Exp Brain Res (2011) 209:415–423
DOI 10.1007/s00221-011-2567-5
RESEARCH ARTICLE
The oculogyral illusion: retinal and oculomotor factors
Jerome Carriot • A. Bryan • P. DiZio
J. R. Lackner
•
Received: 13 April 2010 / Accepted: 19 January 2011 / Published online: 6 February 2011
Ó Springer-Verlag 2011
Abstract Subjects in a dark chamber exposed to angular
acceleration while viewing a head-fixed target experience
motion and displacement of the target relative to their
body. Competing explanations of this phenomenon, known
as the oculogyral illusion, have attributed it to the suppression of the vestibulo-ocular reflex (VOR) or to retinal
slip. In the dark, the VOR evokes compensatory eye
movements in the direction opposite to body acceleration.
A head-fixed visual target will tend to suppress these eye
movements. The VOR suppression hypothesis attributes
the oculogyral illusion to the signals that prevent reflexive
deviation of the eyes from the target thus resulting in
apparent target displacement in the direction of acceleration. The retinal slip hypothesis attributes the illusion to
inadequate fixation of the target with the eyes being
involuntarily deviated in the direction opposite acceleration, the retinal slip being interpreted as target displacement in the direction of acceleration. Another possibility is
that the illusion could arise from a change in the representation of the perceived head midline. To evaluate these
three alternative hypotheses, we tested 8 subjects at 4
acceleration rates (2, 10, 20, 30°/s2) in each of three conditions: (a) fixate and point to a target light; (b) fixate to the
target light and point to the head midline; (c) look straight
ahead in the dark. The displacement magnitude of the
oculogyral illusion was least at 2°/s2 & 2° and was &10° at
the other acceleration rates. The presence of the target light
significantly attenuated eye movements relative to the dark
condition, but eye movements were still present at the 10,
20, and 30°/s2 accelerations. The eye velocity profiles in
J. Carriot (&) A. Bryan P. DiZio J. R. Lackner
Ashton Graybiel Spatial Orientation Laboratory, MS 033,
Brandeis University, Waltham, MA 02454-9110, USA
e-mail: jerome.carriot@mcgill.ca
the dark at different acceleration rates did not show a oneto-one inverse mapping to the magnitude of the oculogyral
illusion at those rates. The perceived head midline was not
significantly displaced at any of the acceleration rates. The
oculogyral illusion thus has at least two contributing factors: the suppression of nystagmus at low acceleration rates
and at higher acceleration rates, a partial suppression
coupled with an integration of the drift of the eyes with
respect to the fixation target.
Keywords Angular acceleration Oculogyral illusion VOR cancelation Retinal slip Eye slow phase velocity Vestibular
Introduction
The oculogyral illusion (OGI) is experienced when subjects
viewing a head-fixed visual target are exposed to angular
acceleration in a dark environment. The target will appear
to move through both space and displace relative to the
subject’s body in the direction of acceleration (Graybiel
and Hupp 1946). The illusion involves a paradoxical dissociation of position and velocity with displacement relative to the body reaching a peak, while the target still seems
to be moving relative to the subject (Brown et al. 1949).
With high acceleration rates and long dwell times at constant velocity, reversals of direction of the illusion may
occur during the constant velocity period as well as after
deceleration to rest (Graybiel et al. 1946). The threshold for
experiencing the OGI is below that for detecting selfrotation (Graybiel et al. 1948).
Explanations of the OGI initially focused on oculomotor
control. Angular acceleration activates the semicircular
canals inducing a reflexive eye response, the vestibuloocular
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reflex (VOR), driving the eyes in the direction opposite
acceleration. The VOR is very important for stabilizing
vision when the head is voluntary moved. It occurs as well,
albeit with reduced gain, during passive body acceleration
in complete darkness producing a nystagmus with slow
phase opposite the direction of body rotation. If a subject
views a head-fixed target in an otherwise dark test chamber, the nystagmus will be attenuated. In this situation,
the central nervous system issues a predictive eye pursuit
command that serves to cancel the VOR (Barnes 1988;
Barnes and Eason 1988). The VOR drive signals presumably are still being generated by the semicircular
canals but are being counteracted by the smooth eye
pursuit system.
