Suppression of eye movements improves balance

Klaus Jahn, Michael Strupp, Siegbert Krafczyk, Olaf Schuler, Stefan Glasauer and Thomas Brandt
Department of Neurology, Klinikum Grosshadern, Ludwig-
Maximilians University, Munich, Germany
Correspondence to: Michael Strupp, MD, University of
Munich, Department of Neurology, Klinikum Grosshadern,
Marchioninistrasse 15, 81377 Munich, Germany
E-mail: kjahn@nefo.med.uni-muenchen.de
Summary
The aim of this study was to investigate the possible
interaction of vestibulo-ocular and vestibulo-spinal
functions. Spontaneous eye movements and anterior
posterior and lateral body sway were recorded simul-
taneously in 10 patients with vestibular neuritis
(Experiment 1) and in 11 healthy subjects (Experiment
2) while all subjects wore a mask that allowed xation
of a head-xed target. For the healthy subjects, there
was no signicant difference in postural sway for the
conditions of eyes open in darkness and xation of the
head-xed target. For the patients, the question was
whether transient suppression of the spontaneous nys-
tagmus by xating the target affected excessive body
sway or whether modulation of nystagmus and postural
sway were largely independent. The mean peak slow-
phase velocity of the spontaneous nystagmus decreased
from 13.5 6 5.6 to 4.3 6 2.4/s during xation. The
suppression of nystagmus also reduced postural sway
while standing on foam rubber. Mean value decreased
from 25.2 6 7.6 to 16.2 6 7.7 mm (rightleft root mean
square values; ANOVA, P = 0.003). Since a head-xed
target was used to suppress spontaneous eye move-
ments, the data cannot be explained by any stabilizing
effect of afferent visual cues. Instead, ocular motor
efference copy signals or reafferences may have contrib-
uted to the postural instability of patients with vestibu-
lar neuritis, which would explain the reduction of
postural sway during xation suppression of the nystag-
mus. Thus, ocular motor signals rather than afferent
visual cues about retinal slip are used for visual control
of postural sway, at least in this experimental para-
digm.
Keywords: vestibular neuritis; postural control; spontaneous nystagmus; posturography
Abbreviations: AP = anteriorposterior; LED = light-emitting diode; RL = rightleft; RMS = root mean square; SPV =
slow-phase velocity; VOG = video-oculography
Introduction
Ocular motor and postural controls are sensorimotor func-
tions that largely operate independently. Both use input from
the vestibular system, which converges with visual and
somatosensory signals and is subsequently processed in
multisensory vestibular structures that are incorporated in
vestibulo-ocular and vestibulo-spinal neuronal circuits.
The stabilizing effect of vision on posture is well known to
clinicians and has long been the object of scientic investi-
gation (Travis, 1945; Edwards, 1946; Nashner, 1970; Lee and
Lishman, 1974). Our current understanding of visual
stabilization of postural sway is based on the detection of
retinal slip due to involuntary head movements relative to the
seen environment. However, several neurophysiological
studies suggest that extraocular proprioception contributes
to the coding of eye, head and body position in relation to
posture and environmental conditions (e.g. Roll et al., 1989)
and that eye movements inuence postural sway (Brandt
et al., 1986; Rushton et al., 1989). There is a conceptual
model of the postural system (Wolsley et al., 1996a, b) which
incorporates a gain control unit for the visuo-postural loop
with inputs from the ocular-cervical proprioceptive system.
Studies on the inuence of motion parallax in the control of
body sway (Bronstein and Buckwell, 1997; Guerraz et al.,
2000) discuss the existence of two modes of visual detection
of body sway: afferent (retinal slip) and efferent (extraretinal
or eye movement-based).
In the light of these studies and the close anatomical
interrelationship of ocular motor and postural control, we
investigated the interaction between the vestibulo-ocular and
vestibulo-spinal functions. Patients with acute unilateral
partial labyrinthine failure due to vestibular neuritis were
examined for spontaneous nystagmus and postural imbal-
ance. The major question was whether transient suppression
of nystagmus by means of a mask that allows xation of a
head-xed stationary target and does not provide any useful
visual cues for postural control had an inuence on excessive
Guarantors of Brain 2002
Brain (2002), 125, 20052011
body sway or whether modulation of nystagmus and postural
sway were largely independent.
Methods
All participants gave their informed consent to participation
in the study. The experiments were performed in accordance
with the Declaration of Helsinki, adopted at the 52nd World
Medical Association General Assembly 2000 in Edinburgh.
