(Investigative Ophthalmology and Visual Science. 2000;41:3798-3804.)
© 2000
by The Association for Research in Vision and Ophthalmology, Inc.
Visual Control of Postural Orientation and Equilibrium in Congenital Nystagmus
Michel Guerraz1,
Josephine Shallo–Hoffmann2,
Kielan Yarrow1,
Kai V. Thilo1,
Adolfo M. Bronstein1 and
Michael A. Gresty1
1 From the Medical Research Council Human Movement and Balance Unit, National Hospital for Neurology and Neurosurgery, London, United Kingdom; and
2 College of Optometry, Nova Southeastern University, Fort Lauderdale, Florida.
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Abstract
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PURPOSE. To investigate how humans with congenital nystagmus (CN) use visual
information to stabilize and orient their bodies in space.
METHODS. Center of foot pressure (COP) and head displacements in the lateral
plane were recorded using a sway platform and Schottky barrier
photodetector, respectively. In experiment 1, a comparison was made of
the oscillatory characteristics of body sway with eyes open compared
with eyes closed. Experiment 2 studied the postural readjustments made
in response to absolute or relative motion (motion parallax) of objects
in the visual scene, generated by lateral displacement of background
scenery.
RESULTS. Experiment 1 revealed that subjects with CN were not able to use visual
information to stabilize COP but were able to stabilize the head at
frequencies lower than 1 Hz. Experiment 2 showed that in response to
the displacement of a visual display, for both absolute motion and
motion parallax, subjects with CN reoriented their body in space in a
manner similar to control subjects.
CONCLUSIONS. The results suggest that despite involuntary eye movements, subjects
with CN use orientation cues to control their posture, but not dynamic
cues useful to control the rapid oscillations that are particularly
important at the level of COP. These findings suggest that in CN,
visual control of posture is restricted by low-frequency sampling of
the visual scene.
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Introduction
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Congenital nystagmus (CN) is an ocular motor disorder
characterized by involuntary oscillatory eye movements that disrupt
foveal target fixation. The onset of nystagmus occurs during the first
6 months of life.1
Typically, the nystagmus is in the
horizontal plane, and each cycle is initiated by slow phases with
exponentially increasing velocity, taking the eyes off the target. A
fast phase returns the eyes to the object of regard, at which time
there is usually a period of transient stability: a foveation period of
10 to more than 100 msec duration within which the target is visually
sampled.2
Despite almost constant eye movement,
oscillopsia, or impairment of visuomotor coordination is rare.
Visual information is an essential factor in the multisensory control
of movement and balance.3
Unlike vestibular information,
visual motion signals are relativistic: that is, a displacement of the
subject or an external object can yield similar patterns of retinal
motion stimuli. Therefore, visual control of posture depends on the
ability to differentiate optical flow due to self-motion from that due
to object motion. Such a differentiation could be compromised in
individuals with involuntary eye movements such as CN. Accordingly, in
addition to increased thresholds for motion detection,4
5
6
7
individuals with CN make less use of visual information to control
stance, measured as center of foot pressure (COP), than do control
subjects.7
We present detailed investigations of the dynamics of visual postural
control in subjects with CN. The first experiment sought to identify
the frequency bands in which visual control of equilibrium (the
oscillatory component of body sway) is disturbed by CN. Because
oscillations of the COP have a higher frequency range than upper parts
of the body8
9
both COP and head oscillations were
recorded. The second experiment determined the extent to which subjects
with CN reorient (i.e., tilt or displace in a given direction) their
bodies in space in response to visual flow. Normal subjects lean in the
direction of motion10
11
12
when viewing a moving
background. This postural adjustment reverses in direction when a
stationary target providing motion parallax cues is placed between the
standing subject and the moving background.13
14
Because
of the intrinsic visual instability and raised thresholds for motion
detection in CN, we hypothesized that these subjects may have disturbed
patterns of postural response to such visual motion stimuli.
