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Stroboscopic Vision to Induce Sensory Reweighting During Postural Control

Article  in  Journal of Sport Rehabilitation · June 2017

DOI: 10.1123/jsr.2017-0035

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“Stroboscopic Vision to Induce Sensory Reweighting During Postural Control” by Kim KM, Kim JS, Grooms DR
Journal of Sport Rehabilitation
© 2017 Human Kinetics, Inc.

Note: This article will be published in a forthcoming issue of

the Journal of Sport Rehabilitation. The article appears here in
its accepted, peer-reviewed form, as it was provided by the
submitting author. It has not been copyedited, proofed, or
formatted by the publisher.

Section: Technical Report

Article Title: Stroboscopic Vision to Induce Sensory Reweighting During Postural Control

Authors: Kyung-Min Kim1, Joo-Sung Kim1, and Dustin R. Grooms2,3

Affiliations: 1Department of Kinesiology and Sport Sciences, University of Miami, Miami, FL.
2
Division of Athletic Training, School of Applied Health Sciences and Wellness, College of
Health Sciences and Professions, Ohio University, Athens, OH. 3Ohio Musculoskeletal &
Neurological Institute, Ohio University, Athens, OH.

Running Head: Sensory reweighting in balance control

Journal: Journal of Sport Rehabilitation

Acceptance Date: May 17, 2017

©2017 Human Kinetics, Inc.

DOI: https://doi.org/10.1123/jsr.2017-0035
 “Stroboscopic Vision to Induce Sensory Reweighting During Postural Control” by Kim KM, Kim JS, Grooms DR
Journal of Sport Rehabilitation
© 2017 Human Kinetics, Inc.

Running Head: Sensory reweighting in balance control

Title: Stroboscopic vision to induce sensory reweighting during postural control

Authors:
Kyung-Min Kim, PhD1

Joo-Sung Kim, MS1

Dustin R. Grooms, PhD2,3

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Affiliations:
1. Department of Kinesiology and Sport Sciences, University of Miami, Miami, FL

USA 33146

2. Division of Athletic Training, School of Applied Health Sciences and Wellness,

College of Health Sciences and Professions, Ohio University, Athens, Ohio USA

45701

3. Ohio Musculoskeletal & Neurological Institute, Ohio University, Athens, Ohio USA

45701

Funding:

This research did not receive any specific grant from funding agencies in the public, commercial,

or not-for-profit sectors.

Conflict of Interest:

None of authors has conflicts of interest.

 “Stroboscopic Vision to Induce Sensory Reweighting During Postural Control” by Kim KM, Kim JS, Grooms DR
Journal of Sport Rehabilitation
© 2017 Human Kinetics, Inc.

ABSTRACT

Context: Patients with somatosensory deficits have been found to rely more on visual feedback
for postural control. However, current balance tests may be limited in identifying increased visual
dependence (sensory reweighting to the visual system), as options are typically limited to eyes
open or closed conditions with no progressions between. Objective: To assess the capability of
stroboscopic glasses to induce sensory reweighting of visual input during single-leg balance.
Design: Descriptive Setting: Laboratory Participants: Eighteen healthy subjects without vision
or balance disorders or lower extremity injury history (9 females; age=22.1±2.1 years;
height=169.8±8.5cm; mass=66.5±10.6kg) participated. Interventions: Subjects performed 3 trials
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of unipedal stance for 10 seconds with eyes open (EO) and closed (EC), and with stroboscopic
vision (SV) that was completed with specialized eyewear that intermittently cycled between
opaque and transparent for 100 milliseconds at a time. Balance tasks were performed on firm and
foam surfaces, with the order randomized. Main Outcome Measures: Ten center-of-pressure
parameters were computed. Results: Separate ANOVAs with repeated measures found significant
differences between the 3 visual conditions on both firm (Ps=<.001) and foam (Ps=<.001 to .005)
surfaces for all measures. For trials on firm surface, almost all measures showed that balance with
SV was significantly impaired relative to EO, but less impaired than EC. On the foam surface,
almost all postural stability measures demonstrated significant impairments with SV compared
with EO, but the impairment with SV was similar to EC. Conclusions: SV impairment of single-
leg balance was large on the firm surface, but not to the same degree as EC. However, the foam
surface disruption to somatosensory processing and sensory reweighting to vision lead to greater
disruptive effects of SV to the same level as EC. This indicates that when the somatosensory
system is perturbed even a moderate decrease in visual feedback (SV) may induce an EC level
impairment to postural control during single-leg stance.

