BASIC AND CLINICAL ASPECTS OF VERTIGO AND DIZZINESS

Vestibular and Proprioceptive Contributions

to Human Balance Corrections
Aiding These with Prosthetic Feedback
C.G.C. Horlings,a M.G. Carpenter,b F. Honegger,a
and J.H.J. Alluma
a
Department of ORL, University Hospital, Basel, Switzerland
b
School of Human Kinetics, University of British Columbia, Vancouver, British
Columbia, Canada

Movement strategies controlling quiet stance and rapid balance corrections may have
common characteristics. We investigated this assumption for lower leg proprioceptive
loss (PL), peripheral vestibular loss (VL), and healthy controls. Our underlying hypoth-
esis was that changes in movement-strategy modulation following sensory loss would
improve with prosthetic biofeedback. Quiet stance was measured under different sen-
sory conditions and compared to corrections induced by multidirection support-surface
tilts. Response synergies were assessed using electromyography recordings from sev-
eral muscles. Biofeedback of trunk sway during gait and stance tasks used lower trunk
rotations to drive head-band-mounted vibro-tactile and auditory actuators. Strategies
of quiet stance were different for roll and pitch, depending on sensory conditions. Si-
multaneously acting strategies were observed for low- and high-frequency sway. PL
induced strategies different from those of VL and controls. VL strategies were identical
to those of controls but with greater amplitudes. Tilt perturbation movement strategies
were similar to high-frequency strategies of quiet stancemultisegmental. VL induced
increased trunk pitch and roll responses with hypermetric trunk muscle responses and
hypometric knee responses but unchanged synergies. Increasing PL up the legs caused
changed synergies. Biofeedback reduced stance body sway in VL and elderly subjects.
In conclusion, several movement strategies underlie quiet stance with high-frequency
strategies being common to those of perturbed stance. PL changes both movement
strategies and synergies, whereas VL only causes pathological changes to the modula-
tion depth. Thus, VL is more easily rectified using trunk sway positional biofeedback.

Key words: balance control; movement strategies; vestibular loss; leg proprioceptive
loss; biofeedback rehabilitation of imbalance

Introduction assumed that an appropriately scaled balance-

Vestibular and proprioceptive sensory infor-
mation is considered essential for stable bal-
ance. If one motion percept is not available
when stance suddenly becomes unstable, it is
Address for correspondence: Prof. Dr. Biomed. Eng. J.H.J. Allum,
Department of Audiology and Neurootology, Universitatsspital Basel, CH-
4031 Basel, Switzerland. Voice: +41-61-265-2040; fax: +41-61-265-2750.
jallum@uhbs.ch
correcting response will not be properly gen-
erated and a fall will occur. This assumption
raises a number of questions concerning the
effect of vestibular or proprioceptive loss (VL
or PL) on movement strategies and underlying
muscle response synergies.
Most evidence indicates that vestibular in-
puts do not trigger balance corrections. Instead,
the role of vestibular-spinal inputs on balance
corrections is to modulate the amplitude of

Basic and Clinical Aspects of Vertigo and Dizziness: Ann. N.Y. Acad. Sci. 1164: 112 (2009).
doi: 10.1111/j.1749-6632.2009.03872.x  c 2009 New York Academy of Sciences.

