744
Motor function in microgravity: movement in weightlessness
James R Lackner 1 and Paul DiZio 2
Microgravity provides unique, though experimentally
challenging, opportunities to study motor control. A traditional
research focus has been the effects of linear acceleration
on vestibular responses to angular acceleration. Evidence
is accumulating that the high-frequency vestibulo-ocular
reflex (VOR) is not affected by transitions from a 1 g linear
force field to microgravity (<1 g); however, it appears that the
three-dimensional organization of the VOR is dependent on
gravitoinertial force levels. Some of the observed effects of
microgravity on head and arm movement control appear to
depend on the previously undetected inputs of cervical and
brachial proprioception, which change almost immediately in
response to alterations in background force levels. Recent
studies of post-flight disturbances of posture and locomotion
are revealing sensorimotor mechanisms that adjust over
periods ranging from hours to weeks.
Addresses
Ashton Graybiel Spatial Orientation Laboratory, Brandeis University,
Waltham, Massachusetts 02954, USA
le-rnail: lackner@binah.cc.brandeis.edu
2e-rnail: dizio@binah.cc.brandeis.edu
Abbreviations
CCS
Coriolis cross-coupled stimulation
g
accelerationdue to gravity
GIF
gravitoinertialresultant force
VOR
vestibulo-ocularreflexes
Current Opinion in Neurobiology 1996, 6:744-750
© Current Biology Ltd ISSN 0959-4388
Introduction
Only a few systematic studies of movement control have
been carried out in microgravity conditions. Here, we will
briefly outline how microgravity is achieved and what
factors need to be taken into account when conducting
and interpreting microgravity movement studies. We also
discuss observations on vestibulo-ocular and oculomotor
function, eye-hand coordination, arm control, and posture
in microgravity. A key emphasis of this review is that in
microgravity, some adaptive changes in m o v e m e n t control
occur extremely rapidly in responw to the changes in
postural load that occur during fol~c changes. We will
conclude by briefly discussing how inertial perturbations
of movement trajectories can serve to discriminate among
various theories of movement control.
' M i c r o g r a v i t y ' a n d h o w it is a c h i e v e d
Parabolic flight and orbital space flight can generate
weightless conditions of significant duration. T h e basic
concept underlying weightlessness in parabolic flight is
illustrated in Figure la. At the top of the parabola, there
is a period of weightlessness or microgravity because
the resultant of the lift, drag and thrust forces acting
on the aircraft is effectively zero. In orbital space flight
(see Figure lb), as the spacecraft moves forward, it is
accelerated towards the earth by the force of gravity,
causing it to move in a curvilinear path around the earth
at a near constant altitude. Thus, in orbit, the spacecraft
continuously 'falls' around the earth. Orbital velocity is
inversely related to orbital elevation, being much greater
for lower elevations. A spacecraft at an elevation of 22 300
miles and an orbital velocity of 1.9 miles s-1 has a period
of revolution of 24h; therefore, it is geosynchronous
and hovers above the same location on the earth. T h e
important point to recognize is that neither in parabolic
flight nor in orbital flight is there true microgravity (or the
absence of an attraction force). Instead, there is a condition
of free fall such that the sum of the mechanical contact
forces acting on the occupants of the craft is effectively
zero. Astronauts experience weightlessness in orbital flight
because of the absence of external contact forces acting
on their body, not because of an absence of gravity (g).
In parabolic flight, the aircraft and pilot fall at the same
rate under the influence of gravity, so they can only exert
momentary unbalanced contact forces on each other.
T h e otolith organs of the inner ear are unloaded in
weightless conditions because the net, external contact
force acting on the body is zero. This means that, except
for voluntary or passively imposed head movements that
will generate transient shear of the otolith membranes,
the otoliths do not provide orientationally relevant signals
in microgravity. Their resting discharge pattern will
not be influenced by static head orientation; therefore,
the static otolith-spinal and otolith-oculomotor influences
that are normally present and that depend on head
orientation relative to gravity are absent. T h e peripheral
hydrodynamics of the semicircular canals are basically
independent of linear acceleration and, therefore, are
unaffected by weightless conditions [1].
To interpret experiments on m o v e m e n t control carried out
in weightlessness, it is critical to realize the importance of
contact forces acting on the body under normal terrestrial
conditions. Einstein's equivalence principle states that no
measuring device can distinguish between inertial and
gravitational forces, nor, by extension, can any sensors
of the body. It is the mechanical cor~tact forces on the
feet that make posture and locomotion control possible in
humans. T h e support surface resists the acceleratory force
of gravity by providing an equal and opposite force that
prevents downward acceleration. It is this resistive force
acting on the feet that a scale measures as weight. Walking
would not be possible except for the frictional resistance
Motor function in microgravity: movement in weightlessness Lackner and DiZio
?45
Figure 1
Two means of generating microgravity.
