Gait & Posture 39 (2014) 397403

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Gait & Posture

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Neck musculature fatigue affects specic frequency bands of postural

dynamics during quiet standing
Zhiqi Liang a,*, Ross Clark b, Adam Bryant b, June Quek a, Yong Hao Pua a
a
Department of Physiotherapy, Singapore General Hospital, Singapore, Singapore
b
School of Exercise Science, Australian Catholic University, Fitzroy, Victoria 3065, Australia

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

Article history: Proprioceptive input from the neck is important for maintenance of upright standing. Although neck
Received 23 November 2011 musculature fatigue has been demonstrated to impair standing balance, there is limited understanding
Received in revised form 5 July 2013 of the underlying postural mechanisms. This study aimed to further examine the effects of neck
Accepted 10 August 2013
musculature fatigue on standing by using modern analysis of center of pressure (CoP) data. Forty-eight
young healthy adults stood quietly on a balance board for 1 min before and after performing repeated
Keywords: weight-resisted scapular elevation exercises. In a supplementary study on 20 participants, we examined
Neck
(i) the effects of visual deprivation and (ii) the testretest reliability of the traditional and wavelet-based
Muscle fatigue
CoP measures. Testretest reliability of the CoP measures was moderate to good (intraclass correlation
Quiet standing
Wavelet analysis coefcients ranged from 0.58 to 0.94). With neck muscle fatigue or without vision, traditional measures
Vision of CoP velocity and standard deviation increased monotonically. Wavelet analysis revealed that CoP
velocity within the ultralow (<0.10 Hz) and moderate (1.566.25 Hz) frequency bands increased post-
fatigue. Without vision, CoP velocity increased in all but the ultralow frequency band. Our data suggest
that post-fatigue, vision may be the main compensatory postural mechanism for altered neck
proprioception. In conclusion, our ndings reveal more nuances than the simple assertion that neck
musculature fatigue increased postural sway and they advocate the use of wavelet analysis in examining
postural mechanisms associated with neck proprioception.
2013 Elsevier B.V. All rights reserved.

1. Introduction musculature fatigue on standing balance have focused on

Proprioceptive input from the neck plays a signicant role in the
maintenance of upright standing posture [1]. Specically, muscle
spindles and Golgi tendon organs of neck musculature provide
important information on head orientation for postural control [2].
When muscle is fatigued, discharge from these sensory receptors is
altered [3,4], affecting standing balance in healthy young adults
[1,5,6] and patients with chronic neck pain [7]. Although existing
studies indicate that neck musculature fatigue impairs postural
performance, they offer limited mechanistic insight as to how the
postural control system compensates to maintain balance. Yet,
such knowledge is important for the development of targeted
interventions for postural dysfunctions associated with neck
musculature fatigue.
The limited exploration of postural mechanisms in previous
studies may be due to a failure in exploiting the richness of
postural data. The available studies examining the effects of neck
* Corresponding author at: Department of Physiotherapy, Singapore General
Hospital, Outram Road, Singapore 169608, Singapore. Tel.: +65 6321 4132.
E-mail addresses: liang.zhiqi@sgh.com.sg, zky_l@hotmail.com (Z. Liang).
traditional stabilometric measures of center of pressure (CoP)
and notably absent from these studies was the use of modern
analytical methods which allow for possible mechanistic charac-
terization of postural sway [8]. One such method is wavelet
analysis which disaggregates postural sway data into multiple
frequency bands. Since different sensorimotor systems are
reportedly associated with specic frequency bands of postural
movement, the individual contributions of the various systems
may be identied when postural sway data is analyzed across the
various frequency bands [8]. Indeed, using wavelet analysis,
decomposition of postural sway data into multiple frequency
bands was successful in identifying shifts in neuromuscular
strategies when a secondary task was implemented; or when
vision was occluded during quiet standing [8]. Moreover, wavelet
analysis of postural sway in elderly adults differentiated frail
adults from the healthy while traditional measures of sway
trajectory length could not [9]. For these reasons, utilization of
wavelet analysis may be advantageous in identifying the postural
strategies employed following neck musculature fatigue.
Against this background, our study proposed to utilize wavelet
analysis to explore the possible postural mechanisms associated
with musculature fatigue of the axio-scapular neck muscles a

