Brain and Cognition 74 (2010) 58–65

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Brain and Cognition

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Impaired emotion recognition in music in Parkinson’s disease

Mirjam J. van Tricht *, Harriet M.M. Smeding, Johannes D. Speelman, Ben A. Schmand
Department of Neurology, Academic Medical Center, University of Amsterdam, The Netherlands

a r t i c l e i n f o a b s t r a c t

Article history: Music has the potential to evoke strong emotions and plays a significant role in the lives of many people.
Accepted 17 June 2010 Music might therefore be an ideal medium to assess emotion recognition. We investigated emotion rec-
Available online 14 July 2010 ognition in music in 20 patients with idiopathic Parkinson’s disease (PD) and 20 matched healthy volun-
teers. The role of cognitive dysfunction and other disease characteristics in emotion recognition was also
Keywords: evaluated.
Emotion recognition We used 32 musical excerpts that expressed happiness, sadness, fear or anger. PD patients were impaired
Music
in recognizing fear and anger in music. Fear recognition was associated with executive functions in PD
Fear
Anger
patients and in healthy controls, but the emotion recognition impairments of PD patients persisted after
Parkinson’s disease adjusting for executive functioning. We found no differences in the recognition of happy or sad music. Emo-
Executive functions tion recognition was not related to depressive symptoms, disease duration or severity of motor symptoms.
We conclude that PD patients are impaired in recognizing complex emotions in music. Although this
impairment is related to executive dysfunction, our findings most likely reflect an additional primary deficit
in emotional processing.
Ó 2010 Elsevier Inc. All rights reserved.

1. Introduction (Breitenstein, Van Lancker, Daum, & Waters, 2001; Dujardin

Patients with Parkinson’s disease (PD) show impairments in
emotion recognition. These impairments occur in the recognition
of emotions from facial expressions (Lawrence, Goerendt, & Brooks,
2007; Sprengelmeyer et al., 2003; Suzuki, Hoshino, Shigemasu, &
Kawamura, 2006; Yoshimura, Kawamura, Masaoka, & Homma,
2005) and emotional prosody (Blonder, Gur, & Gur, 1989; Dara,
Monetta, & Pell, 2008; Drago, Foster, Skidmore, Trifiletti, & Heil-
man, 2008; Yip, Ho, Tsang, Li, & Ho, 2003). Still there is some con-
troversy about which specific emotions are recognized abnormally
in PD. Some researchers report specific impairments in the recog-
nition of fear and sadness (Ariatti, Benuzzi, & Nichelli, 2008; Troisi
et al., 2002), whereas others have reported deficits in recognizing
anger or disgust (Clark, Neargarder, & Cronin-Golomb, 2008; Law-
rence et al., 2007; Sprengelmeyer et al., 2003; Suzuki et al., 2006),
while still others failed to replicate emotion recognition deficits
(Adolphs, Schul, & Tranel, 1998; Mitchell & Boucas, 2009).
The recognition of emotions is a complex process. It consists of
both the perceptual processing of the stimulus and the recognition
of its emotional meaning (Adolphs, 2003). Therefore cognitive
functions, in particular executive functions such as attention and
decision making, play an important role in emotion recognition
* Corresponding author. Address: Academic Medical Center, Department of
Neurology, D2-136, P.O. Box 22660, 1100 DD Amsterdam, The Netherlands. Fax:
+31 205669187.
E-mail address: m.j.vantricht@amc.uva.nl (M.J. van Tricht).
et al., 2004; Gray & Tickle-Degnen, 2010; Ibarretxe-Bilbao et al.,
2009; Mathersul et al., 2008). PD patients show cognitive impair-
ments, executive dysfunctions being most frequent, which in a
considerable proportion of patients develop early in the course of
the disease (Dubois & Pillon, 1997; Muslimovic, Post, Speelman,
& Schmand, 2005; Zgaljardic, Borod, Foldi, & Mattis, 2003). Yet,
the role of cognitive abilities in emotion recognition in PD patients
has not been studied sufficiently. Studies that did take cognitive
functions into account have led to conflicting results (Assogna,
Pontieri, Caltagirone, & Spalletta, 2008). While some authors report
associations between cognitive functions and emotion recognition
(Breitenstein et al., 2001; Dujardin et al., 2004), others have not
(Ariatti et al., 2008; Troisi et al., 2002). This discrepancy may be
due to differences in the cognitive tasks that were administered
or to selection bias in the PD samples.
PD is characterized by a loss of dopaminergic innervation of the
basal ganglia, including the ventral striatum and the subthalamic
nucleus. These structures are richly interconnected with, for in-
stance, the amygdala and the orbitofrontal cortex, brain regions
associated with emotion recognition in faces and prosodic stimuli
(Ariatti et al., 2008; Bertrand et al., 2004; Braak et al., 2003; Brei-
tenstein, Daum, & Ackerman, 1998; Harding, Stimson, Henderson,
& Halliday, 2002; Ibarretxe-Bilbao et al., 2009; Junqué et al.,
2005). Largely the same brain regions are active during the recog-
nition of emotions in music (Gosselin, Peretz, Johnsen, & Adolphs,
2007; Gosselin et al., 2005; Khalfa et al., 2008). Therefore, deficits
in recognizing emotions in music can also be expected in PD. Until

