Laboratory of Neurobiology and Movement, Centre National de la Recherche Scientifique, 13402 Marseille Cedex 20, France
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ABSTRACT |
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Vernazza-Martin, S., N. Martin, and J. Massion. Kinematic Synergy Adaptation to Microgravity During Forward Trunk Movement. J. Neurophysiol. 83: 453-464, 2000. The aim of the present investigation was to see whether the kinematic synergy responsible for equilibrium control during upper trunk movement was preserved in absence of gravity constraints. In this context, forward trunk movements were studied during both straight-and-level flights (earth-normal gravity condition: normogravity) and periods of weightlessness in parabolic flights (microgravity). Five standing adult subjects had their feet attached to a platform, their eyes were open, and their hands were clasped behind their back. They were instructed to bend the trunk (the head and the trunk together) forward by ~35° with respect to the vertical in the sagittal plane as fast as possible in response to a tone, and then to hold the final position for 3 s. The initial and final anteroposterior center of mass (CM) positions (i.e., 200 ms before the onset of the movement and 400 ms after the offset of the movement, respectively), the time course of the anteroposterior CM shift during the movement, and the electromyographic (EMG) pattern of the main muscles involved in the movement were studied under both normo- and microgravity. The kinematic synergy was quantified by performing a principal components analysis on the hip, knee, and ankle angle changes occurring during the movement. The results indicate that 1) the anteroposterior position of the CM remains minimized during performance of forward trunk movement in microgravity, in spite of the absence of equilibrium constraints; 2) the strong joint coupling between hip, knee, and ankle, which characterizes the kinematic synergy in normogravity and which is responsible for the minimization of the CM shift during movement, is preserved in microgravity. It represents an invariant parameter controlled by the CNS. 3) The EMG pattern underlying the kinematic synergy is deeply reorganized. This is in contrast with the invariance of the kinematic synergy. It is concluded that during short-term microgravity episodes, the kinematic synergy that minimizes the anteroposterior CM shift is surprisingly preserved due to fast adaptation of the muscle forces to the new constraint.
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INTRODUCTION |
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Purposeful motor acts consist of two apparently
contradictory tasks. One is to move one or several body segments toward
a goal, and the other is to change the position of other segments to
maintain equilibrium. One of the major functions of the CNS is to
coordinate equilibrium and movement. In humans, static equilibrium during stance is maintained when the center of mass (CM) projection is
located inside the supporting area delimited by the feet. During forward or backward upper trunk movements, a kinematic synergy has been
described by Babinski (1899), which consists in a
simultaneous displacement of the hip and knee in a direction opposite
to the upper trunk movement and which is responsible for the
stabilization of the CM projection within the base of support. This CM
stabilization is here considered as the result of the kinematic synergy
that is defined as the ratio between the hip, knee, and ankle angle changes occurring during the movement.
The control of the kinematic synergy and the minimization of the CM
shift during trunk bending have been demonstrated by two sets of
studies. The first set is based on experimentation in normogravity. The
kinematic synergy may result from two mechanisms: a passive interaction
between body segments and an active control. The dynamic interactions
between segments have been modeled by Ramos and Stark
(1990), who have shown that acceleration of the trunk causes
contiguous segments to accelerate in the opposite direction according
to the action-reaction law. With feet fixed to the floor, the net
result of the interaction is a backward CM shift that would cause
falling. Therefore the kinematic synergy may not be due only to the
dynamic interactions between body segments but also to a central
control that may coordinate the motion of the various joints
participating in the kinematic synergy (Alexandrov et al.
1994
, 1998
; Crenna et al. 1987
;
Oddsson and Thorstenson 1987
; Pedotti et al.
1989
). Indeed, this argument is mainly based on three pieces of
evidence. First, Crenna et al. (1987)
showed that the
peak velocity of both the upper and lower body segments was reached
synchronously in all the subjects studied. There may exist a central
control that synchronizes the timing of the upper and lower body
segmental movements. Second, the kinematic synergy is initiated by a
stable muscle synergy simultaneously involving trunk, thigh, and leg
muscles (Crenna et al. 1987
; Oddsson and Thorstenson 1987
; Pedotti et al. 1989
). This
finding also indicates that a single central command may coordinate the
motion of the various joints participating in the kinematic synergy.
