RESEARCH ARTICLE

Reaching while standing in microgravity: a new postural solutionto oversimplify movement control

Claudia Casellato • Michele Tagliabue •

Alessandra Pedrocchi • Charalambos Papaxanthis •

Giancarlo Ferrigno • Thierry Pozzo

Received: 16 November 2010 / Accepted: 21 October 2011 / Published online: 8 December 2011

� Springer-Verlag 2011

Abstract Many studies showed that both arm movements

and postural control are characterized by strong invariants.

Besides, when a movement requires simultaneous control

of the hand trajectory and balance maintenance, these two

movement components are highly coordinated. It is well

known that the focal and postural invariants are individu-

ally tightly linked to gravity, much less is known about the

role of gravity in their coordination. It is not clear whether

the effect of gravity on different movement components is

such as to keep a strong movement–posture coordination

even in different gravitational conditions or whether

gravitational information is necessary for maintaining

motor synergism. We thus set out to analyze the move-

ments of eleven standing subjects reaching for a target in

front of them beyond arm’s length in normal conditions

and in microgravity. The results showed that subjects

quickly adapted to microgravity and were able to suc-

cessfully accomplish the task. In contrast to the hand tra-

jectory, the postural strategy was strongly affected by

microgravity, so to become incompatible with normo-

gravity balance constraints. The distinct effects of gravity

on the focal and postural components determined a sig-

nificant decrease in their reciprocal coordination. This

finding suggests that movement–posture coupling is

affected by gravity, and thus, it does not represent a unique

hardwired and invariant mode of control. Additional

kinematic and dynamic analyses suggest that the new

motor strategy corresponds to a global oversimplification

of movement control, fulfilling the mechanical and sensory

constraints of the microgravity environment.

Keywords Microgravity � Whole-body reaching �Postural control � Focal control � Coordination �Movement oversimplification

Introduction

Despite the very large number of degrees of freedom

(DOFs) of the human motor system, our movements are

characterized by strong invariant features, which have been

deeply investigated in literature. Most of these studies

analyzed horizontal arm movements and proposed funda-

mental gravity-independent theories (Flash and Hogan

1985; Uno et al. 1989; Harris and Wolpert 1998; Nakano

et al. 1999), but whenever these studies were extended to

motor tasks in the sagittal plane, it has been shown that the

gravitational field plays a fundamental role in motor con-

trol. For instance, the asymmetry of the hand velocity

profiles observed during vertical reaching tasks is

Claudia Casellato and Michele Tagliabue contributed equally to this

work.

C. Casellato (&) � A. Pedrocchi � G. Ferrigno

Bioengineering Department, NearLab, Politecnico di Milano,

P.za Leonardo Da Vinci 32, 20133 Milan, Italy

e-mail: claudia.casellato@mail.polimi.it

M. Tagliabue

CESeM (UMR CNRS 8194), Universite Paris Descartes,

45 rue des Saints Peres, 75270 Paris Cedex 06, France

C. Papaxanthis � T. Pozzo

U-887 Motricite-Plasticite, Institut National de la Sante et de la

Recherche Medicale, BP 27877, 21078 Dijon, France

C. Papaxanthis � T. Pozzo

Universite de Bourgogne, BP 27877, 21078 Dijon, France

T. Pozzo

Italian Institute of Technology, Via Morego 30,

16163 Genoa, Italy

123

Exp Brain Res (2012) 216:203–215

DOI 10.1007/s00221-011-2918-2

systematically affected by the upward or downward

direction of movements (Papaxanthis et al. 2003; Gentili

et al. 2007). The gravity role is evident also during postural

tasks. The central nervous system (CNS) appears, indeed,

to guarantee the maintenance of balance through a direct

control of the projection of the center of mass (CoM) on the

horizontal plane (Massion et al. 1992; Vernazza et al. 1996;

Patla et al. 2002; Massion et al. 2004).

The importance of gravity in the control of arm move-

ments and posture has also been clearly pointed out by

studies performed in microgravity (lG). During the first

pointing movements in parabolic flights (Papaxanthis et al.

2005) and during catching tasks in the first days of a space

mission (McIntyre et al. 2001), the arm appeared to be

controlled as if the gravity was still acting on the body, or so

as to avoid undesirable effects of an unreliable internal

model of gravity (Crevecoeur et al. 2010), resulting in

altered movement kinematics and muscular activations

timing. Only after a longer period of time in lG, CNS

developed a lG-specific strategy. For postural tasks in

weightlessness, the role of gravity is still unclear. Many

studies on trunk bending or leg raising showed that the

neural mechanisms stabilizing the CoM in normal gravity

(NG) persisted in lG, although they were no longer neces-

sary (Clement et al. 1984; Mouchnino et al. 1996; Massion

et al. 1997; Vernazza-Martin et al. 2000; Baroni et al. 2001).

On the other hand, experiments on leg raising during long

lG exposure showed a distinct CoM shift toward the moving

leg with poor evidence of stabilization (Pedrocchi et al.

2002, 2005). A theory able to reconcile these findings has

been proposed: both the persistence of the NG postural

strategy for the trunk bending and its modification for leg-

raising movements would fulfill a new lG-specific stability

constraint requiring the minimization of the dynamic inter-

actions with the environment (Pedrocchi et al. 2003, 2005).

Interestingly, NG studies on complex motor tasks,

which require a simultaneous control of their focal

(reaching/movement) and postural (equilibrium) compo-

nents, showed not only invariant features of the focal and

postural subtasks separately, such as a systematic curvature

of the hand path and a small forward CoM displacement

(Pozzo et al. 2002), but also revealed a tight and robust

relationship between them, suggesting a sharing of neural

commands (Patron et al. 2005). Moreover, a strong cou-

pling between joint angles has been suggested to be a

crucial mode of control dealing with the historical issue

concerning the reduction in motor system redundancy

(Bernstein 1967) and allowing the simultaneous control of

all task-relevant variables. However, whether the coordi-

nation between the focal and postural components of the

movement and the related joint synergism are hardwired

and invariant or dependent on the terrestrial gravity is still

a matter of research.