Subjects
Experiment 1
Ten patients with acute unilateral vestibular failure due to
vestibular neuritis (mean age 58 years, range 3180 years;
two females) were included in the study. Diagnosis of patients
was based on a history of acute onset of severe prolonged
rotational vertigo and nausea, clinical and neuro-ophthalmo-
logical examinations (horizontal-rotatory spontaneous nys-
tagmus towards the unaffected ear without evidence of a
central vestibular lesion, pathological bedside testing of high-
frequency vestibulo-ocular reex, postural imbalance with
ipsiversive Romberg fall) and electronystagmography with
caloric irrigation (hypo- or unresponsiveness of the affected
horizontal semicircular canal). Patients were tested 26 days
after the onset of symptoms. All subjects still exhibited
horizontal nystagmus with their eyes open in darkness.
Experiment 2
Eleven healthy subjects without any history of neurological
disorders (mean age 26 years, range 2536 years; two
females) were tested with the same equipment as the patients.
Posturography
Anteriorposterior and lateral body sway were measured
during upright stance (feet splayed at an angle of 30, arms
hanging) on a stabilometer platform (Type 9261 A; Kistler,
Winterhur, Switzerland), which transduces changes in the
force exerted on the foot support. Changes of the centre of
foot pressure (COP) were measured in the anteriorposterior
and rightleft directions. Subjects were instructed to remain
upright and to refrain from any voluntary movements during
the recording. In order to make balancing more difcult, a
slab of foam rubber (height 10 cm, specic weight 40 g/dm
3
)
was placed under the rigid foot support. This reduces the
reliability of somatosensory signals and therefore enhances
the particular weight of afferent visual and vestibular cues.
The subjects were prevented from falling while standing by a
protective fence at hip height.
Fig. 1 Experimental setup (A) and original registrations of horizontal nystagmus and sway velocity (B). (A) Simultaneous recording of
eye movements and postural sway. Subjects stood on a foam rubber padded platform with the eyes open while wearing a light-occluding
mask with a head-xed LED turned on or off. Eye movements were recorded by video-oculography. Monocular xation of the LED
largely suppressed horizontal nystagmus and reduced lateral (RL) and anteriorposterior (AP) postural sway. (B) Original registrations of
horizontal eye movements, RL and AP sway path in darkness and during xation of the head-stationary LED. When spontaneous
nystagmus was suppressed, postural sway was also reduced. Scaling is the same for both experimental conditions.
2006 K. Jahn et al.
Parameters and testing procedure
Sway was recorded in segments of 20 s duration for off-line
analysis (sampling frequency 40 Hz; low-pass lter cut-off
frequency 20 Hz, 60 dB/decade). After offset elimination,
sway velocity and root mean square (RMS) were calculated
for the X (rightleft) and Y (anteriorposterior) directions
(Hufschmidt et al., 1980; Brandt et al., 1981).
Video-oculography
Two-dimensional monocular video-oculography (VOG) was
performed using an infrared camera system integrated in a
mask that prevented any perception of ambient light or visual
orientation (Mack, Pfaffenhofen, Germany). Sampling fre-
quency for horizontal and vertical eye movements was 50 Hz.
Range was 640 for horizontal and 620 for vertical eye
movements. Maximal signal deviation from actual eye
position was 3% for horizontal and 4% for vertical move-
ments (noise 60.2%), as described previously (Pereira et al.,
2000). Calibration was made by 640 horizontal and 620
vertical saccades; the cross-talk between horizontal and
vertical channels was <1%. Mean slow-phase velocity (SPV)
of each nystagmus beat was measured. The average of the ve
fastest SPV periods was used for further analysis. The mask
ensured that there was complete darkness even with the eyes
open. A mask-integrated, light-emitting diode (LED), located
just below the camera lens, could be turned on for xation.
The light source could be dimmed enough that attempted
xation of the still visible target caused only minimal
suppression of spontaneous nystagmus.
Procedure
Experiment 1
Patients rst performed a routine clinical posturography with
eyes open and eyes closed without mask on rm ground and
on foam rubber. They were then tested in random order while
wearing the VOG mask and standing on: (i) rm ground with
eyes open while xating a head-xed stationary LED; (ii)
rm ground with eyes open in complete darkness; (iii) rm
ground with eyes open while attempting to xate the dimmed
LED; (iv) foam rubber while xating the mask-integrated
LED; (v) foam rubber in darkness; and (vi) foam rubber while
attempting to xate the dimmed LED.
