Exp Brain Res (2000) 130:2–26
© Springer-Verlag 2000
R E V I E W A RT I C L E
James R. Lackner · Paul DiZio
Human orientation and movement control in weightless
and artificial gravity environments
Received: 21 May 1999 / Accepted: 25 May 1999
Abstract Our goal is to summarize what has been
learned from studies of human movement and orientation control in weightless conditions. An understanding
of the physics of weightlessness is essential to appreciate
the dramatic consequences of the absence of continuous
contact forces on orientation and posture. Eye, head,
arm, leg, and whole body movements are discussed, but
only experiments whose results seem relatively incontrovertible are included. Emphasis is placed on distinguishing between virtually immediate adaptive compensations
to weightlessness and those with longer time courses.
The limitations and difficulties of performing experiments in weightless conditions are highlighted. We stress
that when astronauts and cosmonauts return from extended space flight they do so with both physical “plant”
and neural “controller” structurally and functionally altered. Recent developments in adapting humans to artificial gravity conditions are discussed as a way of maintaining sensory-motor and structural integrity in extended missions involving transitions between different force
environments.
Key words Weightlessness · Movement control ·
Adaptation · Orientation · Artificial gravity
Introduction
As plans were being made in the early 1960s for the first
manned space flights, there was great concern about
what effects weightlessness would have on human physiological and psychological function. These concerns included fears of cardiovascular collapse, gastrointestinal
malfunction, muscular discoordination, disorientation,
panic reactions, oculomotor impairments, and sensations
J.R. Lackner (✉) · P. DiZio
Ashton Graybiel Spatial Orientation Laboratory, MS033
Brandeis University, Waltham MA 02454-9110, USA
e-mail: lackner@brandeis.edu
Tel.: +1-781-7362033, Fax: +1-781-7362031
of continuous falling1. Perhaps the most remarkable aspect of human exposure to weightlessness for brief periods, numbered in days, is the relative paucity of severe
side effects. The most obvious adverse consequence experienced by astronauts and cosmonauts is space motion
sickness. This puzzling phenomenon is one consequence
of space travel that was not anticipated. Another unanticipated effect is the severe mal de debarquement occurring after re-entry and landing, the re-entry disturbances
that along with space motion sickness are collectively
called the space adaptation syndrome.
In space-related research, much emphasis has been
placed on vestibular and oculomotor function because of
their inter-relationship with space motion sickness. On
earth, individuals without functioning otoliths are insusceptible to motion sickness (Graybiel and Johnson 1963)
and, because motion sickness emerged as the predominant problem of short-term space flight, it was natural to
study vestibular function in weightlessness. However, as
will be discussed, vestibular changes during short-term
exposure to weightlessness are relatively subtle. Thresholds for angular acceleration change little if at all and
linear acceleration thresholds are inconsistently modified. The gain of the peripheral canal response is not affected during exposures of days or several weeks. However, “velocity storage” of slow-phase vestibular and optokinetic nystagmus velocity is immediately attenuated
in weightless conditions, and post-rotary head movements do not suppress post-rotary nystagmus. This pattern points to alterations in central rather than peripheral
vestibular processing. Saccadic eye movements appear
unaffected in weightlessness but pursuit movements, especially vertical pursuit, can be greatly disrupted.
Predictably, otolith-dependent effects are especially
affected by weightlessness; otolith spinal and H-reflexes
are attenuated. Tonic vibration reflexes, which indicate
muscle spindle gain are also attenuated. Decreased spindle gain – which could reflect both otolith influences and
1
Comments by John Glenn in a lecture to the NASA-NIA conference on Spaceflight and Aging, Washington DC, January, 1997.
3
mechanical unloading of the body – affects the control
and perception of head and limb position. Re-calibration
of spindle activity in relation to movement control will
be shown to be an important aspect of adapting to
weightless conditions and a contributing factor in postflight re-entry disturbances. Alterations in bone and
muscle structure, in motoneuron properties, and perhaps
in brain functional organization also occur during longer
duration missions.
In this review, we emphasize the importance of contact forces and of altered sensory-motor control of the
body as key elements influencing orientation and movement in novel force environments and in giving rise to
re-entry disturbances. Little attention is usually given to
these factors because they are largely perceptually transparent to us. We do not perceive in their true magnitudes
the forces acting on our bodies when they are due to
gravity or our self-generated movements. It is primarily
during transitions between force backgrounds, prior to
full sensory-motor adaptation being achieved to the new
force context, that we are aware of the changed contact
forces and the new background force. However, some
contact forces, such as light, non-mechanically supportive finger-tip contact with a stable surface and simple
presence or absence of directional contact cues, enable
us to maintain postural and movement control across different force environments. We generally remain unaware
of the existence of these cues. Nevertheless, they have
powerful influences on perceived orientation, and the
nervous system seems to use them to make rapid and automatic adjustments of motor output that preserve spatial
patterns of posture and movement in novel force environments. This point will be made again in the section
on using artificial gravity to maintain sensory-motor and
bone and muscle structural integrity during very long duration missions.
The physics of weightlessness
and the importance of contact forces
The weightless conditions of orbital flight are often referred to as 0 g or microgravity conditions2. The otolith
organs of the inner ear – which are linear acceleration
sensitive, and gravity is a linear acceleration – are the
sensory organs most obviously influenced by “microgravity conditions”. This, along with space motion sickness, is why vestibular function has been the focus of so
many space-related experiments. A brief consideration
of the physics of weightlessness will make it easier to
understand the physical situation present in orbital flight
and why there has been such emphasis on the otolith organs. Under normal conditions on earth, the force of
earth gravity accelerates objects, including ourselves,
down toward the surface (center) of the earth. This
2
In this paper, the symbol g (with italics) is a constant representing the acceleration of earth’s gravity at sea level. The symbol g
(without italics) is a variable representing gravitational acceleration in general.
downward acceleration is resisted by the surface on
which we are standing or supported. It is the contact
force acting against gravity that a scale measures as
weight. Contact forces are essential to allow locomotion
to take place both in terms of and vertical jumps, walking and running, the latter requiring frictional contact
forces as well so that the feet do not slip3. Buoyant hydrodynamic and aerodynamic forces are the analogous
forces for aquatic and aerial locomotion and orientation.
The otolith organs of the inner ear can provide orientation dependent signals only when there are contact
forces acting on the body surface. For example, when we
are standing upright on earth, the contact forces of support on our feet oppose the action of gravity, allowing
our musculoskeletal system to support our body and
keep it from buckling to the ground under the action of
gravity. The support of the head on the spinal column allows the otolith organs to provide signals related to head
orientation because the macular plate is supported
against gravity by the head. In this circumstance, the otoconial mass under the influence of gravity generates
shear and compression forces on the macular membrane
causing deformation of cilia (which resist the shear and
compression forces), thereby generating the head-orientation-dependent otolith output (Wilson and Melvill
Jones 1979; Young 1984), as shown in Fig. 1A. The role
of the otolith system as an orientation reference is thus
dependent on the grounding of the body to the environment by means of a chain of mechanical contact forces
that oppose the gravitoinertial acceleration (vector product of linear gravitational and linear inertial accelerations). This chain is absent in free fall.
There are three primary techniques for achieving significant periods of effective weightlessness. These include parabolic flight maneuvers in an aircraft and orbital and interplanetary space flights. Parabolic flight maneuvers typically create alternating periods of weightlessness and of high force level (about 1.8–2.0 g), each
lasting 20–30 s, separated by transitions in force level.
Usually, 30 to 40 parabolas are flown in order to generate multiple periods of weightlessness sufficient for experiments to be conducted. The key to producing weightlessness in parabolic flight is making the resultant of the
lift, drag, and thrust forces on the aircraft equal to zero.
The situation is illustrated in Fig. 1B. By contrast, in
straight and level flight at constant velocity, the sum of
the lift, drag, and thrust forces are precisely opposite the
gravitational force, mg, acting on the aircraft (m=vehicle
mass). Parabolic flight takes place in the earth’s atmosphere usually at altitudes between 15,000 feet and
35,000 feet. Consequently, the gravitational attraction of
earth on the aircraft is nearly 1 g. Weightlessness is generated in parabolic maneuvers because a state of free fall
3 Astronauts bound on the moon because normal walking or running is not possible. The frictional contact force available to support forward locomotion is only one-sixth that on earth because it
is proportional to the coefficient of friction times the normal
force provided by gravity. Moon gravity is one-sixth that of earth
gravity.
4
Fig. 1 Schematic illustration of the forces on an individual at rest
in (A) a normal 1 g terrestrial environment, (B) the free-fall phase
of parabolic flight, and (C) orbital flight. The presence or absence
of a continuous contact force on the feet (solid arrows) is the most
consequential physical difference between the normal and flight
environments; the presence or absence of non-contacting gravitoinertial force (broken arrows) does not distinguish parabolic flight
and orbital flight from terrestrial conditions. When the contact
force is present, a chain of orientation-specific stresses and strains
exist on the body surface and in internal tissue that deform mechanoreceptors, including otolithic cilia. Without the contact force, no
deformation of the body surface or of internal tissue occurs regardless of body orientation
is achieved such that the aircraft and its contents are falling at the same rate under the action of earth gravity.
Therefore, there are no mechanical forces of support exerted by the aircraft on its contents and occupants.
In orbital flight about the earth, it is the force of earth
gravity that keeps the spacecraft moving in its orbital
path. To be in orbit, the vehicle’s forward motion has to
be deflected by a centripetal force, causing it to move in
a curvilinear path. Gravitational attraction between the
space vehicle and the earth provides this force. In orbit,
the centripetal force, mv2/r equals g, where r is the distance from the spacecraft to the center of the earth, m is
the mass of the spacecraft, and v is the linear velocity of
the vehicle. The strength of earth’s gravitational attraction varies with distance (r) from the center of the earth
according to (re2/r2)g, where g=earth gravity at sea level,
approximately 9.8 m/s2; re=radius of the earth, about
6.38×106 m. The acceleration level of earth gravity, g,
on a spacecraft and its contents for a circular orbit
200 miles (3.22×105 m) above the earth’s surface is approximately 8.86 m/s2. This is nearly 90% of earth gravity at sea level – clearly not zero or microgravity. The
physical situation rather is one of near zero contact force
levels exerted by the spacecraft on its contents and inhabitants – all are in a state of free fall or orbit around
the earth (Fig. 1C).
On earth, contact forces are always present on the
body except for brief moments during running, jumps, or
falls. An awake animal has postural tonus that allows it
to maintain an attitude or posture in relation to the acceleration of gravity. We do not have to think about or concentrate on maintaining an attitude in relation to gravity;
the nervous system does it for us at a non-conscious level of integrated activity, as Sherrington and others demonstrated long ago. In the absence of tonus, the body is
limp and disjointed, hence the difficulty in trying to carry someone who is unconscious. By contrast, in a free
fall or weightless situation, tonus is not essential to the
same extent for maintaining orientation or attitude because contact forces are not necessary to maintain a body
configuration. (It would be no trouble to “carry” someone who is unconscious in free fall because the entire
body and its parts free float.) Control of configuration is
determined by the overall balance of muscle forces acting on the head, limbs, and torso. The relaxed position in
free fall is one of slight trunk and leg flexion (Thornton
et al. 1977). When activities are undertaken, a posture
and orientation can be maintained such as when operating a console.