Key words: sensory organization, single-leg balance, visual balance control

 “Stroboscopic Vision to Induce Sensory Reweighting During Postural Control” by Kim KM, Kim JS, Grooms DR
Journal of Sport Rehabilitation
© 2017 Human Kinetics, Inc.

Sensory weighting is the ability of the central nervous system (CNS) to weigh degree of

reliance on the primary modalities of sensory feedback (somatosensory, visual, vestibular) for

postural control.1 The relative weight assigned to each sensory system varies with complexity of

postural task, environmental conditions, and fidelity of input.1, 2 For example, the CNS weighs

somatosensory information more heavily during quiet, unperturbed standing, but decreases

somatosensory weighting during perturbed standing (unstable surface), increasing weight to other,

more reliable sensory modalities (visual, if available) to maintain upright standing. The CNS’s
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ability to change the relative contributions of sensory systems has been termed “sensory re-

weighting”, biasing motor coordination via the most salient and reliable information over less

reliable or perturbed inputs.2

Sensory reweighting provides a compensatory mechanism for altered afferent input arising

from musculoskeletal injuries and aging.3-6 Specifically, a recent meta-analysis3 found that patients

with chronic ankle instability re-weight to visual feedback to maintain single-limb balance, as a

compensatory mechanism for reduced fidelity of somatosensory input from the injured ankle joint.

Similar findings are observed in patients with knee injuries4 and the elderly.5, 6 This visual reliance

may enable patients with somatosensory deficits to maintain standing balance, but it can be

dangerous during activities of daily living or/and sports. These activities often involve multiple

tasks; thus, patients’ visual attention may be largely diverted from balance control, revealing the

deficiencies in the compensatory mechanism and possibly resulting in falls and/or injury. Thus, it

is imperative to identify those who may rely on the visual system during balance and develop

rehabilitative progressions to rectify sensory re-weighting to visual input after injury.

Assessment of sensory reweighting from somatosensory to visual systems requires

mechanisms to disrupt both systems.2 There have been many clinically simple and efficient ways
 “Stroboscopic Vision to Induce Sensory Reweighting During Postural Control” by Kim KM, Kim JS, Grooms DR
Journal of Sport Rehabilitation
© 2017 Human Kinetics, Inc.

to partially disrupt somatosensory input (unstable surface, foam, roller board); however,

perturbations of visual input have been limited to two extreme conditions: full or no vision. This

is because there has been a lack of easily-implemented methods for partially disrupting visual input.

Recent advances in stroboscopic glasses technology provide a mechanism to perturb the

visual system to any degree between eyes closed (EC) and open (EO). Stroboscopic Vision (SV),

characterized by intermittent vision obstruction, may be a clinical tool that will enable clinicians

to examine sensory reweighting of visual information in a progressive fashion from full to no

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vision. Thus, the purpose of this study was to utilize this innovative technology to allow for partial

perturbation of the visual system during single-leg balance on firm and foam surfaces. These two

different surface conditions allow clinicians to use SV to identify sensory re-weighting of the

visual system when fidelity of the somatosensory input is altered.

Methods

This observational study recruited 18 subjects (9 males, 9 females, 22.1±2.1yrs, 169.8±8.5

cm, 66.5±10.6kg) without any injuries in the past 6 months and no history of vision, balance

disorders, or lower extremity injury. The University institutional review board approved the study

requiring informed consent.

The balance testing protocol and data processing were consistent with previously reported

methods.7, 8 Subjects were asked to perform 3 trials of single-leg stance on their dominant limbs

for 10 seconds with EO, EC, and SV, created by a specialized eyewear (Nike SPARQ Vapor

Strobes, Nike Inc, Beaverton, OR, USA), known as stroboscopic glasses that intermittently cycled

between opaque and transparent for 100 millisecond periods (reducing visual feedback by half),

which has been previously described.9 Balance testing was performed on both a firm force plate
 “Stroboscopic Vision to Induce Sensory Reweighting During Postural Control” by Kim KM, Kim JS, Grooms DR
Journal of Sport Rehabilitation
© 2017 Human Kinetics, Inc.

(Accusway Plus, AMTI, Watertown, MA, USA), and a foam pad (Airex Balance Pad, Airex AG,

Sins, Switzerland) that was placed on top of a force plate, with the order randomized. There was a

total of 10 center-of-pressure (COP) parameters computed using the mean of 3 trials for each

balance task, providing comprehensive balance assessments: 6 traditional COP and 4 time-to-

boundary (TTB) measures (Tables 1 and 2). A larger traditional COP and\or a lower TTB indicates

poorer balance.7, 8

For each COP, an analysis of variance with repeated measures was performed using a
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statistics software (IBM SPSS Statistics Version 24; IBM Corporation, Armonk, NY, USA) to

determine difference in balance performance between 3 visual conditions: EO, SV, and EC.