Third, a principal component analysis on the ankle, knee, and hip angle changes occurring during forward and backward trunk movements showed
that only one principal component (PC1: one degree of freedom multijoint movement) accounted for >99% of the whole movement, which
was characterized by fixed ratios between the changes in ankle, knee,
and hip joint angles (Alexandrov et al. 1994
,
1998
). The same proportion of the movement was
represented by PC1 at both fast and slow velocities. These observations
suggest that the high level of coupling between the angles does not
entirely result from dynamic interactions between segments, which
depend on movement velocity, but that this coupling is centrally controlled.
The second set of studies concerns experimentation in microgravity.
Unfortunately, these studies can be usually performed only on a small
number of subjects. The specific aim of these investigations has been
to see whether the kinematic synergy during trunk bending, minimizing
the CM shift during movement under equilibrium constraints, is
abolished when the equilibrium constraints disappear. During long-term
space flights, the CM shift during movement was minimized by a
kinematic synergy that remained invariant in spite of the absence of
equilibrium constraints (Massion et al. 1992, 1993
, 1997
). The same results have been
observed during trunk bending performed under water (Massion et
al. 1995
). These observations suggest that the kinematic
synergy results from a stereotyped control that is centrally programmed
independently from gravity constraints. However, this invariant
kinematic synergy is implemented by a muscular synergy that is strongly
modified in microgravity. For example, backward trunk bending in
normogravity is initiated by a set of muscles behind the body (erector
spinae, semimembranosus, and soleus) (Crenna et al.
1987
; Oddsson and Thorstenson 1987
; Pedotti et al. 1989
). During a long-term space flight,
the early soleus activation is replaced by an early tibialis anterior
activation (Massion et al. 1992
). The preservation of
the kinematic synergy in contrast to the adaptation of the muscle
synergy in microgravity is rather surprising. It suggests that,
although the afferent inputs from sensors monitoring the gravity axis
(otoliths, body graviceptors) (see Dietz et al. 1992
;
Mittelsstaedt 1998
) and the body configuration
(proprioceptive inputs) are biased, an internal representation of the
body segment geometry, mass, and inertia is preserved and is used
during trunk bending to minimize the anteroposterior CM shift. The
sensory inputs from the feet in contact with the shoes and the space
cabin floor to which they are fixed should play an important role in
this representation. The possible perception of body segments inertia
that should remain in microgravity might be another source for updating
the representation (Pagano et al. 1996
).
Previous investigations in microgravity had, however, a series of limitations. First, they had been performed on a restricted number of subjects (only 1 or 2 per flight). Second, they concerned in-flight recording 1 or 2 wk after space flight onset, where long-term adaptation to microgravity already took place. They did not inform about the very short-term adaptation that characterizes the microgravity episodes of parabolic flights. Third, no accurate quantification of the kinematic synergy was performed on the basis of the principal components analysis as well as no extensive analysis of the electromyographic (EMG) pattern including distal, proximal, and axial muscles (the EMG analysis was restricted to the distal muscles). The present study was performed during parabolic flights, with kinematic and EMG data acquisition comparable to ground-based experiments. The three following questions were addressed. 1) Is the anteroposterior position of the CM during trunk movement still minimized in microgravity in absence of equilibrium constraints and how is the time course of the CM shift during movement both in normo- and microgravity? 2) Is the coupling between hip, knee, and ankle angle changes during movement maintained during short-term microgravity episodes? 3) How does the EMG pattern inform on how this coupling is implemented in microgravity?
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METHODS |
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Experimental protocol
Experiments were performed in a Caravelle aircraft on five adult subjects. None of the subjects had previously been exposed to parabolic flight conditions. The subjects wore special shoes that were attached to a platform through a ski binding (Fig. 1). First, they were asked to adopt an erect posture, to look straight ahead, and to keep their hands clasped behind their back. Then, in response to a tone, they were instructed to bend the trunk (the head and the trunk together) forward by ~35°, as fast as possible, to hold the final position for 3 s and then recover the initial erect posture.
