Exp Brain Res (2009) 195:335–343
DOI 10.1007/s00221-009-1785-6
R ES EA R C H N O T E
Angular displacement perception modulated by force background
James R. Lackner · Paul DiZio
Received: 6 August 2008 / Accepted: 25 March 2009 / Published online: 19 April 2009
© Springer-Verlag 2009
Abstract We had recumbent subjects (n = 7) indicate the
amplitude of imposed, passive yaw–axis body rotations in
the 0, 1, and 1.8 g background force levels generated during
parabolic Xight maneuvers. The blindfolded subject,
restrained in a cradle, aligned a gravity-neutral pointer with
the subjective vertical while in an initial position and then
tried to keep it aligned with the same external direction during a body rotation, lasting less than 1.5 s about the z-axis
30°, 60°, or 120° in amplitude. All the rotations were above
semicircular threshold levels for eliciting perception of
angular displacement under terrestrial test conditions. In 1
and 1.8 g test conditions, subjects were able to indicate
both the subjective vertical and the amplitude of the body
rotation reasonably accurately. By contrast in 0 g, when
indicating the subjective vertical, they aligned the pointer
with the body midline and kept it nearly aligned with their
midline during the subsequent body tilts. They also
reported feeling supine throughout the 0 g test periods. The
attenuation of apparent self-displacement in 0 g is discussed in terms of (1) a possible failure of integration of
semicircular canal velocity signals, (2) a contribution of
somatosensory pressure and contact cues, and (3) gravicentric versus body-centric reference frames. The signiWcance
of the Wndings for predicting and preventing motion sickness and disorientation in orbital space Xight and in rotating
artiWcial gravity environments is discussed.
J. R. Lackner (&) · P. DiZio
Ashton Graybiel Spatial Orientation Laboratory,
Brandeis University, MS 033, Waltham,
MA 02454-9110, USA
e-mail: lackner@brandeis.edu
P. DiZio
e-mail: dizio@brandeis.edu
Keywords Spatial orientation · Path integration ·
Semicircular canals · Otoliths · Somatosensation ·
Subjective vertical · Gravity
Introduction
Velocity information from semicircular canal signals is a
key component of updating spatial position. Subjects
brieXy rotated about a vertical axis and deprived of visual
and auditory cues about the earth-Wxed environment can
subsequently counterrotate a pointer to their original heading (Guedry et al. 1971), turn themselves back to their original spatial direction with a manual remote control
(Metcalfe and Gresty 1992), or make saccadic eye movements to the pre-turn location of an earth-Wxed target
(Bloomberg et al. 1988, 1991a), with about 85–90% accuracy. Such results show that mathematical integration of a
head angular velocity signal provided by the semicircular
canals is suYcient for perception of angular displacement
or angular path integration (Beritov 1957, 1959; Mittelstaedt and Mittelstaedt 1980).
Normally, angular path integration cooperates with
visual (Loomis et al. 1999), auditory (Clark and Graybiel
1949), otolithic (Graybiel 1952), proprioceptive (Mergner
et al. 1983), and motor (Gordon et al. 1995; Jurgens et al.
1999) signals in control and perception of self-rotation. For
example, body rotation around an oV-vertical axis is
accompanied by information about rate of turn from the
semicircular canals and attitude information from the otolith organs. Understanding how a representation of angular
displacement is derived from semicircular canal signals and
interrelated with otolith and other signals remains a signiWcant challenge (Glasauer 1992; Angelaki and Hess 1995;
Merfeld 1995; Angelaki et al. 1999; Bortolami et al. 2006b;
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336
Kaptein and Van Gisbergen 2006). One illustration of the
complexity of the integration and convergence process is
the fact that removal of vestibular inputs abolishes head
direction cell selectivity even when visual landmarks and
other sensorimotor signals are available (Brown et al. 2002,
2005).
Experiments in weightless environments have provided
several forms of evidence that the processing of semicircular canal signals may be aVected by graviceptive signals.