In weightless conditions, the otolith organs can only
provide information about transient accelerations and
cannot encode the dc component of head position. When
contact forces are present on the body, such as on earth
or in an accelerating spacecraft, the dc component will
be modulated by head orientation. Neither the otolith organs nor any other type of linear accelerometer will be
able to distinguish whether the acceleration is gravitational or inertial. This is the essence of Einstein’s equivalence principle (Rothman 1989). An important question
is how the output of the otolith organs is interpreted by
the nervous system during exposure to weightlessness
both in terms of static signals and transients generated by
head and body movements. Equally important is how
non-vestibular sensory-motor control mechanisms respond to the altered contact forces on the body surface
and between body articulations.
Spatial orientation
Gravity plays a major role in spatial orientation on earth.
Down is the direction in which there are contact forces
of support on the body surface opposing the acceleration
of gravity. The otolith organs also provide information
about head orientation with respect to the gravitoinertial
5
force vector; under static conditions, this corresponds to
head orientation vis a vis gravity. The viscera may also
provide directional information by activating interoceptive elements (Mittelstaedt 1997). Contact forces on the
body surface contribute as well to a broad range of postural maintenance and righting reflexes (Magnus 1924;
Roberts 1978). In principle, virtually any segment of the
body, e.g., arm or leg or the torso, could be used as a linear accelerometer to gauge the direction of gravity by
sensing in what body-relative orientation the torque necessary to support it against gravity is maximal (or minimal).
In the weightless conditions of orbital flight, the
spacecraft and its occupants are in free fall so there are
no contact forces of support on an astronaut’s body opposing the action of gravity. This means that there are no
gravity-determined tactile cues related to body orientation and no gravity-determined otolith cues about head
orientation. The re-distribution of body fluid and rostral
shift of viscera that occur in the absence of hydrostatic
pressure in the circulatory system would be more in accord with being prone or supine on earth (Vernikos
1996).
Orientation illusions
Many aspects of our environments including ourselves
are “gravitationally polarized”. Trees have tops and people have heads and feet and so on. Artificial structures
and objects are also polarized in relation to gravity – for
instance, rooms have floors and ceilings, tables have
tops. Spacecraft are also architecturally polarized in
terms of an “up” and a “down”, by having a floor and
ceiling, and equipment and test apparatus that are all oriented accordingly. It is important to recognize that on
earth we only view our normal terrestrial environment
from a limited range of perspectives (Lackner 1992a,
1992b; Lackner and DiZio 1998a). For example, when
we walk into a room we see it and its contents from a
“viewing platform” at the elevation of our head; we
don’t see it from ceiling level (unless we climb a ladder
or chair) or from floor level. Moreover, we can only enter from doors or other access points. The key insight is
that we have only certain canonical perspectives from
which we survey and learn our surroundings.
Spaceflight violates many of the regularities that
characterize our orientation on the ground. There no longer are tactile contact cues to provide information about
the orientational down direction. One can assume virtually any position or perspective in the craft, e.g., free
floating facing the deck. Regions of the spacecraft can
be entered in unusual ways, such as by floating through
the top or bottom of an entranceway while in different
orientations relative to the craft than previously experienced or that are even possible on the ground. New developments in virtual environment technology are making similar potentials available for “traveling” in and
learning virtual environments (Durlach and Mavor
1995). One can explore virtual environments from viewing perspectives not possible in real ones. Moreover, one
can “enter” a virtual environment from any location
within it, not just through doors or portals or particular
access routes as in real environments. This can give rise
to orientation illusions and sensations of unfamiliarity
and eeriness similar to those reported by astronauts and
cosmonauts (Lackner and DiZio 1998a). Virtual environments thus provide a way of exploring some of the visual
and cognitive factors that affect orientation illusions in
space flight, although there is not an effective way of
mimicking the absence of contact support stimulation associated with weightlessness.
Sensations of inversion are common in space flight.
Titov, in the second Soviet mission, reported feeling upside down and found head movements to be disorienting
(Titov and Caidin 1962). Since this early report, illusions
of inversion, tilt and virtually every combination of body
orientation and vehicle orientation have been reported.
No correlation has been seen between such reports and
the incidence of space motion sickness (Kornilova
1997). With increased flight duration, such illusions
which can be experienced immediately on transition into
weightlessness tend to abate. Many personal reports have
been collected by having astronauts and cosmonauts, at
the end of their work day, dictate their recollections into
a tape recorder while perusing a questionnaire about experienced orientations (Oman 1988; Oman et al. 1990).
Such reports suggest that there are two general categories of individuals: those who come to rely on the visual
verticals of the spacecraft to gauge their body orientation
and those who rely on the location of their feet for the
direction of down. The former feel upright when they are
aligned with the architectural verticals of the spacecraft
with their head toward the “ceiling”, the latter feel upright regardless of their orientation to the spacecraft.
Systematic studies in the free fall phase of parabolic
flight have shown that various patterns of orientation illusions can occur on entry into weightlessness (Fig. 2);
the patterns experienced depend on whether vision is
permitted and what tactile cues are present on the body
surface (Lackner and Graybiel 1983; Lackner 1992a,
1992b; Lackner and DiZio 1993). Blindfolded subjects if
strapped tightly in a seat by a lap belt generally feel inverted, suspended from the belt. Those strapped in and
allowed full sight of their surroundings may feel upside
down in an upside down aircraft, right-side up in an inverted aircraft, or inverted in an upright aircraft. With
continued exposure, most subjects, when permitted sight
of the aircraft, eventually come to perceive themselves
as upright in an upright aircraft. However, when blindfolded, the tactile cues tend to continue to dominate and
they will feel inverted. Attempts have been made to relate inversion illusions to an “ideotropic vector” that reflects the degree and direction to which otolith saccular
function, integrated over directional polarizations, is biased. A negative bias would predict a sense of inversion
in free fall conditions (Mittelstaedt 1989; Mittelstaedt
and Glasauer 1993a, 1993b). This hypothesis needs to be
6
Fig. 2 Subjects who are free floating typically experience illusory
changes in self- and aircraft orientation if they see their bodies totally separated from the deck of the aircraft. Between A and B, the
free-floating subject redirects his gaze (arrows) foot-ward. The
tail section of the aircraft, which in B is “below” the feet, is interpreted as the floor and, on seeing his feet separated from the
“floor”, the subject experiences the aircraft and himself as inverted. Between A and C, the subject is blindfolded and given a light
contact cue (hand icon) on top of his head. The contact is perceived as coming from the substrate of support, and the subject
feels head down
extended to account for the different varieties of inversion illusions experienced (all combinations of experienced self and aircraft orientations) and their changing
character over time, including in many cases total or
near total abatement.
Astronauts participating in space flight experiments
that produced a sustained linear acceleration gradient did
not perceive it as a vertical reference (Benson et al.
1997). In one flight, four astronauts were accelerated at
20°/s2 to 120°/s pitch or roll rotation about their thorax.
Angular acceleration stimulated the semicircular canals
and produced centripetal and tangential accelerations of
the whole body. After about 30 s at 120°/s rotation, the
semicircular canal activation and tangential accelerations
were gone and just a stable centripetal force gradient was
left, 0.22 g head-ward acceleration at the otoliths, 0 g at
the thorax which was over the rotation axis, and 0.36 g
foot-ward at the feet. None of the astronauts experienced
a change in orientation in darkness during either the ramp
up or at constant velocity. In pre-flight tests with the
same rotations about a vertical axis, three of the four astronauts had reported self-tilt relative to the resultant of
gravity and centripetal acceleration at the otoliths. If otolith stimulation also governed orientation in space, then
the subjects would have felt inverted during constant ve-
locity rotation. However, the experiences in space seem
more in line with the near zero integral of signals from
the somatic graviceptors distributed over the whole body
in a roughly symmetrical acceleration field.
Parabolic flight experiments have also shown that individuals who are free floating with eyes closed may
lose all sense of spatial anchoring to their surroundings
(Lackner and Graybiel 1979). Intellectually, they know
where they are and what their position is in relation to
their surroundings, but they do not experience an orientation with respect to the environment. The sense of spatial position is lost although a sense of relative body configuration is preserved. As soon as somatosensory stimulation is provided by contact with familiar parts of the
environment, a sense of orientation is restored. Reports
from space flights indicate similar experiences in orbital
flight (Schmitt and Reid 1985).
Cognitive as well as visual factors influence orientation in weightless conditions. Viewing one’s body in relation to the deck of the craft in ways that would be
physically impossible on earth unless one were artificially suspended can lead to orientation illusions: changes in
gaze can also lead to changes in experienced orientation
(Fig. 2). The transition from experiencing one body orientation to another is virtually always one of gradually
fading out of the experienced orientation and then feeling more and more compellingly in the new orientation
(Lackner and Graybiel 1983; Lackner 1992a, 1992b). A
physical rotation or spatial displacement of the body
from one orientation to the next is not experienced. This
is likely because semicircular canal, otolith, and tactile
signals that would be associated with a physical change
in body orientation are absent.
Visuo-vestibular interactions in weightlessness
Attempts have been made to gauge the relative importance of visual and tactile cues for orientation in free fall
and to examine visuo-vestibular interactions (Young et
al. 1986, 1993; Young and Shelhamer 1990). Thresholds
of the otolith organs to linear acceleration have also been
measured pre-, per-, and post-flight using linear sleds,
and will be discussed under Vestibuloocular responses.
On earth, rotating visual arrays presented in the frontal
plane to a stationary supine subject can induce full 360°
apparent body rotation about the axis of fixation. By
contrast, when the subject is upright, only a limited extent of apparent roll displacement is induced. With the
subject supine, the input from the otolith organs would
be compatible with full 360° body displacement; but,
with the subject upright, it is not and is thought as a consequence to suppress the magnitude of apparent displacement (Young et al. 1975). In space flight, similar
rotating frontal plane stimulation has been used to induce apparent body rotation (Young and Shelhamer
1990). One might expect it to elicit responses similar to
those on earth with the subject supine because, in each
case, the otolith organ output would be unaffected by
7
1996; Young and Shelhamer 1990). These observations
further emphasize the importance of tactile stimulation
for providing orientation cues in weightless environments. The processing of tactile cues may change as astronauts adapt to space flight, where contact with surfaces does not correlate with a gravitational vertical.
Absence of sensations of falling in weightlessness
Fig. 3 Illustration of visually induced illusory self-rotation in roll
under weightless conditions. The visual stimulus is a hemisphere
covered with randomly spaced dots. The subject (solid outline figure) keeps his optic axis aligned with the visual rotation axis by
clenching a bite board or grasping handles, while letting his feet
float. When the stimulus rotates clockwise (solid arrow), the subject experiences counterclockwise self-displacement (open arrow)
to an angle of displacement seldom greater than 90° (dashed outline figure) with a continued sense of self-motion. Actual angular
displacements of 360° (dotted outline figures) would involve collisions with environmental barriers
constant velocity, physical rotation in roll about the axis
of visual rotation (Fig. 3). Nevertheless, astronauts rarely
report full 360° displacement, but rather limited displacement and a continuing sense of motion. This pattern
corresponds to what is experienced on earth with the
subject upright, limited positional displacement with a
persisting sense of motion. This outcome likely relates to
the type of stimuli that have been used, random visual
patterns that are not spatially polarized. Under groundbased conditions, rotating naturalistic visual stimuli with
architecturally polarized ups and downs can induce 360°
apparent rotation in roll in standing and seated test subjects (Howard and Childerson 1994). It is likely they
would do so in space flight as well, since they have now
been found to be effective in the weightless phases of
parabolic flight (Cheung et al. 1996). It is necessary to
use stimuli that are spatially informative with regard to
relative position. The random dot patterns typically used
in space flight experiments lack this property. Cognitive
factors may also limit the range of experienced body motion in space flight. For example, apparent displacement
in roll may be inhibited if the subject is tested in a confined space (as is usually the case in flight experiments)
such that actual body rotation about the head would lead
to the legs bumping into objects.
