Exp Brain Res (1998) 120:450460
RESEARCH ARTICLE
T. Mergner G. Schweigart F. Botti A. Lehmann
Eye movements evoked by proprioceptive stimulation
along the body axis in humans
Received: 10 October 1997 / Accepted: 22 January 1998
Abstract Proprioceptive input arising from torsional
body movements elicits small reflexive eye movements.
The functional relevance of these eye movements is still
unknown so far. We evaluated their slow components as
a function of stimulus frequency and velocity. The hori-
zontal eye movements of seven adult subjects were re-
corded using an infrared device, while horizontal rota-
tions were applied at three segmental levels of the body
[i.e., between head and shoulders (neck stimulus), shoul-
ders and pelvis (trunk stimulus), and pelvis and feet (leg
stimulus)]. The following results were obtained: (1) Sinu-
soidal leg stimulation evoked an eye response with the
slow component in the direction of the movement of the
feet, while the response to trunk and neck stimulation
was oriented in the opposite direction (i.e., in that of the
head). (2) In contrast, the gain behavior of all three re-
sponses was similar, with very low gain at mid- to high
frequencies (tested up to 0.4 Hz) but increasing gain at
low frequencies (down to 0.0125 Hz). We show that this
gain behavior is mainly due to a gain nonlinearity for low
angular velocities. (3) The responses were compatible
with linear summation when an interaction series was
tested in which the leg stimulus was combined with a ves-
tibular stimulus. (4) There was good correspondence of
the median gain curves when eye responses were com-
pared with psychophysical responses (perceived body ro-
tation in space; additionally recorded in the interaction se-
ries). However, correlation of gain values on a single-trial
basis was poor. (5) During transient neck stimulation
(smoothed position ramp), the neck response noticeably
consisted of two components an initial head-directed
eye shift (phasic component) followed by a shift in the
opposite direction (compensatory tonic component). Both
leg and neck responses can be described by one simple,
dynamic model. In the model the proprioceptive input is
fed into the gaze network via two pathways which differ
in their dynamics and directional sign. The model simu-
)
T. Mergner ( ) G. Schweigart F. Botti A. Lehmann
Neurologische Klinik, Neurozentrum, Universitt Freiburg,
Breisacher Str. 64, D-79106 Freiburg, Germany
e-mail: mergner@sun1.ruf.uni-freiburg.de, Fax: +49-761-270-5310
 Springer-Verlag 1998
lates either leg or neck responses by selecting an appro-
priate weight for the gain of one of the pathways (phasic
component). The interaction results can also be simulated
when a vestibular path is added. This model has similar-
ities to one we recently proposed for human self-motion
perception and postural control. A major difference,
though, is that the proprioceptive input to the gaze-stabi-
lizing network is weak (restricted to low velocities), un-
like that used for perception and postural control. We hold
that the former undergoes involution during ontogenesis,
as subjects depend on the functionally more appropriate
vestibulo-ocular reflex. Yet, the weak proprioceptive
eye responses that remain may have some functional rel-
evance. Their tonic component tends to stabilize the eyes
by slowly shifting them toward the primary head position
relative to the body support. This applies solely to the
earth-horizontal plane in which the vestibular signal has
no static sensitivity.
Key words Proprioceptive eye response
Vestibulo-ocular reflex Cervico-ocular reflex
Interaction Self-motion perception Human
Introduction
It has been known since the beginning of this century that
stimulation of neck afferents by torsion of the head rela-
tive to the trunk elicits a cervico-ocular reflex (COR;
Brny 1906, 1918/1919; Frenzel 1930). The reflex con-
sists of slow (smooth) and fast (saccadic) components;
the present study focuses solely on the slow component
of this reflex. In the neonate human, the COR slow com-
ponent is prominent and directed counter to the head ex-
cursion (Brny 1918/1919; Reisman and Anderson
1989). This direction of the COR may augment the vestib-
ulo-ocular reflex (VOR) during head rotation on the sta-
tionary trunk (compensatory COR). In contrast, COR
magnitude in the intact adult is small and, according to
many previous studies, is oriented in the direction of the
head excursion (anticompensatory COR; Takemori

and Suzuki 1971; Barnes and Forbat 1979; Bronstein and
Hood 1986; Jrgens and Mergner 1989). If the VOR is se-
verely impaired in adults then the COR shows an increase
in gain (G) and the direction becomes compensatory (for
older literature, see Biemond and de Jong 1969; also
Gresty et al. 1977; Kasai and Zee 1978; Barnes 1979;
Leopold et al. 1983; Bles et al. 1984; Bronstein and Hood
1986; Huygen et al. 1991). This compensatory COR helps
to stabilize gaze during eye-head gaze shifts (Dichgans et
al. 1973; Kasai and Zee 1978; Takahashi et al. 1981,
1989). Interestingly, the modification of the COR is re-
versible after recovery of vestibular functions (Bronstein
et al. 1995). The findings in higher mammals correspond
to those in humans (see Fuller 1980; Peterson 1988). De-
spite a considerable amount of work, several questions
concerning the COR are still unresolved.
For instance, it is still unclear whether the weak, anti-
compensatory COR in intact adults has a relevant func-
tional role for the stabilization of gaze. Previously, Meiry
(1971) has suggested that the COR supports the VOR dur-
ing horizontal rotations in the range of low stimulus fre-
quencies where the VOR shows nonideal (high-pass)
transfer characteristics (Fernandez and Goldberg 1971).
