Jenks Vestibular Physiology Laboratory, Massachusetts Eye and Ear Infirmary, Department of Otology and Laryngology, Harvard Medical School, Boston, Massachusetts 02114
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ABSTRACT |
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Merfeld, D. M., L. H. Zupan, and C. A. Gifford. Neural Processing of Gravito-Inertial Cues in Humans. II. Influence of the Semicircular Canals During Eccentric Rotation. J. Neurophysiol. 85: 1648-1660, 2001. All linear accelerometers, including the otolith organs, respond equivalently to gravity and linear acceleration. To investigate how the nervous system resolves this ambiguity, we measured perceived roll tilt and reflexive eye movements in humans in the dark using two different centrifugation motion paradigms (fixed radius and variable radius) combined with two different subject orientations (facing-motion and back-to-motion). In the fixed radius trials, the radius at which the subject was seated was held constant while the rotation speed was changed to yield changes in the centrifugal force. In variable radius trials, the rotation speed was held constant while the radius was varied to yield a centrifugal force that nearly duplicated that measured during the fixed radius condition. The total gravito-inertial force (GIF) measured by the otolith organs was nearly identical in the two paradigms; the primary difference was the presence (fixed radius) or absence (variable radius) of yaw rotational cues. We found that the yaw rotational cues had a large statistically significant effect on the time course of perceived tilt, demonstrating that yaw rotational cues contribute substantially to the neural processing of roll tilt. We also found that the orientation of the subject relative to the centripetal acceleration had a dramatic influence on the eye movements measured during fixed radius centrifugation. Specifically, the horizontal vestibuloocular reflex (VOR) measured in our human subjects was always greater when the subject faced the direction of motion than when the subjects had their backs toward the motion during fixed radius rotation. This difference was consistent with the presence of a horizontal translational VOR response induced by the centripetal acceleration. Most importantly, by comparing the perceptual tilt responses to the eye movement responses, we found that the translational VOR component decayed as the subjective tilt indication aligned with the tilt of the GIF. This was true for both the fixed radius and variable radius conditions even though the time course of the responses was significantly different for these two conditions. These findings are consistent with the hypothesis that the nervous system resolves the ambiguous measurements of GIF into neural estimates of gravity and linear acceleration. More generally, these findings are consistent with the hypothesis that the nervous system uses internal models to process and interpret sensory motor cues.
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INTRODUCTION |
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Einstein's Equivalence
Principle reveals that no single type of device (e.g., no set of linear
accelerometers) can distinguish linear acceleration from gravity. All
linear accelerometers, including physiological graviceptors (e.g.,
otolith organs), measure gravito-inertial force (GIF), which can be
represented as gravity minus linear acceleration.1
However, physiological systems must respond differently to those forces
due to gravity (e.g., postural control) than to those forces due to
linear acceleration [e.g., translational vestibuloocular reflex
(VOR)]. Therefore the presence of this measurement ambiguity requires
the nervous system to develop neural processes to distinguish tilt with
respect to gravity from translation due to linear acceleration. It has
been proposed that simple filtering is utilized to separate ambiguous
GIF into neural representations of tilt and translation. For example,
eye-movement data have been interpreted to indicate that otolith cues
are low-pass filtered to yield tilt responses and high-pass filtered to
yield translation responses (Mayne 1974; Paige
and Tomko 1991
). This explanation is consistent with responses measured during pure translational stimulation but inconsistent with
responses during motion paradigms that include rotation. Therefore we
hypothesized (Merfeld 1990
, 1995b
; Merfeld et al. 1993
) that the otolith measurements of GIF are resolved into
neural estimates of gravity and linear acceleration that, when combined vectorially, approximately equal the otolith measurement of GIF (Fig.
1).
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Several previous studies support the idea that measurements of
ambiguous GIF are resolved into the hypothesized neural representations of gravity and linear acceleration. We measured both tilt (axis of eye
rotation) and translation (translational VOR) responses in squirrel
monkeys and, consistent with the hypothesis, determined that the
horizontal translational VOR decreased as the axis of eye rotation, our
indirect measure of tilt, increased (Merfeld and Young
1995). In the same study, we measured the horizontal VOR during
rapid roll tilts and showed the absence of significant horizontal eye
movements, even though there were substantial high-frequency inter-aural forces measured by the otolith organs. These results have
recently been confirmed in rhesus monkeys (Angelaki et al. 1999
) and substantially extended using combined translation and roll tilt. The responses to combined tilt/translation stimulation include appropriate horizontal translational VOR responses
(Angelaki et al. 1999
) even though the inter-aural force
measured by the otolith organs depended on the relative contribution of
gravitational cues. We have recently extended these findings, showing
that the nervous system uses identical mechanisms to elicit a
translational VOR even in the absence of translation when rotational
cues are available to tilt the neural representation of gravity away
from the graviceptor measurement of GIF (Merfeld et al.
1999
; Zupan et al. 2000
).
