this categorization to identify subgroup specific deficits, especially if there is right-hemispheric lateralization of emotional prosodic processing in the brain (Kotz et al., 2006; Ross & Monnot, 2008). However, few studies have investigated the neural substrates of social cognitive deficits in PD. The orbitofrontal loop has been associated with emotional processing (Bechara, Damasio, & Damasio, 2000) and may play a role in the flat emotional speech observed in PD (Schroder et al., 2006); the basal ganglia and prefrontal cortex have been functionally linked to processing emotional prosody in normal controls (Paulmannet al., 2008; Pell, & Leonard, 2003; Wittfoth et al., 2010). Changes in perception of emotional prosody might be explained by asymmetric degeneration of dopaminergic neurons in the nigrostriatal system, as dopamine may contribute to the regulation of emotional perception (Salgado-Pineda, Delaveau, Blin, & Nieoullon, 2005). Pathological studies show asymmetric neuronal loss in substantia nigra in PD such that there is greater cell loss contralateral to side-of-onset or affected side of body (Kempster, Gibb, Stern, & Lees, 1989). Contralateral reuptake of dopamine has also been found to be significantly lower than the ipsilateral striatal uptake in PD (Booij et al., 1997). Neuronal changes contralateral to the side of initial motor symptoms are maintained long after the disease progresses from unilateral to bilateral (Cronin-Golomb, 2010). Selective deficits in prosodic emotion recognition suggest hemispheric effects in emotion recognition, which may contribute to the impairment of emotional communication in a subset of people with PD. In order to better understand the complexities of emotion processing, some studies highlight hemispheric differences in the processing of emotional valence (Adolphs, Jansari, & Tranel, 2001). Specifically, the right hemisphere may be specialized to process negative emotions whereas the left hemisphere may be specialized to process positive emotions. Adolphs et al. (2001) found that right-hemisphere damaged patients were impaired in recognizing sad faces when presented on the viewer’s left visual field, and left-hemisphere damaged patients were impaired in recognizing happy faces when presented on the viewer’s right visual field. In addition, studies have shown that PD-related emotion recognition deficits may selectively impair negative emotion perception (Dara et al., 2008; Peron et al., 2010; Tessitore et al., 2002). For example, PD may lead to reduced sensitivity to negative emotions, especially when conveyed in tone of voice as opposed to facial cues of emotion. Dara et al. (2008) found that PD participants showed impairments in identifying certain emotions, particularly anger, disgust, and fear, however sadness was not significantly impaired. In contrast, in our study, left-affected PD participants were specifically impaired (i.e., made more errors and were slower) in recognizing prosodic cues of sadness compared to right-affected PD and control participants. However, we did not find any significant differences between our participant groups in recognizing prosodic cues of anger or fear. Some studies have shown that emotion processing is disrupted in left- and right-affected PD regardless of valence (Schroder et al., 2006). Schroder and colleagues found diminished event-related potentials to both happy and sad emotional prosody during a passive listening task, suggesting impaired early preattentive processing for both positive and negative emotions. Our conflicting results may be explained by methodological differences. We separated our PD participants based on affected side whereas Dara et al. (2008) and Schroder et al. (2006) grouped all PD participants together. Dara et al. (2008) also used more complex prosodic stimuli (i.e., they varied the emotional intensity of their sentences from ‘‘low’’ to ‘‘high’’) which may have allowed them to better capture the subtleties of emotional speech processing. Few studies of prosodic emotion recognition in PD consider left- or right-side affectedness. There may be subgroup differences within PD that provide promising leads for intervention and rehabilitation, and this distinction between left- and rightaffected PD individuals should be considered in future PD studies regarding emotion recognition. Performance in the CATS-A test of emotion processing may relate to a person’s overall ability to control emotional responses. Leftaffected PD participants with slower reaction time in recognizing prosodic cues of sadness also had higher BRIEF Emotional Control T scores, indicating decreased emotional control, whereas right-affected PD and control participants with slower reaction times for prosodic