Abstract and Figures

METHODS Sixty-eight elderlies were paired in terms of age and gender and were equally distributed into depressed and nondepressed groups, according to their score on the Beck Depression Questionnaire. The participants performed the Grooved Pegboard Test placing and withdrawing pegs while execution time and error rate were measured. RESULTS This investigation revealed that depressive symptoms exert a broad effect upon motor control, although that the symptom intensity, as well as the interaction between aging and depression intensity, were exclusively correlated with withdrawal task, suggesting that there is a greater effect upon motor acts with higher frontal lobe requirements. CONCLUSION The discrimination of motor control aspects provides a valuable contribution for the understanding of the underlying neurophysiology of the interaction between aging and depression as it represents an indirect measure of cerebral dysfunction. Further, these findings may still have clinical implications, as they can promote more rational approaches to the elaboration of preventive measures that help maintain the functional capability of depressed elderlies.
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Motriz, Rio Claro, v.23, n.4, 2017, e1017110 DOI: http://dx.doi.org/10.1590/S1980-6574201700040005
Introduction
Over the past few years, a growing body of evidence has
demonstrated that depression disorders are gaining relevance
in disease prevention and health promotion1,2. Specically, as
the population ages, the economic impact of neuropsychiatric
disorders is expected to grow signicantly3, posing a consider-
able public health problem4,5. Depression symptoms not only
include mood alterations but an array of other disorders, including
apathy, anedonia, vegetative symptoms and cognitive dysfunc-
tion, which can severely impact the quality of life of the elderly
and their ability to deal with many activities of daily living6,7.
It is common knowledge that aging impairs the mainte-
nance of functional capability as well as several domains of
the cognitive segment. However, the notion that depression
is also associated with alterations in regions of the brain that
are not related to mood control, was acknowledged only in the
last few decades
8
. Specically, neuroscience-based inquiries
have demonstrated depression inuences several areas of the
brain, such as the prefrontal and orbitofrontal cortices, anterior
cingulate, amygdala, and the hippocampus9,10. Consequently,
impairments over executive functions11-13, processing speed14-16,
and episodic memory may occur as a function of depression,
impairing everyday functioning12,17.
Most cognitive impairments associated with depression have
a strict relationship with motor control. These consequences,
usually termed as psychomotor abnormalities, encompass the
engagement of cognitive-control mechanisms into a motor act
18
and have been commonly explored by measures concerning
processing speed, such as reaction time or the control of spatial-
temporal parameters (see Bennabi, Ugrinowitsch, Apolinario-
Souza, Vieira, Albuquerque and Benda19 for a more detailed
review). These measures were included in different analyses,
such as gait
20,21
, drawing tasks
22,23
and eye movements
24,25
.
Because motor slowness was frequently reported in these stud-
ies, the impairments over motor control have been considered a
common feature of depressed individuals and comprises a great
focus of research in the last years. Summarily, these studies have
aimed to uncover the inuences of depression on motor control
in young adults, despite that some of them omitted the medica-
tion status of the sample20,26 or were under medication22, which
might have biased the intended behavior. To our knowledge,
Beheydt, Schrijvers, Docx, Bouckaert, Hulstijn and Sabbe
27
were the only who demonstrated that unmedicated depressive
older adults presented motor control impairments in comparison
to their nondepressed peers. Promising results were observed
as they revealed that the execution and initiation times were
signicantly impaired according to the manipulation of the
cognitive load of a gure copying task27.
The distinction of motor control aspects, on the other hand,
is extremely relevant to understand the issues related to the
interaction between aging and depression since it can provide
an indirect measure of different brain dysfunctions
28
. According
to the classic Woodworth concepts29, which are still followed by
several recent researches
28,30-33
, it is possible to discriminate motor
control aspects manipulating the required time on a motor task.
More precisely, ballistic motor actions don’t require much input
of sensory information and rely mainly on a pre-programmed
phase (planning; initial impulse phase) unlike movements that
are slower which engage high feedback processing (online
control of motor actions; current control phase). Therefore,
by manipulating different motor control requirements, we may,
indirectly, reveal impairments specically linked to different
brain areas.
Original Article (short paper)
Motor control assessment of community-dwelling
older adults with depressive symptoms
Lucas Eduardo Antunes Bicalho1, Maicon Rodrigues Albuquerque1, Jonas Jardim de Paula1, Guilherme Menezes
Lage1*
1Universidade Federal de Minas Gerais, UFMG, Belo Horizonte, MG, Brazil.