0278-2626/$ - see front matter Ó 2010 Elsevier Inc. All rights reserved.
doi:10.1016/j.bandc.2010.06.005
 M.J. van Tricht et al. / Brain and Cognition 74 (2010) 58–65
now, most studies on emotion recognition in PD have used facial or
prosodic stimuli. Emotion recognition in other relevant modalities
such as music or other art forms has received no or scarce atten-
tion. Music is a powerful instrument in evoking emotional re-
sponses (Baumgartner, Esslen, & Jäncke, 2006; Juslin & Sloboda,
2001; Koelsch, 2005; Menon & Levitin, 2005; Peretz, Gagnon, &
Bouchard, 1998). In comparison to non-musical stimuli, such as
pictures, music can elicit stronger emotions (Goldstein, 1980). Mu-
sic might therefore be a better means to investigate emotion recog-
nition in PD than faces or prosodic stimuli.
The primary aim of this study was to investigate the recognition
of emotions in music in a group of PD patients and a group of
healthy volunteers. We aimed at gaining insight in the extent of
emotional deficits in PD patients: if PD patients are indeed less able
to recognize emotions in music than controls, this would entail
even broader deficits in emotion recognition in PD, spanning across
modalities other than faces and prosody. Moreover, given the fact
that music may provoke stronger emotions than other stimuli, our
study might allow a clearer sight at the determinants of emotional
deficits in PD patients.
Based on the above considerations, we hypothesized that PD
patients are impaired in the recognition of emotions in music.
We also expected to find a relationship between emotion recogni-
tion and executive functions. We examined if possible group differ-
ences in emotion recognition would persist after controlling for
executive functioning. If so, then it would imply an independent,
non-cognitive effect of PD on emotion recognition. In view of the
high prevalence of psychiatric disturbances in PD, in particular
depression (Schrag, 2004), we also controlled for depressive symp-
toms. Furthermore, we explored the relationship between emotion
recognition and disease variables, e.g. disease duration, medication
dosage and motor symptoms.
2. Method
2.1. Participants
Twenty patients with idiopathic PD and 20 healthy controls
participated (Table 1). Patients were selected from the control
group of an ongoing study on the neuropsychological effects of
deep brain stimulation in PD (as described in Smeding, Speelman,
Huizenga, Schuurman, & Schmand, 2009; Smeding et al., 2006). All
patients had idiopathic PD for more than 5 years. They were re-
cruited from the outpatient clinic of the AMC and two other hospi-
tals in the region: the Kennemergasthuis in Haarlem and the Vrije
Table 1
Demographic and disease characteristics of Parkinson disease (PD) patients and controls.
Male/female
Education level (Unesco ISCED; range 1–7*)
Age
Level of musical training (range 1–5)
Length of musical training (years)
Frequency of listening to classical music (range 1–5)
Familiarity with the classical music repertoire (range 1–5)
Disease duration (years)
Levodopa equivalent units (LEU)
Unified Parkinson’s Disease Rating Scale (UPDRS); part 3
Values are mean (SD). p = level of significance.
a
Chi-square test.
b
Mann Whitney U test.
c
t-test.
*
United Nations Educational Scientific and Cultural Organization. International Standard Classification of Education. ISCED (1997, 2006). LEU was calculated according to
the following conversion formula: regular levodopa dose  1 + slow release levodopa  0.75 + bromocriptine  10 + apomorphine  10 + ropinirole  20 + pergolide
 100 + pramipexole  100 + [regular levodopa dose + (slow release levodopa  0.75)]  0.2 if taking entacapone (Esselink et al., 2004).
59
Universiteit Medical Center. Exclusion criteria for both groups
were a history of psychiatric disorder, dementia (as defined by a
Mattis’ Dementia Rating Scale (Mattis, 1996) score of less than
123 (Llebaria et al., 2008), other severe neurological or somatic dis-
eases, and moderate or severe hearing loss. The healthy volunteers
were matched to the patients in terms of age, gender, education
and musical training.
The study design was approved by the Medical Ethical Commit-
tee of the Academic Medical Center. Written informed consent of
all the participants was obtained after the nature of the procedures
had been fully explained.
2.2. Materials
2.2.1. Emotion recognition task
The emotion recognition task consisted of 32 musical excerpts
(see Appendix A). The musical excerpts were selected from previ-
ous studies on emotion recognition in music (Baumgartner et al.,
2006; Kallinen, 2005; Koelsch, 2005; Menon & Levitin, 2005; Peretz
et al., 1998; Terwogt & Van Grinsven, 1991). Only excerpts which
had been shown reliable in expressing happiness, sadness, fear or
anger were selected. For happiness and sadness, only excerpts
were selected that were correctly identified by at least 95% of
healthy controls. For anger and fear the percentage correct in
healthy controls was at least 90%. For each of the four emotions,
eight fragments were chosen. The excerpts followed the rules of
the Western tonal system. Only instrumental music was used to
ensure the emotional evaluation would not be influenced by the
lyrics. The excerpts were selected from different periods of the mu-
sical history, including baroque, classical and romantic periods.
Furthermore, different instrumentations, such as solo, chamber
and orchestral music were used. The stimuli lasted on average
17 s (range 9–35 s). The excerpts expressing happiness (13 s) and
anger (16 s) were shorter in duration than the sad and fearful ex-
cerpts (20 s and 21 s respectively). However, since no association
between excerpt duration and emotion recognition has been found
(Bigand, Vieillard, Madurell, Marozeau, & Dacquet, 2005), it is un-
likely that differences in stimulus length influence emotion recog-
nition. The experimental task was preceded by four examples, one
of each emotion. The examples were selected from movie sound-
tracks. All excerpts were presented on a CD-player with two loud-
speakers. The excerpts were presented in random order. No
feedback was given, with exception of the examples. Following
each excerpt, the participants had to judge which of the four
emotions (happiness, sadness, anger or fear) was expressed in
PD patients (n = 20) Controls (n = 20) Statistics (p value)
14/6 10/10 .20a
5.4 (1.4) 5.2 (1.4) .62b
66.0 (8.6) 67.0 (10.6) .75c
1.6 (.8) 2.1 (1.0) .19b
2.3 (4.3) 3.7 (4.8) .36c
3.0 (.8) 2.7 (.7) .33b
2.5 (.8) 2.4 (.8) . 82b
11.9 (4.6) (range: 7–22) – –
747.6 (425.9) (range: 210–1846) – –
25.7 (14.8) (range: 7–64) – –
60 M.J. van Tricht et al. / Brain and Cognition 74 (2010) 58–65