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Materials and Methods
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Subjects
Nine adult subjects with horizontal CN15
and Snellen
visual acuity of at least 0.33 in one eye were studied. Six took part
in experiment 1 (subjects 1–6 in Table 1
), and all participated in experiment 2 (subjects 1–9 in Table 1
). Fourteen healthy, age-matched subjects participated in experiment
1. Six of these control subjects (mean age, 38.5 years) had their
visual acuities artificially reduced to match those of the subjects
with CN (acuity control group). These subjects wore spectacles with
fogging lenses (x1 magnification lenses with ground surfaces) for 15
minutes before the beginning of the experiment. Because two subjects
with CN had extremely low vision in one eye (<0.1), two control
subjects were tested monocularly in addition to fogging. The other
eight subjects (mean age, 40.5 year) were tested with normal vision
(normal control group). Fourteen healthy adults, age matched to the
subjects with CN (mean age, 38 years) and having normal Snellen acuity,
took part in experiment 2. Written informed consent was obtained
according to the Declaration of Helsinki.
Postural Recordings
The studies focus on postural adjustments in the lateral plane in
response to lateral movements of both the visual scene and the eyes,
because a number of published studies as well as our pilot studies have
shown that postural responses are coplanar with the visual motion
stimuli deployed.12
16
17
18
Postural movements in other
directions are uncorrelated. In both experiments, subjects stood
barefoot on a rigid board placed on top of a slab of foam rubber
(height, 5 cm; specific weight, 30 g/dm3) resting
on a sway platform that transduced postural sway as displacement of COP
in the lateral direction. Feet were splayed at 30° with heels
together. The foam increased the instability of the subjects so that
the effect of vision on sway was enhanced.19
20
Subjects
also wore a lightweight helmet, on top of which was mounted an infrared
light-emitting diode. Displacements of the light were transduced by
imaging a top view of the subject onto a two-dimensional Schottky
barrier photodetector (United Detector Technologies, Hawthorne, CA)
situated 40 cm above the head. Light from the diode was projected onto
the detector surface through a Mamiya
medium format lens (45-mm focal length, f 2.8;
Mamiya America Corporation, Elmsford, NY) mounted on the front of the
photodetector. Use of this technique to record complex human movements
has been described previously.21
One axis of the detector
was oriented in the lateral plane to transduce lateral head sway. The
resolution of the detector in the configuration deployed was of 0.1 mm,
linear up to ±8 cm. Head sway values were normalized for each
subjects’ height (signal x mean height of group/individual’s
height). All signals were filtered with a band-pass filter of less than
30 Hz and thereafter digitally sampled at 125 Hz.
Eye Movement Recording
Bitemporal, direct coupled, electro-oculographic recordings of
horizontal eye movements were performed on all subjects with CN during
experiments 1 and 2, to monitor the predominant fast phase direction
and the frequency of the nystagmus.
Experiment 1: Visual Control of Equilibrium
Subjects were tested under two conditions: eyes open and eyes
closed. In both conditions, subjects were instructed to stand still and
relax with hands at the sides. With eyes open, subjects were asked to
fixate a small cross (1 x 1 cm) placed at the center of an
earth-fixed window frame (30 x 24 cm) at a distance of 50 cm from
the eyes. The room was normally illuminated. The order of presentation
of the eyes-open, eyes-closed conditions was counterbalanced. Each
condition was presented for 1 minute, from which the last 50 seconds
were analyzed.
Postural equilibrium in the lateral direction was evaluated as sway
path and also in the frequency domain. The sway path is the length of
the path described by the COP or the head and is defined as the sum of
the distances between sequential points sampled during the analysis
period (50 seconds). To calculate power spectra, the 50-second epochs
were detrended using a line of best fit and then windowed with a
Hanning function. A fast Fourier transform algorithm was then applied
to the entire 6250-point signal (Matlab; The Mathworks, Natick, MA).
The resultant power spectrum had a frequency resolution of 0.02 Hz and
bandwidth from 0 to 62.5 Hz. For subsequent analysis, only the 0- to
5-Hz range was considered. For statistical analysis the frequency
components from 0.02 to 5 Hz were grouped into 20 bands, each spanning
0.25 Hz with 12 or 13 (alternating) discrete frequency components per
band. The power in each of these bands was then calculated by summing
the frequency components.
Analysis of variance (ANOVA) was used to investigate the effects of
vision in the three subject groups. A two-factor design was used for
sway path analysis (3 x 2) with group as the between-subject
factor (CN, acuity controls, and normal controls) and vision as the
within-subject factor (eyes closed versus eyes open). The Tukey test
was used for post hoc comparison. A three-factor design was used for
spectral analysis (3 x 2 x 20), with frequency (0–0.25 Hz
to 4.75–5 Hz) as a second within-subject factor.