(a) Parabolic flight. In straight and level
flight, the external forces of lift (L), drag
(D) and thrust (T) resist the gravitational
pull (mg) on the aircraft. Consequently,
the aircraft maintains level flight. In
parabolic flight, the sum of external forces
is zero, so the aircraft and occupants
fall at the same rate and are unable to
exert sustained contact forces on each
other. (b) Orbital space flight. Outside
the earth's atmosphere, L and D are
negligible, so no T is required to maintain
orbital velocity; therefore, L + D + T - - O .
As the spacecraft in orbital flight is not
exposed to external contact forces, it
cannot exert sustained contact forces
on its occupants.
© 1996 CurrentOpinion in Neurobiology
746
Neural control
of the ground under the feet resisting the backward thrust
force exerted during a forward step.
Contact forces are also critical for other aspects of motor
control. If a rightward head movement is made, the neck
muscles exert a clockwise torque on the head, but they
also exert a counter-clockwise torque on the torso. This
latter torque is countered by the friction between the
feet and the ground if the individual is standing. T h e
same considerations apply to muscle torques generated
by movements of the arms or other parts of the body.
Platform divers use these reaction force couples to change
their body orientation and configuration when moving
through the air. Recognizing the role that contact forces
play in allowing the movement of specific body parts
without displacing the rest of the body is crucial for
both constructing apparatus and designing interpretable
experiments for microgravity conditions.
Factors complicating the interpretation of
microgravity experiments
Before discussing individual experiments, it is useful to
have in mind some of the advantages and disadvantages
of using parabolic and orbital flight for studying movement
control (summarized in Table 1). T h e primary advantage
of parabolic flight is the ability to achieve microgravity
within seconds. The primary disadvantage is the brief period available for carrying out experiments (approximately
20-30s per parabola), which often necessitates having to
make many parabolas per flight (usually about 40) so as
to achieve adequate experimental time. The weightless
phases of the parabolas are separated by transitions to
hypergravity (1.8-2.0g) steady state levels, which also
last 20-25s. Most individuals rapidly adapt to these
fluctuations in the force levels, both in terms of perception
(i.e. how heavy they feel in the high-force periods [2,3])
and in terms of motor control v i s a vis locomotory
movements made during greater than 0g gravitoinertial
force levels [4,5]. Such rapid adaptation has to be taken
into account when interpreting experimental results; for
example, subjects who are allowed to practice movements
or who are only tested after being passively exposed to
many parabolas may be largely adapted to the new force
level before thc collection of data begins.
The main advantage of orbital flight is that it permits
longer exposures to microgravity, ranging from days to
months or even years. The disadvantages, in terms
of experimental interpretation, include the long time
between launch and both being in orbit and being able
to participate in experiments. Astronauts and cosmonauts
wear space suits for launch and have to get out of these
suits when in orbit. In the US space shuttle program, it is
necessary to unstow and set up the experimental apparatus
after entering orbit. Adaptation of motor and 'postural'
control to the 'zero g' environment is taking place
during this time. Before participating in an orbital flight
project, astronauts have to undergo extensive training
in parabolic flight, so they are already experienced at
operating in microgravity. It is usually several hours
after entering orbit before experimental data can be
collected. Moreover, in dedicated life sciences missions,
each participating astronaut or cosmonaut is involved
in many experiments that involve different apparatus.
Setting up the experiments and conducting them can
occupy virtually all of the astronauts' waking hours. Data
collection periods for an individual experiment are usually
very restricted and repeat testing with optimal spacing is
not always possible. For example, the initial test might
take place several hours after entering orbit, and the next
test may only take place several days later; sometimes, the
first test may not even take place during the first flight day.
Many other factors potentially affect test results as well.
For example, there is no hydrostatic pressure in a weightless environment. Consequently, there is a substantial
rostral re-distribution of body fluids that commences upon
entry into weightlessness. This re-distribution of fluids
leads to a decrease in lower-body mass, especially in the
legs, and an increase in blood and lymph perfusion of the
upper body [6]. It is not certain whether this affects muscle
viscosity and compliance. In addition, with continued
exposure to weightlessness, muscle mass and strength
diminish in response to the decreased load demands.