The earliest evidence came from astronauts participating in
the Skylab M-131 experiment, in which it was shown that
the eVects of Coriolis cross-coupling stimulation (CCS) of
the semicircular canals were highly dependent on background force level (Graybiel et al. 1977). CCS is a mechanical response of the semicircular canals to head movements
made out of the plane of an ongoing constant-velocity body
rotation, and is independent of linear force background, and
on Earth, provokes severe motion sickness and a violent
sense of tumbling. The Skylab astronauts had been susceptible to CCS pre-Xight but experienced no motion sickness
or apparent body tumbling during CCS in orbit. Understanding how to predict and circumvent aversive eVects of
CCS is important because CCS is an unavoidable consequence of using rotation to generate artiWcial gravity. The
M-131 experiment was never performed earlier than six
days after insertion into orbit because of fears that CCS
would be so provocative that the astronauts might not be
able to perform mission-critical activities during the initial
Xight days.
Experiments in parabolic Xight have shown that immediately upon exposure to 0 g CCS evokes virtually no motion
sickness or disorientation and elicits smaller nystagmic
responses than in 1 g (DiZio et al. 1987). In addition, CCS
elicits more severe motion sickness and disorientation in
1.8 g than in 1 g (Lackner and Graybiel 1985). Sudden stop
stimulation following constant velocity rotation in parabolic Xight elicits nystagmus with the same peak slow
phase velocity across 0, 1, and 1.8 g force backgrounds
(DiZio and Lackner 1987). However, slow phase velocity
decays in 0 g at a rate which approximates the allometrically inferred peripheral time constant of the horizontal
semicircular canals. The decay rate of nystagmus is little
aVected in 1.8 g compared to 1 g values. Subjects also
report a shorter duration of apparent self-rotation following
sudden stops in 0 g than in 1.8 and 1 g. It has also been
demonstrated that astronauts manually rotated in roll may
lose their orientation relative to the cabin of the spacecraft
unless vibrotactile reference cues are provided (van Erp and
van Veen 2006).
In this experiment, we investigated the sense of displacement relative to the environment which a subject feels
when being tilted in a normal 1 g force background and in
the hyper-g and weightless phases of parabolic Xight. If
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Exp Brain Res (2009) 195:335–343
canal signals elicited during a passive body tilt are accurately integrated over time, they should provide a veridical
sense of angular displacement in weightlessness where
there is no orientation-dependent variation in otolithic signals. G-related variations in spatial updating would point to
a gravitoinertial force dependency of angular path integration per se, an interaction of integrated canal information
and other graviceptive signals, or the emergence of an alternate orientational frame of reference. Portions of the data
were presented at the 2006 annual meeting of the Society
for Neuroscience (Lackner et al. 2006).
Materials and methods
Subjects
The subjects were seven students and staV of the Graybiel
Laboratory, including one of the authors (JRL). Three were
female and four male; the age range was 24–64 years.
Three were participating in their Wrst week of parabolic
Xights and were tested on the second or third Xight day of
the week; one had participated in six previous Xights, and
three had participated in hundreds of prior Xights. None of
the subjects took anti-motion sickness medications. All the
subjects had passed NASA’s medical requirements for parabolic Xight experiments. The procedure was approved by
the Brandeis University Human Subjects Committee and
the NASA JSC CPHS. All the subjects gave their informed
consent.
Apparatus
The experiment was conducted in NASA’s Boeing KC-135
aircraft used for parabolic Xight studies. The aircraft is
Xown such that the resultant of gravity and inertial forces is
perpendicular to the aircraft deck (Karmali and Shelhamer
2008). Periods of high force, 1.8 g, and of 0 g alternate each
lasting about 20–25 s, separated by force transitions lasting
about 5 s. A complete parabola lasted about one minute.
Sets of 10 consecutive parabolas were separated by periods
of level Xight. The experiment was completed in four consecutive days with Xights of 40 parabolas on each day.
The subjects were tested in a bed-like cradle apparatus in
which they were very snugly nestled with straps and pads.
