Disorientation and Postural Ataxia Following Flight
Simulation
ROBERT S. KENNEDY, M.A., Ph.D., KEVIN S. BERBAUM, B.A.,
Ph.D., a n d MICHAEL G. LILIENTHAL
KENNEDY RS, BERBAUMKS, LILIENTHALMG. Disorientation and
postural ataxia f o l l o w i n g f l i g h t simulation. Aviat Space Environ Med
1997; 68:13-7.
Background: Motion sickness-like symptoms can afflict pilots training
in military simulators. This simulator sickness involves symptoms of
gastrointestinal distress, eyestrain and disorientation. A Simulator Sickness Questionnaire (SSQ) with subscales available for each of these
dimensions has been developed to assess the problem. Hypothesis: This
study examined the hypothesis that there is a strong correlation between
the SSQ subscale which summarizes self report of disorientation symptoms and an objective measure of post-simulation postural instability.
Methods: Data from two Navy simulators were analyzed: Device 2F114,
a Weapon Systems Trainer for the A-6E Intruder; and Device 2F143, an
Operational Flight Trainer for the EA-6B. Tests of standing and walking
unsteadiness were administered along with the Simulator Sickness Questionnaire (SSQ). Results: Significant correlations were found between
scores on postural stability tests and the SSQ disorientation subscale
scores, but correlations between scores on postural stability tests and
the SSQ nausea and oculomotor subscale scores were much weaker
and not statistically significant. Conclusions: These results provide some
evidence for the validity of the disorientation subscale of the SSQ and
suggest that the postural instability observed after simulator exposure
may, in fact, result from disorientation.
N THE NAVY'S SURVEY of simulator sickness, incidence from 10 simulator sites between 1980 and 1986
Iranged
from 10-60% (15). In the analysis, "incidence"
was defined as the percentage of exposures reporting
" . . . at least one characteristic motion sickness related
sympton~ (vomiting, retching, increased salivation, nausea, pallor, drowsiness, or sweating), but not accessory
symptoms (e.g., feelings of depression or boredom)" (15,
p. 13). Simulator sickness resembles other forms of motion sickness; however, vomiting is rare and visual symptoms predominate. Like the more classical forms of motion sickness (sea, air, etc.), simulator sickness presents
a complex array of signs and symptoms and is properly
called a syndrome. Of both student and experienced pilots alike, some exhibit all the signs and symptoms of the
syndrome following their simulator exposure whereas
others experience only a few. No single symptom predominates.
A Simulator Sickness Questionnaire (SSQ) has been
developed which provides subscale scores which we hypothesize may be diagnostic of the cause of simulator
sickness in a particular simulator (14). Symptom clusters
were identified by factor analysis. The three distinct
symptom clusters were labelled as: Nausea (N) (nausea,
stomach awareness, increased salivation, burping); OcuAviation, Space, and Environmental Medicine ~ Vol. 68, No. 1 9 January 1997
lomotor (O) (eyestrain, difficulty focusing, blurred vision, headache); and Disorientation (D) (dizziness, vertigo). The existence of three (partially) independent
symptom clusters may indicate that there are separate
physiological mechanisms withfn the human affected by
the simulator exposure. If so, then the subscale scores
provided by SSQ scoring, based on factor analytic models,.may prove useful for diagnostic purposes. A given
simulator may cause symptqms that fall into none, one
or more, or all of these clusters, depending on the mechanism(s) by which the human is affected. Symptom profiles (e.g., excessive report of visual disturbance) may
provide insight for the identification of specific simulator
engineering features that should be targeted for engineering efforts to alleviate the problem.
Postural instability has been documented following
flight simulator training in many (e.g., Kennedy et al.
(10)), but not all, studies (e.g., Hamilton et al. (7)). In the
Navy's survey of simulator sickness, significant decrements in postural stability were observed in all movingbase simulators and one of three fixed-base simulators.
Simulator-induced postural instability which outlasts the
period of exposure may increase the risk associated with
driving or flying, or for balance-critical activities such as
roof repair, bicycling or rock climbing (1,9). Therefore,
such aftereffects have direct implications for safety beyond the obvious effects of the malaise.
This study compared the effects of simulator training
on postural stability and the disorientation subscale of
the Simulator Sickness Questionnaire (SSQ). The immediate goal of this examination was to validate self-report
of disorientation (via the SSQ) with a physiological measure of postural instability. Such a correspondence in the
absence of correlation between postural instability and
the other SSQ subscales would lend support to the notion
that a particular physiological mechanism was involved.
Such a result would encourage us to compare other subFrom the Essex Corporation (R. S. Kennedy); University of Iowa
(K. S. Berbaum); and Naval Medical Research Development Center (M.