Consistent with Meirys suggestion, relevant values of
COR gain occur only in the low-frequency range (Barlow
and Freedman 1980; Bronstein and Hood 1986; Jrgens
and Mergner 1989; Huygen et al. 1991). However, as
mentioned above, the direction of COR (slow phase) in
the intact adult is anticompensatory and therefore would
attenuate rather than augment the VOR during head rota-
tion. Consequently, most researchers in the oculomotor
field consider the COR a relic from ontogenesis but con-
cede that it is a useful dormant, stand-by mechanism in
case of VOR loss.
Furthermore, there are inconsistencies concerning pre-
vious reports on the gain behavior of the COR. While
some authors noted that its gain is highest at low frequen-
cies (Bronstein and Hood 1986; Huygen et al. 1991), oth-
ers reported that it is highest at low angular velocities
(Doerr et al. 1981; selected patients with cervical syn-
dromes, Holtmann et al. 1989). A quantitative comparison
between frequency and velocity-dependent response be-
havior across a broad range of stimulus parameters is still
missing.
Another point is that head turns do not arise only from
torsional movements at the level of the neck, but also be-
tween lower body segments, i.e., at the level of the thorac-
ic and lumbar spinal column or the legs. The latter stimuli
also elicit reflexive eye movements. This has been shown
with rotations of the lower trunk (Grahe 1926; Warabi
1978) or the legs (Botti et al. 1995; active stepping, Bles
et al. 1984; Lackner and DiZio 1984) relative to the sta-
tionary (space-fixed) upper body. Noticeably, rotation of
the arms in the shoulder joints may also elicit a nystagmus
(Brandt et al. 1977). However, the overall picture which
emerges from these studies is by no means consistent.
The direction of the leg response is compensatory, in
the sense that it would be functionally synergistic with
the VOR during a head turn relative to the stationary feet
451
(Botti et al. 1995), while that of the trunk response is ori-
ented in the opposite direction (Warabi 1978), as is the
COR.
Finally, similarities exist between the COR and the
neck contribution to self-motion perception. As men-
tioned above, a COR of relevant gain occurs at low fre-
quencies. The neck contribution to the perception of head
motion in space also shows a relevant magnitude only at
low frequencies (Mergner et al. 1991). One would like to
know, therefore, whether the two phenomena are related
to each other. However, there also exist clear differences;
while the direction of the eye responses evoked at neck or
trunk differs from that at the level of the leg, the proprio-
ceptive effects on self-motion perception are similar
across these segmental levels (see Mergner et al. 1997).
It would be desireable to have formal descriptions of
the two phenomena, since this would ease their compari-
son. There exists a dynamic model for self-motion per-
ception (Mergner et al. 1991). However, a comparable
model for COR is still missing so far.
In the present study we reevaluate the proprioceptive
eye responses in human subjects under the following four
conditions: (1) Firstly, the proprioceptive responses
evoked by stimuli at different segmental levels, i.e., at
the neck, the thoracic-lumbar spinal column and the legs
were directly compared. (2) Secondly, we attempted to
provide a quantitative comparison between frequency
and velocity-dependent response behavior. (3) Further-
more, we investigated the relationship between proprio-
ceptive eye responses and self-motion perception. (4) Fi-
nally, based on our experimental findings, we developed
a conceptual model of how we think proprioceptive input
is fed into the gaze-stabilization network, and we com-
pared this with our previous model for human self-mo-
tion perception. Part of the work on leg-evoked eye
movements was published in a preliminary report (Botti
et al. 1995).
Materials and methods
Subjects, apparatus and stimuli
Seven healthy human subjects (2445 years of age; four men and
three women) with no history of any neurological or vestibular dis-
order were studied. All subjects gave their informed consent to par-
ticipate in the experiments.
Figure 1A shows the experimental setup in schematic form. Sub-
jects were seated on a Brny chair for horizontal body rotation.
Their heads were fixed (15 nose-down) to a chair-mounted head-ro-
tation device by means of a dental bite board and a bitemporal head
clamp. The device allowed relative rotation between head and trunk.
This rotation device also could be used to rotate the subjects shoul-
der girdle relative to pelvic girdle by adding a further clamp which
fixed the shoulder girdle to the head-holder system. Finally, the sub-
jects feet rested on a motor-driven sled that allowed the feet to ro-
tate relative to the pelvic girdle (circumferential path, radius 0.5 m).
All axes of rotation were vertical and passed through the crossing
point of the interaural and naso-occipital lines. Rotations were gen-
erated by position-controlled servo-motors under the control of a
laboratory computer.
The following four stimuli were generated (Fig. 1B): (a) En bloc
rotation of the whole body generated the vestibular stimulus
452
(VEST); (b) en bloc rotation of shoulders, pelvis, and feet relative
to the stationary head generated the neck proprioceptive stimulus
(NECK); (c) rotation of the pelvis and feet relative to the stationary
shoulders and head served as the trunk proprioceptive stimulus
(TRUNK; torsion about the spinal column mainly at lower thoracic
levels); (d) rotation of the feet relative to the stationary pelvis,
shoulders, and head served as the leg proprioceptive stimulus
(LEG; the stimulus mainly arises from the hip joints; see Mergner
et al. 1993). Combinations of these stimuli were also used as spec-
ified below.
