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Academic Department of Neuro-Otology, Division of Neuroscience and Psychological Medicine, Faculty of Medicine, Imperial College London, Charing Cross Hospital, London W6 8RF, United Kingdom
Submitted 24 October 2002; accepted in final form 15 March 2003
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESREFERENCES |
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40°
forward from upright. During head upright/backward conditions, a significant
SVV tilt (P < 0.01) in the direction opposite to rotation was
found that reversed during postrotary responses. The rotationally induced SVV
tilt had a time constant of decay of 30 s. Rotation with the head 30°
forward did not affect SVV, whereas the 40° forward tilt caused a
direction reversal of SVV responses compared with head upright/backward.
Spearman correlation values (Rho) between individual SCC efficiencies in
different head positions and mean SVV tilts were 0.79 for posterior, 0.34 for
anterior, and – 0.80 for horizontal SCCs. Three-dimensional
video-oculography showed that SVV and torsional eye position measurements were
highly correlated (0.83) and in the direction opposite to the slow phase
torsional vestibuloocular reflex. In conclusion: 1) during yaw axis
rotation without reorientation of the head with respect to gravity, the SVV is
influenced by SCC stimulation; 2) this effect is mediated by the
vertical SCCs, particularly the posterior SCCs; 3) rotationally
induced SVV changes are due to torsional ocular tilt; 4) SVV and
ocular tilts occur in the "anticompensatory," fast phase direction
of the torsional nystagmus; and 5) clinically, abnormal SVV tilts
cannot be considered a specific indication of otolith system dysfunction. |
INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESREFERENCES |
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;
Miller and Graybiel 1966). In the upright position, stationary normal subjects
are able to set a luminescent bar with great accuracy to within a mean
deviation of ±2° of the true gravitational vertical (Friedman
1970). As a result, clinical studies emphasize that greater than average tilts
of the subjective visual vertical (SVV) are a sensitive tool for detecting an
imbalance in otolith function (Böhmer
and Mast 1999; Gresty et al.
1992; Halmagyi and Curthoys
1999; Tabak et al.
1997; Vibert et al.
1999).
Early experiments, however, have been neglected. For instance, Holst and
Grisebach (1951), Udo de Haes
and Schöne (1970), and
Stockwell and Guedry (1970)
all noted that the SVV was affected by stimulation of the vertical (anterior
and posterior) semicircular canals (SCCs) during roll plane rotation. More
recently, observations on the subjective visual horizontal (SVH) during
centrifugation in a free-swinging gondola also found a tilt of the SVH
(Tribukait 1999). In this
study, the recorded SVH offset was induced during centrifuge acceleration,
thereby suggesting that the vertical SCCs may have played a role in the
formation of the SVH.
However, a common criticism to roll motion
(Holst and Grisebach 1951;
Stockwell and Guedry 1970;
Udo de Haes and Schöne
1970) and centrifugation studies
(Tribukait 1999) is that both
involve combined SCC and otolith stimulation. Therefore the specific
contribution of the SCCs to the perception of verticality cannot be clearly
deduced.
The purpose of this study is therefore to examine the effect of SCC
stimulation on the SVV during earth-vertical yaw axis angular acceleration
when otolith interaction is minimal. In two studies by Curthoys and coworkers
(Smith et al. 1995;
Wade and Curthoys 1997),
consistent ocular torsional changes during yaw angular acceleration, and a
significant correlation between SVH settings and torsional eye position, were
reported. These studies, however, did not assess a distinct contribution of
the vertical or horizontal SCCs. Therefore the origin of the SVV tilt induced
by yaw rotation and, more generally, the role of the vertical SCC in visual
verticality perception remains unclear.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESREFERENCES |
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Eight healthy normal individuals (6 males, 2 females; mean age: 27.5 yr, range: 21–36 yr) with no evidence of vestibular disturbance participated in the study, which was approved by the local ethics committee. Subjects were seated on a motorized Bárány chair (combined control from Contravez-Goerz, CA, and Acutronic Schweiz AG, Switzerland) fitted with head, foot, and armrests and a safety belt. The SVV apparatus was attached to a chair-mounted framework, supporting a 40-cm-long bar with a 1-mm-wide luminescent strip. This bar could be rotated in the frontal plane and was centered at eye level, 48 cm in front of the subject (Fig. 1A). The framework could be vertically adjusted 13 cm to place the bar closer to primary gaze for each head position. Rotation of the bar was controlled by a wheel located near the subject's right hand via a pulley system. The orientation of the bar was measured using a potentiometer.