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Two experimental series were performed by each subject: one under standard conditions of a steady-level flight and the other during microgravity episodes of the parabolic flight. During the flight, 30 parabolas were executed, each of them providing 20 s at a level of ~0.02 ± 0.018 (SD) g. All recorded parabolas had the same pattern: the pull-up and pull-out phases were both usually stabilized around a 20-s period of 1.8 g. The zero-g phase occurred between the two phases. Two consecutive parabolas were separated by a steady-level flight phase lasting from 2 to 5 min. The subject first performed a set of seven trials in microgravity. Given the short duration of the microgravity episodes, no more than two trials could be performed during each parabolic phase. A second set of seven trials was performed in normogravity during a steady-level flight phase of 5 min.
Recording system and data processing
Kinematic analysis was performed by means of the E.L.I.T.E.
system: an automatic TV-image processor (Ferrigno and Pedotti 1985). Two cameras placed 3.5 m in front of the subject,
recorded the three-dimensional (3D) movements of seven passive
retroflective markers placed on the right side of the subject on the
head (2: external meatus, external angle of orbit), acromion (1), iliac crest (1), trochanter (1), knee joint (at the level of the tibial plateau) (1), and ankle (over the lateral malleolus) (1). Under the
present experimentation, the field of view explored by the system was 2 * 2 * 1 m, and the accuracy was 0.67 mm. Because the movements
were performed in the sagittal plane (perpendicular to the long axis of
the aircraft), only this plane was included in the analysis. The
sampling frequency was 100 Hz.
EMG activity was recorded (using surface bipolar configuration with an interelectrode distance of 2 cm) on the right side of the subject, from the rectus abdominis (RA), erector spinae at the level of L4 (ES), vastus lateralis (VL), semimembranosus (SM), tibialis anterior (TA), and gastrocnemius lateralis (GL). The signal was amplified (gain 1,000) and filtered through a 10- to 200-Hz band-pass. The sampling frequency was 500 Hz.
Parameters recorded
To describe the trunk movement characteristics, the following parameters were measured on the basis of the kinematic recordings: 1) trunk movement duration, 2) trunk movement amplitude (difference between the final stabilized position of the trunk segment 400 ms after the end of the movement and the initial position of this segment), and 3) mean angular velocity of the trunk (Vmean), corresponding to the ratio between the amplitude of the trunk segment and the movement duration.
Biomechanical modeling
A biomechanical model of the CM was developed from the kinematic
data, based on the anthropometrical model of Zatsiorsky and Seluyanov (1983).
For each body segment (i), the anthropometric data of
interest were as follows: 1) the mass of the segment
(mi) and 2) the distance
between the CM position and the axis of rotation of the segmental
distal joint (lCMi). The kinematic data of
interest were as follows: 1) the position of the axis of
rotation of the distal joint (xOi) given
by the position of the markers placed on the body and 2)
the angle defined by each segment (delimited by 2 markers) with respect to the horizontal axis (i).
The general equation obtained was as follows
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Each measure of the theoretical and actual CM shift was the difference between the value at the time of measurement and t0 (200 ms before the movement onset). Then we calculated a CM shift compensation index (CI in %) corresponding to the difference between the theoretical and the actual CM shift normalized with respect to the theoretical CM shift (see Fig. 2). This index is global and does not reflect specific contribution of mechanisms determining the CM horizontal position, such as dynamic interactions between segments, the effect of gravity forces and the active control by the CNS. CI was calculated during two time periods: an early CM compensation from 100 ms after the movement onset to 400 ms after the movement onset, and a late CM compensation from 200 ms before the movement offset to 400 ms after the movement offset. The index values represented in Figs. 6 and 7 correspond to the averaged values calculated for individual trials for each subject.
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The trunk movement onset and offset times were defined as points on the theoretical CM velocity curve (calculated from theoretical isolated trunk displacement), where it crossed a threshold corresponding to 5% of the peak velocity.
