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Brazilian Journal of Motor Behavior
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“Fatigue issue in the performance of motor skills”
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Rinaldin et al.
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Does footedness affect bilateral plantar flexor responses to sudden stance
perturbations under unilateral lower leg muscular fatigue?
CARLA D. P. RINALDIN
1
| JÚLIA Á. OLIVEIRA
2
| CAROLINE R. SOUZA
2
| DANIEL B. COELHO
2,3
| LUIS A. TEIXEIRA
2
1
Graduate Program on Health Technology, Pontifical Catholic University of Paraná, Curitiba, PR, Brazil
2
Human Motor Systems Laboratory, School of Physical Education and Sport, University of São Paulo, São Paulo, SP, Brazil
3
Biomedical Engineering, Federal University of ABC, Santo André, SP, Brazil
Correspondence to:!Carla D.P. Rinaldin.
St. Imaculada Conceição, 1155, Prado Velho, Curitiba, Paraná, Brazil, 80215-901. Phone.: +55 41 9 9937-6390
email: rinaldin99@gmail.com
https://doi.org/10.20338/bjmb.v17i5.381
HIGHLIGHTS
• Bilateral plantar flexors’ activation under unilateral
fatigue of the dominant leg.
• Higher activation of a non-fatigued muscle to
compensate for contralateral fatigue.
• Footedness had no effect on reactive muscular
responses regardless of fatigue.
ABBREVIATIONS
Dom Dominant
LG Lateral gastrocnemius
MG Medial gastrocnemius
MVC Maximum voluntary contraction
N-dom Non-dominant
n
p
2
Partial eta squared
RMS Root mean square
SOL Soleus
PUBLICATION DATA
Received 28 07 2023
Accepted 08 09 2023
Published 30 09 2023
BACKGROUND: Analysis of performance asymmetries has indicated that the right and left
cerebral hemispheres are specialized for specific functions of motor control.
AIM: In the current investigation, we aimed to evaluate the effect of leg dominance on
electrical activation of the plantar flexor muscles in responses to unanticipated stance
perturbations in a state muscular fatigue of the dominant leg.
METHOD: Fatigue was induced through ankle isometric contraction targeting 40% of
maximum voluntary contraction. Muscle activation of the triceps surae of the dominant and
non-dominant legs were compared in reactive responses to unanticipated load released from
the trunk, leading to forward body sway. Muscular responses were analyzed in two states:
pre-fatigue and fatigue of the triceps surae muscles of the dominant leg only.
RESULTS: Analysis of magnitude of muscular activation for balance recovery following
perturbations revealed fatigue-related compensatory activation in the lateral gastrocnemius
muscle, as indicated by over-activation of the non-fatigued/non-dominant leg to compensate
for the low muscular activation of the dominant/fatigued leg in the unilateral fatigue state.
CONCLUSION: Compensatory behavior between the legs was not evident in the medial
gastrocnemius and soleus muscles. Lack of effects related to leg dominance indicates that
footedness did not affect automatic muscular responses either in the pre-fatigue or fatigue
states.
KEYWORDS: Laterality | Leg dominance | Balance perturbation | Muscular fatigue |
Electromyography
INTRODUCTION
Analysis of intermanual performance asymmetry has indicated that the right and left cerebral hemispheres are specialized for
distinct functions of motor control. Sainburg
1
has proposed that the dominant hemisphere is specialized for dynamic control,
characterized by a higher ability to predict the interactive muscular and external torques in voluntary movements. The non-dominant
hemisphere is proposed to be specialized for impedance control, characterized by more effective neuromotor mechanisms leading to
maintenance of a stable posture. From this conceptualization, hemispheric specialization should be seen not only in upper but also lower
limb movements, chiefly in the limb contralateral to a given cerebral hemisphere
2,3
. From this proposition, one could expect that upright
balance control would be better performed through the right hemisphere specialization for impedance control. This assumption has been
supported in the evaluation of individuals who suffered unilateral stroke, with findings of impaired quiet and perturbed body balance in
cases of right but not left hemisphere damage
4
, associated with weaker muscular responses in the contralateral left leg
5
.
Contrary to results in individuals who suffered uni-hemispheric stroke, analysis of interlateral asymmetries of balance control in
healthy people have indicated predominance of symmetric performance between the right and left legs. In one of the earliest studies
addressing this issue, Hoffman et al.