0966-6362/$ see front matter 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.gaitpost.2013.08.007
398 Z. Liang et al. / Gait & Posture 39 (2014) 397403
clinical phenomenon commonly observed in patients with chronic
neck pain during upper limb functional tasks [10]. To facilitate a
clear link between neck musculature fatigue and the observed
changes in postural mechanisms, we chose to study healthy young
adults, without the confounding inuence of impairments
associated with neck pathology or aging. We hypothesized that
neck musculature fatigue will alter postural performance, and
wavelet analysis will reveal changes in specic frequency bands of
postural dynamics. In a small supplementary study, we also
examined (i) the effects of visual deprivation on the wavelet-based
CoP measures and (ii) the testretest reliability of the wavelet-
based and traditional CoP measures.
2. Methods
2.1. Participants
48 young healthy volunteers participated in this study (20
males: mean + SD age = 29 + 5.3 years, body mass = 71.6 + 13.0 kg,
height = 173.4 + 6.1 cm; 28 females: mean + SD age = 26 + 3.7
years, body mass = 52.3 + 7.5 kg, height = 158.8 + 5.6 cm). None
had any pain in the spine or limbs, or history of neck trauma,
vestibular, visual or neurologic disorders. All participants provided
informed consent as outlined by the institutions ethics committee.
2.2. Procedure
2.2.1. Standing balance
Standing balance was assessed using the Wii Balance Board
(Nintendo, Kyoto, Japan) in a protocol previously validated against
a laboratory force-plate [11]. Participants stood quietly on the Wii
Board in their habitual standing posture with arms by their side,
feet hip-width apart, in their usual toe-out angle, and were
instructed to look straight ahead at a dot positioned at eye level
on a plain wall, in a standardized position approximately 1 m
away. To ensure the same feet placement for repeated trials, feet
positions were traced using cellophane tape. Two valid trials of
1 min duration each were performed with a short rest in between.
A third trial was performed immediately following the fatiguing
procedure.
A supplementary experiment was conducted in a subset of 20
participants on a separate day. Participants returned to perform
the same test with eyes open and with eyes closed. Two valid trials
of 1 min duration were performed for each condition. The order of
testing was randomized.
2.2.2. Fatiguing procedure
To fatigue the neck muscles, all participants performed an
exercise in standing with arms by their sides, holding a weight of
920 pounds in each hand. The exercise consisted of shrugging
both scapulas as high as possible repeatedly while keeping the
elbows straight. Participants performed this exercise for as many
repetitions as possible until the subjective exertion level reached at
least very very strong as assessed by the Borg CR-10 scale [12].
Verbal encouragement was given to ensure that participants put in
maximal effort. All participants performed the exercise until they
were no longer able to complete the action. The time lag between
the fatiguing procedure and the post-fatigue standing balance test
was less than 20 s.
2.3. CoP data management
Data were acquired from the Balance Board using a Bluetooth
connection and customized software operating on a Microsoft
Windows-based personal computer. Data for each individual
sensor were streamed to the software, with interpolation of the
streamed data and the timepoint of data acquisition ensuring a
stable 100 Hz sampling rate for further time-frequency domain
analysis [13]. To ensure data integrity in the frequency domain,