In the present study, we investigated tilt/translation processing using
centrifugation, known to provide an inertial cue that is interpreted as
tilt (e.g., Graybiel and Brown 1951). We measured subjective indications of roll tilt to provide a direct measure of
tilt. By combining fixed radius and variable radius centrifugation, we
investigated the question of how yaw rotational cues affect roll tilt estimation. Using identical motion paradigms with
the same set of subjects, we also measured VOR responses, including a
translational VOR component. We then compared these measures of tilt
and translation to investigate the hypothesis that measures of GIF are
resolved into neural representations of gravity and linear acceleration
(Fig. 1). This is the first study to combine perceptual measures of
tilt alongside measures of eye movements, allowing a direct comparison
of tilt and translation responses. Preliminary results have been
presented (Merfeld et al. 1997
, 1998
).
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METHODS |
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A total of 11 healthy subjects aged 21-46 (7 males and 4 females) with no history of peripheral or central vestibular disorders participated in one or more of the centrifugation trials described in the following text. The majority of these subjects were unaware of the specific scientific goals of these investigations. Clinical testing (including but not limited to a standard Barany chair rotation test, Hallpike maneuvers, computerized dynamic posturography, and caloric testing) was performed on most of these subjects (7 of 11). Only subjects without evidence of clinical abnormality were included in the subject pool. Five prospective subjects were removed from our subject pool by our conservative screening in which we were willing to discard some subjects who were probably normal to avoid potentially biasing our results with data from a subject having an undiagnosed clinical disorder. Subjects were instructed about potential risks, including motion sickness. Informed consent for each subject was obtained in accordance with institutional procedures.
Motion device and experimental protocols
All protocols were conducted on a short-arm human centrifuge. A race car seat was mounted on a platform that could translate relative to the rotational arm of the centrifuge. Subjects were restrained using a five-point seat-belt system, lateral shoulder supports, and foot restraints. Subjects' heads were secured using a modified motor cycle helmet (cut longitudinally into 2 pieces) that could apply very firm pressure to both sides of the head when the two pieces were brought together. The arm of the centrifuge was rotated by a DC motor that provided rotation of the centrifuge arm about an earth-vertical axis. The translation of the seat allowed independent control of the chair radius. The combination of independent rotation and translation motions allowed us to perform both "fixed radius" and "variable radius" centrifugation as described in detail in the following text.
Each test session consisted of up to four motion trials. At least two nights separated the individual test sessions. To minimize order effects, lights were turned on for 2 min before each trial while the subjects were upright and stationary. During the trials, subjects were instructed to keep their eyes open and to look straight ahead but not to focus on any point, real or imagined, and were challenged with a perceptual task. This task helped maintain subject alertness in addition to providing tilt data.
FIXED RADIUS TRIALS. Each test subject, with head upright, was seated at one of three radii from the center of rotation (0.54, 0.85, and 1.10 m). Subjects were accelerated in the clockwise (CW) or counter-clockwise (CCW) direction to a constant yaw angular velocity about an earth-vertical axis. (CW and CCW refer to the centrifuge rotation direction observed from above; a CW yaw rotation is toward the subject's right.) Each subject was accelerated to one of three constant angular velocities (250, 200, and 175°/s), which was maintained for 120 s, before a symmetric deceleration brought the subject to a stop. The three radii and three angular velocities were paired such that the steady-state centrifugal force was always roughly 1 G, yielding a GIF tilt of approximately 45°. Acceleration and deceleration phases of the angular velocity trapezoid were carried out over a period of 10 s for each of the three speeds, such that the time course of the centrifugal force was approximately the same for each of the three radii. Since the angular velocity linearly increased during acceleration and decreased during deceleration, the centrifugal force increased and decreased parabolically (i.e., as the square of the angular velocity since the centrifugal force equals the radius times the square of the angular velocity). All 11 subjects were tested in the 250°/s trials; 4 of these subjects (3 male, 1 female) were tested at each of the three speeds.
VARIABLE RADIUS TRIALS. Six of the 11 subjects (5 males, 1 female, aged 22-46) participated in variable radius trials. Subjects were seated at the center of the rotation and accelerated to a constant angular velocity of 250°/s in the dark. After waiting at least 5 min for rotation sensations and eye-movement responses to decay, the radius at which the subjects were seated was varied parabolically to yield the same parabolic centrifugal force profile that was present during the fixed radius trials. While the actual motion experienced during fixed radius and variable radius motion is clearly different, these paradigms present the same centrifugal force, as measured by the otolith organs, while presenting very different rotational cues, as measured by the semicircular canals. More specifically, large yaw rotational cues are present during fixed radius trials; no rotational cues are measured during variable radius trials since the semicircular canal cues have already decayed.
Eye-movement recording
Binocular eye movements were recorded in the dark using a commercial video system (Video Oculography by SMI). Infrared light-emitting diodes (LEDs) provided lighting for the video cameras. To maintain very stable images of the eyes, we modified the commercial camera mount system to include a small lightweight bitebar assembly to allow us to fix the cameras relative to the head. A mold of each subject's mouth was formed on the bite-bar using a dental impression compound (3M Express, 3M Dental Products, St. Paul, MN). The weight of the camera assembly was partially supported by the commercial (SMI) mask system, which was based on a modified scuba goggle.
