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Gait & Posture 40 (2014) 556–560

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Gait & Posture


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

Visual availability, balance performance and movement complexity in


dancers
Ruth Muelas Pérez a, Rafael Sabido Solana b,*, David Barbado Murillo b,
Francisco Javier Moreno Hernández b
a
Professional Dance School of Castilla y León, Burgos, Spain
b
Sport Research Centre, Miguel Hernández University of Elche, Elche, Spain

A R T I C L E I N F O A B S T R A C T

Article history: Research regarding the complex fluctuations of postural sway in an upright standing posture has yielded
Received 28 February 2013 controversial results about the relationship between complexity and the capacity of the system to
Received in revised form 12 May 2014 generate adaptive responses. The aim of this study is to compare the performance and complexity of two
Accepted 30 June 2014
groups with different levels of expertise in postural control during a balance task. We examined the
balance ability and time varying (dynamic) characteristics in a group of 18 contemporary dancers and 30
Keywords: non-dancers in different visual conditions. The task involved maintaining balance for 30 s on a stability
Balance ability
platform with opened or closed eyes. The results showed that dancers exhibited greater balance ability
Complexity
Dance
only in open eyes task than non-dancers. We also observed a lower performance in both groups during
Visual information the test with closed eyes, but only dancers reduced their complexity in closed eyes task. The main
conclusion is that the greater postural control exhibited by dancers depends on the availability of visual
information.
ß 2014 Elsevier B.V. All rights reserved.

1. Introduction Keshner showed the benefits of a balance-training program, in


which the unhealthy participants improved their postural control,
Postural control during the maintenance of an upright standing and the complexity of postural sway was increased [14].
posture is a fundamental motor act that provides the basis for By applying different levels of difficulty, depending on the
locomotion and most other movement tasks [1]. The postural availability of visual information, studies have shown a reduced
control system regulates the body’s postural sway during upright performance associated with less postural sway complexity when
standing through the complex interaction of somatosensory, visual the subjects kept their eyes closed [11,15]. However, some authors
and vestibular sensory feedback networks, numerous brain state that, depending on the specialization of the sample in
regions, and the musculoskeletal system [2–4]. Complexity is proprioceptive tasks, the decrease in performance will generally be
defined as the number of system components and coupling significant. Some results have shown that gymnasts only worsen
functions (interactions) among the components [1]. This complex- their performance on stability tasks with closed eyes compared to
ity can be observed in the upright standing posture through another group of athletes [16].
fluctuations of postural sway [4–6] and has increasingly led However, other studies appear to be inconsistent with this
scientists to analyze postural stability through non-linear mathe- relationship between performance and system complexity. Some
matical tools [7–11]. age-related studies have observed a greater complexity of the
The results observed through this type of analysis have allowed system related to worse performances on postural control tasks
scientists to relate lower complexity levels to a worse performance [9,10]. High levels of complexity may indicate that the system is
[12] related to aged and unhealthy systems [13]. Haran and becoming less sustainable. This assumption is close to the
traditional interpretation of variability as a measure of disorder
and noise [10].
The relationship between complexity and performance in
* Corresponding author at: Sport Research Centre of Elche, Miguel Hernández balance tasks has been previously analyzed in dancers. Stin
University, Avda. de la Universidad s/n, 03202 Elche, Spain. Tel.: +34 965 22 24 37; et al. have observed that young dancers exhibit greater postural
fax: +34 965 22 24 56.
E-mail address: rsabido@umh.es (R. Sabido Solana).
control with greater complexity compared to other groups of

http://dx.doi.org/10.1016/j.gaitpost.2014.06.021
0966-6362/ß 2014 Elsevier B.V. All rights reserved.
R. Muelas Pérez et al. / Gait & Posture 40 (2014) 556–560 557

