Gait & Posture 27 (2008) 294–302

www.elsevier.com/locate/gaitpost

Proprioceptive contribution of postural control as assessed from

very slow oscillations of the support in healthy humans
M. Vaugoyeau a,*, S. Viel a, B. Amblard a, J.P. Azulay a,b, C. Assaiante a
a
Groupe ‘‘Développement et Pathologie de l’Action’’, UMR 6196, CNRS, 31 chemin J. Aiguier, 13402 Marseille Cedex 20, France
b
Department of Neurology, University Hospital Timone, Marseille, France
Received 1 August 2005; received in revised form 22 November 2006; accepted 9 April 2007

Abstract

Maintaining erect human posture depends on graviceptive information. This can come from at least of three origins: vestibular, visual and
somaesthetic. We hypothesize here that subject’s use proprioception rather than visual or vestibular cues for their control of upright body
posture and this even when subjects stand on a tilting body support surface. In order to find experimental evidence for this hypothesis, we
exclude in our experiments visual cues (eyes close) and by keeping frequency and amplitude of the tilt stimulus so low that it would be below
the detection threshold for vestibular semi-circular canal stimuli. The orientations of body segments were analysed during various phases of
the perturbation cycle. Segmental stabilisations were defined in terms of both the global anchoring index calculated during the whole
perturbation cycle and an appropriate sequential anchoring index calculated during various phases in the perturbation cycle. We show that
subjects tend to align their bodies with the space vertical and do so better for their heads than for their upper bodies and lower bodies. A further
finding is that stabilisation is related to the tilt stimulus in the form that it is minimal at the turning points of the tilt, where peak tilt velocity is
minimal with the sinusoidal stimulus used.
These finding suggest first that proprioceptive cues are predominant in the control of body orientation in quasi-static condition and second
that the head and trunk stabilisation strategies used as the basis of postural control depend on the properties of the moving support.
# 2007 Elsevier B.V. All rights reserved.

Keywords: Postural orientation; Segmental stabilisation; Proprioception; Semi-circular canals; Humans

1. Introduction provided by the hydrostatic pressure in large blood vessels

Under static conditions, postural control involves
adopting a given body orientation, and maintaining this
posture despite the perturbing effects of gravity and other
external forces. It has been clearly established that visual,
vestibular and somatosensory cues provide the information
required to estimate verticality. Other somaesthetic grav-
iceptive information may, also be used to control body
verticality. Mittelstaedt [1] has provided evidence for the
existence of graviceptive sensors around the kidneys. This
author also put forward the idea that the information
* Corresponding author at: CNRS, UMR 6196, Groupe DPA, CNRS, 31
chemin J. Aiguier, 13402 Marseille Cedex 20, France.
Tel.: +33 4 91 16 43 63; fax: +33 4 91 77 50.84.
E-mail address: vaugoyau@dpm.cnrs-mrs.fr (M. Vaugoyeau).
might be another good candidate for monitoring body
verticality. Dietz et al. [2] have suggested that the Golgi
tendon organ might monitor the forces exerted by the
muscles counteracting the gravitational forces, which
therefore serve as graviceptors. According to Bisdorff
et al. [3], the perception of body verticality by seated
subjects may thus mainly depend on proprioceptive/contact
cues. Bronstein [4] has also stressed the prominent role
played by somatosensory cues in the perception of body
verticality.
In the present study, we addressed the question as to
whether somaesthetic graviceptive information may suffice
to actively maintain a vertical posture while standing in
quasi-static condition. For this purpose, we used an original
experimental procedure making it possible to isolate the
somaesthetic graviceptive cues. Standing subjects with their

0966-6362/$ – see front matter # 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.gaitpost.2007.04.003
 M. Vaugoyeau et al. / Gait & Posture 27 (2008) 294–302 295

eyes closed were subjected to small angular sinusoidal

perturbations of the support platform on which they were
standing, applied well below the detection threshold of the
semi-circular canal system. The anterior and posterior semi-
circular canals detecting pitch and roll rotations are known
to play a particularly important role in the detection of fast
postural sways, but not low frequency sways such as those
occurring during quiet stance [5,6]. The threshold level at
which the vestibular detection of sway is possible on the
pitch plane is around the 18/s reported to be the threshold
value at which the conscious perception of pitch motion
occurs [7–10]. In fact, according to Henn et al. [11], the
threshold value at which angular acceleration detection
occurs is approximately 0.28/s2. The levels of both the
frequency and the amplitude of the oscillating supporting
platform used here were therefore selected so that they were
not detectable by the semi-circular canals. Although the
otolithic system is theoretically capable of detecting all
frequencies up to null level [12], we were confident that
since the subjects had no use of visual cues, somesthethic
cues were the main type of information used by the present
subjects for postural control.

