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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).
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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).
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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
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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
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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).
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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
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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).
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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. This work was supported by
a grant from the NINDS (R01NS064040) to EAD. EAD was also
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M.I. Ventura et al. / Neuropsychologia 50 (2012) 1936–1945
supported by a grant from the Department of Veterans Affairs
Office of Research and Development, Rehabilitation R&D Service
(1I01RX000181). MIV was supported by the SfN Neuroscience
Scholars Program Fellowship.
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