CI quantifies the compensation for the theoretical CM shift that occurs
during trunk bending. The following three situations can occur.
1) The actual CM shift was equal to or bigger than the
theoretical CM shift. In this case, CI yields a value 0%, which
means that there was no compensation for the CM shift. 2) The actual CM shift was smaller than the theoretical CM shift. The
value of the index ranges between 0 and 100%, expressing the degree of
a partial CM compensation. 3) The actual CM shift was zero
or occurred in the opposite direction to the theoretical CM shift. Here
the value of the index is
100%, which means that either a complete
compensation or overcompensation for the CM shift occurred.
Principal components analysis
Kinematic synergies involved in the CM control during the
movement were quantified by performing a principal components analysis on the angular changes occurring at the hip, knee, and ankle joints using the procedure described by Mah et al. (1994) and
Alexandrov et al. (1998)
. This analysis quantifies
linear covariations occurring over time between these three joint angles.
The general principle is that all the angles studied
(1,
2, and
3: hip, knee, and ankle angle, respectively)
during the trunk movement in the sagittal plane can be expressed by a
transformation matrix as a linear combination of three components
PC1, PC2, and PC3 (see Fig. 3).
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The linear combination is expressed in the form
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The principal component analysis method yields a transformation matrix
M in such a way that the components are linearly independent and ranked in order of decreasing variance. PC1:
the first component is therefore the component with the highest
variance. The percentage participation of a component
PCi variance in the total variance, that is to
say the contribution of a component to the movement is defined by
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To estimate the intertrial variability of the component
PCi contribution to all three angles, an index
V (%) was calculated
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From the principal component analysis, the following variables were
analyzed: 1) the contribution of the
PCi component to the movement,
i, 2) the contribution of a
component PCi to each angle
i(t) represented by
rij, and 3) the index of
intertrial variability of the component PCi contribution to all three angles (V index).
EMG analysis
The EMG analysis was based on the muscle pattern's observation and the qualitative comparison of the superposition of trials under both normo- and microgravity, the results obtained with this method being enough glaring.
Statistical analysis
Not all data could be analyzed. Varying between subjects, the
number of trials used for analysis ranged from three to seven. The
mistrials were due to extreme experimental conditions. Including the
total number of trials in normo- and microgravity, trials that were
lost among all 5 subjects were 18 of 70. A nonparametric test
(Mann-Whitney test) was used for assessing the effect of gravity on the
following variables: the amplitude, duration, mean angular velocity of
the trunk, initial and final CM position, contribution of the
PCi component to the movement
(i), and contribution of
PCi to each angle
(rij). The significance level was set at
P < 0.05.
The CM compensation index was first subjected to the Wilcoxon test to determine whether there existed a significant difference between the calculated index and the 0 value corresponding to a lack of compensation. Then the time courses of both the early and late CI were studied first by performing an ANOVA and then a linear regression analysis, to determine the sign of these changes (increase or decrease during time).
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RESULTS |
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Figure 4 shows a trunk flexion in one subject. Six trials in normogravity (1 trial has been eliminated) and seven trials in microgravity are presented. Both in normo- and microgravity, the shoulder marker moved forward, whereas the hip and knee markers moved in the opposite direction. The only difference was that in microgravity, the initial positions of the shoulder, hip, knee, and CM were more variable. This axial synergy remained unchanged, maintaining in both cases the CM projection within the limits of the support base.
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Kinematic parameters of the trunk movement
The trunk movement amplitude, duration, and the mean angular velocity (Vmean) of the trunk segment were calculated for the five subjects during the forward trunk movement under both normo- and microgravity. The range of individual mean value of the movement amplitude varied from 35 ± 3° to 62 ± 3° in normogravity and from 32 ± 3° to 41.5 ± 8° in microgravity. There was a significant decrease in three of the five subjects (S2: Z = 0.036, P < 0.05; S3: Z = 0.005, P < 0.01; S5: Z = 0.003, P < 0.01), whereas the decrease for the last two did not reach the level of significance. The movement duration remained unchanged (varying between subjects the variation was from 636 ±137 ms to 1,052 ± 93 ms in normogravity and from 650 ± 83 ms to 1,010 ±130 ms in microgravity). This resulted in a lower mean velocity varying between subjects from 34 ± 3°/s to 67 ± 5°/s in normogravity and from 33 ± 7°/s to 56 ± 10°/s in microgravity.