2. Materials and methods

2.1. Subjects and experimental procedure

Ten healthy subjects (aged 28.6  8 years) took part in the

experiment, which was approved by the local ethical committee,
and all the subjects gave their informed consent prior to the
study.
Subjects stood on a motorised one-directional rotating plat-
form with their eyes closed, and the platform was rotated
sinusoidally at 0.01 Hz (108 peak to peak) in either the pitch
or roll direction, depending on the subjects’ position on the
platform. They had to maintain a vertical posture as steadily
as possible, keeping their feet 15 cm apart without flexing their
knees. The trial lasted for 106 s, including a whole cycle of
Fig. 1. Characteristics of the supporting platform movement. The first curve
angular platform movement. The maximum angular accelerations
represents the angular displacements of the supporting platform. The second
of the platform were thus well below the vestibular canal’s represents the angular velocity of the supporting platform and the third
detection threshold, namely 0.28/s2 [11]. Therefore, if any angu- represents the angular acceleration of the supporting platform. The narrow
lar head accelerations occurred beyond this threshold value, they indicate the peak of inclination, of velocity and of acceleration.
would not result directly from the platform movements and would
not be involved in correcting the experimentally induced postural
disturbances. 2.2. Data collection and kinematics analysis
Fig. 1 represents the characteristics of the supporting platform
movements in term of angular displacements, velocity and accel- Data collection was performed with the ELITE automatic
eration. We can note that the maximum velocity was 0.318/s and the motion analyser working at 100 Hz, using passive body markers
maximum acceleration was 0.028/s2. [13]. The subject performed the task facing a couple of ELITE
Preliminary experiments were performed to assess the visual cameras in the case of lateral perturbation, or in side view (right
contribution to both segmental orientation and stabilisation. Five profile) in the case of antero-posterior perturbation. In the case of
subjects were tested with their eyes open and closed while a lateral lateral oscillations, they wore 10 markers (15 mm in diameter) on
perturbation was applied to the supporting platform. Since no the following anatomical points: left and right infra-orbital margins
significant effects of vision were observed, we continued to (markers 1, 2); left and right acromions (3, 4); left and right superior
explore the effects of perturbations to the supporting platform anterior iliac spines (5, 6); left and right great trochanters (7, 8) and
under eyes closed conditions, which seemed to be the most left and right medial malleoli (9, 10). In the case of anterior–
relevant conditions for investigating the proprioceptive contribu- posterior platform oscillations, the subjects wore seven markers on
tion to postural control. Data about the role of vision are presented the right side of the body: the meatus and infra-orbital margin
in Section 3. (markers 1, 2); acromion (3); iliac crest (4), trochanter (5); tibial
296 M. Vaugoyeau et al. / Gait & Posture 27 (2008) 294–302
plate (6) and medial malleolus (7). During both tasks two markers
were placed on the platform to measure its movements. In each
experiment, each subject was subjected to the two types of dis-
turbances, namely lateral and anterior–posterior platform oscilla-
tions, occurring in a pseudo-random order.
2.3. Controlled variables
2.3.1. Mean orientation
At each trial, the mean orientation of each body segment (head,
shoulders, trunk and pelvis in response to lateral oscillations of the
platform; and head, trunk and thigh in response to antero-posterior
oscillations of the platform) was calculated during a whole cycle
(100 s) of platform movement on the plane of the perturbation. A
reference orientation value was obtained for each body segment in
each subject during 10 s of upright stance on a stable support with
the eyes open. Likewise, the mean instantaneous orientation of
each body segment was calculated during each tenth of a cycle
(10 s) of platform movement, in order to assess the time course of
the segmental orientation process.
2.3.2. Attenuation factor
The attenuation factor (AF) of the changes induced in the
segmental orientation due to the movement of the supporting
platform is a variable used to assess the amplitude of the disor-
ientation induced in each segment by the postural perturbation. It
was assessed using the following formula:
sP  sS
AF ¼
sP þ sS
where sP is the standard deviation of the absolute distribution
(with respect to the gravity vertical) of the orientations of the
supporting platform and sS is the standard deviation of the
corresponding distribution of the absolute orientations of a
given segment. AF = 1 would correspond to complete