The stimuli usually had a sinusoidal waveform. The following
frequencies were used: 0.0125, 0.025, 0.05, 0.1, 0.2, and 0.4 Hz.
In some experiments (frequency series), peak angular displace-
ment was kept constant (at 8), and peak angular velocity, vmax, co-
varied with frequency (vmax=0.63, 1.25, 2.5, 5, 10, and 20/s, respec-
tively). In other experiments (velocity series), frequency was kept
constant at 0.05 Hz or 0.2 Hz, while peak velocity was varied
(vmax=0.3, 0.63, 1.25, 2.5, 5, 10/s at 0.05 Hz, and 1.25, 2.5, 5,
10, 20, 40/s at 0.2 Hz), with peak displacement varying correspond-
ingly (1, 2, 4, 8, 16, and 32).
Considering the possibility that subjects heads might perform
small movements in space during the proprioceptive stimuli (thus
possibly giving rise to a VOR), we repeatedly controlled for head Fig. 1A, B Schematic presentation of the experimental setup (A)
stationarity. To this end, a small laser pointer was attached to each and the stimuli used (B). The setup allowed the application of
subjects head which projected a light spot outside of their visual whole-body rotation (a vestibular stimulation, VEST combined chair
fields onto a screen surrounding the chair (radius 0.9 m). Visual in- and foot rotation), of the body under the stationary head (b neck pro-
spection by an experimenter revealed that, during a NECK stimulus prioceptive stimulation, NECK combined chair and foot rotation and
of 8 at 0.1 Hz for instance, the head could slightly move in space. a head-on-trunk rotation of same magnitude, but opposite direction),
However, this movement never exceeded 0.4. Head-in-space of the lower body compared with the upper one (c trunk stimulus,
movements could no longer be detected when stimulus amplitude TRUNK same as NECK, but the shoulders were also fixed to the
was reduced below 4. Comparing these observations with mea- head-holder system), and of the feet compared with the body (d
surements of the VOR during whole-body rotations and with the leg proprioceptive stimulus, LEG rotation of foot sled about the
proprioceptive eye responses (see Results), we concluded that any chair)
contamination by a VOR stemming from imperfect head-in-space
stability was negligible.
In an interaction series we combined sinusoidal LEG and
jects fixated a red light spot (diameter 0.5 of visual angle) that was
VEST. The stimuli were in counter-phase with respect to each other
stationary in space, at a distance of 0.9 m, while they were sinuso-
(Dj=180, denoted in the following by a negative sign, e.g.,
idally rotated (VEST; f=0.1 Hz, A=8). The best three of ten trials
VEST=8, LEG=8). Psychophysical data were also obtained in
were selected and the mean compound eye response (eye-in-head
this series. Subjects indicated perceived body rotation in space with
position, EH) was taken as unity gain. The eyes were located slightly
the help of a pointer, using the same procedure as in a previous study
in front of the chair rotation axis, making the eye-in-head rotation
(Mergner et al. 1993). In short, subjects tried to maintain the chair-
angle somewhat larger than 8 (8.8); the results presented below
mounted pointer in a constant direction in space. Thus, pointer ex-
were corrected for this small error.
cursion relative to the chair, as measured with a high-precision po-
The horizontal and vertical eye-position signals, the horizontal
tentiometer, reflected the reverse of perceived body rotation in
eye-velocity signal, and the position signals of the chair, foot sled,
space. After sign reversal of the potentiometer output and correc-
and head-shoulder rotation device were fed into a computer at a
tions for operator performance (manual ability to perform the indi-
sampling rate of 100 Hz. The analysis was performed off-line.
cation; see Mergner et al. 1991), the signal was taken as a measure
The slow component of the horizontal EH signal was separated from
of perceived body-in-space rotation. Examples of the sign-reversed
the compound response under visual inspection (see Fig. 2, EH
indication signal are given in Fig. 2A, B for VEST and LEG, respec-
slow) using an interactive computer program that detected saccades
tively (note that LEG evoked a small illusion of body rotation in
of more than 0.2. The gaps in the slow EH trace were filled using a
space counter to the foot-sled rotation).
procedure that averaged eye velocity immediately before and after
In a position ramp series a smoothed position ramp was used
the saccade. The eye responses evoked by sinusoidal stimulation
as a neck stimulus to the right or left side. It started from the primary
were analyzed, after the usual drift correction, in terms of gain
body position with velocity v showing a cosine bell trajectory
and phase using the fundamental waves of a fast Fourier transforma-
which contained a single-frequency cosine [v=Afcos(2pft)+Af;
tion (FFT; gain, magnitude ratio of response to stimulus fundamen-
frequency, f=0.05 Hz; displacement, A=8; t, time; vmax=0.8/s].
tals; phase, phase difference between fundamentals, in degrees). In
The experiments were performed in darkness and subjects ears
the amplitude series, which contained stimuli of very small ampli-
were plugged in order to reduce auditory cues. Subjects performed
tude, slow EH responses were averaged prior to the FFT (six original
preinstructed mental arithmetic in order to maintain a high level
responses per subject); this data is presented as across-subjects mean
of vigilance throughout the experimental sessions (the only excep-
values. In all other series, which consisted of stimuli of more than
tion being the interaction series, where subjects performed a psycho-
4, single cycles of the sinusoidal stimulation were analyzed and
physical task).
the median gain and phase values were evaluated (n=2, 2, 4, 4,
and 8 for stimuli with f=0.025, 0.05, 0.1, 0.2, and 0.4 Hz, respective-
ly).
