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Research Article
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Effects of dual task demanding manual dexterity and sit-to-stand in Parkinson disease
individuals
TATIANA B. DE FREITAS
1
| JOSÉ E. POMPEU
2
| BRIANA R. B. DE MORAES
3
| SANDRA M. A. A. POMPEU
2
| KEYTE G.
DA SILVA
2
| CAMILA TORRIANI-PASIN
1
1
Laboratory of motor behavior, School of Physical Education and Sport, University of Sao Paulo, São Paulo, SP, Brazil.
2
Department of Physical Therapy, Speech and Occupational Therapy, School of Medicine, University of Sao Paulo, São Paulo, SP, Brazil.
3
Paulista University, São Paulo, SP, Brazil.
Correspondence to: Camila Torriani-Pasin - PhD, Professor of School of Physical Education and Sport, University of São Paulo. Adress: School of Physical Education and
Sport - Professor Mello Moraes Avenue, 64. Phone +55 11 3091-8786
email: camilatorriani@gmail.com
https://doi.org/10.20338/bjmb.v15i2.197
HIGHLIGHTS
• Parkinson's disease causes loss of
automaticity and impairment in dual task (DT)
performance.
• Individuals with PD could have a pattern of
prioritization of tasks according to their level of
complexity.
• Postural control, upper extremity, and verbal
fluency showed worse performance in the dual
task condition.
ABBREVIATIONS
DT Dual task
DTC Dual task cost
DTI Dual-task interference
GDS Geriatric Depression Scale
H&Y Hoehn and Yard scale
MMSE Mini Mental Status Examination
PD Parkinson’s disease
PMC Premotor cortex
PUBLICATION DATA
Received 21 09 2020
Accepted 26 01 2021
Published 01 06 2021
BACKGROUND: Parkinson's disease (PD) causes loss of automaticity and impairment in dual task (DT)
performance.
AIM: To investigate the performance and pattern of prioritization of individuals with PD in motor and cognitive DT.
METHOD: An observational, transversal, comparative study assessed 20 individuals with PD between stages 1.5
to 3 of the modified Hoehn and Yahr scale. Performance was assessed during the execution of manual dexterity
and sit-to-stand tasks, in a single task or in association with a verbal fluency task.
RESULTS: There was a loss of performance in both dual task conditions. The cost of verbal fluency was higher
than the cost of manual dexterity function.
CONCLUSION: Individuals with PD showed worse DT performance and prioritized the manual dexterity task. There
was no prioritization between sit-to-stand and verbal fluency. These findings suggest that the nature of tasks can
influence the prioritization of dual tasks.
KEYWORDS: Parkinson’s disease | Attention | Upper extremity | Postural control
INTRODUCTION
Parkinson´s disease (PD) is caused by the degeneration of dopaminergic neurons
of substantia nigra and cholinergic neurons of the pedunculopontine nucleus, among other
areas of the brain.
1
The cardinal symptoms of the disease include resting tremor,
bradykinesia, rigidity, and postural instability.
2
Due to lesions on the basal ganglia,
individuals with PD have less automatic postural control, gait disturbances, and poorer
execution of manual tasks.
3
A lack of automaticity results in delayed muscle contraction,
4,5
deficits in dynamic postural control
6–8
, for example, turning
6
and obstacle avoidance
7
, as well
as at upper extremity coordination tasks
9
such as writing
10
.
Individuals with PD often require a heightened attentional focus to compensate for
reduced automation to successfully perform common balance tasks.
11
Thus, individuals use
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cortical mechanisms to control posture and manual tasks that require the use of attentional
resources and result in the division of attention between competing task demands.
12
The division of attention that occurs during simultaneous task performance has
been studied using a dual task (DT) paradigm.
13
In the DT paradigm two or more tasks are
performed at the same time typically identifying the main task as the “primary task” with an
associated “secondary task”.
13
Individuals with PD have demonstrated worse performance
in DT conditions as compared to a single-task condition. Possible mechanisms contributing
to this decrement in task performance are: (1) loss of automaticity; (2) decreased attention
resources and (3) the reduced ability to share attention among two or more tasks.
11,12,14
Previous studies have shown that individuals with PD experience extensive
problems during DT (e.g., decrease in walking speed
16
and higher gait variability
13
).
13,15
But
most studies that have investigated dual-task interference (DTI) in individuals with PD have
focused on gait
13,17,18
and postural control
18–20
, while only a small number of studies have
investigated the effects of DTI on upper limb tasks. Yet interestingly, studies of the upper
limbs have shown impairments of hand dexterity in dual task conditions for individuals with
PD.
21,22
DTI accounted for 44% of the variance in dexterity-related activities of daily living
performance of the dominant hand.
22
Individuals with PD also demonstrate to reduce
performance in a simultaneously performed goal-directed upper-limb motor task when
paired with a cognitive task compared to performance in age-matched controlled subjects.