multiple steps were taken to remove noise. The data for each
individual sensor were ltered using a 12.5 Hz low-pass lter
utilizing a 2-level undecimated Symlet-8 wavelet with the detail
levels removed. This form of wavelet was subjectively selected for
all data ltering and signal separation due to its similarity in shape
to the COP signal, however other wavelet lters such as Daubechies
and Coiet are just as appropriate.
These data were then converted to CoP coordinates using the
equation outlined previously [11], before being low-pass ltered
at 6.25 Hz using a 3-level undecimated Symlet-8 wavelet with
the detail levels removed. Prior to data collection the Wii
Balance Board was calibrated by applying a series of known
loads ranging from 0 to 45 kg directly over each individual
sensor. These values were then used to create an individual
sensor force calibration.
2.3.1. Data analyses
Typical measures of CoP velocity and standard deviation were
calculated for each of the anteroposterior and mediolateral axes
independently, and also for the combined axes CoP coordinate
movement. These outcome measures were also examined inde-
pendently in four distinct bandwidths of the signal: (1) moderate
(1.566.25 Hz), (2) low (0.391.56 Hz), (3) very low (0.10
0.39 Hz), and (4) ultralow (<0.10 Hz) frequency. These thresholds
were chosen because they are hypothesized to capture postural
movements associated with (1) spinal reexive loops and muscle
activity [14,15], (2) cerebellar [15,16], (3) vestibular [17], and (4)
visual systems [8,18,19] respectively. The bandwidths were
separated using a 9-level Symlet-8 wavelet, with multiresolution
analysis used to combine the detail levels to achieve the respective
frequency bands as seen in Fig. 1.
2.4. Statistical analyses
The effects of neck fatiguing exercises on the various measures
of postural control were quantied with separate mixed-model
repeated-measures analyses. Fixed effects in the mixed models
were the effects of muscle fatigue (pre-fatigue vs. post-
fatigue), CoP axes (AP vs. ML), and their interactions. The
random effects were the identity of the subjects and terms
representing within-subject variation in balance performance (i)
between CoP axes and (ii) between pre- and post-fatigue within
each CoP axis.
In the supplementary study, statistical analyses to evaluate the
effects of visual deprivation on the frequency-band CoP measures
followed those described above. To assess testretest reliability of
the various CoP measures, intraclass correlation coefcients,
model 2,2 (ICC2,2) [16], were used as indices of relative reliability,
and these coefcients were calculated in a 2-way analysis of
variance (ANOVA) based on absolute agreement. Absolute
reliability was represented by 3 indices. First, the standard error
of measurement (SEM) for each CoP measure was derived from the
square root of the mean square error term from the respective
repeated ANOVA [17]. Second, the minimum detectable change
(MDC) was calculated for each CoP measure by multiplying the
point estimate of the SEM, the square root of 2 and the z score of
1.64 (90% condence level). Third, the coefcient of variation (CV),
based on logarithmic transformed data, was calculated using the
methods reported by Hopkins [18].
All statistical analyses were performed with R software, version
2.13.1 (R Foundation, Vienna, Austria). Statistical signicance was
determined at the 2-sided 0.05 level, and we used the Holm
Bonferroni method [19] for multiple testing procedures.
 Z. Liang et al. / Gait & Posture 39 (2014) 397403 399