Experiment 2: Visually Induced Body Sway
Postural reorientation was provoked by moving background visual
scenery. The scenery was a flat board (2 x 3 m) subtending
67° height x 90° width of visual angle, oriented in the
transverse plane, 150 cm from the subject. Photoluminescent
yellow-green stripes fixed to the board defined the outline of a house
(Fig. 3) in an otherwise dark room. The board was mounted on a
motorized wheeled chassis running on a linear track. For background
motion, the board first accelerated for 1.25 seconds, rightward or
leftward, and then maintained a constant velocity of 6 cm/sec for 8.5
seconds. The overall displacement was 58 cm, subtending 21° from the
subject’s viewing position.
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Figure 3. Sample records of head displacements (top traces) of a
subject with CN under conditions of absolute motion and motion parallax
during background motion. Upward deflections indicate deviation in the
direction of stimulus motion. The drawings show the setups for
experiment 2.
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Test conditions: In condition 1, subjects were asked to
keep looking straight ahead at the background, which was the only
object in the visual scene, and not to follow any particular point
(absolute motion, Fig. 3A
). In condition 2, subjects fixated a cross
(1 x 1 cm) in the center of a foreground target consisting of a
photoluminescent rectangular window frame lattice (30 cm wide, 24 cm
high). This window was located straight ahead of the subject, 50 cm
from the eyes and 100 cm in front of the visual background. The
background was visible through the window panes (motion parallax, Fig. 3B ). Under each condition, subjects underwent 15 pseudorandomized
trials: 5 with background motion to the right, 5 with motion to the
left, and 5 control trials with the background stationary.
Postural reorientation in the lateral direction was evaluated as the
shift in the average position of the COP and of the head during the
constant-velocity part of stimulus motion, relative to a 4-second
baseline preceding background motion. Trials were averaged for each
subject and visual condition. Student’s t-tests were
used to compare CN with control subject data.
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Results
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Experiment 1
The sway path data measured from COP and head recordings for CN
and the two control groups are given in Table 2
.
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Table 2. Mean Sway Path Length and SD of Both the COP and the Head for the
Eyes–Closed and Eyes–Open Conditions in CN and Acuity and Normal
Control Groups
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Effect of Vision on COP
Comparisons between the sway path lengths measured in the
eyes-open and eyes-closed conditions indicated that visual
stabilization of the COP was more effective in the two control groups
than in the subjects with CN. The sway path of the COP with eyes open
was reduced only by 19% in the subjects with CN compared with 59% and
57% in the acuity control and normal control subjects, respectively.
Figure 1A
illustrates the improvement of stability (%) with vision for each
individual CN and acuity control subject. The significant interaction
between the group factor (CN, acuity control and normal control groups)
and the vision factor (eyes closed versus eyes open) confirmed that
vision was more stabilizing in the two controls groups compared with
the CN group (ANOVA: P < 0.05). Post hoc comparison
indicated that there was no difference among the three groups with eyes
closed (P > 0.05). In the eyes-open condition, the
sway path was longer in subjects with CN than in the other two control
groups (P < 0.01). No differences of any kind were
observed between the acuity control and normal control subjects
(P > 0.05).
Spectral analysis of COP for the CN and the acuity control subjects is
shown in Figure 2
. The frequency characteristics of the visual effect on COP
displacements can be inferred from a comparison of the spectra of sway
obtained with eyes closed versus eyes open.12
In CN,
visual stabilization of the COP was restricted to frequencies lower
than 1 Hz (Fig. 2A)
. In contrast, for acuity control subjects (and
normal control subjects), vision had an effective stabilizing influence
on COP throughout the frequency range 0 to 5 Hz (Fig. 2B
for acuity
control subjects). Visual stabilization of the COP was significantly
more effective in the control subjects (acuity control and normal
control subjects) than in the subjects with CN, reflected by the
significant interaction between the group factor and the vision factor
(ANOVA: P < 0.05). ANOVAs examining for within group
effects indicated that the effect of vision in the subjects with CN
failed to reach significance either as a main effect (P = 0.11) or in interaction with the frequency factor (P = 0.58). The effect of vision was similar in the two control groups
with a significant main effect of vision (P < 0.05)
and no interaction with the frequency factor (P >
0.05).