No attempt was made to place the Frankfort plane precisely
in a vertical orientation, and consequently, all the semicircular canals may have been partially stimulated. The
recumbent subject could be rotated to diVerent positions
about his or her longitudinal axis, i.e., yaw rotation about
the recumbent z axis. The long axis of the apparatus was
positioned parallel to the fuselage of the aircraft, with the
head forward. The cradle could be locked into position at 0°
Exp Brain Res (2009) 195:335–343
337
(supine), and §30° or §60° with a spring-loaded pin that
engaged pre-drilled detents. Positive angles indicate left ear
down tilts in a right-hand coordinate system consistent with
our previous publications (Bortolami et al. 2006a, b; Bryan
et al. 2007). See Fig. 1a. The cradle was equipped with a
pointer stick which subjects could use to indicate diVerent
yaw directions. The pointer was a 20 cm £ 2.5 cm rod pivoting about its midpoint on a shaft parallel to the subject’s
long axis, in the mid-sagittal plane. The pointer axis was
about 20 cm above the torso of the supine subject, and its
rostral–caudal position could be adjusted for comfort. The
subject grasped both ends of the pointer with one hand at
each end. The pointer had a knob on one end to provide
polarity but otherwise it was devoid of tactile orientational
cues. It was gravity neutral so that there was no pendant
position. The angles of the pointer and of the subject’s head
and torso relative to the gravitoinertial vertical (or perpendicular to the fuselage deck in 0 g) were monitored with a
Polhemus Fastrak device at 30 Hz. Before every session,
the tilt sensors were calibrated by recording their output
while the bed was placed in the Wve positions.
To attenuate/mask ambient spatial auditory cues, the
subjects wore earplugs (Howard MaxLite: noise reduction
(from 33.5 db at 125 Hz to 45.2 db at 8,000 Hz) and noise
cancelling (29 dB passive plus 20 dB active noise reduction) Telex Stratus 50-D earphones through which pink
noise was played. The noise level was adjusted to be as
high as the subject could comfortably tolerate through the
earplugs. The experimenter voice channel, which could
interrupt the noise when necessary, was adjusted to be loud
enough to be heard through the ear plugs. Ground-based
pilot experiments indicated subjects utilizing this system
could not localize an external speaker playing back the
recorded cabin sounds of a previous parabolic Xight at a
sound level of 90 dB at the subject’s head. In 0 g, the
engines are throttled back, and the ambient noise level is
about 75 dB.
Testing was conducted in straight and level Xight as well as
in the parabolas. Each Xight consisted of 40 parabolas,
Xown in four sets of 10 separated by periods of straightand-level Xight. Each subject was scheduled to be tested
during 20 parabolas. Subjects were changed in the break
between sets 2 and 3, and 1 g data were collected in
straight-and-level Xight in the breaks between sets 1 and 2
and 3 and 4 as well as before set 1 and after set 4. One of
the seven subjects became motion sick and only completed
ten parabolas of the scheduled 20. He was replaced by
another subject for the remaining ten parabolas. The
remaining six subjects each completed 20 full parabolas.
Each experimental trial involved rotating the recumbent
subject to a new position either in 0 or 1.8 g and having the
subject indicate the subjective vertical and then continue to
indicate that position for the entire duration of the turning
maneuver. The experimenter initiated trials by waiting Wve
sec after a force transition was complete and watching a
computer display of the g level (all three axes) to make sure
it had settled at the desired magnitude. At this point, data
collection was triggered for 15 s, and the subject was asked
to align the pointer stick with the subjective vertical before
the onset of a repositioning turn which would be forthcoming within 5 s. A computer-generated tone cued the experimenter to manually execute the scheduled turn at the
appropriate time. Turns were accomplished by releasing a
locking pin, manually turning the bed, and locking it in the
new position. The whole maneuver took less than 2 s. The
subject’s task was to keep the joystick aligned with the
same spatial direction throughout the turn. The instructions
were, “use gravity as a reference when it is available, and
imagine a constant spatial location in microgravity”. After
the turn was completed and the subject had been given a
chance to make quick Wnal corrections, the apparatus was
moved to the scheduled starting position for the next turn.