6
compared balance stability between the legs in healthy young adults, evaluating quiet stance on a
force plate. They found that center of pressure variability under the feet soles was equivalent between the right and left legs. Further
investigation corroborated equivalent balance stability between the legs in quiet standing
7
, in addition to interlateral symmetric
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coordinative structure
8
and muscular activation
9
. Similar findings of symmetric balance control between the legs has been observed also
in more challenging conditions of unstable support base
10
, dynamic balance
11
, and in response to balance perturbations
12
. Prevalence
of symmetric performance between the legs in healthy young and older individuals in the control of static and dynamic balance tasks was
the major conclusion from a recent systematic review and meta-analysis
13
.
Exceptions to the conclusion of symmetric balance between the legs have been found in specific tasks requiring dynamic
interactive control between the lower limbs. King and Wang
14
examined interpedal asymmetry in the tasks of quiet single leg stance and
in goal directed kicking. Results showed that in quiet unipedal standing performance was symmetric between the legs. Conversely,
supporting the body on the right leg while using the left leg to kick a ball led to greater variability of the center of pressure in the
mediolateral direction than when the legs played the opposite roles. Interpedal balance asymmetry was also observed in tennis players
when performing a landing task following stepping out a support base 40 cm above the ground with the opposite leg
15
. Results showed
shorter time for stabilization of mediolateral center of pressure in the dominant than in the non-dominant legs (see also Yiou et al.
16
).
These findings support the assumption that interpedal balance asymmetries can be detected in conditions in which the two legs interact
asymmetrically for maintenance of balance stability. In this regard, Rinaldin et al.
17
developed a unipedal fatigue protocol for analysis of
reactive postural responses that is able to produce a context of asymmetric muscular activation between the fatigued and non-fatigued
legs, given that muscular fatigue characterized by a decreased maximal capacity to generate force or power output
18
. Rinaldin’s results
showed compensation for the weaker response magnitude of the fatigued leg by an increased response magnitude of the non-fatigued
leg. Furthermore, the descriptive data suggested that in the pre-fatigue state the non-dominant leg achieved higher muscular activation
magnitude when compared to the dominant one. However, in that experiment the effect of leg dominance was not evaluated. This result
raises the possibility that leg dominance affects fatigue-related compensatory control between the legs in automatic postural responses.
Addressing this issue could unveil the extent to which leg dominance affects between-leg compensatory muscular activation. The current
investigation aimed to conduct a secondary analysis of Rinaldin et al.’s
17
data to evaluate the effect of leg dominance on electrical
activation of the plantar flexor muscles in responses to unanticipated stance perturbations in a state muscular fatigue of the dominant leg.
Based on the conceptualization that the non-dominant hemisphere is specialized for impedance control, it was tested the hypothesis of
increased compensatory reactive responses in the non-dominant than the dominant leg in the state of unilateral muscular fatigue.
METHODS
Participants
Eighteen (8 women and 10 men) physically active individuals participated of this experiment, with mean age 24.05 years (SD =
4.70), mean height 170.83 cm (SD = 8.54), and mean weight 69.61 kg (SD = 14.01). The inclusion criteria were absence of joint or
muscle injuries to lower limbs, neurologic dysfunctions, or consumption of medications that might affect their body balance, as self-
declared. The exclusion criteria was incapacity to perform the experimental task following muscular fatigue (no participants were
excluded). Participants provided informed consent, according with the experimental procedures approved by the Research Ethics
Committee of the University of São Paulo (São Paulo, Brazil, approval reference number 3.047.974), in conformity with the ethical
standards laid down by the Declaration of Helsinki. This work is a secondary analysis of a previous published study
17
, that explored
between-leg asymmetry in the production of automatic postural responses to a sudden balance perturbation.
Task and equipment
The postural task was upright bipedal standing with eyes open while resisting against a load pulling the participant’s trunk
backwards. The task consisted of recovering stable upright stance following a perturbation caused by sudden release of the load, leading
to involuntary forward trunk displacement. Loading corresponded to 8% of participant’s body weight. The load applied through a harness
worn at the lumbosacral region connected to the pulling load. The load was connected to the harness backside by means of a steel
cable, being released through a soundless electromagnetic system (for details, see Lima-Pardini et al.
19
). Ensuing a verbal prompt, the
load was released through a remote switch in a time unbeknownst to the participant. The task aim was to recover balance stability
following load release without moving the feet. For evaluation of muscular activation, wireless surface electrodes (Delsys Inc., Boston,
MA, model Trigno) were used, positioned on both legs of the triceps surae muscles: lateral gastrocnemius (LG), medial gastrocnemius
(MG) and soleus (SOL), according to the SENIAM project recommendations (http://www.seniam.org). Data acquisition was made through
the Vicon system (Nexus 2.7).
