Journal of Clinical Neuroscience xxx (xxxx) xxx

Contents lists available at ScienceDirect

Journal of Clinical Neuroscience

journal homepage: www.elsevier.com/locate/jocn

Clinical study

The effects of dual-task in patients with Parkinson’s disease performing

cognitive-motor paradigms
Chang Hsiu-Chen a,b,c, Chen Chiung-Chu a,d,h, Liaw Jiunn-Woei e,f, Chiou Wei-Da b,g, Weng Yi-Hsin a,d,
Chang Ya-Ju d,b,e,1, Lu Chin-Song d,c,1,⇑
a
Division of Movement Disorders, Department of Neurology, Chang Gung Memorial Hospital at Linkou, Taiwan
b
School of Physical Therapy and Graduate Institute of Rehabilitation Science, College of Medicine, Chang Gung University, Taoyuan, Taiwan
c
Professor Lu Neurological Clinic, Taoyuan, Taiwan
d
Neuroscience Research Center, Chang Gung Memorial Hospital at Linkou, Taiwan
e
Healthy Aging Research Center, Chang Gung University, Taoyuan, Taiwan
f
Department of Mechanical Engineering, College of Engineering, Chang Gung University, Taoyuan, Taiwan
g
Department of Physical Rehabilitation, Kaohsiung Armed Forces General Hospital, Kaohsiung, Taiwan
h
School of Medicine, College of Medicine, Chang Gung University, Taoyuan, Taiwan

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

Article history: Patients with Parkinson’s disease (PD) exhibit impaired dual-task (DT) performance. A recent meta-
Received 4 October 2019 analysis confirmed that dual tasking severely affects walking performance in PD patients. However,
Accepted 5 January 2020 one report indicated that a cycling DT paradigm has facilitative effects on cognition. We investigated
Available online xxxx
the effects of dual tasking by using walking and cycling as motor tasks and revealed the clinical determi-
nants associated with DT performance. Twenty-seven eligible participants were enrolled for clinical,
Keywords: cognitive-walking, and cognitive-cycling DT paradigm investigations. The mean age and age at onset of
Parkinson’s disease (PD)
the patients were 59.87 ± 6.3 and 53.11 ± 8.4 years, respectively. Both the off- and on-state akinesia sub-
Dual-task (DT)
Dual-task interference (DTI)
scores were worse on the more-affected side than on the less-affected side. However, the DT effects on
Akinesia the cycling and gait outcomes on both the more-affected and the less-affected side showed no significant
differences. The DT effect on the two motor tasks and cognitive performance during a concurrent walking
task declined. Nevertheless, the DT effect on cognition improved during cycling. The present study also
revealed that the levodopa equivalent daily dosage was highly associated with cognitive-cycling perfor-
mance and that the akinesia subscore was the most relevant factor that contributed to cognitive-walking
performance. In conclusion, DT facilitation or interference might be mediated by the type of motor task
applied. The cognitive-cycling DT paradigm had a facilitative effect on cognition. Cycling exercise may
diminish motor dysfunction has been investigated. We suggest that cognitive-cycling DT training is a
potential adjuvant therapeutic strategy for patients with PD to promote motor and cognitive functions.
Ó 2020 Elsevier Ltd. All rights reserved.

1. Introduction dual-task (DT) paradigms was largest for walking, intermediate

Parkinson’s disease (PD) is a neurodegenerative disorder pri-
marily caused by a loss of dopamine neurons, which in turn leads
to a reduced number of dopamine neurotransmitters, and PD
patients present with impairment of motor function and auto-
maticity [1]. Patients with PD have difficulty performing motor
tasks, and their ability to carry out two tasks simultaneously is
impaired. Yogen-Seligmann et al. indicated that the effect of
⇑ Corresponding author at: Professor Lu Neurological Clinic, 2F, No. 10, Aly. 41,
Ln. 10, Wenhua 1st Rd., Guishan Dist., Taoyuan 333, Taiwan.
E-mail address: bob.cslu@gmail.com (L. Chin-Song).
1
Equally contributing authors.
for cycling, and smallest for standing tasks [2]. A more recent
meta-analysis confirmed that dual tasking severely affects walking
performance in PD patients [3]. However, one report showed that a
cycling DT paradigm had facilitative effects on the cognition of
patients with PD [4]. Thus, the effects of DT on motor and cognition
might rely on the type of motor task being performed.
PD patients have difficulty in the ‘‘automatic execution of
learned motor plans”, and this problem is likely due to impairment
of basal ganglia function [5]. In the early stage of PD, the ability to
perform automatic behaviors is already impaired. Symptoms, such
as akinesia, slowness of simple repetitive movements, reduced arm
swing, decreased stride length, freezing of gait, may be associated
with impaired motor automaticity [6]. The severity of the clinical

https://doi.org/10.1016/j.jocn.2020.01.024
0967-5868/Ó 2020 Elsevier Ltd. All rights reserved.