1
2 Annals of the New York Academy of Sciences
postural muscle responses,14 and is specific to
the roll and pitch planes.5 In contrast, lower
leg proprioceptive feedback has long been con-
sidered critical for triggering and modulating
balance-correcting responses,69 although, re-
cent evidence has indicated that proprioceptive
inputs from more proximal joints (such as the
hip joint) could fulfill this role.1012 For exam-
ple, when the support surface is servoed during
translation so that ankle rotations are negligi-
ble and stretch reflexes in ankle muscles are
absent,3,13 balance corrections are still present
and appropriately modulated to maintain sta-
bility. These results suggest that ankle proprio-
ceptive inputs are not always required for trig-
gering and modulating balance corrections.13
Furthermore, if proprioceptive inputs at other
joints are able to act as a substitute for the ab-
sence of ankle inputs, then movements at other
joints need to have occurred, as has been ver-
ified by observations of multisegmental move-
ment during both translations and rotations of
the support surface.10,16
Movements at joints other than at the ankle
during quiet stance or following a perturbation
to stance are essential if a distributed use of pro-
prioceptive inputs is to contribute to balance
control.3 It has generally been assumed that
the body sways primarily as an inverted pendu-
lum during quiet stance with little movement
at the knee and hip joints.14,15 However, the
concept of movement as an inverted pendulum
has recently been challenged, suggesting that
more than one mode of movement, including
that like an inverted pendulum, occurs simul-
taneously.17,18 Whether or not these modes of
control during quiet stance are affected by PL
or VL is not known. Furthermore, these modes
of control have only been explored in the pitch
plane.
The aim of the current study was to com-
pare the modes of control in healthy, VL, and
PL subjects during quiet stance33 to those un-
derlying balance corrections to support-surface
perturbations.1113,27 Having established dif-
ferences between these populations, our goal
was to apply this knowledge to rehabili-
tation concepts using biofeedback of body
sway.23,24
Methods
Subjects
For investigating movement strategies dur-
ing quiet stance subjects included six VL pa-
tients (all male; mean age [range] 40.7 [21
48] years), six PL patients (three male; 57.5
[2770] years) and 28 healthy, age-matched
controls (16 male; 46.2 [2869] years).33 Sim-
ilar subject demographics and numbers were
used for experiments with support-surface per-
turbations.11 Criteria for subject selection are
listed in previous publications.1113,33 All sub-
jects signed informed consent as approved by
the ethical committees of the University Hos-
pital Basel and the Radboud University Ni-
jmegen Medical Center.
Procedure for Quiet Stance Experiments
Subjects stood without shoes with feet apart
at shoulder width and with their arms hanging
at the sides of their body during two postural
tasks: standing on two legs with eyes closed on
1) a firm support or 2) a foam support surface.
The sequence was randomized for firm and
foam support surfaces to restrict influence of a
training effect. Two spotters were positioned in
case balance was lost. All tasks lasted 3 min or
until balance control was lost. In this case, the
task was repeated; the longest of a maximum
of three trials was used for analysis. However,
trials shorter than 20 sec were excluded from
the analysis.
Two digital angular-rate gyroscopes
(SwayStarTM , Balance International Innova-
tions GmbH, Switzerland) mounted on con-
verted motorcycle kidney belts, were synchro-
nized to measure angular velocity in the roll
(side-to-side) and pitch (fore-aft) planes at
the pelvis and at the shoulder with a rate
of 100 Hz. Pelvis and shoulder velocity data