Cohen’s d effect sizes and associated 95% confidence intervals (CI) were calculated to provide the

magnitude of change in balance performance. The effect size strength was interpreted using

Cohen’s guidelines: less than 0.2 as weak, from 0.21 to 0.5 as small, from 0.51 to 0.8 as moderate,

and greater than 0.8 as large.10 Statistical significance for all analyses was set a priori at P≤0.005

with the Bonferroni correction to control Type I error.

Results

All subjects completed 3 successful trials of single-leg balance on firm surface in 3 visual

conditions: EO, EC, and SV. Eight subjects were excluded on the foam condition as they were

unable to maintain balance with EC and/or SV.

For all traditional COP and TTB measures there were significant differences between the

3 visual conditions on both firm (Ps=<.001, Table 1) and foam (Ps=<.001 to 0.005, Table 2)

surfaces. For trials on firm surface almost all traditional COP and TTB measures showed that

balance with SV was significantly poorer than EO, but less impaired than EC. The disruption with
 “Stroboscopic Vision to Induce Sensory Reweighting During Postural Control” by Kim KM, Kim JS, Grooms DR
Journal of Sport Rehabilitation
© 2017 Human Kinetics, Inc.

SV appears to be of large magnitude (Table 1). Similarly, almost all measures demonstrated that

balance with SV on foam surface was significantly disrupted compared with EO, but the disruption

with SV was similar to EC (Table 2), indicating that SV impaired balance more on foam than firm

surfaces.

Discussion

As has been previously reported,2, 5 we found different contributions of the visual system

to single-leg balance depending on the fidelity of somatosensory input (surface condition).

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However, the novel effects of SV were scaled on the firm surface, with EC inducing the least

postural stability, EO the most, and SV being between the two. Interestingly, on the foam surface

(unreliable somatosensory input), the effects of SV were comparable to EC, reflecting sensory

reweighting to the visual system for postural control. This suggests that SV may have the potential

to help identify the extent of dependency on visual feedback for postural control, as the level of

disruption can be modified until impaired postural control is detected. In addition, the partial nature

and ability to modify the degree of visual input of SV disruption provides a possible intervention

mechanism to bridge EO and EC conditions. Furthermore, 8 subjects failed to maintain a 10-sec

single-leg stance on the foam surface with EC or/and SV, suggesting that failed trials may have

potential to clinically identify those with excessive sensory reweighting to vision without the need

for an instrumented force plate, improving the potential clinical application. One could

progressively increase the SV difficulty until failure to maintain stance occurs and determine

relative visual dependence for postural control.

Balance tests with EC and EO can assess the visual contribution to single-leg balance.

However, engaging in progressive rehabilitation, targeted at sensory reweighting, is difficult,

 “Stroboscopic Vision to Induce Sensory Reweighting During Postural Control” by Kim KM, Kim JS, Grooms DR
Journal of Sport Rehabilitation
© 2017 Human Kinetics, Inc.

especially as EC training may be too extreme for those with injuries. Also, training the visual-

motor system with only complete visual obstruction may limit transfer of postural control training

to new motor tasks. A unique advantage of SV is that dynamic tasks can be completed that are not

possible under EC. Not only does SV allow for progressive rehabilitation (as degree of visual

feedback can be modulated), it can also be used in a variety of visually demanding environments,

forcing increased weighting to the somatosensory system. Using SV to decrease dependency on

visual feedback for patients with somatosensory deficits may result in improved postural control
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and general motor function.4, 9

Thus, this study provides preliminary evidence that portable,

inexpensive stroboscopic glasses may be potentially versatile tools in balance assessment and

training.

Conclusions

Single-leg balance with SV was significantly impaired, with its greater effects on foam

than firm surfaces. These results indicate sensory reweighting to the visual system for postural

control when somatosensory input is altered by surface condition. Stroboscopic glasses capable of

modulating visual feedback may be clinically useful in not only identifying reliance on visual

feedback for postural control in patients with somatosensory deficits, but also allowing for

progressive rehabilitation targeted at visual feedback dependence for motor control.

 “Stroboscopic Vision to Induce Sensory Reweighting During Postural Control” by Kim KM, Kim JS, Grooms DR
Journal of Sport Rehabilitation
© 2017 Human Kinetics, Inc.