Please cite this article as: C. Hsiu-Chen, C. Chiung-Chu, L. Jiunn-Woei et al., The effects of dual-task in patients with Parkinson’s disease performing cog-
nitive-motor paradigms, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2020.01.024
2 C. Hsiu-Chen et al. / Journal of Clinical Neuroscience xxx (xxxx) xxx
symptoms of motor automaticity dysfunction has been shown to
correspond to the Unified Parkinson’s Disease Rating Scale part
III (UPDRS III) motor scores. The akinesia subscores were signifi-
cantly different between the more-affected (MA) and less-
affected (LA) sides, particularly in PD patients with modified
Hoehn and Yahr Stage (mHYS) of 1–1.5 who suffered from unilat-
eral symptoms. Penko et al. observed asymmetric swing phase
durations during gait in individuals with mild to moderate PD
(Hoehn &Yahr 2–4) under DT conditions [7]. Previous studies
reported conflicting results of asymmetric gait under DT conditions
[8–11]. In addition, there are few studies that have investigated the
difference between the MA and LA sides during a cycling DT para-
digm. Therefore, we aimed to investigate the difference between
the LA and MA sides while PD individuals perform walking and
cycling DT paradigms.
The effect of dual tasking is often quantified for a motor task as
an index of the automaticity of motor control. Previous studies
demonstrated that impairment of the sensorimotor striatum in
PD patients hinders automatic control, and the PD patients require
more attentional control to perform daily motor behaviors [6,12].
The relative change in performance associated with dual tasking
is referred to as the dual-task effect (DTE) or dual-task interference
(DTI). DTI occurs when the simultaneous execution of a cognitive
and a motor task leads to a change in performance in one or both
tasks. DTI reflects the competing demands of the two tasks for
access to limited processing resources within the brain [13]. The
effects of dual tasking depend on several factors, including motor
and cognitive function, cognitive reserve, compensatory abilities,
personality, expertise, task type, task difficulty, and task prioritiza-
tion [14]. Several reports have noted that gait quality, falling, freez-
ing, disability, and disease severity were strongly associated with
DT performance in patients with PD [15–18]. Strouwen et al. con-
ducted a comprehensive study to investigate the determinants of
DT performance in PD patients. The authors illustrated that poorer
single-task (ST) performance was the most important determinant
of lower DT performance in motor and cognitive tasks [19]. To date,
few studies have explored the relationship between cycling and
gait performance and the clinical characteristics of PD patients.
We hypothesized that the effects of dual tasking would depend
on the complexity of the motor task being performed. There may
be differences in cycling and gait performance between the LA
and MA sides. In addition, we anticipated that clinical features
would influence motor performance under DT conditions. Thus,
the present study sought to investigate the effects of DT perfor-
mance by using walking and cycling as motor tasks and reveal
the clinical determinants associated with DT performance.
2. Experimental procedures
The data in this study were collected as part of exercise and
cognitive-cycling DT training programs for patients with early
stage PD, which were approved by the Institutional Review Board
of the Chang Gung Medical Foundation (IRB No. 104-8171A3 and
201600213A3) and were conducted in accordance with the decla-
ration of Helsinki. Participants signed an informed consent form
prior to participation.
2.1. Participants
Individuals with PD were recruited from the Division of Move-
ment Disorders in the Department of Neurology at the Chang Gung