Analysis of the center of mass position and compensation index
The CM time course in normo- and microgravity as illustrated in Fig. 4 was further analyzed in two ways. First the initial and final positions were measured in each trial and subject. Second, the CM shift was evaluated by the CI.
Initial and final CM position
The initial and final CM positions obtained through biomechanical modeling were validated in similar experiments performed on the ground, on a force platform. The validation was performed in two subjects (S1 and S4). The results showed that the mean difference between the calculated CM positions and the CM positions measured on the platform were 7.5 ± 2.7 mm and 5.9 ± 3.7 mm, respectively.
Figure 5A shows for each
subject and each trial the initial anteroposterior CM position in
normo- and microgravity, 200 ms before the movement onset. For each
subject, the 0 value corresponds to the ankle joint axis. Varying
between subjects, the mean initial CM position was situated from 2 to
11 cm in front of the ankle joint axis. An ANOVA showed that the
initial CM position did not change significantly in both normo- and
microgravity in four of the five subjects (S1, S2, S3, and
S4). In subject S5, the mean initial CM position
in microgravity was situated 2.8 cm in front of that in normogravity
(S5, Z = 2.68, P < 0.01).
This shift was nevertheless far from exceeding the stability limits.
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Figure 5B shows for each subject and each trial the initial (200 ms before the movement onset) and the final (400 ms after the movement offset) CM position in microgravity. An ANOVA showed that the final CM position did not change with respect to the initial position in any subject except for subject S3, where the mean final CM position was situated 3.1 cm posterior to its initial position (S3, Z = 2.1, P < 0.05).
CM compensation index during movement
EARLY CI. Figure 6 shows for each subject, the mean value of the early CI under both normo- and microgravity. Only indexes statistically different from 0 are linked together in the figure. This figure shows that the index differed significantly from 0 as early as 100 ms after the movement onset in four subjects of five, both in normo- and microgravity.
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LATE CI. Figure 7 shows the late CI in each subject under both normo- and microgravity. This figure shows that in all subjects the index was always significantly different from 0 under both normo- and microgravity. A high level of compensation for the CM shift can be noticed during the final part of the movement and during the final stabilization of the trunk.
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Quantitative analysis of the axial synergies by principal components analysis
The contributions of PC1 and
PC2 to the trunk movement for each subject under
normo- and microgravity are shown in Fig.
8. The figure shows that PC1 accounted
for >99% of the movement (1 > 99%),
whereas the contribution
2 of PC2 was lower
than 1%; the contribution
3 PC3 (not shown)
was negligible (<0.2%) under both normo- and microgravity. These
results indicate that a single component accounts for the forward trunk
movement under both normo- and microgravity. This suggests a strong
coupling between joint angles, expressed by a fixed ratio between the
angles through time (see METHODS).
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The intertrial variability of the PC1 contribution to the three angles
('1,
'2, and
'3) was estimated in terms of the index V1 (%) under both normo- and
microgravity. The index fell between 1.9 and 5.4% under normogravity
and between 4.3 and 9.4% under microgravity. The population average
was 3.1 and 6.5%, respectively. This indicates that the variability of
PC1 contribution to all three angles
(
'1,
'2, and
'3) was twice as high in microgravity as in normogravity. Nevertheless, the intertrial variation remained lower than 10%.
The contributions of PC1 to angles
'1,
'2, and
'3, denoted by
r11,
r12, and
r13, respectively, for each subject
under both normo- and microgravity are given in Fig.
9.
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As can be seen from Fig. 9, the contributions of PC1 to
'1 and
'2
(r11 and
r12) were negative, whereas that to
'3
(r13) was positive. Based on
increasing changes in PC1 observed with time, the negative sign in
r11 and
r12 indicates that
'1 and
'2 decreased with time corresponding to
a trunk flexion and a knee extension. In the same way, the positive
sign in r13 indicates that
'3 increased with time, which
corresponds to an ankle extension. Only subject S1 showed a
positive r12 value in microgravity
corresponding to a knee flexion.