the music. The four emotions were presented to the participant on 2.2.4. Depression and motor scales
a sheet of paper. If the participant chose the intended emotion, the The Geriatric Depression Scale (GDS) was used to screen for
value ‘1’ was assigned. When the selected emotion did not match depressive symptoms in both groups. To assess the severity of PD
the intended emotion, a score of ‘0’ was given. Accordingly, the motor symptoms, standardized motor testing was done with the
maximum score for the emotion recognition task was 32. The max- Unified Parkinson’s Disease Rating Scale (UPDRS; Fahn & Elton,
imum score for each of the four subtests (happiness, sadness, fear 1987) part three by a neurologist specialized in movement disor-
and anger) was 8. Furthermore, following each excerpt, we asked ders while the patient was in optimal motor state. These scales
the participants to indicate to what extent the music sounded were administered in approximately 10 min.
familiar (1 = not familiar; 4 = very familiar). The emotion recogni-
tion task was administered in approximately 10 min.
2.3. Statistical analyses
2.2.2. Perceptual musical abilities
First, a stabilizing z-score transformation of cumulative propor-
Musical stimuli are processed along two dimensions (Juslin &
tions (estimated by Van der Waerden’s formula) was applied for
Sloboda, 2001; Peretz, Champod, & Hyde, 2003): a melodic dimen-
emotion recognition and GDS scores, because these variables were
sion (‘what’) and a temporal dimension (‘when’). To control for def-
not normally distributed. After this transformation, group differ-
icits in one or both of these dimensions and for group differences in
ences in emotion recognition were tested using multivariate anal-
perceptual musical abilities, two subtests of the ‘Montreal Battery
ysis of covariance (MANCOVA, 4 emotions  2 groups), covarying
of Evaluation of Amusia’ (MBEA; Peretz et al., 2003) were adminis-
for depression and executive functioning. Effect sizes were ex-
tered: a melodic and a metric subtest. The melodic test was com-
pressed as partial eta squared (g2p ). To control for differences in
prised of two practice items and 31 experimental items. Each
executive functions between the groups, we calculated a compos-
trial was preceded by a warning tone and consisted of a target mel-
ite measure of executive functioning. We summed age and educa-
ody and a comparison melody, separated by a 2 s silent interval. In
tion corrected T-scores of tests that are frequently used in clinical
15 trials the comparison melody was identical to the target mel-
practice to measure executive functions, i.e. category fluency, letter
ody. In the remaining trials the comparison melody contained a
fluency (COWAT) and the B/A index of the TMT. Group differences
scale violation. Following each trial, the participants had to judge
in education and musical background were assessed using the
whether the two melodies were equal or different. The metric sub-
Mann–Whitney U test. Gender differences between groups were
test consisted of four practice items and 30 experimental items.
evaluated using a Chi square test. Group differences in age and per-
After each trial the participant had to classify the melody as a waltz
formance on the cognitive tasks were assessed using independent
or a march. An adapted version of the Musical Preference Scale
samples t-tests. Pearson correlations (r) were used to analyze the
(Rickard, 2004), was used to obtain information about musical
associations between emotion recognition and depressive symp-
training, listening habits and familiarity with the classical music
toms (Van der Waerden transformed scores), cognitive functions
repertoire. A questionnaire was added to this list to collect infor-
