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Auditory biofeedback substitutes for loss of sensory information in maintaining stance

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The importance of sensory feedback for postural control in stance is evident from the balance improvements occurring when sensory information from the vestibular, somatosensory, and visual systems is available. However, the extent to which also audio-biofeedback (ABF) information can improve balance has not been determined. It is also unknown why additional artificial sensory feedback is more effective for some subjects than others and in some environmental contexts than others. The aim of this study was to determine the relative effectiveness of an ABF system to reduce postural sway in stance in healthy control subjects and in subjects with bilateral vestibular loss, under conditions of reduced vestibular, visual, and somatosensory inputs. This ABF system used a threshold region and non-linear scaling parameters customized for each individual, to provide subjects with pitch and volume coding of their body sway. ABF had the largest effect on reducing the body sway of the subjects with bilateral vestibular loss when the environment provided limited visual and somatosensory information; it had the smallest effect on reducing the sway of subjects with bilateral vestibular loss, when the environment provided full somatosensory information. The extent that all subjects substituted ABF information for their loss of sensory information was related to the extent that each subject was visually dependent or somatosensory-dependent for their postural control. Comparison of postural sway under a variety of sensory conditions suggests that patients with profound bilateral loss of vestibular function show larger than normal information redundancy among the remaining senses and ABF of trunk sway. The results support the hypothesis that the nervous system uses augmented sensory information differently depending both on the environment and on individual proclivities to rely on vestibular, somatosensory or visual information to control sway.
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Exp Brain Res (2007) 178:37–48
DOI 10.1007/s00221-006-0709-y
123
RESEARCH ARTICLE
Auditory biofeedback substitutes for loss of sensory information
in maintaining stance
Marco Dozza · Fay B. Horak · Lorenzo Chiari
Received: 22 August 2005 / Accepted: 7 September 2006 / Published online: 5 October 2006
© Springer-Verlag 2006
Abstract The importance of sensory feedback for
postural control in stance is evident from the balance
improvements occurring when sensory information
from the vestibular, somatosensory, and visual systems
is available. However, the extent to which also audio-
biofeedback (ABF) information can improve balance
has not been determined. It is also unknown why addi-
tional artiWcial sensory feedback is more eVective for
some subjects than others and in some environmental
contexts than others. The aim of this study was to
determine the relative eVectiveness of an ABF system
to reduce postural sway in stance in healthy control
subjects and in subjects with bilateral vestibular loss,
under conditions of reduced vestibular, visual, and
somatosensory inputs. This ABF system used a thresh-
old region and non-linear scaling parameters custom-
ized for each individual, to provide subjects with pitch
and volume coding of their body sway. ABF had the
largest eVect on reducing the body sway of the subjects
with bilateral vestibular loss when the environment
provided limited visual and somatosensory informa-
tion; it had the smallest eVect on reducing the sway of
subjects with bilateral vestibular loss, when the envi-
ronment provided full somatosensory information. The
extent that all subjects substituted ABF information
for their loss of sensory information was related to the
extent that each subject was visually dependent or
somatosensory-dependent for their postural control.
Comparison of postural sway under a variety of sen-
sory conditions suggests that patients with profound
bilateral loss of vestibular function show larger than
normal information redundancy among the remaining
senses and ABF of trunk sway. The results support the
hypothesis that the nervous system uses augmented
sensory information diVerently depending both on the
environment and on individual proclivities to rely on
vestibular, somatosensory or visual information to con-
trol sway.
Keywords Posture · Center of pressure ·
Vestibular loss · Audio-biofeedback ·
Sensory integration · Sensory substitution ·
Posture control
Introduction
The control of postural sway depends on continuous
feedback of sensory information from the vestibular,
somatosensory, and visual senses. The largest increase
in postural sway in stance occurs when somatosensory
information is compromised (Nashner et al. 1982). The
next largest increase occurs when vestibular informa-
tion is lost, and the smallest, when vision is eliminated
by eye closure (Peterka and Black 1990; Macpherson
and Inglis 1993; Horak and Macpherson 1996). These
increases in postural sway suggest that the central ner-
vous system (CNS) relies primarily on somatosensory
information, less so on vestibular information, and even
less so on visual information to control postural sway
during quiet stance. In fact, a linear sensory interaction
M. Dozza · F. B. Horak (&)
Neurological Sciences Institute,
Oregon Health & Science University,
505 NW 185th Ave, Beaverton, OR 97006, USA
e-mail: horakf@ohsu.edu
M. Dozza · L. Chiari
Department of Electronics, Computer Science,
and Systems, University of Bologna, Bologna, Italy
38 Exp Brain Res (2007) 178:37–48
123
model predicts such postural sway in adults during
stance by proposing a 70% dependence on somatosen-
sory information from a Wrm surface, 20% on vestibu-
lar information, and 10% on visual information
(Peterka 2002). However, several studies support the
notion that the CNS re-weighs its relative dependence
on sensory information when the availability of infor-
mation from diVerent senses changes (Jeka et al. 2000;
Black and Nashner 1984; Horak and Hlavacka 2001).
For example, when healthy subjects stand on an oscil-
lating surface with eyes closed, they increasingly
depend on vestibular information and visual informa-
tion and decrease dependence on somatosensory infor-
mation from the surface as the amplitude of the surface
rotations increases (Peterka 2002).
It is as yet unknown the extent to which the CNS re-
weighs its relative dependence on sensory information
in presence of augmented sensory information. Aug-
mentation of sensory information, such as auditory
information, could be useful for rehabilitation of bal-
ance in patients with sensory loss, especially if the CNS
proportionately integrates this information with the
natural sensory information depending on the sensory
demands of the task.
One type of augmentation to reduce postural sway
auditory information in the form of biofeedback—has
received minimal investigation. When audio-biofeedback
(ABF) was investigated, it was usually in conjunction
with visual biofeedback (Nichols 1997; Barclay-Goddard
et al. 2004). In studies of ABF and visual biofeedback,
the sound constituting the ABF was a simple alarm sig-
nal (Wong et al. 1997; Batavia et al. 2001) that was used
to augment the visual biofeedback. However, another
type of ABF, able to represent a complex information
and not limited to an alarm signal, may be especially
useful to augment postural feedback since auditory cues:
(1) are easy to integrate with the remaining senses in
sensory-impaired individuals, such as those with vestib-
ular losses (Wickens and Hollands 2000), (2) do not
interfere with visual information, and (3) are capable of
signaling spatial information (Vinge 1971; Nelson et al.
1998). To illustrate this last point, humans use hearing
for spatial localization whenever we turn our heads to
locate the source of a sound. In addition, it has been
shown that novice pilots can learn how to Xy in a Xight
simulator using either visual information or auditory
tracking for turns, bank angles, and tilt (Forbes 1946),
and it was subsequently determined that healthy sub-
jects can use auditory information nearly as accurately
as visual information to detect body orientation and
motion in space (Vinge 1971).
Auditory and vestibular information are both trans-
mitted to the brain via the VIII cranial nerve, which
projects to the temporal lobe. Auditory cues automati-
cally (subconsciously) inXuence postural alignment,
and postural alignment automatically alters the ability
to locate auditory cues in the environment (Lackner
1974; Lackner and DiZio 2000). Even stationary audi-
tory cues were found to reduce the body sway of con-
trol and blind subjects when the cues were from stereo
speakers in close proximity to both ears (Easton et al.
1998).
Recently, it has been found that subjects with a loss of
vestibular information were able to use both ABF
(Dozza et al. 2005b; Hegeman et al. 2005) and tactile
biofeedback (Tyler et al. 2003; Kentala et al. 2003) that
map their body movement in order to reduce postural
sway. However, subjects with and without vestibular loss
varied widely in their ability to reduce sway with aug-
mented sensory ABF and vibrotactile biofeedback. The
reasons for this inter-subject variability are unknown.
However, similar inter-subject variability was also found
when subjects with and without vestibular loss relied on
their three natural sources of sensory information
(visual, vestibular, and somatosensory) to control pos-
tural sway (Black and Nashner 1984; Lacour et al. 1997).
For example, 50% of subjects with neuromas on the
VIII cranial nerve increased their postural sway in
stance with eyes closed, but 50% decreased or did not
change their sway with eyes closed (Lacour et al. 1997
).