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Figure 2. Average power spectra of displacement of the COP (A,
B) and the head (C, D) in CN and
acuity control subjects in experiment 1. Power spectral density is in
log10 (in square centimeters with a frequency
resolution of 0.02 Hz). Error bars are the SD for each frequency band.
Note that the decay in power with increasing frequency for oscillatory
head movement (C, D) was greater than for
oscillations of the COP.
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Effect of Vision on Head Sway
Comparisons between the eyes-open and the eyes-closed conditions
indicated that the sway path length was shorter in the three groups of
subjects when their eyes were open than when eyes were closed (see
Table 2 ). The sway path length with vision was reduced by 27% in the
subjects with CN, 34% in the acuity control subjects, and 38% in the
normal control subjects, compared with eyes closed. As can be seen in
Figure 1B
, the improvement in stability with vision was similar to that
of acuity control subjects in five of the six subjects with CN.
Statistical analysis (ANOVA) confirmed that the reduction of the sway
path length with vision was similar in the three groups of subjects.
Post hoc comparisons indicated that there was no difference among the
three groups in the eyes-closed condition (P > 0.05).
With eyes open a significant difference between the CN and the normal
control subjects was observed (P < 0.05), but no other
comparison reached significance.
Spectral analysis showed that visual stabilization of the head in the
three groups primarily affected low frequencies of head movement. In
the subjects with CN (Fig. 2C)
visual stabilization of the head was
restricted to less than 1 Hz, whereas in the two control groups, visual
stabilization of the head was apparent up to 2 to 3 Hz (Fig. 2D
for
acuity-control subjects). Although visual stabilization of the head
appeared to have a higher frequency dynamic in the acuity control and
normal control groups, the magnitude of visual stabilization of head
sway was similar in the three groups. This was shown by the absence of
significant interactions in ANOVAs examining interactions among group,
vision, and frequency factors (P > 0.05). The
stabilizing effect of vision was significant in the three groups of
subjects, as a main effect or in interaction with the factor frequency
(P < 0.05).
Experiment 2
Postural responses to leftward and rightward stimuli were always
of similar amplitude, and thus the data were combined (Table 3)
. Figure 3
shows sample records of head displacements for a subject with CN during
background motion, with both absolute motion and motion parallax. With
absolute motion, the displacement of the background induced a
displacement of the head (and COP) in the same direction as the
background, followed by a return to baseline posture on cessation of
the stimulus. In both the CN-affected and control subjects, a postural
adjustment in the direction of motion was observed in response to
absolute motion, with a similar amplitude in the two groups, both for
the COP (t = 0.13, P > 0.05) and for
the head (t = 0.21, P > 0.05).
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Table 3. Average Position and SD of the COP and the Head under Conditions of
Absolute Motion and Motion Parallax, with Moving or Stationary
Background in Subjects with CN and Control Subjects
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With a foreground target (i.e., motion parallax) a shift of head
position (and COP) in the direction opposite to stimulus motion was
induced (Fig. 3)
. These postural adjustments in the direction opposite
to background motion were significant departures from baseline and were
of similar amplitude in the two subject groups (COP: t = 0.27, P > 0.05; head: t = 0.38,
P > 0.05).
An additional analysis was made of the results from the seven subjects
with CN who had sustained, unidirectionally beating nystagmus (Table 1)
to test whether the direction of nystagmus affected the postural
readjustment to leftward and rightward stimuli. The postural responses
were inverted in the two subjects with CN with right-beating nystagmus
to make their data comparable with that of the other five subjects with
CN with left-beating nystagmus. Student’s t-tests comparing
response amplitudes in the same versus opposite direction to the
nystagmus fast phase showed that the nystagmus direction had no effect
on COP and head data, either for absolute motion or motion parallax
(P > 0.05).
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Discussion
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Experiment 1 showed that visual control of equilibrium in the
lateral direction in subjects with CN appears to have greatest efficacy
for low-frequency components of sway (<1 Hz). However, visual control
of equilibrium was less effective in subjects with CN than in control
subjects. We could detect a marginal loss of visual stabilization of
high-frequency head movements in subjects with CN compared with control
subjects. However, high-frequency components to head movement were
minimal in both the CN-affected and the control subjects (acuity and
normal controls) and thus had little implication for postural stability
as measured. COP had more power at high frequencies than head movement.