(b)
stick
angle (+)
physical
vertical
head
midline
LED
120
0g
1g
1.8 g
Head
Stick
0
-120
RED
Velocity (deg/sec)
head
angle (+)
Position (deg)
(a)
Flight procedure
120
1 sec
0
- 120
Fig. 1 a Schematic of conventions used to measure head and stick
angles relative to space. Positive angles refer to left ear down (LED)
tilt. b Time series of head (dotted traces) and joystick (solid traces)
rotation relative to space during typical trials in diVerent force
backgrounds. The arrows mark the points where initial and Wnal head
and stick positions were measured to compute displacements. Trials
with diVerent tilt amplitudes, directions, and positional ranges are
illustrated in diVerent force backgrounds
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Exp Brain Res (2009) 195:335–343
The displacements included magnitudes of 30°, 60°, and
120° to the right and left, starting and ending at one of the
Wve positions in which the bed could be locked—30° and
60° left and right—and 0° (subject horizontal). Each 20
parabola session included 18 turns in 0 g and 18 in 1.8 g
(with two parabolas of rest), with six displacements of each
magnitude, half to the left and half to the right. The three
tilts for each combination of amplitude and direction were
chosen randomly from the permutations presented in
Table 1.
Manual bed rotation
The traces of Fig. 1b indicate that the manually executed
tilts of the bed had quasi-sinusoidal velocity proWles. The
average durations of the 30°, 60°, and 120° turns were
0.76 s, 1.07 s, and 1.54 s, respectively. The median velocities were 42°/s, 44°/s, and 53°/s for turn amplitudes of 30°,
60°, and 120°. Angular acceleration was computed with a
2-point diVerence algorithm. The median acceleration noise
when the body was stationary was 17°/s2, and acceleration
exceeded the median noise 84%, 88%, and 91% of the time
during turns of 30°, 60°, and 120° amplitude, respectively.
The durations of the 120° amplitude turns averaged 1.51 s
and 1.56 s in 0 and 1.8 g, respectively. The peak velocities
of the 120° amplitude turns averaged 58°/s and 50°/s in 0
and 1.8 g, respectively. Neither of these diVerences was
signiWcant.
Data reduction
Before processing, all the raw data were calibrated, Wltered
(5 Hz low pass, 5th order Butterworth), diVerentiated (2
point diVerence), and Wltered again (5 Hz low pass). The
beginning and end of the head motion was identiWed with
algorithms that identiWed peak head angular velocity and
then searched, backward and forward, for the points where
velocity fell below 5% of the absolute value of the peak.
The beginning of each individual trial was deWned as the
onset of head motion, and the end of the trial was deWned as
1 sec after the end of head motion (see arrows in Fig. 1b).
At the deWned endpoint, stick motion was always complete.
The RMS diVerence between the head and torso tilt signals
Fig. 2 a Plot of Wnal stick displacement versus recumbent yaw–axis 䉴
head displacement. Subjects were attempting to continuously align the
stick with the subjective vertical in the diVerent force backgrounds.
The horizontal dashed line indicates a constant orientation of the stick
to the spatial vertical and the diagonal dashed line indicate a constant
stick position relative to the body. b Plot of RMS stick displacement
versus head displacement. c Plot of subjective vertical versus head angle at the end of each trial. The horizontal dashed line corresponds to
perfect indication of the vertical, and positive sloping functions correspond to bias of pointing responses toward the body midline (diagonal
dashed line)
from the beginning to end of trials averaged 0.854° and did
not diVer signiWcantly across g levels. Therefore, only the
head motion signal was used for subsequent analysis. Typical traces of head and stick motion relative to space are
shown in Fig. 1b for each force background. The three
examples also depict 30°, 60°, and 120° displacements of
the body with diVerent initial and Wnal tilt angles.
Two measures were extracted to determine how well the
subjects maintained the stick spatially stationary during
body displacements. As a measure of Wnal stick stability in
space, we computed the diVerence in spatial stick position
from the beginning to the end of the trial. However, this
measure would not identify response lags, subsequent
catch-up movements, and Wnal retrospective adjustments
that were allowed after the cradle stopped moving. To capture such dynamics of compensatory stick movements, we
also computed the RMS stick displacement relative to the
head throughout the trial. These two measures are plotted
against head displacement relative to space in Fig. 2a and b.
