BJMB
Brazilian Journal of Motor Behavior
Special issue:
“Control of Gait and Posture: a tribute to Professor Lilian T. B.
Gobbi”
!
Freitas et al.
2023
VOL.17
N.4
109 of 107
Do motor subtypes of Parkinson’s disease impact the learning of motor tasks?
TATIANA B. FREITAS
1
| GIORDANO M. G. BONUZZI
2
| ROSEMEYRE A. NUVOLINI
3
| KEYTE G. SILVA
3
| GISELE C.
S. PALMA
1
| ANDREA M. FREUDENHEIM
1
| JOSÉ E. POMPEU
3
| CAMILA TORIANI-PASIN
4
1
Laboratory of Motor Behavior, School of Physical Education and Sport, University of São Paulo, SP, Brazil
2
Department of Physical Education, State University of Piaui, Piaui, Brazil
3
Department of Physical Therapy, Speech and Occupational Therapy, School of Medicine, University of Sao Paulo, Sao Paulo, SP, Brazil
4
The University of Texas El Passo, El Passo, USA
Correspondence to:!Tatiana Beline de Freitas. School of Physical Education and Sport, University of São Paulo - Professor Mello Moraes Avenue, 64, Phone +55 11
3091-8786
email: tatibeline@gmail.com
https://doi.org/10.20338/bjmb.v17i4.361
HIGHLIGHTS
• Individuals with postural instability and gait difficulty
(PIGD) and tremor-dominant (TD) motor subtypes of
Parkinson’s Disease can acquire and maintain postural
control skills over extended periods;
• The performance during the practice of the PIGD motor
subtype in postural control skills is worse than TD motor
subtypes, but it does not affect the long-term motor
learning process;
• The PD motor subtype does not influence the learning
of postural control skills.
ABBREVIATIONS
APAs Anticipatory postural adjustments
COP Center of pressure
ES Effect size
MDS-UPDRS Unified Scale Evaluation of Parkinson's
Disease
MiniBEStest Mini Balance Evaluation System Test
MoCA Montreal Cognitive Assessment
PD Parkinson’s disease
PIGD Postural instability and gait difficulty
TD Tremor-dominant
PUBLICATION DATA
Received 21 04 2023
Accepted 18 06 2023
Published 20 06 2023
BACKGROUND: Previous studies have demonstrated that people with Parkinson's disease
(PD) can acquire postural control skills even with the degeneration of motor areas responsible
for consolidation of the representation regarding the learned motor skill in long-term memory.
However, these findings have not considered the PD motor subtypes – tremor-dominant (TD),
and postural instability and gait difficulty (PIGD). Although there is considerable heterogeneity
in motor and non-motor symptoms between TD and PIGD, no study has addressed the effect
of the PD subtype on learning postural control skills.
AIM: We investigated the influence of PD motor subtypes on the learning of tasks with
different postural control demands.
METHOD: Fourteen individuals with PD (7 TD, 7 PIGD) practiced four motor tasks with high
postural and cognitive demands. Participants completed 13 one-hour sessions (2x/week for 7
weeks). We considered the first and last practice sessions, pre-test and post-test,
respectively. Also, we conducted one-week and one-month retention tests to assess
performance persistence (motor learning). We assessed motor performance through the
scores achieved on each motor task.
RESULTS: Both groups demonstrated improvement in performance during the acquisition
phase. However, the TD group outperformed the PIGD group in all motor tasks, despite both
groups showing improvement in motor performance when comparing the results of pre-test
with the post-test, and the improved performance was maintained in retention tests. The
performance differences between groups are dissipated during consolidation, and they did not
directly affect motor learning.
INTERPRETATION: The TD and PIGD motor subtypes learned postural control tasks with
different motor and cognitive demands.