On the one hand, recent studies on motor coordination

showed a decoupling between the postural synergies and

the focal movement, demonstrating that the CNS is able to

combine or separate the movement into autonomous

functional synergies according to the task requirements

(Robert et al. 2007; Berret et al. 2009). Furthermore, our

highly synergic movements appear to be the result of

a learning process along the individual development

(Ivanenko et al. 2004), during which we optimally adapt to

the earth’s gravitational environment (Edgerton and Roy

2000), rather than an innate and invariant characteristic.

Therefore, the persistence of movement synergism should

not be taken for granted in case of strong environmental

change, as microgravity. Indeed, theories, as minimum

intervention principle, would predict that in weightless-

ness, our CNS would selectively suppress the terrestrial

equilibrium-related synergies, because in microgravity, the

position of the CoM becomes an irrelevant variable

(Todorov and Jordan 2002; Scott 2004).

On the other hand, the few studies which investigated

the joint coupling and the coordination between postural

and focal components of the movement in lG observed a

persistence of high kinematic synergies, suggesting that

they are gravity-independent features of our motor behav-

ior (Vernazza-Martin et al. 2000; Baroni et al. 2001; Patron

et al. 2005).

In order to try to reconcile these apparently contrasting

findings, we studied reaching movements beyond arm’s

length while standing, performed in normal conditions and

in transient microgravity, and we investigated the effects of

gravity on movement–posture coordination, joint syner-

gies, and dynamics. The experimental protocol was spe-

cifically designed to effectively investigate a potential

effect of gravity on the coupling between focal and postural

components of movement. In particular, in contrast to most

of previous lG studies on movement–posture coordination,

we tried to guarantee the possibility of a direct comparison

between the focal component of the movement in lG and

in NG by having selected an external, and thus univocally

defined, goal of the movement (external visual target).

Indeed, in tasks as the classical trunk bending (Massion

et al. 1997; Vernazza-Martin et al. 2000; Baroni et al.

2001), this direct comparison was not always possible

because the goal achievement might be perceived in lG, in

contrast to NG, mainly as joint displacement rather than as

absolute trunk orientation. Moreover, in order to stress the

movement–posture coordination mechanisms, we ensured

that the reaching movement accomplishment would sig-

nificantly perturb the equilibrium in NG by placing the

target at a significant distance in front of the subject, and

not close to the subject feet, as in the few previous

microgravity studies on reaching beyond arm’s length

protocols, where the task could be easily achieved with

204 Exp Brain Res (2012) 216:203–215

123

small horizontal displacement of the CoM (Kingma et al.

1999; Patron et al. 2005).

If in microgravity the coupling between the focal and

postural components of this reaching-from-standing task

persists, the idea of an innate, and invariant, neural

mechanism of coordination between movement and pos-

ture would prevail. Otherwise, the notion of learned, and

flexible, coordination between parallel controls should be

privileged.

Materials and methods

Experimental protocol and procedures

Participants

Twelve volunteer healthy male adults (mean height

176 ± 4 cm; mean weight 71.7 ± 8 kg) gave informed

consent to participate in this study. Each subject passed a

complete medical examination before the experiments.

None had a previous history of neuromuscular diseases,

and none had ever experienced lG conditions before. All

subjects received ScopDex, a drug to relieve the effects of

motion sickness. Experiments were conducted in accor-

dance with ethical guidelines laid down by the Universite

de Bourgogne and the Centre National d’Etudes Spatiales

(CNES).

Protocol

Data were collected from two 3-day parabolic flight cam-

paigns (Airbus A-300, CNES, and Novespace). During

each flight day, 30 parabolas were performed. The parab-

olas were staggered by \2 min of NG steady level and

each provided 20 s of zero gravity (mean: 0.0007 G;

r = 0.0018 G), preceded, and followed by two 20-s peri-

ods of increased gravity (Fisk et al. 1993). The subject was

asked to stand with his arms by his sides for 2 s and then to

reach at a natural speed, with both index fingers simulta-

neously, to two targets symmetrically placed on a hori-

zontal bar. This symmetric task requirement reduced the

intervention of rotational components of the movement and

allowed movement analysis in the sagittal plane. No

instructions were given concerning the body segment

involvement. The bar was placed in front of the subject, at

a distance and height equal to 60% of subject’s height,

measured from the external malleolus (Fig. 1a). The sub-

ject had to brush the targets with the tips of the index

fingers without applying any force. The feet were anchored

to the floor, preventing heel raising, both in NG and in lG.

This protocol was performed by subjects in normo-

gravity (inside the plane on ground) and in microgravity

during the parabolas. For each subject, the movements

during the first 7 consecutive parabolas were analyzed.

During the rest of the flight, the participants were involved

in other experiments. One of the twelve subjects was

excluded because of motion sickness.

Data collection and preprocessing

Movement kinematics were recorded using a 3D motion

capture device (SMART-BTSTM, Italy), with a sampling

rate of 120 Hz. Five cameras were used to measure the 3D

position of 14 retroreflective markers (15 mm in diameter),

which were placed at different anatomical locations on the

right side of the body (external cantus of the eye, midline

of eyebrows, chin, C7 vertebra, acromion, humeral lateral

epicondyle, ulnar styloid process, apex of the index finger,

anterior superior iliac spine, posterior superior iliac spine

(PSIS), iliac crest, greater trochanter, knee interstitial joint

space, and external malleolus). Two additional markers

were placed on the target bar. Force platform data were

recorded (KistlerTM, sampling rate 960 Hz) and synchro-

nized with the motion system, to estimate the body center

of pressure (CoP) and the ground reaction forces in NG.

All data analyses were performed with custom-written

software using Matlab7� (Mathworks Inc., Massachusetts).

In order to verify whether the motion could be analyzed

only in the sagittal plane (xy), the movement planarity was

tested by performing a principal component analysis on the

3D trajectories of all markers. On average across subjects,

the angle between the medio–lateral axis and the direction

of minimal variability of the data, i.e., 3rd eigenvector, was

only 6.5� and the variability along this direction was equal

to 2.1% of the total variability. The movement was thus

considered to be planar.