We also measured the static subjective vertical by comparing the body (head) position and stick setting relative to the
vertical at the end of the trial (see Fig. 2c).
Comparison of 1 g ground-based and Xight data
Each subject was tested on the ground both before and after
the parabolic Xight tests with the same procedure and
sequence of tilt amplitudes/directions as they received during the 1 g periods of level Xight. A repeated measures
MANOVA of all the dependent measures showed no eVects
of test repetition, and subsequent pairwise comparisons at
each tilt amplitude/direction showed no diVerences between
the 1 g Xight data and the combined pre- and post-Xight
Table 1 The set of movements from which displacements of diVerent magnitude were selected
Displacement magnitude
Start to End position
123
+30°
¡30°
+60°
¡60°
+120°
¡120°
¡60 to 60
60 to ¡60
¡60 to ¡30
60 to 30
¡60 to 0
60 to 0
¡30 to 0
30 to 0
¡30 to 30
30 to ¡30
0 to 30
0 to ¡30
0 to 60
0 to ¡60
30 to 60
¡30 to ¡60
Exp Brain Res (2009) 195:335–343
Results
LED 120
0g
90
1g
Stick displacement re space
(deg)
(a)
339
Stick displacement during head tilt
1.8 g
60
30
-0
-30
-60
-90
RED -120
-120 -90 -60 -30 -0
RED
30 60 90 120
LED
Head displacement re space (deg)
(b)
0g
RMS stick displacement re body
(deg)
90
1g
1.8 g
60
30
0
-120 -90 -60 -30 -0
RED
30 60 90 120
LED
Head displacement re space (deg)
(c)
LED 60
0g
Subjective vertical
(deg)
1g
1.8 g
30
0
-30
RED -60
-60
RED
-30
0
30
60
LED
Head angle (deg)
data (Bonferoni-corrected t tests, critical P = 0.0083,
power = 0.812 at least). Therefore, subsequent analyses
compared only the 1 g level Xight condition to the 0 and
1.8 g Xight conditions.
When subjects were tilted to a new angle in the 0 g phase
of a parabola, the pointer and head displacement traces
showed parallel deXections (see Fig. 1b, left panel).
Between the beginning and end of body tilts, the body
and stick pointer excursions were almost equal (see
Fig. 2a). In other words, the subjects did not move the
pointer relative to their body during angular displacements of the body in 0 g, which is reXected in the low
RMS deviation of the pointer relative to the body (see
Fig. 2b). When each tilting trial was over and for the rest
of the duration of the 0 g portion of the parabolas,
subjects held the pointer nearly aligned with their body
midline, so that the pointer orientation was almost the
same as the body tilt (see Fig. 2c).
By contrast, when subjects were tilted in 1 or 1.8 g,
there was a transient period in which the pointer moved
with the body, but after a short reaction time, subjects
started compensating and kept the stick nearly perfectly
stationary relative to the vertical (see Fig. 1b, center and
right panels). The total displacement of the pointer relative to space during body turns was only about 10–20% of
body displacement in 1 and 1.8 g (see Fig. 2a) because
subjects made large compensatory movements of the
pointer relative to their bodies as they attempted to maintain a constant pointing position in space in 1 and 1.8 g
(see Fig. 2b).
A repeated measures, two way analysis of variance
(SPSS v16) was performed to assess the eVects of g level
(0, 1 and 1.8 g) and tilt magnitude on pointer displacement relative to space during body tilts. It revealed a
signiWcant eVect of tilt angle (F(5,30) = 51.7, P < 0.001)
and an interaction of tilt angle and g level (F(10,60) = 62.1,
P < 0.0001). Pairwise analyses (Bonferoni corrected
t tests, critical P = 0.0083) indicated that the spatial stick
displacements at each of the six body-displacement magnitudes were greater in 0 g than in 1 g. Linear regression
analyses showed that a straight line was a signiWcant Wt to
stick displacement as a function of body displacement in
each force background (P < 0.01, at least; r2 > 0.978 at
least). In 0 g, the slope of stick displacement relative to
body displacement was 0.82, and in 1 g and 1.8 g the
slopes were 0.21 and 0.13, respectively. The conWdence
interval of the slope of the 0 g function was non-overlapping with both the 1 g and 1.8 g slopes. The conWdence
intervals of 1 and 1.8 g slopes were also non-overlapping. These analyses indicate that subjects’ self-displacement estimates were about 18% of their actual
displacements in 0 g, about 79% in 1 g, and about 87%
in 1.8 g.