23
Additionally, there are writing deficits in the dual task writing condition compared to age-
matched controls, more specifically during small-amplitude movements.
24
Based on the different attention mechanisms between postural control tasks and
upper extremity functional tasks, we speculate that the task which requires the most
attentional demand, may be more impacted by dual task performance, and worsen the
performance of the primary task. Thus, this study aimed to compare the effect of DT during
the performance of postural control task (i.e., 30-s chair stand) and an upper-extremity
functional task (i.e., Box and Blocks test) of individuals with PD. We assessed prioritization
patterns during the dual tasks involving sit-to-stand and manual dexterity performed in
concert with a cognitive task.
METHODS
Subjects
This cross-sectional study was approved by the Ethical Committee of the University
(CEP/ICS/UNIP: 641.783). Subjects were invited to participate in the study and were asked
to sign the Consent Term in which the objectives and procedures of the study were explained
in detail.
Twenty individuals with PD of both sexes were enrolled in this study. The inclusion
criteria were: (1) diagnosis of idiopathic PD; (2) individuals between stages 1.0 to 3 of the
modified Hoehn and Yard scale (H&Y);
25
(3) on levodopa replacement therapy and (4) no
signs of dementia as evaluated by the Mini-Mental Status Examination (MMSE).
26
We
adopted cutoff scores of MMSE based on educational level (>20 for illiterates; > 25 for
patients with from 1 to 4 years of education; > 26 for patients with 5 to 8; > 28 for patients
with 9 to 11 years; > 29 for individuals with more than 11 years of education).
27
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Individuals with other neurological, orthopedic, cardiac, or pulmonary diseases or
who were unable to perform the required tasks were excluded from the study.
Procedures
For sample characterization, we performed the Geriatric Depression Scale (GDS)
and recorded the age, sex, H&Y, and MMSE of each participant.
Single task assessment
We assessed the performance in single and dual task conditions. Single- and dual-
task accomplishments were assessed during the “on” PD medication period, about 40
minutes to two hours after Levodopa was administered. Primary tasks included the postural
control task (the 30-s sit-to-stand) and manual dexterity task (Box and Blocks Test),
respectively. A secondary, cognitive task (reciting the weekdays backward) was assessed
in setting as a baseline condition and associated with each of the primary tasks to form a
dual task condition. Each task was performed and recorded for 30 seconds.
Manual dexterity was assessed using the Box and Block test. Individuals seated
comfortably on a chair in front of a table where there was a wood box with two compartments
of equal dimensions. Inside the box, there were 150 woodblocks. The manual dexterity task
consisted of transferring the greater number of blocks from one side of the box to the other
side, being one block each time, as fast as possible, and using the dominant hand
28
for 30
seconds. The number of blocks transferred from one to the other side was recorded.
29
Postural control was assessed using the 30-s sit-to-stand. Each participant began
the task seated on a chair without arms and was asked to stand up and sit back down many
times as possible and as fast as possible during 30-second intervals. The 30-s sit-to-stand
was performed on a chair with a seat height of approximately 44 cm, according to the
description in Duncan et al.
30
The subject sat on the center of the chair, with the back straight,
the feet parallel and separated by a distance equivalent to the shoulder width, and arms
folded across the chest.
30
The number of times the participant stood up from the chair was
recorded.
31
The 30-s sit-to-stand test was selected as a measure of postural control because
it is a dynamic test which the performance of individuals with PD is related to PD motor
impairments. Such as balance disorders and bradykinesia, and postural control to change
from one posture to another requires a complex control of the center of mass.
32
It is an easy-
to-use and reliable test to assess the risk of falling of this population.
30
Dual task assessment
We paired each primary task with a simultaneous performance of the cognitive task
to form a dual task condition. Verbal instructions were given to the participant to perform the
two tasks as best as possible with no prioritization. We recorded the number of blocks
transferred from one to the other side, the number of times the individuals stood up from the
chair and the number of weekdays recited correctly. We randomized the order of task
performance, including single task (30-s chair stand and manual dexterity) as well as single
x dual task.
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Dual task cost
The dual task cost (DTC) is a measure of the impact of performing a secondary task
on the performance of a reference task.
13
The DTC allows a more direct comparison of dual-
task deficits across studies and provides a way to assess the relative effects of individual,
tasks, and environmental factors.
13
The DTC was calculated by the difference between performance on the dual task
condition and performance on each single task condition, as described by McDowd
33
: DTC
(%) = [(dual task – single task) / single task] x 100%.
Statistical analysis
SPSS was used to perform statistical analysis.
