Postural control system

Jean Massion

Laboratory of Neurobiology and Movements, CNRS, Marseille, France

The postural control system has two main functions: first, to build up posture
against gravity and ensure that balance is maintained; and second, to fix the
orientation and position of the segments that serve as a reference frame for
perception and action with respect to the external world. This dual function
of postural control is based on four components: reference values, such
as orientation of body segments and position of the center of gravity (an
internal representation of the body or postural body scheme); multisensory
inputs regulating orientation and stabilization of body segments; and flexible
postural reactions or anticipations for balance recovery after disturbance, or
postural stabilization during voluntary movement. The recent data related to
the organization of this system will be discussed in normal subjects (during
ontogenesis), the elderly and in patients with relevant deficits.

Current Opinion in Neurobiology 1994, 4:877-887

Introduction body orientation with respect to verticality. The postu-

ral reactions, like the ‘anticipatory’ postural adjustments
Body posture is built up by a set of assembled segments, associated with voluntary movements, are organized on
each with its own mass, that are linked together by the basis of this internal representation, as is the whole set
flexible joints controlled by the neuromuscular system. of interactions involved in perception and action towards
The central organization of posture involves interactions the external world.
between external forces, such as gravity, the mechanical
Because of the complexity of the postural control system,
properties of the body and the neuromuscular forces.
many aspects have given rise to some debate. How are
In order to understand the present trends in studies on posture and equilibrium centrally organized? How does
postural organization, one should bear in mind that pos- the organism adapt to changes, such as microgravity, in
ture serves two main functions. First, it has a mechani- the environment? How is the system built up during on-
cal antigravity function whereby the reference posture togenesis? What impairments affect it in the elderly and
(stance) is built up; equilibrium also depends on this diseased?
antigravity function, which requires the center of grav- Progress in research often depends on new methodologi-
ity (CG) projection to remain inside the supporting cal approaches. A new method has recently been used
surface under static conditions. Second, it serves as a in this field to analyze postural control in the absence
reference frame for perception and action with respect of external disturbances. Classical methods of analysis,
to the external world. The position and orientation of such as recording the center of pressure oscillations from
body segments such as the head, trunk or arms serve as a a force platform under normal stance, have been re-ex-
reference frame for calculating target locations in the ex- amined. The stationary properties of postural sway have
ternal world and for organizing movements toward these been questioned [l]. New techniques of analysis using
targets. the chaotic dynamic approach have been proposed in
In line with the complexity of the functions mediated order to identify putative ‘attractors’ in postural sway
by posture, central organization of its control system in- [2]. Collins and De Luca [3’] have carried out stochas-
volves many interacting elements. On the sensory side, tic analyses on the center of pressure oscillations during
multisensory (visual, labyrinthine, proprioceptive and quiet stance to identify the open-loop and closed-loop
cutaneous) inputs contribute to orienting the postural components of these oscillations. A cross-correlation
segments with respect both to each other and the ex- method has been used on simultaneously recorded kine-
ternal world (vertical gravity vector). These classes of matic parameters at various levels of the multijoint chain
sensors monitor any mismatch between the intended involved in erect posture, with a view to identif+ng the
and actual positions. A so-called ‘postural body scheme’ kinematic strategies used under various sensory condi-
provides an internal representation of the body geom- tions ([4*], see also IS]). Several mathematical analyses
etry, the body dynamics (support conditions) and the have been carried out on multijoint changes to elucidate

Abbreviations
CC-center of gravity; EMG-electromyograph,

0 Current Biology Ltd ISSN 0959-4388 877

878 Neural control

Postural control

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1 Orienta’;‘;’ 1 1 ;;““ility 1 fX3y