Experiment 2
Only two conditions were tested in healthy subjects: (i)
standing on foam rubber while xating the mask-integrated
LED; and (ii) standing on foam rubber with eyes open in
complete darkness (mask). Figure 1 illustrates the experi-
mental setup.
Statistical analysis
Sway velocity, RMS values and SPV were tested for normal
distribution. A repeated measures ANOVA (analysis of
variation; Table 1) was performed on the patient data
(Experiment 1) with three within-subjects levels (Ground:
rm ground versus foam rubber; Vision: space-xed target
versus head-xed bright LED versus darkness versus head-
xed dim LED; RLAP: rightleft versus anteriorposterior).
Post hoc analysis was done using the Bonferroni method to
control for multiple testing. One-way ANOVA was used to
test for signicant differences in mean peak SPV (patients)
and RMS values (healthy subjects, Experiment 2).
Results
Experiment 1: patients with vestibular neuritis
Of the 10 patients, eight had vestibular neuritis on the left side
and showed horizontal-rotatory nystagmus to the right; the
two patients with vestibular neuritis on the right side had
nystagmus to the left. Mean peak SPV of horizontal
nystagmus in complete darkness for all patients was
13.5 6 5.6/s. Fixation of the mask-integrated LED reduced
mean peak SPV to 4.3 6 2.4/s (P = 0.016). Fixation of the
dimmed LED reduced SPV to 10.0 6 3.5/s (not signicant).
When input from the visual (darkness) and somatosensory
(foam rubber) system was reduced, all patients showed
excessive postural sway. The mean RMS values were
25.2 6 7.6 mm (rightleft, RL) and 26.7 6 7.3 mm
Table 1 Results of the repeated measures ANOVA performed on the RMS values of patients with vestibular neuritis (n = 10)
ANOVA Degrees of freedom F P
Ground (rm ground versus foam rubber) 1, 9 48.05 0.000068
Vision (space xed target vs. bright head-xed LED
versus darkness versus dim head-xed LED)
3, 27 26.26 <0.000001
Vision 3 Ground 3, 27 21.98 <0.000001
Vision 3 RLAP 3, 27 13.40 0.000015
RLAP (right/left versus anterior/posterior) 1, 9 7.68 0.022
RLAP 3 Vision 3 Ground 3, 27 3.90 0.019
The ANOVA had three within-subjects levels (Ground = rm ground versus foam rubber; Vision = space-xed target versus head-xed
bright LED versus darkness versus head-xed dim LED; RLAP = rightleft versus anteriorposterior). Signicant interactions are also
shown (Vision 3 Ground, Vision 3 RLAP, RLAP 3 Vision 3 Ground).
Suppression of eye movements improves balance 2007
(anteriorposterior; AP). Post hoc inspection of the data using
the Bonferroni method revealed that sway on foam rubber
while xating a head-stationary LED was signicantly less
than in darkness (P = 0.003) or when attempting to xate a
dim LED (P = 0.019). For xation of the bright LED, mean
RMS values were 16.2 6 7.7 mm (RL) and 16.4 6 5.5 mm
(AP; P = 0.003). The difference between the darkness and the
dim LED conditions [mean RMS values 21.4 68.1 (RL) and
27.6 6 8.7 (AP)] was not signicant. Figure 2 also shows
xation of a space-stationary target to demonstrate postural
sway with optimal suppression of nystagmus and visual
control. The reduction of postural sway with suppression of
vestibular nystagmus was only present on foam rubber. On
rm ground, there was no signicant difference between the
four visual conditions (Fig. 2). Analysis of sway velocity
gave similar results to the RMS values described above, the
absolute values of which are presented in Table 2.
There was a clear correlation between body sway and mean
peak SPV in patients with vestibular neuritis (r = 0.64,
P = 0.0001). Body sway on foam rubber (RMS values) is
plotted against mean peak SPV of spontaneous nystagmus for
the three conditions of eyes open in darkness, xation of a
head-xed LED and attempted xation of a dimmed LED in
Fig. 3.
Experiment 2: young healthy subjects
Healthy subjects were tested on foam rubber under two
conditions: eyes open in darkness and xation of a head-
bound LED. In darkness, RMS values were 6.2 6 2.8 mm
(RL) and 10.4 6 4.6 mm (AP). The sway parameters showed
no signicant difference for the xation condition. RMS
values increased slightly (non-signicantly) to 6.6 6 2.2 mm
(RL) and 12.6 6 7.8 mm (AP).