Eye-movement measurement and analysis The cosine-bell velocity stimulus profile was used only with
NECK. The responses evoked were generally very weak and were
Subjects horizontal and vertical eye movements were recorded us- partially masked by spontaneous eye drifts. Averaging across all
ing an infrared technique (IRIS, Skalar). The recording of the verti- subjects was performed separately for NECK in either direction
cal movements served to detect eye blinks and allowed us to exclude (seven subjects, 12 responses each), after individual responses were
considerable vertical response components arising with the horizon- submitted to a drift correction (based on an extrapolation of the pre-
tal rotations. For calibration of the horizontal eye recording, the sub- stimulus eye velocity).

Fig. 2A, B Examples of original recordings obtained with vestib-
ular stimulation (A VEST) and leg stimulation (B LEG). Position
traces of turntable, foot sled, pointer indication of perceived body
rotation in space, eye in head (EH), and slow component of EH.
Note that in B an EH response is missing for the first cycle of
leg stimulation
Results
Frequency series
Vestibular stimulation
VOR was recorded in all subjects to test the integrity of
their vestibular system. The obtained data also served as
comparisons with the proprioceptive eye responses. An
example of an original VOR recording from one subject
is shown in Fig. 2A. All subjects median gain and phase
values (and the 95% confidence intervals of the medians)
are given in Fig. 3A. They show the typical VOR behav-
ior known for sinusoidal stimulation in the dark; the gain
is clearly below unity at high frequency and is further at-
tenuated at low frequencies, where the phase develops
some lead with respect to ideal compensation
(Dj=180 re head position in space). Note that the rather
low gain of the VOR is an artifact known to occur with
periodic (here sinusoidal) stimulation (e.g., Gauthier and
Vercher 1990).
Leg stimulation
Rotation of subjects feet with head, shoulders, and pelvis
stationary elicited a small eye response (representative
example in Fig. 2B). Median gain was small in the mid-
to high-frequency range, but increased considerably when
stimulus frequency was decreased (Fig. 3B). The direc-
tion of the LEG response was approximately compensato-
ry (i.e., counter to the head rotation relative to the feet).
Median phase slightly lagged exact compensation (180)
by about 18, on average.
453
Trunk stimulation
Rotation of the subjects pelvis and feet under the station-
ary head and shoulder yielded a weak response (G<0.2) at
high frequency, which increased at low frequency
(G=0.43 at 0.0125 Hz; Fig. 3C). The response was anti-
compensatory (i.e., approximately in phase with head ex-
cursion relative to lower trunk and feet), the phase re-
maining essentially constant across frequencies.
Neck stimulation
Median gain and phase values of our subjects COR are
given in Fig. 3D. Gain was very low at high frequencies
but increased at low frequencies (G=0.41 at 0.0125 Hz).
The response was approximately anticompensatory at
high frequencies (i.e., in phase with head excursion),
but showed a clear phase lead at low frequencies.
Note from Fig. 3AD that the gain of the propriocep-
tive responses showed considerable variability between
subjects (large confidence intervals), which was compara-
ble with that of the VOR. In contrast, phase variability
was considerably smaller for the VOR than for the pro-
prioceptive responses (exception, VOR at 0.025 Hz). No-
ticeably, variations in the phase of proprioceptive re-
sponses were smallest at high frequency, despite very
low gain, and increased considerably at lower frequen-
cies, when the gain was higher.
Velocity series
In the frequency series described above, peak angular
displacement was kept constant (8), while peak veloc-
ity covaried with frequency (see Materials and Methods).
Thus, the observed changes of the proprioceptive re-
sponses with frequency (Fig. 3BD) might actually re-
flect a dependency on stimulus velocity rather than fre-
quency. To test this possibility, we performed an addi-
tional experimental series for both NECK and LEG, in
which frequency was kept constant and peak velocity
was varied.
Leg stimulation
Figure 3 E shows the data for both 0.05 Hz and 0.2 Hz
(mean gain and phase values only; see Materials and
methods). The curves for 0.05 Hz and 0.2 Hz show sim-
ilar increases in gain with decreasing velocity. The curves
are also similar to the data of the previous frequency se-
ries (replotted from Fig. 3B as a function of peak veloci-
ty). The phase curve for 0.05 Hz lags the exact counter-
phase of head displacement relative to the feet by a sim-
ilar amount, as was seen in the frequency series at 0.05 Hz.
No mean phase values were evaluated for the 0.2-Hz
stimuli, because they were rather unreliable with the
low amplitudes of the stimuli.
454
Fig. 3AF Results of frequency series (AD) and velocity series (E,
F). Gain and phase values of eye responses obtained with sinusoidal
horizontal rotations are plotted as a function of stimulus frequency
and peak stimulus velocity, respectively (AD interconnected medi-
an values and their 95% confidence intervals; E, F mean values).