Several space flight and parabolic flight studies indicate that the apparent displacement and motion of the
body induced by roll visual stimulation can be partially
suppressed by tactile cues on the feet generated by bungee cord loading of the body (Young et al. 1984, 1986,
Being weightless in orbital flight is a situation that from
the standpoint of the otolith organs and the absence of
contact forces on the body surface might be expected to
evoke sensations of falling and displacement through
space. For example, when we fall out of a tree, until impact with the ground, the stimulation of the otolith organs and somatosensory receptors will be similar to that
in orbital flight. Reports of astronauts experiencing sensations of falling and displacing through space are virtually non-existent. One astronaut (Storey Musgrave, personal communication) has reported that he had been puzzled by this discrepancy and tried to find how he could
make himself feel as if he were falling when in orbital
flight. He was able to do this by closing his eyes and
imagining that he had jumped off a cliff and could see
himself moving in relation to visual objects. This elicited
stunningly intense sensations of falling. On earth, the
same sensations could not be evoked by visualization.
Such considerations suggest that there are a range of
cognitive and visual factors influencing the sense of falling. On earth, during falling, there is usually sudden loss
of support, awareness of loss of support and of impending danger, and movement of the body in relation to a
stable visual environment so that visual displacement
cues are present. In an enclosed elevator, the sense of
body motion and displacement occurs primarily during
stops and starts. By contrast, in a glass-walled elevator,
the sense of motion and displacement is continuous
throughout the actual motion. The transitions to free fall
in orbital flight and in the weightless phase of parabolic
flight are relatively gradual and the individual is within
an enclosed chamber with a stable visual field. These
factors are likely important in suppressing a sense of
falling. Visual situations that would elicit height vertigo
and protective reactions against falling on earth, e.g., being above the “floor” without any restraining contact
forces on the body, do not have similar effects in orbital
or parabolic flight (Lackner 1992c). The key factor here
may be the absence of a tendency of the body to displace
in relation to the craft, such as would be the case on
earth. In space flight, the craft and its occupants are all
moving together in the same path or trajectory.
In conclusion, the sense of orientation in free fall is
influenced primarily by visual and contact cues. In their
absence, astronauts do not feel disoriented but can feel
non-oriented. The structural polarity of the visual scene
in terms of an architectural “up” or “down” is of particular significance, indicating that cognitive factors play a
role.
8
Posture and locomotion
Controlling posture on earth and in weightless conditions
involves very different constraints. On earth, to maintain
static upright balance, the center of mass of the body
must be kept (except for momentary excursions) above
the support area of the feet or the body will topple. In addition, the relative configuration of the different body
segments must be regulated to prevent collapse of the
body under the action of gravity. All body movements
that affect the static and dynamic position of the center
of mass must be preceded or accompanied by adjustments of other segments to maintain balance. Reaction
torques generated by limb and head and torso movements must be coordinated with compensatory adjustments of other musculature to maintain the desired configuration of the body (Nashner and Cordo 1981; Cordo
and Nashner 1982). This kinetic chain of torques is finally “grounded” by reaction torques at the feet. The muscle
innervation patterns necessary to produce particular body
relative movements depend on body orientation to gravity. For example, when touching the toes from a standing
position, flexion of the torso is achieved by controlled
lengthening of dorsal musculature; when doing a sit-up
from a recumbent position, ventral muscles strain to
raise the torso against the action of gravity. This orientation-dependent modulation of the torques necessary to
move and support the body is characteristic of all movements made in our natural terrestrial environment.
In weightless conditions, the situation is very different. There no longer are effective gravitational torques
on the body segments (the entire body is in free fall).
Consequently, the notion of posture takes on a different
meaning, one of maintenance of a particular body configuration or of assuming a particular orientation in relation to the spatial layout of the vehicle. In this circumstance, the relaxed body configuration will be determined by the relative tonus of the skeletal muscles.
Moreover, there will not be otolith spinal reflexes that
differentially modulate the antigravity musculature depending on head orientation such as is the case on earth.
Maintaining a particular attitude in relation to the craft
requires holding on or having some form of attachment.
Anticipatory postural compensations
for voluntary movements
On earth, when a standing subject raises his or her arm
rapidly, innervations of leg muscles precede the arm raising and compensate appropriately for the impending reaction torques and change in center of mass of the body
(Nashner and Cordo 1981; Cordo and Nashner 1982).
This nicely stabilizes balance and posture. Several experiments have explored what types of anticipatory compensations are made for limb and trunk movements when
cosmonauts are in an anchored stance with their feet attached to the space craft deck. Arm-raising maneuvers
have been studied in this anchored stance (Clément et al.
1984, 1985). Early in a mission, compensatory innervations of the leg muscles are present during rapid arm raises, even though the anchored feet absorb the dynamic reaction thrust and compensation for a change in final arm
posture is functionally unnecessary because of the
weightless conditions. With additional time in flight,
compensation for the shift in center of mass during arm
raising becomes eliminated by reducing the associated
activation of the leg flexors, soleus, and gastrocnemius.
This reflects an adaptation to the weightless condition, in
which center of mass location is no longer relevant for
“stance”. Kingma et al. (1999a) calculated that controlling the center of mass would be biomechanically advantageous in a lifting task done in weightlessness. They
found in parabolic flight experiments that subjects with
their feet anchored while bending and lifting an object
change their joint angle trajectories as early as the second trial to compensate for an abnormal backward shift
of the center of mass on the first trial.
Rapid flexion and extension movements of the trunk
under terrestrial conditions must be accompanied by
backward and forward displacements of the hips and
knees for balance to be preserved. In space flight, with
feet anchored, similar trunk movements are accompanied
by corresponding movements of the hips and knees with
similar kinematics (Massion 1992; Massion et al. 1993).
These patterns are present during the first in-flight tests
made and are significant because they reflect a considerable reorganization of motor control to preserve terrestrial kinematic patterns of complex synergies. The goal of
the motor adjustments could be to preserve synergies either in terms of relative configurations of body parts or
in terms of posture and movement relative to external
surroundings, such as the spacecraft cabin. Pozzo et al.
(1995) found that joint angles are changed more than
head and hand paths in a space shuttle experiment when
crew members lifted a box with their whole body while
their feet were anchored. This pattern implies that motor
control adjustments in orbit are geared to preserve the
external spatial coordinates of terrestrial movement trajectories. Preserving axial synergies in free fall involves
generating muscle innervation patterns that are greatly
different from those on earth owing to the absence of effective gravity torques. The parabolic flight study of
Kingma et al. (1999a), cited above, indicates that some
postural changes seen in space flight testing that first begins hours or days after insertion into orbit may actually
reflect rapid adaptation requiring only a small number of
attempted movements with appropriate knowledge of results.
The time course of postural changes in space flight
may be affected by various factors. For example, anchored quiet stance shows changes over time in space
flight (Clément et al. 1984). Initially, the basic posture
and angle of the body assumed in relation to the stance
surface are similar to those exhibited on earth. Later in a
mission, if vision is denied, a more pitched forward posture is maintained relative to the attachment surface.
This forward displacement has been attributed to a rela-
9
tive shift in the balance of extensor and flexor activity.
However, it could also relate to decreases in strength and
alterations in structural properties of the antigravity musculature that occur with prolonged exposure to weightlessness.
Making motor compensations aimed at preserving kinematic synergies requires accurate monitoring of one’s
movements in the relevant spatial reference frame. Individuals exposed to alterations in background force level
in parabolic flight are able to control their static head
and body postures and their limb movements surprisingly well when their feet are anchored and sight of the aircraft is permitted (Amblard et al. 1997). For example,
the head can be maintained in a constant roll orientation
relative to the aircraft during voluntary lateral trunk
movements made with eyes closed. An extended learning period is not necessary – performance is very good
on the very first parabola, indicating that dynamic vestibular and other kinesthetic signals are successful in
preserving an orientation framework for the head. This
had been anticipated by Graybiel et al. (1967) who
showed that Gemini astronauts wearing goggles that displayed only a collimated luminous line could set it parallel to an unseen spatial referent – an instrument panel –
in the space capsule.
H-reflex and otolith-spinal reflexes are attenuated
in weightlessness
The excitability of spinal cord alpha motoneurons is
modified in space flight as shown by changes in the Hreflex, which is elicited by stimulating the popliteal
nerve electrically and recording the latency and magnitude of the EMG response of the gastrocnemius muscle.
The H-reflex is under otolith-spinal influence and is augmented during brief drops on earth in which a suspended
subject is released to fall a short distance (Reschke et al.
1984). A normal H-reflex response is seen early in space
flight when “drops” are produced by bungee cord accelerations of the body. However, by the seventh day of
flight, acceleration-induced modulation is no longer seen
and, immediately upon return to earth, there is a potentiation of drop-related H-reflex modulation (Reschke et al.
1986). Otolith-spinal reflexes induced by bungee cord
accelerations have also been measured in space flight
and show a lower amplitude initially relative to preflight, then still further declines during the course of a
mission (Watt et al. 1986, 1989). These observations are
consistent with the changes in tonic vibration responses
of the leg muscles that occur in-flight (see Limb proprioception section). Overall, both the arm and leg movement data are in keeping with a decreased vestibulo-spinal influence on alpha and gamma motoneuron control,
and active re-mappings of this relationship over time.
Sensory-motor adaptation to altered body weight
Changes in the perception of self-motion and of the apparent stability of the immediate environment occur on
exposure to increases or decreases in background force
level relative to 1 g. Subjects who raise and lower their
body in deep knee-bend maneuvers in parabolic flight
misperceive their motion and simultaneously perceive
the aircraft to move as they move (Lackner and Graybiel
1981). The illusory motions have opposite patterns for
movements made in less than 1 g and those made in
greater than 1 g force backgrounds. In less than 1 g,
downward body motions are perceived as being abnormally slow and the aircraft feels and visually is seen to
move downward at the same time. In 1.8 g, the downward movements are experienced as being too rapid and,
simultaneously, the aircraft is felt and seen to move upward.
This pattern is a consequence of the associated changes in effective body weight for the motor control of the
body in altered g levels. Muscle spindle discharge level
in skeletal muscle is correlated with muscle length and
rate of change of muscle length and is centrally interpreted in relation to the intended movement and orientation
of the body. When a deep knee bend is made in a less
than 1 g force level, the weight of the body is less than
normal. Therefore, during lowering of the body, the antigravity muscles that are undergoing eccentric contraction
will lengthen more slowly than for a lowering movement
of the body in 1 g. As a consequence, the rate of change
of muscle spindle activity in the antigravity muscles will
be abnormally low during the course of the movement.