Feedback control
of posture

Cunent Opinion in Neurobiology

Fig. 1. Central organization of postural control. This schematic diagram summarizes the main components involved in the central organization
of postural control. There are two sets of reference values, one is related to body segment orientation and the other is related to whole body
stability (equilibrium control). These references values, and their maintenance against external or internal disturbances, are based on a body
schema or internal representation of the body, which include several components, namely, body geometry and kinetics, representation of
verticality and reference frame. In addition, postural networks contribute to the execution of the postural tasks. Multisensory inputs are used for
building up the body schema. These inputs also act as error-detecting sensors for evaluating the mismatch between the prescribed orientation
and stability, and the actual posture. The postural reactions in the presence of an error message, as well as the anticipatory postural adjustments
in association with voluntary movements, are exerted through the postural networks on one or several segments. The execution of the postural
reactions or anticipations are controlled on line by local feedbacks.

the control processes involved in the kinematic control
of posture [6*,7*]. Biomechanical modelling is another
interesting means of studying the postural strategies de-
veloped, depending on the constraints [8*,9’,10-121.
This review will focus on four aspects of the postural
control system, where the main contributions have been
made recently. These advances are related to the control
of the center of gravity, the concept of postural body
schema, postural reactions and anticipation, and age-re-
lated changes.
Center of gravity control versus body geometry
When stance is disturbed in bipeds or quadru-
peds, the resulting postural reactions tend to move the
body back toward its initial position, as long as the
imposed disturbance does not overcome given limits.
During stance, there is thus a reference position that
is stabilized. Some controversy has arisen as to whether
the reference value stabilized to preserve balance is the
center of gravity position with respect to the ground, or
whether the body geometry is the main value regulated.
In the former situation, the fictive point (CG), which is
the result of the masses of the individual body segments,
would be directly regulated, whereas in the latter, this
fictive point would be regulated secondarily as a result
of body geometry control.
Lacquaniti has provided evidence (see [13]) that in the
cat under normal stance, it is the body geometry rather
than the CG that is regulated. First, the length and an-
gle of the limb axis with respect to the vertical were kept
constant when the supporting platform was tilted in the
sagittal plane. Second, the CG moved when a load was
added in front of the CG position, indicating that no
direct regulation of the CG position occurred. In a re-
cent study, Lacquanti and Maioli [14**] identified two
separate control systems, one regulating limb length and
axis with respect to the vertical, and the other the hori-
zontal contact forces (lever component) exerted by fore
and hindlimbs in order to stabilize the body. This kinetic
control system presumably plays a role in maintaining the
CG within the support area. In fact two parallel control
systems therefore exist, the one focusing on the body
geometry and the other on stability [14*-l (Fig. 1).
Is the limb axis, with respect to the vertical, the ge-
ometrical reference value which is regulated during