Fig. 1. Wavelet decomposition representation of a 30-s segment of the anteriorposterior CoP signal of a subject. Time-frequency spectrograms and fast Fourier transform
power spectral density analyses for the signal as a whole (top row of graphs), and the moderate, low, very low and ultralow signals (2nd to bottom rows respectively) are
provided, with the COP trace for each band overlayed at the top of the spectrogram (white data trace spanning the duration of the trace).

3. Results moderate (1.566.25 Hz) and ultralow (<0.10 Hz) frequency

3.1. Main study
Across all measures, no signicant interaction effects between
the effects of muscle fatigue and CoP axes were observed whilst
CoP measures were consistently greater in the AP plane than in the
ML plane (ps < 0.01). Mixed-model analyses revealed signicant
fatigue effects for CoP SD, velocity, and velocity measures from the
bands: F(1,141) = 16.5, HolmBonferroni corrected p < 0.001;
F(1,141) = 7.8, p = 0.02; F(1,141) = 10.4, p = 0.01, F(1,141) = 16.7,
p < 0.001, respectively. As shown in Fig. 2, CoP measures increased
post muscle fatiguegoing from a 6.1% increase for CoP AP-Velocity
to a 30.4% increase for ultralow frequency CoP ML-Velocity. No
signicant main effects of muscle fatigue were observed for the
velocity measures from the low (0.391.56 Hz) and very low (0.10
0.39 Hz) frequency bands.
400 Z. Liang et al. / Gait & Posture 39 (2014) 397403
Fig. 2. Main effect of neck fatiguing exercises on measures of postural control (all HolmBonferroni corrected ps < 0.05). Error bars denote standard deviation.
3.2. Supplementary study
Mixed-model analyses revealed signicant visual effects for all
frequency band measures except for the ultralow (<0.10 Hz) band
(F(1,57) = 3.9, p = 0.06). Fig. 3 shows the percentage change in
average CoP velocities across the four frequency bands from the (a)
pre- to post-muscle fatigue state and (b) eyes-open to eyes-closed
state. In direct contrast to the pre- to post muscle fatigue state
where the ultralow frequency band showed the greatest percent-
age increase, this measure increased the least (and non-signi-
cantly) from eyes open to eyes closed. Table 1 shows the reliability
estimates of the various CoP measures. With the exception of CoP
ML-SD, the ICC values were 0.70 for all measures. With respect to
absolute reliability, the CVs ranged from 7.2% to 34.3% for all
measures.
4. Discussion
Our study explored, in young healthy subjects, the effects of
neck musculature fatigue on quiet standing, indexed by both
traditional and wavelet-based CoP measures. Before doing so, we
examined and demonstrated moderate to good testretest
reliability of the various CoP measures (Table 1). Our main
ndings were that post-fatigue, traditional measures of CoP SD and
velocity increased whilst wavelet analysis showed signicant
increases in the moderate (1.566.25 Hz) and ultralow (<0.10 Hz)
frequency band measures. To strengthen the interpretation of
these ndings, we performed a supplementary study to elucidate
the inuence of visual deprivation on the various CoP measures.
We found that without vision, traditional measures of CoP SD and
velocity increased monotonically but the ultralow frequency band
CoP measure did not signicantly increase. Collectively, our
studies suggest that unlike traditional stabilometric measures,
wavelet-based CoP measures may offer ner distinction of postural
performance and hence, provide greater insight into postural
mechanisms.
Reviewing the literature and limiting our comparisons to
traditional CoP measures, our ndings of a signicant increase in
both CoP SD and velocity post-fatigue differ from those of Gosselin
et al. [5] and Vuillerme et al. [1], both of which found no signicant
 Z. Liang et al. / Gait & Posture 39 (2014) 397403 401

Fig. 3. Dotplot showing mean and 95% condence intervals for percentage change (increase) in the frequency band CoP measures from pre- to post-neck fatiguing exercise
state and (A) eyes open to eyes closed state (B).

increases in traditional CoP measures post neck musculature
fatigue. Pertaining to the rst study [5], our disparity in results may
be explained by the differences in fatiguing procedure [5]. Gosselin
et al. [5] examined the fatiguing effects of neck extensor muscles
whilst we investigated that of the scapular elevation muscles. It is
highly possible that activation of both anterior and posterior neck
muscles in the scapular elevation exercise of our study had a
greater inuence on neck proprioception than fatiguing of the neck
extensors alone. It is more difcult to reconcile our ndings with
those from Vuillerme et al. [1] because these authors utilized a
similar fatiguing procedure to ours. That said, our study was larger
than Vuillermes (48 versus 14 participants), and our use of a
longer sampling duration during balance testing (60 s versus 32 s)
allowed the CoP measurements to stabilize [20] which, in turn,
ostensibly allowed us to draw more robust conclusions.
The greatest increase in CoP velocity was observed in the
ultralow frequency band (<0.10 Hz) post-fatigue. We interpret this
nding to suggest that the postural control system utilized
vision to a greater extent post-fatigue and results of our
supplementary study support this interpretation. Particularly,
removal of vision in our supplementary study increased CoP
velocity in all but the ultralow frequency band, suggesting that
postural sway in the ultralow range (<0.10 Hz) may be strongly
associated with visual contribution. This is in accordance with
earlier studies, which have similarly linked vision to extremely
low frequency postural movement [8,18,19]. Using wavelet
analysis, Chagdes et al. [8] measured the signal energy content
(a variable describing the amount of activity in the data trace)
within different frequency bands and found that without vision,
signal energy content in all frequency bands increased except
the lowest, which decreased. Since the frequency band of their
lowest range corresponds to our ultralow band, their ndings
coincide with ours to reafrm the relationship between vision
and postural sway in this range.