Such depressed activity is interpreted as the muscles undergoing slower lengthening than they actually are and is
referred to the joints controlled by the muscles (Matthews 1981, 1988). Decreased extension rate is centrally
interpreted as the knees, ankles, and hips being less
flexed than they actually are, and this is attributed to the
support surface moving down under the feet. Importantly, the deep knee bend illusion is abolished if the hand is
kept in light, non-supportive contact with the aircraft fuselage at a fairly constant force level (Lackner and DiZio
1993). Thus, the orientation system (1) seems to make
predictions about how commanded actions will displace
the body relative to the support surface and (2) uses nonload bearing contact information to confirm the achieved
displacement.
When the hand is not used as a guide, adaptation
gradually eliminates the illusion if repeated deep knee
bends are made in the low or high force phases of parabolic flight maneuvers. Self-motion perception progressively becomes more accurate and the aircraft is again
perceived to be stable under the feet. This phenomenon
has been described in detail because it represents an
important aspect of the re-entry disturbances experienced by astronauts following space flight, and similar
effects occur with the arms. Figure 4 compares the time
course of the deep knee bend illusion in parabolic flight
to the time courses of a sample of in-flight postural
10
Fig. 4 Alterations in posture and postural control in 0 g, orbital
flight and in 1.8 g parabolic flight. The most common finding
from orbital flight experiments is an absence of a change from the
1 g baseline initially followed by gradual divergence from baseline, in some cases toward hypo- and in other cases hyper-function; this pattern suggests the existence of immediate compensation mechanisms, which have received little attention. An exception is the aberrant perception of self- and aircraft motion when
subjects first move about in either the low or high force phases of
parabolic flight. With repeated exposure, these illusions abate,
suggesting re-calibration of central nervous system internal models of the relationship between willed actions and body movement
relative to the environment. ––– Ankle angle in static anchored
posture in 0 g, orbital flight (Clement et al. 1985); – · · – · postural
compensation for arm movements in 0 g, orbital flight (Massion et
al. 1992); –·–·– H-reflex in 0 g, orbital flight (Reschke et al.
1984); ······· otolith-spinal reflex in 0 g, orbital flight (Watt et al.
1986); – – – – deep knee bend illusion in parabolic flight (Lackner
and Graybiel 1981)
changes. The fact that such illusions do not occur when
deep knee bends are made on earth while bearing substantial loads indicates that these loads are taken into
account in determining the relationship between body
movement, efferent commands, and associated feedback.
Influence of touch on postural control
The importance of touch of the hand in postural control
has recently been shown in a range of experiments
(Holden et al. 1994; Jeka and Lackner 1994, 1995a,
1995b; Jeka et al. 1996). Labyrinthine-defective subjects
who cannot stand heel to toe for more than a few seconds with their eyes closed without falling can balance
as stably as normal subjects when allowed hand contact
at mechanically non-supportive force levels with a stable
surface (Lackner et al. 1999). Light touch can also override the destabilizing consequences of mechanical vibration of leg muscles (Lackner et al. 1996). Studies carried
out in parabolic flight (illustrated in Fig. 5) show that
subjects standing with anchored feet are much more stable when making deep knee bends at steady state 0 g or
1.8 g acceleration levels if allowed light touch of their
Fig. 5 A Distance that subjects voluntarily lower themselves during deep knee bends in parabolic flight with and without precision
contact, for one subject lacking labyrinthine function (open symbols) and four controls. B Range of fore-aft head movement when
the body descends. The touch cue does not prevent the body from
descending further in 1.8 g than 0 g, but it helps all subjects maintain a narrower range of fore-aft motion, especially in 0 g
hand with a stable surface (DiZio et al., unpublished observations).
Limb proprioception
The perception of limb position is not determined by
sensory input alone (Matthews 1981, 1988). Sensory signals from spindle receptors within the muscles controlling the limbs, and possibly also from joint receptor endings and Golgi tendon organs, are decoded in relation to
patterns of alpha and gamma motoneuronal activity.
Mechanisms must also exist for updating the calibration
of position sense, and make use of tactile and visual
feedback. Under terrestrial conditions, head orientation
in relation to the gravitoinertial resultant modulates
muscle spindle sensitivity through otolith spinal mechanisms acting on the anti-gravity musculature of the body
(Wilson and Melvill Jones 1979). There are many anecdotal reports that limb proprioception is affected by exposure to weightlessness. Astronauts and cosmonauts
have reported that on awakening in the dark they may
not feel where their arms are, or if they see a luminous
watch dial they may not immediately realize that it is on
their wrist (Schmitt and Reid 1985).
Tonic vibration reflexes and control of anchored stance
Proprioception in weightless conditions has been studied
in two ways: (1) by eliciting tonic vibration reflexes in
arm or leg muscles and determining their effects on arm
11
position or anchored posture and (2) by studying the
ability of subjects to reproduce particular kinds of practiced arm movements. Tonic vibration reflexes are elicited by mechanically vibrating a muscle with a physiotherapy vibrator to activate the muscle spindle receptors,
which in turn excite the muscle via their 1a and 2b afferent fibers to the spinal cord. Tonic vibration reflexes
show immediate g-related effects in parabolic flight, being diminished in weightlessness and enhanced in 1.8 g
(Lackner and DiZio 1992; Lackner et al. 1992). This implies that muscle spindle sensitivity is diminished in 0 g.
A decrease in gamma motoneuron activity resulting from
altered otolith-spinal influences would be one way to
achieve this lower spindle response gain.
It is likely that leg movement control is similarly affected. In space flight, cosmonauts tested in anchored
stance without vision initially exhibit a backward sway
when their soleus-gastrocnemius muscles are vibrated bilaterally (Roll et al. 1993, 1998). By the seventh in-flight
day, this effect is absent and apparently does not recur
until the third post-flight day. In addition, the illusory
changes in posture that are initially elicited by leg muscle vibration when vision is denied change in character
over time. At first, exaggerated forward body tilt is experienced; on later flight days, a change in foot angle relative to a stationary body will be experienced. Thus, central reinterpretations of muscle spindle activity and of
postural control are taking place with continued exposure to weightlessness.
Arm movements and object manipulation
Subjects trained to make rhythmical unconstrained forearm movements of a particular amplitude at several different speeds and in horizontal and vertical planes show systematic kinematic differences during exposure to variations in gravitoinertial force level in parabolic flight (Fisk
et al. 1993). Movements in 0 g, regardless of arm orientation, are of smaller amplitude and have more frequent dynamic overshoots of final position than 1 g movements.
By contrast, movements in 1.8 g have larger amplitude and
fewer dynamic overshoots than 1 g movements. If allowed
visual feedback of arm position, subjects can achieve accurate control. These findings are consistent with a decrease in muscle spindle gain in 0 g and an increase in
1.8 g relative to 1 g baseline. A decreased spindle gain
would also account for the impairments in perception of
arm position reported by astronauts when they do not have
sight of their limbs. Astronauts who point to targets immediately after closing their eyes to prevent visual feedback
about their movements show diminished accuracy relative
to 1 g baseline, again consistent with diminished position
sense (Watt 1997). Bock et al. (1992) found similar degradation of visually open loop pointing in the weightless
phase of parabolic flight, and they concluded that alterations in proprioception were responsible.
Manipulating objects and using tools are quintessential
aspects of limb movement control. Subjects even in their
very first exposure to altered force levels have no difficulties in holding or manipulating objects indicating that
automatic adjustments of grasp forces, such as occurs on
earth, are not seriously affected by background force level. This may be because the fingers are sensitive to microslips of a grasped object and rapid adjustments of grip
force are automatically made based on internal models of
the motor apparatus and the held object (Johansson 1991;
Flanagan and Wing 1997). In a parabolic flight experiment, in which subjects were to raise an 8-kg box from
the floor with their whole body, they spontateously exerted nine times less force when weightless than on the
ground (Kingma et al. 1999b). Without this adjustment,
but instead they rose more slowly than normal in 0 g. The
new lifting speed and force were adopted on the very first
0 g trial and remained constant across trials, although
subjects were permitted vision so this could represent visual regulation.
Experiments evaluating how discrimination of the
“heaviness” of hefted objects is affected by background
force level show performance decrements in weightless
conditions (Ross et al. 1984, 1986a, 1986b). Difference
discrimination thresholds are increased nearly twofold. If
the hefting frequency is increased, resolution improves.
This is predictable because rapid arm movements are
less dependent on spindle feedback for their accurate execution than slow movements, and they have also been
found to be less affected than slow ones by exposure to
alterations in background force level (Fisk et al. 1993).
Consequently, errors in movement execution likely influence the perception of heaviness for slow hefting in 0 g
and relate back to alterations in spindle control.
Recently, the haptic judgment of an (unseen) object’s
length has been shown to be affected by background
force level (Kunkler-Peck et al., unpublished observations). Subjects wielding unseen rods of different lengths
and using a visual marker to indicate rod length show
small but systematic changes as a function of background force level. Rods are perceived as shorter in 0 g
and longer in 1.8 g relative to 1 g settings. On earth, perception of rod length is influence by the object’s inertia
tensor, which depends only on the mass distribution of
the object, not its weight (Turvey 1996). If the inertia
tensor were accurately resolved across different force
levels, the apparent length of a hefted rod should remain
constant regardless of background force. Small disparities between achieved and intended arm movements dependent on force level, undershoots in 0 g and overshoots in 1.8 g, would produce systematic errors in judgments of the inertia tensor and predict the reported
length differences actually occurring in 0 g and 1.8 g. As
discussed above, precisely such changes in arm movement control occur (Fisk et al. 1993).
In summary, spindle gain attenuations in weightlessness affect position sense, arm and leg movement control, judgments of object heaviness and mass, and the
perception of object length. The influence is relatively
small but highly systematic and consistent. Visual feedback can eliminate errors when sight of the acting limb
12
is allowed. Grip force adjustments are made appropriately without conscious awareness.
for quite long periods in orbital flight, and fatigue is certainly a complication in post-flight assessments of
thresholds and vestibulo-ocular reflexes.
Vestibular thresholds and vestibulo-ocular reflexes
Vestibulo-ocular responses
Thresholds for angular and linear acceleration
Thresholds for angular acceleration detection were first
assessed in the Skylab missions, with the oculogyral illusion being used as an indicator of semicircular canal activation (Graybiel et al. 1977). This illusion, the apparent
displacement of a head-fixed visual target relative to the
observer, has a much lower threshold than that for perception of body rotation. Four of the eight astronauts
participating showed no change relative to ground-based
control tests; four showed modest elevations. In general,
there was no evidence for significant changes in canal
thresholds.
Absolute thresholds for the perception of linear acceleration have been measured systematically for all three
primary axes using a space sled, designed for the Space
Lab missions, that could deliver controlled accelerations
to astronauts positioned in different orientations relative
to the sled track (Arrott and Young 1986; Benson et al.