Muscle fiber types may also undergo changes, with a shift
toward fast, fatiguable response types [7,8°]. Moreover,
approximately 70% of astronauts experience space motion
sickness to some degree during the first three or four
flight days [9]. T h e anti-motion sickness drugs that are
commonly used to combat sickness, such as scopolamine
and promethazine, have soporific effects. These factors,
coupled with the many tests involved, can lead to chronic
fatigue.
Post-flight testing is also subject to a number of complications. Astronauts on shuttle flights generally are excited
the 'night' before re-entry and have a hard time sleeping
(the same is true before launch). After landing, before
leaving the space shuttle, many astronauts intentionally
move around to re-adapt themselves to 1 g so that they
will be able to walk off the shuttle. This re-adaptation
complicates the interpretation of post-flight assessments
of posture, balance, and movement control. In addition,
astronauts experience considerable fatigue post-flight,
both because they have busy in-flight and post-flight
schedules and because they have to re-adapt their bodies
to a 1 g force level. Moreover, the post-flight tests (which
are used to gather data for comparisons with the in-flight
observations) also place great time and physical demands
on the astronauts.
In sum, many factors complicate the interpretation
of in-flight and post-flight data. Ground-based mission
simulations that precisely mimic in-flight and post-flight
time lines and experimental protocols have not yet been
developed. Such simulations are expensive and time
Motor function in microgravity: movement in weightlessness Lackner and DiZio
747
Table 1
Experimental advantages and disadvantages of parabolic flight and orbital flight.
Experimental factor
Parabolic flight
Orbital flight
Duration of
microgravity
20-30S (which limits test duration and
and trial frequency)
Days (which enables observation of
long-term effects)
Periodicity of
microgravity
Alternates between micro- and hypergravity
about every 30 s (confounding factors
include interactions between adjustments
to force transitions and adjustments to
Continuous microgravity (confounding factors
include musculo-skeletal deconditioning,
fluid shifts and neuromotor adjustments)
microgravity)
Delays before testing
Possible to test immediately after
transition to microgravity (which
permits observation of transient
changes and rapid adaption)
Testing only possible an hour or more after
exposure to microgravity and extensive
activity (which prevents observation of
transient and rapid adjustments)
Test schedule
Controlled by experimenter
Constrained by the astronaut's busy schedule
Workload/fatigue
The subject's only task is to serve as a
subject, within a normal sleep schedule
The astronaut's time as a subject is a small
part of the busy schedule performed while
working shifts
Angular acceleration
Aircraft rotation is a significant
factor in some experiments
Significant angular accelerations
are exceptional
Motion sickness
30-50% of subjects are sick if not taking
medication, but the type and amount of
medication can be controlled
50-70% of astronauts are sick the
first 3-4 days, and the experimenter
does not control the medication
consuming, but they would be enormously helpful for
interpreting space flight data.
Vestibulo-ocular
reflexes
A primary concern in studies of movement control
in weightless conditions has been to understand the
conjoint action of the weight-sensitive otoliths and the
weight-insensitive semicircular canals [10]. In the 70s, a
study called the skylab M-131 experiment was designed
to assess responses to Coriolis cross-coupled stimulation
(CCS), an unusual combination of linear and angular
acceleration that is elicited by tilting the head while
sitting in a rotating chair [10]. CCS usually evokes severe
disorientation and nausea on earth. When first tested in
orbit on mission day six, the astronauts in the study found
that CCS elicited no disorientation or nausea [10]. These
dramatic results had no clear interpretation, however,
because of the time delay before testing in orbit and an
absence of eye movement recordings. A later series of
parabolic flight studies assessed whether the change in
response to CCS was immediate or developed gradually
in microgravity (discussed below).
Step changes in angular velocity coupled with eye
movement (nystagmus) recordings were used to study the
influence of gravitoinertial force levels on the vestibuloocular reflexes (VOR) in parabolic flight. These studies
showed that the gravitoinertial force level had no influence
on the peak slow phase velocity of nystagmus, indicating
that the peripheral response of the semicircular canals is
(during brief exposures at least) independent of linear
acceleration [11]. T h e time constant of nystagmus decay
is lower both at 0g and 1.8g than at lg, indicating
an immediate decrease in velocity storage. Suppression
of post-rotary nystagmus by post-rotary tilting of the
head (so-called 'dumping') has not been observed in 0g
[12]. Such findings implicate tonic levels of otolithic and
somatosensory discharge along with canalicular, cervical
and motor activity in regulating the velocity storage
mechanism of the VOR. Space flight observations have
confirmed the absence of gain changes and the absence of
nystagmus dumping by head movements in 0g [13,14°].