The main observation in this figure is that microgravity can generate, in some subjects, a change in PC1 contribution to the three angles. The change predominates at the knee level (r12) and is characterized by decreased knee extension or by switching from knee extension in normogravity to knee flexion in microgravity.
EMG study
Figure 10 shows the EMG pattern
during seven trunk flexions in two representative subjects in both
normo- and microgravity. It can be seen from this figure that the onset
of the trunk movement (as detected on the trunk CM velocity curve,
vertical line) was preceded in normogravity by an early activation of
RA, VL, and TA. The early TA activation has been suggested to be at the
origin of an initial backward shift of the center of pressure, which results in an initial forward CM acceleration (Crenna and Frigo 1991). These agonist EMG activities are followed by an
activation of antagonist muscles (ES, SM, and GL) during the braking
phase of the movement. This muscular synergy has been previously
described in the literature (Crenna et al. 1987
;
Oddsson and Thorstenson 1987
; Pedotti et al.
1989
). Three main effects of microgravity on the muscular
synergy can be seen in Fig. 10. First, tonic EMG activity was
increased, both during erect posture and movement (subject
1: RA and SM; subject 3: VL and TA). Similar
observations were made in the other subjects (not shown, subject
2: VL, TA, and GL; subject 4: RA and VL; subject
5: VL, SM, and TA). Co-contraction was often seen. Joint stiffness
should reduce the intersegmental disturbance when marked changes in the
constraint related to the microgravity makes the control of the
movement less accurate and biases the sensory information
(graviceptors, proprioceptors) on which the control relies. Second, the
initial agonist bursts were reduced or masked by the increased tonic
activity (subject 1 in the figure, subject 4 not
shown). Third, the antagonist bursts involved in the movement during
the braking phase disappeared or were strongly reduced (subjects
1 and 3 in the figure, subjects 2, 4, and
5 not shown). These results demonstrate a marked
reorganization of the EMG activity in microgravity in the whole
population of subjects.
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DISCUSSION |
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The aim of this study on the trunk bending was to answer
three main questions. The first question was whether the
anteroposterior CM position during trunk bending was still regulated
during short-term microgravity in absence of equilibrium constraints
and how was the time course of the control of the CM position organized
under both normo- and microgravity. Three main results were obtained: first, the initial CM position under microgravity was close to that
under normogravity. Second, the final CM position in microgravity was
close to its initial position in the same condition, and third, the
actual CM shift during the movement was always smaller than a
theoretical CM shift, which would have been induced by trunk movement
alone. These results indicate that the CM shift remains minimized in
short-term microgravity episodes, in spite of no equilibrium
constraints and that this minimization persists throughout the whole
movement, as well as during the final period of trunk stabilization. In
addition, the time course of this minimization remains qualitatively
the same under both normo- and microgravity. The minimization of the
anteroposterior CM shift during trunk bending has been also observed
during a long-term (2-3 wk) space flight (Massion et al.
1993, 1997
) and under water, which simulates microgravity environment (Massion et al. 1998
). A
minimization of CM shift was also seen during microgravity episodes of
parabolic flights when subjects performed a leg-raising movement, where a trunk inclination in the opposite direction to the raised leg compensated precisely for the CM shift expected to occur
(Mouchnino et al. 1996
). In this paradigm, it was,
however, noticed that the CM shift toward the supporting leg, which
preceded leg raising in normogravity was not present in microgravity
and was thus gravity dependent. These observations suggest that there
exists an internal model of the body segment mass and inertia, which is
preserved in microgravity and is used to minimize anteroposterior or
lateral CM shifts that the movement may provoke.