1986; Young et al. 1986; Arrott et al. 1990). Detection
thresholds were found to be elevated in some astronauts
and lowered in others for some axes, relative to groundbased control observations. Post-flight tests showed similar variability. Another measure of linear acceleration
sensitivity, the time elapsed from acceleration onset to
reports of self-motion (which varies inversely with magnitude of acceleration) has been more consistent. This
velocity constant (analogous to Block’s law in visual
psychophysics) seems to be elevated for the z axis and
lowered for the x and y axes. Consistent with this, astronauts on landing day are poorer than pre-flight at nulling
out pseudo-random, roll-axis motion without vision
(Merfeld 1996). Neurophysiological asymmetries in otolithic response properties could be the source of this pattern (Fernandez and Goldberg 1976). The saccular receptor plates, which are roughly parallel with the z-axis of
the head, seem less sensitive than the utricular receptors
to linear acceleration.
In interpreting thresholds for angular and linear acceleration in weightless conditions, it is very difficult to
rule out a contribution of somatosensation. On earth,
there are always compressional support forces on the
body surface (countering the acceleration of gravity)
provided by the test apparatus. This undoubtedly produces adaptation of some somatosensory receptors. The
same level of adaptation will not be present in orbital
conditions, the subject will be conveyed by the apparatus, not supported and conveyed. Consequently, somatosensory cues from all body contact points with the apparatus may be more important. It is also difficult to control for fatigue in space flight. Chronic fatigue, an aspect
of the sopite syndrome component of space motion sickness (Graybiel and Knepton 1976), can be experienced
The angular vestibulo-ocular and optokinetic reflexes are
important aspects of gaze control during active head and
body movements and during passive displacement of the
individual or of the visual array. The semicircular canals,
otolith organs, and neck proprioceptors contribute to vestibulo-ocular reflexes (VORs). The VOR has been extensively studied in parabolic flight and orbital flight for
both active and passive head movements. On earth, with
the head upright, yaw head movements stimulate primarily the horizontal semicircular canals and elicit movements of the eyes compensatory for the head displacement so that (depending on instructions) gaze, the sum
of eye and head positions relative to space, can remain
constant. The yaw VOR during voluntary head movements has been measured in orbital flight over frequencies from 0.25 Hz to 1.0 Hz with a visual fixation target
present (Benson and Vieville 1986). Relative to groundbased tests, a slight decrease in gain has been observed,
which potentially could relate to decreased arousal.
Velocity storage, vestibular and optokinetic
The VOR evoked by passive stimulation of the horizontal semicircular canals has been studied during both parabolic and orbital flight (DiZio et al. 1987a, DiZio and
Lackner 1988; Oman and Kulbaski 1988; Oman and
Balkwill 1993). Acceleration to constant velocity in the
dark evokes a compensatory nystagmus with slow phase
opposite the direction of rotation. An important feature
of this nystagmus is that it considerably outlasts the peripheral activation of the semicircular canals. This phenomenon known as “velocity storage” is important because it represents a central integration or storage of activity conveyed by an “indirect” vestibular projection to
the brain stem (Cohen et al. 1977, 1983; Raphan et al.
1977). This same storage mechanism is activated by optokinetic stimulation and is responsible for the phenomenon of optokinetic after-nystagmus, a nystagmus that
persists in the dark after prolonged optokinetic stimulation. By measuring the peak slow-phase velocity of vestibular nystagmus, the gain of the peripheral canal response can be determined. The time constant of slowphase velocity decay serves as an index of storage. Velocity storage is reduced when the otolith organs are ablated; in this circumstance, the time constant of nystagmus decay represents the time constant of the cupula-endolymph system of the canal (Cohen et al. 1983).
Weightless conditions, which unload the otolith organs,
are consequently of great interest for VOR studies because some insight into central integrative mechanisms
may be achieved.
13
Studies both in the weightless phases of parabolic
flight and in orbital flight have found that the peak
slow-phase velocity of a post-rotary nystagmus evoked
by sudden deceleration from constant velocity rotation is
unaffected, but that the time constant is considerably
shortened relative to ground-based tests, but not to
the theoretical limit of the canal dynamics (DiZio et
al. 1987a, DiZio and Lackner 1988, 1992; Oman and
Balkwill 1993). This pattern has been repeatedly confirmed and suggests that g level does not alter peripheral
vestibular afferent responses to acceleration but does affect central vestibular processing. Attenuation also occurs during exposure to 1.8 g force levels (although the
time constant does not decrease by quite so much), suggesting that departures in either direction from 1 g diminish velocity storage (DiZio et al. 1987a). As mentioned above, optokinetic after-nystagmus is also a reflection of velocity storage, and it too has a shorter time
constant in weightless (and high force) conditions (DiZio
and Lackner 1992). On earth, post-rotary nystagmus is
shortened if the head is tilted following body deceleration to rest, a phenomenon referred to as “dumping” of
velocity storage (Benson and Bodin 1966a, 1966b).
Dumping has not been observed in weightless conditions
either in parabolic flight or in orbital flight (Fig. 6), but
it does occur in the high-force period of parabolic flight.
Pre- and post-space flight testing of four rhesus monkeys flown on two space flights, two on each flight, has
revealed changes in the three-dimensional organization
of velocity storage and vestibulo- and visuo-ocular
responses to linear acceleration. Normally, on earth, if
the axis of optokinetic stimulation is off vertical, then
when the lights go out the axis of optokinetic afternystagmus shifts away from this axis and moves toward
the gravitational vertical, because the eigenvector of
three-dimensional velocity storage is gravitationally oriented (Raphan et al. 1992). When tested post-flight, one
animal whose pre-flight optokinetic after-nystagmus had
shown the normal pattern of velocity storage orientation,
showed an after-nystagmus axis that drifted toward
the body z-axis, indicating a reorientation of velocity
storage (Dai et al. 1994). Another animal that pre-flight
had shown normal dumping of velocity storage by postrotary tilts showed no dumping post-flight (Dai et al.
1994). Both of these monkeys on return from space
flight exhibited a reduced or absent modulation of ocular
vergence by off-vertical axis rotation (Dai et al. 1996).
Across all four, there was an average 70% reduction
in ocular counter-rolling post-flight, but none of the
animals showed a change in gain of semicircular-canalelicited, horizontal and vertical angular vestibulo-ocular
reflexes (Dai et al. 1994). Single-unit recordings from
horizontal semicircular canal afferents during 60°/s yaw
velocity steps showed increased gain post-flight for the
two monkeys on the first flight relative to control monkeys who had not flown and a decreased gain for the pair
of monkeys from the second flight (Correia et al. 1992;
Correia 1998). This overall pattern suggests central adjustments in vestibular processing are made in micro-
Fig. 6 The gain of the vestibuloocular reflex following sudden
stop stimulation is not affected by alternating exposure to 0 g, 1 g
and 1.8 g in parabolic flight; however, the decay constant is lower
in 1.8 g than in 1 g and lower still in 0 g. After 4–5 days of continuous exposure to 0 g, the time constant is back to baseline. Postrotary head tilts reduce the time constant (dumping) in 1 g and in
1.8 g but not with periodic or continuous exposure to 0 g
gravity to compensate for altered semicircular canal and
otolith input. The three dimensional organization of velocity storage and its relationship to linear acceleration
and the otolith organs are certain to be a topic of continued intensive study in space-flight experiments, with humans and monkeys.
Ocular counter-rolling and torsional eye movements
Under terrestrial conditions, maintained tilts of the head
evoke sustained counter-rolls of the eyes in the opposite
direction (Lorente de Nó 1932). Ocular counter-rolling
compensates only partially for the amplitude of head tilt
and rarely exceeds 8–10°. It is virtually absent in individuals without functioning otolith organs (Woellner and
Graybiel 1960). Dynamic tilts of the head activate semicircular canals as well as affecting the otolith organs; head
tilts in roll generate a torsional VOR. Clarke et al. (1993)
measured the torsional VOR response to voluntary roll
head movements in orbital flight. Initially, as might be anticipated, there tends to be decreased gain, but on later test
days, there can be an increased gain relative to pre-flight
14
baselines. Torsional eye position measured in space with
the head upright on the shoulders is offset from its preflight position measured with the head vertical; there is
also more binocular torsional disconjugacy aloft and it can
persist up to 13 days post-flight (Diamond and Markham
1991, 1998; Markham and Diamond 1992).
On the ground, linear acceleration along the y axis
(inter-aural axis) when the subject is upright elicits torsional eye movements. Pre- and post-flight assessments
of torsional eye movement responses to y-axis linear acceleration have shown that gain decreases post-flight
(Young et al. 1984; Arrott and Young 1986). Ocular
counter-rolling during static body tilt has also been measured pre- and post-flight, with mixed results. Several
studies report astronauts’ post-flight counter-rolling is
diminished relative to pre-flight and can remain reduced
for more than several weeks (Vogel and Kass 1986;
Hofstetter-Degen et al. 1993). Rhesus monkeys also
show post-flight reductions in counter-rolling (Dai et al.
1994). Other studies of astronauts have shown postflight increases of counter-rolling that also last for days
(Matsnev et al. 1985; Diamond and Markham 1998).
Ocular responses to pitch head movements have been assessed in orbital flight (Berthoz et al. 1986; Viéville et
al. 1986), but the results have not been consistent and
large variations within and across individuals make additional observations necessary before firm conclusions
can be made. The overall pattern of VOR responses in
weightlessness is in accord with a decreased role of the
otolith and somatic graviceptor organs.
Caloric nystagmus elicited in weightlessness
An unexpected finding in the Spacelab-1 mission was
the elicitation of caloric nystagmus, a finding clearly
contrary to the thermal convection theory of caloric nystagmus proposed originally by Barany (Scherer et al.
1986; Von Baumgarten 1986). This finding has since
been confirmed with a variety of controls to exclude possible confounds related to auditory stimulation (Clarke et
al. 1988, 1989). Caloric effects have also been reported
in parabolic flight, but these results are much more difficult to interpret, because nystagmus would be predicted
by the thermal convection theory in the non-weightless
parts of parabolas and a secondary nystagmus could then
appear in the weightless phases of flight (Graybiel et al.
1980). A full explanation of the caloric response in orbital flight is still lacking.
In summary, vestibular thresholds for linear and angular acceleration are little affected by exposure to weightlessness. The gain of the angular vestibulo-ocular reflex
is unchanged, but velocity storage is attenuated for both
vestibular and optokinetic slow-phase velocity. Torsional
eye movements are initially suppressed in-flight but gain
increases later. Post-flight, ocular counter-rolling is attenuated for some astronauts and cosmonauts and enhanced in others. Counter to expectations, caloric nystagmus can be evoked in weightlessness.
Oculomotor control
The eyes occupy a privileged position from the standpoint of motor control. Gravity torques have relatively
little influence on them because they are roughly spherical, their center of rotation is close to their center of
mass, and they are of relatively small mass (Mach 1959).
Consequently, they can be controlled more simply than
the arms, legs, or torso. Saccadic eye movements are
largely generated open loop with visual feedback at the
end of a movement serving to update control. Pursuit eye
movements are dependent on visual error feedback, although predictability permits essentially phase-locked,
zero-lag tracking; somatosensory and proprioceptive signals enhance tracking capability as well (Koerner and
Schiller 1972; Carpenter 1988; Becker 1989).