For each subject, the NG behavior was defined from a

number of trials equal to the number of the performed lG

trials averaged across subjects (22 trials). The lG behavior

was quantified for each of the 7 parabolas. The very first

movement for each parabola was individually investigated

and excluded if it did not fit the expected task require-

ments; indeed, the initial upright stance stabilization was

often perturbed by the sudden transition between hyper-

and microgravity.

Data analysis

Movement timing

Movement onset (to) and end (te) were defined using a

velocity threshold algorithm: to was the instant when at

least one marker moved (i.e., the last motion captures

frame when the velocities of all markers was less than 5%

of their peaks), te the instant when all the markers were still

Exp Brain Res (2012) 216:203–215 205

123

in space again (Tagliabue et al. 2009); the movement

duration was defined as T = te - to.

Hand trajectory parameters

Index finger (IF) Right hand reaching performance was

quantified by the accuracy, computed as the distance

between the target and the final finger position, and by the

variability, computed as the interquartile range of IF final

position (Adamovich et al. 2001). Kinematic focal

parameters already described in arm-pointing studies (Pa-

paxanthis et al. 2005) were calculated: mean and peak

velocities, finger path curvature (path/L: ratio between the

finger path length and the distance (L) between its initial

and final position), Time to velocity peak (TVP: relative

instant when peak velocity occurs) and hand movement

duration. To estimate this last parameter, the threshold

algorithm described above for the whole movement was

applied to the IF marker only. It follows than if the IF

marker is not the first one to overcome the velocity

threshold and the last one to return to velocity below the

threshold, the durations of the whole body, and of the hand

movements do not correspond.

Body mass control

Center of mass (CoM) The position of the whole-body

CoM in the sagittal plane was calculated using a biome-

chanical model consisting of the following eight rigid

segments: hand, forearm, upper arm, trunk head, pelvis,

thigh, shank, and foot. The pelvis was included as indi-

vidual segment because it optimizes the calculation of the

CoM by reducing the error associated with variable trunk

segment length (de Looze et al. 1992). Documented

anthropometric parameters were used (Zatsiorsky and

Seluyanov 1983; Winter 1990) and, by computing the

ankle torque and the reaction forces at the foot by inverse

dynamics on the biomechanical model, the CoP trajectory

was estimated. In order to tailor the model, a validation

procedure was performed (Tagliabue et al. 2008, 2009).

This procedure optimizes, for each subject, the parameters

of the biomechanical model to minimize the difference

between the CoP trajectory calculated through the model

and the CoP recorded by the force platform in NG (root

mean square error across subjects was 6.9%).

In order to describe the postural strategy, the antero–

posterior CoM positions at beginning and end of movement

(CoMx(to) and CoMx(te), respectively) were estimated. The

Lower Body CoMx (LCoMx), including lower limbs and

pelvis, and the Upper Body CoMx (UCoMx), including

trunk, head, and upper limbs, were also evaluated as the

main parameters representative of postural adjustments and

focal movement, respectively. To decouple the upper- and

lower-body contributions, the positions of the whole-body

CoM and LCoM were calculated as distances from the

heels, whereas the UCoM position was referenced to the

lumbar spine, midway between the PSISs. For each par-

ticipant, the CoMx was expressed as percentage of the

length of his base of support (BoS), to allow a direct

comparison between subjects and to provide explicit

information about balancing. LCoMx and UCoMx were also

expressed as BoS%, for consistency of units with the CoMx.

Movement–posture coordination

Hand–CoM coupling To assess the time coupling

between focal and balance components of the movement,

the cross-correlation function (CCF) between the curvi-

linear velocity profiles of the IF (velIF) and of the CoM

(velCoM) was calculated (Patron et al. 2005). Furthermore,

in order to focus on balance control, the cross-correlation

in the antero–posterior direction (CCFx), between velIFx

and velCoMx, was computed. The maximum of CCF,

max(CCF), and the corresponding time lag (Lagmax(CCF))

were analyzed.

Joint kinematics

The angular trajectories, hi(t), of six joint angles (ankle,

knee, hip, shoulder, elbow, and wrist) were identified. Each

Fig. 1 Experimental setup (a).

Stick diagrams in the sagittal

plane (xy) referred to

representative subject’s trials in

normal gravity, NG (b), and in

microgravity, lG (c). In b and cpanels, the CoM trajectory, its

projection on the base of

support (CoMx) and the finger

path are depicted. The distance

between target and subject’s

malleolus is represented

206 Exp Brain Res (2012) 216:203–215

123

joint (i) was therefore associated with its joint displace-

ment, Dhi, that is, its maximal excursion during movement

(Dhi = maxhi(t) - minhi(t)). The averaged joint displace-

ment, Dh, over the six joints was computed to give a global

index of joint motions Dh ¼ 16

P6i¼1 Dhi

� �. To compensate

for the inter-subject variability at the joint level, which

is due to the numerous possible body configurations

allowing the target reaching, we calculated the lG effect

individually for each subject, on each joint separately

DhðlG�NGÞ;i ¼ DhlG;i � DhNG;i and on average across joints

DhðlG�NGÞ;i ¼ DhlG;i � DhNG;i.

Principal component analysis (PCA) was carried out on

the six joint angles trajectories; each joint angular trajectory

was translated to set the initial position at zero and normal-

ized relative to its active physiological range of motion. This

method, extracting the commonality between the angular

displacements, determines the global joint covariation. The

% ratio between the first eigenvalue and the sum of all

eigenvalues can be viewed as an index of whole-body

coordination (PC1%); for instance, a PC1% value equal to

100% means that all angles are linearly correlated together

(Alexandrov et al. 1998a, b; Baroni et al. 2001).