Evaluation of leg dominance was made through a short version of the Waterloo Footedness Questionnaire
20
including balance
tasks only. To provoke fatigue of the triceps surae muscles, participants applied isometric plantar flexion torque at the ankle of the
dominant leg for balance tasks in the standing posture. During the fatiguing activity, the contralateral non-dominant leg was kept relaxed,
lightly touching the support surface. The heels were supported on the base of a custom-made support base (individual for each foot)
equipped with load cells. Target ankle torques was 40% of maximum voluntary contraction (MVC). The actual and the target torque
(normalized by MVC) were displayed on a frontal monitor as feedback. The experimental setup is represented in Figure 1.
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Figure 1. Representation of the experimental setup: (A) equipment used to induce fatigue of the plantar flexor muscles and to measure maximum
voluntary contraction (MVC); (B) ankle of the dominant lower limb for balance tasks attached to the support base; (C) amplifier electrical circuit; (D)
provision of visual biofeedback about torques applied at the ankle. The arrow indicates positioning of EMG electrodes.
Experimental design and procedures
Participants were divided into two groups according to individual lower limb dominance for balance tasks: eight were left-footers
(left group) and 10 right-footers (right group). To test the effect of muscular fatigue of the dominant leg between left- and right-footers on
bipedal responses to stance perturbations, evaluations were conducted over two states, in the following sequence: (a) pre-fatigue,
immediately before the fatiguing activity; and (b) under muscular fatigue of the dominant leg. In each state, reactive responses were
evaluated through 10 trials of stance perturbation through load release. However, for this study, the first trial of the pre-fatigue and of the
under-fatigue states were used only. Intertrial intervals were about 15 s, with the whole series of perturbations lasting approximately 3
min. Anticipation of load release was prevented by means of variable intervals of 2-5 s between the verbal prompt and perturbation onset
(see Rinaldin et al.
17
for a detailed description).
To determine load magnitude for muscular fatiguing, torque achieved in MVC of the fatiguing leg was measured in three trials.
The highest value across trials was considered for the calculation of MVC 40% for the fatigue protocol. For MVC assessment, the
corresponding EMG signals from the MG, LG and SOL muscles were measured for normalization purposes (maximum value between
trials).
During the fatiguing activity, plantar flexion isometric contraction was maintained for a time length in which participants were
able to sustain torque application. When the applied torque fell below the individual target, participants were motivated to keep applying
torque. They rated their subjective fatigue state every minute, based on the Borg scale
21
. The fatiguing activity was interrupted when the
participant reported maximum score in the Borg scale and failed to maintain at least 5% of MVC during a continuous interval of 30 s. To
prevent fatigue dissipation, the interval between the end of the fatiguing activity and under-fatigue probing trials was about 10 s.
Data collection and analysis
The sampling frequency for EMG data was set at 2 KHz. Raw data were processed through Matlab (Mathworks, Natick, MA)
routines. Electromyography signals were amplified with a gain of 1000, and digitally band-pass filtered through a dual-pass fourth-order
Butterworth filter in the 20-400 Hz window.
For statistical analysis, the time interval of 200 ms before load release was taken as reference of the resting state. Magnitude of
muscle activation was analyzed as the dependent variable, as indicated by the root mean square (RMS) of the normalized EMG signal in
the time window of muscle activation onset (two standard deviations above the resting state) up to the ensuing 150 ms
22
. To test for data
distribution normality, the Shapiro-Wilk test was used, and to test for sphericity the Mauchly test was used. Data analysis was made
separately for the LG, MG and SOL muscles by means of three-way 2 (group: footedness [right x left leg dominance]) x 2 (leg: dominant
x non-dominant) x 2 (fatigue: pre-fatigue x under fatigue) general linear model ANOVAs with repeated measures on the last two factors.
Post hoc comparisons were made through Bonferroni procedures. Analyses were performed through the Statistica software (version 7.0,
Statsoft). Statistical significance was set at p < 0.05. Effect sizes are given by partial eta squared (η
p
2
), considering values as small (<
0.06), moderate (>0.06-0.14) and large (>0.14)
23
.
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RESULTS
As a description of the fatiguing activity, the average duration time of plantar flexion isometric contraction across participants
was 33.38 min. (SD = 15.82). All participants reported having reached the maximum fatigue score on the Borg scale. From this report, it
can be assumed that the fatiguing activity led to full exhaustion of the plantar flexor muscles. Part of data failed to show normal
distribution. However, failure to achieve normal data distribution has been shown to do not impair results interpretation from analyses
based on F-tests
24
. When sphericity assumptions were violated (p <0.05), the Greenhouse–Geisser correction
25
was used.