Abstract — Aims: The purpose of this study was to investigate how depressive symptoms mediate different motor
control requirements in elderlies and to assess the concurring effects fomented by the interaction between aging and
depressive symptoms, providing indirect measures of brain functionality. Methods: Sixty-eight elderlies were paired in
terms of age and gender and were equally distributed into depressed and nondepressed groups, according to their score
on the Beck Depression Questionnaire. The participants performed the Grooved Pegboard Test placing and withdrawing
pegs while execution time and error rate were measured. Results: This investigation revealed that depressive symptoms
exert a broad effect upon motor control, although that the symptom intensity, as well as the interaction between aging
and depression intensity, were exclusively correlated with withdrawal task, suggesting that there is a greater effect upon
motor acts with higher frontal lobe requirements. Conclusion: The discrimination of motor control aspects provides
a valuable contribution for the understanding of the underlying neurophysiology of the interaction between aging and
depression as it represents an indirect measure of cerebral dysfunction. Further, these ndings may still have clinical
implications, as they can promote more rational approaches to the elaboration of preventive measures that help maintain
the functional capability of depressed elderlies.
Keywords: aging, depression, psychomotor, psychiatric disorders, elderly, hand function.
2Motriz, Rio Claro, v.23, n.4, 2017, e1017110
Bicalho L.E.A. & Albuquerque M.R. & de Paula J.J. & Lage G.M.
Further, the estimation of the intensity of depression is also
of fundamental concern to the understanding of the interaction
between aging and depression since it has been reported as one
possible source of variation in the degree of cognitive impair-
ment27,34. Sex is another factor that might inuence the move-
ment planning and control of depressed elderlies. Specically,
Fernandes, Ugrinowitsch, Oliveira, Bicalho and Lage35 have
recently demonstrated that response strategies in aiming con-
trol are inuenced by sex in different task constraints. Still,
neurobiological differences (dimorphisms) have been observed
in many neurological domains (see Sacher, Sacher, Neumann,
Okon-Singer, Gotowiec and Villringer36 for a review) which
reveal that sex is also a relevant subject in the inquiries of
neuroscience and consequently, in motor control.
Overall, the discrimination of different aspects involved in
the motor control of elderlies with depressive symptoms can
bring useful information regarding the interaction between aging
and depression. Particularly, we expect to conrm that depressed
older adults present more prominent impairments in the most
complex task, (i.e., the peg placement task), and further, unravel
distinct associations with their motor performance.
Material and Methods
Participants
Older adults, who were originally participating in a social
project headed by the local city hall, were invited to participate
in this study. Firstly, the volunteers were submitted to a struc-
tured interview in order to exclude individuals with previous
history of psychiatric disorder, neurological disease, with
uncorrected or abnormal vision or using medication that
might impair motor control. Also, the level of education of
the volunteers was measured according to years of study. The
Edinburgh Handedness Inventory (EHI)37 was then applied to
determinate the participant’s laterality index and to exclude
individuals who presented a preference index of 70 points
or below. Subsequently, the Mini-Mental State Examination
(MMSE)38 was employed to screen dementia cases, exclud-
ing individuals who scored less than 24 points39 . The Beck
Depression Index (BDI)40 was then applied for the assessment
of depression symptoms and to allocate participants into two
groups, depressed elderlies (DE) or nondepressed elderlies
(NE), according to their score, following the cut-off point for
mild depression (10)41,42. The BDI is a self-evaluation scale
which is used worldwide in the general population and in
primary care43. Is easy to administer, is inexpensive44 and is
considered one of the most commonly used scales for identify-
ing the severity of depression symptoms.
After the exclusion of individuals who didn’t meet the
proposed criteria, 34 individuals (65.47 ± 3.14 years) with a
score equal to or higher than 10 (mild symptoms and above)
on the BDI were allocated into DE. Then, thirty-four indi-
viduals who paired in terms of level of education, age (65.35
± 5.13 years) and gender (4 males and 30 females) and pre-
sented a score lower than 10 on the BDI were allocated as
controls (Figure 1).
Figure 1. Flowchart overview of sample selection and experimental procedures.
Volunteers recruited from a
social project led by the city
hall
Edinburgh
Handedness Inventory
Mini-Mental State
Examination
Structured
interview
Beck’s Depression
Inventory
Sample pairing in terms
of gender and age
Depressed (n=36)
- 4 male, 30 females (65.79 ± 4.95 years)
Nondepressed (n=36)
- 4 male, 30 females (66.15 ± 2.99 years)
Pegboard Grooved Test
- Placement
- Removal
Motriz, Rio Claro, v.23, n.4, 2017, e1017110 3
Motor control and depressive symptoms
After the sample selection, all volunteers were oriented
regarding the experimental procedures and signed a consent
form before joining the study, which was conducted in ac-
cordance with the Declaration of Helsinki, and was approved
by the local Ethics Committee (CEP-FUMEC 03/2011). All
participants gave written consent for participation.