Stimulus modality as indicated at top of each panel. Note in AD
that the phase of the LEG response is compensatory, like that of
the VEST response, whereas the TRUNK and the NECK responses
are anticompensatory. The data in E and F suggest that the proprio-
ceptive responses are mainly dependent on stimulus velocity rather
than on frequency
Neck stimulation
The gain curves for both 0.05 Hz and 0.2 Hz almost overlay
each other (Fig. 3F) and also overlay the replotted frequen-
cy series data (taken from Fig. 3D). The phase curve for
0.2 Hz shows only a slight lead with respect to head excur-
sion relative to the feet, but that for the 0.05-Hz series
shows a more pronounced lead (exception, 0.63/s), corre-
sponding closely to what we observed before for the fre-
quency series at 0.2 Hz and 0.05 Hz, respectively. Apart
from the exception mentioned, the phase curves for 0.2 Hz
and 0.05 Hz are almost constant across stimulus velocity.
Combined VEST-LEG stimulation (interaction series)
Eye responses during vestibular-neck interaction have
been studied in some detail previously (Jrgens and
Mergner 1989). We therefore concentrated here on vestib-
ular-leg interaction. Five different stimulus combinations
were applied, each at 0.025, 0.05, 0.1, 0.2, and 0.4 Hz. In
all combinations VEST was constant (peak displacement
8), while LEG was varied (16, 12, 8, 4, and 0; mi-
nus sign indicating counter-phase between the two sinuso-
idal stimuli). Subjects performed a psychophysical task
during the trials, which were presented in random order
(see Materials and methods).
Figure 4 A gives median gain and phase values of the
eye responses as a function of both stimulus combination
and frequency. In the combination VEST=8, LEG=0
(VEST only), the results described above for VEST were
reproduced (compare Fig. 3A). When LEG stimuli were
added, the gain remained approximately unchanged at
high stimulus frequencies. However, at low frequencies,
the magnitude of the reduction in gain that is normally
seen, gradually diminished as LEG amplitude increased.
This can be appreciated, for instance, for the combination
in which LEG amplitude was equal and opposite to VEST
(LEG, 8; en bloc rotation of head, shoulder, and pelvis
about the stationary feet). However, the effect saturated,
when LEG amplitude was further enlarged, with gain re-
maining essentially constant (e.g., to 16; foot rotation in
space of same magnitude as, but counter to the head rota-
tion in space). LEG had only a minor effect on the phase
of the response, in that the slight phase advance observed
with VEST-only at low frequencies became less.
 455
Fig. 4A Eye responses obtained
during combined leg and ves-
tibular stimulation. Median gain
and phase values are plotted as a
function of stimulus combina-
tion and frequency (three-di-
mensional plot). Note that the
LEG stimulus slightly improves
gain and phase of the eye re-
sponses. B Correlation of eye
movement with perceptual data.
Gain values of eye-in-head (EH)
responses are plotted against
gain of concurrently indicated
body-in-space rotation for the
vestibular-leg stimulus combi-
nations at 0.025 Hz (a) and
LEG-only stimulation (b). Note
that correlations are weak, but
they are statistically significant
(VEST-LEG combinations,
a P<0.05; LEG-only,
b P<0.001)

difference was that, at low frequency, the psychophysical

Fig. 5A, B Slow eye responses (grand means) to a smoothed, ramp-
like NECK stimulus (superpositions of individual stimuli) toward
the right (A) and the left (B). Stimulus curves represent rotations
of chair-mounted head gear (head-on-trunk rotation; see Materials
and methods). Note that the eye responses show a phasic anticom-
pensatory component (in the direction of the head) which is super-
imposed on a tonic compensatory component
Relation between LEG-evoked eye response
and self-motion perception
The psychophysical data obtained in the interaction series
(indication of subjective body rotation in space) closely
resembled those previously obtained in a psychophysical
study on human self-motion perception (Mergner et al.
1993) and therefore are not presented here. The median
curves of the psychophysical data closely corresponded
to those of the eye responses shown in Fig. 4A. The only
response continuously increased with the increase in LEG
amplitude (0 to 16), whereas the eye response saturat-
ed when LEG amplitude exceeded 8. Furthermore, a
high similarity between the median curves for eye re-
sponse and perception was observed for LEG alone
(LEG-only; a repetition of the series shown in Fig. 3B).
We wondered whether such a similarity also exists on
a single-trial basis. Correlations for gain between eye and
perceptual responses were calculated for two conditions
in which gain varied as a function of LEG. This applied
to the VEST-LEG combinations at 0.025 Hz as well as
to LEG-only across frequency. Only weak, though statis-
tically significant, correlations were observed for the
VEST-LEG combination (r=0.37, P<0.05; Fig. 4B, a)
and LEG-only (r=0.53, P<0.001; Fig. 4B, b).
Neck response to a position ramp
There are anecdotal reports in the literature that the COR
may consist of two components, one compensatory and
the other anticompensatory (see Discussion). In our data
we found no clear evidence for two COR components.
However, to counter the possibility that the frequency
range of our sinusoidal stimuli was too small to identify
two distinct components from the frequency behavior,
we applied a transient NECK stimulus.
The eye responses to the rightward and leftward
NECK stimuli (position ramp series) are shown in
Fig. 5. These responses did indeed show two components.
There was an initial eye shift in the direction of NECK,
i.e., that of head-on-trunk excursion (which will be de-
456
scribed as initial anticompensatory component), but
clearly before the stimulus ended the response reversed;
it developed a shift in the opposite direction and crossed
the baseline (late compensatory component). This late
component continued somewhat after the stimulus ended,
shifting the eye toward the trunk and foot position.