Analysis of LG activation magnitude showed a significant main effect of leg
a
, [F(1, 15) = 4.94, p = 0.04, η
p
2
= 0.25], and a
significant leg by fatigue interaction, [F (1, 15) = 9.95, p = 0.006, η
p
2
= 0.40]. Post hoc comparisons indicated significantly lower values of
the fatigued compared to the non-fatigued leg in the under-fatigue state (p = 0.006), mean delta = 25.06 (SD = 6.28) (Figure 2A). Results
for magnitude of the MG muscle activation showed a significant main effect of leg [F (1, 16) = 10.39, p = 0.005, η
p
2
= 0.40]. This effect
was due to lower values for the dominant than the non-dominant leg, mean delta = 16.24 (SD = 4.67) (Figure 2B). Analysis of SOL
activation magnitude showed no significant main or interaction effects (p values > 0.1) (Figure 2C).
Figure 2. Normalized magnitude of muscular activation. Mean and standard errors (vertical bars) are shown for the medial gastrocnemius (MG), lateral
gastrocnemius (LG) and soleus (SOL) muscles. Comparison between the dominant (Dom) and non-dominant (N-dom) legs over the pre-fatigue and
under fatigue states between groups of right- and left-footers. Statistically significant differences are indicated through asterisks.
!
a
There was a failure in the recording of part of data from one participant for LG. The analysis for this muscle was conducted on 17 participants.
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DISCUSSION
The current investigation aimed to evaluate the effect of leg dominance on muscular responses to stance perturbations in a
state of fatigue of plantar flexor muscles of the dominant leg. Our results revealed fatigue-related compensatory activation in the LG
muscle, as indicated by a higher activation of the non-fatigued (non-dominant) as compared to the fatigued (dominant) leg in the fatigue
state. A leg effect was found for the MG muscle, with higher activation of the non-dominant than the dominant leg regardless of muscular
fatigue state. While this was a result associated with leg dominance, it seems to have not being specific to the effects of fatigue, and thus
will not be further discussed. Lack of significant effects for the SOL muscle in the generation of reactive postural responses showed low
sensitivity of this muscle to our experimental manipulations. The differential participation of the three muscles is consistent with previous
analyses of the roles played by each muscle of the triceps surae in equivalent conditions of body balance perturbation
26,27
. Absence of
effects related to group indicates that footedness had no effect on automatic muscular responses either in the pre-fatigue or in the fatigue
state.
Compensatory control between the legs
Our results of a higher activation of the non-fatigued than the fatigued leg for the LG muscle under fatigue showed an
asymmetric activation between these homologous muscles, differently from the equivalent activation observed in the pre-fatigue state.
Although analysis showed lack of interaction associated with the fatigue state, descriptive data suggest that asymmetric muscular
activation for the LG muscle under unilateral fatigue was due to an over-activation of the non-fatigued leg combined with a weak
muscular activation of the fatigued leg. It is interesting to note that increased muscular activation of the non-fatigued leg in the fatigue
state is contradictory with a cross-over effect of muscle fatigue on the contralateral limb reported in previous investigation
28
. From this
point, we suggest that the higher activation of the non-fatigued LG muscle in the very first trial in the fatigue state was functional to
compensate for the decreased activation contralateral homologous muscle, suppressing a possible cross-over effect of muscular fatigue.
We conceptualize that the current findings support the conjecture that in the condition of unilateral fatigue of the plantar flexor muscles,
homologous muscles of the non-fatigued leg are over-activated to preserve the required power of the global muscular response to
achieve the task aim of maintaining upright stance. Based on this assumption, it can be conceived that at the cortical level of balance
control each cerebral hemisphere is able to send individualized motor drives to the contralateral leg, so that both legs work in a
complementary way as a functional unit
29
. Accordingly, the current results of between-leg compensatory LG activation in the condition of
unilateral fatigue suggest that the descending motor drives are scaled differently for the muscles of the fatigued and non-fatigued legs
based on their individual capacity to respond to the perturbation of upright balance.
An additional point of interest was that the compensatory behavior of the LG muscle between the legs took place in the very
first muscular response in the fatigued state. This result is consistent with our previous findings of first trial rescaling of hip and ankle
movements following fatiguing of both legs in automatic postural responses
30
. By considering that on the first trial following the fatiguing
activity there was no feedback available on the respective impairment of the postural response, it seems that the central nervous system
was able to anticipate the consequence of unilateral muscular fatigue on the reactive responses. Compensatory muscular activation
between homologous muscles without prior experience can be explained by an internal forward model predicting the consequences of
unilateral muscular fatigue and guiding the magnitude of the over-activation of the non-fatigued leg
31
.