Whiteside et al. (1965) proposed that the OGI arises
because the pursuit signal to override the VOR is centrally
interpreted as a displacement of the eyes. They assumed
that stable fixation is maintained, and consequently, a
visual target would be perceived as displacing in the same
direction and by the same magnitude as the change in
registered eye position. This hypothesis accounts for why
the OGI is in the direction of acceleration and presumes
that the CNS mechanisms determining visual direction do
not monitor or take into account the reflexive VOR drive
on the eye muscles that is being countered.
An alternative hypothesis is that there is incomplete
suppression of the VOR during the OGI. In this case, the
target would be displaced off the foveae during the slow
phase of nystagmus. Assuming the reflexive drive on the
eyes is not centrally monitored, this would lead to an
apparent displacement of the target in the direction of
acceleration. Like the suppression hypothesis, the eye drift
hypothesis assumes that the involuntary reflexive drive is
not taken into account in computing visual direction.
During angular acceleration in the dark, the beating field of
the nystagmus elicited (the Schlagfeld) may deviate in the
direction opposite acceleration. Thus, the average position
of the eyes could be displaced in the head relative to the
straight ahead. If the smooth eye pursuit command to
override the nystagmus when a target is present effectively
overcomes this average position shift, then the magnitude
of the displacement component of the OGI should be of
comparable magnitude but opposite sign.
A third hypothesis concerning the OGI relates to the fact
that sound localization is also affected by angular acceleration. If an auditory rather than visual target is presented
in a subject’s midline during acceleration, it will be heard
to displace in the direction opposite acceleration, a phenomenon known as the audiogyral illusion (Clark and
Graybiel 1949). A shift in the apparent midline of the head
is one possible explanation of the audiogyral illusion
(Lester and Morant 1969). Changes in apparent head
position have also been associated with errors in localizing
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Exp Brain Res (2011) 209:415–423
visual targets (Lackner and Levine 1979; Prieur et al. 2005;
Ceyte et al. 2007) and might also explain the OGI.
Recently, a strong correlation has been found between the
errors in visual, auditory, and tactile localizations that are
elicited during exposure to linear acceleration (Lackner and
DiZio 2010).
Our goal in the present experiments was to determine
the extent to which the OGI is related to (1) suppression of
nystagmus, (2) retinal slip resulting from inadequate nystagmus suppression, and (3) change in the apparent midline
of the head.
Materials and methods
Subjects
Eight male subjects (aged 26, 26, 28, 29, 31, 32, 39 and
55 years) participated. They completed a health questionnaire and signed informed consent forms approved by the
Human Subjects Research Committee of Brandeis University. All were in good physical health, and none had a
history of visual, auditory, balance, or vestibular disorders.
The VOR gains and time constants for all subjects were
within the normal ranges and were symmetric across
rotation directions.
Apparatus
Labyrinthine stimulation was provided by means of a
rotating chair that permitted a precise alignment of the
physical Z-axis of the subject’s head with the axis of chair
rotation, see Fig. 1. The subject’s head was ventriflexed
approximately 25° and stabilized by an individually molded dental bite plate. This head position placed the horizontal semicircular canals approximately in the plane of
rotation. Two crossed shoulder belts and a lap belt stabilized the torso. The chair was powered by a Neurokinetics
servo motor. The velocity profile and rotation direction of
the chair were controlled using custom-designed software.
A red light–emitting diode that served as a fixation target
was mounted in front of the subject, in alignment with the
physical head midline, at an approximate distance of 30 cm
from the bridge of the nose. The subject used a hand-held
pointer to indicate the position of the target (see Fig. 1).