sadness trials had lower BRIEF Emotional Control T scores, indicating better emotional control. The Emotional Control scale in the BRIEF measures the impact of executive function problems on emotional expression; it is part of the Behavioral Regulation Index, which captures an individuals’ ability to maintain appropriate regulatory control of their own behavior and emotional responses (Roth et al., 2005). Left-affected PD participants with emotion recognition deficits may have more difficulty modulating or regulating emotions overall. This subset of PD participants may also have other cognitive disturbances, for example in attentional control processes, that may exacerbate their overall difficulty in regulating emotions. Detecting subtle cognitive decline, such as reduced emotional control, may aid in the prediction of subsequent decline in mildly cognitively impaired individuals (Rabin et al., 2006). Early executive dysfunction in PD has been shown to predict progression of cognitive decline to dementia (Janvin, Aarsland, & Larsen, 2005; Levy et al., 2002; Mahieux et al., 1998; Woods & Tröster, 2003; see Kehagia, Barker, & Robbins, 2010 for review) and ultimately mortality (Levy et al., 2002). Cognitive challenges such as decreased emotional control and behavioral regulation can lead to frustration and stress, and subsequently negative affect and depression in PD (Gray & Tickle-Degnen, 2010). However, performance on our emotion recognition tasks did not correlate with the Geriatric Depression Scale (GDS), ruling out the hypothesis that emotion recognition impairment of PD participants can be attributed to depression (Ariatti et al., 2008). Author's personal copy M.I. Ventura et al. / Neuropsychologia 50 (2012) 1936–1945 4.2. Multi-modal tests of emotion recognition ability Facial and prosodic cues, as well as body gestures, play a role in communicating affective states. In the current study, we have attempted to explore at least two modalities with comparable facial and prosodic control tasks. There is some evidence that the recognition of emotions is disrupted in PD regardless of modality (Ariatti et al., 2008). Specifically, Ariatti et al. (2008) found that left- and right-affected PD participants showed impairments in both facial and prosodic emotion recognition. However, results are not consistent across studies. Clark et al. (2008) found facial emotion recognition deficits in PD, while prosodic recognition remained intact. However, their assessment of prosodic emotion recognition was not as extensive as the ones used in Ariatti et al. (2008) or in the present investigation. In Clark et al. (2008) participants were simply required to identify sentences with prosodic cues of anger, disgust, fear, happiness, sadness and positive surprise. In contrast, in our study, as well as in Ariatti et al. (2008), at least three prosodic tests were used: identity discrimination, emotional and non-emotional prosody discrimination, and prosody identification. Our study also included a complex prosody processing task (i.e., subtest 8, Conflicting Prosody and Meaning — Attend to Prosody). Thus, these conflicting findings may be due, at least in part, to differences in the sensitivity of the evaluation tool. Conversely, the facial emotion recognition task used by Clark et al. (2010) was sophisticated and potentially more statistically powerful than the one used here. They used an extensive visual eye tracking paradigm to specifically investigate abnormalities in visual scanning while PD participants performed a facial emotion recognition task and a non-emotional control task, landscape categorization. Their use of a visually complex landscape control task did provide evidence for disruptions in visual scanning abilities in PD during the facial emotion recognition task. The selective impairment they observed in facial emotion recognition may be due to disruptions in visual attention or visuospatial processing in PD. Sprengelmeyer et al. (2003) used tests of familiar versus unfamiliar face identity, eye gaze perception (i.e., whether or not eye gaze direction influenced the perception of facial cues of emotion), and gender recognition (i.e., whether male or female facial expressions of emotion were easier to recognize). While our study did include multiple tasks in the visual modality (i.e., subtest 4, Identity Discrimination, subtest 5, Affect Discrimination, and subtest 6, Name Affect), future studies will benefit from including more complex facial emotion recognition tasks and non-emotional control tasks. Conflicting findings may also be due to individual differences in the manifestation of PD. There is a well-described series of parallel frontal-subcortical circuits in which the basal ganglia projects