Memorial Hospital in Linkou, a referring medical center in Taiwan.
Individuals were eligible for the study if they fulfilled the inclusion
criteria described in our previous work [20].
Please cite this article as: C. Hsiu-Chen, C. Chiung-Chu, L. Jiunn-Woei et al., The effects of dual-task in patients with Parkinson’s disease performing cog-
nitive-motor paradigms, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2020.01.024
2.2. Study procedures
Each eligible patient underwent clinical assessments and two
DT paradigm tests (cognitive-cycling and cognitive-walking).
All clinical assessments were performed after 12 h of overnight
withdrawal from antiparkinsonian medications (24 h of with-
drawal was needed if the participants were taking prolonged
release dopaminergic agonists). The next morning, the UPDRS III
and mHYS were administered in the off-state. Then, the medica-
tions were self-administered by each patient. The mHYS, UPDRS
III, Timed Up and Go (TUG) test, and cognitive-walking DT tests
were performed 40–60 min later in the patients’ best on-state.
After 2–3 days, the patients completed the cognitive-cycling DT
test in their best on-state.
2.3. Dual-task paradigm
We adopted two types of DT paradigms, cognitive-cycling and
cognitive-walking. Each DT paradigm contained three sections: 1)
motor single-task (ST), 2) cognitive ST, and 3) cognitive-motor
DT without task prioritization. Under the cognitive ST and DT sec-
tions, the three cognitive tasks (i.e., calculation, spatial memory,
and Stroop color-word tasks) were randomly assigned.
2.4. Cognitive task
In the calculation task, the participants had to subtract 3 from a
number five times after they saw the instructions (e.g., ‘‘95 – 3 =
?”). In the spatial memory task, a yellow block appeared every sec-
ond. When a 3
3 grid with numbers appeared on the screen, the
participants were instructed to read the numbers in each yellow
block. In the Stroop color-word task, the participants answered
with the color of the word (Supplementary 1). The cognitive per-
formance outcomes were reaction time (milliseconds), accuracy
(%), the composite score, and DTI on the composite score (%).
2.5. Cognitive-cycling DT paradigm
The patients completed the cognitive ST test on a stationary
bicycle located approximately 1.5 m from a 50-in LCD monitor
but did not pedal the bicycle. The patients were then required to
complete the ST cycling and DT cycling tests in a specific order.
The order of the ST cycling and DT cognitive-cycling tests was
assigned randomly. The patients rested for 30 min after the ST test
and after the DT cycling test. Before cycling, the patients were
instructed to pedal the bike at a self-selected, comfortable cadence
(Supplementary 2). Cycling cadence (measured in revolutions per
minute, rpm) was captured using Arduino I/O board hardware
and Arduino IDE software (Arduino CC., Italy). The cycling perfor-
mance outcomes were cycling cadence (rpm) and DTI on cycling
cadence (%).
2.6. Cognitive-walking DT paradigm
As in the ST walking section, the patients were instructed to
walk at ‘‘preferred speed” and ‘‘fast speed” twice. Afterwards, the
patients sat on a chair located approximately 6 m from a projection
screen to perform the ST cognitive section followed by the DT
walking section twice. After the ST cognitive and DT sections, the
ST walking section was performed once. In addition, the patients
rested for 2 min between each cognitive task (Supplementary 3).
Gait performance was analyzed using GAITRite (CIR Systems, Inc.,
Franklin NJ, USA) on a 3.66-m-long and 0.9-m-wide instrumented
walkway. The walking outcomes were the spatiotemporal gait
parameters, including gait speed (cm/s), step length (cm), step
width (cm), step time (s), double limb support time (DLST, s), DTI
 C. Hsiu-Chen et al. / Journal of Clinical Neuroscience xxx (xxxx) xxx 3