attenuation, which means that a given segment has remained
vertical in response to the perturbation. By contrast, AF = 0
would mean that no attenuation had occurred, in other words,
that a given segment has moved with the same amplitude as
the supporting platform. Lastly, if AF is negative, this means
that the subject has moved more than the supporting platform
and may run the risk of falling off it. The main advantage of
this index is that it takes into account the whole signal,
whereas peak-to-peak analysis would focus only on two short
periods of time during the behaviour of interest.
2.3.3. Anchoring index
Segmental stabilisation was defined in terms of the global
anchoring index calculated during the whole cycle of perturbation
[14–18] and with the moving anchoring index calculated during
various phases of the perturbation cycle. The moving anchoring
index was calculated based on the formula developed for the
anchoring index during successive 10-s steps (10 s) in each trial,
in order to establish the time course of the segmental responses to
very slow angular perturbations of the supporting platform, thus
showing the existence of any changes in these responses.
The segmental anchoring index was used to compare the
stabilisation of a given segment with respect to both an external
reference value and the moving platform. This index was calculated
at each trial as follows, as shown in Fig. 2.
s 2r  s 2a
AI ¼
s 2r þ s 2a
where sa is the standard deviation of the angular distribution
about the roll or pitch axis of the segment under investiga-
tion with respect to the allocentric reference (absolute
vertical direction) value and sr is the corresponding standard
deviation of the angular distribution with respect to the
moving platform.
A positive value indicates a better segmental stabilisation along
the absolute vertical or horizontal axis than in response to the
moving platform, whereas a negative value indicates a better
segmental stabilisation on the platform than. The segmental
anchoring index was therefore used to compare the level of
stabilisation of a given segment achieved by the subject in relation
to the gravity vertical or to the biased orientation of the supporting
platform.
2.4. Statistical analysis
At least two trials were run with each subject on each variable
investigated under both experimental conditions. At each trial, the
reference value was subtracted from the mean orientation of each
body segment in each subject. The average difference among all
subjects was then compared to zero using a single-sample analysis
t-test.
Anchoring indexes, moving anchoring indexes and attenuation
factor were also compared to zero, using a single-sample analysis
(t-test) against the null hypothesis. Since these indices were in the
1 to +1 range, we used a z transform to convert the values into an
unbiased Gaussian distribution. Comparisons were made between
the head and trunk orientation and stabilisation performances in
response to the two kinds of disturbance, using an ANOVA.
Changes in the ability to use a given mode of segmental
stabilisation during platform perturbations were assessed in terms
of the coefficient of correlation between the moving anchoring
index obtained with a given segment and the corresponding slope of
the supporting platform, regardless of the direction in which the
platform was tilted. A coefficient of correlation differing signifi-
cantly from zero would show the existence of some linkage
between the segmental stabilisation strategy used and the slope
of the supporting platform.
3. Results
3.1. Role of proprioception
3.1.1. Postural orientation
3.1.1.1. Mean orientation. The mean orientation of the various
segments was never significantly different from the reference value,
on either plane of perturbation
3.1.1.2. Sequential orientation and attenuation factor. The
time course of the segmental orientation process occurring in
response to the lateral and antero-posterior perturbations is shown
in Fig. 3, respectively, in the various segments of interest. This
sequential orientation process showed few variations with time.
 M. Vaugoyeau et al. / Gait & Posture 27 (2008) 294–302 297

Fig. 2. (Left upper part) Diagram of the head roll angle with respect to the external axis, ua, and of the head roll angle with respect to the support, ur. (Right upper
part) Roll angular displacement of the supporting platform (upper trace), the head (middle trace) and the relative angular movement of the head with respect to
the supporting platform (lower trace). (Left lower part) Diagram of the absolute and relative roll dispersions of the head, according to the definition of the
anchoring index (AI). In this example, AI is positive, which means that the head is stabilized in space independently of the support movements. (Right lower
part) Principles used to calculate the moving anchoring index during successive 12-s steps in the perturbation cycle.