G. Lilienthal).
This manuscript was received for review in December 1995. It was
revised in August 1996 and accepted for publication in September 1996.
Address reprint requests to Dr. Robert S. Kennedy, Vice President,
Essex Corporation, 1040 Woodcock Road, Suite 227, Orlando, FL 32803.
Reprint & Copyright 9 by Aerospace Medical Association, Alexandria, VA.
13
DISORIENTATION & ATAXIA--KENNEDY ET AL.
scales with corresponding physiological measures with
the ultimate goal of testing whether there is a physiological basis for the decomposition of the SSQ into subscales.
METHODS
Pilots: The pilots flying these simulators were part of
a replacement air group and were second-tour pilots who
were members of a squadron. They were all experienced
naval aviators who were designated for at least a year
prior to the study. The lowest rank among them was
lieutenant. Their flight hours ranged between 200 and
5600 hours. The pilots who flew these simulators did so
as part of their regular flight training, not for an experiment. They completed our tests as part of their regular
duties and were provided the opportunity to decline
having their data included in the data base; none declined. The pilots included 44 who flew the 2F143 and
27 who flew the 2Fl14.
Simulator characteristics: T h e simulators used in this
study were Device 2Fl14, a Weapon Systems Trainer
for the A-6E Intruder and Device 2F143, an Operational
Flight Trainer for the EA-6B. The A-6E and EA-6B are
essentially the same airframe which fly similar tasks but
for different missions. The A-6E is a bomber aircraft, the
EA-6B is an airborne/surface electronic jamming platform. Both aircraft and simulators have side-by-side
cockpits and fly essentially the same routes at the same
altitudes and airspeed although there are differences in
mission. Types of missions flown include: low level navigation, formation flight, aerial refueling (tanking), carrier
landings, aerobatics, bombing maneuvers, air-to-ground
weapons delivery, emergency procedures, departure
from normal flight (i.e., spins). Altitudes flown range as
high as 10,000 ft and as low as 200-500 ft.
Device 2Fl14: The 2Fl14 has a 24-ft dome which is
necessary to obtain the vertical field of view required
for air-to-ground maneuvers. The image generator is an
Evans & Sutherland ESIG 500 SPX (Salt Lake City, UT)
which operates at 60 hz with an approximate transport
delay of 120 ms (67 ms for visual computation, flight
information updated at 20 hz). An existing Reflectone 6~
of freedom motion base is disabled to accommodate
dome display. It should be stressed that, as the motion
base was disabled, the 2Fl14 was essentially a fixed-base
simulator. Consequently, the nature a n d / o r magnitude
of reported simulator sickness may have been different
from that experienced in a motion-base simulator such
as the 2F143. The device is used by the U.S. Navy for
refresher and tactics training and there is a syllabus for
Medium Attack Readiness.
Device 2F143: The 2F143 has a Redifussion (Great Britain) wide wrap-around visual display that is 180~ (h) •
45~ (v). The image generator is an Evans & Sutherland
SPX 500. The motion base made by Reflectone permits
6~ of freedom and includes an inset buffet platform to
shake the cockpit to produce tremor without shaking
projectors during stalls, and other departures from normal flight (i.e., spins).
This study only reflects the levels of sickness associated with the use of these simulators during a 2-too period in the summer of 1992; both devices have since undergone modification which may have changed the levels and profiles of symptoms they occasion.
14
Simulator Sickness Questionnaire (SSQ): The theory behind scaling motion sickness severity is that vomiting,
the cardinal sign of motion sickness, is ordinarily preceded by a combination of symptoms (18). Wendt (28)
employed a 3-point continuum scale in which vomiting
was rated higher than "nausea without vomiting" which,
in turn, was rated higher than discomfort. Later, Navy
scientists at the U.S. Naval Aerospace Medical Laboratory in Pensacola, FL, tested over 200 aviation personnel
in standardized conditions aboard a slowly rotating
room. Verbal protocols of the pilots' comments about
symptoms they had experienced were collected to form
the basis of a questionnaire. The first version of the Pensacola Motion Sickness Questionnaire (MSQ) was a
checklist of symptoms ordinarily associated with motion
sickness. The MSQ was developed for use in experiments
in the Pensacola Slow Rotation Room (6,11). Later, it was
used in studies of air and sea sickness (12,16,17). The
MSQ was deemed suitable for assessing the polysymptomatic nature of motion sickness--multiple symptoms
were scored because different individuals experience different symptoms. From this checklist, a diagnostic scoring procedure was applied to produce a single, 5-point
scale reflecting overall discomfort.