participants without experience in balance skills [7]. However, The participants were instructed to adopt a shoulder-width
Schmit et al. did not observe differences in postural control stance with their arms held at their sides. The participants were
between dancers and track athletes [11]. These authors observed further directed not to speak during the trials. At the beginning of
differences in behavioral complexity between both groups with each trial, the participants assumed the aforementioned stance.
greater complexity or irregularity in the postural stability of Data collection was initiated after the participants felt comfortable
dancers. Schmit et al. argued that there is a qualitative difference, and ready. The participants were allowed to rest for 3 min between
rather than quantitative, in the balance task between these two the conditions.
groups [11]. To ensure that there was no rest of vision during the closed eyes
Because of the controversy in the results, the aim of this study condition, all participants placed an ocular mask on their face.
was to evaluate the relationship between complexity and
performance through a comparison of two groups of different 2.4. Data analysis and reduction
levels of expertise in postural control (dancers and non-dancers),
and two levels of availability of visual information during a balance Data obtained from electrogoniometer was subsampled to
task. The following are the hypotheses of this study: (1) expert 100 Hz. To evaluate the performance in postural stability, the
dancers will show greater complexity and a better performance absolute error of the tilt platform was measured as the average of
during the balance task than non-dancers in both visual conditions, the absolute distance (AE) to the horizontal angle of the platform.
and (2) both groups will show a greater complexity with a better In addition, we assessed participant’s balance control trough the
performance in the balance task when visual information is standard deviation (SD) and mean velocity (MV).
available. Non-linear time series analysis was applied to the angular
displacement of the platform. The complexity of the postural sway
dynamics was calculated by two methods: Sample Entropy
2. Method (SampEn) and Permutation Entropy (PE). Higher values of SampEn
thus represent lower repeatability of vectors of length m to that of
2.1. Participants m + 1, which marks a lower predictability of future data points and
a greater irregularity within the time series. SampEn was
Eighteen undergraduate dancers (all females) from the Spanish performed using the following input parameters for the analysis
Royal Conservatory of Dance and thirty healthy young women algorithms: 0.15 for tolerance (r) (in proportion to the SD of the
without any experience in dance participated in the study. All signal) and 2 for vector length (m). The selection of these values
dancers were specifically trained in contemporary dance and ballet was based on the procedures suggested by Cavanaugh et al. [18].
for a minimum of five years. The remaining thirty women served as We have included PE to reduce the influence of the magnitude of
a control group and were not explicitly trained in balance tasks. the time series, and therefore the influence of the tolerance
The participants signed a written informed consent document window parameter. Permutation entropy is independent of the
prior to the experimental session. Table 1 shows the descriptive data magnitude because it measures the entropy of sequences of
data, including age, weight and height of the sample. The study ordinal patterns derived from m-dimensional delay embedding
protocol was approved by the ethics committee of Extremadura vectors [19]. PE was performed using 5 for vector length (m).
University. In order to assess the robustness of SampEn and PE method, we
have applied them modifying input parameter: SampEn was
2.2. Performance task and apparatus applied on angular displacement signal using different r (0.15, 0.20
and 0.25 in proportion to the SD of the signal) and m (2, 3 and 4). PE
The performance task used to measure balance ability was a was applied modifying m from 4 to 6. Higher r and m values
stabilometer (Model 16020, Lafayette Instrument Inc., Lafayette, increased entropy output. Nevertheless its influence seems similar
IN), in which the tilt angle, recorded by a SMEG330 electro- in all conditions and does not affect result interpretation.
goniometer (1-KHz data collection rate) represented the criterion
measure. The tilt angle was the participant’s error score reflecting 2.5. Statistical analysis
deviation (medio-lateral) from the target horizontal platform
position (08). Normality of the data distribution was evaluated by calculating
The stabilometer platform (0.66 m  1.08 m  0.025 m) was asymmetry, kurtosis and the Kolmogorov–Smirnov method with
placed 0.16 m from the frame and 0.22 m from the floor. The range the Lilliefors correction. All variables were normally distributed. A
of the stabilometer was set to 208 from a horizontal position. The mixed-design analysis of variance (ANOVA) was performed to test
stabilometer task has been shown as a valid and reliable measure of the mean differences between the two groups (dancers and
balance [17]. control), vision conditions (repeated measures factors) and
interactions. A post hoc analysis with a Bonferroni adjustment
2.3. Procedure was used for multiple comparisons. Pearson’s correlation coeffi-
cient tested for correlations between the variables of the present
The participants were asked to stand barefoot on the platform study. Significance was established at p < 0.05. SPSS 16.0 (SPSS Inc,
maintaining stability from the horizontal position for 30 s in two Chicago, IL, USA) was used for all statistical procedures.
visual conditions: open eyes (OE) and closed eyes (CE). The order of
the conditions was randomized between the participants.
3. Results