Pilot studies indicated that the ability to maintain the
pointer in a desired location was not affected by angular
acceleration. The angular position of the pointer was
indicated by a potentiometer signal sent to the data collection computer, which also collected eye position and
chair velocity signals. These continuous signals were
sampled at a rate of 60 Hz. These data were then transformed and filtered using MATLAB-based programs.
Exp Brain Res (2011) 209:415–423
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subjects tried to fixate its remembered straight ahead
position. The trials were completed in two sessions conducted at least 2 days apart. The three conditions were
presented in balanced order with the second condition for
each subject divided between the two sessions. Acceleration rates of 2, 10, 20, and 30°/s2 were run in alternating
clockwise and counterclockwise directions. The same order
of accelerations was used across conditions for each subject, but the orders were counterbalanced across subjects.
Data analysis
OGI condition
Fig. 1 Servo-controlled rotating chair used to stimulate the semicircular canals and to present a visual target
The time course of the OGI was determined from the
pointer displacement by subtracting its position during
the first 5 s of the baseline period from its position during
the entire test period up to the onset of deceleration. The
extent of retinal slip was determined by measuring the slow
phase velocity and deviation of the eyes during the rotation
periods and computing a cumulative slow phase displacement (SPD) based on the signed sum of all slow phase eye
displacements.
Eye movement recordings
Head midline condition
Eye position was recorded using an ISCAN eye camera
(model EC-501) mounted on the bill of a baseball cap to
track the position of the left eye. The cap was secured to
the head and was stable throughout all trials. Eye position
was recorded in both the horizontal and vertical planes, but
only the horizontal movements of the eyes were analyzed
because our experimental manipulations only affect that
plane. Eye movement calibration was achieved by having
the subject fixate in turn each of three light-emitting
diodes: one in the head midline and the others 20° to the
left and right on the same azimuthal plane. This procedure
was done before each experimental session and periodically repeated. The calibrations indicated that measurement
drift was below 1°.
Experimental conditions and procedure
Each subject participated in three conditions involving a
total of 24 trials. A trial included 10 s of baseline data
collection, 5 s during acceleration, 30 s during constant
velocity rotation, followed by 5 s of deceleration to rest.
The three conditions included (1) OGI: the target light was
present and subjects tried to fixate it and point continuously
to it, (2) HM: the target light was present, subjects tried to
fixate it and to point continuously to their apparent head
midline, and (3) Dark: the target light was present during
the 10-s pre-rotation period and subjects fixated it; the
target light was turned off at the onset of rotation, and
The time course of the HM was determined by the pointer
displacements during rotation in relation to baseline as
done for the OGI condition.
Dark condition
The slow phase velocity of the eyes and the cumulative
slow phase displacement were calculated for the rotation
period relative to baseline. The Schlagfeld deviation of the
eyes from the straight ahead position during baseline was
computed.
Assessing eye movement suppression in the OGI conditions
To estimate the magnitude of the nystagmus suppression,
we compared the time course of the cumulative SPD of the
eyes in the OGI and dark conditions for the different
acceleration rates. The resulting differences were used in
statistical comparisons. Cross-correlations were also performed on the OGI time course and other variables
including OGI velocity, unsuppressed eye velocity, and
cumulative SPD in the OGI condition. To compare the OGI
time course with other variables, a least-squares piecewise
linear fit was calculated (1) for the acceleration period, (2)
from the end of acceleration to the peak of the variable, and
(3) from the variable’s peak value to the end of the perrotation period.
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To relate the slow phase displacement of the eyes
in the OGI and dark conditions with the OGI time course,
we estimated the coefficients of the equation
OGIðtÞ ¼ gain SPDðtÞ
where OGI is the pointer displacement in the OGI condition, and SPD is slow phase eye displacement. This equation is generally found in the form X = bias ? gain 9 Y.
We considered the bias equal to zero because without
acceleration the eyes were stably fixating. To compare the
model’s ability to estimate the pointer displacement, the
variance-accounted-for was computed: {VAF = 1 - [var
(mod - OGI)/var (OGI)]} (Cullen et al. 1996). Mod represents the modeled pointer displacement, and OGI represents the actual pointer displacements in the OGI condition.