An off-line analysis by the commercial software provided measurements of the horizontal and vertical coordinates of the pupil center for each field of the video image (59.94 video fields/s). The video system was calibrated by having the subject sequentially direct gaze at nine horizontal and seven vertical targets. Targets were separated by roughly 5°, providing a thorough calibration over ±20° for horizontal eye position and ±15° for vertical eye position. Eye position data (resolution better than 0.05°) were digitally filtered and differentiated to yield eye velocity. Fast phases were removed using a computer algorithm based on peak acceleration detection, with some editing by experienced personnel, leaving the slow phase eye velocity (SPV).
Perceptual tilt
All subjects were methodically trained in the psychophysical procedures described in the following text. They were first trained by making settings in the dark to the perceived horizontal while upright then during roll tilts about an axis through the center of the head. When comfortable with these tasks, they practiced making tilt settings on the centrifuge during fixed radius rotation before proceeding with this investigation. The subjects did not receive any feedback regarding their performance.
VISUAL TILT MEASURE.
During some trials, we measured subjective tilt using traditional
visual methods like those used by other investigators (e.g., Dai
et al. 1989). A visual bar, consisting of a dimly illuminated straight row of five LEDs set in a bar 10 cm long, was attached to the
chair 60 cm from the subjects eyes, subtending a 9.5° angle. It was
centrally placed at the subject's eye level so that the bar position
could be adjusted about its center, coplanar with the subject's
coronal plane. The bar could be rotated by a small motor, which was
controlled by means of two push buttons located near the subject's
hand. The bar could rotate clockwise or counterclockwise at a constant
velocity of 13°/s. Subjects made fine adjustments of bar orientation
by briefly tapping one of the two buttons. Having positioned the bar
with respect to their subjective horizontal, subjects indicated their
setting by pressing an "OK" button. A precision potentiometer
(0.5% linearity), co-axial with the shaft of the bar, provided an
accurate analog signal indicating bar orientation. Subjects were
instructed to "as quickly and accurately as possible set the bar so
that it appears to be horizontal." To help minimize any undue
influence of the previous setting, the LEDs turned off briefly
(approximately 0.5 s) after each setting. Furthermore the subjects
offset ("wiggled") the bar in both directions using the motor
command buttons before making the setting to minimize any undue
influence of the previous setting.
SOMATOSENSORY TILT MEASURE.
An alternate subjective tilt measure was also used. Subjects provided
indications of their perceived tilt using a "somatosensory" task
(Wade and Curthoys 1997), which requires subjects to set a handheld bar in alignment with the perceived horizontal. This task
complements the visual measure and has two main advantages: the
somatosensory settings are not contaminated by offsets due to torsional
eye movements, which could occur during centrifugation, and the task
can be performed while simultaneously recording reflexive eye movements.
DATA FITS.
To determine amplitude and time constants, a constrained nonlinear
optimization algorithm was used (const in Matlab 5.2 for Macintosh, The Mathworks). The tilt perception data were fit with an
analytical function P(t) = A[1 exp(
t/T)]. Similarly,
the per-rotatory horizontal slow phase eye velocity was fit with an analytical function E(t) = A
exp(
t/T). For both analytical functions, A is the amplitude and T the time constant of the
exponential fit.
STATISTICS. Statistical analyses were performed with Systat 7.0 (SPSS). Repeated measures ANOVA was used to determine the significance of steady-state tilt and time constants of tilt perception as a function of speed of rotation, rotation direction, and subject orientation. Similar procedures were used to analyze VOR peak velocities and time constants.
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RESULTS |
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Tilt psychophysics
FIXED RADIUS. During angular acceleration to an angular velocity of 250°/s at a radius of 0.54 m, the centrifugal force per unit mass increases from 0 G (at rest) to a steady-state value of approximately 1 G. For both facing-motion and back-to-motion orientations, the perception of tilt lags significantly behind the tilt of the gravito-inertial force measured by the otolith organs (and also measured by all other graviceptors) but then aligns with the tilted GIF roughly 30-50 s after the GIF tilt reaches its steady-state level of 45° (Fig. 2, A and C). Using a first-order exponential fit, we found that the average time constants were larger for facing-motion trials than for back-to-motion trials for both CW (28.1 > 14.6 s) and CCW (27.5 > 16.4 s) centrifugation; this orientation dependence was significant (P < 0.03). During deceleration, the centrifugal force decreases from 1 to 0 G (at rest). For both facing-motion and back-to-motion orientations, the perception of tilt remains better aligned with the tilt of the GIF during deceleration with little lag between perceived tilt and the actual tilt of the GIF (Fig. 2, B and D).