Movement dynamics

To calculate joint torques, inverse dynamic method was

applied to the biomechanical model of the body. Beginning

from the hand segment, at the extremity of which no

contact force was applied, and descending through the open

kinematic chain down to the ankle, Newton’s equations

were used to estimate the joint force and torque reactions

necessary to produce the observed segments’ kinematics.

The time course of the ankle torque sankleð Þ, and its abso-

lute mean sanklej jð Þ, was computed to quantify the dynamic

interactions with the environment (Pedrocchi et al. 2003).

jsanklej ¼1

T

Zte

to

sanklej jdt

Simulation of lG on NG kinematics Simulation was

carried out on the normo-gravity kinematics by assuming

gravity effect on the body segments as null in the inverse

dynamic calculations, thus obtaining only the inertial

component of the joint torque sin;ankle

��

��

� �. The mean

absolute inertial torque at the ankle in NG sin;ankle

��

��

� �and

the actual mean absolute ankle torque in lG were then

compared. The purpose of this simulation was to verify

whether the dynamics of the microgravity behavior simply

corresponded to terrestrial dynamics without the contribu-

tion of gravity, or whether the lG kinematics required a

different dynamic strategy.

Simulation of NG timing on lG data Possible differences

in inertial ankle torque can be due to two different factors:

contributions of each segment and movement velocity. To

distinguish between the effects of these two factors, an

artificial constraint was placed on the markers trajectories

in NG and lG, so that all have the same duration (median

of the NG duration). The ankle torque (time-simulated

ankle torque: sanklej jts) was then recomputed by applying

the inverse dynamic method on these new simulated

movements. The obtained duration-independent ankle tor-

ques were compared between the two gravity conditions.

Dynamic compensation strategy In order to analyze the

contribution of different segments motion to the total ankle

torque, the total angular momentum at the ankle (CtotAnkle)

was computed as sum of the contributions of all segments

(CjAnkle). Indeed, since the second Newton’s law states that

the ankle torque can be computed as the derivative of

CtotAnkle, we were able, by computing an index of com-

pensation, IC (Pedrocchi et al. 2003), to quantitatively

assess whether a compensation between the contributions

of the different segments to the ankle torque was present:

IC ¼1T

R tet0

C2totAnkle

� �dt

P7j¼1

1T

R teto

CjAnkle

� �2dt

� �

IC equal to zero means that a complete segment dynamic

compensation is present; IC values between 0 and 1

correspond to a partial compensation; values of IC greater

than 1 account for a concurrent summation of segment

contributions to the ankle momentum: the bigger IC, the

smaller the dynamic compensation.

Statistical analysis

All statistical analyses were carried out using the software

Statistica� (StatSoft Inc., Oklahoma). Lilliefors test was

applied to evaluate normality of the distribution. Since

most parameters did not show a normal distribution, non-

parametric analyses were performed. Each parameter is

reported as median and interquartile range, IQR (the dif-

ference between the 75th and 25th percentiles). To test the

adaptation along the parabolas, and in particular to assess

after which parabola the subjects’ motor behavior could be

considered stabilized, first, a Friedman test for repeated

measures was employed, on the most representative

parameters. Then, differences between all consecutive

parabolas (P1 vs. P2, …, P6 vs. P7) were evaluated through

nonparametric Wilcoxon matched pairs tests. Once the

stable ‘‘time window’’ for the lG motor control was

defined, Wilcoxon tests were used, with the gravity con-

dition as independent factor and the parameter of interest as

dependent factor, in order to verify the lG effect on the

Exp Brain Res (2012) 216:203–215 207

123

movement variables. In order to quantify the effect of lG

on the intra-subject repeatability of the motor strategy, for

each subject, we computed the individual IQR of the most

representative parameters.

To correlate the different aspects of motor control,

Spearman’s nonparametric linear regression was performed

between the task-relevant variables and the kinematic and

dynamic strategy indexes. In all statistical analyses, two

significant thresholds were set: P \ 0.05 and P \ 0.01.

Results

To evaluate the differences between the subject’s motor

behavior in NG and lG conditions, an example of which is

reported in Fig. 1b, c, first, we compared the whole

movement duration; second, the focal and postural com-

ponents of the movement, represented by the hand tra-

jectory and by the body mass and joints displacement

control, were investigated. Afterward, we estimated the

effect of lG on the coordination between these two task

components by evaluating the coupling between the hand

and CoM motion and the synergism among joints. Finally,

we analyzed the movement dynamics to better understand

why subjects changed their motor strategy in microgravity.

Performance stabilization

Figure 2 reports the NG value and the trend during

parabolas (from P1 to P7) of movement duration, T, hand

trajectory straightness, path/L, and final CoM position,

which represent the global movement execution and its

focal and postural components, respectively. A global

effect of the progressive number of parabolas could be

observed on path/L (v2 = 12.77, P \ 0.05) and on

CoMx(te) (v2 = 11.9, P \ 0.05), but not on T. While the

Wilcoxon tests between consecutive parabolas show sig-

nificant differences between P2 and P3 for all three

parameters (T: Z = 2.31, P \ 0.05; path/L: Z = 1.98,

P \ 0.05; CoMx(te): Z = 2.22, P \ 0.05), later in flight, a

significant difference could be observed only for CoMx(te)

(P6 vs. P7, Z = 2.09, P \ 0.05). Because this late change

in postural strategy seems to be not ascribable to the global

stabilization process, but to the design of the parabolic

flights, which have a long pause after five parabolas, and

because at the worst the temporary effect of this pause

could induce a conservative underestimation of the global

lG effect, the subjects’ behavior was considered suffi-

ciently stable after two parabolas. This choice was also

supported by a similar intra-subject variability (IQR) in NG

and after two parabolas for all three parameters: T (NG:

0.38 (0.23); lG: 0.30 (0.25) s); path/L (NG: 0.09 (0.10);

lG: 0.09 (0.09)); CoMx(te) (NG: 9.3 (20.6); lG: 7.9 (5.8)

BoS%). Therefore, for the following analyses, P3/P7 data

were averaged to represent the lG condition and to be

compared with NG.