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SVV procedure
Subjects were instructed to close their eyes, offset the luminescent bar by a random large amount, clockwise or counter-clockwise, then open their eyes and reset the bar to their perceived gravitational vertical. A pushbutton, in the subject's left hand, was used to signify satisfaction with the adjustment. A pilot study indicated that the average SVV measured using this procedure was the same as that measured with the experimenter offsetting the bar while the subject's eyes were closed. Experiments were conducted in a dark room, and the subject was observed with an infra-red camera.
Stimuli
The SVV was measured under a static condition, during clockwise (= rightward) and counter-clockwise whole body yaw rotations about an earth-vertical axis and during the postrotary periods. Rotations were velocity steps of 60-s constant velocity at 90°/s and acceleration/deceleration periods of 2 s.
In the static condition, subjects repeated the SVV procedure six times. In the rotation conditions, subjects were instructed to repeat the SVV procedure continuously, throughout the yaw rotation and during a 60-s postrotary period. For each rotation and postrotary period, an average of eight settings was obtained from each subject. Subjects completed one rotation and postrotary period for each direction, clockwise and counterclockwise.
Head positions
Subjects were rotated about an earth-vertical axis with different head positions to vary the relative amount of horizontal and vertical SCC stimulation. The static and rotation conditions were repeated with four different pitch positions: head "normal" (HN) with the subject looking straight ahead in a comfortable position; head up (HU) with the occiput pitched backward ca 30° from the normal position; head down (HD) with the nose pitched downward ca 30° from the normal position; and head further down (HFD) ca 40° from the normal position (Fig. 1B). The degree of tilt in HU and HFD was limited by the comfortable range of motion that could be achieved by subjects. A rigid arc-shaped metal head restraint placed against the occiput and a chin rest, both appropriately padded, secured the head in each pitch position. The head was located at the center of chair rotation for maximal SCC and minimal otolith stimulation.
To measure changes in the head angle accurately, a rigid plastic rod was
attached with surgical tape to the subject's head throughout the experiment.
This rod represented a line from the superior border of the external auditory
meatus to the outer canthus of the eye (Reid's plane). The orientation of this
line with respect to the gravitational horizontal was measured using a large
protractor with an attached spirit level. The head angle was measured before
and at the end of rotation in each head position. In HN, the anterior end of
the plastic rod was 10° above horizontal. The order in which the
different head positions were used and the initial rotation direction in each
head position were randomized between subjects.
For each head position, an estimate of the relative magnitude of
stimulation of the horizontal, anterior, and posterior canal planes was
calculated using the average planar equations from Blanks et al.
(1975). The efficiency of canal
stimulation was calculated from the projection of the canal plane onto the
stimulus (earth-horizontal) plane for each individual's measured head
position. The planar equations given by Blanks et al.
(1975) are referenced to the
Reid stereotaxic coordinate system in which the inferior margin of the orbits
and the center points of the two external auditory canals lie in the
horizontal plane. The general form of these planar equations is
x + 
+ z = 0. When the subject's
head is pitched by 
degrees from the Reid reference position (positive
for forward pitch), then the efficiency of canal stimulation by
earth-horizontal yaw acceleration is given by (– sin +
cos ). Peak efficiency, or optimal plane of stimulation, is
obtained when the canal plane lies closest to the earth-horizontal plane; zero
stimulation occurs when the canal plane is vertical, and a sign reversal
indicates a reversal in the stimulation direction of the canal.
Data analysis
The orientation of the bar, the push-button signal and chair velocity were recorded at a sampling frequency of 50 Hz. The SVV values were taken as the angular deviations of the luminescent bar from true gravitational vertical at the times indicated by the push-button signal. Tilt of the top of the luminescent bar to the subject's right was indicated as a positive value and a tilt toward the left negative. For each subject, in each head position, the average SVV during the static condition was used as a baseline for the subsequent rotational SVV values. Data points occurring during the 2-s periods of acceleration were discarded.