Discussion
In line with previous work, we found that the COR slow
component is anticompensatory and only has appreciable
gain at low stimulus frequencies (see Introduction). Our
findings clarify the question of whether the gain mainly
depends on frequency or velocity; we show that the gain
is determined mainly by a velocity nonlinearity (velocity
saturation). Furthermore, we show that the eye response
resulting from trunk proprioceptive stimulation is similar
to the COR with respect to its gain behavior and its anti-
compensatory direction (exception: it does not show the
phase lead of the COR at low frequencies). The eye re-
sponse evoked by leg proprioceptive stimulation, in con-
Fig. 6 A Model of proprioceptive input to the gaze-stabilizing net-
work (HB _ head-on-body velocity, BF _ body-on-feet velocity, HS
head-in-space velocity). The proprioceptive input (box PROP)
shows ideal transfer characteristics (1), whereas the vestibular input
(VEST) shows high pass characteristics (icon for high pass filter).
In the direct proprioceptive path (I) the signal is mainly shaped by a
satturation (a), whereas in the modifying path (II) there is an addi-
tional high pass filtering (d) and a gain element (e). Further details in
text. BD Simulation data obtained with the model in A for sinuso-
idal LEG (B input BF) and NECK (C input HB) _ stimulation (a, fre-
quency series; b velocity series) and for the position-ramp stimulus
(D dotted curve, LEG response; thick solid curve, NECK response)
trast, is oriented in the opposite direction, although show-
ing a similar gain behavior. The discrepancy concerning
the direction appears puzzling, since work on human
self-motion perception suggests that neck, trunk, and leg
proprioceptive inputs may be viewed as one propriocep-
tive system along the body axis, yielding equivalent sig-
nals of head-on-foot excursion at the different interseg-
mental levels (Mergner et al. 1997). Taken together, the
findings suggest that the effect of proprioceptive input
on gaze stabilization of the adult human is weak.
Why, then, study the slow proprioceptive eye respons-
es? We think it is worth identifying, on a behavioral basis,
the vestibular-proprioceptive interaction network in the
intact adult. This will help us understand the modification
of the network which occurs during ontogenesis and adap-
tation. Furthermore, it is of interest to compare the net-
work for gaze with that for self-motion perception and
posture control. As a basis for comparison and discussion,
we first give a description of our findings, on both the
neck and leg response, in the form of a dynamic model
(the most parsimonious form of description we can think
of), before considering functional aspects. In the model,
we designed a common single mechanism for both re-
sponses, rather than trying to invent a particular mecha-
nism for each intersegmental level. We think that the
model, although still speculative, also applies to many
previous observations in the literature.
Model
As a point of departure, we start with the leg response. Its
gain depends on stimulus velocity, while the phase re-

mains constant across frequency and velocity. This find-
ing was implemented in the model (Fig. 6A) by a satura-
tion residing at a central site where the proprioceptive sig-
nal encodes angular velocity (step a; input: body velocity
relative to the feet, BF;_ box PROP contains ideal, 1,
transfer characteristics). The signal is used, via a direct
path (I), after sign reversal (b) and an integration (c), to
yield a tonic EH signal as output, which is directed coun-
ter to the body-on-foot excursion (referred to as tonic
compensatory component in the following text). This di-
rect proprioceptive path might correspond to that de-
scribed earlier in the decerebrate cat for the COR by
Hikosaka and Maeda (1973). According to their study, a
rightward head turn, for instance, activates neck afferents
on the left side. These, in turn, activate abducens moto-
neurons on the left side via a double-crossing pathway
through the vestibular nuclei on the right side, yielding
a leftward (compensatory) eye response. The neck pro-
prioceptive input might reach the vestibular nuclei via
the central cervical nucleus (Sato et al. 1997). It appears
to stem mainly from muscle spindle afferents (Richmond
and Abrahams 1979; Mergner et al. 1982).
For the neck responses (anticompensatory COR) ob-
tained in our experiments, we assume that it is based on
the direct mechanism just described, but in addition con-
tains a frequency-dependent (phasic) and sign-reversed
(anticompensatory) component that overrides the com-
pensatory tonic one. The evidence for this assumption is
based on the frequency-dependent phase behavior of the
sinusoid response (Fig. 3D) and on the response with
the transient stimulus (Fig. 5). In the model of Fig. 6A
we account for the neck proprioceptive part of the system
by using the same network as before, but giving it a dif-
_ in re-
ferent input (head velocity relative to the body, HB;
ality there would almost certainly be a chain of several
networks, one for each intersegmental joint). The phasic
anticompensatory component is implemented in the form
of a modifying path (II) which contains a high-pass fil-
ter (Fig. 6A, d) and has the opposite sign to the direct one.
The filter has a time constant of 16 s which, noticeably,
corresponds to the known behavioral time constant of
the VOR. The strength of this pathway is determined by
a modifiable gain element (Fig. 6A, e) which, if high en-
ough, reverses the direction of the EH output, making it
anticompensatory. Interestingly, there have been reports
in the literature that the COR, although being mostly an-
ticompensatory, may become intermittently compensato-
ry, or that its direction may vary across individuals
(e.g., Fuller 1980; Holtmann et al. 1989; Reisman and
Anderson 1989). These findings may indicate that the
modifiable path is variable across individuals and time.