After surgery to remove the neuroma, the same sub-
jects, who were visually dependent (i.e., relied more on
visual than on somatosensory information to maintain
balance) before the surgery, no longer increased their
sway with eyes closed, whereas those subjects who were
not visually dependent increased their sway with eyes
closed after surgery. Further, as people age or are
exposed to weightlessness in space for a long time,
many, but not all, increased their relative dependence
on visual and somatosensory information to maintain
balance (Paloski et al. 1992; Woollacott 1993). Sensory
compensation for pathological loss of sensory informa-
tion has also been found to vary among subjects with
profound bilateral loss of vestibular information (BVL,
bilateral vestibular loss). Fifty percent of these subjects
were able to signiWcantly reduce body sway during sur-
face oscillations by opening their eyes, whereas the
other Wfty percent could not (Buchanan and Horak
2001). Studying BVL subjects using a custom-made
ABF, Hegeman et al. (2005) reported balance improve-
ments when they stood with eyes open on Wrm surface
but not on foam surface or with eyes closed. However,
Hegeman et al. (2005) did not perform any analysis
aimed at understanding how and why individual subjects
were able or unable to use the ABF information to
improve their stability in the diVerent postural tasks.
Exp Brain Res (2007) 178:37–48 39
123
In the study described here, we investigated how
individual subjects’ relative dependence on a particular
sensory channel inXuenced their ability to reduce pos-
tural sway in stance when they used ABF information
to control body sway. The objectives of this research
were (1) to determine the extent to which ABF infor-
mation helps control postural sway given limited
visual, vestibular, and surface somatosensory informa-
tion and (2) to account for why the relative eVective-
ness of ABF varies among individuals across sensory
environments. We used an ABF system, which we
designed to mimic aspects of otolith vestibular infor-
mation by monitoring accelerations in the transverse
plane (Chiari et al. 2005).
Methods
Participants
Nine subjects, four men and Wve women, with pro-
found BVL and nine age- and gender-matched, healthy
control subjects participated in this study. There were
no signiWcant age, height, and weight diVerences
(P > 0.05) between the BVL and control subjects,
respectively: age 55 years (38–73) versus 55 years (33–
72); height 171 cm (160–193) versus 167 cm (151–180);
and weight 71 kg (51–115) versus 73 kg (65–86).
Table 1 summarizes the BVL subjects’ pathologies,
ages, duration of their vestibular loss, and their hori-
zontal vestibulo-ocular reXex (VOR) gain at 0.05 Hz.
Normal VOR gains range from 0.7 to 1 for the control
subjects. All BVL subjects had a bilaterally absent
response to warm and cold water on caloric tests and a
VOR gain of less than 0.3 across a range of oscillations
between 0.01 and 0.1 Hz, indicating severe loss of ves-
tibular function (Peterka and Black 1990). In addition,
each BVL subject fell without an apparent postural
response soon after the start of surface sway-referenc-
ing trials with eyes closed, consistent with their BVL
(Nashner et al. 1982). All of the BVL and control sub-
jects were free of hearing, orthopedic, and neurological
diseases or disorders, except the vestibular pathology
for BVL subjects. Written informed consent was
obtained from all subjects prior to their participation.
The rights of the participants were protected according
to the 1964-Declaration of Helsinki.
Apparatus
For all experiments, the BVL and the control subjects
wore a custom-made ABF system (Chiari et al. 2005)
while standing on an AMTI OR6–6 force plate. The
ABF system provided auditory information to the sub-
jects about their body sway while they stood on the
force plate.
The ABF system is comprised of three main parts:
the sensory unit, the sensory processing unit, and the
audio output unit (Chiari et al. 2005). The sensory unit
consists of a small (1.5 £ 3 £ 3cm
3
) sensor that is
mounted on the subject’s back at L5 with a Velcro belt.
The sensory unit uses 3031 Eurosensor accelerometers
(range §0–50, resolution 2 £ 10
¡4
g, noise 1 v p-p,
temperature error-zero ¡0.05 mV/°C) to sense the lin-
ear accelerations along the anterior–posterior (AP)
and medial–lateral (ML) directions near the body
center of mass. L5 was chosen because its position is
minimally aVected by movement artifacts, such as
respiration, heartbeat, and voluntary head or limb
movement. The processing unit consists of a laptop
computer (Intel Celeron 2.4 GHz) equipped with an
A/D board (DAQCard NI 6024E). It acquires, records,
and processes the AP and ML accelerations sensed by
the sensory unit and encode them into two analog sine
waves that constitute the ABF stereo sound. The
closed-loop delay introduced by the processing was
estimated to be 5 ms. We developed the software for
the processing unit using Matlab© 6 R12 and Matlab
Data Acquisition Toolbox (Chiari et al. 2005). The
audio output unit consists of an ampliWer (Fostex PH-
5) that boosts the two sine waves provided by the com-
puter so that the subjects are able to hear tones
through the earphones (Philips SBC HP-140), with the
tones representing the degree and direction of the
body accelerations.
The force plate estimates body sway in the AP and
ML directions by recording forces and torques under
the subject’s feet. In certain testing conditions, the
force plate was covered with a 10 cm-thick, medium-
density Temper
TM
foam (indentation force deXection
at 25%: 116 N, tensile strength: 125 kN/m
2
, elongation:
109%, when temperature is 22.2°C and relative humidity
Table 1 C
h
aracter
i
st
i
cs of BVL su
bj
ects
i
nc
l
u
di
ng t
h
e vest
ib
u
l
e-
ocular reXex gain (VOR)
Subject’s
ID
Age Diagnosis Duration
of loss (years)
VOR
#1 46 Ototoxicity 7 0.030
#2 50 Idiopathic 12 0.006
#3 56 Idiopathic 14 0.005
#4 60 Ramsey Hunt 3 0.020
#5 61 Ototoxicity 10 0.047
#6 38 Auto immune
disease
70.140
#7 53 Ototoxicity 7 0.260
#8 56 Ototoxicity 10 0.007
#9 73 Ototoxicity 9 0.022
40 Exp Brain Res (2007) 178:37–48
123
is 50%) to reduce somatosensory information about
body sway from the feet. When a subject stands on the
foam, the distance between the subject’s feet and the
force plate continuously changes due to the compliance
of the foam itself. As a consequence, the estimation of
the center of pressure (COP) displacement was theo-
retically not as accurate as without foam. However, the
error of estimation was calculated in post-process and
found to be smaller than 10%. Linear accelerations
from the sensory unit, as well as forces and torques
from the force plate, were acquired with a 100-Hz sam-
ple rate.
Figure 1 shows, from a top-down perspective, four
directions of sway and the relative ABF stereo sound
changes in each earphone, for each direction. The ABF
left–right balance and the volume in the earphones
change according to ML body sway, and the pitch and
volume of the stereo sounds change according to AP
body sway (Chiari et al. 2005). In this study, all sounds
were dynamically adjusted for each subject based on
unique deWnitions of: (1) the region of natural sway
(Mayagoitia et al. 2002), and (2) the area of the sup-
port base that is the region of a safe sway. Using an
inverted-pendulum model (Gage et al. 2004), the
region of natural sway and the region of safe sway were
uniquely calculated for each subject. SpeciWcally, the
region of natural sway was determined by the range of
AP and ML accelerations compatible with an oscilla-
tion of §1° around the vertical, which depended upon
the subject’s height. The region of the safe sway was
determined by the range of AP and ML accelerations
compatible with the subject’s COM projection on the
ground, not exceeding the subject’s base of foot sup-
port. Thus, the region of natural sway and region of
safe sway were used to customize and to optimize the
ABF tones for each subject.