on gait speed (%), step length (%), step width (%), step time (%), and Table 1
DLST (%). Clinical characteristics and assessments.

Outcomes Mean ± SD Range

2.7. Data analysis Clinical characteristics

AAE, years 59.87 ± 6.3 47–68
Gender Female/Male = 9/18 
In this study, the effect of dual tasking was defined as the DTI
Education, years 15.07 ± 2.25 12–19
and calculated as the difference between ST and DT performance, AAO, years 53.11 ± 8.40 35–65
expressed as a percentage of ST performance, as follows: DD, years 6.75 ± 3.53 2.21–14.25
LEDD, mg/daily 628.74 ± 270.38 200–1242
DTperformance  STperformance MoCA 28.19 ± 1.44 26–30
DTIð%Þ ¼
100 Clinical subtype AR/Mixed = 11/16 –
STperformance
Clinical assessments
We measured the participants’ accuracies and reaction time and Off-state
computed a composite score that accounted for speed–accuracy mHYS 1.96 ± 0.41 1–2.5
UPDRS III 22.22 ± 7.05 6–36
trade-offs [21]. Thus, cognitive performance was described as a
Tremor subscores 0.67 ± 1.00 0–3
composite score: Rigidity subscores 4.33 ± 2.91 0–9
Akinesia subscores 9.78 ± 3.42 4–17
Accuracyð%Þ LA 3.78 ± 2.03 0–7
Compositescoreð%Þ ¼
100
ReactiontimeðmsÞ MA 6 ± 1.94* 3–10
PIGD subscores 1.63 ± 0.84 0–3
The data on cycling cadence and reaction time were analyzed by On-state
using custom LabVIEW scripts. MoCA 28.19 ± 1.44 26–30
mHYS 1.85 ± 0.43 1–2.5
UPDRS III 15.00 ± 5.96 3–28
3. Statistics Tremor subscores 0.37 ± 0.79 0–3
Rigidity subscores 3.19 ± 2.7 0–9
Akinesia subscores 6.30. ± 2.66 1–12
All statistical analyses were conducted using SPSS (version 22.0, LA 2.11 ± 1.42 0–4
IBM Corp., Armonk, NY, USA) software. Descriptive statistics are MA 4.19 ± 1.96* 0–8
reported as the mean ± standard deviation. The Wilcoxon signed- PIGD subscores 1.22 ± 0.97 0–3
rank test was used to test paired samples. To identify the indepen- TUG, sec 7.42 ± 1.29 5.77–11.15
dent variables most relevant to the outcomes, a stepwise forward AR: Akinetic-rigid; AAE: Age at examination; AAO: Age at onset; DD: Duration of
procedure (often called ‘‘forward selection”) was applied. The pre- disease; LEDD: Levodopa equivalent daily dosage; MoCA: Montreal cognitive
dictors included in this study were age at onset (AAO, years), dura- assessment; mHYS: Modified Hoehn and Yahr; UPDRS III: Unified Parkinson’s Dis-
ease Rating Scale part III; Tremor subscores: item 20 (tremor at rest); Rigidity
tion of disease (DD, years), levodopa equivalent daily dosage
subscores: item 22 (rigidity); Akinesia subscores; items 23–26 (finger taps, hand
(LEDD, mg/day), clinical subtype (tremor dominant, akinetic- movements, rapid alternating movements of the hands, and leg agility); PIGD
rigid, and mixed) [22,23], MoCA score, TUG (sec); off- and on- subscores; items 29, 30 (gait, postural stability); TUG: Time Up and Go; MA: more-
state mHYS, UPDRS III score, and the tremor, rigidity, akinesia, affected side; LA: less-affected side; *: Wilcoxon signed-rank test (LA vs. MA),
and PIGD subscores. The TUG was excluded from the independent p < 0.001.

variables of the gait outcomes. The correlation coefficients

between the relevant factors and outcomes were assessed using
simple linear regression (Pearson correlation for continuous vari-
ables, Spearman’s correlation for ordinal variables, eta for categor-
ical variables). Statistical significance was defined as p < 0.05.
4. Results
4.1. Clinical characteristics
Table 1 presents the detailed clinical data of the participants.
Twenty-seven eligible participants (33.33% of whom were female)
were enrolled in this study. The participants had a mean age of 59.
87 ± 6.3 years and a mean AAO of 53.11 ± 8.40 years. The mean DD
was 6.75 ± 3.53 years, the mean LEDD was 628.74 ± 270.38 mg/day,
and the mean MoCA score was 28.19 ± 1.44. The off- and on-state
UPDRS III scores were 22.22 ± 7.05 and 15.00 ± 5.96, respectively.
Both the off- and the on-state akinesia subscores were consider-
ably worse on the MA side than on the LA side.
4.2. Motor task performance
respectively. The cycling outcomes on both the MA and the LA side
exhibited no significant difference.
The gait speed under the DT walking condition (85.93 ± 21.3,
89.37 ± 22.95, and 92.63 ± 20.26 cm/s for calculation, spatial
memory, and Stroop color-word, respectively) was lower
than that under the ST walking condition at the preferred speed
(106.48 ± 16.9 cm/s). Under the ST walking condition at preferred
speed, the step time was longer on the MA side than on the LA side
(p = 0.017), but the DLST was longer on the LA side than on the MA
side (p = 0.03). In addition, the DLST was longer on the LA side than
on the MA side (p = 0.013) during the Stroop color-word DT walk-
ing condition. The DTI on the gait outcomes was similar between
the MA and LA sides.
Fig. 1A illustrates the DTI on the processing speed of motor
tasks. During the DT section, the DTI on cycling cadence was
4.68% ± 11.73%, 0.62% ± 10.28%, and 1.74% ± 10.82%, and the
DTI on gait speed was 19.84% ± 12.97%, 18.46% ± 16.27%, and
13.67% ± 9.72% for the calculation, spatial memory, and Stroop
color-word tasks, respectively. Compared with the DTI on cycling
cadence, the DTI on gait speed was significantly affected.