We assume it is also variable across the different inter-
segmental joints, possibly depending on how a given seg-
ment is used most frequently in gaze control.
Simulations of the model were performed with the si-
nusoidal stimuli and the transient stimulus (Fig. 6BD).
For sinusoidal leg stimulation (input BF) _ the gain of
the modifying path (II) was set at a low value (G=0.3),
but for neck stimulation (input HB) _ it was accentuated
457
(G=1.6). The simulations yielded results which closely re-
sembled the experimental data, with respect to the gain
and phase curves of both the frequency series (a in
Fig. 6B, C) and the amplitude series (b in Fig. 6B, C).
For the transient stimulus, the same low- and high-gain
values were used, yielding an essentially tonic compensa-
tory leg response, and an initially anticompensatory,
then later compensatory neck response, respectively
(Fig. 6D). Note that a change of the gain element in the
model modifies the phase of the responses, without much
affecting the gain behavior of the system. The model was
also used to simulate the vestibular-leg interaction data
(Fig. 4A). For the implementation of a vestibular path
(VOR), we adopted the model of Robinson (1977) and ad-
justed its parameters to meet the VOR in our subjects (all
transfer characteristics contained in the box VEST of
Fig. 6A). The simulated data (not shown) closely corre-
sponded to the ones depicted in Fig. 4A, indicating that
the improvement of the VOR at low frequency, when
there is an additional leg stimulus, can be described sim-
ply by a summation of the VOR with the LEG input (es-
sentially the direct path).
Interestingly, without velocity saturation and with
G=1, the neck input in the model (HB) _ would exactly
compensate the deficiency of the vestibular transfer func-
tion (compare the idea of Meiry, 1971, in the Introduc-
tion): For example, in conditions in which HS _ HB _
(head-in-space velocity equals head-on-body velocity),
_
EHlHS+(1l) _ (l, nonideal vestibular transfer
HB
function, symbolized in Fig. 6A by high-pass icons). This
form of the model largely corresponds to that previously
designed for human self-motion perception (Mergner et
al. 1991, 1993, 1997). The latter also includes two pro-
prioceptive signals. One of these carries l and is sign-re-
versed (analogous to pathway II). Perceptually, it is used
to channel the vestibular signal down, along all the body
segments, to the body support, in order to evaluate the ki-
nematic state of the support (proprioceptive down-chan-
neling). The other shows essentially ideal transfer char-
acteristics (analogous to pathway I) and is used to per-
ceive movements of our body segments relative to the
support (proprioceptive up-channeling). For perceived
head-in-space rotation during neck stimulation, the down-
and up-going proprioceptive signals do not cancel each
other completely; the stimulus evokes a head-turning illu-
sion which is small at high frequencies, but increases in
magnitude at low frequencies, similar to the eye response.
Noticeably, the down and up channeling concept also ap-
plies to postural control of human upright stance
(Mergner et al. 1997), to perception of visual object mo-
tion in space (Mergner et al. 1992) and to the updating of
visual object location in space (Maurer et al. 1997).
Thus, from a global view, there is a high similarity be-
tween the networks used for self-motion perception and
gaze stabilization. Parts of the two networks may be iden-
tical early in ontogenesis or at early stages of central pro-
cessing (vestibular-proprioceptive interaction already
starts at the level of vestibular nuclear neurons: Boyle
and Pompeiano 1981; Anastasopoulos and Mergner
458
1982). However, there are also differences between the
two, apart from the fact that the output signals for self-
motion perception and gaze stabilization have opposite
signs. The most relevant difference for us would be the
modifiable gain in the gaze network, which allows for a
reversal of response direction; nothing comparable was
found for perception. Other findings also let us assume
a separation of the two systems, at least at higher levels
of processing. For instance, despite the fact that the medi-
an curves for the perceptual and the eye responses in the
interaction series were similar, the correlation between
them on the basis of the single-trial data was very weak
(Fig. 4B). In this context it should also be mentioned that
it is certainly not the self-motion perception which deter-
mines the eye response: during low-frequency neck stim-
ulation, perceived head and trunk turning in space have
opposite directions; shifting attention from one to the oth-
er perception does not considerably affect the COR slow
component (Jrgens and Mergner 1989).
Functional relevance of the proprioceptive eye responses
Before dealing with our findings, we would like to briefly
consider three general aspects. First, we deem it likely
that under most normal conditions (an illuminated envi-
ronment) visual mechanisms overrule the proprioceptive
ones for gaze stabilization and therefore are more relevant
for accurate vision. In the range of low stimulus frequen-
cies or velocities, where the proprioceptive responses
reach a considerable gain, the optokinetic and smooth-
pursuit closed-loop systems clearly dominate in both
monkey and man (see Schweigart et al. 1995, 1997). Sec-
ond, we believe that in the intact adult the proprioceptive
input is more important for gaze reorientation than for sta-
bilization, i.e., for the generation of saccades that shift
gaze into a new direction, as suggested earlier (animal ex-
periments: Mirenowicz and Hardy 1992; humans: Jrgens
and Mergner 1989). Third, proprioceptive eye responses
can by no means fully substitute the VOR, because the
latter compensates head motion in space (e.g., evoked
by motion of the body support), whereas the propriocep-
tive responses react solely to inter-segmental rotations.