The ABF system was designed so that the tones
changed, depending on the subject’s sway relative to
the calculated region of natural sway. When a subject
swayed within his or her calculated region of natural
sway in the ML and AP directions, the same constant,
low-volume (20 dB-SPL), 400-Hz tone was fed back to
the subject through each earphone. However, when a
subject swayed outside his or her region of natural
sway in the ML direction, the tones in the earphones
simultaneously became louder in the ear correspond-
ing to the direction of body sway and quieter in the
other ear. When the subject swayed outside the region
of natural sway in the anterior direction, the tones
changed equally in both ears and became louder (up to
50 dB-SPL) in volume and higher in pitch (following a
linear function up to 1000 Hz). When the subject
swayed outside the region of natural sway in the pos-
terior direction, the tones changed equally in both ears
and became louder in volume and lower in pitch (fol-
lowing a linear function down to 150 Hz). When the
subject swayed outside the region of natural sway in an
oblique direction, for example in the anterior-left
direction, the tones became higher in pitch in both
ears, louder in volume in the left ear, and quieter in
volume in the right ear. All the equations used to gen-
erate the ABF sound using sigmoidal function are
reported in detail in Chiari et al. (2005).
Procedure
Subjects stood on the force plate and kept their feet 1
externally rotated and their heels 1 cm apart (narrow
stance position). They were instructed to maintain
quiet stance throughout all testing when using and not
using the ABF device. Before the experimental proto-
col began, subjects practiced with the ABF system for a
few minutes on a Wrm surface with eyes open by volun-
tarily swaying at diVerent angles and directions, and lis-
tening to the corresponding changes in tones in the
earphones until they understood how the trunk infor-
mation was coded into the ABF sound. The subjects
were instructed to correct their body sway by using the
tones, i.e., to maintain their sway within the region of
natural sway by achieving a constant 400-Hz tone in
Fig. 1 ABF sound dynamics
encoding postural sway. Pitch
and volume change in the two
earphones, depending on the
direction of sway. The arrows
in the middle of the force
plate (outlined) indicate the
direction of sway. The regions
of natural sway (NS) and safe
sway (SS) were customized
for each subject
Exp Brain Res (2007) 178:37–48 41
123
each earphone. Once they understood how to change
their body sway to achieve the constant 400-Hz tone,
they performed three practice trials with eyes closed
and without ABF, followed by three practice trials with
eyes open on foam and without ABF. The purpose of
the practice trials was for the subjects to gain conW-
dence in standing with eyes closed or standing on the
foam-covered force plate without falling, and to mini-
mize the initial eVects of standing on the foam. Data
from these practice exercises and trials were not con-
sidered in the analyses.
BVL subjects repeated a block of six conditions
three times (18 trials total), and the control subjects
repeated the same block of six conditions Wve times (30
trials total). For each of these blocks, the six conditions
were presented in random order; three conditions were
with and three conditions were without ABF. Condi-
tions one and two were: eyes closed on a Wrm surface
without ABF and with ABF. Conditions three and four
were: eyes open on foam surface without ABF and
with ABF. Conditions Wve and six were: eyes closed on
foam surface without ABF and with ABF. We did not
test the eyes-open on Wrm-surface condition since, in
this condition, the sway of both the BVL and the con-
trol subjects is expected to be inside the region of natu-
ral sway, so there is no need for additional ABF
information (Nashner et al. 1982). The BVL subjects
performed fewer trials to limit fatigue. Each trial lasted
1min.
Data and statistical analysis
From the 2D, planar COP displacement, we quantiWed
postural sway with two independent parameters (Pri-
eto et al. 1996; Rocchi et al. 2004; Maurer et al. 2004):
the root-mean-square distance (COP-RMS) and the
frequency below which the 95% of the power of the
signal is included (F95%). From the 2D, planar accel-
eration measured by the sensory unit, we computed the
RMS (Acc-RMS). To determine the eVect on sway of
subject groups, conditions, and ABF, we performed a
three-way ANOVA, 2 groups (BVL and control) £ 3
sensory conditions (vestibular, somatosensory, and
visual), repeated (eyes closed, eyes open on foam, and
eyes closed on foam) £ 2 ABF conditions, repeated
(ABF on and oV) for each parameter (COP-RMS,
F95%, and Acc-RMS). The threshold for statistical sig-
niWcance was P = 0.05.
To evaluate the correlation between severity of ves-
tibular loss and the eVect of ABF on sway amplitude in
the eyes closed on foam condition, a robust regression
correlation analysis was performed between the VOR
gain and the percentage reduction in COP-RMS, with
and without ABF for BVL subjects. To assess whether
ABF was eVective in helping subjects reduce body
sway in proportion to each subject’s level of depen-
dency on visual and somatosensory information, a
robust regression correlation analysis was performed
between the levels of sensory dependency and the
eVect of ABF on COP-RMS when only visual (eyes
open on foam with ABF condition) or only somatosen-
sory information (eyes closed with ABF condition) was
available. The levels of visual dependency and somato-
sensory dependency were estimated for each subject as
the percentage of the body sway reduction occurring
when visual or somatosensory information was added
(visual information, in the eyes open on foam condi-
tion and somatosensory information, in the eyes closed
condition) and were compared to the reference eyes
closed on foam condition (when neither visual and
somatosensory information was available).
Results
Center of pressure displacement
For BVL and control subjects, body sway increased as
natural sensory information or ABF information
became absent or unreliable. Further, COP-RMS was
signiWcantly larger in the eyes open on foam condition
than in the eyes closed condition (P < 0.05). COP-RMS
was also signiWcantly larger when eyes were closed than
when eyes were open while subjects stood on foam
without ABF (P < 0.01). In the eyes closed, eyes open
on foam, and eyes closed on foam conditions, BVL sub-
jects’ COP-RMS was signiWcantly larger than the con-
trol subjects’ COP-RMS (P < 0.001). Figure
2 shows the
anterior–posterior versus lateral COP displacements of
one representative BVL subject (Fig. 2a) and one rep-
resentative control subject (Fig. 2b), in all six condi-
tions. Table 2 reports the COP-RMS values in the eyes
closed, eyes open on foam, and eyes closed on foam
conditions for both subject groups.
In the three ABF conditions, both groups beneWted
from ABF. That is, ABF signiWcantly decreased COP-
RMS for both the BVL and control groups (P <0.05).
The percentage of changes in COP-RMS due to ABF is
shown in Table 3. No signiWcant interaction was found
between the groups and the conditions tested since
COP-RMS was larger in BVL subjects than in control
subjects in every condition. In addition, there was no
signiWcant interaction between the groups and ABF as
both groups improved in the conditions tested. A sig-
niWcant interaction was found between the condition
factor and the ABF factor (P < 0.001) due to ABF
42 Exp Brain Res (2007) 178:37–48
123
decreasing COP-RMS more in the eyes closed on foam
condition than in the eyes closed or eyes open on foam
condition (Table 3). For the BVL subjects in the eyes
closed on foam condition, a signiWcant interaction was
found among all three ANOVA factors (P <0.001)
due to ABF decreasing COP-RMS the most in the eyes
closed on foam condition for all BVL subjects.
Figure 3 shows the average COP-RMS reduction
when BVL and control subjects used ABF on foam
with eyes closed. As shown in Fig. 3, all but one of the
BVL subjects able to perform the eyes closed on foam
condition beneWted from ABF in this condition. In
addition, BVL subject #2 fell a few times in the eyes
closed on foam condition, but she never fell in this con-
dition while using ABF. BVL subject #1 fell consis-
tently in the eyes closed on foam condition but also
never fell in this condition while using ABF. BVL sub-
ject #8 beneWted from ABF, although minimally when
compared to the other BVL subjects. BVL subject #5
(Fig. 3) was not able to stand in the eyes closed on
foam condition, with or without ABF, although he ben-
eWted from ABF in the other conditions (eyes closed
and eyes open on foam). Also as shown in Fig. 3, all
control subjects beneWted from ABF in the eyes closed
on foam condition.
Frequency spectrum
For BVL and control subjects, the amount of postural
corrections (indicated by the parameter F95%)
decreased as natural sensory information became
available or reliable and increased when ABF informa-
tion was available. SpeciWcally, the frequency spectrum
components of the COP were signiWcantly aVected by
the diVerent test conditions, with the power at the
higher frequencies increasing when visual and/or
somatosensory sensory information was reduced
(P < 0.001). F95% was higher in the eyes closed on
foam condition than in the eyes open on foam condi-
tion (P < 0.05), and higher in the eyes open on foam
condition than in the eyes closed condition (P <0.05).