For each acceleration rate, we averaged the individual
gains obtained during the previous fitting procedure. Then,
we predicted the pointer displacement for the temporally
averaged SPD (across subjects) and compared it with the
actual average pointer displacement (across subjects). We
also repeated the same procedures using a common gain
across acceleration rates. The VAF shows how well the
actual OGI displacement is predicted by the individualized
or common gains in the model. Prediction of physiologic
data by a linear model is typically considered good when
the VAF is greater than 0.5.
Exp Brain Res (2011) 209:415–423
fits. The slope during 10°/s2 acceleration was steeper than
at 20 and 30°/s2 (0.16 vs. 0.07 vs. 0.08, respectively). In
contrast, the slopes for these three acceleration rates did
not statistically differ between the end of acceleration
and the peak of the OGI and between the peak of the
OGI and the end of the constant velocity period. Finally,
the variability was greater at 2 and 10°/s2 than at 20
and 30°/s2.
OGI velocity
These results are presented in Fig. 2b. Acceleration affected velocity [F(3,21) = 3.01, P = 0.053]. A post hoc
Newman–Keuls analysis indicated that OGI velocity was
least at 2°/s2 (*3°/s), highest (*6.5°/s) at 10 and 20°/s2,
and not different at 30°/s2 from 2, 10, and 20°/s2 (*5°/s).
Peak OGI velocity tended to be concomitant with the end
of the acceleration period; consequently, the least-squares
piecewise linear fit slopes were calculated from the onset of
acceleration to the peak of the variables and from this peak
to the end of the constant velocity period. The slopes were
not significantly different during the accelerations, but the
velocity decreased faster at 10°/s2 than at the other three
acceleration rates, which did not differ.
Slow phase eye velocity
Results
OGI condition
OGI magnitude
For each acceleration rate and direction, every subject
reported body-relative target displacement in the direction
of acceleration. Data averaged across direction of rotation
are presented in Fig. 2a. A 2 9 4 ANOVA with repeated
measures was used to determine the effects of rotation
direction (clockwise vs. counterclockwise) and acceleration
rate (2, 10, 20, 30°/s2) on the peak magnitude of the OGI.
Acceleration rate but not direction had a significant effect
[F(3,21) = 5.93; P = 0.04], and there was no interaction.
A post hoc Newman–Keuls analysis indicated that the
illusion was least at 2°/s2 (*2°) and not different in magnitude (*10°) at the other acceleration rates. For the 10, 20
and 30°/s2 accelerations, the OGI maximum deviation was
reached at different times during the constant velocity
periods. The maxima were reached approximately 10 s
(8.7 s ± 13.4) after the beginning of constant velocity for
10°/s2, and 20 s afterward for 20 and 30°/s2 (18.6 s ± 5.8,
17.6 s ± 6.2, respectively). These differences were also
reflected in the slopes of the least-squares piecewise linear
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To determine whether retinal slip could be responsible for
the OGI, we analyzed the eye movements present despite
the presence of the fixation target (Fig. 2c). VOR suppression was not complete during acceleration except at
2°/s2. The peak slow phase velocity of eye movements was
compensatory for body rotation and was approximately
5°/s at 10°/s2 and 10°/s at 20°/s2 and 30°/s2 accelerations.
Peak slow phase eye velocity did not differ from the OGI
peak velocity at 10°/s2 but was less than half of it at the 20
and 30°/s2 acceleration rates. The slopes of the leastsquares piecewise linear fits did not differ during the
window beginning with the onset of acceleration to the
peak of the variable, but did differ at 20 and 30°/s2 during
the window from the peak of the variable to the end of the
constant velocity period. The coefficients of the crosscorrelation maxima were non-significant (-0.26, -0.18,
and -0.38 for 10, 20, and 30°/s2, respectively). Thus, the
velocity of unsuppressed eye movements and the velocity
of the OGI were not related one-to-one.