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340
Role of experience in angular displacement estimates
Stick displacement amplitudes during 120° turns (average
of the absolute values for both directions) for the four subjects who had experienced six or fewer previous parabolic
Xights were compared to the estimates of the three subjects
with greater than 200 Xights. Separate non-directional,
independent groups t tests were performed for the 0 and
1.8 g conditions, and no signiWcant diVerences were found
(minimum power = 0.71). In addition, related groups t tests
including all subjects showed no diVerence in displacement
estimates of 120° turns between the Wrst and last Wve parabolas, in 0 and 1.8 g (minimum power = 0.81).
Static subjective vertical
Static subjective vertical settings were slightly biased in the
direction of body tilt in 1 and 1.8 g. In 0 g, subjects localized the subjective vertical almost in line with the midline
of their body. See Fig. 2c. A repeated two way analysis of
variance measures revealed a signiWcant eVect of tilt angle
(F(4,24) = 48.8, P < 0.0001) and an interaction of tilt angle
and g level (F(8,48) = 66.1, P < 0.0001). Pairwise analyses
(Bonferoni-corrected t tests, critical P = 0.0125) indicated
that the spatial stick displacements at the ¡60°, ¡30°, 30°,
and 60° body tilts were greater in 0 g than in 1 g. Linear
regression analyses showed that a straight line was a signiWcant Wt to stick displacement as a function of body displacement in each force background (P < 0.01, at least;
r2 > 0.955 at least). In 0 g, the slope of stick displacement
relative to body displacement was 0.882, and in 1 and 1.8 g
the slopes were 0.164 and 0.153, respectively. The conWdence interval of the slope of the 0 g function encompassed
a slope of 1 but was non-overlapping with both the 1 and
1.8 g slopes. The 1 and 1.8 g slopes had overlapping conWdence intervals. These analyses indicate that subjective vertical was aligned with the body midline in 0 g and was
biased about 15% in the direction of body tilt in 1 and 1.8 g.
Subjective reports
When subjects were stationary, pre-positioned in tilted
positions, and during transitions in background force level
from 1.8 to 0 g, they all reported displacement from a tilted
to a horizontal position. When they were pre-tilted during
transitions out of 0 g, they experienced the reverse. The
perceptual transitions due to changes in force background
were always completed before onset of the experimental
body tilts. During body tilts in 1 and 1.8 g, all the subjects
experienced self-displacement, and at the end of the turn,
they experienced a diVerent static orientation than before.
During body tilts in 0 g, two subjects denied ever experiencing any self-displacement, although they experienced a
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Exp Brain Res (2009) 195:335–343
brief “push” or “tug” in the direction of the physical displacement. The remaining Wve estimated the spatial extent
of their displacements in 0 g to be 5–20% of their displacements in 1 and 1.8 g. The durations of 0 g displacements
were also estimated to be less than 20% of the duration of
turns in 1 and 1.8 g, with their onset coinciding with a sensation of pressure cues on the body from the cradle.
Discussion
Subjects’ pointing responses vastly undercompensated for
recumbent yaw displacements in 0 g and compensated
slightly but signiWcantly better in 1.8 g than in 1 g. The
attenuated pointing responses in 0 g were consistent with
the subjective reports which greatly underestimated actual
self-displacement. The pointing responses and subjective
reports indicated that subjects felt like they were in an
almost constant supine orientation in 0 g but had a fairly
accurate perception of their turn amplitude and the direction of the vertical in 1 and 1.8 g.