Unfortunately, the MSQ has limitations for use in
studying simulator sickness. The single global score does
not preserve specific information about the symptoms
which could potentially reveal causes (e.g., visual distortion might cause eyestrain whereas some types of linear
motions might be expected to cause nausea). Also, the
MSQ scoring lacked statistical normalization.
In order to obtain information about the separable dimensions of simulator sickness, more than 1000 Motion
Sickness Questionnaires were factor-analyzed (14). This
resulted in three specific factors and one general factor
which could then be used to develop subscale diagnostic
scoring. The weightings and statistical solutions are described in detail elsewhere (14). Scores on the Nausea
(N) subscale are based on the report of symptoms which
relate to gastrointestinal distress such as nausea, stomach
awareness, salivation, and burping. Scores on the Oculomotor (O) subscale reflect the report of oculomotor-related symptoms such as eyestrain, difficulty focusing,
blurred vision, and headache. Scores on the Disorientation (D) subscale are related to vestibular disarrangement
such as dizziness and vertigo. The subscales are believed
to reflect the sensitivity of different "target" systems in
the human, each of which produces a different kind of
undesirable symptom. In addition to the three subscales,
an overall Total Severity (TS) score, similar in meaning
to the old MSQ score, is obtained. It was also found that
the list of symptoms could be abbreviated to 16 items
without loss in accuracy. A Simulator Sickness Questionnaire (SSQ) was developed based on these 16 symptoms
only. Each SSQ subscale was scaled to have a 0 point of
100 and a standard deviation of 15.
Table ! shows which symptoms are scored in each of
the SSQ subscales. The severity of each of the 16 symptoms listed in the first column are rated by pilots as
"none" which is scored as 0, "slight" which is scored as
1, "moderate" which is scored as 2, or "severe" which
is scored as 3. The subscales, N, O, D, TS, are computed
by summing the ratings of all symptoms that apply and
Aviation, Space, and Environmental Medicine 9 Vol. 68, No. 1 ~ January 1997
DISORIENTATION & ATAXIA--KENNEDY ET AL.
TABLE I. SCORING OF SIMULATOR SICKNESS
QUESTIONNAIRE.
Subscales
Symptom
Nausea
Oculomotor
Disorientation
General discomfort
Fatigue
Headache
Eye Strain
Difficulty focusing
Increased salivation
Sweating
Nausea
Difficulty concentrating
Head fullness
Blurred vision
Dizzy (eyes open)
Dizzy (eyes closed)
Vertigo
Stomach awareness
Burping
X
X
X
X
X
X
X
X
X
X
X
Standing on Non-Preferred Leg (SONL): The procedure
for this test was identical to that of the SOPL test except
that pilots stood on their non-preferred leg. Thoml4y et
al. (25) showed the non-preferred leg score to be the
more reliable. Whereas the preferred leg test was limited
to one trial before and after simulator training in order
to minimize the pilot's testing time (a costly commodity
in these situations), the non-preferred leg test employed
the best three of five trials.
PROCEDURE
X
X
X
X
X
X
X
X
X
X
then multiplying by an appropriate weight. This weight
is 9.54 for N, 13.92 for D, and 7.58 for O. TS is computed
by adding the sums of symptom ratings for N, O, and
D and multiplying by 3.7.
Postural stability tests: The tests of standing steadiness employed in this research were adapted from the 'test battery
developed by Fregly and Graybiel (5). This battery of floor
tests was empirically validated against the Fregly-Graybiel
Rail Test which was itself validated in experiments using
bilateral labyrinthine defectives as subjects, in experiments
with subject-administered alcohol of various dosages, and
in experiments with Coriolis induced stimuli in the Slow
Rotation Room (cf. Fregly, 1974 for a review of this earlier
work) (5). The standing tests do not require the use of special
apparatus, an important consideration because experiments
such as these are expected that they would not interfere
with the operational training environment. Selection of postural tests for the current experiment was guided by the
results of a previous study on the metric properties of floorbased ataxia tests. Thomley, et al. (26) studied the effects of
practice, reliability and factor structure. Their factor analysis
of the postural tests showed a strong, large, general factor
and two ~maller factors which were carried by the walking
and standing tests. Test performance showed some learning,
but the battery otherwise appeared stable over trials. Hamilton et al. (6) also examined the psychometric properties of
ataxia tests. They concluded that, in well-practiced subjects,
the one-leg stand and the Sharpened Romberg were reliable,
but the walking tests had reh'abilities too low for sensitivity
to simulator-reduced ataxia. The postural stability tests used
in this experiment were as follows:
Standing on Preferred Leg (SOPL): This test of standing
steadiness required pilots to first determine which leg
they preferred to stand on. Pilots were asked to stand,
fold their arms against their chest, close their eyes, lift
their non-preferred leg and lay it about two-thirds of the
way up the standing leg's calf. They attempted to remain
in that position for 30 s. If they moved their pivot foot,
moved their raised foot away from their standing leg, or
grossly lost their erect body position, the trial ended and
the time up to that point (in seconds) was recorded as
the score for that trial.