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VARIABLE RADIUS. To investigate the influence of rotational cues on the neural processing of gravito-inertial cues, we also performed variable radius centrifugation where we matched the centrifugal force of the fixed radius trials while eliminating dynamic cues from the canals. When the radius and force increased (Fig. 5, A and C), the subjective sensation of tilt changed substantially more rapidly during these variable radius trials, more closely aligning with actual tilt of GIF, than during the fixed radius trials (Fig. 4, A and C). This difference was statistically significant for both the visual (P < 0.002) and somatosensory measures (P < 0.03). Since the primary difference between the fixed radius and variable radius trials was the presence (fixed radius) or absence (variable radius) of a dynamic yaw rotational cue from the semicircular canals, the difference in the responses must be due to the sensory cues from the canals. Hence the yaw rotational cue from the canals must influence the neural processing of the ambiguous GIF roll tilt cues.
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Eye-movement responses
Having established that yaw canal cues influence roll tilt perception, we sought to investigate the influence of the yaw canal cues on eye movement responses using identical paradigms.
FIXED RADIUS HORIZONTAL VOR. The motion conditions were precisely matched to those used for the perceptual tilt investigation. A substantial horizontal VOR is evident during both acceleration and deceleration for both facing-motion and back-to-motion orientations (Fig. 6). This is expected since the response includes a robust angular VOR in response to the angular acceleration and deceleration along with any additional influence of the large inertial cues (i.e., centripetal acceleration) during centrifugation. It can also be noted that the facing-motion response during and following angular acceleration (Fig. 6A) is greater than the equivalent back-to-motion response (Fig. 6C). Using a first-order exponential fit to the per-rotatory eye movements, the absolute value of the peak horizontal eye velocity is greater for facing-motion than for back-to-motion for both CW (131.3 > 74.5°/s) and CCW (114.1 > 66.5°/s) centrifugation. This orientation effect on the peak response is statistically significant (P < 0.004). Similarly, the horizontal time constant is greater for facing-motion than for back-to-motion for both CW (11.6 > 8.3 s) and CCW (12.6 > 8.7 s) centrifugation. This orientation effect on the decay time constant is statistically significant (P < 0.004). At the same time, little or no difference exists between the facing-motion and back-to-motion responses during and following deceleration.
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VARIABLE RADIUS HORIZONTAL VOR. We also measured eye movements during the variable radius protocol (Fig. 7). Nearly symmetric horizontal responses can be observed in the facing-motion and back-to-motion orientations (Fig. 7). These responses included a brief transient component having a peak of nearly 5°/s followed by a smaller but long-lasting steady-state component of a few degrees per second. The direction of the horizontal VOR was consistent with a compensatory translational VOR caused by the centripetal acceleration toward the center of rotation. No consistent vertical VOR was observed during variable radius centrifugation (not shown).
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DIFFERENCE IN HORIZONTAL VOR DURING CENTRIFUGATION.
To emphasize and quantify how the horizontal responses depend on
subject orientation, the difference between the fixed radius facing-motion and back-to-motion responses during and following acceleration and deceleration was computed. This calculation acts to
eliminate the angular VOR since the angular response is identical for
both subject orientations. Earlier investigators (Merfeld and
Young 1995; Young 1967
) have suggested that the
difference between the facing-motion and back-to-motion responses
represents a translational VOR because this response component is in
the correct direction to compensate for the linear (centripetal)
acceleration experienced by the test subjects. A relatively large
difference (~25°/s) existed transiently between the facing-motion
and back-to-motion responses during and following acceleration (Fig.
8A), while only a very small
difference between the facing-motion and back-to-motion responses
existed during and following deceleration (Fig. 8B). A small
continuous horizontal response of a few degrees per second was
maintained in the dark throughout the 2-min period prior to deceleration. The steady-state response was also in the direction that
would compensate for linear acceleration toward the center of rotation
(i.e., centripetal acceleration). These findings are consistent with
previous findings in several species including humans (Lansberg
et al. 1965
), squirrel monkeys (Merfeld and Young 1995
), and one rhesus monkey (Wearne et al.
1999
), but inconsistent with the responses measured in
cynomolgus monkeys (Wearne et al. 1999
).
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DISCUSSION |
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Only two previous studies report both tilt and translation
responses (Merfeld and Young 1995; Merfeld et al.
1999
) using the same test subjects and motion protocols.
Several other studies report tilt responses alone (Hess and
Angelaki 1999
) or translational responses alone and infer what
must be occurring with tilt (e.g., Angelaki et al. 1999
;
Zupan et al. 2000
). Therefore the most important contribution of this study may derive from the comparison of tilt and
translation responses. In the following section, we first discuss tilt
psychophysics and then eye movements before proceeding with a
comparison of tilt and translation responses.
Tilt psychophysics
The time course of the perceived roll tilt was quite different in the fixed radius and variable radius experiments. This finding was independent of the measurement method. Since the principal difference between these experiments was the presence (fixed radius) or absence (variable radius) of dynamic cues from the semicircular canals, these tilt data show that yaw rotation cues from the semicircular canals influence perceived roll tilt. To our knowledge, this is the first study to clearly demonstrate the influence of the yaw semicircular canals on the perception of roll tilt.