stance? An alternative explanation has been proposed
by Macpherson [15**] and by Fung and Macpherson
[PI. By changing the interlimb distance in the sagit-
tal and frontal plane, they concluded that the length
and the orientation of the trunk with respect to the
supporting surface, i.e. an external reference frame, is ac-
tually regulated, the legs being used as levers to maintain
the trunk length constant, while the interlimb distance
is varied. These authors concluded that the preferred in-
terlimb distance during natural stance corresponds to the
distance involving the least energy consumption [Y].
Is the CG regulated in human? In human bipedal stance,
the narrow support surface provided by the foot area and
height of the body with respect to the ground make
for a much smaller safety margin than in quadrupeds.
It has been established previously that after stance dis-
turbances, one of the strategies used, namely the hip
strategy, consists of flexing or extending the hip, in or-
der to keep the CG within the stability limits [lb]. The
same change in body geometry occurs when a voluntary
movement of the upper trunk is performed; this would
entail a movement of the CG in the same direction if no
corrective processes intervened. Opposite displacements
of the lower segments then occur however, which re-
sults in the maintenance of CG within the support area.
This has been termed ‘synergy’ by Babinski [17] but a
more appropriate name might be ‘kinematic strategy’, in
line with the hip strategy known to counteract imposed
disturbances. These findings indicate that in humans, the
body geometry changes in order to regulate the CG po-
sition.
The question then arises as to how the CG is regulated,
especially when a voluntary movement is performed
which would induce imbalance. The kinematic strat-
egy observed during upper trunk bending has been ana-
lyzed using the principal components analysis method.
Surprisingly, both the movement and the CG regula-
tion carried out using the kinematic strategy were ex-
pressed by the first principal component as fully as 99%
in the case of forward upper trunk movements [7’] and
96% in backward movements. This indicates that a single
central control fixes the ratios between angular changes
in the hip, knee and ankle joints and synchronizes their
changes with time. The axial kinematic changes associ-
ated with upper trunk movements thus constitute an au-
tomatic control, probably learned in childhood, whereby
the movement and the CG position are controlled simul-
taneously This would explain why angular changes asso-
ciated with upper trunk movements remain unchanged
under microgravity, in the absence of any equilibrium
constraints [ 181.
In addition to the stabilization of the CG position, the
orientation of several body segments has also been re-
ported to be regulated simultaneously during stance,
movement or locomotion. For example, the head axis
is often stabilized with respect to the vertical during lo-
comotion [19,20]. This stabilization provides a reference
value aligned with the vertical axis, used for monitor-
Postural control system Massion 879
ing, via visual and vestibular inputs, the head and body
movements with respect to the environment. Head- and
trunk-centered reference Ii-ames are also used for target
location and movement trajectory planning (see [21]).
The trunk axis is actively stabilized during locomotion
in both the frontal and sagittal planes, due to the ac-
tion of the hip muscles [22*,23]. The trunk stabilization
in the frontal plane is increased in labyrinthine defective
patients [24]. The trunk axis also remains vertically ori-
ented during leg raising, especially in dancers [25]. As
the trunk axis serves as an egocentric reference frame
for calculating leg position [26*], vertical orientation of
the trunk may be used for direct calculation of the leg
position with respect to space.
To conclude, the results of recent investigations indicate
that in cats and humans, two control systems can be
identified: one fixes the orientation of the body seg-
ments with respect to the external world, while the
other ensures the stability of the body and contributes
to stabilizing the CG (Fig. 1).
Postural body scheme
According to Gurfinkel [27], there is an internal repre-
sentation of the body, or postural body scheme, which
is not primarily based on sensory information and deals
with the body kinematics and kinetics as well as the ori-
entation of the body with respect to the vertical. This
representation is “used for the perception of body posi-
tion and its orientation in space and is also used for mo-
tor control, including reactions directed towards main-
taining stable body position”[27].
The body scheme remains quite stable during dras-
tic changes in environmental conditions, such as those
occurring under microgravity, where the vestibular and
proprioceptive inputs are greatly modified (see [28-l). As
ascertained by testing subjects’ perception of complex
tactile stimuli [29] or by asking them to draw ellipses
with prescribed orientations [30], the egocentric refer-
ence frame is still used in the absence of gravity to per-
form perceptual and spatial orientation tasks efficiently.
The amplitude of forearm movements in the vertical and
horizontal planes remains roughly unchanged under mi-
crogravity, except in the case of slow movements, which
are disturbed because they are controlled by propriocep-
tive feedbacks, which are depressed under microgravity
[28*]. The ability of subjects to point to remembered
target positions deteriorates in space [31].
The sensors that contribute to estimating the body’s
orientation, configuration and support conditions have
been further investigated. One of the questions currently
under debate concerns the estimation of the gravity vec-
tor. Besides the well-known contribution of labyrinthne
inputs and vision to monitoring the vertical axis, a pu-
tative role of body graviceptors has been suggested in
the past [32,33], and this idea has recently been indi-
880 Neural control