Horlings et al.: Vestibular and Proprioceptive Contributions to Balance
were integrated to yield position data and
then partitioned into low-frequency and
high-frequency sway, after removal of the very
low-frequency trend using wavelet analysis.
The remaining swayoriginal data minus the
low-frequency trendwas further analyzed
in two separate frequency bands. The first
band consisted of low-pass filtered sway with a
cutoff frequency of 0.7 Hz. The second band
consisted of high-pass filtered sway with a
cutoff frequency of 3 Hz. Once these data were
low- or high-pass filtered, a weighted total
least-squares algorithm was used for fitting
a regression line to the shoulderpelvis x-y
plots.
Procedure for Perturbed Stance
Balance control was examined in a simi-
lar way as in previous studies.5,1120 Briefly,
subjects stood barefoot with their feet lightly
strapped into heel guides fixed to the surface of
a dual-axis rotating platform. Thus the subjects
used in-place balance-correcting strategy, not
stepping reactions, to correct for the support-
surface tilt. Stance width was the same for all
subjects (14 cm). Subjects were requested to
stand with their arms hanging by their sides.
Two handrails (adjusted to the height of the
wrist of each subject) were located 40 cm from
the sides of the platform center. Two spotters
were positioned to lend support in case of a fall.
Perturbations to upright stance were deliv-
ered by rotating the platform randomly in one
of eight different directions with a constant ve-
locity of 60 deg/sec and constant amplitude
of 7.5 deg. The perturbation directions were
forward (toes-down or 0 deg), backward (toes-
up or 180 deg), right (90 deg), left (270 deg)
and four combinations of pitch and roll, in-
cluding forward right (45 deg), backward right
(135 deg), backward left (225 deg), and forward
left (315 deg).
Recordings of all biomechanical and elec-
tromyographical (EMG) data commenced 100
msec prior to perturbation onset and were
collected for 1 sec. Full body kinematic data
3
were collected using a three-dimensional opti-
cal tracking system with 21 infrared-emitting
diodes (IREDs) (Optotrak, Northern Digi-
tal). Marker positions and joint angle anal-
ysis procedures are described in Visser and
colleagues.20
Head linear and angular accelerations were
computed from the outputs of four dual-axis
linear accelerometers (Entran), with ranges
of 5 g, each mounted at 90 deg separation on
a lightweight, adjustable, tight head-band.5,11
All analog computed signals were sampled at 1
KHz.
EMG recordings were obtained using pre-
viously described techniques.4,5,11 To record
EMG signals, pairs of silversilver chloride elec-
trodes were placed approximately 3 cm apart
along the muscle bellies of left tibialis anterior,
soleus, quadriceps, hamstrings, left and right
gluteus medius, left and right paraspinals at the
L1-L2 level of the spine, left biceps, and left
medial deltoid muscles.
Following analog to digital conversion of the
data, all biomechanical and EMG signals were
averaged offline across each perturbation direc-
tion. Subject averages were pooled to produce
population averages for a single direction. Zero
latency was defined as the onset of platform
rotation measured with potentiometer systems
on platform axes.
Results
Movement Strategies during
Quiet Stance
In controls the low-frequency movements of
the shoulder and pelvis were found to be in
phase in both the pitch and roll planes (Fig. 1B
and G).33 When the pelvis and shoulder
movements were plotted against one another
(Fig. 1C) control values for pitch slopes were
approximately 52 deg, regardless of stance con-
dition. This indicates an approximate 1-to-1
movement of shoulder and pelvis, as expected
from an inverted pendulum mode of sway. In
4 Annals of the New York Academy of Sciences