It is worth noting another very small difference between fixed radius and variable radius stimulation. During the acceleration and deceleration phases of fixed radius rotation, a small tangential acceleration is aligned with the subject's naso-occipital axis. This acceleration is perpendicular to the centripetal acceleration aligned with the inter-aural axis and is very small, almost two orders of magnitude smaller than the centripetal acceleration. In contrast, during the radial movement of the variable radius trials, a small coriolis acceleration is present. This acceleration is similar in both direction and magnitude to the tangential force.
The influence of yaw rotation cues on the perception of roll tilt may
seem somewhat oblique. It is easier to imagine roll cues from the
semicircular canals influencing roll tilt since these coplanar cues
(roll rotation and roll tilt) are directly coupled mechanically; the
upright head cannot rotate in roll without tilting in roll. Several
studies have demonstrated direct influences of the semicircular canals
on the perception of tilt. For example, it was reported that
postrotational yaw cues from the canals following barbecue-spit
rotation yielded illusory yaw tilt (von Holst and Grisebach
1951). We have recently confirmed these measurements (Merfeld et al. 1999
) showing that yaw canal cues
influence the perception of yaw tilt following post rotational tilt
("dumping"). Others (Stockwell and Guedry 1970
) have
shown the influence of roll rotation cues from the semicircular canals
on perceived roll tilt using actual dynamic roll tilts. Our human
modeling work (Merfeld 1995a
; Merfeld and Zupan,
unpublished results) provides some clues why yaw rotation might
influence the perception of roll tilt. Roll tilt accompanied by yaw
rotation would normally yield a rotating gravitational stimulation,
like that experienced during off-vertical axis rotation (OVAR).
Therefore the illusion of steady roll tilt is not consistent with the
yaw rotational cue measured by the semicircular canals. In the
models, this conflict slows the time course of the illusory roll tilt
via the internal models since the conflict is not present if the
illusion of tilt is inhibited. Consistent with this prediction, the
measured tilt illusion builds up gradually with a time course not
unlike the decay of the angular response.
The perceptual roll tilt responses lagged well behind the tilt of GIF
during acceleration with little lag evident during deceleration. This
is consistent with earlier published studies using visual (Clark
and Graybiel 1951, 1963
, 1966
; Graybiel and Brown
1951
) and somatosensory (Curthoys 1996
)
measures. The results differ subtly from those reported by
Curthoys (1996)
because he showed that the time course
of perceived tilt was slightly slower when the subjects faced the
direction of motion than with their back toward the motion. We found no
significant asymmetry, but the perceptual tasks were slightly
different. Curthoys used a continuous task, whereas we used an
intermittent task, like the task that Curthoys later developed
(Wade and Curthoys 1997
). Another consideration is the
somewhat different motion profiles. Curthoys accelerated and
decelerated his subjects over a period of 20 s, twice the 10 second period we used. In any event, even if the time course of
perceived roll does depend subtly on subject orientation, this would
remain consistent with our primary psychophysical finding that yaw
rotational cues from the canals influence the time course of the
perception of roll tilt.
The results from the variable radius centrifuge trials appear
qualitatively consistent with the only other study of which we are
aware using similar stimuli (Seidman et al. 1998). This study utilized a variable radius centrifuge and moved the subject forward and backward yielding pitch tilt of the GIF as opposed to the
roll tilt stimulation we investigated. The time course of measured
pitch tilt was much slower than our roll tilt measurements. We do not
think that subject orientation (pitch vs. roll) explains this
difference. Our experience with a continuous somatosensory task in which the subjects did not offset the bar between successive tilt indications (like the continuous task used by Seidman and colleagues) showed very slow shifts in perceived tilt (Fig.
9). Since these indications of tilt were
much slower than the indications provided by the visual (Fig. 2) or
discrete somatosensory measure (Fig. 3), we think that the
continuous somatosensory task affected the time course of the measured
tilt, perhaps because past tilt indications influenced future
indications. To escape this difficulty, we developed and utilized the
intermittent task presented in this paper in which the subject had to
offset the bar before proceeding with their next setting. The average
time course measured using this intermittent task (Fig. 4) was similar
to that measured using the visual task, providing some validation of
each measure. Furthermore this intermittent task is identical to that
developed, tested, and validated by colleagues (Wade and
Curthoys 1997
).