The fact that the initial CM position was also maintained during
erect posture in microgravity episodes of the parabolic flight might
indicate that the internal model of the body geometry and mass as well
as of the segments' orientation with respect to the external world is
preserved despite missing information from otoliths and body
graviceptors (Dietz 1994; Mittelstaedt
1998
; Roll et al. 1993
) and biased input from
muscle proprioceptors. However, this internal model is no more adequate
when microgravity is long-lasting. A forward inclined posture was
described by Clement et al. (1984)
during the first days
in flight; a forward body inclination was also observed under water
(Massion et al. 1995
). This initial inclined posture was
compensated after 1 wk in-flight. Thereafter, the anteroposterior
positioning of the CM with respect to the feet and the body segment
orientation with respect to the space seem to be regulated
independently, indicating different control mechanisms. Concerning
first the anteroposterior CM position, a backward CM positioning has
been described by Pozzo et al. (1995)
before the
performance of a whole body lifting task after 2 wk in-flight, and was
interpreted as being task dependent. However, during long-term
microgravity episodes (150 days), the backward shift of the CM initial
position, which can be seen after 3 wk in-flight, is progressively
reduced and is replaced by a ground-based positioning inside the
support area at the end of the flight (Baroni et al.
1999
). Concerning the segment orientation with respect to the space, it is rather preserved in microgravity. The head axis
remains vertical during long-term microgravity (Amblard et al.
2000), even when oscillatory movements are performed as it is
during parabolic flight (Amblard et al. 1995
,
1997
). The trunk axis is inclined forward
(Massion et al. 1997
) or is close to the vertical
(Pedrocchi et al. 2000). In fact, data from the
literature suggest that body orientation is mainly based on a top-down
model starting from the head position with respect to the space
(Mergner et al. 1997
). In contrast, the CM position with
respect to the floor is probably based on a bottom-up organization from
the feet to the head (Assaiante and Amblard 1995
) and
depends on sensors input from the feet. In the present experimental
condition, the cutaneous information from the feet was present, due to
the attachment of the feet to the floor. In absence of otolithic and
accurate proprioceptive information about the gravity vector, this
information, probably together with a short-term memorized sensorimotor
representation, may have been used for an accurate positioning of the
CM during erect posture.
The second question raised in this study concerns the maintained
kinematic synergy and the associated coupling between hip, knee, and
ankle angle changes in microgravity. Two main results emerge from the
principal components analysis of the hip, knee, and ankle angle changes
occurring during the movement. The first one is that under both normo-
and microgravity, the contribution of only one component (PC1) accounts
for >99% of the movement (1 > 99%). This result
indicates that the kinematic synergy is characterized by a strong
coupling between angles. The coupling remained fixed through the course
of the movement even if its variability (V1)
was increased in microgravity. The maintenance of the strong coupling
between angles in absence of equilibrium constraints suggests that the
kinematic synergy is an invariant parameter controlled by the CNS
(Alexandrov et al. 1998
), which is independent from the
gravity constraint according to the present experimentation. The second
result concerns the relative contribution of PC1 to the hip, knee, and
ankle angles, which is changed very little in microgravity. When a
change was present, it was preponderant at the knee level: it consisted
of a decrease in knee extension (from 2.6 to 5.5° varying between
subjects) or in a change from a knee extension in normogravity (mean
value of 3.9°) to a knee flexion in microgravity (mean value of
7.1°). It is interesting to note that on the basis of the
anthropometric model of Winter (1990)
, Alexandrov
et al. (1998)
previously calculated, the relative effect of
hip, knee, and ankle angle changes on the CM shift for a standard
subject weighing 70 kg and measuring 170 cm. These authors demonstrated
that a 1° change in the ankle angle generates a CM shift of 1.43 cm,
which is twice as large as that generated by a 1° change in the knee
angle (CM shift of 0.75 cm) and eight times larger than that generated
by a 1° change in the hip angle (CM shift of 0.17 cm). These results
indicate that the trend to knee flexion observed in microgravity should
shift the final CM position backward. This was actually observed in
subject S3. In subjects S1 and
S5 where the increase in knee flexion was significant, the backward CM shift was prevented by a simultaneously decreased ankle
dorsiflexion (see Figs. 5 and 9). A motor equivalent appears that is
probably able to maintain an efficient CM minimization during the
movement in microgravity.