Thresholds for angular acceleration in the human have
been reported to be as low as 0.035°/s2 and as high as 4°/s2;
typical values are about 0.5–1.0°/s2 (Fitzpatrick and
McCloskey 1994; Grabherr et al. 2008). In all force backgrounds, the rotations in our test conditions involved angular accelerations that were much greater than these values.
As a consequence, signiWcant above-threshold activation of
horizontal canal aVerents must have been achieved in all
our test trials. Thus, the diminished appreciation of self-displacement in 0 g could not have been due to insuYcient
semicircular canal stimulation.
During body rotations in 0 g, the semicircular canals
were activated, but because the otoliths and somatosensory
mechanoreceptors were unloaded no static orientationdependent shearing occurred. During vertical axis rotations
in 1 g, the graviceptors are not unloaded but their output is
unchanging and canal signals are suYcient to yield a sense
of angular displacement. (Guedry et al. 1971; Bloomberg
et al. 1991b; Metcalfe and Gresty 1992). Thus, one interpretation of our Wnding of decreased updating of spatial
position during recumbent yaw rotation in 0 g relative to
1 g and 1.8 g is that the temporal integration of canal velocity signals to generate apparent spatial displacement of the
body is nearly lost when the otoliths and somatosensory
mechanoreceptors are unloaded in 0 g. This is consistent
with subjective reports of attenuated or complete absence
of apparent self-rotation in 0 g.
In the present experiment, subjects always felt horizontal
when being tilted in 0 g. This replicates our previous Wnding that subjects always feel horizontal when statically
placed in any recumbent yaw orientation in 0 g (Bryan
et al. 2007). In both situations, subjects were Wrmly nestled
Exp Brain Res (2009) 195:335–343
in the cradle apparatus with symmetric touch and pressure
cues on their back and front and left and right sides regardless of their tilt angle in 0 g. The static, symmetric distribution of somatosensory stimulation may have been adequate
to make them feel horizontal and keep the pointer aligned
with their midsagittal plane. A transient asymmetric pattern
of touch-and-pressure cues on the body was present while
the body was undergoing angular acceleration and deceleration in 0 g, and these cues may have contributed to transient stick motion in the direction opposite to rotation and
the small reported body displacements. Thus, a second
interpretation of the decreased updating of spatial position
during recumbent yaw rotation in 0 g is that an unchanging
somatosensory “vertical” derived from evenly distributed
pressure cues overrode any sense of displacement that
might have been derived from integration of canal velocity
signals and transient somatosensory or otolith signals.
The methodology we used also permits a third interpretation of the results. We asked subjects to “use gravity as a
reference when it is available, and imagine a constant spatial location in microgravity.” It is possible that the inability
to use gravity as a reference in 0 g might have been confusing and caused the subjects to switch to a body-centric
frame of reference after the completion of the turn. The
attenuated displacement compensations seen in 0 g in
Fig. 2a, however, do not reXect a spatial compensation during the bed turn followed by a retrospective drift back to a
body-centric axis in the period allowed for Wnal adjustments after the bed stopped moving. If this had happened in
0 g, the RMS values would have been increased in 0 g relative to 1 and 1.8 g, but Fig. 2b shows this not to be the case.
The perceptual reports favor the elimination of semicircular canal signal integration in 0 g over the alternatives of
an overriding of an integrated canal signal by symmetric
somatosensory signals or of switching to an egocentric
frame of reference. When we asked our Wrst subject (in the
middle of his test session) why he did not move the pointer
in 0 g, he reported that he did not experience any body displacement. Subsequent subjects were briefed to pay attention to their self-displacement (although the pointing
response was still primary), and all reported no or greatly
attenuated displacement in 0 g relative to the other force
backgrounds. No subject reported a paradoxical sense of
body displacement in the absence of a change in apparent
direction of the vertical, which we would expect if an unimpaired canal-derived displacement signal had been overridden by an unchanging somatosensory derivation of the
vertical. However, additional studies will be required to
establish whether the 0 g attenuation of spatial updating is
due entirely to graviceptive unloading or is partially inXuenced by haptic contact cues or reliance on an egocentric
frame of reference. We are currently assessing apparent
angular self-displacement during upright and recumbent
341
yaw–axis rotations in hyper- and hypo-g force backgrounds
using a method which is independent of reference to gravitational or egocentric reference frames.