Discussion
The data show a clear association between the suppression of
spontaneous nystagmus and the reduction of postural sway in
patients with vestibular neuritis. Since a head-xed target was
used to suppress spontaneous nystagmus, the data cannot
simply be explained by the stabilizing effect of any afferent
visual cue. In the following we rst discuss other clinical and
experimental evidence indicating that eye movements and
postural sway interact and then try to identify the particular
Fig. 2 Body sway of patients suffering from vestibular neuritis
under different visual conditions. Mean and standard deviation of
RMS values on rm ground (circles) and foam rubber (squares).
Lateral (dark grey and white symbols) and anteriorposterior sway
(black and light grey symbols) are shown. Fixation of a bright
head-xed LED only reduced sway when the subject stood on
foam rubber. Attempted xation of a dim LED with minor
suppression of spontaneous eye movements had no signicant
effect.
Table 2 Absolute values (mean 6 standard deviation) of sway velocity (SV) and root mean square (RMS) values of
patients with acute unilateral vestibular failure due to vestibular neuritis (Experiment 1) and healthy subjects (Experiment
2) for lateral (RL) and anteriorposterior (AP) sway with eyes open and with or without xation of a head-xed LED
RL sway AP sway
SV RMS SV RMS
(m/min) (mm) (m/min) (mm)
Experiment 1: patients with vestibular neuritis (n = 10)
Standing on rm ground
Fixation of bright LED 0.7 6 0.3 4.9 6 3.3 1.1 6 0.6 6.4 6 3.4
Darkness 0.8 6 0.4 4.8 6 3.1 1.1 6 0.6 7.4 6 4.2
Fixation of dim LED 1.2 6 0.4 6.7 6 5.9 1.2 6 0.9 8.2 6 4.9
Standing on foam rubber
Fixation of bright LED 2.0 6 0.9 16.2 6 7.7 2.7 6 1.2 16.4 6 5.5
Darkness 3.6 6 1.3 25.2 6 7.6 4.6 6 1.2 26.7 6 7.3
Fixation of dim LED 3.6 6 2.0 21.4 6 8.1 4.3 6 1.9 27.6 6 8.7
Experiment 2: healthy subjects (n = 11)
Standing on foam rubber
Fixation of bright LED 0.9 6 0.3 6.6 6 2.2 1.7 6 0.6 12.6 6 7.8
Darkness 1.0 6 0.3 6.2 6 2.8 1.6 6 0.4 10.4 6 4.6
2008 K. Jahn et al.
sensory cue which may be used to reduce body sway during
suppression of spontaneous eye movements.
Association and dissociation of eye movements
and postural sway in vestibular syndromes
Spontaneous nystagmus in vestibular neuritis is caused by a
tone imbalance of the vestibulo-ocular reex. Neuronal
vestibular pathways also include ascending input to thala-
mocortical projections for perception (vertigo) as well as
descending input to vestibulospinal projections for adjust-
ments of head and body posture. Stimulation or unilateral
failure of the peripheral vestibular organ is known to cause
perceptual, ocular motor and postural effects that correlate in
severity (Brandt and Daroff, 1980). The patients tested in this
study showed all signs and symptoms of the vestibular
syndrome.
On the other hand, central vestibular pathway lesions may
cause syndromes in which perceptual, ocular motor and
postural manifestations differ in severity. Examples are (i)
cerebellar lesions with central positional nystagmus without
associated positional vertigo or postural imbalance (Buttner
et al., 1999); (ii) acute ischaemic lesions in the parieto-insular
vestibular cortex with contraversive tilts of the perceived
vertical without associated ocular motor disturbances (Brandt
et al., 1994); (iii) skew deviation with paroxysmal room tilt
without body tilt (Tiliket et al., 1996); (iv) unilateral
pontomesencephalic lesions of the medial longitudinal
fascicle with contraversive skew torsion of the eyes and tilt
of the perceived visual vertical without accompanying head
or body tilt (Brandt and Dieterich, 1993).
Thus, perceptual, ocular motor and spinal aspects of
vestibular function can operate in either a linked or a separate
mode, depending on the site of the lesion or stimulation.