Figure 1. Modes of movement in the roll and pitch planes during quiet standing on foam
with eyes closed. The original traces of roll (A) and pitch (F) deviations of the shoulders and
the pelvis are shown for 50 sec of data with the trend of the drift estimated by a wavelet filter.
With the trend removed, the data was then low-pass filtered (at 0.7 Hz) to reveal deviations
shown in B for roll and G for pitch. A smaller section of the high-pass (3 Hz) filtered data is
shown in D for roll and I for pitch. Shoulder versus pelvis deviations over the complete 180
sec of each trial, corresponding to the traces shown in B, D, G, and I, are plotted in C, E, H,
and J, respectively as x-y plots. A regression line has been drawn through the x-y data. Note
the approximate in-phase movements of shoulder and pelvis in C and H for low-frequency
roll and pitch, respectively, and the out-of-phase movement in E and J for high frequencies of
sway. (Data reproduced from Ref. 33.)

the roll plane, greater shoulder movement rel-
ative to pelvis movement was observed when
standing on firm compared to foam sup-
port surfaces (79.5 2.0 deg versus 60.2
1.9 deg).
There was no difference in the pattern of
low-frequency displacements of the shoulder
and pelvis between controls and patients with
VL or PL in either the pitch or roll planes.33 Al-
though synchronization of the shoulderpelvis
Horlings et al.: Vestibular and Proprioceptive Contributions to Balance
Figure 2. Eyes-closed movement-strategies
changes as depicted by slopes of high-frequency
modes of pelvis and shoulder motion. Changes
with support surface and with vestibular (VL) or
proprioceptive loss (PL) are apparent. The mean
and standard error of the mean of the slopes are
shown by a column and vertical bar, respectively.
As slopes of +90 and 90 are equal, we referred high-frequency patterns of shoulder and pelvis
all slopes to one sign (that of the majority) for
purposes of computing a mean. For roll, significant
differences were noted with support surface. For the
higher-frequency pitch mode, significant differences
between PL and controls are marked ( ). There were
no significant differences in slope between VL and
control subjects, only amplitude differences. (Data
reproduced from Ref. 33.)
was unaffected by VL or PL, both groups had
differences in the amplitude modulation of both
body segments during quiet stance compared to
controls. Larger amplitude low-frequency dis-
placements of the shoulder and pelvis were ob-
served in both VL and PL patients compared
to controls in the pitch plane. Likewise, in the
roll plane, larger amplitude low-frequency dis-
placements were observed in PL subjects on
a firm surface and in VL subjects on a foam
surface.
High-frequency displacements in the shoul-
der and pelvis were controlled differently in
the pitch and roll planes.33 In the pitch plane,
shoulder and pelvis displacements were uncor-
related and slightly antiphasic during stance on
both firm and foam surfaces (Fig. 2) for VL
and controls. In the roll plane, stance on a
firm surface was dominated primarily by high-
frequency corrections at the shoulder, with lit-
tle corrective movement observed at the pelvis
5
(Fig. 2). In contrast, stance on foam surfaces
was controlled by antiphasic corrections in
the roll plane at both the shoulder and pelvis
(Figs. 1 and 2). There were no significant
differences between VL patients and con-
trols in the pattern of high-frequency displace-
ments of the shoulder and pelvis for either
plane or surface type. Significant high-
frequency differences were observed between
PL patients and controls during quiet stance
in the pitch plane.33 When standing on firm
and foam support, PL subjects pitch-plane
corrections were accomplished almost ex-
clusively through shoulder movements (with
slopes of pelvisshoulder plots being on
average 80 deg), implying that these subjects
attempted to keep their ankle joints as still as
possible. In contrast, PL patients had similar
displacements compared with controls in the
roll plane when standing on both firm and foam
support.
Movement Strategies following
Support-Surface Tilt: Unifying Findings
on Vestibular Loss with Previous Findings
on Proprioceptive Loss
During a pitch-plane, toe-up rotation of the
support surface, the body does not act as an
inverted pendulum. Instead the platform per-
turbation induces-high frequency (>1 Hz) dis-
placement of the legs in the backward direction,
while the trunk is rotated forward to counter the
backward displacement of the center of mass
(CoM).10 Compared with controls, VL sub-
jects responded to backward support-surface
tilts with increased forward pitch of the trunk
followed by increased backward pitching of the
trunk (Figs. 3 and 4).1,5,11 Underlying these
changes are, as shown in the lower part of
Figure 4, an increased early activity in trunk
flexors followed by increased late activity in the
trunk extensors, paraspinals. This instability is
enhanced by decreased activity in the leg mus-
cles, tibialis anterior, and quadriceps, which
thereby fail to rotate the body forward about
the ankle joints.13
6 Annals of the New York Academy of Sciences

Figure 3. Stick figure representation of knee movements to right tilt of the support-surface
and trunk movements to backward tilt. A typical control is shown on the left and a typical VL
patient on the right. The 64 time frames recorded over 1sec, are indicated by the color code,
with blue colors marking the early frames and red colors the late frames. The support-surface
rotation of 7.5 deg started at frame 6. Note the differences in left (uphill) knee flexion and
right (downhill) knee extension between control and VL subjects.