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As shown in Fig. 5, the perception of tilt during variable radius
motion lags behind the tilt of GIF, even when there are no yaw rotation
cues from the semicircular canals. We agree with Seidman and
colleagues (1998), who suggested that this "difference is
probably attributed to the lack of coplanar canal stimulation that is
present during true tilt." Seidman and colleagues
(1998)
reported that the forward and backward tilt responses
were much more gradual during fixed radius rotation than during
variable radius rotation. Our data match this previous report. The
paper suggested that this might be because the "prolonged response
derived from the semicircular canals ... appears to mask or
overwhelm tilt perception." We disagree with this assessment because
this explanation appears to ignore modeling simulations that predicted
this influence of the canals on the time course of perceived tilt
(Merfeld 1995a
) and, more importantly, also ignores the
influence of the canals on tilt processing (Hess and Angelaki
1999
; Merfeld et al. 1999
; Stockwell and
Guedry 1970
; von Holst and Grisebach 1951
). In
our studies, we found no evidence to support the hypothesis that the canals mask or overwhelm the perception of tilt. Instead, as discussed previously, it appears that the yaw rotational cues act to slow the
development of the tilt illusion through the sensory integration processes described previously not via masking or confusion.
It is interesting to note that perceived tilt returned to upright
(0°) a little more rapidly when the centrifugal force was removed by
returning to the center of rotation than the perceived tilt built up
when the centrifugal force was applied by increasing the radius
(Fig. 5). This suggests that other influences on tilt perception may
also be relevant. Specifically, these data are consistent with
Mittelstaedt's idiotropic vector (Mittelstaedt 1986),
the idea that perception of tilt may have some tendency to remain
aligned with the body. Hence the perceived tilt moves toward alignment
with the body more rapidly than it tilts away from alignment from the
body. Other explanations, such as that the addition of tactile cues
when the radius increases is different from the removal of tactile cues
when the radius decreases, may also be relevant but are not addressed
by our study.
Eye movements
We showed that the horizontal VOR was much larger when the
subjects faced the motion than with their backs to the motion. Previous
publications (Merfeld 1995a,b
; Merfeld and Young
1995
; Young 1967
) have suggested that the
facing-motion versus back-to-motion differences can be explained by the
presence of a translational VOR that augments the angular VOR when the
subject is facing the motion and deducts when the subject is oriented
with back-to-motion. Consider that the angular VOR for a CW rotation is
a horizontal response with slow phase to the left. The centripetal
acceleration during centrifugation always points toward the center of
rotation. For CW rotation while facing-motion, the centripetal linear
acceleration is toward the subject's right. Therefore the compensatory
translational VOR would be a horizontal VOR with slow phases to the
left, augmenting the angular VOR. For CW rotation with back to motion,
the centripetal linear acceleration is toward the subject's left.
Therefore the compensatory translational response should be a
horizontal VOR with slow phases to the right, decrementing from the
angular VOR response. For CCW rotation, the direction of the angular
VOR reverses as does the predicted translational response. Since both
angular and translational VOR components reverse, the expected
compensatory response to the centripetal acceleration still augments
the magnitude of the angular VOR while facing-motion and decrements
from the magnitude of the angular VOR for back-to-motion. When this
explanation was first presented (Young 1967
), the
existence of a translational VOR was not widely accepted. Since it is
now widely known that inter-aural linear accelerations elicit reflexive
horizontal eye movements (Paige and Tomko 1991
;
Schwarz and Miles 1991
; Schwarz et al.
1989
), this explanation has added cogency.
To calculate the putative translational VOR, we took the
difference between the facing-motion response and the back-to-motion response (and divided by 2). It is important to note that this difference calculation is an approximation. For simplicity, we assume
that the angular VOR and translational VOR sum linearly but recognize
that the nervous system includes nonlinearities and processes of
sensory integration (e.g., Merfeld 1990, 1995b
; Merfeld et al. 1993
). Nonetheless the linear
approximation is justified by previous experiments that specifically
considered how the translational and angular VOR responses combined
(Sargent and Paige 1991
). This calculation is further
justified by the fact that the canal cue is identical in both orientations.
The amplitude of the putative translational VOR component, having a
peak of roughly 25°/s per G, is consistent with other human data
showing responses to inter-aural acceleration having a sensitivity of
between 15 and 30°/s per G in the dark (Baloh et al.
1988; Buizza et al. 1980
; Niven et al.
1966
; Shelhamer and Young 1994
). The response we
report does not have the high-frequency characteristics that are
observed during pure translational stimulation. For example, the
response has a time constant of roughly 12 s (determined with an
exponential fit to the response), which would be equivalent to a
high-pass filter with a cutoff frequency of 0.0133 Hz
[F = 1/(2
T)]. This cutoff frequency is
well below the translational VOR cutoff frequency measured during
purely translational stimuli. Furthermore the decay of the response
during deceleration is significantly different from that during
acceleration. This is inconsistent with simple filtering.
At first, these characteristics may appear to weigh against it being a
compensatory response to linear acceleration (i.e., a translational
VOR). However, the high-pass filtering characteristics are not an
inherent VOR characteristic because numerous studies (e.g.,
Angelaki et al. 1999; Merfeld and Young
1995
; von Holst and Grisebach 1951
; Zupan
et al. 2000
) have shown that the semicircular canals influence
the interpretation of GIF for both perceptual and eye movement
responses. Furthermore, modeling work (Merfeld 1995a
) also predicted
this translational VOR in humans.