References

1. Peterka RJ, Loughlin PJ. Dynamic regulation of sensorimotor integration in human

postural control. J Neurophysiol 2004;91(1):410-23.
2. Asslander L, Peterka RJ. Sensory reweighting dynamics in human postural control. J
Neurophysiol 2014;111(9):1852-64.
3. Song K, Burcal CJ, Hertel J, Wikstrom EA. Increased Visual Use in Chronic Ankle
Instability: A Meta-analysis. Med Sci Sports Exerc 2016;48(10):2046-56.
4. Grooms D, Appelbaum G, Onate J. Neuroplasticity Following Anterior Cruciate
Ligament Injury: A Framework for Visual-Motor Training Approaches in Rehabilitation.
J Orthop Sports Phys Ther 2015;45(5):381-93.
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5. Bugnariu N, Fung J. Aging and selective sensorimotor strategies in the regulation of

upright balance. J Neuroeng Rehabil 2007;4:19.
6. Franz JR, Francis CA, Allen MS, O'Connor SM, Thelen DG. Advanced age brings a
greater reliance on visual feedback to maintain balance during walking. Hum Mov Sci
2015;40:381-92.
7. Hertel J, Olmsted-Kramer LC, Challis JH. Time-to-boundary measures of postural
control during single leg quiet standing. J Appl Biomech 2006;22(1):67-73.
8. Kim KM, Hart JM, Saliba SA, Hertel J. Effects of focal ankle joint cooling on unipedal
static balance in individuals with and without chronic ankle instability. Gait Posture
2015;41(1):282-7.
9. Clark JF, Ellis JK, Bench J, Khoury J, Graman P. High-performance vision training
improves batting statistics for University of Cincinnati baseball players. PLoS One
2012;7(1):e29109.
10. Cohen J. Statistical Power Analysis for the Behavioral Sciences. 2 ed. Hillsdale:
Lawrence Erlbaum Association; 1988.
 “Stroboscopic Vision to Induce Sensory Reweighting During Postural Control” by Kim KM, Kim JS, Grooms DR
Journal of Sport Rehabilitation
© 2017 Human Kinetics, Inc.

Table 1. Descriptive summary of center of pressure (COP) measures during 10-sec single-leg stance on firm surface

Eyes Open Stroboscopic Eyes Closed Effect Sizea Effect Sizea Effect Sizea
COP parameters RMANOVA
(EO) Vision (SV) (EC) (SV and EO) (EC and EO) (EC and SV)

F2,34=37.72, P<.001 0.79±0.2 1.34±0.4 1.85±0.7 1.83(1.05, 2.61) 1.95(1.16, 2.75) 0.87(0.18, 1.55)
Velocity ML (cm/s)*
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F2,34=26.81, P<.001 0.71±0.2 1.12±0.5 1.69±0.8 1.21(0.50, 1.92) 1.69(0.93, 2.45) 0.87(0.18, 1.55)
Velocity AP (cm/s)*
F2,34=99.32, P<.001 0.19±0.0 0.32±0.1 0.40±0.1 2.05(1.24, 2.85) 3.52(2.48, 4.57) 1.13(0.42, 1.83)
SD ML*
F2,34=26.96, P<.001 0.26±0.1 0.35±0.1 0.44±0.1 1.00(0.30, 1.69) 1.99(1.19, 2.79) 0.92(0.23, 1.61)
SD AP*
Percent range ML F2,34=32.23, P<.001 9.48±1.4 15.01±2.7 18.79±6.3 2.59(1.71, 3.48) 2.04(1.23, 2.84) 0.78(0.10, 1.45)
(%)*
F2,34=30.10, P<.001 4.57±1.1 6.68±2.0 8.27±2.2 1.29(0.57, 2.01) 2.09(1.28, 2.90) 0.74(0.07, 1.42)
Percent range AP (%)*
F2,34=93.82, P<.001 5.28±1.5 2.93±0.7 2.44±0.8 -2.04(-2.85, -1.23) -2.37(-3.22, -1.52) -0.64(-1.31, 0.03)
Mean Min.TTBML(s)*
F2,34=199.81, P<.001 14.77±3.5 9.44±2.9 6.53±2.3 -1.66(-2.42, -0.90) -2.75(-3.66, -1.84) -1.11(-1.81, -0.41)
Mean Min.TTBAP(s)*
F2,34=21.43, P<.001 4.38±1.9 2.36±0.8 2.35±1.1 -1.40(-2.13, -0.67) -1.33(-2.05, -0.61) -0.01(-0.66, 0.64)
SD Min. TTBML§
F2,34=72.47, P<.001 9.65±3.1 5.92±2.0 4.38±1.8 -1.41(-2.14, -0.68) -2.05(-2.86, -1.24) -0.79(-1.47, -0.11)
SD Min. TTBAP*