The damping of the oscillations induced in the anatomical
segments was assessed in terms of the attenuation factor (AF).
All the segmental movements were noticeably damped in compar-
ison with movements of the supporting platform, since the AF
differed significantly from zero in the case of lateral (t = 8.38,
p < 0.0001; t = 12.23, p < 0.0001; t = 17.46, p < 0.001; t = 7.48,
p < 0.0001, for head, shoulders, trunk, and pelvis, respectively) as
well as antero-posterior platform perturbations (t = 3.891,
p < 0.001; t = 8.33, p < 0.001; t = 10.12, p < 0.0001, for head,
trunk and thigh, respectively).
In the case of lateral perturbations, these AF ranged roughly
between 0.3 and 0.6. No significant between-segments differences
were observed in the AF between the head, shoulders, trunk and
pelvis. Nor were any significant differences observed in the case of
antero-posterior perturbations, between the AF occurring in the
head, trunk and thigh.
3.1.2. Postural stabilisation
3.1.2.1. Global anchoring indexes. The mean anchoring
indexes of each anatomical segment (with S.D.s) are shown in
Fig. 4.
With both kinds of platform perturbations, the anchoring
indexes (AI) were significantly positive in all the segments, show-
ing that good stabilisation of the segments was achieved in space (in
the case of lateral platform perturbations: t = 7.19, p < 0.0001;
t = 6.54, p < 0.0001; t = 8.57, p < 0.001; t = 3.35, p = 0.01, for
head, shoulders, trunk, and pelvis respectively; and in the case of
antero-posterior platform perturbations: (t = 4.46, p < 0.01;
t = 9.04, p = 0.0001; t = 6.81, p = 0.0001, for head, trunk and thigh
respectively). Comparisons were also carried out on the degrees of
stabilisation achieved at the various anatomical levels. No signifi-
cant differences were detected between the AI values obtained on
the head, shoulder, trunk and pelvis under lateral perturbation
conditions or between those obtained on the head, trunk and pelvis
under antero-posterior perturbation conditions.
3.1.2.2. Moving anchoring index. In order to determine
whether any changes occurred in the segmental stabilisation stra-
tegies used during the long cycle (100 s) of the very slow angular
platform perturbations, the head and trunk AI were calculated in
successive 10-s steps during each trial. This sequential AI is shown
in Fig. 5 for each segment. The coefficients of correlation between
the sequential AI and the time course of the absolute slope of the
supporting platform were also calculated and are given in Fig. 5.
Similar stabilisation strategies were observed at both head and
trunk level under both support perturbation conditions. These
segments were well stabilized in space during the perturbation,
but when the maximum absolute platform slope was reached, the
strategy preferentially used to stabilize the head and trunk was lost
and the value of the anchoring index decreased to zero. In other
words, the segmental stabilisation performances depended on the
absolute slope of the supporting platform. The coefficients of
correlation were significantly negative with all segments under
both conditions of perturbation (in the case of lateral perturbation
of the support: t = 3.15, p = 0.01; t = 4.78, p = 0.001; for head and
trunk, respectively; and in the case of antero-posterior support
perturbations: t = 4.78, p = 0.001; t = 5.61, p = 0.01; for head and
trunk, respectively). The negative values of the coefficients indi-
cated that an increase in the slope of the supporting platform
resulted in a decrease in the value of the anchoring index.
298 M. Vaugoyeau et al. / Gait & Posture 27 (2008) 294–302

Fig. 3. Sequential orientation of the various segments (left) and mean and standard deviation of attenuation factor the various anatomic levels studied, in
response to lateral (part a) and antero-posterior (part b) movement of the supporting platform when no visual cues were available.

Fig. 4. (Left part) Mean global anchoring indexes with respect to the supporting platform and standard deviation of head, shoulders, trunk and pelvis when
lateral perturbations to were applied to the supporting platform and no visual cues were available. (Right part) Mean global anchoring indexes with respect to the
supporting platform and standard deviation of head, trunk and thigh when antero-posterior perturbations were applied to the supporting platform and no visual
cues were available.
 M. Vaugoyeau et al. / Gait & Posture 27 (2008) 294–302 299

Fig. 5. (Left part) Moving anchoring indexes of head and trunk when lateral perturbations were applied to the supporting platform. (Right part) Moving
anchoring indexes of head and trunk with respect to the antero-posterior perturbation of the supporting platform. The gray points and lines represent the variation
of the inclination of the support. The coefficients of correlation (CC) were calculated between the segmental moving anchoring index and the corresponding
absolute orientation of the supporting platform.