Symmetric responses between the dominant and non-dominant legs
The main objective of this investigation was to evaluate possible implications of footedness to automatic postural responses in
a condition of unilateral leg fatigue of the plantar flexor muscles. Based on the conceptualization that the non-dominant hemisphere is
specialized for impedance control
1
, and that respective behavioral consequence is manifested mainly in the contralateral body side
2,3
,
one could expect differential compensatory responses between the dominant and non-dominant legs. Given that handedness and
footedness have distinct interindividual profiles
32
, groups of right- and left-footers were compared to evaluate potential laterality-related
effects. Our results showed lack of effects of leg dominance on reactive responses under unilateral fatigue, refuting our hypothesis of
increased compensatory reactive responses in the non-dominant than the dominant leg in the state of unilateral muscular fatigue. On the
other hand, the current results are consistent with prevalent findings of symmetric control between the legs for body balance control
13
.
Closely related to the muscular responses required in our experiment, Vieira et al.
12
showed that reactive responses in unipedal stance
were symmetric between the legs in onset delay for muscular activation following a sudden stance perturbation
33
. Previous comparisons
between the legs in the performance of tasks with different levels of difficulty failed to show asymmetries in balance stability
10
and in
lower leg muscular responses
9,34
. Results of symmetric muscular responses between the legs are congruent with findings of bilateral
activation of the primary sensory and motor areas
35,36
and dorsolateral prefrontal cortices
37
during feet-in-place reactive responses to
balance perturbations. Symmetric bi-hemispheric activation in the production of reactive postural responses lend support for a bi-
hemispheric cortical participation in response generation. Such a bi-hemispheric cortical activation in the primary sensory and motor
areas may indicate that both cerebral hemispheres participate in body balance control. Given that upright balance requires control of the
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whole body rather than only of the lower limbs, it is plausible that laterality in stance regulation is manifested differently from motor
asymmetries seen in the upper limb movements
38
. We underscore that to keep the center of mass over the support base all body
segments have to be controlled in coordination, involving the regulation of right and left body sides, and so requiring participation of both
cerebral hemispheres. Additionally, balance control requires a large participation of sub-cortical structures, like cerebellum and basal
ganglia, while inter-lateral asymmetries have been evidenced in voluntary manual movements being regulated mainly by cerebral cortical
areas
39
. In this sense, it is possible that lack of effect of footedness is due to a reduced lateralization of balance control, with each
cerebral hemisphere participating in the muscular activation of both the dominant and non-dominant legs.
Limitations
As a main limitation, it was not feasible to estimate if asymmetric weight-bearing preceding and during stance perturbations due
to muscular fatigue
17
affected the magnitude of muscular responses in the dominant and non-dominant legs.
CONCLUSION
Our results support the following conclusions: (1) footedness had no effect on muscular activation when responding to
unanticipated stance perturbations, with equivalent results between right- and left-footers; and (2) in the fatigue state, the LG muscle of
the non-fatigued leg presented higher activation than the homologous muscle of the fatigued leg, suggesting a compensatory control
between the fatigued and non-fatigued legs to preserve upright stance.
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Citation: Rinaldin CDP, Oliveira JA, Souza CR, Coelho DB, Teixeira LA. (2023).!Does footedness affect bilateral plantar flexor responses to sudden stance perturbations
under unilateral lower leg muscular fatigue?. Brazilian Journal of Motor Behavior, 17(5):186-192.
Editor-in-chief: Dr Fabio Augusto Barbieri - São Paulo State University (UNESP), Bauru, SP, Brazil. !
Associate editors: Dr José Angelo Barela - São Paulo State University (UNESP), Rio Claro, SP, Brazil; Dr Natalia Madalena Rinaldi - Federal University of Espírito Santo
(UFES), Vitória, ES, Brazil; Dr Renato de Moraes – University of São Paulo (USP), Ribeirão Preto, SP, Brazil.
Guest editors: Dr Bruno Bedo – University of São Paulo (USP), São Paulo, SP, Brazil; Dr Carlos Augusto Kalva-Filho - São Paulo State University (UNESP), Bauru, SP,
Brazil. !
Copyright:© 2023 Rinaldin, Oliveira, Souza, Coelho and Teixeira and BJMB. This is an open-access article distributed under the terms of the Creative Commons
Attribution-Non Commercial-No Derivatives 4.0 International License which permits unrestricted use, distribution, and reproduction in any medium, provided the original
author and source are credited.
Funding: This work was supported by Brazilian agencies, CNPq (grant number 306323/2019-2), and CAPES.
Competing interests: The authors have declared that no competing interests exist.
DOI:!https://doi.org/10.20338/bjmb.v17i5.381