and disease variables. Pearson’s correlation analyses were also
mation on age, gender, hand preference and education. These tests
used to investigate associations between musical background and
and questionnaires were administered in approximately 10 min.
abilities, familiarity with the musical excerpts and emotion recog-
nition. For all tests, alpha of 6 0.05 was considered statistically
2.2.3. Cognitive tasks
significant.
To further clarify the relation between emotion recognition and
cognitive functions, the following cognitive tests were adminis-
tered: Mattis’ Dementia Rating Scale (DRS; Mattis, 1996); category
3. Results
fluency, animals and occupations (Luteijn & Ploeg van der, 1998);
Controlled Oral Word Association Test (Benton & Hamsher, 1989);
3.1. Neuropsychological findings
Trail Making Test (TMT) parts A and B (Reitan, 1992); Wechsler Adult
Intelligence Scale (WAIS) – III: subtest Digit Span (Wechsler, 2001)
PD patients were impaired on a number of cognitive tests
and Groninger Intelligence Test (GIT): subtest Visuospatial reason-
(Table 2). They worked slower than controls on parts A
ing (Luteijn et al., 1998). The fluency tasks, TMT and Digit Span Back-
t(38) = 3.8, p = .001, and B of the Trail Making Test, t(38) = 4.1,
ward were administered to test the hypothesis on the relation
p < .001. In addition, the demographically corrected T-scores for
between emotion recognition and executive functions. For the
the TMT B/A index were lower in the PD group, t(38) = 2.8,
TMT the B/A index, that is seconds on Part B divided by seconds on
p = .01, and there was a trend towards differences in the raw B/A
part A, was used to assess executive functions. In addition, demo-
index, t(38) = 1.8, p = .08. PD patients also performed worse on
graphically corrected T-scores for the B/A index (Schmand, Houx, &
the visuospatial reasoning test, t(38) = 3.1, p < .01. There was a
de Koning, 2003) were reported. The visuospatial reasoning test con-
trend towards differences between the groups on the category flu-
sists of a series of tangram-like problems in which subjects are asked
ency task (T-score occupations: t(38) = 1.9, p = .07). Finally, PD pa-
to indicate which of several smaller geometric figures are needed to
tients scored lower on the composite measure of executive
fill a larger geometric figure. This test was administered to assess vis-
functions than controls, t(38) = 2.33, p = .02.
uospatial abilities, rather than executive functions. PD patients per-
We found no group differences on the subtests of the Montreal
form worse than controls on this task (Muslimovic et al., 2005). To
Battery of Evaluation of Amusia (MBEA). PD patients did tend to re-
demonstrate that emotion recognition was associated with execu-
port more depressive symptoms as assessed with the Geriatric
tive functions and not with other cognitive functions, we predicted
Depression Scale, U = 128.0, p = .06 (statistical trend).
no relationship of this task with emotion recognition in music. In
support of this prediction, a clear relationship between emotion rec-
ognition and visuospatial abilities has not been demonstrated 3.2. Emotion recognition
(Adolphs et al., 1998; Gray & Tickle-Degnen, 2010; Kan, Kawanura,
Hasegawa, Mochizuki, & Nakamura, 2002; Pell & Leonard, 2005). A MANCOVA was done, using the transformed scores of the four
Both raw scores and age or age and education corrected T-scores emotion recognition tasks as dependent variables, and the com-
were reported. The cognitive tasks were administered in approxi- posite measure of executive functions and the transformed GDS
mately 60 min. score as covariates. The assumptions of equal covariance matrices
 M.J. van Tricht et al. / Brain and Cognition 74 (2010) 58–65 61