KEYWORDS: Parkinson’s disease | Motor subtypes | Postural control | Motor learning
INTRODUCTION
Motor learning is defined as a series of processes associated with practice and/or experience that led to a relatively permanent
change in the ability to perform a motor skill
1
. In neurologically healthy individuals, this process depends on subcortical structures,
including cerebellum and basal ganglia
2–5
. Specifically, the consolidation of the representation regarding the learned motor skill in long-
term memory involves striatum nucleus
6
. In Parkinson's disease (PD) there is degeneration of dopaminergic neurons in the substantia
nigra of the basal nuclei
7,8
, which could impact motor learning in these individuals. Individuals with Parkinson's disease present cognitive
and motor symptoms that can make it challenging to practice motor skills
6
, an essential aspect of motor learning9.
Despite having well-defined symptoms, PD is a heterogeneous disease in terms of symptoms that can be classified into PD
subtypes: dominant tremor (TD) and postural instability and gait difficulty (PIGD)
10,11
. The TD motor subtype predominates resting tremor,
low prevalence of cognitive symptoms, slow progression, and better prognosis. The PIGD motor subtype, on the other hand, presents a
predominance of bradykinesia, rigidity and alterations related to posture and gait, higher incidence of dementia, faster progression, and
worse prognosis
12
.
Classification of motor subtypes is important in the initial phase of PD, as identifying subtypes can help predict the disease
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clinical course of the disease
13
. Thus, correctly diagnosing subtypes supports predicting how the disease will progress, guiding early
treatment options
13
. However, the motor subtype can change across the disease progression, mainly from the TD motor subtype to PIGD
14,15
. An effective method for tracking subtype changes and distinguishing between PIGD and TD motor subtypes is evaluating the
standing center of pressure (COP) time series, a crucial aspect of postural control
13
.
Postural instability is the most refractory to treatment based on dopaminergic replacement through levodopa and its agonists
16
and, with the evolution of the disease, postural control is affected by both cognitive and motor impairment since it requires the complex
interaction of these systems
17
, especially among individuals of the PIGD motor subtype
16,17
.
Several studies have demonstrated that PD does not preclude the learning of motor skills
5,14–21
, including postural control skills
18–20
. However, given the heterogeneity of cognitive and motor symptoms between individuals with TD and PIGD, we supposed that the
characteristics of each PD motor subtype could influence the learning of postural control tasks. There is a lack in the motor learning
scientific literature about the effects of PD motor subtypes on motor learning, even with a current call for new studies to consider the
investigation of PD subtypes on motor and cognitive outcomes
21
.
Only one study, carried out by Vakil et al
22
, included the motor symptoms (predominance of bradykinesia or resting tremor) and
procedural memory in PD. The performed task was the stacking of disks in the Tower of Hanoi. There were two outcomes regarding task
performance, the execution time and the number of disk movements in three different moments (immediately, 30 minutes later and one
week after task practice). The bradykinesia predominance group improved the execution time of the task without improvement in the
number of disc movements. The tremor predominance group improved the execution time and the number of disc movements without
significant differences to the control group (non-disabled people)
22
.
The results of the Vakil et al
22
, despite not classifying the groups by motor subtypes but by the predominance of symptoms, we
could relate the group with a predominance of bradykinesia with the motor subtype PIGD, and the group with a predominance of tremor
with the motor subtype TD. In this study, the TD motor subtype was superior to the PIGD in learning the proposed task.
In this sense, we questioned whether the same behavior would be maintained in tasks with a high demand for postural control
since this is the main symptom of the PIGD motor subtype. Only studies in the Motor Control area of study were found in the literature,
specifically to postural control tasks. Some studies have demonstrated that the TD subtype performs better than PIGD in balance and
gait tasks
23,24
and challenging postural tasks
25
. In this sense, if the PIGD group presents an inferior performance in tasks with high
demand for postural control, we hypothesized that this performance could affect the learning of challenging skills with high postural
control demands. This study aimed to verify the motor learning process of PD individuals, considering the motor subtypes (TD and
PIGD).