Figure 4. Pitch and roll responses of control and VL subjects. The mean population traces
are shown for a pure left roll (270 deg direction) in the upper row of traces. Increased trunk
roll and uphill quadriceps responses but decreased hamstring responses were present for VL
patients. The lower row of traces shows responses to pure backward pitch (180 deg direction).
Increased early activity in external obliques and increased late activity in paraspinals can be
associated with the early increased pitch of the trunk and later backward-pitch trunk motion.
Horlings et al.: Vestibular and Proprioceptive Contributions to Balance
In contrast, differences that emerge with pro-
prioceptive loss subjects are associated with de-
layed ankle torque and trunk displacements
with respect to controls.13 The delay in trunk
motion was accompanied by a longer phase of
backward trunk rotation compared to controls,
leading to instability. While there is a slight
decrease in activity in tibialis anterior mus-
cles with PL, there is also decreased activity
in paraspinal muscles, and, with this pattern
of activity, less instability compared with VL
patients.13
Normal responses to support-surface roll in-
clude flexion of the uphill knee, extension of the
downhill knee, and trunk lateral rotation in the
opposite direction to support-surface tilt. The
characteristic feature of an unstable reaction
to tilt in the roll direction is insufficient uphill
knee flexion and downhill knee extension.11,19
After the initial stimulus induced uphill trunk
roll, the trunk movement reverses direction in
VL subjects.11 The motion of the CoM is in the
same direction, and a fall is induced downhill
(Fig. 4). This would explain the activity illus-
trated in Figure 4, the uphill knee-flexing mus-
cle, the hamstrings, responds more weakly than
normal after 200 msec, and the uphill knee-
extending muscle, the quadriceps, extends the
knee too much.
In contrast to VL subjects, a subject with
total proprioceptive loss (TPL) in the legs
demonstrates a reversal of trunk roll to the
downhill direction far earlier.12 Two reasons
probably underlie this difference. First, the
common characteristic of TPL is a change in
the response synergy pattern with deactivation
of trunk and leg muscle responses when nor-
mal responses are active.12 Second TPL sub-
jects have enhanced background muscle activ-
ity, which causes them to generally stiffen up.
Their trunk-roll responses are then very like
those of normal subjects whose bodies have
been stiffened with a corset.21 It can well be
imagined that patients with only lower leg pro-
prioceptive loss (termed PL patients here) have
less difficulty with rapid-roll tilts of the sup-
port surface because sensory inputs required
7
to characterize the stimulus are intact (pelvis
muscle proprioceptive and head-roll accelera-
tion vestibular inputs). Indeed this appears to
be the case (Bloem and Allum, unpublished
observations, 2000).
Effect of Trunk Sway Biofeedback
on Balance Control
Given the similarity of balance-correcting
strategies between VL subjects and controls
described above, it would seem logical that a
biofeedback system23 that aimed simply to re-
duce sway would be effective for these two pop-
ulations. Presumably proprioceptive loss sub-
jects would require a feedback device that
helped to change the strategy used to correct
balance instability. As Figure 5 shows, healthy
young and elderly subjects reduced their trunk
sway considerably when the source of feedback
was trunk sway measured at the level of the
lower trunk.24 The actual feedback is equiv-
alent to summed angular motion of the lower
trunk and pelvis for roll and the angular motion
of the lower trunk for pitch (Allum and Kueng,
unpublished observations, 2008). The sway re-
duction with feedback was greater than the re-
duction brought about by training alone.24,25
Furthermore, as the plots in Figure 5 indi-
cate, both young and elderly benefited from
the feedback, with those with the greatest sway
prior to feedback use benefiting most. This im-
plies that patients with balance disorders hav-
ing increased body sway due to predominantly
vestibular problems would presumably benefit
most from feedback use.
Figure 6 provides an example of such im-
provement from ongoing trials with patients.
The patient in question had a unilateral
vestibular loss, which had not been compen-
sated (failure of low-frequency vestibulo-ocular
reflex [VOR] gain to be normal) within the
normal recovery time of 3 months.25 The im-
provement for the typical tests for which this
type of patient is unstable26 was clearly present
after training with the vibrotactile feedback de-
vice and using it to control sway during the
8 Annals of the New York Academy of Sciences

Figure 5. Relationship between pretest peak-to-peak trunk sway and the reduction in sway achieved
with feedback. Roll- and pitch-angle changes for two different tests are shown. The tests were standing feet
together eyes closed on a firm surface on the left (A, roll; C, pitch) and walking tandem steps eyes closed (B,
roll; D, pitch). Regression lines through the data have been drawn separately for elderly and young subjects.
Positive changes mean that sway was reduced with feedback (Data from Davis et al. 2008).