T h e physiological data available are quite preliminary
but suggest an increase in end-organ activity with
continued exposure to microgravity [15] but no difference
in post-flight VOR gain or velocity storage relative to
pre-flight values [16].
T h e torsional VOR under terrestrial conditions is influenced both by gravitational force and by the dynamic
linear accelerations generated by head movements. In
space flight, the tonic shear owing to gravity is absent.
Preliminary evidence suggests that the torsional VOR goes
through adaptive changes [17]. Gain initially decreases,
then increases during the flight to greater than pie-flight
levels. Post-flight, there is a decreased gain, relative to
pre-flight, apparent even after four days.
Oculomotor
control
Gaze maintenance in the dark (in response to the
instruction 'fixate straight ahead') has been studied in
parabolic flight both during transitions and at steady
748
Neuralcontrol
state force levels [18]. Many individuals experience body
inversion upon the transition to microgravity, so that
changes in gaze can reflect either vestibulo-ocular or
perceptual effects [19]. Studies of vertical optokinetic
nystagmus tend to show an increase in the slow phase
velocity for 'downward' visual motion, a decrease for
upward slow phase velocity in 1.8-2.0 gz, and a slight (or
insignificant) reverse relationship in 0 gz relative to straight
and level flight [20]. (Here, upward and downward are
specified in relation to the body's longitudinal z-axis.)
Space flight observations point to a tendency for both
upward and downward optokinetic nystagmus gain to be
diminished in microgravity [21,22]. In general, the findings
support a roughly linear summation of optokinetic eye
velocity and otolith signals, the latter being diminished in
microgravity (<1 g) and enhanced in hypergravity (>1 g).
In space flight, saccadic eye movements display increased
latencies and decreased peak velocities in some studies
(see [23]), but the opposite in others [24]. T h e studies
showing diminished performance were conducted early in
flight, often on motion sick subjects; the study reporting
enhanced performance [24] was conducted on the last
flight day in orbit. Horizontal pursuit eye movements, both
with head-free and head-fixed conditions, show no inflight changes. By contrast, vertical pursuit eye movements
are affected: upward pursuit being accomplished primarily
by saccades and downward pursuit by a combination of
saccades and smooth eye movements [23].
Arm movement control
Several parabolic flight studies have shown an enhancement of tonic vibration reflexes in 1.8 g and a diminution
in microgravity [25,26]. This suggests a decreased muscle
spindle gain, at least during initial exposure to microgravity. A systematic study of arm movement kinematics
supports this conclusion: subjects trained under l g
conditions made unsupported forearm movements of
particular amplitudes and frequencies in a horizontal and a
vertical plane [27]. When subjects were tested blindfolded,
in parabolic flight, rapid movements were found to be
unaffected by the g level or arm orientation. By contrast,
slow movements showed a smaller amplitude and more
frequent dynamic overshoots of final position in 0 g relative
to 1 g, both for horizontal and vertical arm orientations.
These findings are consistent with a decreased spindle
gain in 0 g, which would also imply a decrease in position
sense accuracy. (The latter changes are commonly reported
by astronauts [28].) An important feature of this study is
the absence of gravitoinertial resultant force (GIF)-related
differences for horizontal and vertical forearm movements.
It indicates that the activity of the muscles that are
not directly involved in the movements of the forearm
but that support the forearm are involved in planning
movements involving the forearm. This means that the
support musculature for maintaining posture can function
as a linear accelerometer, keying the nervous system into
the expected load demands for movements in different
axes. Thus, considerable 'automatic self-adjustment' for
background force level takes place simply by virtue of
exposure to a changed background force level.
Eye-hand coordination
Few studies of eye-hand coordination have been carried
out. Early observations in parabolic flight were often
contradictory: some showed overreaching in 0g and
underreaching in hypergravity [29], whereas others showed
the opposite [30]. Such studies are complicated by the fact
that perceptual mislocalizations of isolated targets occur
as a function of background force level. In 0g, a target
will be seen below its true position, whereas in 1.8g, it
will be seen above its true position. This phenomenon is
called the 'elevator illusion' and is a variant form of the
oculogravic illusion [31-35].
Postural control in microgravity
In a weightless environment, posture does not have
the same meaning as on earth where posture is the
maintenance of a body attitude against gravity. Early
studies focused on postural sub-systems such as excitability of motor neuron pools [36], but recent ones have
concentrated on functional synergies [37-40].