3.2. Role of vision
3.2.1. Postural orientation
3.2.1.1. Mean orientation. The subjects were able to maintain
a good vertical position under both visual conditions, as shown by
the absence of any significant effects of vision observed in the
ANOVA analysis.
3.2.1.2. Attenuation factor. Under lateral support disturbance
conditions, the averaged AF recorded in each segment is given in
Fig. 6. The AF ranged roughly between 0.3 and 0.6 in both
conditions with and without vision. No significant visual effects
were detected in any of the segments.
3.2.2. Postural stabilisation
The AI are shown in Fig. 6. No significant differences were
observed between the AI values recorded with the subjects’ eyes
open and closed. The significant positive anchoring index obtained
indicated that the segments were all stabilized on space under both
visual conditions.
4. Discussion
In this experiment, the subjects were able to keep their
body upright despite the absence of visual cues and semi-
circular canal information from the support platform
movements. On both planes of perturbation, the subjects’
head and trunk stabilisation strategies were lost when the
support was tilted to the maximum, corresponding to the
minimum velocity. This finding suggests that the head and
trunk stabilisation strategies used as the basis of postural
control depend on the properties of the movement of the
support in term of acceleration, velocity and inclination.

Fig. 6. Part a: Mean attenuation factor and standard deviation of head, shoulders, trunk and pelvis with vision (in white) and without vision (in black) when
lateral perturbation were applied to the supporting platform. Part b: Mean global anchoring index and standard deviation of head, shoulders, trunk and pelvis
with vision (in white) and without vision (in black) when lateral perturbations were applied to the supporting platform.
300 M. Vaugoyeau et al. / Gait & Posture 27 (2008) 294–302
4.1. Proprioceptive inputs suffice to control vertical
body orientation in healthy adults
In this study, the mean orientation of the body segments
never differed from the reference values measured with the
eyes open and without support motion. In addition, the time
course of the segmental orientation process occurring when
lateral and antero-posterior perturbations were applied to the
support showed few variations. These findings clearly show
that in the absence of vision, postural perturbations applied
below the vestibular canal detection threshold did not affect
upright stance in healthy young subjects. This means that
somatosensory cues, possibly along with otholitic informa-
tion, easily sufficed for the subjects to efficiently maintain
both their overall and segmental body orientation.
Although the otolithic organs were previously thought to
provide the subject with information about the vertical pull
of gravity, some authors have challenged this idea.
Stoffregen and Riccio [19] put forward the alternative
hypothesis that perceived orientation may be mainly
determined by the dynamically defined direction of balance;
thanks to sensory integration processes [20,21].
As described Bacsi and Colebatch [25], the vestibular
system may contribute to postural control by two ways: by
way of the conscious perception or by the way of reflex
responses to imposed displacements. Concerning the
conscious perception of body verticality, Bringoux et al.
[22] reported, using a perturbation comparable to our as
concerns peak velocity or acceleration of the tilt stimuli, that
gravity-based somaesthetic cues are more informative than
otolithic cues for the perception of a quasi-static body
orientation. On the other hand, Bronstein [4] established that
the subjective postural vertical was never biased in patients
with acute unilateral vestibular disorders. In a recent study,
Bringoux et al. [23] reported that blindfolded bilateral
labyrinthine-defective subjects performed as accurately as
healthy subjects when asked to detect the slow changes
occurring in their body orientation when they were passively
displaced from the upright to an angle of 0.058/s. These
results, suggest that the accurate perception of body
orientation under quasi-static conditions may be mainly
allowed on somatosensory rather than otolithic information.
Recent data by Teasdale et al. [24] have also suggested that
under static conditions, the otoliths are poor detectors of the
gravity force direction and that the accuracy of the
perception of body orientation improves when propriocep-
tive information can be dynamically integrated. But, tthese
study concern more the body orientation perception than the
control of postural orientation.
Concerning the implication of reflex responses to
imposed displacements, Mergner and Rosemeier [26] have
proposed a ‘new concept’ of postural control, which
postulates that the vestibular signal is used in a feed
forward way, while the body-on-support adjustments are
handled mainly by proprioceptive control mechanisms. With