Since in many behavioral situations the head-in-space
movement does not match the head-on-trunk movement,
or both may even have opposite directions, Fuller
(1980) considered the possibility of short-term modifica-
tions of the COR, or even a switching of its direction, de-
pending on the particular situation. However, there is no
experimental evidence for this rapid modification, at least
in humans (Jrgens and Mergner 1989). Yet, as men-
tioned before, the slow, proprioceptive eye responses
are of interest, not only for comparison with perception
but also in view of their development during ontogenesis
and their role for adaptation after loss of the VOR.
Studies on the ontogenesis of the COR are scarce, but
the pattern which emerges from them is rather clear.
Barany (1918/1919) observed a tonic, compensatory
COR in premature babies and also up to 3 days after reg-
ular births (according to him, the response was obscured
at later tests by visual input). The only other related work
we are aware of is by Reisman and Anderson (1989), who
performed quantitative eye-movement recordings in the
dark in 2- and 4-month-old infants. With neck stimula-
tion, the slow COR components could be either compen-
satory or anticompensatory, with the gain of both compo-
nents depending on rotational frequency (larger at 0.1 Hz
than at 0.5 Hz). The compensatory component was found
to be larger in the 2-month-old (G=0.77 at 0.1 Hz) than in
the 4-month-old infant (G=0.38). Furthermore, anticom-
pensatory components were hardly observed in the 2-
month-old infants, but regularly in the 4-month-old in-
fants. Considering also that the COR in adults is anticom-
pensatory and weak, it appears that there is an involution
of the COR during ontogenesis with respect to its re-
sponse gain, and that the compensatory response becomes
obscured by the anticompensatory one (compare Fig. 5).
What signal(s) could induce the involution of the COR
gain? We deem it likely that it is mainly a vestibular
head-in-space velocity signal which becomes effective
when the VOR develops functional relevance in early in-
fancy. As mentioned above, an eye-in-space stabilization
by the VOR is certainly more functionally relevant for vi-
sion than an eye-relative-to-body (or foot) stabilization by
the COR, so that the former suppresses the latter. Why is
the proprioceptive input to the gaze network then not
completely removed? This may be related to the nonideal
vestibular canal dynamics, by which the VOR deteriorates
at low stimulus frequency during earth-horizontal rota-
tions, unlike during vertical rotations, where the canal sig-
nals are complemented by otolith signals. There are, to
our knowledge, no COR studies related to this problem
in humans, but there is work on the COR in rabbit which
is compensatory. This work supports the hypothesis; the
vertical COR is poor compared with the horizontal
COR (Barmack et al. 1981), and the horizontal COR
maintains its spatiotopic plane when head and trunk of
the animal are tilted together (brought about by a compen-
satory change in orbitotopic coordinates, induced by oto-
lith input; Pettorossi et al. 1987).
What kind of adaptation of the proprioceptive eye re-
sponses occur in the adult and how can they be related
to the model in Fig. 6A? A compensatory COR with in-
creased gain is found in patients within several weeks fol-
lowing loss of the VOR, although the gain that is reached
appears to vary considerably among patients (Gresty et al.
1977; Kasai and Zee 1978; Barnes 1979; Leopold et al.
1983; Bles et al. 1984; Bronstein and Hood 1986; Huygen
et al. 1991). It is generally held that this COR helps the
patients to stabilize gaze, but the exact mechanism is still
not understood. There is general agreement that the COR
found with passive stimulation alone (passive COR)
would be insufficient to compensate for VOR loss, and
that its latency would be too long if one considers saccad-
ic gaze shifts containing rapid head movements (Gresty
1976). Therefore, the compensatory mechanisms must in-
volve some central (e.g., efference copy) signal arising
with active head movements (Dichgans et al. 1973; Taka-

hashi et al. 1981, 1989). In the model in Fig. 6A, a com-
pensatory COR of considerable gain can be obtained by
setting the gain of the modifying pathway close to zero
and opening the velocity saturation. Since the restriction
of the neck input to low velocities (saturation) is a result
of involution, its reversal to higher values certainly would
take considerable time. This may explain why the in-
crease in COR gain following VOR loss occurs slowly
(Dichgans et al. 1973) as compared to the well-known ad-
aptation of the VOR by altered visual input, for instance.
Such a visually induced plastic change is also observed
for the COR in vestibular-loss patients after minutes to
hours (Heimbrand et al. 1996). However, it is likely to in-
volve mechanisms other than those considered in the
model.
Given that the proprioceptive eye responses in the in-
tact adult are weak and restricted to horizontal stimuli at
low frequency, one could still ask whether they play a
functional role. We speculate that the tonic compensatory
component might serve to stabilize the eyes in the hori-
zontal plane by shifting them slowly to the primary
head-on-foot position; this as a default, because there is
no static vestibular set point value in this plane. Given
that an eye shift in the direction of the trunk or feet by
the tonic component is not desireable, it can transiently
be neutralized by the phasic one. The finding of a phasic
component in the neck, but not in the leg response, can be
related to functional aspects; reorienting gaze shifts nor-
mally involve head movements at the level of the neck
(or upper trunk), but rarely at the level of the legs, so it
is likely that no phasic response ever developed for the
latter condition.
Acknowledgement This work was supported by DFG Me 715.
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