One method for studying posture in microgravity is to
attach an astronaut's feet to the deck of the spacecraft.
In some experiments, the body is also artificially loaded
by means of bungee cords. Space flight experiments
have shown that the posture assumed when the feet
ate attached in-weightlessness differs from that assumed
on earth, in that there is greater flexion of the knees
and trunk [41]. On earth, arm raising is associated with
anticipatory postural adjustments that compensate for the
impending balance consequences of the arm movement,
both dynamic and static [42]. In weightlessness, arm
raising is associated with anticipatory compensations of
the hip, similar to those exhibited on earth, but the
head exhibits more displacement. Rapid backward and
forward bending movements of the trunk made with the
feet attached are associated with forward and backward
displacements of the hips and knees, as under terrestrial
conditions. T h e kinematics are also similar, especially for
forward trunk displacements. Interestingly, the patterns of
muscle activity necessary to create these axial synergies in
microgravity are quite different from on earth [38].
These and other observations suggest that there is a
gradual re-interpretation of muscle proprioceptive signals
during prolonged exposure to microgravity. Proprioceptive
illusions of body displacement induced by ankle muscle
vibration during bungee loading reflect a shift from
perceived changes in whole body orientation to changes
in foot angle [40]. Post-flight studies of posture and
locomotion have shown that return to normal occurs over
several hours for some forms of adjustment, but can take
days or even weeks for other forms [43°,44°,45].
Motor function in microgravity: movement in weightlessness Lackner and DiZio
749
Figure 2
A Coriolis force (FCor) is generated
when a person sitting in a rotating room
voluntarily moves an arm (or other body
part). The force is proportional to the
limb's mass (m), its velocity (v) relative
to the room, and the angular velocity of
room rotation (o)). The Coriolis force is
always perpendicular to the movement
direction: for example, it is rightward for
forward-reaching movements made during
counter-clockwise rotation.
Inertial force perturbations of movement
trajectory
Artificial gravity environments are useful for studying
adaptive m o v e m e n t control. Artificial gravity is the centripetal force associated with rotation [46,47°]. In a rotating
spacecraft, the walls serve as the 'floor' on which astronauts
walk. On earth, if one is at the center of a fully enclosed
rotating room, the centripetal force associated with low
rates of revolution (e.g. 5-10 rpm) is negligible and below
threshold for the otolith organs. In these circumstances,
all the forces on the body are normal unless one moves.
Then, if a pointing m o v e m e n t is made, an inertial Coriolis
force is generated (Figure 2). This force is proportional to
the product of the velocity of the arm (or other body part)
m o v e m e n t and the rotational velocity of the environment,
and it acts in the direction opposite to that of rotation. T h e
Coriolis force is an inertial non-contact force (unlike the
mechanical forces used in traditional load compensation
and m o v e m e n t perturbation experiments) that is present
only during the arm m o v e m e n t and acts only on the arm.
By contrast, one cannot put just the arm in microgravity.
Studies using Coriolis perturbations [46,47 °] have provided
compelling evidence against c~ equilibrium point models
of m o v e m e n t control [48], showing both a failure of
equifinality predictions as well as independent adaptation of m o v e m e n t path and end position. Moreover,
extraordinarily rapid adaptation occurs, with m o v e m e n t
accuracy being regained after five or ten movements. T h e
advantage of this paradigm is that the rotating room can be
brought up to speed very slowly so that the subject ahvays
feels perfectly stationary and never experiences unusual
forces until trying to move a limb. By contrast, both
in parabolic flight and orbital flight, the subject's entire
body is exposed to the unusual force level and, therefore,
senses the changed force level before initiating movement.
Rotating chairs are inadequate tools for studying Coriolis
perturbations of m o v e m e n t trajectories because subjects
sense the self-rotation and may attempt to compensate for
it voluntarily or automatically.
Conclusions
Space flight provides opportunities to study long-term
motor adaptation to weightlessness, especially for motor
mechanisms with relatively long adaptive time constants. Parabolic flight is better suited to studying the
consequences of force transitions and rapidly adapting
motor processes. Virtually immediate adjustments of motor
control can be carried out on the basis of the nervous
system detecting changed force demands for maintaining
posture. T h e use of Coriolis inertial perturbations provides
a new experimental tool for studying adaptive m o v e m e n t
control.
Acknowledgements
The authors' work is supported by National Aeronautic and Space
Administration grants NAGW-4374 and NAGW-4375.
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