Slow phase eye displacement
The peak of the cumulative SPD of the eyes in the OGI
condition increased with the acceleration rates (-41.3°,
-69.5°, and -90.6 for 10, 20, and 30°/s2, respectively,
D
OGI magnitude (deg.)
SPV (°/s)
C
419
2°/s2
10°/s2
20°/s2
30°/s2
15
150
10
100
50
5
0
5
5
5
5
3
3
3
3
1
1
1
1
-1
-1
-1
-1
-3
-3
-3
-3
0
0
0
0
-5
-5
-5
-5
-10
-10
-10
-10
-15
-15
-15
-15
15
15
15
15
10
10
10
10
5
5
5
5
0
0
0
10
20
30
40
0
0
0
10
20
30
40
Chair Velocity (°/s)
B
OGI velocity (°/s)
A
OGI magnitude (deg.)
Exp Brain Res (2011) 209:415–423
0
10
20
30
40
0
10
20
30
40
Time (s)
OGI Magnitude
Prediction based on the gain of the acceleration rates values
Prediction based on the averaged gain
Fig. 2 a Mean time course and standard error of the OGI determined
by pointer position (in degrees) for the four acceleration rates (2, 10,
20, and 30°/s2). The chair velocity is presented on the right ordinate
(in °/s); 5 s of pre-rotation, 5 s of acceleration, and 30 s of constant
velocity are presented. b Mean time course and standard error of the
OGI velocity for the four acceleration rates. c Slow phase velocity
mean time course and standard error for the four acceleration rates.
d OGI magnitude (gray line) and model predictions made with a
particular gain for each acceleration rate (green line) or with a
common gain across the acceleration rates (blue line). The shading
represents the standard error
P = 0.003). As described in the ‘‘Data analysis’’ section,
we estimated the coefficients of the following equation to
relate the OGI time course to the SPD of the eyes:
Table 1 Averaged gain and variance-accounted-for (VAF) for
acceleration rates 10, 20, and 30°/s2 for the comparison between the
pointer displacement and the slow phase eye displacement during the
OGI condition
OGIðtÞ ¼ gain SPDðtÞ :
The averaged gains and VAFs are presented in
Table 1 for each acceleration rate. Based on these
gains, we predicted the pointer displacement for the
averaged SPD values (across subjects) and compared it
with the actual average pointer displacement (across
subjects). In this context, the VAF represents the model’s
ability to predict the OGI magnitude. The results are
presented in Fig. 2d. The VAF was 0.56, 0.83, and 0.86
for 10, 20, and 30°/s2, respectively with a different gain
for each acceleration rate and 0.57, 0.76, and 0.58 using
a common gain for each acceleration rate. Whether the
gain used in the model was common or specific to each
acceleration rate, the OGI magnitude is increased by the
eye drift resulting from the slow phase velocity present
despite the target light.
Acceleration rates (°/s2)
Gain
VAF
2
10
-0.14 (±0.09)
0.54 (±0.26)
20
-0.09 (±0.06)
0.59 (±0.22)
30
-0.07 (±0.04)
0.70 (±0.25)
No residual eye velocity was found at 2°/s
2
Standard error in italic
Schlagfeld deviation
Although retinal slip did occur in the OGI conditions,
except at the 2°/s2 acceleration rate, the average position of
the eyes was not significantly displaced from the target
light for any of the acceleration rates [F(3,21) = 1.17;
P = 0.37].
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Exp Brain Res (2011) 209:415–423
Dark condition
The eye movements recorded in total darkness compared
with those recorded in the OGI condition allowed us to
determine the amount of suppression in the OGI condition.
Slow phase eye velocity
Slow phase velocity was significantly affected by acceleration [F(3,21) = 37.28; P = 0.002] (see Fig. 3a). It was
lowest at 2°/s2 (-5.5°/s) and highest at 30°/s2 (-35.5°/s)
and intermediate at 10°/s2 (-17.7°/s) and 20°/s2 (-22°/s).