The facing-motion versus back-to-motion asymmetry in the horizontal
response that we observed (Figs. 6 and 8) is consistent with previous
measurements in humans (Lansberg et al. 1965), squirrel monkeys (Merfeld and Young 1995
), and one rhesus monkey
(Wearne et al. 1999
) but inconsistent with the responses
reported in cynomolgus monkeys (Wearne et al. 1999
). We
cannot explain the cause of this species dependence, but it seems
reasonable to consider that previous testing experience could lead to
different responses in the different species. However, to the best of
our knowledge this hypothesis has not been directly investigated for
canal-otolith interactions. Wearne and colleagues suggested that the
observed facing-motion versus back-to-motion difference in cynomolgus
monkey responses was caused by the presence of vertical nystagmus. They
indicated that the tilted GIF induced a shift in the axis of eye
rotation that included a vertical component in addition to the
horizontal angular VOR. Since the upward VOR has a different time
constant in cynomolgus monkeys than the downward VOR, they suggested
that the vertical response couples back into the horizontal response and affects the amplitude and time constant of the horizontal VOR.
This explanation is inconsistent with the fact that the horizontal VOR
is greater when facing-motion than with back-to-motion in man, squirrel
monkeys, and one rhesus monkey because any vertical coupling would lead
to the opposite asymmetry. Furthermore, it is worth noting that
the vertical responses measured during centrifugation (not shown due to
space limitations) were very small in our human subjects, consistent
with earlier human studies using centrifugation (Haslwanter et
al. 1996) and postrotational tilt (Fetter 1996
; Fetter et al. 1992
). Furthermore, the presence of an
up/down asymmetry in humans, like that reported for some other nonhuman
primates, is questionable. Some human studies report an optokinetic
vertical asymmetry (Murasugi and Howard 1989
; Wei
et al. 1994
) while others report no optokinetic asymmetry or an
asymmetry in only a minority of subjects (Baloh et al.
1986
). No consistent vertical VOR asymmetry has been reported
in humans (Allum et al. 1988
; Baloh and Demer 1991
; Baloh et al. 1983
). Given all of these
human data, it seems reasonable to conclude that any coupling of the
vertical responses to the horizontal responses, as suggested by Wearne
and colleagues for cynomolgus monkeys, is unlikely to influence human responses.
Tilt/translationcomparison of tilt perception and
eye-movement responses
Figures 2-4 show that during fixed radius centrifugation there is a substantial difference between the GIF tilt and the subjective tilt during acceleration with little or no difference during deceleration. The GIF resolution hypothesis (Fig. 1) suggests that a substantial horizontal translational VOR should exist whenever there is a substantial difference between the measured GIF and the neural representation of tilt. Combining this hypothesis with the measurements of tilt, the hypothesis predicts that a substantial horizontal translational VOR component should be observed during and following acceleration with little or no translational VOR during deceleration. This prediction matches the horizontal translational VOR components shown in Fig. 8, A and B. Furthermore the GIF resolution hypothesis predicts that the horizontal VOR component should decay to a steady-state level with a time course that approximately matches the time course with which the subjective tilt reaches its steady-state value. This prediction was also confirmed by our data.
During variable radius centrifugation, we measured a smaller lag between the tilt of the GIF and the perceived tilt when the subject moved out along the radial arm than during fixed radius centrifugation. Little or no lag was evident as the subject returned to the center. Therefore there was only a small difference between the GIF tilt and subjective tilt as the subject moved outward and little or no difference when the subject moved back to the center. Given these tilt results, the GIF resolution hypothesis predicts that a small horizontal translational VOR component should be measured as the subjects moved radially outward and that little or no horizontal translational VOR should be measured as the subjects moved back to the center. This prediction matches the horizontal translational VOR component shown in Fig. 8, C and D.
Multi-sensory integration
Several earlier studies have shown that rotational cues influence
the neural processing of otolith cues (Dichgans et al.
1972; Stockwell and Guedry 1970
; von
Holst and Grisebach 1951
). Similar multisensory influences were
recognized and discussed by Young (1984)
and
Guedry (1974)
. Even Mayne (1974)
, who
included simple low- and high-pass filtering of GIF cues in his model,
recognized the influence of canal cues on the interpretation of
ambiguous GIF cues and also included a simple nongeneralized influence
of the canals on the processing of otolith cues. Following these and
other investigations (Hein and Held 1961
; Held
1961
; Oman 1982
; Sperry 1950
;
von Uexkull 1926
), we hypothesized that the nervous
system uses internal
models2
to process GIF and other sensory cues
(Merfeld 1990
, 1995b
; Merfeld et al.
1993
). Like earlier models (e.g., Hain 1986
;
Raphan and Sturm 1991
), our model included the influence
of gravitational cues on the angular responses (e.g., "dumping" and
"axis-shifts") but extended the earlier models by including the
influence of rotational cues on tilt and translation responses. Our
internal model hypothesis explicitly included neural representations of the influence of the semicircular canals on the estimated orientation of gravity, the fact that otolith measurements of GIF are resolved into
estimates of gravity and linear acceleration that when combined approximately equal the otolith measured GIF, and the dynamics of the
sensory systems including the semicircular canals. These hypotheses
were tested experimentally using rapid roll tilts and centrifugation.