F95% was also higher for the BVL subject group than
for the control group in all conditions (P <0.001).
Table 2 reports F95% values in the three conditions
tested without ABF for the BVL and control subjects.
The use of ABF signiWcantly increased F95% for both
the BVL and control subjects in all conditions
(P <0.001). Table3 shows the percent of increase in
F95% when controls and BVL subjects used ABF in
each condition. There was a signiWcant interaction
(P < 0.05) between the condition tested and the pres-
ence of a vestibular deWcit, with F95% increasing in the
Fig. 2 COP displacement in the horizontal plane is represented
for a one representative bilateral vestibular loss subject and b one
control subject in the three conditions: (1) eyes closed (EC), (2)
eyes open on foam (EOF), and (3) eyes closed on foam (ECF),
without (black) and with (gray) ABF
a
b
Table 2 Mean values and standard deviation (in parenthesis) of postural parameters for bilateral vestibular loss (BVL) and control sub-
j
ects in the three conditions tested without audio-biofeedback (ABF)
Root mean square distance (RMS) is reported for the center of pressure displacement (COP) and for the acceleration sensed at trunk
level
(
Acc
)
. Also
,
the values of fre
q
uenc
y,
below which the 95% of the
p
ower of the COP si
g
nal is included
,
are re
p
orted
Parameter Eyes closed Eyes open and foam Eyes closed and foam
BVL Control BVL Control BVL Control
COP-RMS (mm) 13.82 (8.9) 8.31 (2.8) 14.01 (9.7) 9.34 (1.2) 24.66 (7.58) 14.92 (3.7)
F95% (Hz) 1.85 (0.55) 1.31 (0.15) 1.87 (0.52) 1.39 (0.19) 2.51 (0.31) 1.59 (0.18)
Acc-RMS (mm/s
2
) 14.12 (8.07) 12.61 (2.4) 16.79 (9.50) 13.48 (1.9) 56.09 (19.13) 21.84 (5.60)
Exp Brain Res (2007) 178:37–48 43
123
BVL subject group more than in the control group,
particularly in the eyes closed on foam condition.
Sensory substitution
Subjects beneWted from ABF information in relation to
the lack of natural sensory information. For most BVL
subjects, the extent that they reduced their body sway
with ABF in the eyes closed on foam condition corre-
lated with the extent of their vestibular loss (r =0.76;
P < 0.05). Table 1 shows the VOR gains and percent-
age of improvement in sway for all of the subjects using
ABF. One subject with very low VOR gain (#9) could
only stand with the ABF in this condition so the per-
centage of improvement could not be calculated.
For both the BVL and control groups, the eVective-
ness of ABF in reducing body sway was related to how
dependent each subject was on visual or somatosen-
sory information, but not on the amount of sway in the
baseline eyes closed on foam condition. Somatosen-
sory-dependent subjects beneWted the most from ABF
when somatosensory information was missing, and
vision-dependent subjects beneWted the most from
ABF when visual information was missing. Figure 4
shows the relative dependence of each subject on
visual or somatosensory information versus the
amount of beneWt that each received from ABF under
conditions in which visual or somatosensory informa-
tion was limited (i.e., the eyes closed and eyes open on
foam conditions). A linear relationship for the BVL
subjects and the control subjects was found between
the degree of beneWt from ABF and their dependence
on visual and somatosensory information, shown by
the greater number of circles in the top-right and bot-
tom-left quadrants of Fig. 4. The circles in the top-right
quadrant represent the subjects who were somatosen-
sory-dependent and beneWted the most from ABF
when somatosensory information was missing. The cir-
cles in the bottom-left quadrant represent subjects who
were vision-dependent and beneWted the most from
ABF when visual information was missing.
Discussion
ABF eYcacy in reducing sway is related
to the availability of sensory information
Results from this study show that the amount that ABF
compensates for missing sensory information depends
on the extent of sensory loss. When somatosensory
information was reduced (the eyes open on foam
Fig. 3 The percentage of COP-RMS reduction using ABF is re-
ported for each bilateral vetibular loss (a) and control (b) subject
in the condition eyes closed on foam. Data were ordered by per-
centage improvement using ABF. Subject numbers indicate
matching subjects between the groups. 9 BVL Subject 2 fell twice
without ABF but never fell during trials using ABF. ‡ BVL Sub-
j
ect 9 fell repeatedly with and without ABF. § BVL Subject 1
could stand only with the help of ABF. Black, dashed lines repre-
sent the mean reduction using ABF. Gray, shadowed areas repre-
sent the standard error of the reduction using ABF
b
a
Table 3 Mean percentage
di
Verence of eac
h
postura
l
parameter w
i
t
h
an
d
w
i
t
h
out au
di
o-
bi
ofee
db
ac
k
(
ABF
)
for
bil
atera
l
vest
ib
u
l
ar
l
oss
(BVL) and control subjects
Root mean square distance (RMS) is reported for the center of pressure displacement (COP) and for the acceleration sensed at trunk
level (Acc). Also, the values of frequency, below which the 95% of the power of the COP signal is included, are reported
Parameter Eyes closed Eyes open and foam Eyes closed and foam
BVL Control BVL Control BVL Control
COP-RMS ¡3.24 ¡10.87 ¡9.98 ¡5.42 ¡23.07 ¡15.90
F95% 21.90 23.01 10.54 18.89 8.38 9.28
Acc-RMS ¡20.82 ¡35.24 ¡27.38 ¡40.56 ¡46.18 ¡32.15
44 Exp Brain Res (2007) 178:37–48
123
condition) and the more that BVL and control subjects
were somatosensory-dependent, the more they beneWted
from ABF and were able to reduce their sway. When
visual information was not available (the eyes closed
condition) and the more that BVL and control subjects
were visually dependent, the more they also beneWted
from ABF and were able to reduce their sway. When
both somatosensory information and visual information
were limited (the eyes closed on foam condition), both
BVL and control groups showed the most beneWt from
ABF. Thus, we hypothesize that the degree to which
subjects beneWt from ABF to reduce postural sway
depends on their degree of visual, somatosensory and
vestibular loss (Lacour et al. 1997; Kluzik et al. 2005).
Our results also showed a trend in which the more
severe the vestibular loss, the more subjects beneWted
from ABF. This trend needs further testing with more
subjects in order to show statistical signiWcance. Our
Wndings are consistent with other studies that also
reported that control and BVL subjects were able to
reduce postural sway with visual, tactile, and audio-
biofeedback (Wall et al. 2001; Hegeman et al. 2005).
However, our study, for the Wrst time, has identiWed a
potential relationship between beneWts from ABF
information and limitation of sensory information.
Both BVL and control subjects’ postural sway
increased when sensory information was limited, con-
Wrming the commonly held hypothesis that the control
of postural sway depends on the amount of available
sensory feedback that is available (Horak et al. 2002;
Dickstein et al. 2001; Peterka 2002). Our BVL subjects
showed signiWcantly larger sway than did our control
subjects in all conditions tested, in agreement with
other studies (Hufschmidt et al. 1980; Black and Nash-
ner 1984; Gagey and Toupet 1991). However, the BVL
subjects’ degree of sway reduction via ABF when
either visual information or somatosensory informa-
tion was available was not related to the extent of their
vestibular loss. This Wnding may be due to the sub-
jects’ hesitance to rely on novel sensory information
(available via ABF) when ordinary sensory informa-
tion normally and extensively used to compensate the
loss of vestibular information (Lacour et al. 1997) was
also available. However, this Wnding may also be
explained by the ABF information not yet being inte-
grated with the subjects’ existing somatosensory and
visual information since they used ABF for only
15 min or less during testing. This lack of integration is
also supported by another study in which we found
that the use of ABF requires a larger number of rapid
postural corrections (Dozza et al. 2005a). Lack of inte-
gration may be the consequence of the subjects’ pay-
ing excessive attention to the ABF, thus interfering
with the attention paid to other sensory information.
It has been shown how dual-task interference
decreases with practice over time when tasks become
quasi-automatic (Schumacher et al. 2001). Conse-
quently, it may be possible for ABF information to
become more integrated with other sensory informa-
tion as when ABF is used after a longer period of time
than just the few minutes in our study (Dault and
Frank 2004
).