Table 2 presents both cycling and gait performance.
The mean ST cycling cadence was 43.31 ± 11.15 rpm, and the DT
cycling cadences during the calculation, spatial memory, and
Stroop color-word tasks were 40.63 ± 9.71, 42.47 ± 10.04, and
41.98 ± 10.15 rpm, respectively. The DTI on cycling cadence during
the calculation, spatial memory, and Stroop color-word tasks
were  4.68% ± 11.73%, 0.62% ± 10.28%, and 1.74% ± 10.83%,
4.3. Cognitive performance
The cognitive DT performance improved during the cycling DT
paradigm, and the composite score of the DT calculation task sig-
nificantly increased (7.07 ± 2.42 vs. 7.89 ± 2.57, p = 0.013) com-
pared with that of the ST cognitive section. The DTI on the
calculation, spatial memory, and Stroop color-word cognitive tasks

Please cite this article as: C. Hsiu-Chen, C. Chiung-Chu, L. Jiunn-Woei et al., The effects of dual-task in patients with Parkinson’s disease performing cog-
nitive-motor paradigms, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2020.01.024
4 C. Hsiu-Chen et al. / Journal of Clinical Neuroscience xxx (xxxx) xxx

Table 2
Motor task performance under DT paradigm.

Outcomes ST DT DTI, %
Preferred Fast speed Calculation Spatial Stroop color- Calculation Spatial Stroop color-
speed memory word memory word
Cycling cadence,
rpm
Overall 43.31 ± 11.15 ND 40.63 ± 9.71 42.47 ± 10.04 41.98 ± 10.15 4.68 ± 11.73 0.62 ± 10.28 1.74 ± 10.83
LA ND 40.26 ± 10.04 41.94 ± 10.26 41.5 ± 10.40 5.18 ± 14.33 1.33 ± 13.89 3.05 ± 12.64
MA ND 40.25 ± 10.06 41.97 ± 10.25 41.49 ± 10.45 5.83 ± 12.7 1.89 ± 12.29 2.32 ± 14.58
Gait parameters
Gait speed, cm/sec 106.48 ± 16.9 148.24 ± 23.5 85.93 ± 21.3 89.37 ± 22.95 92.63 ± 20.26 19.84 ± 12.97 18.46 ± 16.27 13.67 ± 9.72
Step length, cm
Overall 56.17 ± 6.41 67.99 ± 8.31 49.91 ± 8.15 49.41 ± 8.32 51.24 ± 6.96 10.96 ± 10.35 13.15 ± 11.61 8.84 ± 6.52
LA 56.3 ± 6.81 68.09 ± 8.75 49.97 ± 7.92 49.67 ± 8.4 51.81 ± 7 11.02 ± 9.59 12.73 ± 11.16 8.11 ± 6.64
MA 56.03 ± 6.53 67.89 ± 8.18 49.84 ± 9.2 49.15 ± 8.76 50.67 ± 7.88 10.97 ± 12.13 13.57 ± 12.73 9.64 ± 7.57
Step width, cm
Overall 10.23 ± 2.5 10.04 ± 2.34 11.96 ± 3.47 11.53 ± 3.3 11.19 ± 3.06 16.66 ± 21.27 12.37 ± 14.21 9.11 ± 15.83
LA 10.19 ± 2.53 10.03 ± 2.46 11.96 ± 3.49 11.52 ± 3.32 11.24 ± 3.04 17.33 ± 21.27 12.58 ± 14.49 10.69 ± 17.39
MA 10.28 ± 2.49 10.05 ± 2.26 11.96 ± 3.47 11.54 ± 3.29 11.15 ± 3.08 16.16 ± 21.94 12.41 ± 14.97 7.72 ± 15.37
Step time, sec
Overall 0.53 ± 0.05 0.46 ± 0.05 0.6 ± 0.1 0.57 ± 0.1 0.57 ± 0.07 12.4 ± 11.48 8.48 ± 12.78 6.32 ± 8.01
LA 0.53 ± 0.05 0.46 ± 0.05 0.6 ± 0.11 0.57 ± 0.1 0.56 ± 0.08 13.25 ± 11.84 8.66 ± 12.70 6.33 ± 7.89
MA 0.54 ± 0.04* 0.46 ± 0.05 0.6 ± 0.1 0.58 ± 0.1 0.57 ± 0.07 11.53 ± 12.03 8.26 ± 13.34 6.30 ± 8.73
DLST, sec
Overall 0.25 ± 0.05 0.17 ± 0.04 0.33 ± 0.11 0.31 ± 0.12 0.30 ± 0.08 28.85 ± 27.99 24.99 ± 32.98 15.38 ± 15.89
LA 0.26 ± 0.05* 0.17 ± 0.04 0.33 ± 0.12 0.31 ± 0.12 0.30 ± 0.08* 28.48 ± 27.81 25.03 ± 33.07 15.73 ± 15.71
MA 0.25 ± 0.05 0.17 ± 0.04 0.33 ± 0.11 0.31 ± 0.12 0.30 ± 0.08 29.28 ± 28.37 24.99 ± 33.13 15.06 ± 16.25