this in mind, Maurer et al. [27] have investigated the control
of upright stance in patients with bilateral vestibular loss and
control subjects when visual and somatosensory orientation
cues are removed. Postural responses to sinusoidal tilts of a
motion platform in the sagittal plane (28, f = 0.05, 0.1, 0.2
and 0.4 Hz) were studied in normal subjects and vestibular
loss patients. They found that absence of vestibular cues and
removal of vision had little effect on stabilization of upright
body posture in space. They conclude that in the absence of
both vestibular and visual cues, somatosensory graviception
still provided some information on body orientation during
slow perturbation of the support. These findings confirm the
predominance of somatosensory cues for postural control in
quasi-static condition as suggested by the model proposed
by Mergner and Rosemeier [26].
These data and our results taken together suggest a major
influence of somesthetic information, in perception of body
orientation and in postural orientation control in quasi-static
condition.
Nevertheless, the vestibular inputs may become much
more useful for more dynamical situations (for more rapid
tilts). It has also been demonstrated that when proprioceptive
and visual cues are unavailable, postural control appears to
require intact vestibular function [25].
4.2. Segmental stabilisation depends on the movement
of the support
In the absence of both vestibular canalar and visual cues,
the subjects were able to stabilize their body segments in
space in response to support perturbations. This shows the
importance of the contribution of somesthetic cues to
segmental stabilisation. However, the time course of the
segmental stabilisation showed that the segmental stabilisa-
tion strategy used depended on the direction in which the
support disturbances were applied.
Gianna et al. [28] have established that the lowest
frequency at which motion direction is detectable during
passive lateral whole-body acceleration in healthy subjects
is about 4.84 cm/s2 (range 2.9–6.3). In our experiments, the
highest linear acceleration (peak value) at the head level in
strictly en bloc-subjects worked out at 3.35 cm/s in subjects
1 m 70 in height. This means that subjects’ head acceleration
was mostly below the threshold value reported by Gianna
et al. [28]. In addition, because of the damping known to
occur at the head level, the subjects in our study must have
adopted a segmental strategy decreasing the linear head
acceleration rather than an en bloc strategy. They therefore
probably stabilised their bodies using the proprioceptive
inputs rather than the vestibular system. In addition,
experiments carried out under microgravity condition
showed that segmental stabilisation does not depend
crucially on static vestibular afferents [29].
Interestingly, we also established that the segmental
stabilisation strategies were correlated with the angle at
which the support was tilted. More specifically, the fact that
head and trunk anchoring indexes became null when the
 M. Vaugoyeau et al. / Gait & Posture 27 (2008) 294–302
largest tilt angles were applied to the supporting platform,
indicates that the subjects loose the reference frame used to
stabilize their segments. However, since the movements
applied to the supporting platform were sinusoidal, the
greatest amplitudes corresponded to the lowest speeds.
The fact that the segmental stabilisation in space may be
dependent of the orientation of the support was never
described up to now. This is an interesting result, since
segmental stabilisation, and especially that of the head, was
supposed to be devoted to a better body equilibrium during
dynamic destabilisation, such as during skiing or surfing.
Our results seem to indicate that this ability is not
necessarily spontaneously present, but may have to be
trained while moving on an irregular and/or tilted terrain.
In conclusion, there are three kind of sensory information
available to control posture: the visual, the vestibular and the
somatosensory information. Our data confirm the predomi-
nance of proprioceptive information in the control of
postural orientation in quasi-static condition, the vestibular
system requiring large postural change to detect any change
in body orientation. Concerning the segmental stabilization,
this study shows that head and trunk stabilisation depends on
the parameters of the support’s destabilisation. Further
studies on patients with proprioceptive integration deficits,
such as parkinsonian patients or deafferented patients, are
now required to be able to understand more clearly the role
of proprioception in postural control.
Acknowledgments
We are grateful to the subjects who participated in this
study. We thank Jessica Anderson-Blanc for revising the
English. This research was supported by the French Medical
Research Foundation (FRM).
Conflict of interest
We declare that we have no conflict of interest.
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