Attention to natural sensory information may have
limited ABF eYcacy in BVL subjects
Although BVL subjects reduced their sway more than
the control subjects did in the eyes closed on foam
condition, they did not in the eyes open or in the Wrm
Fig. 4 Subjects in terms of their vision and somatosensory depen-
dency. There is a correlation between the use of ABF in the eyes
closed and eyes open on foam conditions, and visual and somato-
sensory dependency. Each subject’s tendency to rely, more on vi-
sion or somatosensory information is reported on the horizonta
l
axis. Negative values imply a dependency on vision more than on
somatosensory information, whereas positive values imply a
dependency on somatosensory more than on vision information
(a zero value on the horizontal axis indicates a subject who relies
on vision as much as on somatosensory information to maintain
balance in stance). The vertical axis shows the eVect of ABF for
each subject. Positive values imply ABF reduces sway more when
somatosensory information is made unreliable by standing on
foam, negative values imply ABF reduces sway more when visual
information is missing (a zero value on the vertical axis indicates
a subject who, when using ABF, reduces sway when vision infor-
mation is limited as much as when somatosensory information is
inadequate). The Pearson coeYcient for the regression line is
r = 0.57 comprising data from both group and is statistically sig-
niWcant (P < 0.05). The Pearson coeYcients reported in the Wgure
for the two groups of subjects separated (r = 0.62 and r = 0.65 for
bilateral vestibular loss and control subjects, respectively) are not
statistically signiWcant (P > 0.05), however they are close to statis-
tical signiWcance P =0.06
Exp Brain Res (2007) 178:37–48 45
123
surface conditions. In contrast, Hegeman et al. (2005)
found that BVL subjects reduced sway in stance using
ABF only with eyes open on a Wrm surface, but not
with eyes closed and/or when on foam. This diVerent
eVect of ABF may be related to diVerences in: (1) the
design of the ABF systems, (2) the use of trunk angular
velocity instead of linear acceleration that was fed back
to the subjects, (3) the linear algorithm chosen to map
trunk movement into sound, (4) subject selection, and
(5) how postural sway was measured and quantiWed. In
our study, the high degree of attention that BVL sub-
jects normally pay to visual and somatosensory infor-
mation in the eyes closed and eyes open on foam
conditions may have limited their ability to use ABF
since the initial use of ABF requires some a degree of
attention to the tones in the earphones (Dozza et al.
2005a). Indeed, during the rehabilitation period of
BVL subjects, they are taught to pay more voluntary
attention to visual and somatosensory information
than would be the case if they did not have the BVL, to
compensate for the vestibular loss (Shumway-Cook
and Horak 1990; Shumway-Cook et al. 1996). Conse-
quently, focusing more on visual information and
somatosensory information available in the eyes open
on foam and eyes closed conditions, may have inter-
fered with their ability to concentrate on the ABF
(Shumway-Cook et al. 1997; Redfern et al. 2004).
However, in the eyes closed on foam condition, when
visual information and somatosensory information
were limited, subjects could focus their attention on
the ABF. Another explanation for subjects’ decreasing
their sway with ABF is that their use of ABF and the
headphone equipment inXuenced them to pay more
attention to their sway. However, in studies in which
subjects were instructed to deliberately focus their
attention on their body sway and to increase their con-
trol of posture, they did not reduce their sway
(Vuillerme and Nafati 2005). Thus, we believe that the
large sway reduction induced by ABF in BVL subjects
was not likely only due to the subjects’ paying more
attention to their sway.
Use of ABF reduced BVL subjects’ inter-subject
variability
We found a high inter-subject variability among BVL
subjects for all the parameters analyzed, which agrees
with Wndings from many other studies (Hufschmidt
et al. 1980; Black et al. 1988; Gagey and Toupet 1991).
Indeed, two of the nine subjects did not beneWt from
ABF in the eyes closed condition. Some of this vari-
ability may be explained in terms of how individual
BVL subjects compensate for the vestibular loss, which
is by increasing reliance on either visual or somatosen-
sory information (Zacharias and Young 1981; Lacour
et al. 1997). If inter-subject variability depends on the
degree of visual or somatosensory dependency, we
may expect inter-subject variability to decrease when
visual information and somatosensory information are
limited (the eyes closed on foam condition). Indeed,
we found a consistent decrease in inter-subject vari-
ability in this condition, when BVL subjects exhibited
relatively smaller standard deviations (Table 2),
although their sway was larger than in the eyes open on
foam and eyes closed conditions (Black et al. 1999).
Our BVL subjects showed signiWcantly higher fre-
quency of postural corrections (F95%) than did our
control subjects in all conditions tested. This result sug-
gests that BVL subjects were using a diVerent mode of
controlling their balance than were the control subjects
(Creath et al. 2005). However, without kinematic mea-
sures, we cannot distinguish between ankle and hip
sway strategies, as it was done by Creath et al. (2005).
The higher frequency of postural corrections that the
BVL subjects exhibited may also be related to the
higher sensory noise due to the vestibular loss that
BVL have compared to control subjects.
ABF redundancy with sensory information was higher
for BVL than control subjects
In order to better highlight the diV
erence in the use of
ABF information between BVL and control subjects,
we performed a meta-analysis which combined the
results from BVL and control subjects in all the condi-
tion presented in this study in terms of sensory infor-
mation redundancy using Venn diagrams. Redundancy
of sensory information occurs when the same informa-
tion is provided by more than one sensory channel.
Sensory integration for balance is driven by—that is, is
dependent on—redundancy of natural sensory infor-
mation from somatosensory, visual, and vestibular
channels (Creath et al. 2002). Extensive redundancy of
sensory information provides persons with a better
estimate of body segment position and kinematics,
which results in smaller postural sway (Kuo et al. 1998;
van der Kooij et al. 2001).
To quantify sensory redundancy among the natural
sensory information and ABF, we averaged the sway
reduction occurred in the conditions tested (when nat-
ural and ABF sensory information was available) and
represented these averages using Venn diagrams.
Figure 5 shows two Venn diagrams (one for the BVL
subjects and one for the control subjects) that represent
the contributions when all or some of the sensory infor-
mation channels were contributing sensory information to
46 Exp Brain Res (2007) 178:37–48
123
control sway. The size of each diagram and their
percentages represent the percent of COP sway reduc-
tion occurred from a condition in which ABF, somato-
sensory, and visual information are all limited (by
turning oV the ABF device, by using foam, by closing
the eyes, respectively; i.e., the eyes closed on foam
condition without ABF) and a condition when only
one of these information is available.
The redundancy between the ABF contribution in
reducing sway and the contribution from each of the
other sensory information was larger for BVL subjects
(Fig. 5a) than for control subjects (Fig. 5b). For BVL
subjects, ABF reduced sway 46% (4, 11, and 31%)
compared to 32% (12, 7, and 13%) for control subjects
(each of the three percentages in parenthesis is the
amount of redundancy between ABF information and
visual, somatosensory, and both visual and somatosen-
sory, respectively). From these analyses, for BVL sub-
jects, the redundancy among somatosensory, visual,
and ABF information was higher (31%) than for con-
trol subjects (13%). The greater redundancy in BVL
than control subjects suggests that compensating for
vestibular loss depends on more extensive sensory
redundancy between visual and somatosensory infor-
mation. Figure 5 shows that ABF information can also
be redundant with visual and somatosensory sensory
information, suggesting that the CNS may treat ABF
information similarly to natural sensory information.
Also, since redundancy between ABF information and
other sensory information is greater for BVL subjects
than for control subjects, BVL subjects may beneWt
more from the ABF information than may control sub-
jects, especially in sensory-deprived situations. In fact,
with more practice, ABF information may also facili-
tate a more accurate integration and calibration of
sensory information, induced by the CNS continually
comparing natural sensory information to ABF infor-
mation.
The use of foam to limit somatosensory information
may have limited in the accuracy of sensory redun-
dancy estimation. In fact, when determining the role
that the somatosensory information plays in reducing
sway (Fig. 5), we did not include all somatosensory
information that the CNS received from the entire
body but only the somatosensory information from the
subject’s feet which was restricted by using the foam.