Supplementary experiments
EXPERIMENT 2: SIMULTANEOUS SVV AND EYE-MOVEMENT RECORDINGS AFTER HN YAW ANGULAR ACCELERATION. In a separate session, four of the subjects were rotated in the HN position, while wearing a three-dimensional (3D) video-oculography mask (SensoMotoric Instruments, Berlin, Germany) fixed with heavy-duty occipital bands and a two-way adjustable helmet. The video-oculography system consisted of a free-field-of-view mask and a battery-powered video recorder, to tape high-quality images of the subject's right eye, at 25 frames/s. The tape recording was analyzed off-line using field sampling (alternate analysis of odd and even lines in the video image), to give horizontal, vertical, and torsional eye position at 50 Hz. Spatial resolution was 0.1° for the torsional channel and <0.03° for horizontal and vertical eye position. During these experiments, the subjects were asked to keep their eyes open all the time and to continuously adjust the luminescent bar to subjective verticality.
EXPERIMENT 3: EFFECT OF VERTICAL EYE POSITION ON THE SVV AFTER HN YAW ANGULAR ACCELERATION. In Experiment 1, the center of the luminescent bar was at eye level during the HN condition. However, due to mechanical limitations of the framework, the center of the bar remained below primary gaze in the HU condition and above primary gaze in the HD and HFD conditions. As a supplementary experiment, the effect of vertical eye position on SVV measurements was investigated by repeating the static and rotation conditions in the HN position with the subject's eyes in normal primary gaze (eyes normal, EN), with eyes looking up (EU), or with eyes down (ED).
Eight subjects (6 males, 2 females; mean age: 27.5 yr, range: 21–41 yr), three of whom had also participated in Experiment 1, were seated on the Bárány chair. Seat height was adjusted for each individual so that primary gaze was at the same level for all subjects. The subject always fixated the center of the luminescent bar, which was positioned straight-ahead (EN), 19 cm (21.5°) above (EU), or 40 cm (39.8°) below (ED) the primary gaze direction. The eye deviations in the EU and ED conditions were specified to match the average deviations from primary gaze that were present during the HD and HU conditions, respectively, in Experiment 1. During these trials, participants were asked to keep their eyes open and to use the adjustment wheel to continuously maintain the luminescent bar at their perceived vertical.
For the vertical eye position experiments, the continuous SVV responses to the four rotational stimuli were normalized in polarity for direction and averaged. The peak SVV change, from the average prestimulus baseline, was measured.
Statistics
All statistical analyses were performed using the SPSS software package (SPSS, Chicago, IL). Data are presented as means ± SE (n = 8). In Experiment 1, the effect of head position on SVV tilt, both for the static condition and the rotational stimuli, was analyzed as a one-factor repeated-measures ANOVA. For the rotational stimuli, the polarity of the right rotation and left stop responses was reversed, prior to combining with left rotation and right stop responses, to find the average SVV tilt. A one-factor repeated-measures ANOVA was also performed to look at the effect of the four individual rotational stimuli on SVV tilt in each head position. The average response from the first 20 s of stimulation for each subject was used for both analyses. When significant differences were indicated by the ANOVA, Bonferroni post hoc tests were performed. The same statistical methodology was used to test the effect of varying vertical eye positions on SVV tilt. The nonparametric Spearman correlation coefficient was used to compare estimated SCC efficiency with mean SVV tilt.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESREFERENCES |
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Inspection of raw records for HN and HU showed that yaw rotation induced a tilt of the SVV settings in the opposite direction to rotation. During stopping, the direction of the SVV tilt reversed. The SVV tilt was larger with HU, not discernible with HD, and often reversed in polarity during HFD. Detailed analyses now follow.
Under static conditions, the mean value of the SVV tilt was not significantly dependent on head position, although the combined signed average for all subjects showed a slightly greater tilt of the SVV in HFD (1.6 ± 0.9°; mean ± SE) than in the other three head positions (0.7 ± 0.7° in HN and 1.1 ± 0.7° in HU and HD).
The rotational stimuli evoked SVV tilt with respect to the static values. In the HN and HU positions, rotation to the left and the cessation of rotation to the right both produced a right (positive) SVV tilt, whereas yaw rotation to the right and the cessation of yaw rotation to the left both produced a negative SVV tilt. However, SVV tilt direction was typically reversed in the HFD position (25 of 32 test trials) compared with that in the HN, HU, and HD positions (Fig. 2; NB: a trial is a single rotation or postrotary period). Tilts of the SVV in all rotations mostly occurred during the initial 5 s of each stimulus, reaching peak values within 20 s and then decaying (Fig. 3). It should be noted that SVV settings were always in the direction opposite to that expected if the SVV tilts were due to the slow phase torsional vestibuloocular reflex (VOR; see DISCUSSION). At the end of each 60-s window (per- and postrotary period) an average tilt of 1°, with respect to the static values, remained in all head positions.