Table 1 An example of a medio-lateral deviation of the platform tilt angle from the target
Descriptive and anthropometric data of all participants. horizontal position (08) for dancers and non-dancers in both visual conditions is
shown in Fig. 1. Higher medio-lateral deviations can be observed in the CE condition
Group Age (years) Weight (kg) Height (cm) compared to OE condition. The data from the dancer performance show lower
(average  SD) (average  SD) (average  SD) deviation than non-dancer mainly in the OE condition.
Table 2 shows the relationship between the AE, SD and MV of the tilt platform
Dancers 23.32  2.58 65.73  7.96 171.91  7.02
and the vision conditions. All the participants performed significantly better in the
Non-dancers 22.23  1.79 65.94  10.53 169.97  7.56
balance task in the OE condition compared to the CE condition. Both groups
[(Fig._1)TD$IG]
558 R. Muelas Pérez et al. / Gait & Posture 40 (2014) 556–560

Fig. 1. An example of the medio-lateral deviation of the platform tilt angle from the target horizontal position (08) for dancers and non-dancers in both visual conditions.

increased their values in AE, SD and MV when standing on the platform in the CE The analysis of the complexity of the tilt platform excursion showed significant
condition. Regarding the differences between the groups (Table 3), the dancers main effects for the visual condition in SampEn and for group in PE (Table 2).
showed better postural stability (lower absolute error and standard deviation) than Nevertheless, the interaction effects indicate that the visual conditions affect the
non-dancers only in the OE condition (p < 0.05). Furthermore, MV was higher in groups differently. Pairwise comparisons showed lower entropy values for dancers
dancers in both conditions (p < 0.05). in CE condition compared with OE condition. In addition, dancers exhibited lower
entropy than non-dancers in CE condition. The results indicate that dancers exhibit

Table 2
Mixed ANOVA testing mean differences between the dancers and non-dancers Table 3
(group) and the repeated measures factors of visual condition (vision) and Mean and standard deviations of absolute error along the medio-lateral axis (AE),
interaction. standard deviation (SD), mean velocity (MV), sample entropy (SampEn) and
permutation entropy (PE) for dancers and non-dancers in the two visual conditions.
F1,46 P
N Open eyes Closed eyes
AE Vision 48.187 .001
Group 3.313 .075 AE ND 30 11.45  1.11a 12.57  1.30B
Vision  group 2.256 .140 D 18 10.61  1.13 12.34  1.24B

SD Vision 37.538 .001 SD ND 30 12.85  1.60A 13.74  1.61B


Group 6.758 .013 D 18 11.45  1.02 13.41  0.81B
Vision  group 6.845 .012
MV ND 30 40.82  11.69a 43.94  11.11A
MV Vision 7.793 .008 D 18 33.67  5.86 36.01  3.45b
Group 7.962 .007
Vision  group .120 .731 SampEn ND 30 0.094  0.030 0.082  0.037a
D 18 0.096  0.028 0.058  0.024B
SampEn Vision 19.108 .000
Group 2.288 .137 PE ND 30 0.58  0.12 0.60  0.10A
Vision  group 5.804 .020 D 18 0.54  0.06 0.44  0.07B
a
Different from the dancers using the Bonferroni correction. Pairwise compari-
PE Vision 3.064 .087
son, p < .05.
Group 13.324 .000 A
Different from the dancers using the Bonferroni correction. Pairwise
Vision  group 24.708 .000
comparison, p < .01.
B
AE, absolute error; SD, standard deviation; MV, mean velocity; SampEn, sample Different from the open eyes condition using the Bonferroni correction.
entropy; PE, permutation entropy. Pairwise comparison, p < .01.
R. Muelas Pérez et al. / Gait & Posture 40 (2014) 556–560 559