Mean ± SD, range; *: Wilcoxon-signed rank test (LA vs. MA), p < 0.05; ST: Single-task; DT: Dual-task; DTI: Dual-task interference; DLST: Double limb support time; MA: more-
affected side; LA: less-affected side; ND: Not done

Fig. 1. Dual-task interference (DTI) comparison between the two cognitive-motor paradigms. A. Both cognitive-motor paradigms yielded DTI on the motor task. The DT effect
on the processing speed of the motor task showed that gait speed was more affected than was cycling cadence. Values are Mean ± SD B. Dual-task facilitative effect on the
three cognitive tasks during cycling. The dual-task interference on the calculation and spatial memory cognitive tasks while walking. The DT interference on cognition was
clearly affected during the walking DT paradigm.

were 12.77% ± 25.42%, 9.19% ± 61.85%, and 14.55% ± 65.38%,
respectively. These findings revealed that cycling had a facilitative
effect on cognition. With the walking DT paradigm, the DT cogni-
tive performance declined, and the composite score of the DT cal-
culation task significantly decreased (p = 0.044). However, the DT
Stroop color-word task performance significantly increased
(p = 0.041) compared with that of the cognitive ST section. The
DTI values on the calculation, spatial memory, and Stroop color-
word cognitive tasks were  6.48% ± 15.77%, 3.24% ± 21.11%,
and 5.23% ± 14.43%, respectively. These findings revealed that cal-
culation and spatial memory cognitive performance deteriorated
while walking (Supplementary 4). In contrast to the DTI on cogni-
tion during the cycling DT paradigm, the DTI on cognition was
affected considerably during the walking DT paradigm (Fig. 1B).
4.4. Relationship between motor performance and clinical
characteristics
Table 3 shows that the AAO, LEDD, MoCA score, and akinesia
subscores contributed to motor performance. Under the cycling
DT paradigm, a higher AAO contributed significantly to a lower
ST cycling cadence (r = 0.598, p = 0.001), and LEDD was a key
determinant of cycling DT performance. A higher LEDD corre-
sponded to higher cycling cadence (calculation, r = 0.639,
p < 0.0001; spatial memory, r = 0.64, p < 0.0001; Stroop color-
word, r = 0.615, p < 0.0001). Under the ST walking condition at
preferred and fast speeds, a higher MoCA score contributed consid-
erably to a narrower step width; under the DT walking condition
(spatial memory and Stroop color-word tasks), a higher akinesia

Please cite this article as: C. Hsiu-Chen, C. Chiung-Chu, L. Jiunn-Woei et al., The effects of dual-task in patients with Parkinson’s disease performing cog-
nitive-motor paradigms, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2020.01.024
 C. Hsiu-Chen et al. / Journal of Clinical Neuroscience xxx (xxxx) xxx 5

Table 3
Correlations between most relevant clinical characteristics and motor performance.

Outcomes ST DT
Preferred speed Fast speed Calculation Spatial memory Stroop color-word
Cycling DT paradigm
Cycling cadence AAO NA LEDD LEDD LEDD
r 0.598 NA 0.639 0.640 0.615
p 0.001 NA < 0.0001 < 0.0001 < 0.0001
Walking DT paradigm
Gait speed None None None None None
r – – – – –
p – – – – –
Step length None None None None None
r – – – – –
p – – – – –
Step width MoCA MoCA None Akinesia (on) Akinesia (on)
r 0.412 0.39 – 0.464 s 0.404 s
p 0.033 0.044 – 0.015 0.037
Step time None mHYS (off) None None None
r 0.377 s – – –
p 0.053 – – –
DLST None None None None
r – – – – –
p – – – – –

s: Spearmen correlation coefficient r; e: Eta correlation coefficient r; ST: Single-task; DT: Dual- task; NA: Not available; DLST: Double limb support time; AAO: Age at onset;
LEDD: Levodopa equivalent daily dosage; MoCA: Montreal cognitive assessment; mHYS: Modified Hoehn and Yahr; Akinesia subscores; items 23–26 (finger taps, hand
movements, rapid alternating movements of the hands, and leg agility).