Experimental procedures
After the sample selection, the participants were oriented
concerning the experimental tasks procedures. Specically,
the participants were asked to take 25 pegs (1 mm diameter
and 25 mm length) placed on a receptacle, and place them in
the row of holes of the pegboard, or withdraw the pegs from
the pegboard to the receptacle as quickly as possible and in a
standardized, prescribed order (place and withdraw pegs from
left to right using their right hand). The Pegboard Grooved
Test (Lafayette Instruments # 32025) was then applied in both
groups to analyze the motor control of the volunteers (Figure
2). Each condition was repeated and the order of execution was
randomized. The tests and interviews were conducted in the
residences of the volunteers.
Figure 2. Schematic representation of the prescribed order of peg placement (a) and withdrawal (b) on the Grooved Pegboard Task. Adapted from
Salvador et al.54
With the assistance of a chronometer, participants were
timed during the GPT execution for both tasks (placement and
withdrawal). Specically, the time between the start stimulus
until the placement/withdrawal of the last peg was measured as
execution duration. Execution errors, which include attempts
in which the pins fell during placement/withdrawal, and order
errors, were also measured by the experimenter. Furthermore,
the association of motor control measures with depression
symptoms, depression intensity, and the interaction between
aging*depression intensity were determined with correlation
analysis performed in a statistical software package.
Statistical analysis
For all motor control variables, data from two trials of each
condition were averaged for each participant. Then, the ho-
mogeneity of variances was veried with a Shapiro-Wilks test
and subsequent tests were chosen accordingly. Mann-Whitney
U-tests were used to test overall group differences regarding
mean values of execution time and errors for both tasks, and
for sex differences. Spearman’s rank correlation coefcients
were computed to assess the association between the presence
of depressive symptoms, depression intensity, and the interac-
tion between aging and depression intensity with motor control
variables. Statistical analysis was conducted with SPSS 23.0 for
Windows (Statistical Package for Social Sciences, Chicago, IL,
USA) and α ≤ .05 was used as signicance criterion.
Results
Sample characteristics
No differences in terms of age (F
1,66
=.127 p=.723), level of hand-
edness (EHI; F1,66=3.873, p=.053) and cognitive status (MMSE;
4Motriz, Rio Claro, v.23, n.4, 2017, e1017110
Bicalho L.E.A. & Albuquerque M.R. & de Paula J.J. & Lage G.M.
Pegs placement
According to the Mann-Whitney U-test, depressed older
adults presented a longer execution duration of peg placement
(MWU=349, Z=-2.810, p=.005) (Figure 3A) and a higher amount
of errors (MWU=383.0, Z=-2.472, p=.013) (Figure 3B) than
their non-depressed peers. Separate analysis revealed that the
results can’t be partially attributed to sex differences. Mann-
Whitney U-test analysis revealed no differences between males
and females regarding peg placement duration (MWU=152.5,
Z=-1.666, p=.096) and peg placement error (MWU=171.5,
Z=-1.344, p=.179) taking sex as factor. Spearman’s rank test
revealed a weak association between the presence of symptoms
and placement duration (r=0.296, p=.014) but, marginally, no
association with placement errors (r=0.233, p=.056). No signi-
cant correlations between scores of the depression rating (DBI)
with placement duration (r=0.238, p=.050) and placement errors
(r=0.085, p=.489) were revealed, either. However, a weak asso-
ciation between the interaction of aging*symptom intensity with
placement duration (r=0.260, p=.033) was observed, while no
associations with placement error (r=0.082, p=.506) were shown.
Withdrawal of pegs
The Mann-Whitney U-test also revealed that depressed older
adults present a higher withdrawal time (MWU=244.5, Z=-
4.099, p=.000) (Figure 3A) and withdrawal errors (MWU=426.5,
Z=-2.904, p=0.004) (Figure 3B) than their non-depressed coun-
terparts. The Mann-Whitney U-test analysis revealed no differ-
ences between males and females with and without depressive
symptoms regarding the duration of peg withdrawal (MWU=157,
Z=-1.584, p=.113) and withdrawal error (MWU=200, Z=-1.237,
p=.216). Correlation analysis revealed a weak association be-
tween the presence of depression symptoms and peg withdrawal
duration (r=0.472, p=.000) and with withdrawal errors (r=0.320,
p=.008). However, a moderate association between withdrawal
duration and symptom intensity (r=0.527, p=.000) (Figure 3C)
was revealed, as well as with the interaction of aging*symptom
intensity (r=0.531, p=.000). Regarding withdrawal errors,
Spearman’s rank test revealed a very weak association with
symptom intensity (r=0.242, p=.047) (Figure 3C) and a weak
association with the interaction of symptom intensity*aging
(r=0.441, p=.000).