Optokinetic responses
Given the above considerations, one might expect that
oculomotor control would be relatively unaffected by
background force level. Some astronauts and cosmonauts, however, exhibit a spontaneous horizontal or vertical nystagmus in flight (Kornilova et al. 1993). On
earth, optokinetic responses to moving striped patterns
tend to be symmetric for leftward and rightward horizontal stimulation, but for some individuals the gain of their
vertical responses is asymmetric for upward and downward stimulation, with upward stimulation tending to
elicit higher gain responses. This asymmetry tends to be
eliminated in space flight and the gains of both upward
and downward (relative to the head) optokinetic responses tend to be diminished (Clément and Berthoz 1988,
1990; Clément et al. 1986, 1993). In the 0 g phases of
parabolic flight, there is a tendency for upward slowphase velocity to be attenuated and downward optokinetic responses to be augmented (Clément et al. 1992a,
1992b). The overall effect both in parabolic and space
flight may be related to otolith-dependent changes in eye
position which, in themselves, affect slow-phase velocity
according to “Alexander’s Law” (Camis 1930; Evanoff
and Lackner 1986). For the same visual or vestibular
stimulus, the slow phase velocity of the eyes is enhanced
when the overall position of the eyes is shifted in the direction of the nystagmus fast phase (Fig. 7). The pattern
of results is consistent with a “summation” of eye velocity and otolith signals, with the latter being modulated by
background force level.
Saccadic and pursuit eye movements
Saccadic eye movements in orbital flight show increased
latencies and decreased peak velocities relative to baseline observations (André-Deshays et al. 1993). Fatigue
related to space motion sickness may be a factor in studies showing increased latencies and decreased peak velocities because these studies usually have been conduct-
15
Post-flight disturbances of posture, locomotion,
and movement control
Fig. 7 Illustration of how otolith-driven changes in static eye posture and Alexander’s law could alter the symmetry of vertical nystagmus. The amplitudes of nystagmus slow and quick phases increase when gaze is directed toward the nystagmus beating field
(arrows); beat frequency is unchanged, so slow-phase velocity increases (top) relative to normal conditions (middle). Maintaining
ocular deviation in the slow-phase direction slightly suppresses
the nystagmus (bottom). U up, D down
ed relatively early in a flight. A striking influence of
weightlessness has been found on pursuit eye movements. Although horizontal (relative to the head) eye
movements are affected little or not at all, regardless of
whether the head is fixed or participates in the tracking,
vertical pursuit movements are disrupted (AndréDeshays et al. 1993). Attempted upward (relative to the
head) visual pursuit results mainly in saccadic eye movements with little evidence of pursuit. Downward visual
pursuit is less dramatically affected but is carried out
with a combination of pursuit movements interspersed
with catch-up saccades. This degradation of performance
may relate to the altered otolith input in weightless conditions but its severity is surprising. As already mentioned, the VOR during pitch head movement tends to
vary greatly within and across subjects in orbital flight.
This may result in part from impairments of the vertical
pursuit system. Pitch head movements are most evocative of motion sickness during exposure to weightless
conditions (Lackner and Graybiel 1984a, 1984b). This is
consistent with the impaired vertical pursuit and VOR
performance in weightlessness and may represent a significant etiological factor in space motion sickness.
In sum, weightlessness induces small changes in optokinetic responses, little if any alteration in saccadic eye
movements, but considerable disruptions of vertical pursuit eye movements.
Following re-entry, astronauts feel abnormally heavy and
their movements seem to require much greater than normal effort (Harm and Parker 1993; Reschke et al. 1994a,
1994b). Some even have difficulty moving their limbs at
all after re-entry. The ground feels unstable under their
feet as they walk, and if they attempt a shallow knee
bend, the ground seems to move under their feet; they
misperceive their own motion as well. (This is precisely
what subjects report after making repeated deep knee
bends in 0.5 g when they return to 1 g again and attempt
to make deep knee bends.) Post-flight head movements
made during walking are very destabilizing. Without a
well-structured visual environment loss of orientation
and balance are likely. Turning movements of the body
are especially destabilizing: walking into door frames
when turning to walk through a doorway is common.
These re-reentry disturbances greatly impair the ability
of astronauts to carry out critical mission activities immediately upon landing. For example, a rapid emergency
egress simply would not be possible for many astronauts.
Both posture and locomotion have been studied postflight. It has not been possible to test astronauts in the
initial minutes following re-entry and sometimes not for
hours or even days afterwards. Consequently, some
abatement of post-flight disturbances, especially those
with short time constants, will already have occurred and
observed performance decrements will not reflect the
full magnitude of the initial post-flight disturbances.
Study of re-adaptation phenomena with short time constants is critical for understanding how to overcome reentry disturbances that would affect performance in an
emergency after landing and may provide clues for understanding longer term re-entry disturbances.
Static and dynamic assessment of postural control
Post-flight assessments of postural control have been
carried out since the Apollo missions (Homick and
Miller 1975; Homick et al. 1977; Homick and Reschke
1977; Kenyon and Young 1986). The Fregley-Graybiel
rail test battery (the test subject tries to balance heel-totoe on rails of different widths, with eyes open and
closed) has shown post-flight impairments, especially for
eyes-closed conditions, in all astronauts tested (Homick
et al. 1977; Graybiel 1980). Performance decrements
persist for days and are more severe after longer duration
missions. Force plate recordings of center of pressure reveal increases in mean sway amplitude that can persist
for many days. Tests in which the support surface is displaced or rotated to perturb stance also show post-flight
performance decrements: perturbations elicit displacements of the center of pressure and of hip and shoulder
that are larger than pre-flight, and the settling time to
pre-perturbation baseline is longer too (Anderson et al.
1986).
16
The Equitest system has been used to study the postflight balance of astronauts returning from 5- to 15-day
space-shuttle missions (Paloski et al. 1992a, 1992b). The
test battery involves six different combinations of visual
and support surface conditions: (1) eyes closed, stationary surface, (2) eyes closed, sway referenced surface in
which the surface tilts with the body to prevent changes
at the ankles, (3) eyes closed, swaying surface, (4) eyes
open, stationary visual surround and stationary support
surface, (5) eyes open, stationary surface, visual sway
referencing in which the visual field is stabilized in relation to the subject’s body, and (6) eyes open, sway referenced surface, sway referenced visual array. Every astronaut tested, some as early as 2–4 h post-flight, has
shown decreased performance on all six test conditions
relative to pre-flight baseline. An increased dependence
on vision post-flight is also apparent with conditions
involving sway referencing of vision being especially
disabling. Recovery follows a dual exponential time
course. Rapid improvement takes place over the first ten
or so post-flight hours followed by a more gradual return
over 4–10 days toward pre-flight baseline. This 4- to
10-day recovery period is strikingly long, given that the
mission durations of the astronauts tested were in the
5- to 15-day range.
Post-flight postural disequilibrium has also been studied using a technique that attempts to discriminate postural fluctuations occurring on a short time scale, thought
to be open-loop, from longer fluctuations that are under
sensory feedback control (Collins et al. 1995). Of four
astronauts tested following a 14-day shuttle flight, three
showed greater random fluctuation in the quick, openloop mode one day after landing relative to pre-flight;
postural control returned to pre-flight performance by
the ninth post-flight day. Importantly, as long as the head
was not voluntarily moved, vision could stabilize body
posture to the surroundings despite the changes in vestibular and proprioceptive function that occurred inflight.
Lasting post-flight changes in response to postural
perturbations have also been documented in cosmonauts. Two MIR crew members who had been in orbit
for 151 days, and another for 241 days, were tested for
their ability to recover postural stability after receiving a
sudden push on their chest. Post-flight, less force was
necessary to perturb posture and recovery time was
greater as shown by force plate recordings. Post-flight,
the cosmonauts showed much greater increases in muscle activity levels following a push relative to pre-flight.
Eleven days after re-entry, these differences were still
significant (Gregoriev et al. 1991). Later tests were not
made. These findings could also relate to leg muscle atrophy.
In summary, all post-flight assessments of postural
stance have shown performance decrements. These decrements are greatest for situations denying visual input
or rendering visual input inappropriate by referencing it
to body sway, i.e., the visual array is stabilized in relation to the subject rather than external world. Full recov-
Fig. 8 Schematization of alterations in posture and gait after adaptation to 0 g exposure. The most common finding is an immediate performance decrement upon return to 1 g followed by gradual
return (rates of return are not represented) to the 1 g baseline. This
pattern suggests that immediate compensation is not possible in
1 g for the structural and neural control system changes that occurred in 0 g and that re-calibration to 1 g can be more difficult
than adaptation to 0 g. –––– Sway during quiet stance, after orbital
flight (Collins et al. 1985); –··–· sway during perturbed visual
and support conditions; after orbital flight (Paloski et al, 1992);
–·–·– variability of treadmill gait, after orbital flight (McDonald et
al. 1996); ········· Otolith-spinal reflex, after orbital flight (Watt et
al. 1986); – – – – deep knee bend illusion after parabolic flight
(Lackner and Graybiel 1981).
ery of performance takes days or weeks. Post-flight assessments of static postural performance might show
even greater differences relative to pre-flight if astronauts and cosmonauts did not adopt very stiff postures to
avoid falling during the tests. Figure 8 illustrates the pattern of these changes, which differs sharply from the
time course of in-flight changes.
Evaluations of walking control
As already mentioned, locomotor instability is commonplace post-flight when astronauts attempt to walk unaided and turn corners. Recently, attempts have been made
to quantify these post-flight changes using treadmill locomotion (McDonald et al. 1996; Layne et al. 1997). Astronauts tested within 4 h after landing show greater
variability in the timing of the toe-off and heel-strike
phases of walking relative to pre-flight. These are phases
of the step cycle that require fine neural control of muscle activation, because this is where maximum energy
transfer occurs. Consequently, these changes have a major detrimental influence on locomotor stability.
Modifications of locomotion have also been investigated from the perspective of head stabilization. Bloomberg et al. (1997) measured the head and trunk movements made by 23 astronauts during treadmill walking as
they viewed an eye-level target, pre- and post-flight. All
showed a similar pattern. Pre-flight, the head pitched up
17
when the trunk was descending and pitched down when
the trunk was ascending, assisting target fixation. Postflight, pitch head angle was loosely coupled to trunk elevation; these results are from tests performed 2–4 h after
landing. The frequency and amplitude of head movements was lower than pre-flight, so the astronauts may
have been self-limiting their head movements to avoid
motion sickness, relying on eye–head coordination to
maintain target fixation.
Ataxia, postural disorientation, and gait disturbances
occur on return to earth from space flight. These disturbances reflect in part sensory-motor adaptations to
weightlessness, the persistence of which affects vestibulo-ocular and vestibulo-spinal reflexes, and voluntary
control of balance, movement, and locomotion until readaptation occurs. The disturbances likely result in part
from progressive structural changes in muscle and bone
and from plastic central nervous system reorganizations
of motor units and their response characteristics, and of
cortical maps (Correia et al. 1992; Holick 1992; Ross
1992, 1993, 1994; Edgerton and Roy 1995; Edgerton et
al. 1995; Kaas 1995; Allen et al. 1996).