The lowest and highest acceleration rates were significantly
different (P B 0.007) from the middle two that were not
different from each other, by Newman–Keuls tests
(P = 0.13). The velocity of the OGI was not predictable
from the slow phase velocity of the eyes in the dark condition because the coefficients of cross-correlation maxima
were low (-0.16 ± 0.32, -0.52 ± 0.11, -0.47 ± 0.14,
and -0.45 ± 0.16 for 2, 10, 20, and 30°/s2, respectively).
Slow phase eye displacement
The cumulative slow phase displacement of the eyes was
least at 2°/s2 (-77°), highest at 30°/s2 (-414.5°), and
intermediate at 10 and 20°/s2 acceleration rates (-226.6°,
2°/s2
B
OGI magnitude (deg.)
SPV (°/s)
A
Suppression of the SPV (°/s)
Schlagfeld deviation
A one-way ANOVA of Schlagfeld deviation as a function
of acceleration rate failed to show a significant difference.
However, the general shape was slightly biased in the
direction opposite to acceleration.
Head midline condition
Only small, non-significant changes in head midline settings were present regardless of acceleration rate or
direction (see Table 3). The inter-individual variability did
not relate to the patterns seen in the OGI condition. The
head-midline remapping hypothesis can be ruled out of as
an explanation of the OGI.
10°/s2
20°/s2
30°/s2
0
0
0
0
-10
-10
-10
-10
-20
-20
-20
-20
-30
-30
-30
-30
-40
-40
-40
-40
15
15
15
15
10
10
10
10
5
5
5
5
0
0
0
0
Prediction based on the gain of the acceleration rates values
OGI Magnitude
C
-228.4°, respectively). We also estimated the gain and
calculated the VAF for the relationship between OGI
magnitude and cumulative SPD. The results are presented
in Table 2, and each VAF value was significantly different
from 0, t test, P B 0.004. Fig. 3b shows the OGI magnitude and the best gain per acceleration rate (VAF: 0.67,
0.43, 0.53, and 0.79 for 2, 10, 20, and 30°/s2) and prediction with a common gain across the acceleration rates
(VAF = 0.65, 0.49, 0.79, and 0.24). The cumulative slow
phase displacement clearly parallels the OGI.
Prediction based on the averaged gain
0
0
0
0
-10
-10
-10
-10
-20
-20
-20
-20
-30
-30
-30
0
10
20
30
10
20
30
Fig. 3 a Mean time course and standard error of the slow phase
velocity recorded in complete darkness for the four acceleration rates.
b OGI magnitude (gray line) from the OGI condition and model
predictions made with a particular gain for each acceleration rate
(green line) or with a common gain across the acceleration rates (blue
123
-30
10
20
30
10
20
30
40
Time (s)
line). The shading represents the standard error. c Mean time course
and standard error of the slow phase velocity suppression for the four
acceleration rates. Slow phase velocity suppression is obtained by
subtracting the slow phase velocity recorded during the OGI condition
from the slow phase velocity recorded in complete darkness
Exp Brain Res (2011) 209:415–423
421
Table 2 Averaged gain and variance-accounted-for (VAF) for each
acceleration rate for the comparison between the OGI magnitude and
the slow phase eye displacement occurring during the dark condition
Table 4 Averaged gain and variance-accounted-for (VAF) for each
acceleration rate for the comparison between the OGI magnitude and
the suppression of the slow phase eye displacement
Acceleration rates (°/s2)
Acceleration rates (°/s2)
Gain
VAF
Gain
VAF
2
-0.02 (±0.05)
0.34 (±0.28)
2
-0.05 (±0.28)
0.34 (±0.30)
10
-0.03 (±0.04)
0.51 (±0.30)
10
-0.05 (±0.30)
0.47 (±0.33)
20
30
-0.05 (±0.07)
-0.02 (±0.02)
0.60 (±0.15)
0.66 (±0.24)
20
30
-0.004 (±0.11)
-0.02 (±0.02)
0.43 (±0.23)
0.57 (±0.32)
Standard error in italic
Standard error in italic
Comparison of eye movements in the OGI and dark
condition
and suppression are accounting for the OGI magnitude but
their particular contribution is varying with acceleration
rate (minimal retinal slip at 2°/s2, primarily suppression).