Movement timing

The lG strategy was characterized by a significant and

persistent longer duration of the body movement, T (NG:

1.34 (0.8); lG: 1.9 (0.7) s; Z = 2.67, P \ 0.01), Fig. 2a.

Hand trajectory parameters

The effect of microgravity on the focal component of the

movement appears to be negligible. As shown in Fig. 2b,

there was not significant modification of finger path cur-

vature, path/L (NG: 1.11 (0.10); lG: 1.10 (0.10)). Simi-

larly, no significant differences were found in the reaching

error (NG: 0.93 (0.54); lG: 1.0 (0.50) cm) and in its var-

iability (NG: 4.1 (4.9); lG: 4.9 (10) cm). Also, the veloc-

ity-dependent characteristics of the hand trajectory, as the

mean velocity (NG: 0.73 (0.20); lG: 0.62 (0.10) m/s), the

peak velocity (NG: 2.33 (0.69); lG: 1.88 (0.72) m/s), and

the hand movement duration (NG: 0.83 (0.33); lG: 0.9

(0.2) s), were not affected by lG. Finally, the asymmetry of

the velocity profile, TVP, was not significantly different

between NG and lG either (NG: 41.7 (11); lG: 42.8 (8)

%).

Body mass control

Postural strategy appears to be deeply affected by lack of

equilibrium constraint due to lG. Figure 2c shows a sig-

nificant increase in the final antero–posterior distance of

the CoM from the heels, CoMx(te) (NG: 89 (24); lG: 114

(49) BoS%; Z = 2.75, P \ 0.01). Note that in lG, subjects

moved their CoM even beyond the extremity of the toe

corresponding to 100 BoS% (the ankle was, on average,

around 25 BoS%). This seems to be due to the disappear-

ance of the postural adjustments, which in NG consist in

moving backward the lower body to compensate for the

forward displacement of the upper body, but which are no

more necessary to succeed the task in microgravity. The

final position of the lower CoM, LCoMx(te), was indeed

significantly farther in lG (NG: 52 (35); lG: 64 (53)

BoS%; Z = 2.22, P \ 0.05). In contrast, microgravity did

not affect the upper body contribution to the mass dis-

placement, UCoMx(te), (NG: 112.7 (48); 112.4 (19)

BoS%). The individual subjects’ CoMx(te), LCoMx(te), and

UCoMx(te) are reported in Fig. 2d, e, and f, respectively.

To understand whether the change in the final CoM posi-

tion rose from an initial upright posture shift or from a

different postural control, the initial CoM position,

CoMx(to), was also analyzed: CoMx(to)was more variable,

208 Exp Brain Res (2012) 216:203–215

123

but not significantly affected by gravity (NG: 50 (16); lG:

67 (37) BoS%).

Movement–posture coordination

In NG, the hand–CoM correlation between both the curvi-

linear velocities and the antero–posterior velocities (Fig. 3a,

b) confirmed the strong coupling observed in previous

studies (e.g., Patron et al. 2005): the maximum of CCF was

close to one and the relative time lag was close to zero. In

turn, in lG, although a relatively high coupling between

curvilinear velocities persisted, a strong decoupling of the

antero–posterior velocity components (Fig. 3c, d) was found

(all values in Fig. 3e). The decoupling between the hand and

CoM movements appears to be due to both different shapes

(decrease in max(CCFx)) and a time delay (increase in

Lagmax(CCFx)) between the IF and CoM velocity profiles.

Moreover, the ratio between the duration of the finger and

whole movements significantly decreases in lG (NG: 0.57

(0.1); 0.52 (0.09); Z = 2.4, P \ 0.05).

Joint kinematics

To better understand the postural strategy modification, we

compared the joints contribution in the two gravitational

conditions. An example is shown in Fig. 4a. The lack of

typical ‘‘terrestrial’’ postural adjustments in lG appears to

be related to a global reduction in joint motions compared

to NG strategy. The averaged displacement of the six joints

was indeed significantly smaller in lG than in NG

(DhðlG�NGÞ= -6.4 (11.2)�, Z = 2.85, P \ 0.01), Fig. 4b.

To verify that this result was not due mainly to distal joints,

such as the wrist and elbow, the average joint displacement

was re-computed with only the proximal joints (ankle,

knee, hip, and shoulder), confirming the reduction in lG

(-9 (16)�, Z = 2.66, P \ 0.01). In particular, as shown in

Fig. 4b, the hip and shoulder contributions were reduced

in lG for all subjects but one (DhðlG�NGÞ;hip: -10 (18)�,

Z = 2.66, P \ 0.01; DhðlG�NGÞ;shoulder: -10 (13)�, Z =

2.58, P \ 0.01) and a similar tendency characterized the

contribution of the knee (DhðlG�NGÞ;knee: -2 (29)�) for

Fig. 2 Movement duration

T (a), curvature of the finger

trajectory Path/L (b) and

distance from the heel, along x-

axis, of the center of mass at the

end of the movement, CoMx(te),as % of base of support (c) in

normal gravity, NG, and in each

of the seven parabolas (P1/P7).

The dots correspond to the

median across subjects, and the

error bars represent the 25th

and 75th percentiles. Values in

light gray (P1/P2) have been

excluded from further analyses.

** significant difference

(P \ 0.01) between NG and lG

(P3/P7), based on Wilcoxon

test. Individual final positions of

whole body (d), lower body (e),

and upper body (f) center of

mass along x-axis, reported as %

of base of support. Dark circlescorrespond to NG condition

(median value across trials for

each subject), while graytriangles correspond to lG

condition (median value across

trials for each subject in P3/P7).

* and ** significant difference

(P \ 0.05 and P \ 0.01,

respectively) between NG and

lG, based on Wilcoxon test

Exp Brain Res (2012) 216:203–215 209

123

those subjects that used it in NG. The contributions of the

other joints were substantially unaffected. The relationship

between the modification of the postural and the joint

strategy was also supported by a significant correlation

between them (Dh vs. CoMx(te): R = -0.5, P \ 0.05). The

more Dh decreased, the more the CoM moved forward,

indicating the reduction in compensatory joints displace-

ments in opposite direction in the new postural strategy.