Table 1
Testretest reliability analysis of the COP measures.

Test mean (SD) Retest mean (SD) ICC[2,2] (95% CI) SEM (95% ULCI) CV (%) MDC

AP axis
Range (cm) 1.79 (0.54) 1.84 (0.70) 0.83 (0.580.93) 0.33 (0.48) 16.7 0.54
SD (cm) 0.35 (0.14) 0.38 (0.18) 0.76 (0.410.91) 0.10 (0.14) 24.3 0.16
Velocity (cm/s) 0.49 (0.11) 0.45 (0.08) 0.84 (0.550.94) 0.05 (0.07) 9.7 0.08
<0.10 Hz (cm/s) 0.052 (0.025) 0.050 (0.024) 0.87 (0.670.95) 0.011 (0.016) 22.6 0.018
0.100.49 Hz (cm/s) 0.15 (0.046) 0.14 (0.035) 0.81(0.520.92) 0.023 (0.03) 16.0 0.038
0.491.49 Hz (cm/s) 0.35 (0.11) 0.31 (0.06) 0.83 (0.510.93) 0.045 (0.07) 11.7 0.075
1.496.25 Hz (cm/s) 0.29 (0.06) 0.28 (0.06) 0.91 (0.770.96) 0.026 (0.040) 9.6 0.042
ML axis
Range (cm) 0.90 (0.34) 0.88 (0.35) 0.73(0.290.82) 0.23 (0.33) 24.5 0.37
SD (cm) 0.16 (0.07) 0.18 (0.09) 0.58 (0.000.83) 0.06 (0.09) 34.3 0.103
Velocity (cm/s) 0.32 (0.08) 0.30 (0.07) 0.88 (0.680.95) 0.03 (0.05) 9.5 0.05
<0.10 Hz (cm/s) 0.017 (0.006) 0.019 (0.007) 0.85 (0.640.94) 0.003 (0.005) 19.2 0.006
0.100.49 Hz (cm/s) 0.07 (0.05) 0.06 (0.03) 0.70 (0.290.89) 0.027 (0.04) 28.0 0.044
0.491.49 Hz (cm/s) 0.19 (0.06) 0.17 (0.05) 0.79 (0.490.92) 0.029 (0.04) 15.9 0.048
1.496.25 Hz (cm/s) 0.23 (0.06) 0.22 (0.06) 0.94 (0.840.97) 0.020 (0.03) 7.2 0.033