Aviation, Space, and Environmental Medicine 9 VoL 68, No. 1 9 January 1997
All individuals reporting for simulator training at the
selected sites were asked to participate for the duration
of the survey period. The pilots were told that all data
would be confidential and that anyone could have their
data removed from the sample if he or she so desired;
however, no one elected to do so. Immediately before
and after the simulator flight, participants were tested in
the,same way to acquire pre-exposure and post-exposure
measures.
RESULTS
Subjects who reported themselves not in their usual
state of fitness prior to the simulator training session
were excluded from analysis.
Our initial analysis of differences in our measures between the two devices was conducted as a preliminary
step toward combining the data from both devices in
analyses of the relationship of SSQ subscale scores and
postural test scores. The devices did not differ statistically from each other on any of their subscale scores
(nausea: t(69) = -1.00, p = 0.32; oculomotor: t(69) =
-0.76, p = 0.45; disorientation: t(69) = -1.55, p = 0.13).
The two standing tests of postural stability also showed
no significant'difference between the two devices (SOPL:
t(69) = -1.05, p = 0.30; SONL: t(69) = -1.32, p = 0.19).
The measures showed no difference, indicating that we
are generally sampling a single population using data
from the two devices.
Our next analysis combined data from both devices to
form a sample sufficient to reveal relationships between
post-exposure SSQ subscale scores an~d post-exposure
postural stability test scores. Of course, with three SSQ
subscales and two posture tests, there were nine correlations so that a probability correction is needed for the
number of tests (p K (0.05/6) = 0.009). At this corrected
alpha level, only two of the correlations to be performed
were statistically significant: post-simulation disorientation score with standing on non-preferred leg (r =
-0.339, p K 0.004) and post-simulation disorientation
score with standing on preferred leg (r = -0.375, p
0.001). Since the graphs of these two relationships are
virtually identical, only the former is demonstrated in
detail in Fig. 1. (These strong correlations of standing
steadiness with disorientation remain significant in a
rank order correlation.) Correlations of postural tests
with SSQ nausea were near zero; correlations of the
standing steadiness tests with the SSQ oculomotor subscale were not significant even using an uncorrected
alpha. The correlations of SOPL with the nausea and
oculomotor subscales were r = -0.18, p = 0.13 and r =
-0.20, p = 0.09, respectively. The correlations of SONL
15
DISORIENTATION & ATAXIA--KENNEDY ET AL.
35
.
30
+
n=71
=
2 5
r = -.375
p < .001
-
y = 25.3- (.27 * x)
z
~~
m
-
oo
;
~15i-t
10
45
0
i,,~,l,,W,l,,,~ll,,,i,,,~l,,,,i,,,,t,,,,i,,,,i,,,,i,,,,i
O
5
10
15 20
25 30
Disorientation
35
40
45
50
55
Score
Fig. 1. Post-simulation stand on non-preferred leg scores plotted as
a function of post-simulation disorientation score. Dots are data from
the 2F114, crosses are data from the 2F143. Some locations have multiple points.
with the nausea and oculomotor subscales were r =
-0.11, p = 0.37 and r = -0.19, p = 0.11, respectively.
DISCUSSION
The convergence found here of significant correlations
between tests of standing steadiness and the SSQ disorientation subscale following exposure to simulated flight,
coupled with the lack of correlation of steadiness and
the nausea and oculomotor subscales, provides some evidence that the disorientation subscale of the SSQ is registering states (i.e., dizziness, vertigo) that are accompanied by a loss of postural stability (cf. Campbell & Fiske,
1959, for further discussion of the importance of convergent and divergent validation) (2). We are encouraged
by these data as providing partial support for the factor
analytic breakout of the SSQ. For example, perhaps subsequent post-simulation tests of gaze stability (or dark
focus of accommodation) will correspond to scores on
the oculomotor subscale and gastric motility will correspond to scores on the nausea subscale. These hypotheses
will require rigorous testing, but hold an opportunity
for improved understanding of this and other motion
sickness maladies.