Table 2
Scores on cognitive and emotional tests for Parkinson’s disease (PD) patients and healthy controls.

PD patients (n = 20) Controls (n = 20) Statistics (p value)

Dementia rating scale
Total 138.7 (4.9) 138.6 (5.2) .95
Attention 36.2 (.9) 36.2 (1.1) .88
Initiation/perseveration 35.9 (1.9) 36.2 (1.6) .66
Construction 5.9 (.2) 6.0 (.0) .32
Conceptualization 37.2 (2.4) 36.7 (2.4) .51
Memory 23.4 (2.6) 23.6 (1.8) .83
Semantic fluency
Animals (#correct in 1 min) 23.7 (5.6) 25.0 (4.8) .42
Animals* 51.2 (9.5) 53.6 (7.1) .36
Occupations (#correct in 1 min) 16.5 (4.8) 18.9 (4.5) .12
Occupations* 45.7 (9.6) 50.8 (7.3) .06
Category fluency total* 48.8 (8.8) 52.6 (6.4) .13
Letter fluency (COWAT)
#of correct words in 3 min 37.2 (12.1) 39.0 (9.8) .61
T-score 49.2 (10.6) 52.0 (7.7) .34
WAIS Digit Span
Forward (#correct items) 8.0 (1.8) 8.4 (1.7) .49
Backward (#correct items) 5.9 (1.9) 6.0 (1.8) .80
Total score 13.9 (3.4) 14.4 (3.1) .57
T-score 49.7 (11.2) 52.6 (9.5) .39
Visual-spatial reasoning
Raw score 9.8 (3.4) 12.4 (3.4) .019
T-score 46.7 (10.1) 55.7 (8.7) .004
Trail Making Test
Part A (sec) 49.8 (17.6) 38.3 (16.2) .044
Part A* 46.2 (9.4) 57.2 (8.5) <.001
Part B (sec) 143.4 (87.6) 88.2 (35.7) .013
Part B* 42.3 (12.2) 56.2 (12.6) <.001
Trail Making Test B|A* 43.6 (12.4) 50.4 (10.0) .009
B|A index** 2.8 (1.1) 2.3 (.6) .081
MBEA
Melodic subtest (correct) 27.2 (2.6) 26.5 (3.1) .47
Rhythm subtest (correct) 25.3 (3.2) 26.3 (3.1) .38
Geriatric Depression Scale 3.5 (3.5) 1.5 (1.5) .06

Values are mean (SD).

*
T-scores (mean = 50, SD = 10) are corrected for age (category fluency, Digit span and visual-spatial reasoning) or age and education (other).
**
#seconds on TMT B/#seconds TMT A, COWAT = Controlled Oral Association Task; WAIS = Wechsler Adult Intelligence Scale – III; MBEA = Montreal Battery of Evaluation of
Amusia.

(Box’s test, p = .70) and of homogeneity of variance were met (Le-

vene’s tests, p P .06).
The multivariate test revealed that PD patients performed
worse than controls on the emotion recognition task, F
(4, 33) = 6.117, p = .001, g2p = .43, after covarying for executive func-
tioning (p = .043) and GDS score (p = .014). Univariate tests showed
significant group differences on the fear subtask, F (1, 36) = 17.1,
p = .0002, g2p = .32, after adjusting for executive functions and
depressive symptoms. We also found a group effect for the anger
subtask, F (1, 36) = 4.9, p = .03, g2p = .12, after removing variance
due to executive functions and the GDS score. There were no group
differences in the recognition of happiness and sadness (p = .67 and
p = .43, respectively). The score distributions on the four subtests of
the emotion recognition task are presented in Fig. 1.

3.2.1. Emotion recognition in relation to cognitive functioning

In the PD group, the composite measure of executive function-
ing correlated strongly with performance on the fear subtest (Ta-
ble 3). A scatter plot of these correlations is presented in Fig. 2.
This strong effect is due to correlations between the score on the Fig. 1. Box plot of the scores on the four subtests of the emotion recognition task in
fear subtest and performance on part B and the B/A index of the PD patients (black lines, gray boxes) and controls (gray lines, white boxes). On the
TMT, and performance on the category fluency task. Next, a lower happiness subtest all subjects obtained the maximum score except two subjects (+).
number correct on the subtest fear was related to a lower total For the fear recognition subtask, none of the controls scored below 5, therefore the
downward error bar is absent.
score on Mattis’ DRS in the PD group. This correlation mainly
seems to be due to the associations between fear recognition and
performance on the subtests ‘Initiation – Perseveration’ and In the control group, we also found modest correlations be-
‘Conceptualization’. tween fear recognition and cognitive functions. A lower score on
62 M.J. van Tricht et al. / Brain and Cognition 74 (2010) 58–65

Table 3
Pearson correlation coefficients for fear and anger recognition and cognitive tasks.

Fear recognition Anger recognition

PD patients Controls PD patients Controls
Mattis DRS Total .56** .41 .29 .17
Attention .29 .19 .02 .23
a
Construction .10 – .18 –
Conceptualization .46* .19 .10 .07
Initiation-perseveration .47* .35 .21 .13
Memory .34 .48* .30 .32
Trail Making Test Part A (T) .12 .46* .36 .37
Part B (T) .59** .02 .26 .29
B/A index .58** .22 .26 .04
T-score B/A .63** .12 .14 .01
Fluency Animals (T) .40# .22 .06 .09
Occupations (T) .56* .36 .07 .14
Semantic fluency total (T) .53* .34 .06 .02
Letter fluency (T) .32 .40# .19 .22
Visuospatial #Correct .23 .07 .26 .11
reasoning T-score .14 .05 .26 .02
Digit Span Forward (#items correct) .29 .35 .18 .37
Backward (#items correct) .15 .37 .11 .20
Total (#items correct) .18 .01 .16 .31
T-score .14 .03 .20 .36
Executive functions Summed T-scores for COWAT, category fluency and TMT B/A .60** .45* .03 .12

Bold indicates significant values (two-tailed).