rectly supported. By adding loads under water, where
the body’s weight is cancelled by the water pressure, or
by adding a horizontal force equal to the body weight
while the subject is lying down, the previously absent
postural reaction to ‘support’ disturbances can be re-
stored. These results argue in favour of the presence of
graviceptors distributed among the segments.
Which sensors are used to monitor the load? One
possible explanation might be that the muscle effort
opposing the effects of gravity or other forces may be
estimated by the Golgi tendon organs, whose discharge
pattern correlates with the number of active motor units
[34,35]. U sm. g a d’1ff erent approach, based on a subjective
estimation of verticality, Riccio, Martin and Stoffregen
[36] reached similar conclusions by artificially dissociat-
ing the gravity vector horn the axis of the ground reac-
tion forces that have to be controlled in order to maintain
equilibrium. These authors concluded that the subjective
vertical depends on both the gravity vector and the di-
rection of the ground reaction forces needed to control
balance. Interactions between the orientation of the vi-
sual reference frame and somatosensory inputs relating
to the body orientation with respect to the vertical in
the perceived subjective vertical have also been found
to occur by Nemire and Cohen [37], indicating the
importance of the trunk axis (idiotropic vector) in the
perceived vertical [33]. Under microgravity, the percep-
tion of the subjective vertical in the absence of vision
may depend on the ‘saccular’ Z bias, that is, on the
difference between the mean resting discharges of sac-
cular units polarized in the rostra1 and caudal directions.
Other cues - such as tactile, visual and proprioceptive
- also play an important role in body orientation under
microgravity [38].
One of the most clearly emerging properties of the sen-
sory inputs that contributes to the body scheme is the
marked dependence of these inputs on context, partic-
ularly on the reference frame used for their analysis (see
discussion in DiZio it a/. [39-l). For example, the illu-
sory or effective body sways that result horn artificial Ia
inputs produced by vibrating bilaterally the tendon of
either the gastrocnemius or tibialis anterior muscle in
a standing subject tend to disappear under microgravity
[40*]. These ‘postural’ illusions or reactions are therefore
gravity-dependent.
The role played by vestibular and proprioceptive inputs
in human self-motion perception in space also depends
on the reference frame. Mergner ETal. [41*], using vari-
ous combinations of head, trunk and feet rotation, have
proposed a model in which the vestibular signal and the
proprioceptive input arising along the whole body axis
were used to reconstruct the perception of head, trunk
and feet position in space. In vestibular patients, the
perception of trunk rotation in space with the head
free is deficient contrary to normal subjects, indicat-
ing that vestibular inputs are normally responsible for
this perception [42*]. With the head fixed during trunk
rotation, patients perceived an illusory head movement
(due to the nuccal afferents). As soon as a fixed visual or
tactile reference frame was used, the same patients with
vestibular deficits perceived the real trunk rotation. Sim-
ilar results were obtained by Guxfinkel and Levik [43-l
in normal subjects, using very slow trunk rotations that
were not perceived at all with the head f?ee. With the
head fixed, illusory head rotation is perceived; whereas
when the hand is in contact with a rigid handle fixed to
the wall, the real trunk rotation is perceived [43*]. How
the proprioceptice input is interpreted by the subject is
therefore highly dependent on the reference frame used
at the same time.
Postural responses are also markedly context-depen-
dent. This is illustrated by the responses induced by
labyrinthine stimulation [44*]. A standing subject’s re-
sponse to galvanic stimulation of the labyrinth consists
of a postural sway in the direction of the ear behind
which the anode is placed. As previously established,
the direction of the sway changes with the head posi-
tion with respect to the trunk, and that of the trunk
with reference to the legs; the direction of sway therefore
depends on the body geometry at the time of stimula-
tion. The electrbmyograph (EMG) response associated
with the sway (the late component of the response) de-
pends on the support conditions: it occurs in the arm
muscles when part of the body support is exerted by the
hands, and disappears in the soleus in the sitting sub-
ject. It therefore occurs in the muscles that are actively
engaged in balance. Moreover, reduced responses were
observed when other sources of afferent information are
available, for example when the subjects touched a fixed
support or when their eyes were open.
Postural reactions
Postural reactions are elicited on the basis of sensory sig-
nals that indicate a disturbance ofposture and/or equilib-
rium. Experimental stance disturbances are usually pro-
duced by moving the supporting platform. Disturbances
restricted to the hip level have also been tested and con-
pared between normal and hemiparetic patients [45].
Discrete disturbances have usually been used; pseudo-
random disturbances have also been tested [46]. The
central organization of the postural reactions will not
be specifically discussed here (see Jankowska and Ed-
gley [47] on the spinal cord organization). It is worth
mentioning however that chronic spinal cats show very
poor postural control [48].
One of the emerging ideas about the organization of
postural reactions is that the central nervous system is
unable to control individual muscles separately and that
it controls only a small number of degrees of freedom by
activating functional synergies, involving a set of muscles
regulated as a whole [49,50]. Synergies have commonly
been observed in postural reactions. They appear to be
flexible and depend on external constraints such as the