Even with these qualiWcations, Fig. 5 provides new
insight into the mechanisms of sensory redundancy and
sensory re-weighing during human stance.
Conclusions
We found that the BVL and the control subjects used
ABF information about their trunk acceleration to
control sway, in proportion to the extent that their
other sensory information was reduced. In addition, all
subjects used ABF diVerently, depending on their indi-
vidual proclivities to rely on vestibular, somatosensory,
or visual information in order to control sway. Redun-
dancy between sensory information from diVerent sen-
sory channels and ABF information was larger in BVL
subjects than in control subjects, suggesting that ABF
information may help subjects compensate for vestibu-
lar loss by facilitating the CNS’s integration of sensory
information.
Acknowledgments We would like to thank Dr. Conrad Wall
and Dr. Angelo Cappello for stimulating inspiration, Dr. Sandra
Oster for English editing and education, Andrew Owings and Dr.
Charles Russell for technical support, Triana Nagel-Nelson for
recruitment of subjects, and all of our subjects for donating their
time. We also thank Dr. Velio Macellari and Dr. Daniele Gian-
santi for having made available the portable measurement sys-
tem. This study was supported by NIH grants DC01849,
DC04082, and DC06201.
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... Additional sensory cues can be provided through auditory, tactile, or visual systems. Multiple studies have reported improvement in balance control during sensory augmentation for healthy adults [11][12][13][14][15][16], healthy older adults [17], and in adults with vestibular dysfunction [13,[18][19][20][21][22][23][24]. A reduction in the body sway amplitude, with additional sensory cues, is inversely related to the reliability of intrinsic sensory feedback. ...
... A reduction in the body sway amplitude, with additional sensory cues, is inversely related to the reliability of intrinsic sensory feedback. Therefore, populations with balance control impairment benefit the most from additional sensory cues [12][13][14]22]. Healthy young adults have little improvement potential, likely because of a ceiling effect [22]. ...
... Therefore, populations with balance control impairment benefit the most from additional sensory cues [12][13][14]22]. Healthy young adults have little improvement potential, likely because of a ceiling effect [22]. Contrary to the visual and auditory stimuli, the tactile ...
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For individuals with altered sensory cues, vibrotactile feedback improves their balance control. However, should vibrotactile feedback be provided every time balance control is compromised, or only one-third of the time their balance is compromised? We hypothesized that vibrotactile feedback would improve balance control more when provided every time their balance is compromised. Healthy young adults were randomly assigned to two groups: group 33% feedback (6 males and 6 females) and group 100% feedback (6 males and 6 females). Vibrotactile feedbacks related to the body’s sway angle amplitude and direction were provided, while participants stood upright on a foam surface with their eyes closed. Then, we assessed if balance control improvement lasted when the vibrotactile feedback was removed (i.e., post-vibration condition). Finally, we verified whether or not vibrotactile feedback unrelated to the body’s sway angle and direction (sham condition) altered balance control. The results revealed no significant group difference in balance control improvement during vibrotactile feedback. Immediately following vibrotactile feedback, both groups reduced their balance control commands; body sway velocity and the ground reaction forces variability decreased. For both groups, unrelated vibrotactile feedback worsened balance control. These results confirmed that participants processed and implemented vibrotactile feedback to control their body sways. Less vibrotactile feedback was effective in improving balance control.
... In the past, there has been much discussion about biofeedback systems for the prevention of falls through training and/or the use of wearable systems. Several studies have been developed based on audio, video, and vibrotactile biofeedback systems [4][5][6][7][8][9][10][11][12][13][14][15][16][17][18][19], some involving some of us as authors [8,13]. Many of these wearable systems were considered even before the smartphone boom as we know it today [9][10][11][12][13][14][15][16][17][18][19]. ...
... Several studies have been developed based on audio, video, and vibrotactile biofeedback systems [4][5][6][7][8][9][10][11][12][13][14][15][16][17][18][19], some involving some of us as authors [8,13]. Many of these wearable systems were considered even before the smartphone boom as we know it today [9][10][11][12][13][14][15][16][17][18][19]. Some recent studies are continuing in this direction [20][21][22][23]. ...
... Some recent studies are continuing in this direction [20][21][22][23]. The use of inertial sensors, such as accelerometers, for stability control [24][25][26] integrated in wearable systems equipped with biofeedback [4][5][6][7][8][9][10][11][12][13][14][15][16][17][18][19][20][21][22][23] will certainly provide an increasingly important response in the prevention of falls. ...
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We are writing to you as the corresponding authors of the interesting systematic review study “Pathway of Trends and Technologies in Fall Detection: A Systematic Review” [...]
... IMUs are particularly well suited for sensory-augmented balance and coordination training, since they are widely integrated into wearable or portable wireless devices, such as smartwatches and phones. Regardless of the specific type of feedback modality (vibrotactile feedback [42], surface electrode stimulation of the vestibular nerve [43], electric currents applied to the tongue [44][45][46], auditory [47,48], visual [49], or multimodal feedback [50]), participants with sensory disabilities (e.g., vestibular disabilities [42,51], peripheral neuropathy [52], and motor disabilities (e.g., Parkinson's disease [53][54][55]) have used SA cues to make postural and gait-related corrections. ...
... Ellipse area captures the amplitude of the overall displacement of the individual from their initial position over the course of the 30-second exercise, and path length captures the "angular distance" traveled within that displacement. Lower RMS sway, path length, and ellipse area values are associated with increased postural stability [42,48]. Higher RMS Sway Velocities can indicate increased sway amplitude or sway frequency [72]. ...
... Ellipse area captures the amplitude of the overall displacement of the participant from their initial position over the course of the 30-second exercise, and path length captures the "angular distance" traveled within that displacement. Lower RMS sway, path length, and ellipse area values are associated with increased postural stability [42,48]. Higher RMS Sway Velocities can indicate increased sway amplitude or sway frequency [72]. ...
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Intensive balance and coordination training is the mainstay of treatment for symptoms of impaired balance and mobility in individuals with hereditary cerebellar ataxia. In this study, we compared the effects of home-based balance and coordination training with and without vibrotactile SA for individuals with hereditary cerebellar ataxia. Ten participants (five males, five females; 47 ± 12 years) with inherited forms of cerebellar ataxia were recruited to participate in a 12-week crossover study during which they completed two six-week blocks of balance and coordination training with and without vibrotactile SA. Participants were instructed to perform balance and coordination exercises five times per week using smartphone balance trainers that provided written, graphic, and video guidance and measured trunk sway. The pre-, per-, and post-training performance were assessed using the Scale for the Assessment and Rating of Ataxia (SARA), SARAposture&gait sub-scores, Dynamic Gait Index, modified Clinical Test of Sensory Interaction in Balance, Timed Up and Go performed with and without a cup of water, and multiple kinematic measures of postural sway measured with a single inertial measurement unit placed on the participants’ trunks. To explore the effects of training with and without vibrotactile SA, we compared the changes in performance achieved after participants completed each six-week block of training. Among the seven participants who completed both blocks of training, the change in the SARA scores and SARAposture&gait sub-scores following training with vibrotactile SA was not significantly different from the change achieved following training without SA (p>0.05). However, a trend toward improved SARA scores and SARAposture&gait sub-scores was observed following training with vibrotactile SA; compared to their pre-vibrotacile SA training scores, participants significantly improved their SARA scores (mean=−1.21, p=0.02) and SARAposture&gait sub-scores (mean=−1.00, p=0.01). In contrast, no significant changes in SARAposture&gait sub-scores were observed following the six weeks of training without SA compared to their pre-training scores immediately preceding the training block without vibrotactile SA (p>0.05). No significant changes in trunk kinematic sway parameters were observed as a result of training (p>0.05). Based on the findings from this preliminary study, balance and coordination training improved the participants’ motor performance, as captured through the SARA. Vibrotactile SA may be a beneficial addition to training regimens for individuals with hereditary cerebellar ataxia, but additional research with larger sample sizes is needed to assess the significance and generalizability of these findings.