F1,66=1.086, p=.301) were revealed between groups. In sum, non-
depressed older adults presented a range of 0 to 9 of depression
intensity on the BDI questionnaire, 80-100 on EHI, and 24-30
on MMSE; depressed elderlies presented a range of 10 to 50
on BDI, 80 to 100 on EHI, and 24-30 on MMSE. Descriptive
statistics for the entire sample are represented below on Table 1.
Table 1. Demographic characterization of depressed and non-depressed participants. Comparisons between groups were performed with univari-
ate analysis of variance (ANOVA). *p ≤ .05; **p ≤ .01
Participants
Nondepressed Depressed
Age (years) 66.15 ± 2.99 65.79 ± 4.95
Beck Depression Inventory 5.38 ± 2.24 ** 16.94 ± 9.46
Edinburgh Laterality Index 99.12 ± 3.79 97.94 ± 5.38
Gender 30 ♀ / 4 ♂ 30 ♀ / 4 ♂
Mini-Mental State Examination 29.03 ± 1.98 28.38 ± 1.61
Years of education 7.41 ± 4.44 7.94 ± 4.01
epressed elderlies (c). *p ≤ .05; **p ≤ .01
Figure 3. Mean (± SD) values of peg placement/withdrawal duration (a), errors (b) and a representation of the rate of change between peg with-
drawal duration/errors and depression intensity (BDI score) of depressed and nond
Duration (s)
Depressed
Nondepressed
**
120
110
100
90
80
70
60
50
40
30
20
10
**
a
Average of erros
**
2.5
2.0
1.5
1.0
0.5
0.0
-0.5
**
b
Placement Withdrawal
Withdrawal Time
Withdrawal Error
Linear Fit
Linear Fit
1.0
0.8
0.6
0.4
0.2
0.0
-0.2
-0.4 0 10 20 30 40 50
36
34
32
30
28
26
24
22
20
18
16
Withdrawal Time (s)
Withdrawal Errors (mean)
c
Depression Intensity (DBI Index)
Motriz, Rio Claro, v.23, n.4, 2017, e1017110 5
Motor control and depressive symptoms
Discussion
The goal of this study was to (a) distinguish motor control
between older adults with and without depressive symptoms
based on different motor requirements (placement/withdrawal
of pegs) and (b) estimate the association between the presence
of depressive symptoms, depression intensity, and interaction
effects between aging and depression intensity, with motor
control. In sum, our results showed that depressed older adults
present a general worse performance than their nondepressed
peers and the depressive symptoms were correlated with motor
control, although its intensity and the interaction between aging
and depression intensity were correlated circumstantially. This
means that depression can impair both motor control require-
ments, although its intensity as the interaction between aging
and depression intensity is related with motor control contextu-
ally. Although we didn’t have enough samples to verify if the
classication of the symptoms of BDI can distinguish motor
performance of depressed older adults, the correlations, in turn,
revealed that the intensity of the symptoms, such as the interaction
between symptom intensity and aging, are strongly associated
with a greater slowness on withdrawal of pegs performance.
The GPT, originally, involves the analysis of the placement
of small shaped key-pegs which must be oriented correctly to
t in a hole with a random orientation. Assessing the with-
drawal of these pegs, Bryden and Roy45 suggested that we can
discriminate measures of visuomotor amplitude (placement) to
a simple measurement of motor speed (withdrawal). However,
since GPT measures how quickly the 25 pegs are placed and
withdrawn, it could be argued that these tasks, in fact, cover a
hybrid control phase, which consist of both initial impulse and
current control phases, although the current control is more
robust in the placement task as it demands more accuracy from
the participant28.
Withdrawal of pins from the instrument holes, therefore,
can be interpreted as the performance of a movement in a
ballistic form to the vicinity of a target that involves mainly a
pre-programmed phase without sufcient feedback processing,
while the placement of pegs into the holes incorporates higher
visual and proprioceptive information of the limb and the target
reference point. In this manner, the GPT enables the comparison
between the execution of two similar motor tasks with different
motor requirements; or more precisely, the distinction between a
higher feedback processing versus an effortless planning process,
and their respective brain associations.