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The magnitude of the SVV rotational response (for each subject, in each
head position) was quantified by averaging all SVV settings occurring within
the first 20 s of each stimulus (after reversing the sign of the right
rotation and left stop responses). Individual subjects made, on average, 2.6
SVV settings within the first 20 s of each stimulus, giving a total of 83
responses for each head position (8 subjects, 4 stimuli). One-factor
repeated-measures ANOVA showed a significant effect of head position on tilt
of the SVV (P < 0.01). Bonferroni post hoc comparisons showed a
significant difference for SVV tilt (P 
0.04) among all head
positions with the greatest differences (P < 0.01) found between
HU (mean SVV tilt: 3.0 ± 0.4°) and HD (0.4 ± 0.2°),
between HU and HFD (–0.7 ± 0.3°), and between HN (1.9
± 0.3°) and HFD (Fig.
4).
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There was a significant dependence of the SVV on the direction of the
rotational stimulus in both HN and HU positions (P < 0.01), but
there was no significant dependence in the HD and HFD positions. For HN and
HU, Bonferroni post hoc comparisons showed significant differences when right
rotation or left stop were compared with left rotation or right stop
(P 0.01), but there was no difference between right rotation and
left stop responses or between left rotation and right stop responses. The
statistical differences found in HN and HU relate to response polarity (sign)
but not magnitude of tilt, which was similar for both left and right per- and
postrotary periods.
Figure 5 illustrates the relationship between the mean SVV tilt and SCC efficiency as defined in METHODS. The degree of SVV tilt was smallest in the HD position, where the estimated magnitude of posterior and anterior canal stimulation was low (average efficiencies of 0.14 and –0.17, respectively) but the horizontal canal stimulation was near its peak (average efficiency of 0.96). The degree of SVV tilt tended to increase as the head was pitched backward and the vertical canals were brought progressively into the earth-horizontal plane. Because the geometrical relations between all canals are anatomically fixed, increasing activation of one pair of canals, e.g., the posterior canals, is associated with decreasing activation in a different pair, e.g., the horizontal canals. Thus for HN, canal stimulation increased for the posterior canal (average efficiency: 0.54) and remained high for the horizontal and low for the anterior canal (average efficiencies: 0.76 and 0.18, respectively). In the HU position, the average efficiencies of the posterior and anterior canals reached 0.78 and 0.47, respectively, but the horizontal efficiency was reduced to 0.34. A Spearman correlation of the magnitude of SVV tilt versus the degree of canal efficiency indicated a strong positive correlation for the posterior canal (rho = 0.79), a weaker correlation for the anterior canal (rho = 0.34), and a strong negative correlation for the horizontal canal (rho = –0.80). Thus as can be seen in Fig. 5, the largest SVV tilts occurred for head positions with the strongest posterior and weakest horizontal canal stimulation, whereas the smallest SVV tilts occurred for head positions in which stimulation of the posterior canal was minimal but stimulation of the horizontal canal was strongest. Also the pitch angle of the head at which the zero crossing of the SVV tilt occurred (at about +20°, Fig. 5) seemed to correspond most closely with the zero crossing of the canal efficiency plot for the posterior canal. Note that over this range of head angles (0–40°), the efficiency of the horizontal canal remains essentially constant. For anterior canal stimulation, the weaker correlation is due to the fact that the magnitude of anterior canal stimulation in the HN and HD positions is fairly similar (although the direction of the stimulation is reversed), but the SVV tilt is much larger in the HN position (Fig. 5). A change in sign of the canal efficiency indicates a reversal in the stimulation direction for the canal and, for the posterior canal, this corresponded to the reversal of the SVV tilt.
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Given that the SCCs are generally seen as acting in pairs, it is important to explain how the analysis deals with this fact. The horizontal SCCs on the right and left sides of the head are symmetrically placed about the sagittal plane. Because our experiments only involve different pitch head positions and rotational stimulation in the earth-horizontal plane, the projections of the canal planes onto the plane of stimulation or in other words the "efficiency" of canal stimulation will be identical for the right and left sides. Depending on the direction of chair rotation, one side will produce an ON response and the other side will produce an OFF response, but the strength of the combined response depends on the canal efficiency; similarly for the posterior canal pair and the anterior canal pair.