The strength of the relationship between SSQ disorientation and postural change and its specificity may seem
somewhat surprising. The SSQ scoring was based on the
use of unit weights on variables identified by varimax
rotation (14). As such, the subscales found are more
highly correlated than would be obtained from hierarchical factor rotation. Measures based on the group factors
with the general factor removed would likely be purer
indicators of causes than those based on the less independent varimax factors. The varimax factors were used because they offer great scale robustness; that is, they are
16
defined in the mathematical sense for the limited set of
symptoms contained in the SSQ.
The specific correspondence between SSQ disorientation and postural instability has implications beyond
supporting the validity of the disorientation subscale.
Diagnostic subscale scoring challenges the notion that
motion sickness is a unitary entity. Kennedy et al. (14)
developed the SSQ subscales based on concordance of
symptoms or "clusters" of symptoms as identified by
factor analysis. Correspondences between objective tests
of different physiological function and SSQ subscales
tend to support the hypothesis that the symptom clusters
each have their own physiological basis. Perhaps total
severity is nothing more than a convenient summary of
the impact of simulator exposure on different target systems within the human. If so, then the mix of the three
types of symptoms produced by a given simulator would
depend on the physiological mechanisms by which the
human is affected. The practical importance of separate
dimensions in simulator sickness is that the methods for
control of symptoms may be different for these dimensions. Evidence that different symptom clusters result
from inter-simulator differences has been reviewed by
Kennedy et al. (13)
The nature of the link between motion sickness and
postural instability has been controversial. Reason and
Brand (24) hypothesized that conflicting inputs from visual and vestibular afferents are responsible for motion
sickness. In a more general form of sensory conflict theory, incompatible percepts in different sensory channels
or a percept incompatible with an expectation produces
motion sickness and postural instability (19,20). A divergent view has been presented by Riccio and Stoffregen
(25) who state: "prolonged postural instability is the
cause of motion-sickness." Whether symptoms associated with motion sickness produce postural instability
or postural instability produces the symptoms remains
in question.
These two views of motion sickness have different interpretations for the postural instability observed after
simulator training. For Riccio and Stoffregen (25), the
adjustment to the simulator is simply to adapt to the
newly presented, optically specified, motion until it has
no effect on postural control. Ataxia experienced after
simulation is the natural consequence of that adaptation
or learning. For sensory conflict theory, the adaptation
may be to the altered correspondence between inertial
and visual motion (27). Postural control adapts to different environments by integrating visual, vestibular and
kinesthetic inputs and changing the influence of each to
fit the circumstance (3). Postural instability would result
from a mix of influences that are appropriate for the
simulation but not the ordinary environment.
Postural instability observed in astronauts upon return
to earth forms an interesting corollary/contrast to postsimulation postural instability. Paloski and his colleagues (22,23) report ataxia following shuttle flights of
greater severity and duration than has been observed
following simulation training. This is not surprising considering the magnitude of change in gravity during
spaceflight and the extended duration of the exposure.
These investigators noted an initial rapid component of
readaptation to terrestrial force which gave way to a
Aviation, Space, and Environmental Medicine ~ Vol. 68, No. 1 9 January 1997
DISORIENTATION & ATAXIA--KENNEDY ET AL.
slower component, each of which accounted for about
half of the recovery of stability. The fast component had
a time constant of about 3 h whereas the slow component
had a time constant of about 100 h. Given that the magnitude of the disruption in stability is so much less following simulator flights than spaceflight, it is possible that
recovery from post-simulation instability also has two
components but only the first is readily apparent. The
longer-term manifestations that have been documented
(1,9) may reflect continued slower component recovery.
Whereas decoupling of visual and vestibular signals
is a condition to be avoided insofar as possible in most
flight simulation, it is the condition which is sought for
the purpose of spaceflight pre-adaptation training (PAT)
(8). The most widely accepted explanation for space sickness and its postural posteffect is the one based on neurosensory recalibration, specifically the otolith tilt-transla-.
tion hypothesis (8,21). The adaptation produced in PAT
involves a new relationship between otolith gravicepter
and visual motion signals that is found in space. Parker
et al. (21), discussing progress in preflight adaptation
training, indicate that assessing the adaptation produced
by the trainer remains uncertain. We believe that by
studying the interrelationships between subscale scoring
of the SSQ and physiological measures of posture and
gaze stability, and autonomic activity, we may be able
to develop more reliable and precise measurements of
the adaptation in ordinary simulators and in PAT. This
will enhance our ability to reduce or intensify their impact as appropriate for training simulators.
ACKNOWLEDGMENTS
This work was sponsored in part by the Naval Air Systems Command, Washington, D.C., under Contract number N00019-92-C-0157;
the National Science Foundation, Washington, D.C., Grant number
DMI-9400189; and NASA, Houston, TX, Contract number NAS9-19106.
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17