The reduction of COP instability due to vision, was smaller in subjects
with CN than in control subjects across all frequencies, but
particularly at frequencies of more than 1 Hz. No difference was
observed between the two control groups tested (acuity controls and
normal controls), indicating that the differences between the subjects
with CN and the control subjects was not a consequence of the slightly
reduced visual acuity of the subjects with CN included in experiment 1.
With eyes closed, COP and head stability were similar in the subjects
with CN and the control subjects. These results are consistent with
previous observations,7
which support the thesis that
somatosensory and vestibular controls of posture in subjects with CN
are normal.
Experiment 2 showed that the use of visual information to control body
orientation in space (i.e., overall tilt) was normal in CN. Visually
induced body sway under conditions of absolute motion and motion
parallax did not differ among subject groups. Consistent with reports
in the literature, absolute motion induced ipsidirectional body
sway,10
11
12
whereas juxtaposing a stationary target
between subject and background provoked sway contradirectional to
background motion.13
14
Thus, despite their nystagmus,
subjects with CN made normal use of visual motion cues, including
motion parallax, to control postural orientation.
Insight into the impairment of visual control of high-frequency
postural instability in CN is given by the behavior of normal subjects
in stroboscopic light, when the flashes are presented at a strobing
frequency of 3 to 5 Hz.22
23
24
25
26
27
This frequency range is
similar to the nystagmus frequency in this sample of subjects with CN
(see Table 1
). Isableu et al.22
showed that subjects with
normal vision, standing in front of a tilted frame, leaned in the
direction of tilt under normal or stroboscopic lighting (2.8 Hz).
Displacement of an oscillating background under strobed light also
causes a continuous modulation of low-frequency postural
sway.23
These results indicate that discrete visual
sampling is sufficient for controlling body orientation. However,
unlike body orientation, normal equilibrium appears to be degraded
under stroboscopic vision at frequencies lower than 6
Hz.24
25
26
Measured at different levels, from ankle to
head, the destabilizing effect of such discrete visual sampling
principally affects the lower parts of the body.27
The
latter investigators concluded that discrete visual information (static
cues) were sufficient to control the upper part of the body, which has
predominantly low-frequency dynamics. Visual motion cues (dynamic cues)
control oscillations of the lower part of the body, which extend
through a higher frequency range. Thus, subjects with CN appear to be
similar to normal subjects in stroboscopic light, in that they share
some ability to orient and control low-frequency head instability but
are less able to control the higher frequency instabilities of the COP
with the visual cues available. Dynamic visual cues, requiring
continuous visual feedback, appear to be particularly crucial for fast
stabilization of the COP.
The similarity between normal subjects in stroboscopic light and
subjects with CN is consistent with the concept that the waveform of CN
affords intermittent, low-frequency visual sampling at the time of the
foveation periods. Subjects with CN do not behave as though they were
exposed to continuous visual motion because of their nystagmus, and
this intermittent sampling of vision to control posture may be related
to the mechanism whereby they suppress oscillopsia.
The mechanisms proposed for suppressing oscillopsia in CN include a
reduced sensitivity to retinal image motion5
6
28
; an
ability to extract visual information during foveation periods (the
parts of the nystagmus waveform when the eyes are quiescent and
images are most stable on the fovea) and to ignore the smeared vision
during high-velocity slow phases2
29
30
; and the use of
extraretinal signals—i.e., efference copy of the CN waveform—to
negate the visual effects of the oscillation.4
31
32
Of
these, the most recent evidence suggests that the efference copy of the
CN waveform is the major factor in oscillopsia
suppression.4
32
Although foveation periods may not be
primarily responsible for oscillopsia suppression, they are important
for visual acuity,32
and they may be responsible for the
discrete sampling of visual cues to postural orientation in CN.
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Acknowledgements
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The authors thank the volunteers who enthusiastically participated
in this project.
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Footnotes
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Submitted for publication October 18, 1999; revised April 4 and June 16, 2000; accepted July 5, 2000.
Commercial relationships policy: N.
Corresponding author: Michel Guerraz, MRC Human Movement and Balance Unit, Institute of Neurology, National Hospital for Neurology and Neurosurgery, 8-11 Queen Square, London WC1N 3BG, UK. m.guerraz{at}ion.ucl.ac.uk
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Top
Abstract
Introduction
) and acuity control (
) subject for both the COP
(A) and the head (B) in experiment 1. This index
of performance was computed as: [(eyes-closed score - eyes-open
score)/(eyes-closed score)] x 100.