The homogeneity of variance was performed using the Kolmogorov-Smirnov and
Levene test, respectively, and these tests showed that our data presented normality
conditions. We applied a Student paired t-test to compare the performance in single and
dual task conditions (i.e., manual dexterity in single task versus manual dexterity in the dual
task; sit-to-stand in single task versus sit-to-stand in the dual task).
The performance of the secondary tasks in the three conditions (single task versus
manual dexterity in the dual task versus sit-to-stand in the dual task) was assessed using a
one-way ANOVA. To detect differences among the conditions, we conducted a Tukey post
hoc test.
We also ran a one-way ANOVA followed by a Tukey post hoc test to compare the
DTC between the different conditions. An alpha level of 0.05 was selected as statistical
significance.
RESULTS
The sample consisted of twenty individuals with idiopathic PD, characteristics of the
sample are highlighted in Table 1. All participants were being treated with levodopa and/or
its synergists.
All participants completed the tests. The number of times that the participants were
able to sit and stand and the number of blocks that were transferred from one box to another
on the single task was higher than in the dual task (p=0.002 and p<0.001, respectively).
(Table 2).
Table 1 – Characteristics of participants.
Sex
HY
Age
(Years)
Disease
(Years)
MMSE
(Score)
GDS-15
(Score)
Mean (SD)
13 men
7 women
25%: 1.0
25%: 1.5
25%: 2.0
20%: 2.5
5%: 3.0
60.1 (10.4)
7.9 (4.0)
27.0 (2.8)
3.5 (3.1)
Legend: SD, Standard Deviation; HY: Hoehn and Yard modified scale; MMSE, Mini Mental Status Examination; GDS-15,
Geriatric Depression Scale – 15.
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Performance of verbal fluency in the single task was higher than in the dual task
conditions (ANOVA, Tukey post hoc test, p<0.001) (Table 3).
The cost of verbal fluency was higher than the cost of manual dexterity (ANOVA,
Tukey post hoc test: * p=0.019) (Table 4). There was no difference between the costs of
manual dexterity and postural control tasks.
DISCUSSION
The main results of the present study were: (1) sit-to-stand, manual dexterity, and
verbal fluency reduced performance in DT, and (2) the cost of verbal fluency associated with
manual dexterity was higher than the costs of the other tasks. Together, these results
showed that individuals with PD prioritized tasks according to the level of complexity.
Hierarchically, postural control (represented by the 30-sit-to-stand task) is less dependent
on superior cortical function. This is followed by manual dexterity, and then language,
respectively.
34
The higher the level of attention required by the task, the higher the DT cost
is per condition.
35–38
In the present study, individuals with PD demonstrated worse performance of upper
extremity and postural control when each of these tasks was performed togeher with a verbal
fluency task. The poorer performance associated with DT condition performance in DT may
Table 2 – Sit-to-Stand task, manual dexterity, single- and dual-task
Mean (SD)
(numbers of times)
p value
Cohen D
Sit-to-Stand task - single task
9.9 (3.80)
0.002*
2.42
Sit-to-Stand task - dual task
8.0 (3.08)
Manual dexterity - single task
18.8 (7.40)
0.000*
1.27
Manual dexterity - dual task
14.7 (5.79)
Legend: SD: standard deviation; *: difference between single and dual task.
Table 3 – Performance of verbal fluency, single- and dual- task
Mean (SD)
(words)
p value
Verbal fluency - single task
30.2 (12.80)
<0.001*
Verbal fluency - Sit-to-Stand task
18.5 (9.54)
Verbal fluency - Manual dexterity
15.9 (7.18)
Legend: SD: standard deviation; *: difference between single and dual task.
Table 4 – Costs in dual task conditions
Mean (SD) (%)
p value
Sit-to-Stand task
15.5 (24.08)
0.019
a
Manual dexterity
20.8 (13.20)
Verbal fluency
44.9 (22.21)
Legend: SD: standard deviation;
a
difference between cost of verbal fluency and manual dexterity
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be related to the division of attention between the tasks or with the reduced attentional
resources.
3
Individuals with neurological disorders may be susceptible to DTI, as higher
attentional demand is required to perform the primary task. Due to the raised attentional
demand, there are fewer attentional resources available for the simultaneous performance
of tasks.
39
Specifically in individuals with PD, the damage to the lesion on the basal ganglia
can cause loss of automaticity. Studies show that movements that were automatic before
the disease become more dependent upon cortical areas, and tasks that were once
automatic now require attentional resources for successful performance. Lesions of the
basal ganglia can result in hyper-connectivity between the inferior parietal lobule and
premotor cortex (PMC) and between the cerebellum and the PMC and primary motor.
8
This
hyper-connectivity can overload the system, causing an increase in DTC.
8,19,40,41
Wu & Hallet
42
also demonstrated that individuals with PD had greater activity in the
cerebellum, premotor area, parietal cortex, precuneus, and prefrontal cortex compared to
non-PD subjects while performing automatic movements in DT condition. However, the
increased activation of cortical areas during steps tasks in the DT condition was not found
by Pelicioni et al.