Since the withdrawal task mainly involves a planning process,
these associations can be explained by the observed depression
consequences to the frontal lobe functioning46-48. Specically,
studies have demonstrated that damage to the inferior parietal
lobe, frontal lobes, or basal ganglia hamper the performance of
tasks that require more of a planning process32,49. Furthermore,
previous ndings have also demonstrated that individuals with
depressive symptoms increase the activation of frontostriatal
circuitry as an attempt to compensate cognitive failures
50
. These
observations lead us to hypothesize that a low involvement of
the frontal lobe (e.g. working memory) on the placement task
might be responsible for the absence of signicant associations.
Furthermore, the detrimental effects to the performance of tasks
that require, predominantly, a current control phase have been
usually associated with damage on the superior parietal lobe
or cerebellum32,49. In this manner, we can infer that depression
symptoms exert a broad effect upon motor control, although their
intensity as the interaction between aging*depression intensity
are only associated with motor acts that presents higher frontal
lobe requirements.
Apparently, our results and hypothesis corroborate with
the ndings of Pier, Pier, Hulstijn and Sabbe51 who observed
signicant associations between symptom intensity and motor
control only in the task that involved, mostly, pre-programmed
components of motor planning (r=0.28, p=0.046) and with the
highest complexity task that was guided, essentially, by feedback
control (r=0.41, p=0.005). Although these associations were
made with a different clinical scale, BDI correlations on this
study presented similar results, revealing positive associations
between different performance measures (initiation time: r=0.31,
p=0.032; movement time: r=0.34, p=0.020, and re-inspection
time: r=0.32, p=0.027) with symptom intensity exclusively in
the most complex task that involved, predominantly, a current
control phase. Following the hypothesis raised by our study, the
lack of association between motor control and symptom intensity
(BDI score) revealed in the ballistic task in their study can be
explained by the absence of the aging and depression interaction
effects, while the higher association in the most complex task
can be justied by high complexity implied by the number of
segments to be copied, and thus, the increased participation of
working memory.
Despite the evident biomechanical differences between
men and women, such as the size of their ngers relative to
the size of pegs, this study didn’t reveal sex-dependent effect
between depressed and nondepressed elderlies. Surprisingly,
the results of this study contrast with those of Briden and Roy45
who revealed performance differences between the sexes dur-
ing removal/placement of pegs. However, some confounding
variables such as menopause status and menstrual cycle phase
that can promote changes in woman physiology and further
inuence motor control response of elderly women was not
controlled in our study. Therefore, the sex differences analysis
of our study might be somewhat awed and could justify the
lack of signicant results. It might also be an interesting avenue
for further investigations.
In conclusion, our study provides the rst evidence of a motor
control-dependent effect on the interaction between depression
symptoms and aging. The results herein strengthen the need to
take careful considerations in dening the requirements of a task
into the assessment of motor control of depressed individuals
as there are indirect evidences that frontal lobe dysfunctions
present a considerable association with the interaction between
aging*depression intensity as well with depression intensity
itself. Furthermore, ours ndings may have clinical implications
since the determination of mechanisms that leads to disability in
aging are extremely important for the elaboration of preventive
measures to help maintain their functional capability
52,53
. It adds
evidence to support the claim that the progression of depressive
symptoms deserves a closer look when the disorder is established.
6Motriz, Rio Claro, v.23, n.4, 2017, e1017110
Bicalho L.E.A. & Albuquerque M.R. & de Paula J.J. & Lage G.M.
Conclusion
The present ndings revealed that depressive symptoms can
impair the motor control of elderlies and revealed contextual
associations between aging and illness intensity with motor
performance. The discrimination of motor control aspects raised
by this study provides a valuable contribution to the underlying
neurophysiology of the interaction between aging and depression
symptoms, suggesting the existence of a relevant association
between frontal lobe dysfunction and motor control impairments.
These indirect measures of cerebral dysfunction can also offer
a new path to more rational approaches aimed at assessing and
elaborating of preventive measures for depressed elderlies.
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Corresponding author
Guilherme Menezes Lage
Department of Sports, School of Physical Education, Physiotherapy and Occupa-
tional Therapy, Universidade Federal de Minas Gerais, Av. Presidente Carlos Luz
6627, Pampulha - Belo Horizonte, MG - Brazil.
Email: menezeslage@gmail.com
Manuscript received on August 3, 2017
Manuscript accepted on October 1, 2017
Motriz. The Journal of Physical Education. UNESP. Rio Claro, SP, Brazil
- eISSN: 1980-6574 – under a license Creative Commons - Version 3.0
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