direction of the forces disturbing posture. The bifunc-
tional muscles that extend across two joints contribute
largely to this flexibility, because their activity depends
more strongly on sensory inputs than the single joint
muscles, and they might serve to orient the force vec-
tor exerted by the single joint muscles depending on the
requirements of the postural task [51*].
It has been suggested by Horak and Nashner [16] that
a higher level of organization may be involved in the
postural reactions to stance disturbance: at this level
strategies are selected that each define a given type of
action for restauring balance. Hip strategy (torques and
movement at the hip joint), ankle strategy (torques and
movement at the ankle joint), and stepping are different
ways of restoring balance, depending on the intensity of
the balance disturbance and the constraints. The mus-
cle synergy may be a lower level of organization, imple-
menting the strategy by providing the appropriate muscle
forces.
Recent data tend to show that the strategy level is also
flexible and adaptable to task constraints. For exam-
ple, the hip and ankle strategies are not ‘all or none’
reactions but rather form a continuum under progres-
sively changing external constraints. Horak and Moore
[52*] have observed that a continuum occurs in postural
changes involving gradually more hip strategy and less
ankle strategy when leaning forward is increased. The
postural response to stance disturbance is also adapted
when a disturbance to equilibrium is used as a sig-
nal for gait initiation; in this situation, goal-directed
changes in postural responses were found to occur [53].
Conclusions on the same lines were reached by Al-
lum et al. [54-l, who disturbed standing posture by
random combinations of rotation (triggering the hip
strategy) and translation (triggering the ankle strategy)
of a supporting surface. On the basis of kinematic and
EMG analysis, they established that one out of two
discrete muscle synergies was selected on the basis of
leg afferent input. In addition, segmental velocity re-
lated inputs continuously update the initial pattern. A
comparable updating of the basic pattern by segmental
inputs was also reported by Forssberg and Hirschfeld
[55-l during disturbance of the sitting position. A depen-
dence on the biomechanical constraints was also found
in the case of the ‘force constraint strategy’ observed in
the cat, whatever the direction of the stance disturbance
[9*,15**]. This strategy does not depend on prior experi-
ence and is therefore part of the animal’s repertoire [56].
It is characterized by the fact that the force directions ex-
erted to restore balance under individual paws are always
oriented forward and backward whatever the direction
of the balance disturbance. This strategy disappears with
small interpaw distances. On the basis of a biomechani-
cal analysis, Macpherson and Fung [9*] have proposed
that this strategy may be aimed at preventing a lateral
bending of the trunk, thus maintaining the back length
invariant when lateral disturbing forces are present. With
shorter interlimb distances, the back incurvation seems
to be prevented by an increase in back stiffiless [9*].
Postural control system Massion 881
There is also some flexibility in compensatory stepping
observed in response to stance disturbance. This response
depends on the velocity of the disturbance as well as on
the instructions given to the subjects. Aborted reactions
are also observed where only the initial weight transfer
toward the supporting limb occurs [57,58]. The step-
ping response is thus composed of several stages, each of
which includes a decision made on the basis of sensory
cues.
Role of sensory inputs
Some recent investigations have been carried out on the
respective roles of the various categories of sensory in-
puts involved in postural stability.
To what extent do the vestibular inputs contribute to the
postural reactions to stance disturbance? In cats, with
bilateral labyrinthectomy, no change in the force con-