The very high movement synergism, characterizing the

subject behavior in NG significantly decreased in lG.

Indeed, as shown in Fig. 4c, the variance explained by the

first principal component, PC1%, which represents the joint

coupling, was significantly smaller in lG (NG: 99 (0.7);

lG: 96 (5) %; Z = 2.93, P \ 0.01). Moreover, the tight

correlation between PC1% and CoMx(te) suggests that the

increase in the forward CoM displacement was function-

ally associated with the reduction in joint synergism (PC1

vs. CoMx(te): R = -0.83, P \ 0.01).

Movement dynamics

As expected, the mean absolute ankle torque, jsanklej, which

represents the dynamic interaction with the environment,

was much higher in NG than in lG (NG: 73 (29); lG: 12.4

(5.7) Nm; Z = 2.93; P \ 0.01) because of the mechanical

action of gravity.

Simulation of lG on NG kinematics

When the contribution of gravity was artificially removed

from the ankle torque in NG, the remaining inertial

component was obviously significantly lower than the total

torque (jsanklej in NG: 73 (29); jsin;anklej in NG: 12.7 (6)

Nm; Z = 2.8, P \ 0.01), but it was significantly larger than

the ankle torque in lG (NG: 12.7 (6); lG: 12.4 (5.6) Nm;

Z = 2.56, P \ 0.01), with a median intra-subject differ-

ence equal to 2.1 (2.4) Nm (Fig. 5). A comparison of the

NG jsin;anklej and the lG jsanklej for a representative subject

is reported in Fig. 5a. This result suggests that the decrease

in the ankle torque in lG is not only due to a mere

mechanical effect of the lack of gravity force, but also to a

change in the motor strategy.

Simulation of NG timing on lG data

When simulating the lG movement as executed at NG

speed, the difference between the NG jsin;anklejts and the lG

jsanklejts disappeared (NG: 14.8 (14); lG: 15.1 (30) Nm),

showing that the movement slowdown, and not the new

postural strategy, contributed to reduce the ankle interac-

tion torque.

Dynamic compensation strategy

Both NG and lG movements were characterized by a poor

compensation of the joint torques through the body kine-

matic chain (IC always [ 1), since the protocol target

placement imposes an ample forward leaning. However, in

lG, the IC values were even higher than in NG, showing a

smaller dynamic compensation between segments (NG: 1.5

(1.2); lG: 2 (0.9); Z = 1.9, P \ 0.05) due to the concurrent

rotation of all segments toward the target.

Fig. 3 Index finger (solid line) and center of mass (dashed line)

antero–posterior velocities, in NG (a) and lG (c) in exemplificative

subject’s trials. Cross-correlation functions, CCFx, between these

exemplificative velIFx and velCoMx profiles, in NG (b) and lG (d).

Table (e): median and interquartile ranges, across all subjects, for the

maximum of cross-correlation function, CCF, and of CCFx, and of the

time lag at the peak of CCF and of CCFx, in NG and lG. The lastcolumn reports the P values of the Wilcoxon test between NG and lG,

for each considered parameter

210 Exp Brain Res (2012) 216:203–215

123

Discussion

The movements of standing subjects reaching for a target

placed in front of them beyond arm’s length in normal

conditions and in microgravity were analyzed, in order to

understand how gravity affects the focal and postural

components of a complex movement, as well as their

coordination.

Invariance of the focal component

The results show similar accuracy and precision of the

reaching in NG and in lG. In contrast to previous studies

on lG arm movements (Mechtcheriakov et al. 2002,

Crevecoeur et al. 2010), here the duration of the hand

movement appears to be not affected by gravity. This

difference could be related to the fact that in these studies,

the hand accuracy and stability represent significantly more

stringent requirements than in the task analyzed here.

Significant changes of the hand path and velocity profile

symmetry could not be detected either. This is a very

surprising finding because the asymmetry of the hand

velocity profile observed in NG, consistent with previous

studies on vertical arm movement (Papaxanthis et al.

2003), suggests a role of gravity in the control strategy, and

hence an effect of weightlessness would have been

expected, as found in a previous study of arm movements

during parabolic flights (Papaxanthis et al. 2005). Such a

discrepancy could be partially attributed to the fact that in

the present protocol, in contrast to the Papaxanthis study,

the hand movement was mainly horizontal and it was

previously shown that the symmetry of horizontal pointing

movement is not affected by lG (Mechtcheriakov et al.

2002).

The negligible effect of lG on the focal component,

despite the large postural changes, is consistent with the

spatial and temporal invariance of the hand motion

observed during ‘‘step and reach’’ task perturbed by

asymmetric modifications of the body mass distribution

(Robert et al. 2007), and it could be the result of a sensory-

motor integration process including dynamic vestibular

signals, which even in lG can provide information about

the head displacements generated by the trunk and leg

movements. In particular, the possibility to detect changes

Fig. 4 a Mean joint displacements (ankle, knee, hip, shoulder, elbow,

and wrist) in normal gravity (NG) and microgravity (lG) for one

representative subject. Each joint profile is normalized on the

corresponding maximal physiological active range of motion. Darkgray and light gray areas represent the variability for the NG and lG

conditions, respectively. Profiles are normalized in time before

averaging across trials. b Effect of gravity on the joint displacement,

DhðlG�NGÞ, on average across the 6 joints (A) and for each joint

separately (a ankle, k knee, h hip, s shoulder, e elbow, and w wrist).

Each dot represents one subject. ** significant difference (P \ 0.01)

between NG and lG, based on Wilcoxon test. c Cumulative roles of

PCs (%) in the representation of joint displacements, in NG and lG.