to frontal cortex and other cortical sites responsible for emotion processing (Alexander, DeLong, & Strick, 1986; Cummings, 1993). Lesions in any of the three frontal-subcortical circuits (dorsolateral prefrontal cortex, lateral orbital cortex and anterior cingulate cortex) can produce alterations to cognition and emotion (Cummings, 1993). For example, Paulmann et al. (2008) found disruptions to emotional speech processing after focal lesions in the basal ganglia and suggest that deficits in emotion processing are not only due to cortical dysfunction, but that basal ganglia may be specifically involved in emotional speech processing. In addition, Zatorre Evans, Meyer, and Gyedde, (1992) found activation in right prefrontal cortex during pitch discrimination (the main element of prosody that conveys emotion). Thus, prosodic emotion recognition is likely subserved by a neural network that is known to be impaired in PD, and individual differences in the deterioration of these networks may contribute to the variability observed across studies. 1943 Similarly, Schaffer et al. (2009) suggested that facial emotion processing is attributed to a widespread neural network, including the amygdala, basal ganglia, occipito-temporal cortex and parietal cortex (Adolphs, 2002). The amygdala plays a role in emotion processing, including responses to faces and vocal signals (Adolphs, 2009; Lane et al., 1997). Thus, compensatory strategies may be more efficient when processing facial stimuli versus prosodic stimuli. Another possibility to consider is that problems with perception of dynamic cues are more affected in PD as part of the larger syndrome that affects mental flexibility (e.g., Wisconsin Card Sorting Task; Monchi et al., 2004). Stimuli in the CATS facial subtests were static, as opposed to stimuli in the prosodic subtests, which were dynamic and required integration of tone over time. Perhaps the coordination of neural networks needed to decipher temporally complex social cues is specifically disrupted in PD. Future studies on emotion processing in PD should continue to consider asymmetric degeneration of neural circuits and the impact on social cognitive functioning. Difficulties with selective aspects of executive function such as regulation of attention can impact several domains, including social functioning and emotional control. Our study also included and a cross-modal task (i.e., subtest 7, Match Emotional Prosody and Face). This subtest may be more demanding than the single modality subtests and therefore require more attentional processing. Interestingly in this subtest, left-affected PD participants had significantly faster reaction times than right-affected PD participants despite poorer performance in this cross-modal task. Disturbed frontal regulation of attention has been found in PD (Stam et al., 1993) and deficits in selective attention may explain this relationship between reaction time and accuracy in our leftaffected PD group. An alternative explanation could be that rightaffected PD participants had slower reaction times and were able to perform better than the LPD group in the cross-modal subtest because they took their time. RPD participants were better able to compensate on this more demanding cross-modal task. Although attention processing was not measured directly in our study, future emotion recognition studies will benefit from including tests of selective attention in order to evaluate the influence that attention may have on emotional processing. 4.3. Potential intervention and rehabilitation Social cognitive deficits have been identified in other neurological disorders, and tailored cognitive rehabilitation has been shown to be an effective treatment. For example, cognitive rehabilitation focused on social knowledge has been shown to improve social cognitive abilities in schizophrenic populations (Matsui et al., 2009); remediation of language and communication deficits has been shown in traumatic brain injury and stroke patients (for review, see Cicerone et al., 2000); and computerized cognitive rehabilitation of executive, interpersonal, and social functioning has also been used with traumatic brain injury patients with some success (Adams, Adams, & Coleman, 2006). Our results may be useful for identifying emotion recognition deficits in people with PD and for directing treatment, such as tailored computerized cognitive rehabilitation, for people with these deficits. Acknowledgments The authors would like to thank Dr. Vicki Wheelock, Dr. Lin Zhang and Dr. Norika Malhado-Chang for their assistance with recruitment of PD participants, and Christine Lee and Kim Russo for their contributions to this project. 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