... Balance and enhancement of functional movement are important variables for rehabilitation in patients with stroke [9]. Providing additional sensations via the vestibular, visual, and somatosensory systems as biofeedback during the process of training balance and weight shifting in post-stroke patients is more effective in enhancing balance ability by activating sensation and motor integration in the central nervous system [10,11]. This helps to teach accurate movements by correcting errors while performing tasks by receiving feedback stimulation from the exercise performed by oneself or information related to movement from the vestibular, visual, and somatosensory systems [12]. ...
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Training with visual and auditory biofeedback, in patients with stroke, improved balance ability and asymmetric posture. We developed a new biofeedback training device to prevent falls and improve balance ability in patients with stroke. This device corrects motion errors by collecting the pressure information of patients in real-time. This randomized crossover study aimed to investigate the effect of this biofeedback training on the static balance ability and weight distribution symmetry index in 24 patients with chronic stroke. Pressure sensor-based vibrotactile biofeedback, visual biofeedback providing posture information, and standing without biofeedback were randomly applied for 1 d each with 24 h washout intervals to minimize adaptation. The static balance ability was measured for each biofeedback training type, and the weight distribution symmetry index was calculated using the collected weight-bearing rate data. The static balance ability and weight distribution symmetry index differed significantly according to the type of biofeedback training used. Post-hoc analysis revealed significant differences in the order of newly developed vibrotactile biofeedback, visual biofeedback, and standing without biofeedback. These findings provide evidence that pressure sensor-based vibrotactile biofeedback improves static balance ability and weight support rates by proposing better intervention for patients with chronic stroke in the clinical environment.
... Limitations and future research. Systems that provide sound feedback on movement in real-time have been found to increase bodily awareness and influence movement (e.g., 46,47 ) and are increasingly being used in the context of musical expression 95 , dance (e.g., 96 ), sports (e.g., [97][98][99], general physical activity (e.g., 38,45 ) and physical rehabilitation (e.g., 100,101 ) for example, in people with chronic stroke [102][103][104][105] , vestibular disorders (e.g., 106,107 ), chronic pain (e.g., 47,49 ) or autism (e.g. 108 ). ...
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The effects of music on bodily movement and feelings, such as when people are dancing or engaged in physical activity, are well-documented—people may move in response to the sound cues, feel powerful, less tired. How sounds and bodily movements relate to create such effects? Here we deconstruct the problem and investigate how different auditory features affect people’s body-representation and feelings even when paired with the same movement. In three experiments, participants executed a simple arm raise synchronised with changing pitch in simple tones (Experiment 1), rich musical sounds (Experiment 2) and within different frequency ranges (Experiment 3), while we recorded indirect and direct measures on their movement, body-representations and feelings. Changes in pitch influenced people’s general emotional state as well as the various bodily dimensions investigated—movement, proprioceptive awareness and feelings about one’s body and movement. Adding harmonic content amplified the differences between ascending and descending sounds, while shifting the absolute frequency range had a general effect on movement amplitude, bodily feelings and emotional state. These results provide new insights in the role of auditory and musical features in dance and exercise, and have implications for the design of sound-based applications supporting movement expression, physical activity, or rehabilitation.
... If this is achieved, the sonified feedback can theoretically highlight task-relevant information already present in intrinsic channels, facilitating sensorimotor associative learning below the level of conscious perception (Makino et al., 2016;Morone et al., 2021). Alternatively, sonification can be used as a form of sensory substitution, filling in for another task-critical sensory stream that is either damaged or missing, such as vestibular, visual or somatosensory loss in balance training (Dozza et al., 2007;Costantini et al., 2018). ...
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Interactive sonification of biomechanical quantities is gaining relevance as a motor learning aid in movement rehabilitation, as well as a monitoring tool. However, existing gaps in sonification research (issues related to meaning, aesthetics, and clinical effects) have prevented its widespread recognition and adoption in such applications. The incorporation of embodied principles and musical structures in sonification design has gradually become popular, particularly in applications related to human movement. In this study, we propose a general sonification model for the sit-to-stand (STS) transfer, an important activity of daily living. The model contains a fixed component independent of the use-case, which represents the rising motion of the body as an ascending melody using the physical model of a flute. In addition, a flexible component concurrently sonifies STS features of clinical interest in a particular rehabilitative/monitoring situation. Here, we chose to represent shank angular jerk and movement stoppages (freezes), through perceptually salient pitch modulations and bell sounds. We outline the details of our technical implementation of the model. We evaluated the model by means of a listening test experiment with 25 healthy participants, who were asked to identify six normal and simulated impaired STS patterns from sonified versions containing various combinations of the constituent mappings of the model. Overall, we found that the participants were able to classify the patterns accurately (86.67 ± 14.69% correct responses with the full model, 71.56% overall), confidently (64.95 ± 16.52% self-reported rating), and in a timely manner (response time: 4.28 ± 1.52 s). The amount of sonified kinematic information significantly impacted classification accuracy. The six STS patterns were also classified with significantly different accuracy depending on their kinematic characteristics. Learning effects were seen in the form of increased accuracy and confidence with repeated exposure to the sound sequences. We found no significant accuracy differences based on the participants' level of music training. Overall, we see our model as a concrete conceptual and technical starting point for STS sonification design catering to rehabilitative and clinical monitoring applications.
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Background: A method for prescribing the difficulty or intensity of standing balance exercises has been validated in a healthy population, but requires additional validation in individuals with vestibular disorders. Objective: This study validated the use of ratings of perceived difficulty for estimation of balance exercise intensity in individuals with vestibular disorders. Methods: Eight participants with a confirmed diagnosis of a vestibular disorder and 16 healthy participants performed two sets of 16 randomized static standing exercises across varying levels of difficulty. Root Mean Square (RMS) of trunk angular velocity was recorded using an inertial measurement unit. In addition, participants rated the perceived difficulty of each exercise using a numerical scale ranging from 0 (very easy) to 10 (very difficult). To explore the concurrent validity of rating of perceived difficulty scale, the relationship between ratings of perceived difficulty and sway velocity was assessed using multiple linear regression for each group. Results: The rating of perceived difficulty scale demonstrated moderate positive correlations RMS of trunk velocity in the pitch (r = 0.51, p < 0.001) and roll (r = 0.73, p < 0.001) directions in participants with vestibular disorders demonstrating acceptable concurrent validity. Conclusions: Ratings of perceived difficulty can be used to estimate the intensity of standing balance exercises in individuals with vestibular disorders.
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This study investigated claims of disrupted equilibrium when listening to the Shepard–Risset glissando (which creates an auditory illusion of perpetually ascending/descending pitch). During each trial, 23 participants stood quietly on a force plate for 90 s with their eyes either open or closed (30 s pre-sound, 30 s of sound and 30 s post-sound). Their centre of foot pressure (CoP) was continuously recorded during the trial and a verbal measure of illusory self-motion (i.e., vection) was obtained directly afterwards. As expected, vection was stronger during Shepard–Risset glissandi than during white noise or phase-scrambled auditory control stimuli. Individual differences in auditorily evoked postural sway (observed during sound) were also found to predict the strength of this vection. Importantly, the patterns of sway induced by Shepard–Risset glissandi differed significantly from those during our auditory control stimuli — but only in terms of their temporal dynamics. Since significant sound type differences were not seen in terms of sway magnitude, this stresses the importance of investigating the temporal dynamics of sound–posture interactions.
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This study assessed whether stationary auditory information could affect body and head sway (as does vi-sual and haptic information) in sighted and congenitally blind people. Two speakers, one placed adjacent to each ear, significantly stabilized center-of-foot-pressure sway in a tandem Romberg stance, while neither a single speak-er in front of subjects nor a head-mounted sonar device reduced center-of-pressure sway. Center-of-pressure sway was reduced to the same level in the two-speaker condi-tion for sighted and blind subjects. Both groups also evi-denced reduced head sway in the two-speaker condition, although blind subjects head sway was significantly larg-er than that of sighted subjects. The advantage of the two-speaker condition was probably attributable to the nature of distance compared with directional auditory informa-tion. The results rule out a deficit model of spatial hearing in blind people and are consistent with one version of a compensation model. Analysis of maximum cross-corre-lations between center-of-pressure and head sway, and as-sociated time lags suggest that blind and sighted people may use different sensorimotor strategies to achieve sta-bility.