Similarly, cat experiments have shown that stimulation of
vestibular afferents that originate from the otolith organs
activate second-order neurones in the vestibular nuclei, the
majority of which project either to vestibulo-spinal or to
vestibulo-ocular pathways (Kushiro et al., 2000). In humans,
click-evoked vestibular myogenic potentials, which have
been shown to originate from the saccule in guinea-pigs,
affect vestibulo-spinal but not ocular motor function
(Colebatch, 2001).
Eye movements and postural sway interacted in patients
with acquired ocular oscillations, such as down-beating
nystagmus. Simultaneous recordings of eye movements and
postural sway in these patients showed that lateral gaze or
head extension that increased the nystagmus also increased
postural sway (Buchele et al., 1983). Visual xation of a
mask-integrated LED not only suppressed nicotine-induced
nystagmus but also decreased body sway in healthy subjects
(Pereira et al., 2001). Voluntary saccades or sinusoidal
pursuit eye movements increased anteriorposterior and
lateral body sway in normal subjects (Brandt et al., 1986;
Hunter and Hoffman, 2001).
Afferent or efferent cues for visual stabilization
of posture?
The visual stabilization of posture is dependent on several
parameters, including the central and peripheral visual elds,
illumination, visual acuity, eyeobject distance and motion
parallax (Paulus et al., 1984, 1989; Bronstein and Buckwell,
1997). The detection of retinal slip due to involuntary head
movements relative to the seen environment is believed to be
the most important cue for the visual stabilization of posture.
Head and eye movements in one direction cause relative
motion of the visual scene on the retina in the opposite
direction. The data in our experiments cannot be explained by
this mechanism, since the stationary target was head-xed
and therefore did not provide any information about head
sway relative to the environment. The question arises as to
whether the correlation between the amount of nystagmus
and the reduction of postural sway is merely an association or
a sign of causality between eye movements and postural
control.
Three alternative mechanisms should be considered. First,
the mere xation task could induce a change in the postural
strategy to achieve optimal balance, e.g. by co-contraction of
antigravity muscles. Co-contraction strategies are used in
unfamiliar postural tasks and in situations posing a higher risk
of falls (Smith, 1981; De Luca and Mambrito, 1987). This
mechanism is not supported by the data. Fixation of the head-
xed target in healthy subjects had no effect on postural sway.
Similarly, an attempted xation of the dimmed target by
patients, with minor reduction of nystagmus, also caused a
minor reduction in postural sway, which was not signicant.
Fig. 3 Correlation of mean peak slow-phase velocity (SPV) and
total postural sway (RMS). There was a correlation of eye and
body movements (r = 0.64, P = 0.0001). Symbols represent
nystagmus in darkness (black), during xation of a dim head-xed
LED (grey) and during xation of a bright head-xed LED
(white).
Suppression of eye movements improves balance 2009
Secondly, a shift of the particular sensory weight for
postural control from the vestibular to the visual systemmight
reduce the relative contribution of vestibulo-spinal signals to
multisensory control. In our study, vestibulo-spinal output
was destabilizing in patients and stabilizing in healthy
subjects. If the relative contribution of vision were increased
by xation of the head-xed target, we would expect
destabilization, since there was a mismatch between the
actual head movements and the visual signal of no head
movement.
The third alternative is based on the assumption that
information about eye movements rather than afferent visual
signals is used to inuence body sway. It is known from
earlier studies that eye-movement signals are relevant for
postural control (Roll et al., 1989; Wolsley et al., 1996a, b;
Guerraz et al., 2000). If this were true, the intensity of sway
would correlate with the intensity of the nystagmus. This was
the case under all conditions tested. It also ts earlier results
showing a correlation between eye movements and postural
sway (Buchele et al., 1983; Brandt et al., 1986; Hunter and
Hoffman, 2001; Pereira et al., 2001). Theoretically, an
efference copy of the signal from the tonic ocular motor
neural integrator for eye movements in the brainstemcould be
used. The experiments do not allow us to determine the
particular cue or the sensorymotor signal that links eye
movements and postural sway. Since spontaneous vestibular
nystagmus is an involuntary ocular oscillation, re-afferent
input about eye movements may be an alternative signal.
In conclusion, the nding that suppression of spontaneous
nystagmus reduces postural sway is compatible with the
functional concept that visual stabilization of posture is not
only dependent on afferent visual cues but also on ocular
motor signals.
Acknowledgements
We wish to thank J. Benson for copy-editing the manuscript.
The work was supported by the Deutsche
Forschungsgemeinschaft.
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Received January 7, 2002. Revised March 4, 2002
Accepted April 21, 2002
Suppression of eye movements improves balance 2011