tests. In fact, measures of sway for the two tests
shown under feedback conditions were within
normal bounds for the subjects age.
Discussion
The aim of this paper was to compare strate-
gies used in quiet stance to maintain a sta-
ble posture with those used when the sup-
port surface is suddenly tilted. The strategies
during quiet stance could be split into low-
and high-frequency components.33 The high-
frequency modes of movement during quiet
stance were multilink as were balance correc-
tions to support-surface tilt. These latter bal-
ance corrections involved knee movements for
both forward and lateral tilt, in addition to an-
kle, hip, and lumbosacral movements. When we
examined differences between patient groups
with vestibular loss (VL) or proprioceptive loss
(PL), we found that VL subjects suffer from
a lack of appropriate modulation of their at-
tempted balance corrections. In contrast, PL
patients exhibited changed synergies in re-
sponse to imbalance. As we will expand on
below, this insight suggests it will be easier to
rehabilitate VL than PL subjects using artifi-
cial feedback signals, because once the vestibu-
lar loss subjects are informed, via feedback, of
their inadequate response conditions, then pre-
sumably they would be able to modulate their
responses adequately. On the other hand, pro-
viding feedback information alone may not en-
able the PL subjects to change their response
strategies.
The response strategies PL patients employ
to control quiet stance appear to be different
from those correcting perturbed stance. Dur-
ing quiet stance, PL subjects could execute slow
movements (those with frequencies less than
Horlings et al.: Vestibular and Proprioceptive Contributions to Balance 9

Figure 6. Improvements in trunk sway with biofeedback for an uncompensated unilateral

peripheral vestibular loss patient. The improvements for two different tests are shown; standing
on two legs eyes closed on foam (A and B) and walking eight tandem steps, eyes open in C
and D. On left the time traces with and without feedback are shown. To the right angle and
angular velocity plots before training and with no feedback compared with post training and
with feedback are shown as x-y plots of roll and pitch deviations. Notice the considerable
reduction with feedback. An envelope (the convex hull) has been drawn around the x-y
plots.