A time constant for the decay phase of the SVV response was estimated using data from the HU condition because this condition induced the largest tilts. The signs of the right rotation and left stop responses were reversed then the data from all of the subjects and the four stimuli were averaged in 5-s bins. The mean peak SVV response was 3.3° (at 15–20 s after acceleration; see Fig. 3). The time constant for the decay of this response was taken as the time required for the average response to decrease to 37% of its peak value and was measured to be 30 s.
Experiment 2: simultaneous SVV and eye-movement recordings following HN yaw angular acceleration
The rotational stimuli produced nystagmic responses and torsional deviation
of the eyes. Yaw rotation to the left and the cessation of yaw rotation to the
right both induced a left-beating horizontal nystagmus and torsional deviation
of the eyes to the right (top of the eye tilting toward the subject's right
shoulder). Stimuli in the opposite direction (yaw rotation to the right and
the cessation of yaw rotation to the left) induced a right-beating horizontal
nystagmus and torsional deviation of the eyes to the left. Torsional nystagmus
was less consistently observed. All of the eye-movement responses decayed
during the constant velocity phase of the stimulus. The torsional eye movement
responses (4 subjects x 4 stimuli) were averaged to produce a
"mean" response in which the torsional eye position reached a peak
6 s after the onset of the stimulus. The averaged torsional response
remained fairly steady for 5 s and then decayed in an approximately
exponential fashion with a time constant of 23 s.
Figure 6 illustrates one
subject's responses to the initiation and cessation of yaw rotation to the
left [NB: the additional small up-beating nystagmus observed is a common
occurrence in 1/3 of normal subjects and is tilt sensitive
(Bisdorff et al. 2000;
Kim et al. 2000)].
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The continuous SVV measured during the 3D video-oculography recordings was in accordance with the SVV data obtained during HN stimulation in Experiment 1. In Experiment 2, simultaneous 3D video-oculography and SVV recordings showed that the SVV tended to follow the torsional eye position; all individual data are shown in Fig. 7. A normalized cross-correlation of torsional eye position and SVV angle was calculated for each 120-s trial; the mean peak correlation value (excluding left rotation data for subject S3 due to the erratic SVV settings and excessive blinking) was 0.83. The individual correlation coefficients of torsional eye position with SVV angles were 0.87 (S1), 0.84 (S2), 0.92 (S3), and 0.77 (S4). SVV settings lagged torsional eye position by an average of 3.5 s, the delay allowing for all the preceding perceptual and manual processes involved in the task. We measured the ratio of peak change in SVV angle with respect to peak change in torsional eye position. The mean change in SVV tilt was 76% of the torsional eye position change, with individual values of 69% for S1 and S2 and 80 and 84% for S3 and S4, respectively.
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Surprisingly, both the ocular tilt and SVV settings were in a direction opposite to the direction of yaw acceleration, i.e., an opposite direction to that which may have been expected from the slow phase torsional VOR (see DISCUSSION). For this reason, the individual eye-movement recordings were visually inspected. Clear torsional nystagmic patterns were identified in 3/4 subjects. In 50% of the trials, the net change in ocular torsional position was due to fast phase activity rather than to the slow phase component of the torsional VOR (Fig. 6). However, in the remaining cases, the net torsional deviation could not be confidently ascribed to clearly defined slow or fast phase eye movements.
Experiment 3: effect of vertical eye position on the SVV following HN yaw angular acceleration
This was a control experiment to see whether SVV recordings in Experiment 1 might have been influenced by different vertical eye positions. As expected, the rotational SVV response in this experiment, with continuous visual vertical adjustment, was generally similar to that recorded in the original HN experiment (Experiment 1). The mean peak tilt of the SVV in the EN condition was 2.6 ± 0.4°. The response was similar in the EU condition (mean peak tilt: 2.7 ± 0.5°). However, in the ED condition the average peak SVV tilt was reduced to 1.4 ± 0.6°.
Repeated measures ANOVA indicated a statistically significant effect of eye position on SVV tilt (P = 0.04) but further analysis with Bonferroni post hoc comparisons failed to indicate any significant mean differences between various eye positions. Static averages showed no significant difference between eye positions.