43
The authors found that the PD group demonstrated reduced cortical
activity in the dorsolateral prefrontal cortex, supplementary motor area, and PMC during
more complex stepping tasks that required inhibitory control.
43
Investigation of secondary task performance is extremely important in the DT
paradigm because the performance of the primary task can be maintained or at least, less
affected to the detriment of the secondary task.
44
In the present study, our results showed
that there was worsening performance in both the primary and secondary task suggesting
that the secondary task was also affected.
In order to compare the effect of dual tasks on the primary and secondary tasks we
analyzed the cost of the dual task over the primary and secondary tasks. The cost of the
dual task analysis allowed an investigation of task prioritizations. In other words, we intend
to understand how individuals with PD share attention between the different tasks. Verbal
fluency in association with upper extremity function demonstrated the greatest DTC. In this
condition, verbal fluency had a cost of approximately 50%. The decreased attentional
reserves may be insufficient to be shared between the two tasks (i.e., language and upper
extremity function). Thus, both tasks can compete for cortical resources.
3,9,12,45
Previous
studies showed that lesions on dopaminergic neurons can cause deficiencies in the capacity
to share attention among tasks.
9,11,46
Consistent with the results of this study, other studies showed a loss of upper
extremity performance in dual task conditions with prioritization of the motor task.
9,12
Nocera
et al
47
showed that individuals with PD had a worse performance of the cognitive task, thus
suggesting prioritization of the motor task. Pradhan et al
48
assessed the performance of
individuals with PD in a dual task condition that incorporated a finger opposition as the
primary task of this study paired with a secondary subtraction task. In the dual task condition,
individuals showed worsening of performance during both tasks, but with a greater decrease
of performance of the secondary task. Proud and Morris
21
replicated these results using a
manual accuracy task and an associated subtraction task. Results also showed that
performance was worse in the dual task condition, but with prioritization of the manual task.
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According to our findings, these results show that individuals with PD prioritized
upper extremity function over verbal fluency task in a DT condition. Task prioritization
suggests that when there is competition for attentional resources, the person must decide
how to prioritize the two tasks. This self-selected strategy of task prioritization is determined
by the need to reduce the danger and maximize the pleasure.
39,49
On the other hand, there was no difference between the cost of postural control and
the cost of verbal fluency in the dual task condition when combining these two tasks. Dual
task affects the costs of postural control and verbal fluency similarly in terms of prioritization
pattern between these tasks. Kelly et al
46
suggested that the severity of the disease should
be a factor to consider. In the more severe stages of PD, there is a clear task prioritization
pattern. In fact, this clear issue could explain our findings since most of our sample is
composed of individuals with PD who showed mild motor impairments. Also, Freitas et al
50
did not find prioritization between the task of sitting and standing (postural control task) and
the secondary task in a dual task condition.
The lack of prioritization between postural control and verbal fluency also can be
explained by the nature of the two tasks. Postural control depends mainly on the brain steam,
the spinal cord, and the cerebellum, integrating information of vestibular, visual, and
somatosensory systems.
51
Verbal fluency is a cognitive task that is controlled by cortical
areas associated with language and executive functions, the association of the cortex of the
left frontal, the parietal and the temporal regions.
34
Therefore, postural control and verbal
fluency do not compete for the same resources of attention and cortical circuits. A review by
Stuart et al
52
demonstrated that the cortical activity appears to increase from baseline in
postural control task in PD, and it may represent cortical compensation for subcortical
dysfunction with the pathology of the PD. However, despite the absence of prioritization,
both tasks showed a decreased performance in a dual task condition. Marchese et al
53
stated
that postural control in PD can be affected because individuals have to use more attention
to compensate for the deficiencies of balance due to lesions on the basal ganglia. Therefore,
we speculate that the worsening of the postural control in a dual task condition can occur
due to the reduction of attention caused by the associated cognitive task.
One limitation of our study is the lack of a control group with neurologically healthy
older participants and the small sample size. Thus, we were unable to determine whether or
not these results are exclusively caused by the disease, or whether age could have an
impact on the prioritization pattern during dual task conditions.
Individuals with PD have difficulty with DTs, which limits participation in the
community. In this study, we explored the impact of carrying out DT in tasks with different
demands. The relevant results here can be used to guide clinicians to develop strategies to
navigate task prioritization and improve function in this population.
CONCLUSION
The assessment of individuals with PD in conditions associating postural control
and upper-extremity function with a cognitive task of verbal fluency showed that all tasks
were negatively impacted by the dual task performance. The tasks of postural control,
manual dexterity, and verbal fluency performed worse in the dual task condition as compared
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to each task in a single task condition. However, the cost of verbal fluency was higher than </