Artificial gravity
Long-duration exposure to weightless conditions has severe adverse consequences on skeletal and muscle integrity and sensory-motor control mechanisms, despite the
various in-flight countermeasures that have been used
(Vernikos 1996). Even with hours of daily exercise on
treadmills under 1 g bungee-cord loading of the body,
approximately 1% of bone mineral content is lost each
month in orbital flight (Holick 1992). If a mission to
Mars that might last 2 years or more were carried out,
there is a strong likelihood that astronauts would be unable to deal with an emergency on re-entry into a significant g-field because of inability to control their movements. The capacity to carry out an emergency egress on
landing would likely be absent. Even with brief duration
flights, e.g., 2 weeks, sensory motor control is compromised for some period following landing. The use of
some form of artificial gravity device may provide an effective way to offset the detrimental effects of weightlessness.
Artificial gravity sleepers
“Artificial gravity sleepers”, coffin-like enclosures that
function as short arm centrifuges, with the head positioned at the center of rotation, are being explored as a
way of preventing cardiovascular deconditioning and
bone loss in space flight (Diamandis 1997). For example,
with rotation at 23 rpm, a gravity gradient ranging from
0 g at the axis of rotation to about 1 g at the feet would
be created for a 6-foot subject (Fig. 9). This would generate a hydrostatic gradient in the circulatory system,
making the heart work harder and thereby help maintain
Fig. 9 Illustration of forces in an artificial gravity sleeper on a
space vehicle where the background force is 0 g. A centrifugal
force gradient from 0 g at the head to 1 g at the feet (solid arrows)
is generated on a six-foot subject rotating at 23 rpm about the head
(rotation axis indicated by a cross). Straps and cushions must provide restraining contact forces (dotted arrows)
cardiovascular fitness. The force gradient along the long
axis of the body would load the skeleton and help maintain bone integrity. Given the experience with 1 g bungee-cord loading and exercise in space flight and the fact
that the gradient would be 1 g at the feet but only 0.5 g at
the center of mass, it seems unlikely that passive exposure to a 1 g sleeper would have much effect in preserving bone structural integrity unless very high rotational
rates were used.
Head movements made out of the axis of rotation in
an artificial gravity sleeper would elicit Coriolis, cross
coupling stimulation of the semicircular canals and otolith organs. Under terrestrial conditions at high velocities
of rotation, this would be extraordinarily provocative of
motion sickness. In space flight conditions, however,
with the head at the axis of rotation, the gravitoinertial
resultant force would be quite small, and Coriolis stimulation of the vestibular system is much less provocative
in 0 g (Lackner and Graybiel 1984a, 1984b, 1985, 1986,
1987; DiZio et al. 1987b). Consequently, an artificial
gravity sleeper might not make astronauts very motion
sick unless they were already sensitized. Moreover, the
notion is to use a head restraint to minimize movements
of the head thereby limiting cross-coupling and Coriolis
stimulation of the semicircular canals (Diamandis 1997).
If visual motion cues were absent, the astronaut would
feel stationary despite actually undergoing high velocity
rotation and the force gradient in the sleeper would make
him or her feel as if standing upright. This might initially
affect sleep patterns until the astronaut became used to
sleeping “upright”.
Artificial gravity sleepers would contribute little to
the maintenance of sensory-motor calibration of movement control mechanisms of the body. Consequently,
they would be unlikely to attenuate the severe re-entry
disturbances of movements and postural control that,
along with radiation hazards, skeletal mineral loss, and
cardiovascular deconditioning, are some of the most
18
dangerous aspects of interplanetary space flight. It is
unclear what effect artificial gravity sleepers would
have on the regulation of body fluid volume. Entry into
weightlessness causes rostal redistribution of body fluid that leads to activation of homeostatic mechanisms
that decrease overall circulating blood volume and produce other far reaching changes. With blood volume reduced, an artificial gravity sleeper might produce orthostatic intolerance and syncope. Possibly fluid loading before entering a sleeper, such as is used prior to reentry from space flight, and an anti-g suit would help to
alleviate this problem. It is unclear what effect cyclic
exposures to weightless and then loaded conditions
would have on the circulatory system and hormonal
regulation, and whether after long-term usage there
would be cyclical aftereffects following return to earth.
Remodeling of the bones of the feet, ankles, and legs
would also occur with many hours of “daily” constant
exposure to contact forces on the feet. The potential extent and functional significance of such changes has not
yet been explored.
Rotating environments
An alternative approach to the generation of artificial
gravity is to rotate an entire space vehicle or a large
chamber within it. In this circumstance, the centripetal
force provided by the “walls” of the vehicle serves as the
artificial gravity, and the astronauts use the walls as their
floor for locomotion. For short radius devices, significant gravity gradients would exist so that if an object
were raised up from the floor (toward the center of
rotation) it would become lighter, and then heavier
again as it was lowered (Stone 1970; Nicogossian and
McCormack 1987). Similarly, if an astronaut in a short
radius device walked rapidly in the direction of rotation,
his or her effective body weight would increase, and
conversely decrease for walking in the direction opposite
rotation. Interestingly, these effects and others related to
vehicle radius tend to asymptote at about a 10-m radius
(Stone 1970). At 10 rpm, this would produce an artificial
gravity level of approximately1.1 g.
One of the major drawbacks of a rotating environment is the generation of Coriolis forces, both radial and
tangential. Figure 10 illustrates how these accelerations
deflect the paths of moving objects tending to displace
them in their direction. Voluntary movements are also
deviated by Coriolis accelerations potentially disrupting
motor performance. One important theory of movement
control, the alpha equilibrium point hypothesis, predicts
that although movement paths would be deviated, the intended endpoints of the movements would be accurately
attained (Bizzi et al. 1992). If final position were accurately achieved in a rotating environment, an astronaut
would have to learn to compensate only for movement
trajectory deviations. Unfortunately, this turns out not to
be the case – both movement paths and endpoints are
disrupted. However, adaptation can be rapidly achieved
Fig. 10 Top view of Coriolis forces in a counterclockwise rotating
room. The Coriolis force (FCor) acting on an object is orthogonal
to its direction of motion and proportional to its linear velocity (v),
mass (m) and the angular velocity of the room (ω): FCor=
–2 m(ω×v). The Coriolis force magnitude does not depend on the
location within the rotating room (compare case A and case B)
(Lackner and DiZio 1994; DiZio and Lackner 1995a,
1995b), as illustrated in Fig. 11 and Fig. 12. Coriolis
forces, as already discussed, also affect the vestibular
system during head movements.
A pioneering series of studies in the 1960s on human
performance in a slow-rotation room studied the maximal rates of rotation to which subjects were able to
adapt. Individuals lived in the rotating room for periods
of up to 3 weeks (Graybiel et al. 1960, 1965; Kennedy
and Graybiel 1962; Guedry et al. 1964). At rates of rotation above 3.5 rpm, motion sickness was a problem because of the Coriolis stimulation of the vestibular
system generated when head movements were made out
of the axis of rotation. Subjects who were exposed to
room rotation at 10 rpm never fully adapted in terms of
complete abatement of symptoms of motion sickness
and being able to move their head in novel ways without
eliciting symptoms. On return to zero rotation velocity,
the subjects again experienced symptoms of motion
sickness when they moved their heads, indicating that
they were no longer fully adapted to the stationary environment.
These experiments involved a single-step exposure to
constant velocity rotation. It has since been shown that if
individuals are brought up gradually to the terminal rotation velocity, and make many head movements at each
dwell velocity, then they can readily adapt to room
velocities of 10 rpm without ever experiencing any
symptoms of motion sickness (Graybiel and Wood 1969;
Reason and Graybiel 1970; Graybiel 1975). These subjects, on return to 0 rpm, unlike those who are exposed
in a single-step to peak room rotation velocity, do not experience severe symptoms of motion sickness (Graybiel
and Knepton 1978). This resistance to motion sickness
following incremental adaptation protocols has been
termed “overadaptation”.
19
Fig. 12 Lateral endpoints errors of reaching (Arm), toe-pointing
(Leg) and pitch head movements (Head) before, during, and after
rotation that generated rightward Coriolis forces
Fig. 11 Paths of the first movements made during rotation (perrotation) and the first movements made when rotation ceased
(post-rotation) after the subjects had adapted to the Coriolis forces; compared with baseline movements (pre-rotation). Top views
of the fingertip and toe are plotted for reaching (Arm) and toepointing (Leg) movements, respectively. For pitch head movements (Head), the trace is of a point between the eyes from a perspective roughly orthogonal to the movement path; the icons show
the initial and final head orientations
Rapid adaptation to Coriolis force perturbations of arm,
leg, and head movements
The early rotating room studies of Graybiel and his colleagues also noted disruptions of eye–hand coordination
and locomotion that gradually adapted with continued
exposure. However, on cessation of rotation, the subjects
exhibited aftereffects in movement and locomotion control so that their motor performance was again disrupted.
In these studies, there was no systematic attempt to control movement exposure history in the slow rotation
room. Recent studies are showing that if movement behavior is controlled and repeated movements are made,
for example, pointing movements to a target, then adaptation occurs very rapidly (Lackner and DiZio 1994;
DiZio and Lackner 1995b). For reaching movements to a
single target, full adaptation can be achieved within
10–20 reaches, even if visual feedback about reaching
accuracy is denied. Such rapid and complete adaptation
was totally unexpected given the findings of the early
studies. Part of the difference may relate to the same
movement pattern being attempted a number of times in
a row, allowing the nervous system to gauge the deviation from the expected trajectory, thus permitting adaptive accommodations to be initiated. If each movement
that is made has a different direction or distance or velocity, it is more difficult for the nervous system to identify the character of the Coriolis perturbation because its
magnitude can be different each time.
Ongoing studies are also showing remarkably rapid
adaptation of leg movement control during rotation
(Fig. 11 and Fig. 12) (DiZio and Lackner 1997; Lackner
and DiZio 1998c). The final position of leg movements
initially made during room rotation tends to be more deviated than that of initial arm movements during body
rotation at the same velocity. This likely relates to the
greater inertial mass of the leg and thus the larger Coriolis force for movements with similar velocity profiles.
Head movements made during rotation are of particular interest because the Coriolis forces generated act on
the head (and otoconia) as an inertial mass, as well as
causing cross-coupling stimulation of the semicircular canals. The resulting trajectory of the head in relation to its
intended one shows the effect of both factors, a lateral deviation in relation to the torso caused by the Coriolis
force on the head and rotary deviations in yaw and roll
related to the semicircular canal activation. The displacement created by the Coriolis acceleration acting on the
head as a mass adapts very rapidly, the semicircular canal-driven component takes considerably longer to adapt.
20
Nevertheless, with repeated head movements, movement
path can be restored to normal within 30 to 40 movements (Lackner and DiZio 1998c). Movement aftereffects
of opposite sign occur post-rotation (Fig. 11 and Fig. 12).
Studies currently under way are exploring whether
adaptation transfers across different rotation rates, from
one arm to the other, to different locations within the
workspace, and to different movement velocities. Identifying the factors that allow generalization of motor adaptation to the entire environment rather than to restricted
sets of related movements made during rotation will allow optimal exposure schedules to be developed. A key
issue is whether adaptation can be simultaneously maintained to more than one force environment so that individuals would be able to go back and forth between them
with minimal or no performance decrements. The slow
rotation room studies clearly reveal such a potential. All
regular on-board experimenters acquire such adaptation
in the course of carrying out their everyday activities in
the slow-rotation room. They feel and act completely
normally in the rotating room and don’t have aftereffects
when the room stops rotating, analogous to the overadaptation of motion sickness mentioned earlier.