Figure 4 shows that the retinal slip contribution increases
with increasing acceleration rate, while the contribution of
the suppression parallels its magnitude through the acceleration rates (Fig. 4, common gain, dashed line).
The extent of suppression of slow phase velocity in the
OGI condition was estimated by subtracting the eye
movements in the OGI conditions from those in the dark
conditions (Fig. 3c). For the lowest acceleration rate, 2°/s2,
suppression was complete in the OGI condition, with virtually no residual eye movements. The slow phase velocity
suppression was 19.4°/s at 30°/s2 and 12.5 and 9°/s at 10
and 20°/s2, respectively. These last values do not differ.
The velocity of the OGI and the magnitude of suppression
of slow phase velocity differ at all acceleration rates [F(1,
7) = 31.05, P = 0.003] and the acceleration rates affected
these variables differently [F(3,21) = 8.16, P = 0.01]. The
coefficients of cross-correlation maximum were relatively
low (-0.27, -0.3, -0.37, and -0.33 for 2, 10, 20, and
30°/s2, respectively). Thus, suppression of slow phase
velocity per se cannot explain the OGI except at the 2°/s2
acceleration rate.
The relative suppression of SPD in the OGI conditions
was determined through comparison with the corresponding SPD in the dark condition. We then estimated the gain
and calculated the VAF for SPD versus OGI time course
for the different acceleration levels. Table 4 presents the
results for the estimation analysis, and Fig. 3b presents the
results of the model predictions. VAF values ranged from
0.32 to 0.77 using individual gains for each acceleration
rate and were 0.67, 0.52, 0.69, and 0.66 using a common
gain for the four acceleration rates. These results show that
the magnitude of the suppressed SPD of the eyes in the
OGI condition correlates very well with illusory visual
displacement magnitude.
Together with the results on retinal slip present in the
OGI condition, these findings show that both retinal slip
Discussion
The OGI represents one of the fundamental illusions
encountered in aviation and aerospace when pilots are
exposed to angular acceleration. The oculogravic illusion,
the visual mislocalization associated with exposure to linear acceleration is another. Such illusions are contingent on
unusual patterns of vestibular stimulation, patterns that are
not experienced under normal conditions of voluntary selfmotion. They are generally associated with apparent selfmotion or changes in apparent orientation. An interesting
feature of the OGI is that its threshold is very low, an order
of magnitude below that of generating the percept of selfrotation, \0.1°/s vs. *1°/s.
Our experimental results allowed us to evaluate the three
primary explanations of the OGI that have been proposed a
change in apparent head midline, nystagmus suppression,
and retinal slip. A remapping of the apparent midline of the
head—as reported in studies of other illusions, (e.g., Taylor
and McCloskey 1991; Karnath et al. 2002; Lackner and
DiZio 2010; Schindler et al. 2002)—cannot account for the
OGI magnitudes in our study because the apparent head
midline did not vary significantly from baseline at any of
the acceleration rates.
The efference monitoring hypothesis of Whiteside et al.