Consistent with the internal model hypothesis, we found little or no
horizontal response following rapid roll tilts that included
high-frequency stimulation (Merfeld and Young 1995
). The
centrifugation studies (Merfeld and Young 1995
) also showed a difference in the horizontal VOR of squirrel monkeys during
acceleration with little or no difference during deceleration. We
calculated this difference and suggested that it might indicate the
presence of a translational VOR. Using the axis of eye rotation as an
indirect measure of estimated tilt, we showed that the putative translational VOR decayed to zero with a time course matching the time
course of the estimated tilt of the squirrel monkey. These findings,
while somewhat indirect, matched the predictions of our hypothesis
(Fig. 1) as well as model predictions (Merfeld 1995b
).
These findings are confirmed and extended by the findings of this human
centrifugation study.
More recently, these hypotheses and experimental findings have been
confirmed and extended using completely different motion paradigms.
Hess and Angelaki (1999) performed a thorough analysis of eye-movement data acquired during translation and off vertical axis
rotations. Using Listing's law as an indirect tilt measure, similar to
the indirect axis shift measure that we used during our monkey
centrifugation studies, the authors concluded that the nervous system
distinguishes gravity from linear acceleration. At about the same time,
Angelaki and colleagues (1999)
published a study in
which they used sinusoidal tilt alone, sinusoidal translation alone,
and combined sinusoidal tilt and translation to show that canal cues
help the nervous system separate tilt from translation. The study
showed that rhesus monkeys are able to respond to translational motion
even when combined with tilt stimulation. To explain these findings,
the authors hypothesized neural processes that exactly matched portions
of our hypothesized internal model (Merfeld 1990
, 1995b
;
Merfeld et al. 1993
). At almost the same time, we
measured horizontal VOR responses following postrotational tilt in
eight different orientations (Merfeld et al. 1999
;
Zupan et al. 2000
). The results showed that when
contradictory cues are provided by the semicircular canals and otolith
organs, humans elicit a translational VOR even in the absence of true
linear acceleration. This is also consistent with the hypothesis that
the nervous system uses internal models to separate measures of GIF
into neural estimates of gravity and linear acceleration (Fig. 1).
Conclusion
By combining quantitative perceptual and eye movement recordings in the same set of subjects using identical motion paradigms, the present human centrifugation studies show how cues from different sensory systems (i.e., semicircular canals) influence the interpretation of cues from other sensory systems (i.e., otolith organs). As discussed in detail in the preceding text, the data are consistent with the hypothesis that rotational cues from the semicircular canals influence the processing of ambiguous GIF cues and the hypothesis that the nervous system separates measured GIF into neural estimates of gravity and linear acceleration that combine vectorially to approximately equal the measured GIF (Fig. 1). More generally because both of these hypotheses are internal model components, this study appears to add further support to the hypothesis that the nervous system uses internal models to process and integrate sensory motor cues to estimate and control motion.
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ACKNOWLEDGMENTS |
---|
We thank Dr. F. Owen Black for assistance throughout this project, T. Bennett for operational help as well as for assistance completing the construction of the centrifuge and related equipment, and R. Lewis for comments on an early draft of the manuscript. We also thank P. Cunningham, S. Pesznecker, V. Stallings, and S. Wade for assistance.
This work was supported by National Institute on Deafness and Other Communication Disorders Grant DC-03066 and also in part by a grant from the European Space Agency External Fellowship Program (L. H. Zupan).
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FOOTNOTES |
---|
Address for reprint requests: D. M. Merfeld, Jenks Vestibular Physiology Laboratory, Suite 421, Massachusetts Eye and Ear Infirmary, 243 Charles St., Boston, MA 02114 (E-mail: dan_merfeld{at}meei.harvard.edu).
1
GIF per unit mass (f) is
gravitational force per unit mass (g) plus the inertial
force per unit mass (fa) due to linear
acceleration (a), f = g + fa. The inertial force per unit mass due to
linear acceleration is equal and opposite the linear acceleration
(fa = a), so f = g + (
a) or f = g
- a. We use the notation, f = g
- a, throughout. We will also use the term graviceptor
throughout to refer to any and all sensory systems that measure GIF.
The otolith organs are one example.
2
We define internal models as neural systems that mimic
physical principles associated with sensory transduction and/or body movement in some relevant way. To allow experimental investigation, we
use an even more conservative definition, limiting internal models to
those neural systems that mimic physical principles that we can
unambiguously represent mathematically (e.g., f = g a, Fig. 1). This conservative
definition makes it possible to validate or reject a hypothesized
internal model objectively.
Received 31 July 2000; accepted in final form 29 November 2000.
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REFERENCES |
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