Studies of adaptation to Coriolis force perturbations of
reaching movements and of head movements have also
been carried out in parabolic flight. At issue is whether
adaptation occurs similarly in different background force
levels. Coriolis accelerations of comparable magnitude
have roughly comparable influences on movement trajectories and endpoints independent of background force
level, albeit there is a tendency for movements to be more
deviated in 0 g than in 1 g. Adaptation occurs even in the
absence of visual feedback but with a somewhat longer
time constant in 1.8 g and 0 g relative to 1 g (Lackner and
DiZio 1998b; DiZio and Lackner unpublished observations). Similar results have been obtained for the head.
This means that background force level has a modulating
influence on the ability to adapt to Coriolis force perturbations of movement trajectories. This modulation may
be related to muscle spindle sensitivity which, as discussed in the section on Limb proprioception, is under
control of background gravitoinertial force. An important
feature of arm, leg, and head movement adaptation in a
rotating environment is that when adaptation is achieved,
the Coriolis forces generated by these movements are no
longer perceived. The adapted subject’s movements again
feel perfectly normal and the Coriolis forces no longer
seem to be present during movement although their magnitude is physically unchanged. This may result from the
nervous system adjusting its internal forward model of
the feedback expected when a movement is initiated (Miall and Wolpert 1996).
Object manipulation, tool use and locomotion
in rotating environments
An object that is moved or shaken is subjected to Coriolis forces in a rotating environment, as is the arm doing
the moving or shaking. Ongoing studies are showing that
the perception of an unseen object’s structural properties
is virtually unaffected by Coriolis accelerations. For example, when a rigid rod is shaken up and down, lateral
Coriolis forces are generated. These, in principle, could
lead to the perception of the object bending laterally
from tip to shaft in the direction of the Coriolis force as
it is shaken. This does not happen; a rod is correctly perceived as being rigid even when it is not visible as it is
being shaken by the subject. These results, at rotation
rates of 10 rpm, are promising in suggesting only minor
problems in manipulating and controlling relatively nonmassive objects during rotation (Kunkler-Peck et al., unpublished observations).
Whole body locomotion, moving the large mass of
the body from one place to another during rotation, is a
more complex adaptation yet to be studied quantitatively
in ground-based rotating environments. It would be a
less difficult adaptation in a cylindrical space vehicle rotating to generate artificial gravity because, in that case,
the wall of the vehicle would be the floor on which the
astronauts locomoted and their distance from the center
of rotation would be relatively constant. In a rotating vehicle with a radius that was large relative to the astronauts’ height, the Coriolis forces and variations in centripetal force (artificial gravity) acting on their bodies
during voluntary movements would be small. By contrast, in a rotating vehicle on earth without a central axle,
an individual can walk anywhere on the floor including
through the center of rotation. When moving toward the
walls, a centripetal “force” of greater and greater magnitude will be encountered; by contrast, at the center of rotation, this force goes to zero. In a rotating space vehicle,
unlike a terrestrial rotating room, the effect of Coriolis
forces on the semicircular canal system of an “upright”
subject would vary with body orientation relative to the
axis of rotation.
Stance initially is less stable in a rotating environment
because body sway motion can elicit vestibular crosscoupling stimulation and Coriolis forces on the body,
thus increasing sway. However, light touch of the hand
with a stationary surface at non-mechanically supportive
contact force levels reduces sway to non-rotating levels,
both in normal subjects and those without labyrinthine
function. The light touch also enhances postural adaptation to the rotating conditions (see Fig. 13, and Fig. 5 for
related findings). These observations mean that a highly
integrative task, like stance, adapts quickly to rotation
when the proper sensory cues and adaptation schedule
are provided.
Much remains to be done to determine the limits of
human adaptation to rotating environments. Research
has only recently been restarted after a nearly 30-year hiatus. The results are already promising in showing that
the early conclusions of a 3- to 3.5-rpm limit on adaptability are unrealistically low. Ten rpm can be achieved
using an incremental exposure schedule and would allow
relatively short-radius vehicles. Controlled exposure to
the proper stimuli in the appropriate schedule might
21
Fig. 13 Performance of a typical subject attempting to stand “as
still as possible” before, during and after 10 rpm exposure in the
center of a rotating room. In alternate trials, subjects either maintained about 40 g fingertip contact with a stable bar or held their
hand above the bar with no contact. The conditions in all trials
were eyes closed and feet positioned in tandem. The range of foreaft center of mass motion is presented for every trial
make rapid adaptation possible even for complex movements like locomotion and head movements. The reviewed studies suggest that there are dual adaptation
processes involving rapid motor adjustments to Coriolis
force deviations of an entire appendage and a slower adaptation to vestibular cross-coupled stimulation. Overall
functional adaptation may be hastened with controlled
exposures that sequentially engage each sub-system.
An unexpected outcome of current research has been
the demonstration that adaptation of movement control to
rotation is a well-established human capacity. During every day life, our brief, multi-axis voluntary head rotations
generate vestibular cross-coupling. We commonly expose
ourselves to linear Coriolis forces by reaching for objects
while simultaneously rotating our torsos. Kinematic measurements of such arm and torso movements indicate that
torso peak velocity commonly reaches 180°/s, or 30 rpm.
The Coriolis forces generated by reaching movements in
these circumstances are much higher than those generated
by reaching movements made in a rotating room turning
at 10 rpm, yet motor performance is accurate (Pigeon et
Table 1 Extraneous factors in
weightless and artificial gravity
environments that can be controlled in 1 g, laboratory experiments (1=always a problem,
2=sometimes a problem,
3=never a problem)
al. 1999, Bartolami et al. 1999). This means that the nervous system must automatically compensate for the Coriolis forces associated with voluntary trunk rotation,
switching compensations on when torso rotation is taking
place and omitting them when the torso is stationary. This
capability casts adaptation to a rotating physical environment as a much less novel problem for the nervous
system to solve than originally thought. Adaptation to rotation rates as high as 10 rpm, once thought to be impossible, now seems quite likely for all aspects of spatially
oriented movement behavior. In addition, there is evidence that adaptation to self-generated Coriolis forces is
context specific (Cohn et al. 1996, 1999).
Conclusions
Considerable progress has been made in understanding
human movement and orientation in weightless conditions. Much emphasis to date has been placed on vestibular function and oculomotor control because of the obvious influence of gravitoinertial force level on the otolith organs. Future work will need to address broader issues of movement control and orientation, especially
with regard to adaptation to different gravitoinertial reference frames and making transitions between them.
Tool use, object manipulation, and locomotion also need
systematic study.
In interpreting space-related experiments, it is important to be aware of the restrictions that investigators face,
some of which are listed in Table 1. Conducting an experiment in weightless conditions is totally unlike
ground-based experimentation. Techniques for head and
body restraint that work well on earth are inappropriate;
debris, detritus, loose tools and cables float about and
can interfere with subjects’ performance and equipment.
These are problems investigators regularly overcome.
Performing rigorous assessments and calibrations of
flight equipment while on a mission is rarely possible for
comparison with ground-based apparatus. Even more
Factor
Modes of attaching subjects to motion device
Modes of delivering stimuli to somatic surfaces
Delay of initial tests after force transition
No control over frequency of testing
Ability to repeat tests to replace lost data
Calibration of equipment close to time of experiment
Last minute adjustment of protocols
Latency of experimenter access to data
Control of activities/conditions just before the experiment
Motion sickness, fatigue, attention
Realistic timeline simulation in 1 g
Equipment design and setup
Interactions with other experiments
Dual role of subject and experimenter
Environment
Orbital
Flight
Parabolic
flight
Rotating
room
1
1
1
1
1
1
1
2
1
2
1
1
1
1
1
1
3
2
2
3
3
3
3
2
3
3
3
2
2
2
3
3
3
3
3
3
3
2
3
3
3
3
22
difficult to deal with, however, are the restrictions of
working with structured time windows. In space-shuttle
flights, each astronaut is following time lines, and segments of time are assigned to a wide range of tasks and
activities. Often the experimenter cannot control the time
of the first test, the frequency of testing, nor the inter-test
intervals. This means that some adaptive accommodations to weightless conditions may have already occurred
before the first test protocol on a particular experiment
and that it is difficult to get an accurate tracking of the
time course of in-flight changes. In the event of an
equipment failure or lost data collection, it may not be
possible to repeat the observations. Often it is not feasible to control the activities that precede testing so as to
eliminate potential interference. These same considerations apply to post-flight testing. It is not always possible to collect data during the optimal time periods nor to
control astronaut activity prior to testing. The net result
is that operational constraints make it very difficult to
answer conclusively even relatively simple questions.
The development of the International Space Station will
ameliorate many of these problems.
Space-shuttle flights, especially those with scientific
missions, are incredibly packed periods of time. Consequently, in interpreting threshold increases or performance decrements, it is important to take into account
factors such as excitement, fatigue, disrupted sleep cycles, and during the early part of a mission, space motion
sickness. Ground-based simulations of an entire mission
profile with all of the time lines filled with tasks as close
to operational conditions as possible would be useful in
interpreting performance changes. It is difficult, however, to get the time and resources to carry out such simulations and they can never be fully informative.
In considering post-flight disturbances, one must realize that, even after brief missions, astronauts and cosmonauts are not returning with the same physical “plants”
and neural “controllers” as when they departed. Structural changes in muscle and skeleton, and neurophysiological changes in brain and motor unit properties have occurred that need to be reversed in order to readapt movement control and orientation to earth gravity conditions.
The remarkable fact is how rapidly the accommodations
to unusual force conditions can occur. It is notable that
normally we are largely unaware perceptually of the
forces acting on our bodies as a consequence of our own
activities. These forces are largely transparent to us; for
example, when we shift from two-legged to one-legged
stance we do not feel a great increase in force on the sole
of the stance foot, although that force has doubled. Similarly, we do not perceive the magnitude of the forces associated with our own locomotory or orientational movements, although they can be several g. Subjects who
have adapted to Coriolis force perturbations of their
reaching movements in a rotating room no longer feel
the Coriolis forces when they reach; everything feels
normal again, despite the continued generation of these
forces by their movements. It is likely that subjects fully
adapted to moving and walking in a rotating room would
Fig. 14 Diagram of the interactions among factors involved in
changes brought about by transitions between different force environments. The pervasive alteration of contact force has immediate
and long-term effects on body tissue, perceptual and motor performance, and sensorimotor control. Bidirectional relationships
among behaviors and control mechanisms (including internal
models) cause additional short- and long-term changes
not be able to tell whether their environment was stationary or rotating unless they had a window or an accelerometer much like the inhabitants of Plato’s cave need extra information to determine what corresponds to reality.
Figure 14 provides a conceptual integration of some
of the factors involved in adapting orientation and movement control to different gravitoinertial force backgrounds. It illustrates the important role of contact forces
on the body as well as altered vestibular function, altered
skeletal-muscular loading, altered modes of locomoting
and orienting, loads or objects that are being borne, and
cognitive information about the environmental situation
(whether one is rotating, in free fall, etc.), and the multiple modes of interrelating motor, efference copy, predicted sensory feedback, and sensory signals in adaptive
movement control.
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