The % variances explained by each of the six principal components of

the joint angles time profiles are reported: dots and error barsrepresent median values and corresponding interquartile ranges

Fig. 5 a Time course of the inertial ankle torque in normal gravity

(NG) and ankle torque in microgravity (lG), for a representative

subject. Mean profiles and standard deviation across NG trials (darkgray) and lG trials (light gray) are displayed. b median value and

interquartile range across subjects of the mean absolute ankle torque

in NG jsanklejð Þ, and individual values of the mean absolute inertial

ankle torque in NG jsin;anklej� �

, and of the mean absolute ankle torque

in lG jsanklejð Þ. Each filled symbol corresponds to the median value

across trials for each subject in NG (circle) and in lG (triangle).

** significant difference (P \ 0.01) between NG and lG, based on

Wilcoxon test

Exp Brain Res (2012) 216:203–215 211

123

in the lower body and trunk motion in lG could have

allowed their compensation through arm movement

adjustments, so that the hand-in-space trajectory was not

significantly affected.

Modification of the postural component

The results clearly show that the gravitational condition has

a large effect on the postural strategy. The subjects, who in

NG condition tended to keep the CoM within the natural

base of support, in microgravity developed a new postural

strategy resulting in a CoM displacement beyond the feet

extremity. While in NG condition, subjects tended to move

backward the pelvis to compensate for the forward mass

displacement due to trunk leaning, in microgravity, these

postural adjustments disappeared. In turn, the upper body

was not responsible for the increment of the total CoM

forward displacement. In terms of joint strategy, the typical

NG axial synergies, that is to say opposite rotations of the

trunk and leg segments, were replaced in lG by a new

strategy with concurrent motions of all segments toward

the target. The reduction in the axial synergies character-

izing the new lG strategy was accompanied by a small but

significant decrease in the joint coupling, which was

directly correlated with the increase in the CoM forward

displacement. Interestingly, a similar relationship between

small differences in joint synergism and in CoM stabil-

ization was observed in a trunk bending study where the

smaller joint coupling for Parkinsonian patients with

respect to healthy subjects was associated with larger CoM

displacements (Alexandrov et al. 1998a). Therefore, our

results suggest, in agreement with these and other works

(Freitas et al. 2006), that the antero–posterior CoM position

in NG would be one of the variable directly controlled by

the CNS through joint angle covariation and that the lack of

need to control the CoM in lG would allow our brain to

partially release this synergism constraint.

In the frame of literature about motor control in

weightlessness, the large effect of gravity on the postural

control observed here is a very intriguing result. Several

studies have previously shown a persistence of the terres-

trial postural control during movements performed under-

water (Massion et al. 1995), in short-term microgravity

(Mouchnino et al. 1996; Vernazza-Martin et al. 2000) as

well as in orbital space missions (Massion et al. 1993,

1997; Baroni et al. 2001). The main difference between our

results and these studies could be related to the fact that

their protocols did not have a clear externally defined goal.

Analogously to what was observed for a forearm stabil-

ization task (Viel et al. 2010), in weightlessness, the lack of

external goal and gravitational information could induce

the subjects to represent the motor goal egocentrically,

rather than in an external reference frame as in NG. For the

trunk bending protocols, this means that, instead of pro-

ducing a target inclination of the trunk with respect to the

vertical, in lG, the subjects could represent the task in

terms of hip flexion. Since the hip angle depends on the

orientation of the lower limbs, the egocentric and exo-

centric representations of the motor goal are not always

equivalent. Two of the aforementioned studies (Vernazza-

Martin et al. 2000; Baroni et al. 2001), indeed, reported a

significant decrease in amplitude of the trunk inclination in

weightlessness compared with NG. It follows that repre-

senting and performing the task in different reference

frames would not always produce the same perturbation of

posture. Being the observed motor behavior the result of

the interaction between the postural control strategy and

the level of the perturbation, differences in this latter due to

the goal perception could have masked possible changes of

the postural strategy. That could explain why, in contrast to

our results, these studies in microgravity did not show

significant modifications in CoM control during movement.

Our findings also differ from previous lG studies of

downward whole-body reaching tasks where no perturba-

tion, or a very fast recovery, of the terrestrial balance strategy

was observed (Kingma et al. 1999; Patron et al. 2005). This

may be because in these studies, the task fulfillment induced

a very reduced balance perturbation with respect to our

protocol. Indeed, even if the considerable number of DOFs

characterizing such whole-body movement could allow the

use of different joint and muscular strategies, the focal

component of the task did not lead to significant perturba-

tions of the equilibrium, because a large forward displace-

ment of the CoM would have not contributed to reach the

target, which was located close to the subject feet.

We can, hence, conclude that, when the focal compo-

nent of the movement produces an inevitable and sub-

stantial perturbation of balance, as in the task considered

here, the neural mechanisms controlling posture are

strongly dependent on gravity level.

Movement–posture coordination

As it could be expected, because of the strong effect of the

lack of gravity on the postural, but not on the focal, com-

ponent of whole-body reaching movements, the coordina-

tion between these two elements appeared to be perturbed.

In particular, in contrast to the persistence of a high tem-

poral coupling between the hand and CoM motion toward

the target observed during downward whole-body reaching

movements in lG (Patron et al. 2005), here a decrease in

this coupling was shown. As previously mentioned, the

discrepancy with respect to the Patron’s study is likely to

be due to a different location of the target.

Our results suggest that movement and posture do not

respond to a unique hardwired and invariant control

212 Exp Brain Res (2012) 216:203–215

123

mechanism, but to parallel neural commands, the coordi-

nation of which is flexible and adaptable to the gravita-

tional conditions. This hypothesis is supported by previous

studies on the neural activations related to the coordination

between paw reaching movement and balance in cats,

which showed that populations of neurons of the ponto-

medullary reticular formation encode posture and move-

ment independently and others encode a common signal

that contributes to their coordination (Schepens and Drew

2004). Furthermore, noninvasive behavioral studies on

humans showed that supplementary motor area and basal

ganglia are involved in the coordination between posture

and movement (Viallet et al. 1992; Gantchev et al. 1996;

Tagliabue et al. 2009); therefore, the decoupling between

the two subtasks observed here suggests that the gravita-

tional signals would be crucially integrated in the neural

activity of these CNS areas.