COP: center of pressure; CI: condence interval; ULCI: upper limit condence interval; ICC: intraclass correlation coefcient (95% CI); SEM: standard error of measurement
(upper one-sided 95% CI); MDC: minimal detectable change (estimated using the z-value for 90% CI); CV: coefcient of variation (calculated from logarithmic transformed
data); SD: standard deviation; AP: anteroposterior; ML: mediolateral.
402 Z. Liang et al. / Gait & Posture 39 (2014) 397403
Reweighting of various sensory input by the central nervous
system is a mechanism through which balance is effectively
maintained [21,22]. Our results suggest that post neck muscula-
ture fatigue, visual input was utilized to a greater extent during the
quiet standing task. Since fatigue alters discharge from sensory
receptors of neck muscles [3,4], we speculated that increased
weighting on visual input by the postural control system occurred
to stabilize movements of the head [23].
Re-weighting of visual input is not the only neurophysiological
change post-fatigue. CoP velocity within the moderate frequency
band (1.566.25 Hz) also increased, albeit at a smaller magnitude
compared with the ultralow frequency band measure. Postural
movements captured within this band have been attributed to
spinal reexive loops and muscle activity [14,15] and we offer
three possible interpretations of why these may be augmented
post-fatigue. First, open-loop mechanisms may be utilized to a
greater extent because open loop postural control is thought to be
operating within this frequency band [24,25]. From a theoretical
standpoint, this is not unreasonable if postural control of quiet
standing utilizes both closed-loop (feedback) and open-loop
mechanisms [24,25]. As proprioceptive input from the neck is
compromised with fatigue, intermittent open-loop control may be
utilized to a greater extent to minimize the effects of sensory noise
[24]. Second, sensory reweighting mechanisms may have initiated
increased weighting of lower limb proprioceptive input to
compensate for neck proprioceptive insufciencies [22], triggering
increased activation of ankle plantarexor muscles whose actions
in standing lie within this frequency band [26]. Third, amplied
muscle activity post-fatigue can also represent excessive correc-
tive muscle torque. As the postural control system reweighs or
compensates for loading on sensory input, over-generation of
corrective muscle torque may occur, resulting in more rapid
changes of direction and a consequent increase in signal within the
moderate frequency band [21]. Further research is required to
determine the most likely interpretation.
Our ndings have both research and clinical implications. First,
the results demonstrate that wavelet analysis is capable of detecting
specic postural control changes associated with altered proprio-
ceptive input from the neck. Future studies on postural dysfunctions
associated with the neck, such as chronic neck pain, should therefore
consider utilizing wavelet analysis for greater characterization of
postural performance. Second, our study shows that neck muscula-
ture fatigue alone, in the absence of other impairments, can induce
alterations in postural control, thus emphasizing the importance of
addressing neck-scapular muscular dysfunctions in the treatment of
balance disorders in chronic neck pain. Furthermore, if vision is the
main compensatory mechanism that accommodates for altered
neck input, then assessing the visual aspects of postural control may
be necessary in patients with neck pain and complaints of
unsteadiness or poor balance.
Our study has limitations. Although our study used a repeated-
measure design, we cannot negate the possibility that our
instruction to our participants to look straight ahead at a mark on
the wall during the test may have directed the utilization of vision to
a greater extent than otherwise post-fatigue. Nonetheless, our
current data show a clear shift toward visual reliance post-fatigue,
and theoretical basis for such an interpretation, as described above,
supports this nding. In the same vein, our interpretations could
have been further strengthened if we had tested the joint effects of
visual deprivation and neck muscle fatigue on standing balance.
Future research combining the two may be warranted.
5. Conclusions
We have shown that fatigue to the neck muscles increased
traditional stabilometric measures of CoP SD and Velocity, whilst
wavelet analysis revealed signicant increases of CoP velocity in
the ultralow and moderate frequency bands of postural movement.
Together with the results of our supplementary study, these
ndings reafrm that visual aspects of postural control are
detectable within the ultralow frequency band, and were utilized
to a greater extent when proprioceptive input from the neck was
compromised by fatigue. Other postural mechanisms which
resulted in augmented muscle activity were also activated and
further research is necessary to identify them. Our ndings are
more nuanced than the simple assertion that neck fatiguing
exercises increased postural sway and they advocate the use of
wavelet analysis in examining postural mechanisms associated
with neck proprioception.
Grant support
This study was supported by a Singapore Physiotherapy
Association Research Grant (RF09-004) and a SingHealth Founda-
tion grant (SHF/FG551S/2011).
Role of funding source
The grant sponsors had no involvement in study design,
collection, analysis and interpretation of the data; writing of the
manuscript and in the decision to submit the manuscript for
publication.
Acknowledgements
We wish to express our gratitude to all participants of this
study. We also thank Ms Tan Bee Yee, Ms Jennifer Liaw, and Ms
Karen Koh for supporting this study.
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