*
p < .05.
**
p < .01.
#
statistical trend (p < .1). T = T-scores (mean = 50, SD = 10) corrected for age (category fluency, digit span and visual-spatial reasoning) or age and education (other).
a
All control subjects obtained the maximum score on this subtest.

emotion recognition subtest associated with disease duration,

Fig. 2. Scatter plot of the correlations between fear recognition and the composite
measure of executive functions (category fluency, COWAT and TMT) in PD patients
(continuous line and crosses) and controls (broken line and triangles).
the fear recognition subtest was related to a lower score on the
subtest ‘Memory’ of the DRS, a lower T-score on TMT part A and
a lower T-score on the letter fluency task (statistical trend). Finally,
the performance on the fear subtest was also related to the com-
posite measure of executive functions in healthy controls.
We found no significant correlations between anger recognition
and cognitive functions in the PD or in the control group. Neither
did we find significant correlations between the recognition of
happiness or sadness and the performance on the cognitive tasks
in PD patients and controls (r < |.18|).
As predicted, scores on the distinct subtests of the emotion rec-
ognition task did not correlate significantly with the visuospatial
reasoning task.
3.2.2. Emotion recognition in relation to demographic and disease
characteristics
No significant correlations between the performance on the
emotion recognition task and any of the demographic characteris-
tics were found (r < |.15|). Nor was the performance on any of the
medication expressed in levodopa equivalent units (LEU), severity
of the motor symptoms, or the GDS score (r < |.15|). To further clar-
ify the relationship between other disease variables (e.g. disease
severity and cognitive and emotional impairments), we correlated
disease characteristics, i.e. length of the disease and UPDRS motor
scores, and the administered cognitive and emotional tests. We
found that a higher UPDRS score was related to a lower perfor-
mance on the subtest ‘Initiation – Perseveration’ of Mattis’ DRS
(r = .63, p = .01). We also found a trend towards a relationship be-
tween our composite measure of executive functions and the
UPDRS score (r = .42, p = .09). Finally, a higher score on the UPDRS
was related to a higher score on the GDS (r = .51, p = .04). We found
no significant correlations between the disease length and the
administered cognitive or emotional tasks.
3.2.3. Emotion recognition in relation to musical background
In view of the cognitive and emotional impairments in the PD
group, the relation between emotion recognition and musical
background variables was examined in both groups separately. In
the PD group, emotion recognition was not related to familiarity
with the classical music repertoire, frequency of classical music lis-
tening nor the level of musical training. Moreover, performance on
the emotion recognition task was not related to perceptual musical
abilities as assessed with the MBEA; all correlation coefficients
were below |0.22|. Neither was familiarity with an excerpt related
to the performance on this excerpt (all correlation coeffi-
cients 6 |0.17|). There were no significant correlations between
the performance on the emotion recognition task and overall
familiarity and/or familiarity with the excerpts on the distinct sub-
tests (all correlation coefficients 6 |0.20|). In the control group,
similar results were found (all correlation coefficients 6 |0.29|).
4. Discussion
Our study demonstrated that PD patients are impaired in
recognizing fear and anger in music. Although fear recognition
 M.J. van Tricht et al. / Brain and Cognition 74 (2010) 58–65
was related to executive functions, these impairments persisted
after adjusting for executive functions. There were no differences
between PD patients and controls in the ability to recognize happi-
ness or sadness in music. The finding that deficits in emotion rec-
ognition only occurred in negative and more complex emotions
concurs with research in other modalities (Ariatti et al., 2008; Law-
rence et al., 2007; Yip et al., 2003; Yoshimura et al., 2005). We
found no indication that the ability to recognize emotions in music
was related to depressive symptoms or any of the other disease
characteristics that we examined. Finally, emotion recognition
was not related to perceptual musical abilities or other musical
background variables.
Before drawing conclusions, we need to examine the possibility
that the deficits in the recognition of fear or anger might be an arti-
fact of executive task demands. In our study, subjects were asked
to direct their attention to the stimuli, to explicitly identify emo-
tions, and to choose which of the four emotions was expressed in
a particular musical selection. As a consequence, the task taxed
executive functions to a certain extent. There are two reasons,
however, why we think that our findings reflect impaired emotion
recognition per se, and not solely impaired executive functioning.
First, the PD group showed no deficits in the MBEA subtests which
require similar directing of attention and decision making. Second,
no impairments in recognizing happiness and sadness were ob-
served, even though impairments in the recognition of sadness
have been reported in other modalities (Ariatti et al., 2008; Troisi
et al., 2002). If the task demands had been the bottleneck, then
we would have found impairments in these emotions too. We
therefore suggest that the correct identification of emotions, espe-
cially complex emotions, may be viewed as an amalgam of an emo-
tional process and a cognitive process, both of which are impaired
in PD. The cognitive part of the process requires functions like
working memory, attention, and perhaps still other executive func-
tions (Assogna et al., 2008; Dolan, 2002). This is reflected in the
correlation between executive functioning and fear recognition
for both patients and controls (Fig. 2 and Table 3). The existence