In none of the three experiments did subjects volunteer illusions of body tilt. Four additional subjects were separately rotated while viewing the static luminous line placed vertically in the four head positions and were specifically asked to report any body tilt sensations. All responses were always negative.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESREFERENCES |
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;
Brandt and Dieterich 1994;
Gresty et al. 1992;
Halmagyi and Curthoys 1999;
Tabak et al. 1997;
Vibert et al. 1999). First we
will discuss the effect of rotation on the SVV and then the relation between
the SVV and eye movements. Subjective visual vertical and vertical semicircular canal activity
In these experiments, SCC stimulation was delivered by on-axis angular rotation about an earth-vertical axis. In this way, there was no net stimulus delivered to the otoliths. Thus the differences in SVV tilt due to rotation with the head in different positions (HN, HU, HD, HFD) relate to the variable proportion of stimulation given to the horizontal or vertical SCCs.
Most previous work on the effect of SCC stimulation on the SVV involved
roll plane rotation around an earth-horizontal axis
(Holst and Grisebach 1951;
Stockwell and Guedry 1970;
Udo de Haes and Schöne
1970) or centrifugation
(Tribukait 1999), which
stimulated not only the SCC but also the otoliths. Tribukait
(1999) influenced the
subjective visual horizontal by centrifugation with a free-swinging gondola so
that the subject's main longitudinal body axis aligned itself with the net
gravitational vector. [NB: for simplicity, we will consider that subjective
horizontal and vertical are equivalent although dissociation between these two
measurements can occur (Betts and Curthoys
1998; Pettorossi et al.
1998)]. It was argued that the actual body tilt with respect to
earth-vertical could only be sensed by the vertical SCC and that there was no
roll stimulus to the otolith organs. However, Tribukait
(1999) admitted that some
subjects correctly perceived that they were tilted with respect to earth
vertical and that the magnitude of the visual tilt was a function of the
g levels attained. In view of these two factors, namely tilt
perception and g-level dependence, how much of the visual tilt
observed could be attributed to the vertical SCCs in these experiments is not
clear. The experiments by Curthoys and coworkers
(Smith et al. 1995;
Wade and Curthoys 1997), with
yaw rotation in the normal upright position (i.e., no otolith stimulus)
produced a bias in torsional eye position that correlated closely with the
rotationally induced tilts of the visual horizontal. The effect was attributed
to SCC stimulation and "cross-coupling of the horizontal head-velocity
signal to a torsional eye position integrator," but the specific
possibility that the vertical SCCs could have induced the ocular or SVH tilt
was not raised.
Our experiments were based on the hypothesis that SVV tilt during earth-vertical axis yaw rotation is due to vertical SCC stimulation. This was confirmed by the existence of a positive correlation between vertical SCC stimulation and mean SVV tilt as indicated by Fig. 5. When the head was pitched back (HU), both vertical SCC stimulation and SVV tilt were greater than for any other head position tested. When the head was tilted forward (HD), vertical SCC stimulation was minimal and there was no measurable effect of rotation on the SVV. Had the SVV tilt been mediated by horizontal canal activity, then the effect would have been larger in this particular head position because the horizontal canal planes were closely aligned with the rotational plane. Moreover, even in HFD where the horizontal canals continued to experience strong stimulation in the same rotational direction, the tilt of the SVV was reversed with respect to HN or HU as expected if the vertical canals mediated the observed effects (Fig. 5). Although both anterior and posterior canals are contributory, the reversal in SVV tilt responses coincided with the change in the direction of posterior SCC stimulation, and, in fact, correlation analysis showed that SVV tilt was more strongly associated with posterior rather than anterior SCC stimulation.
Ocular movements and subjective visual vertical
Several aspects deserve discussion: whether the SVV effects described could be an artifact related to vertical eye position, the relation between torsional eye position and the SVV, including the polarity and the duration of the rotationally induced SVV tilt.
VERTICAL EYE DEVIATION. During Experiment 1, the subjects' eyes were not in primary gaze for all head positions tested, so it was important to ensure that our results were not due to varying vertical eye position. The rotational SVV responses in the supplementary eye positions experiment (Experiment 3) were similar to those recorded in Experiment 1 but with rotationally induced SVV tilts being smaller with ED than with EN and EU. This trend was statistically significant with the ANOVA (P = 0.04) but post hoc Bonferroni comparisons failed to confirm significant differences between SVV values in the different eye positions. Because ED in the original experiment was adopted during HU, the results of the eye-position experiment indicated that, if anything, the effect observed during the HU condition could have been underestimated. Our experiments with the normal head position (HN) kept the eyes around primary gaze thus vertical ocular deviation was never an issue. It may be worth mentioning that convergence is not a confounding issue either due to the fact that nasion-target distance was kept constant in all conditions.