Finally, the idea of a flexible coordination between

parallel control mechanisms for focal and postural subtasks

agrees with the theories, which assess that a control system

consisting of semiautonomous subsystems better adapts to

complicated environmental changes (Putrino et al. 2010)

and it would allow a better exploitation of the DOFs of the

motor system, by avoiding the control of irrelevant aspects

of the motor performance (Todorov and Jordan 2002), as

the equilibrium in lG.

Why changes in postural strategy?

The observed effect of microgravity on postural control

could be discussed from a sensory point of view. Indeed, it

has been proposed that the CNS could control posture by

using a body scheme model (Massion 1994), which allows

the estimation of the absolute body configuration through

the combination of proprioception with external source of

sensory information, such as gravitational signals and

tactile information from the feet. Since in microgravity

such external information is strongly modified and thus

difficult to be interpreted, the CNS may not be able to

correctly estimate the CoM position. The observed differ-

ence in postural control in lG could be therefore due not to

the lack of necessity to keep the balance, but to the diffi-

culty in estimating the CoM position. However, if this was

the case, a randomized effect of lG on postural control and

a consequent increase in individual postural variability

should have been found, rather that the systematic modi-

fication here reported.

An additional possible interpretation of the postural

changes observed here could be related to an incomplete

updating of the internal model of gravity used by the CNS

to compute the motor commands necessary to reach the

target and to the consequent use of a partially terrestrial set

of muscle activations to perform the task in lG. However,

although it is very likely that the CNS did not fully adapt

during the short lG periods provided by parabolic flights,

the use in lG of an inaccurate internal model of gravity

should affect not only the postural component of the

movement, but also the focal one. Indeed, if the subjects

had activated their muscles in lG as if a ‘‘residual’’ gravity

was still acting on the body, larger upward accelerations of

the hand should have also been observed. The fact that lG

strongly affected the postural, but not the focal control,

therefore, suggests that the incomplete adaptation of the

internal model of gravity is not the main cause of the

postural modification found here.

The question that can arise is whether there is a specific

reason, or optimality criterion, leading to the observed

systematic change in postural behavior. Indeed, even recent

optimal feedback control theories (Todorov and Jordan

2002; Scott 2004), which would predict a lack of stabil-

ization of an irrelevant variable, such as the CoM in lG,

would have to include some specific optimality criteria to

predict the systematic forward displacement of the body

mass. In order to identify this criterion, we first tested the

hypothesis that in lG, the CNS develops a new motor

strategy aimed at minimizing the torque at the ankle joint

to reduce the dynamic interactions with the environment,

which could make the body control difficult in weight-

lessness (Pedrocchi et al. 2003, 2005). As a matter of fact,

the here detected lG strategy resulted into a decrease in the

ankle torque with respect to the standard NG solution, and

this was true even if the mechanical effect of gravity was

artificially eliminated for the on-ground movements, sug-

gesting that the torque difference was in fact due to

changes in movement strategy and not merely to the lack of

segments’ weight. Differences between the ankle torque in

NG and lG, however, disappeared when the longer

microgravity movements were artificially modified to

match the on-ground movement duration. It follows that, in

contrast to the aforementioned studies, the observed

reduction in the dynamic interactions with the environment

was due to a slower execution of the movement with

respect to NG and not to the modified CoM control, which,

on the contrary, contributed to increase the ankle torque

(significant decrease in the dynamic compensations among

segments). These findings are therefore consistent with the

idea that the increase in the execution time in transient

microgravity would reflect a lG-specific strategy and not

just a difficulty in accomplishing the task (Mechtcheriakov

et al. 2002, Crevecoeur et al. 2010): the slowing of

movement is the way employed by the motor system to

reduce the inter-limb dynamics and to preserve movement

accuracy despite inaccuracies of the internal model of the

weightlessness environment.

If this new postural strategy does not lead directly to the

reduction in interactions with the environment, why does

Exp Brain Res (2012) 216:203–215 213

123

the CNS reduce the axial synergies in lG? The results

suggest than the lG strategy would reflect an oversimpli-

fication of the motor execution. Indeed, in contrast to the

terrestrial movements, which are characterized by two

components (focal and postural), by a significant involve-

ment of a large number of DoFs and by complex learnt

synergisms able to compensate for the destabilizing effect

of the highly non-linear mechanical interactions between

the movement components, the new lG strategy is reduced

to the focal component only (disappearance of the postural

adjustments); it is characterized by a reduced contribution

of some of the joints and by a reduction in the complex

dynamic compensations among segments. In other words,

the oversimplified strategy consists in the slow motion of

all body segments in the target direction, without postural

and dynamic compensations and in a reduced rotation of

the segments with big inertia such as the trunk, so as to

decrease the perturbation due to the focal component of the

movement, instead of using complex dynamic strategy to

compensate for it. Analogously to the increased level of

muscle co-contraction during the first phases of motor

learning in a new dynamical environment (Milner and

Franklin 2005; Hinder and Milner 2007), the ‘‘oversim-

plified strategy’’ observed in the present study appears as

an effective, but not very ‘‘elegant’’ nor energetically

efficient, solution to guarantee the success of the whole-

body reaching despite an imperfect knowledge of the

environment dynamics. This ‘‘motor oversimplification’’

could be therefore a transitory solution. It is likely, for

instance, that after a very prolonged time in orbit, the

internal model of lG will be accurate and motor strategies

involving lengthy execution times would not be compatible

with the everyday life in space where the amount of tasks

to be accomplished can be extremely high. On the other

hand, given the persistent lack of equilibrium constraint in

lG, it is likely that the astronauts will never develop a

terrestrial postural strategy. Analyses of similar tasks dur-

ing long-term space missions on board the International

Space Station should reveal the trend and the lasting

optimal strategy chosen by the brain.

Acknowledgments This work was supported by the Italian Space

Agency (ASI), by Centre National d’Etudes Spatiales (CNES) and by

the Italian Institute of Technology (IIT).

Conflict of interest The authors declare that they have no conflict

of interest.

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