of another, purely emotional part of the recognition process is sug-
gested by the fact that the differences between the groups in rec-
ognition of fear and anger persisted after adjusting for executive
functioning. PD patients are also impaired in this emotional part
of the process. This is reflected in the downward shift of the pa-
tients’ regression line in Fig. 2.
In PD patients, recognition of fear appeared to be related to
executive functioning in particular, not to cognitive functioning
in general. Accordingly, emotion recognition was not related to
subtests that are less executive in nature, e.g. Trailmaking Test part
A, the DRS subtests memory and construction, or the visuospatial
reasoning task. This association between emotion recognition
and executive functions concurs with the findings of two studies
examining emotion recognition in faces in PD (Breitenstein et al.,
2001; Dujardin et al., 2004). We therefore emphasize the impor-
tance of evaluating executive functions in studies on emotion rec-
ognition in PD.
In the control group, we also found modest correlations be-
tween fear recognition and the performance on the Memory sub-
test of the DRS, Trailmaking Test part A, letter fluency and the
composite measure of executive functions. These findings suggest
that the association with executive functioning is not limited to
PD. Thus, the recognition of complex emotions to some extent also
taxes cognitive functions in healthy subjects. The lack of correla-
tions between fear recognition and other executive measures in
controls, however, suggests that the relationship is not uniform
in PD patients and controls.
Contrary to our finding of a relationship between fear recogni-
tion and executive functions, we found no evidence of such a rela-
tion for anger recognition. An explanation for these diverging
63
results might be that different neural substrates are responsible
for fear and anger recognition (Fusar-Poli et al., 2009; Hornek,
Rolls, and Wade, 1996; Panksepp, 2006). If this is correct, different
patterns of associations with executive functioning are to be ex-
pected for fear and anger. The key structure for fear recognition,
the amygdala, has a modulating influence on cortical regions,
including the (pre)frontal cortex (Hariri, Mattay, Tessitore, Fera,
& Weinberger, 2003; Morris et al., 1996; Sprengelmeyer, Rausch,
Eysel, & Przuntek, 1998). As frontal structures are also subserving
executive functions, this may account for our finding of a specific
relationship between fear recognition and executive functions. Dif-
ferent neural structures, the insular cortex in particular (Fusar-Poli
et al., 2009), are involved in anger recognition. In addition, the
amygdalar activation by fear stimuli seems to be stronger com-
pared to the insular activation by anger stimuli (Fusar-Poli et al.,
2009). This may explain why PD patients are impaired in anger rec-
ognition, while a relationship with executive functions is less clear.
These hypotheses should be tested in neuroimaging studies.
We found no associations between the ability to recognize emo-
tions and the length of the disease or the severity of the motor
symptoms, as assessed with the UPDRS. These findings imply that
the emotion recognition impairment of our PD group is indepen-
dent of these disease characteristics. To our knowledge only few
studies have reported significant correlations between clinical
characteristics and emotion recognition (Gray & Tickle-Degnen,
2010). We found no relationship between emotion recognition
and dopamine dosage. Others did report associations between
dopaminergic treatment and emotion recognition. For instance,
acute dopaminergic blockade in healthy subjects temporarily trig-
gers an impairment in the recognition of anger, but not of other
emotions (Lawrence et al., 2007). Contrary to this report, a recent
meta-analysis on emotion recognition in PD found no significant
effect of medication status on emotion recognition (Gray &
Tickle-Degnen, 2010).
Our study contributes to the literature on emotion recognition
in PD by demonstrating deficits in yet another modality. By using
musical stimuli we hoped to find strong effects, stronger than
those found with for example photographs of facial expressions.
Sprengelmeyer and colleagues (2003) investigated facial emotion
recognition in medicated and unmedicated PD patients. Their sam-
ple of 20 medicated PD patients was comparable to ours with re-
spect to age, estimated IQ, disease length and UPDRS score. They
reported a smaller effect size of fear recognition in facial stimuli
than we did in musical stimuli (Cohen’s d = 0.8 and 1.3, respec-
tively). Gray and Tickle-Degnen (2010) even report mean effect
sizes in the order of 0.3 for recognition of fear and anger in faces
and prosody. This suggests that musical stimuli are indeed very
useful for studying emotion recognition.
Our findings and those of previous studies suggest that PD re-
sults in a reduced ability to appreciate the meaning of emotional
stimuli in several modalities. This impairment may be related to
social and emotional functioning in daily life. Recognizing emo-
tions is important for social communication (Adolphs, 2009; Gray
& Tickle-Degnen, 2010). Deficits in emotion recognition may con-
tribute to a patient’s difficulties in drawing inferences from social
situations (Snowden et al., 2003).
A limitation of our study is the relatively small size of the PD
and control groups. In light of the diverse cognitive, emotional
and motor disturbances in PD, a large number of variables had to
be taken into account. Unfortunately, the small sample did not al-
low statistical control for all these variables. Another limitation is
that we may have selected relatively well functioning PD patients.
In spite of mean disease duration of 12 years, which is roughly
comparable to those of similar studies in this field, we found no
significant differences between PD patients and controls on most
cognitive measures. Other studies have found more cognitive
64 M.J. van Tricht et al. / Brain and Cognition 74 (2010) 58–65