TORSIONAL EYE POSITION. 3D video-oculography showed that SVV settings and torsional eye position followed a similar temporal and directional pattern with torsional deviation of the eyes and SVV tilt occurring in the same direction for identical stimulation, with a similar time constant and a mean peak correlation coefficient of 0.83. An amplitude comparison showed that 76% of the torsional change is reported by subjects as SVV tilt or, in other words, that only 24% of ocular tilt is not reported by subjects as SVV tilt.
These findings confirm those of Wade and Curthoys
(1997), but a limitation
present in their experiment, namely the technical impossibility of obtaining
simultaneous ocular and SVV recordings, was overcome in the present study.
This allowed us to cross-correlate the two measurements and measure the
average delay between torsional eye position changes and SVV settings, which
was found to be 3.6 s. In agreement with Wade and Curthoys
(1997), we conclude that
ocular torsional position plays a critical role in SVV tilt perception and
that both are influenced not only by otolith
(Brandt and Dieterich 1994;
Miller and Graybiel 1966; Mittelstaedt
1992) but also by vertical SCC activity. During body tilt,
somatosensory input also plays a role in the perception of the SVV
(Anastasopoulos and Bronstein
1999; Bronstein
1999).
One should not conclude, however, that all rotationally induced SCC effects
on tilt perception relate to changes in ocular torsional position. Recently,
Merfeld et al. (2001)
conducted human centrifuge experiments and observed changes in the time course
of visual (SVV) and somatosensory tilt perception, according to the presence
or absence of earth-vertical yaw rotational cues. Clearly, yaw effects on the
somatosensory task cannot be ascribed to ocular torsional changes.
Unfortunately, the possibility that yaw rotation effects on tilt perception
may be due to vertical SCC activation was not considered nor were torsional
eye movements recorded. This consideration, however, may be of value in
interpreting some differences between two sets of similar experiments in the
literature (Merfeld et al.
2001; Seidman et al.
1998). In these experiments, subjects were centrifuged with the
head in the upright position with the variable radius (or dynamic-radius)
technique. Essentially, subjects are initially rotated on axis and then, when
all canal effects are extinguished, linearly displaced to the eccentric
position. In doing so, subjects are exposed to the centrifugal acceleration
without further canal signals and accordingly report body and visual tilt. In
the Merfeld et al. (2001)
experiment, subjects were displaced laterally along the interaural axis, and
the subjective tilt reported was in the roll plane. In the Seidman et al.
(1998) experiments, subjects
were displaced in the fore-aft axis, and so the tilt experienced was in the
pitch plane. Whereas the findings in these two experiments are overall in
agreement, it is not clear why the development of the tilt illusion was
considerably slower in the fore-aft displacement experiments. We would suggest
that the addition of roll-motion cues arising from activation of the vertical
SCCs during head-upright rotation (as discussed in this study) may facilitate
the development of the tilt illusion in the roll plane but not in the pitch
plane. We are, however, skeptical of our own suggestion. One would expect that
centrifugation in the side-on position should produce larger/faster tilt
illusions when subjects face the direction of motion than when they are moving
backward on the basis that in the facing motion position, vertical SCCs and
otolith input would signal roll-motion and roll-tilt outward congruently. For
instance, clockwise rotation facing motion will deliver a leftward roll-motion
stimulus to the vertical canals and a re-orientation of the gravitoinertial
vector interpreted as left tilt. When backing the direction of motion, canal
cues remain identical but the tilt effect is inverted, so creating
otolith-canal directional conflict. Thus one would expect better tilt
perception while facing motion, but actually the opposite is the case
(Merfeld et al. 2001). On the
basis of this finding, our suggestion that differences in the time course of
the pitch and roll tilt illusions during centrifugation are due to co-planar
vertical SCCs cues in the roll plane is less likely to be appropriate.
Repeating the side-on centrifugation experiments with different head positions
as in our study could help settle this problem.