lower complexity, lower entropy values, when visual information is not available performance but in their system flexibility to adapt to different
(Table 3).
situations of postural control [11]. Thus, the differences would be
The results of the correlation analysis performed on the sample of non-dancers
showed that there is a positive relationship between AE (r = .465, p < .05), SD more qualitative than quantitative. For this reason, we might have
(r = .504, p < .01) and MV (r = .786, p < .01) in the OE and CE conditions. Thus, the only observed differences between both groups in their behavioral
higher the performance stability test in OE condition, the greater the performance complexity during the balance tasks in CE conditions, where
stability test in CE condition. However, the performance of dancers between the two difference in the performance between the groups practically
stability tests is not significantly correlated. The better performance of the dancers
in the OE condition is not associated with a higher yield in the test with CE.
disappears. Sensory deprivation increases the difficulty of the task,
Comparing the absolute error of the platform angle with the complexity and the group of dancers changed their behavior, freezing their
measured through SampEn, the results in the dancer group showed negative degrees of freedom in a reduced effectiveness of their strategy to
correlations between the AE and complexity of the tilt angle for both conditions. stabilize and prevent falls, thus resulting in lower values of entropy
This behavior is exhibited in both the OE (r = .605, p  .01) and CE conditions
[31].
(r = .711, p  .01). Similar correlations has been observed between SampEn and SD
in OE condition (r = . 483, p < .05) and CE condition (r = .807, p < .01). Thus, as Regarding the relationship between complexity and perfor-
the complexity increases, the performance improves, regardless of the availability mance, we have found contradictory results. On the one hand,
of visual information. The non-dancers also showed these negative correlations in correlation analysis in both groups showed that the participants
both conditions between AE and SampEn (OE: r = .579, p < .01; CE: r = .594, with higher complexity exhibited higher performance regardless
p < .01), and between SD and SampEn (OE: r = .602, p < .01; CE: r = .648,
p < .01).
of the availability of visual information. On the other hand, even
though dancers exhibited better performance than non-dancers in
OE, they there was not differences in complexity between groups.
4. Discussion In addition, the decrease in performance of non-dancers in the CE
condition compared to OE condition was not related to lower
The results are consistent with other studies in which behavioral complexity. In this regard, the relationship between
performance on the stability test in the OE condition was better performance and complexity is not linear or is mediated by other
than the performance in the CE condition [11,15,20]. Moreover, variables [1]. Some authors suggested that an increase in entropy
and partially confirming the first hypothesis, the group of dancers variables is not necessarily synonymous with an increase in
performed better only on the balancing task with OE. These results physiologic complexity [13] and the relationship between entropy
may be because of the increased specialization of dancers in tasks variables and physiologic complexity is not linear. In this sense,
in which postural control is regulated through visual feedback according with Stergiou and Decker, there would be inverse U-
[11,21,22]. Rist states that dancers are used to regulate their shape relationship between entropy variables and complexity [32].
posture through visual information from the initial moment of In summary, the differences in balance ability between dancers
learning [23]. Teasdale et al. claim that a specialization in learning and non-dancers are only meaningful in the OE condition, thus
leads to a specialization in the information channel used in indicating that the best performance in the former group is coupled
execution [24]. Thus, the greater the visual information used with the use of information from vision to control balance
during the learning process, the greater the decrease in perfor- adjustments. The deprivation of visual information increases the
mance when vision is removed [25]. This idea was also observed by difficulty of the task, which is more significant in dancers because
Gerbino et al., who observed highly significant reductions in the of their specialization in learning through visual information.
balance performance of dancers in the CE condition [26]. Decreases in the complexity of postural control in the dancers
Our results show that the deprivation of visual information entail a decrease in performance. These results may be observed
matches the performance of both groups in the balance task. These because of specific strategies developed to control a novel balance
results confirm the dependence of dancers on visual information to tasks. The non-linear analysis methods allow us to explain both the
regulate their posture, as argued by other authors in several studies differences observed between the different levels of difficulty in
[21,27]. Kavounoudias et al. suggested that superficial plantar the balance tasks and those observed between the different levels
mechanoreceptors provide the CNS with information relative to of expertise in the participants.
the position of the body with respect to the vertical reference [28].
Exclusion of the vision would render the CNS rely on vestibular and
proprioception systems. Perrin et al. argued that dance training Conflict of interest statement
strengthens the accuracy of proprioceptive inputs in a lower way
than other sports [27], developing specific modalities of balance There are no financial or personal relationships between any of
not transferable to posture control in CE situations [21]. the authors and other people or organizations that could
In relation to the entropy values, opposed to the hypothesis, the inappropriately influence this study.
group of dancers shows lower behavioral complexity than non-
dancers during the tasks only in the CE condition. Indeed,
comparing both visual conditions, only the dancers entropy values References
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