How the CNS is able to perform the same kinematic performance in
microgravity in spite of the equilibrium constraints disappearing was
the third question raised in this study. In this context, the
hierarchical model of the central organization of postural control
including two stages as proposed by Clement et al.
(1984) and Gurfinkel et al. (1981)
(see
Massion 1997
) is strongly supported by experiments in
microgravity (Clement et al. 1984
; Clement and Lestienne 1988
). The first stage of the model comprises an
internal representation of the body. This includes a representation of body kinematics based on proprioceptive input from muscles from the
eyes to the feet (Gurfinkel et al. 1988
; Roll
and Roll 1988
), a representation of contact forces
(Cordo and Nashner 1982
; Marsden et al.
1981
), of the body mass and inertia (Dietz et al.
1989
, 1992
), as well as the orientation of the
body with respect to the external world (Hlavacka et al.
1995
; Mergner et al. 1993
). According to
Gurfinkel et al. (1993a
,b
), this body schema remains rather stable in microgravity, although there are important changes in
the sensory input. Perception of complex tactile stimuli or orientation
of drawn ellipses, for example, are unchanged under microgravity,
indicating that an egocentric reference frame is still used in the
absence of gravity to perform perceptual or spatial orientation tasks
efficiently. The second stage of the model concerns the implementation
of postural control by muscle forces assisted by local feedback. The
invariant kinematic synergy that minimizes the CM shift during trunk
bending both in normo- and microgravity as observed in the present
study seems to depend on the level of the internal body representation.
This allows us to predict the consequence of the trunk movement on
equilibrium and to select the appropriate coupling between joints to
minimize the CM shift. The kinematic synergy reflects an organization
in term of postural space. According Feldman and Levin
(1995)
, a referent body configuration in terms of joints
position in space can be defined by setting the threshold of the
stretch reflex of the various muscles at an appropriate level. The
actual body posture differs from the referent posture due to the
influence of the external forces such as gravity. Examples of movements organized in terms of postural space were given by Desmurget et al. (1996)
for reaching movements and by Feldman and
Levin (1995)
for pointing movements. The implementation of the
kinematic synergy by the muscle forces has to adapt to the changes in
constraints due to the microgravity. It might be performed in line with
the equilibrium point theory (Bizzi et al. 1982
,
1992
; Feldman 1980
; Feldman and
Levin 1995
) indicating that a new referent joint position is
planned. Alternatively, it could be implemented by an inverse dynamic
model build up through learning (Gomi and Kawato 1996
). In both alternatives, the muscle forces in microgravity should be
modified as a function of the new constraints. It has been previously
observed during a long-term space flight that an early soleus
activation observed during backward trunk bending is replaced by an
early tibialis anterior activation (Massion et al. 1992
, 1993
). In the present study, during a parabolic flight,
the EMG activity showed an important reorganization to preserve the
invariant synergy at the kinematic level. These results are in
agreement with the observation of Lackner and Dizio
(1992
, 1996
) on single movement performance in
microgravity and with Macpherson's hypothesis (Macpherson
1988
) proposing that the muscle synergy in the postural domain
is flexible and determined by biomechanical constraints.
In conclusion, the results of the present study show that the anteroposterior CM shift remains minimized in short-term microgravity, both during erect posture and during trunk bending. This minimization occurs through a kinematic synergy, which is an invariant parameter controlled by the CNS, which fixes the ratio between the hip, knee, and ankle angle changes during the movement. This control depends on both an internal representation of the body segment geometry and mass, which remains stable in microgravity thanks to an adaptable muscle synergy.
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ACKNOWLEDGMENTS |
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The authors thank B. Amblard for reading and commenting on the manuscript and M. Zedka for revising the English language.
This research was supported by the Center National d'Etudes Spatiales.
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FOOTNOTES |
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Address for reprint requests: S. Vernazza, Laboratory of Neurobiology and Movements, Centre National de la Recherche Scientifique, 31 chemin Joseph Aiguier, 13402 Marseille Cedex 20, France.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 20 May 1999; accepted in final form 3 September 1999.
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