subscore in the on-state determined a wider step width (r = 0.464,
p = 0.015; r = 0.404, p = 0.037).
5. Discussion
This study had several main findings. First, in agreement with
previous studies, we observed that the DTI was higher for walking
than for cycling. In addition, the cognitive-cycling DT condition
revealed facilitative effects on cognition in PD patients. As we
hypothesized, the effect of a DT paradigm depended on the type
of motor task employed in the DT paradigm. Second, the severity
of the clinical symptoms of motor automaticity dysfunction corre-
sponded to the UPDRS motor scores. The akinesia subscores were
significantly different between the MA and LA sides. However,
the measured cycling cadence, most of the gait parameters, and
DTI on motor performance exhibited no difference between the
MA and LA sides. Third, a lower AAO and a higher LEDD con-
tributed significantly to cycling performance. Finally, the MoCA
score and akinesia subscores were closely correlated with gait
performance.
During the DT section, the reduction in gait speed was exacer-
bated compared with that of cycling cadence. Locomotor rhythmic
activity relies on the auto-activity of localized networks of neurons
or central pattern generators within the nervous system [24]. How-
ever, walking is no longer considered merely an automated motor
activity. A neuroimaging study demonstrated that patients with PD
required greater activation during imagined usual walking than
did healthy older adults [25]. Additionally, patients with PD exhib-
ited more brain activity during complex imagined walking condi-
tions (e.g., obstacle negotiation and turning) [25,26]. A number of
investigations have demonstrated that walking relies on the use
of cognition. For example, poor executive function has been shown
to be associated with gait dysfunction in patients with PD [27–30].
These findings support the notion that walking relies on the use of
several cognitive domains. In contrast to lower limb cycling, walk-
ing represents a complex motor task requiring both bilateral coor-
dination and dynamic postural control, which are continuously
monitored by cognitive resources. This result confirmed our
hypothesis that the effect of a DT paradigm depends on the com-
plexity of the motor task being performed.
We observed a trend of cognition facilitative effects when the
patients with PD performed the cognitive-cycling DT section. Even
if cognitive performance improved under DT conditions, the possi-
bility of ‘‘posture second” strategy could not be obviated [31]. The
individuals with PD might prioritize the cognitive task over main-
tenance of motor task. During the cycling DT section, the average
DTI on cycling cadence exhibited a minimal decline, but a facilita-
tive effect was observed on cognition. A previous study suggested
that the arousal and attentional demands (AAD) model [32] can
explain this facilitative effect on cognition while cycling. Addition-
ally, exercise-related arousal has been associated with increased
cognitive resources, improvement in processing speed [33–35],
and increased release of dopamine [36]. According to the AAD
model, DTI appears if the additional level of arousal cannot provide
adequate cognitive resources to maintain DT performance. Con-
trary to an increase in DTI, an increase in arousal when the
demands of a DT are less than anticipated might result in DT
benefits.
The present results showed that the degree of automaticity dys-
function in the extremities (as shown by the akinesia subscores)
was markedly asymmetric; however, cycling performance in the
bilateral lower extremities showed similar results. The same
results were observed for gait performance as well, except for
the step time and DLST gait parameters. Previous reports have
noted gait asymmetry (GA) in the early stages of PD [11], but the
degree of asymmetry was not associated with the level of asymme-
try in motor symptoms [10,37]. Increased GA implies less bilateral
coordination. During usual walking, patients with advanced PD
with motor fluctuations exhibited increased GA while they were
in the off-state, with higher GA being observed in patients with
PD who suffered from freezing of gait [10]. These previous observa-
tions suggest that bilateral coordination becomes worse during the
course of PD progression. Poor bilateral coordination seems to
reflect the pathological processes of PD. In contrast, the current
study recruited patients with early PD with a mHYS score of
1–2.5 in the off-state. Compared with usual walking, patients with
PD exhibited significantly increased GA during the walking DT