impairments even in earlier stages of PD (Dubois & Pillon, 1997;
Muslimovic et al., 2005). This selection bias is a general problem
of studies that use samples of prevalent cases (Foltynie, Brayne,
Robbins, & Barker, 2004; Muslimovic, Post, Speelman, de Haan, &
Schmand, 2009). On the other hand, the selection of well function-
ing PD patients may also be viewed as a strength of our study: even
stronger emotion recognition deficits can be expected in more ad-
vanced PD patients.
We conclude that patients with Parkinson’s disease are im-
paired in recognizing fear and anger in music. The ability to recog-
nize fear in music was related to executive functions in PD patients
and controls, but the emotion recognition impairments of PD pa-
tients persisted after adjusting for executive dysfunction. This sug-
gests that recognition of emotion in music relies on cognitive as
well as emotional processes, both of which are impaired in PD.
Acknowledgments
We are very grateful for the time and effort the reviewers and
the editor invested in improving our manuscript. We also thank
Professor A.H. Zwinderman for his statistical advice and J. Aaron-
son and A. Rienstra for their careful reading of the manuscript.

Appendix A

Composer Composition Duration (s) Instrumentation Emotion

Bach, J.S. Brandenburg concerto no. 2 (first movement) 18 Orchestra Happiness
Beethoven, L. van Pianoconcerto no. 4 9 Piano and orchestra Happiness
Mozart, W.A. Eine Kleine Nachtmusik (first movement) 10 String orchestra Happiness
Mozart, W.A. Pianoconcerto no. 23 (third movement) 13 Piano Happiness
Prokovief, S. Peter and the wolf 17 Orchestra Happiness
Saint-Saëns, C. Carnaval des Animaux (Final) 9 Piano and orchestra Happiness
Verdi, G. La Traviata: preludio. 10 Orchestra Happiness
Vivaldi, A. L’Autonnu (first movement) 18 String orchestra Happiness
Albinoni, T. Adagio 18 Orchestra Sadness
Beethoven, L. van Triple concert (first movement) 20 Orchestra Sadness
Bruch, M. Kol Nidrei 22 Cello and orchestra Sadness
Grieg, E. Peer Gynt’s Suite (Aases tod) 24 Orchestra Sadness
Mahler, G. Third symphony (sixth movement) 26 Orchestra Sadness
Mendelssohn, F. Song without words, Op. 30; no. 6 in F. 19 Orchestra Sadness
Schumann, R. Fourth Symphony (Romanze) 15 Orchestra Sadness
Schubert, F. Stringquartet no. 14 (second movement) 18 String quartet Sadness
Holst, G. The Planets (Mars) 30 Orchestra Fear
Honegger, A. Second symphony (first movement) 20 Orchestra Fear
Mussorgsky, M. Night on the bare mountain 9 Orchestra Fear
Prokovief, S. Peter and the wolf 12 Orchestra Fear
Sjostakovitsj, D. Tenth symphony (first movement) 29 Orchestra Fear
Sjostakovitsj, D. Ninth symphony (second movement) 16 Orchestra Fear
Sibelius En Saga, Op. 9 36 Orchestra Fear
Stravinsky, I. Le sacre du printemps, L’adoration de la terre. 13 Orchestra Fear
Borodin, A. Second symphony (first movement) 19 Orchestra Anger
Chopin, F. Piano sonata in b, op 58, final 9 Piano Anger
Elgar, E. Enigma Variations (Troyte) 9 Orchestra Anger
Liszt, F. Totentanz 22 Piano Anger
Mozart, W.A. Pianoconcerto no. 20 (first movement) 12 Orchestra Anger
Prokovief, S. Peter and the wolf (‘feeling itself caught’) 16 Orchestra Anger
Sjostakovitsj, D. Ninth symphony (fourth movement) 27 Orchestra Anger
Stravinsky, I. Le sacre du printemps 11 Orchestra Anger

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