The small improvement we found in spatial updating in
1.8 g relative to 1 g provides insight into how a representation of angular displacement derived from integrated semicircular canal signals might merge with otolith and other
graviceptive signals. Estimates of the subjective vertical
during static recumbent yaw tilts are the same in both 1 and
1.8 g (Bryan et al. 2007), which is not the case for roll and
pitch tilts which show greater errors in judging the vertical
in hyper g than in 1 g (Correia et al. 1968). Thus, estimates
of recumbent yaw displacement would be expected to have
equivalent contributions from graviceptive otolith and
somatosensory cues in 1 g and hyper-g environments. In
addition to these equivalent, direct graviceptive attitude signals, there may be in 1 g an additional contribution from
integrated canal signals to computation of the dynamic subjective visual vertical (Kaptein and Van Gisbergen 2006).
The present Wndings also have signiWcance for physiological studies of spatial perception. Place cells in the hippocampus (O’Keefe et al. 1975) and head direction cells in
the anterior-dorsal thalamic nucleus (Taube 1995) and the
primate pre-subiculum (Robertson et al. 1999) code an animal’s spatial position and head direction in relation to its
environment. These cells are updated during changes in
body position even in the absence of visual landmarks.
Integration of vestibular signals is necessary for this process (Taube and Burton 1995). The selectivity of rat hippocampal place cells has been found to be disrupted in orbital
Xight although maps can reform to some extent (Knierim
et al. 2000). Head direction cells in the anterior dorsal thalamus also lose their direction-speciWcity when a rat climbs
the walls or the ceiling of its cage in 0 g (Taube 1998;
Taube et al. 2004). Aberrant head direction cell activity
also occurs during inverted locomotion on the cage ceiling
in 1 g (Calton and Taube 2005), which may provide a 1 g
paradigm for comparing the roles of static graviceptive
cues in angular path integration in humans and animals.
The present results are also consistent with the Skylab
and parabolic Xight experiments evaluating the eVects of
CCS in 0 g because in all the cases, there is a powerful
semicircular canal stimulus which is not registered as a spatial displacement. The M-131 motion sickness results are
often attributed to the lack of an intravestibular, canal-otolith conXict in 0 g (Guedry and Benson 1978); however,
this explanation would predict an increased magnitude and
duration of tumbling sensation elicited by CCS but the
actual result was a complete absence of apparent tumbling.
Our parabolic Xight experiments in which perceptual
reports of tumbling were the primary task of subjects conWrmed that CCS in 0 g evokes both briefer and attenuated
body tumbling than in 1 and 1.8 g, as well as a nearly
123
342
complete abolition of motion sickness (DiZio and Lackner
1989, 1995). Failure of integration of canal signals in 0 g or
of their incorporation in the downstream processing could
account for suppression of motion sickness and apparent
tumbling elicited by CCS.
An important question is what level of graviceptive input
is necessary to achieve spatial updating. In ongoing experiments, we are Wnding that the 0.38 g level of Martian gravity is not likely to be adequate because preliminary results
are showing exposure to CCS at 0.38 g to be comparable to
exposure in 0 g. This is practically important because it
implies that a rotating artiWcial gravity environment that
produces 0.38 g or less of static gravitoinertial force will
not elicit motion sickness or disorientation during head
movements despite the presence of CCS. However, attenuated perception of angular self-displacement could also
contribute to spatial disorientation in non-rotating, 0 g
space Xight operations. For example, astronauts might
underestimate the amplitude of spacecraft reorientation
maneuvers they are monitoring or controlling manually or
in collaboration with autonomous systems. Designing the
best countermeasures will require understanding the mechanisms of self-displacement perception.
Acknowledgments Air Force OYce of ScientiWc Research grant
F49620-01-10171, NASA grant NAG9-1466.
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