Please cite this article as: C. Hsiu-Chen, C. Chiung-Chu, L. Jiunn-Woei et al., The effects of dual-task in patients with Parkinson’s disease performing cog-
nitive-motor paradigms, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2020.01.024
6 C. Hsiu-Chen et al. / Journal of Clinical Neuroscience xxx (xxxx) xxx
condition [37]. Penko et al. reported that PD patients presented
lower extremity asymmetries during pedaling while cycling. The
authors also found that the asymmetries in pedaling were not cor-
related with the UPDRS subscores of postural instability and gait
disturbance [38]. Based on the previous observations, we con-
cluded that bilateral coordination worsens during the course of
PD; thus, asymmetric motor symptoms affect bilateral motor coor-
dination less in patients with early stage PD.
Traditionally, levodopa has been the most efficient therapy to
improve PD motor dysfunction. The improvement in motor func-
tion or physical activities was associated with the LEDD. A higher
LEDD contributed considerably to cycling DT performance. In con-
trast to the cycling performance in the cycling DT paradigm, motor
performance in the walking DT paradigm did not correspond to the
LEDD. Compared with walking, cycling is a simple motor task and
is considered a type of physical activity that may require a much
smaller amount of attentional resources. These findings imply that
automatic walking might be a less efficient medical treatment for
patients with PD. Workman et al. reported that dopaminergic med-
ication did not improve gait automaticity of PD patients under DT
conditions [39]. Thus, we were not surprised to observe that a
higher LEDD contributed considerably to DT cycling performance.
The present study showed that even during the ST walking section,
lower MoCA scores were associated with a worse step width. This
evidence indicates there is a relationship between cognitive func-
tion and gait abnormalities. Walking relies on the use of several
cognitive domains, including executive-attentional function, visu-
ospatial abilities, and even memory resources. Many studies have
demonstrated an association between gait abnormalities and poor
executive/attention ability in older adults [5,6] and in patients
with PD [27–29].
Our results indicated that disease progression–related motor
dysfunction impacts gait automaticity in patients with PD. During
the walking DT section, the akinesia subscore in the on-state was
the most relevant factor that contributed to gait performance. Aki-
nesia (or bradykinesia) is the primary feature contributing to
motor difficulties in PD patients, and it can affect almost all activ-
ities of daily living [40]. The severity of akinesia is correlated with
the striatal dopamine terminal integrity in vivo, with maximal
involvement appearing in the posterior putamen [41]. Therefore,
the alleviation of akinesia symptoms has great clinical significance
and should be highlighted in the treatment of patients with early
stage PD. Our previous research demonstrated that cycling exercise
improved akinesia subscores by approximately 54% and 36% in the
off- and on-states, respectively [20].
There are still several limitations that should be considered.
First, the cognitive-cycling paradigm was applied after 2–3 days
of a wash-out period after the cognitive-walking paradigm, and
there may be learning effects on the cognitive task performance.
Second, cognitive-walking was performed using a 3.66 m (12 foot)
GAITRite walkway, which only allowed 1–3 trials for each cogni-
tive task. Third, task prioritization influences DT performance. No
instructions were provided regarding the prioritization of a task;
therefore, the strategy of specific-task priority might differ consid-
erably between each PD individual. Fourth, we did not estimate the
study sample size in advance, and the conclusions presented might
be conservative.
In conclusion, DT facilitation or interference on both motor and
cognitive performance might be mediated by the type of motor
task applied. The cognitive-cycling paradigm had a facilitative
effect on cognition. In addition, the akinesia subscore was the most
relevant factor contributing to DT walking. Cycling exercise may
diminish motor dysfunction has been investigated. We suggest
that cognitive-cycling DT training is a potential adjuvant therapeu-
tic strategy for patients with PD to promote motor and cognitive
functions.
Please cite this article as: C. Hsiu-Chen, C. Chiung-Chu, L. Jiunn-Woei et al., The effects of dual-task in patients with Parkinson’s disease performing cog-
nitive-motor paradigms, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2020.01.024
Funding
This work was supported by the Chang Gung Medical
Foundation and Ministry of Science and Technology, Taiwan
(grant number CMRPG3F1341, CMRPG3F1342 to CS Lu, MOST
108-2218-E-182-010 to YJ Chang, and CMRPD1G0041, MOST
107-2218-E-182-003 to JW Liaw).
The authors declare there are no financial or other conflicts of
interest.
Appendix A. Supplementary data
Supplementary data to this article can be found online at
https://doi.org/10.1016/j.jocn.2020.01.024.
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