(1965) relates OGI to the suppression of a covert
Table 3 Mean head midline displacement, standard errors, and P values
Acceleration rates (°/s2)
2
10
20
30
Head midline displacement (deg)
0.26 (±0.68)
20.89 (±1.17)
20.69 (±1.82)
20.48 (±1.78)
P = 0.37
P = 0.3
P = 0.37
P = 0.32
Standard error in italic
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VAF
A
B
OGI condition
C
Dark condition
1
1
1
0.8
0.8
0.8
0.6
0.6
0.6
0.4
0.4
0.4
0.2
0.2
0.2
Particular
0
0
10
Common
20
Particular
0
30
Suppression data
0
10
Common
20
Acceleration rates
Particular
0
30
0
10
Common
20
30
(°/s2)
Fig. 4 Variance-accounted-for (VAF) between the actual pointer
displacement and the predicted slow phase displacement during the
OGI condition (a), in the dark condition (b) and the suppression of the
slow phase displacement (c). The solid line represents the predictions
based on a particular gain per acceleration rate, and the dashed line
represents the prediction based on a common gain. No residual eye
velocity was found at 28/s2 in OGI condition
nystagmus, with the illusion being dependent on the magnitude of the smooth eye pursuit commands necessary to
stabilize the eyes. There was significant suppression of slow
phase velocity by the presence of fixation target in the OGI
conditions, and it was complete at 2°/s2. However, residual
eye movements in the direction opposite to the rotation
were present at the 10, 20, and 30°/s2 acceleration rates.
The best explanation of the OGI at the different acceleration rates can be obtained by relating the retinal slip
present and the magnitude of suppression of involuntary eye
movements. These results, taken additively, predict the
magnitudes and the time courses of the OGI at the different
acceleration rates. Our linear model with a common gain for
all the acceleration rates predicts the OGI as corresponding
to *10% of slow phase eye displacement in the OGI
condition and *3% of the suppressed slow phase displacement in the OGI condition (the retinal slip minus the
slow phase displacement in the OGI condition). Our results
seem parallel to the data of Lackner and Levine (1979) and
Seizova-Cajic and colleagues (Seizova-Cajic et al. 2006;
Seizova-Cajic and Sachtler 2007) concerning the propriogyral illusion induced by neck muscle vibration, where no
single factor can explain the illusory target displacement.
Clark and Stewart (1969) showed that the angular sensitivity threshold to detect the OGI was lower than that to
detect self-motion, on average 0.11°/s2 vs 1.1°/s2 and that
variability was much less for perception of the OGI. In
other studies, Fluur et al. (1966), Guedry (1965) and
Seemungal et al. (2004) have also found the threshold for
eliciting nystagmus higher than for the OGI and for the
perception of self-rotation. The present study has consequences for experiments that use a head-fixed target to
cancel the VOR in humans (for example, Bloomberg et al.
1988, 1991; Israël et al. 1993; Blouin et al. 1997; Quarck
et al. 2009) and non-human primates (Chowdhury et al.
2009; Takahashi et al. 2007). Spatial constancy has often
been studied using the following paradigm: ‘‘(1) the subject
fixates a central head-fixed target, (2) a peripheral space-
fixed target is briefly flashed, (3) after the peripheral target
is extinguished, the subject is either rotated or translated to
a new position (while maintaining fixation on the headfixed target that moves along with them), and (4) once the
motion ends, the subject makes a saccade to the remembered location of the space-fixed target. Updating ability is
then measured by examining the accuracy of the remembered saccade’’ (Angelaki et al. 2009). Typically, subjects
rotated in yaw are unable to accurately update the target
position (Baker et al. 2003; Blouin et al. 1995a, b). By
contrast, performance is better for roll rotation that
involves both canal and otolith stimulation (Angelaki et al.
2009). Our findings give a possible explanation. In passive
yaw, there may be an illusory displacement of the central
head-fixed target in the direction of body rotation. Thus,
the distance of the fixated target relative to the goal target
would be misjudged and lead to a ‘‘look-back’’ saccade of
inappropriate magnitude.
In conclusion, our results show that at very low acceleration rates, the OGI is closely related to the suppression
of nystagmus and to incomplete suppression coupled with
retinal slip at higher acceleration rates (C*5°/s2). After
constant velocity is achieved, the OGI remains at considerable amplitude even when eye movements are no longer
present or need to be suppressed to maintain target fixation
(e.g., Figs. 2, 4). This pattern suggests that velocity storage
signals also contribute and have different time constants for
affecting visual perception of target location and for driving eye movements.
123
Acknowledgments Research support was provided by US Airforce
Office of Scientific Research grant FA9550 06 1 0102.
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