METHODS
The study was approved by the Ethics and Research Committee of the School of Physical Education and Sport of the
University of São Paulo (CAAE: 44795315.8.1001.5391). This study is part of a larger randomized clinical trial (registration: RBR-27kqv5)
that aimed to investigate the effects of a virtual reality intervention in the rehabilitation of individuals with PD
26
. In a complementary study,
Freitas et al
27
, assessed the performance in the virtual reality intervention using a motor learning experimental design approach
(experimental study, with parallel groups (PD x neurologically healthy individuals) including pre, post, and retention tests) to evaluate the
motor learning of individuals with PD. In our study, we reanalyzed the Freitas et al
27
to evaluate the impact of PD subtypes on their
results
27
.
Inclusion and exclusion criteria
Inclusion criteria were individuals diagnosed with idiopathic PD, between stages 1.0 and 3.0 of the Hoehn and Yahr scale
28
,
motor subtypes TD and PIGD, treated with levodopa and/or its synergists; score < 28 on the Mini Balance Evaluation System Test
(MiniBEStest)
29
; who do not have other detectable neurological or orthopedic diseases; who were able to walk with or without the use of
aids, with normal or corrected visual acuity; good auditory acuity, these last two criteria being clinically evaluated; without previous
experience with the Kinect Adventures!® game and signed the Informed Consent Form for the study.
The exclusion criteria were no other detectable neurological, cardiorespiratory, or orthopedic diseases; no signs of dementia
30
(score of >14/30 on the Montreal Cognitive Assessment (MoCA))
, if they were part of a rehabilitation program within the last six months
or if they presented any clinical deficits that made it impossible to perform physical exercises in standing positions, i.e., fall occurrences,
freezing observed both at the initial evaluation and during the intervention.
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Special issue:
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Experimental design
The experimental design was published in Silva
32
and Freitas
27
. Figure 1 displays the distinct phases involved in this design.
Figure 1. Experimental design.
Initially, the classification of the motor subtypes was determined through Unified Scale Evaluation of Parkinson's Disease
(MDS-UPDRS) section III, specifically through items 10 (Gait), 11 (Freezing of gait), 12 (Postural stability), 15 (Postural tremor of the right
hands and left), 16 (Kinetic tremor of the right and left hands), 17 (Resting tremor amplitude in the right and left upper limbs, right and left
lower limbs, and lip/jaw) and 18 (Persistence of resting tremor)
10
. This classification is an adaptation of the process described by
Stebbbins
10
.
We collected initial information about the participants in the initial assessment considering age, sex, education, time since
diagnosis of PD, medication, motor disease severity assessed with the Hoehn and Yahr Scale
28
, the Unified Scale Evaluation of
Parkinson's Disease (MDS-UPDRS) section III
33
, MiniBESTest and MoCA.
After the initial evaluation, participants participated in 13 training sessions using four Kinect Adventure! games as learning tasks
(Xbox 360, Microsoft, Redmond, CA). Whole-body movements were captured with the Kinect camera. Training sessions were conducted
individually in a laboratory setting under the supervision of an experienced neurological physical therapist. When needed, participants
were offered short rest periods.
The first session consisted of a familiarization period (two trials per task) and a pre-test. A researcher provided detailed
instructions about performing the tasks and achieving the goals. The researcher offered movement and posture corrections through
manual guidance and verbal commands when needed. During the pre-test, participants performed five trials for each task. The
acquisition phase consisted of 11 one-hour sessions offered twice a week. Each session consisted of variable practice in blocks of four
tasks, with five trials for each task
34
.
The post-test session comprised the same blocks as the acquisition phase but two days after the acquisition phase was
finished. If the participant missed a practice session in the acquisition phase, the session was rescheduled for the same week to avoid
impacting the practice interval between the experimental sessions.
We administered the short-term retention test one week after the post-test and the long-term retention test one month later. We
used the same tasks of the acquisition phase for the retention phase.
The initial assessment and all practice sessions were performed in the ON period of dopaminergic replacement therapy.
Task description
The tasks were selected on the available Kinect Adventure! Games. The selection process was based on a pilot study
36
to
ensure: (A) constant displacement of the participant's center of mass through the movement of the upper limbs; (B) weight transfer