POLARITY OF THE ROTATIONALLY INDUCED TILT OF THE SVV. Although
it can be concluded that the SVV tilt observed is due to vertical SCC
stimulation, attention should be drawn to the polarity of such tilt. With the
head in HN or HU positions, chair rotation to the right stimulates the
vertical SCC as in roll motion to the left. If the SVV effect followed the
slow phase torsional VOR, the expected SVV tilt would be in the opposite
direction to that of roll stimulation, i.e., SVV tilt to the right during
chair rotation to the right. However, this is not the case. Our results show
that the SVV settings are tilted in the same direction as the angular
acceleration to the vertical SCC and so, unexpectedly, cannot be explained by
the slow phase of the torsional VOR. Although Wade and Curthoys
(1997) recorded the same
polarity that we did, the observation was not discussed. We believe that the
unexpected polarity of SVV and ocular tilts results from an
"anticompensatory" ocular torsional deviation. This term was
coined by Melvill Jones (1964)
as he observed that during fast head rotations the predominant deviation of
the eyes within the orbit was not in the expected, compensatory, slow phase
direction of the VOR but in the opposite, anticompensatory direction. Such
deviation of the eyes is brought about by the fast phase components of
vestibular nystagmus and is particularly noticeable during high-velocity,
sustained head rotations (Melvill Jones
1964). The saccadic origin of this anticompensatory eye deviation
was observed in half of the Experiment 2 trials
(Fig. 6), but, in the rest of
the trials, characterization of the eye movements was difficult, a fact also
discussed by Melvill Jones
(1964). These anticompensatory
gaze shifts have since been observed with optokinetic
(Hood and Leech 1974),
vestibular (Barnes 1979;
Melvill Jones 1964), and
cervical (Bronstein and Hood
1986) stimuli and so appear to be a general property of the
oculomotor system that allow the eyes to be "... automatically thrown
into the position which will most quickly pick up the new point of
interest" (Melvill Jones
1964). It is possible that the predominantly saccadic basis for
this torsional eye deviation was not observed in the experiments by Smith et
al. (1995) and Wade and
Curthoys (1997) due to the low
video rate used (6 Hz). The sample rate we used (50 Hz) is an improvement, but
definitive identification of fast or slow phase components underlying the
anticompensatory torsional deviation would require even faster sampling
rates.
DURATION OF THE SVV AND OCULAR TORSIONAL RESPONSES. The time
constant of decay of the SVV tilt and the ocular torsional position deviation
were unusually long. The mean time constant for the decay of the response in
our experiments was 30 s for the SVV and 23 s for torsion, and it was common
to observe that by the end of the 60-s window there were often ocular and SVV
tilts remaining of 1° (see Fig.
3). Both Tribukait
(1999) and Smith et al.
(1995) also reported
long-lasting effects, much longer in duration than the expected time constant
of the horizontal (16 s) (Benson
1968; Cohen et al.
1981; Okada et al.
1999) and torsional (5 s)
(Jáuregui-Renaud et al.
2001; Seidman and Leigh
1989) VOR responses. VOR time constants generally represent the
progressive decay in slow phase velocity. Our experiments, however, show that
the SVV tilts are mediated by an anticompensatory, probably fast
phase-mediated, torsional ocular deviation. As such, the duration and time
constant of the response is not dictated by the dynamics of the slow phase
mechanisms. Pursuit or saccadic eye movements can correct position biases in
the vertical or horizontal planes of the oculomotor system, but a positional
bias in the torsional oculomotor system cannot be corrected in this way due to
absence of any tangible pursuit or voluntary saccades in this plane.
Accordingly, any position bias such as the one induced by our rotational
stimuli is likely to last until new stimuli induce torsional VOR activity. We
do not know whether spontaneous drifts or occasional "spontaneous"
torsional saccades can occur to reset torsional eye position to normal.
In summary, these experiments show that SCC stimulation consistently influences the perception of the SVV. These effects are mediated by the vertical, particularly posterior, SCCs. The SVV tilts follow changes in ocular torsional position that are due to an anticompensatory eye deviation rather than the slow phase torsional VOR. The strong warning to the clinical community is that, in light of these findings, it is incorrect to interpret lesion-induced tilts of the SVV as a result of damage only to otolith receptors and pathways.
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DISCLOSURES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESREFERENCES |
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FOOTNOTES |
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Address for reprint requests: A. M. Bronstein, Academic Dept. of Neurootology, Div. of Neuroscience and Psychological Medicine, Imperial College London, Charing Cross Hospital, Fulham Palace Road, London W6 8RF UK (E-mail: a.bronstein{at}imperial.ac.uk).
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) and stop
(
), right rotation (
) stimuli. Note the reversal
in SVV settings for identical per- and post rotary conditions in HU and HFD.
Data points have been fitted with a 3rd-order polynomial trendline so as to
portray the effect more clearly.