0.7 Hz) just like controls, moving the body
as an inverted pendulum. However for high-
frequency (greater than 3 Hz) movements for
which relative movements between the lower
and upper body segments are unavoidable, PL
subjects attempted to hold their legs as still as
possible, a strategy that is different from that
used by VL and normal subjects. When, how-
ever, the same high-frequency motion is im-
posed by stance perturbations as a result of
tilts of the support surface, PL subjects could
not avoid motion of the ankle joints.13 Further-
more, they need to adopt a response synergy
different from that of VL and healthy patients
because ankle stretch reflexes were absent, and
therefore the biomechanical effect of these re-
flexes, too. In fact, lower-leg PL patients adapt
well to the requirements for a change in the re-
sponse strategy given delayed or absent reflex
responses, just as the elderly do,29 possibly be-
cause there are a number of other somatosen-
sory signals that can replace the lower leg pro-
prioceptive inputs. Only when the PL extends
up the legs to encompass the knee and hip joints
is the loss so profound that the changed re-
sponse strategies become destabilizing.12
Traditionally, balance responses have re-
ceived a different focus on two-legged humans
and four-legged animals. Studies on the ef-
fect of VL on humans have concentrated pri-
marily on balance corrections that maintain
pitch-plane stability.35,9,14,16,22 Animal studies
have focused more on responses to roll.28,30,31
In animal studies, it is generally accepted
that vestibularspinal inputs contribute signif-
icantly to muscle responses flexing the uphill
limbs and extending the downhill limbs.30,31 In
these studies it also appears that VL results in
10
lower-than-expected amplitudes of muscle ac-
tivity, as if the CNS were responding to a tilt that
was less than the actual tilt. Studies in humans
have demonstrated a similar situation occurs
for roll and pitch in the leg muscles.5,11 That
is, leg muscle responses (such as ankle muscles)
are hypometric as shown by the current and
previous results.4,5,11 In contrast to the animal
studies however, trunk and neck muscle activity
appears to be hypermetric in humans as shown
by the current and previous results.4,5,11
The reason for the difference between ani-
mal and human responses is probably biome-
chanical. For example, in humans when the
support surface tilts, the legs, pelvis, and center
of mass move in the direction of tilt, but
the trunk and head tilt in the opposite direc-
tion.11,31 In animals all segments tilt downhill.28
This difference has three consequences. First,
in order to maintain stable stance in humans,
proprioceptive information from both the an-
kle and lumbosacral joints is required. Second,
because the head movements to tilt are in the
opposite direction for bipedal stance of humans
and quadrupeds, the neural circuitry under-
lying the vestibulospinal-driven uphill knee
flexion response and downhill kneeextension
responses must have opposite polarity too.
Third, if the same neurobiomechanical mech-
anisms underlie the control of quiet stance,
then this would provide an explanation for
the characteristics of low-frequency, inverted-
pendulum mode of stance following VL. VL
movements are characterized by greater shoul-
der and pelvis motion in the pitch and roll
planes, with both having greater amplitudes
than those of normals.32,33 However, the shoul-
der motion coherent with the pelvis motion is
greater than that of pelvis in VL subjects but less
in controls.33 This suggests that during quiet
stance excessive trunk muscle activity after VL
tends to cause an overreaction of the trunk mo-
tion instead of keeping it aligned with that of
the pelvis.
The question arises whether, in groups with
presumably near optimally functioning sensory
modalities, biofeedback of trunk sway can be ef-
Annals of the New York Academy of Sciences
fective in improving balance control. We found
that it was effective not only in the young but
also in the elderly and those with VL. These re-
sults imply that the CNS can utilize the types of
sensory information artificially provided here
to optimize postural control. We have assumed
that this process occurs via a direct change
in the amplitudes of muscle activity. Whether
this feedback can be used to change unstable
balance-correcting strategies, as we have iden-
tified in proprioceptive loss and other patient
groups (e.g. spinocerebellar ataxia19 ), remains
to be investigated.
The biofeedback signals provided in our de-
vice are all facilitated by supraspinal pathways:
the trigeminal nerve for vibrotactile informa-
tion, the vestibular-cochlear nerve for auditory
and possibly otolithic stimulation, and at the ex-
tremes of sway for the optic nerve visual infor-
mation. The proximity of these supraspinal to
cortical centers integrating sensory signals into
balance commands may be beneficial in elim-
inating any errors in sensory integration that
occur in spinal pathways, regardless of whether
these are due to conduction delays in peripheral
nerves.
The improvement we noted with biofeed-
back was proportional to initial balance perfor-
mance of test subjects. That is, those with the
largest initial balance deficits were most aided
by having biofeedback of their postural sway
available to them. It is possible that the modal-
ity we used may have promoted this scalar im-
provement. The visual feedback was set only to
be active at the extremes of stability for a given
task and this rarely occurred, but when it did, it
was very obvious to the subject. The vibrotac-
tile feedback was set to be extremely sensitive to
sway, and subjects immediately felt it. However,
the auditory feedback was by nature more com-
plex as two signals need to be coded into four
directions of sway. By providing this feedback
in the mid-range of sway and having its ampli-
tude continuously increase with sway, we hoped
to overcome some of the processing problems
that might occur if the auditory feedback was
constant. It may well be worthwhile to consider
Horlings et al.: Vestibular and Proprioceptive Contributions to Balance
replacing the auditory feedback with a graded
vibrotactile feedback. As vibrotactile feedback
increases with intensity it is also perceived au-
ditorily as a bone-conducted signal.
In this study we have explored differences
in the balance-correcting strategies following
vestibular and proprioceptive loss. We have
argued that there are common elements to
these strategies for quiet and perturbed stance.
The lack of adequate modulation of movement
strategies of balance instability following VL or
aging indicates that these are amenable to rec-
tification using biofeedback that provides ad-
ditional artificial sensory information on body
sway.
Acknowledgments
The research reported here was supported
by a grant from the Swiss National Research
Foundation (No. 320000-117950) to J.H.J. Al-
lum. Some of the work described here draws
on findings established with our colleagues
B.R. Bloem, J.R. Davis, U.M. Kueng, and L.
Oude-Nijhuis whose contribution we gratefully
acknowledge.
Conflicts of Interest
The authors declare no conflicts of interest.
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