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An adaptive estimator model of human spatial orientation is presented. The adaptive model dynamically weights sensory error signals. More specific, the model weights the difference between expected and actual sensory signals as a function of environmental conditions. The model does not require any changes in model parameters. Differences with existing models of spatial orientation are that: (1) environmental conditions are not specified but estimated, (2) the sensor noise characteristics are the only parameters supplied by the model designer, (3) history-dependent effects and mental resources can be modelled, and (4) vestibular thresholds are not included in the model; instead vestibular-related threshold effects are predicted by the model. The model was applied to human stance control and evaluated with results of a visually induced sway experiment. From these experiments it is known that the amplitude of visually induced sway reaches a saturation level as the stimulus level increases. This saturation level is higher when the support base is sway referenced. For subjects experiencing vestibular loss, these saturation effects do not occur. Unknown sensory noise characteristics were found by matching model predictions with these experimental results. Using only five model parameters, far more than five data points were successfully predicted. Model predictions showed that both the saturation levels are vestibular related since removal of the vestibular organs in the model removed the saturation effects, as was also shown in the e xperiments. It seems that the nature of these vestibular-related threshold effects is not physical, since in the model no threshold is included. The model results suggest that vestibular-related thresholds are the result of the processing of noisy sensory and motor output signals. Model analysis suggests that, especially for slow and small movements, the environment postural orientation can not be estimated optimally, which causes sensory illusions. The model also confirms the experimental finding that postural orientation is history dependent and can be shaped by instruction or mental knowledge. In addition the model predicts that: (1) vestibular-loss patients cannot handle sensory conflicting situations and will fall down, (2) during sinusoidal support-base translations vestibular function is needed to prevent falling, (3) loss of somatosensory information from the feet results in larger postural sway for sinusoidal support-base translations, and (4) loss of vestibular function results in falling for large support-base rotations with the eyes closed. These predictions are in agreement with experimental results.
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It is generally accepted that human bipedal upright stance is achieved by feedback mechanisms that generate an appropriate corrective torque based on body-sway motion detected primarily by visual, vestibular, and proprioceptive sensory systems. Because orientation information from the various senses is not always available (eyes closed) or accurate (compliant support surface), the postural control system must somehow adjust to maintain stance in a wide variety of environmental conditions. This is the sensorimotor integration problem that we investigated by evoking anterior-posterior (AP) body sway using pseudorandom rotation of the visual surround and/or support surface (amplitudes 0.5–8°) in both normal subjects and subjects with severe bilateral vestibular loss (VL). AP rotation of body center-of-mass (COM) was measured in response to six conditions offering different combinations of available sensory information. Stimulus-response data were analyzed using spectral analysis to compute transfer functions and coherence functions over a frequency range from 0.017 to 2.23 Hz. Stimulus-response data were quite linear for any given condition and amplitude. However, overall behavior in normal subjects was nonlinear because gain decreased and phase functions sometimes changed with increasing stimulus amplitude. “Sensory channel reweighting” could account for this nonlinear behavior with subjects showing increasing reliance on vestibular cues as stimulus amplitudes increased. VL subjects could not perform this reweighting, and their stimulus-response behavior remained quite linear. Transfer function curve fits based on a simple feedback control model provided estimates of postural stiffness, damping, and feedback time delay. There were only small changes in these parameters with increasing visual stimulus amplitude. However, stiffness increased as much as 60% with increasing support surface amplitude. To maintain postural stability and avoid resonant behavior, an increase in stiffness should be accompanied by a corresponding increase in damping. Increased damping was achieved primarily by decreasing the apparent time delay of feedback control rather than by changing the damping coefficient (i.e., corrective torque related to body-sway velocity). In normal subjects, stiffness and damping were highly correlated with body mass and moment of inertia, with stiffness always about 1/3 larger than necessary to resist the destabilizing torque due to gravity. The stiffness parameter in some VL subjects was larger compared with normal subjects, suggesting that they may use increased stiffness to help compensate for their loss. Overall results show that the simple act of standing quietly depends on a remarkably complex sensorimotor control system.
Chapter
The second edition of this definitive text, covering all clinical aspects of human locomotion and its disorders. Multidisciplinary in authorship and approach, it is divided into sections on normal development, assessment, clinical disorders, rehabilitation, and problems specific to the elderly, maintaining the clinical focus throughout. The text has been updated and revised throughout, incorporating both existing knowledge and new developments. Important additions to the second edition include new chapters on techniques for gait analysis, peripheral neuropathies and dizziness.
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It is generally accepted that human bipedal upright stance is achieved by feedback mechanisms that generate an appropriate corrective torque based on body-sway motion detected primarily by visual, vestibular, and proprioceptive sensory systems. Because orientation information from the various senses is not always available (eyes closed) or accurate (compliant support surface), the postural control system must somehow adjust to maintain stance in a wide variety of environmental conditions. This is the sensorimotor integration problem that we investigated by evoking anterior-posterior (AP) body sway using pseudorandom rotation of the visual surround and/or support surface (amplitudes 0.5-8degrees) in both normal subjects and subjects with severe bilateral vestibular loss (VL). AP rotation of body center-of-mass (COM) was measured in response to six conditions offering different combinations of available sensory information. Stimulus-response data were analyzed using spectral analysis to compute transfer functions and coherence functions over a frequency range from 0.017 to 2.23 Hz. Stimulus-response data were quite linear for any given condition and amplitude. However, overall behavior in normal subjects was nonlinear because gain decreased and phase functions sometimes changed with increasing stimulus amplitude. "Sensory channel reweighting" could account for this nonlinear behavior with subjects showing increasing reliance on vestibular cues as stimulus amplitudes increased. VL subjects could not perform this reweighting, and their stimulus-response behavior remained quite linear. Transfer function curve fits based on a simple feedback control model provided estimates of postural stiffness, damping, and feedback time delay. There were only small changes in these parameters with increasing visual stimulus amplitude. However, stiffness increased as much as 60% with increasing support surface amplitude. To maintain postural stability and avoid resonant behavior, an increase in stiffness should be accompanied by a corresponding increase in damping. Increased damping was achieved primarily by decreasing the apparent time delay of feedback control rather than by changing the damping coefficient (i.e., corrective torque related to body-sway velocity). In normal subjects, stiffness and damping were highly correlated with body mass and moment of inertia, with stiffness always about 1/3 larger than necessary to resist the destabilizing torque due to gravity. The stiffness parameter in some VL subjects was larger compared with normal subjects, suggesting that they may use increased stiffness to help compensate for their loss. Overall results show that the simple act of standing quietly depends on a remarkably complex sensorimotor control system.
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Abnormal vestibular function disrupts a subject's reference to gravity (earth) vertical, and prevents resolution of conflicting or inaccurate visual and somatosensory spatial references. However, errors which patients make when attempting to resolve conflicting visual and somatosensory orientation inputs during upright stance differed markedly in patients with (1) symmetric or asymmetric reduced vestibular function, (2) benign paroxysmal positional nystagmus and vertigo, and (3) a combination of distorted and reduced function. Objective characterization of spatial orientation systems and compensatory strategies under altered sensory conditions is an essential first step toward identifying optimal treatment methods for each of these three types of vestibular deficient patients.
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Despite extensive research on the influence of visual, vestibular and somatosensory information on human postural control, it remains unclear how these sensory channels are fused for self-orientation. The focus of the present study was to test whether a linear additive model could account for the fusion of touch and vision for postural control. We simultaneously manipulated visual and somatosensory (touch) stimuli in five conditions of single- and multisensory stimulation. The visual stimulus was a display of random dots projected onto a screen in front of the standing subject. The somatosensory stimulus was a rigid plate which subjects contacted lightly (<1N of force) with their right index fingertip. In each condition, one sensory stimulus oscillated (dynamic) in the medial-lateral direction while the other stimulus was either dynamic, static or absent. The results qualitatively supported five predictions of the linear additive model in that the patterns of gain and variability across conditions were consistent with model predictions. However, a strict quantitative comparison revealed significant deviations from model predictions, indicating that the sensory fusion process clearly has nonlinear aspects. We suggest that the sensory fusion process behaved in an approximately linear fashion because the experimental paradigm tested postural control very close to the equilibrium point of vertical upright.