Abbreviation: RMANOVA, repeated measures analysis of variance; SD, standard deviation; ML, mediolateral; AP, anteroposterior; TTB, time-to-boundary; Min,
minima
a
Cohen’s d estimate of effect size was calculated between two of 3 balance conditions (eyes open, stroboscopic vision, and eyes closed) using pooled standard
deviation, along with its associated 95% confidence interval.
It is noted that a greater traditional COP measure indicates poorer balance that is also determined by a lower TTB measure, which causes directional differences in
effect size and confidence interval measurements.
*Single-leg balance with SV was significantly poorer than EO, but less impaired than EC
§
Single-leg balance with SV was significantly poorer than EO, but did not differ from EC
 “Stroboscopic Vision to Induce Sensory Reweighting During Postural Control” by Kim KM, Kim JS, Grooms DR
Journal of Sport Rehabilitation
© 2017 Human Kinetics, Inc.

Table 2. Descriptive summary of center of pressure (COP) measures during 10-sec single-leg stance on foam surface

Eyes
Stroboscopic Eyes Closed Effect Sizea Effect Sizea Effect Sizea
COP parameters RMANOVA Open
Vision (SV) (EC) (SV and EO) (EC and EO) (EC and SV)
(EO)
F2,18=24.08, 1.13±0.3 2.34±0.8 2.53±0.6 2.01(0.93, 3.08) 2.80(1.57, 4.04) 0.25(-0.63, 1.13)
Velocity ML (cm/s)§
P<.001
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F2,18=22.92, 0.98±0.2 2.17±0.8 2.72±0.9 2.02(0.94, 3.09) 2.72(1.51, 3.94) 0.67(-0.23, 1.57)
Velocity AP (cm/s)§
P<.001
F2,18=45.40, 0.24±0.0 0.43±0.1 0.46±0.1 2.53(1.35, 3.71) 3.49(2.10, 4.88) 0.28(-0.60, 1.17)
SD ML§
P<.001
F2,18=26.54, 0.30±0.1 0.61±0.1 0.67±0.1 3.87(2.39, 5.36) 3.36(2.00, 4.72) 0.44(-0.45, 1.33)
SD AP§
P<.001
F2,18=25.55, 12.27±2.0 19.94±4.4 20.13±2.9 2.24(1.13, 3.36) 3.18(1.86, 4.50) 0.05(-0.83, 0.93)
Percent range ML (%)§
P<.001
F2,18=26.42, 5.66±0.8 11.43±2.8 12.85±2.7 2.81(1.57, 4.04) 3.63(2.20, 5.05) 0.51(-0.38, 1.40)
Percent range AP (%)§
P<.001
F2,18=20.79, 3.32±1.2 1.64±0.6 1.56±0.6 -1.72(-2.74, -0.69) -1.80(-2.84, -0.76) -0.14(-1.02, 0.74)
Mean Min.TTBML(s)§
P<.001
F2,18=56.98, 10.44±2.9 4.77±1.8 3.71±1.2 -2.37(-3.51, -1.22) -3.05(-4.34, -1.76) -0.69(-1.60, 0.21)
Mean Min.TTBAP(s)*
P<.001
F2,18=7.33, P=.005 2.58±1.1 1.26±0.7 1.43±0.8 -1.40(-2.38, -0.43) -1.17(-2.11, -0.22) 0.22(-0.66, 1.10)
SD Min. TTBML§
F2,18=28.66, 7.05±2.6 2.71±1.4 2.30±1.1 -2.09(-3.19, -1.00) -2.40(-3.55, -1.25) -0.33(-1.22, 0.55)
SD Min. TTBAP§
P<.001
Abbreviation: RMANOVA, repeated measures analysis of variance; SD, standard deviation; ML, mediolateral; AP, anteroposterior; TTB, time-to-boundary;
Min, minima
a
Cohen’s d estimate of effect size was calculated between two of 3 balance conditions (eyes open, stroboscopic vision, and eyes closed) using pooled standard
deviation, along with its associated 95% confidence interval.
It is noted that a greater traditional COP measure indicates poorer balance that is also determined by a lower TTB measure, which causes directional differences
in effect size and confidence interval measurements.
*Single-leg balance with SV was significantly poorer than EO, but less impaired than EC
§
Single-leg balance with SV was significantly poorer than EO, but did not differ from EC

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