straint strategy nor in the muscle synergy afier stance
disturbance was detected [59]. Hypermetric responses
are seen early after the operation. In humans, a spe-
cial device for producing phasic vestibular linear stim-
ulation by displacing the head was tested. This stimula-
tion induced postural responses in leg and trunk muscles
in standing subjects. These responses were rather weak,
however, suggesting that vestibular inputs do not con-
tribute strongly to early postural reactions to balance
stance disturbances [60*]. The vestibular system plays
a role in organizating hip strategy [61]. Imposed ankle
joint rotation induces a hip strategy in normal subjects,
which disappears in vestibular patients and is replaced by
a rather inefficient ankle strategy [54*]. It should also be
mentioned that no vestibular deficits were detected in
Parkinsonian patients with impaired balance [62], and
that, generally speaking, the usual multisensory inputs
are properly integrated in these patients [63]: this suggests
that the disorder affects only the control of the postural
reactions.
The role of leg somatosensory inputs in postural stabil-
ity has also been investigated. For example, longitudinal
platform oscillations at 8-24 Hz markedly increased the
subjects’ postural instability [64]. The somatosensory
inputs are not only involved in postural stability: so-
matosensory inputs Gem the lower leg also contribute
directly to the stabilization of the head as do the vi-
sual and vestibular inputs 1651. Are the somatosensory
inputs from the leg needed to trigger and scale human
automatic postural responses? In patients with lower limb
neuropathy, the postural reactions to stance disturbance
are still present, but their latency increases (2@3Oms)
[66*]. This suggests that leg somatosensory inputs are
actually used to trigger and scale the postural reactions;
however, other inputs (trunk, vestibular and visual) may
replace the missing inputs.
How are somatosensory inputs used to scale the postural
response in ccrebellar patients [67’]! Interestingly, in pa-
tients with anterior lobe pathology, feedback-controlled
scaling, depending on the velocity of the disturbance, is
882 Neural control
still possible. In contrast, scaling of the response am-
plitude, which depends on presetting before the dis-
turbance onset, disappears and is replaced by tendency
towards hypermetria.
Concerning the role of vision in postural control, it has
been shown that postural sway is equally controlled by
peripheral and central visual fields [68].The effects of a
moving visual environment on postural oscillations have
been investigated by Previc et al. [69] and Dijkstra et
al. [70]. The latter paper concludes that retinal slip
minimization does not explain the coupling between
a moving visual environment and postural sway, and
that a dynamic coupling between the two must exist.
Vision has been found to shorten the latency of postural
responses [71]. Vection has been shown to shorten or de-
lay the onset of balance recovery in unexpected forward
falls, depending on the direction of the moving scene
[72]. Lastly, the respective roles of the somatosensory
and visual inputs in stabilizating body motion depend
on the stance width. With a larger supporting base, the
role of vision in body stabilization in the frontal plane
decreases in favor of somatosensory inputs [ll]. Visual
motion compensates in the cat for loss of vestibular in-
put during the early stages of recovery after unilateral
labyrinthectomy. The vestibular nucleus response to op-
tokinetic stimuli on the deafferented side shows an in-
creased band width [73].
Anticipatory postural adjustments
Unlike the postural reactions in response to the onset of
posture or balance disturbances, the anticipatory postural
adjustments precede the disturbance onset and therefore
minimize the effects of the forthcoming disturbance in
a feedforward manner.
Anticipatory postural adjustments usually occur in asso-
ciation with voluntary movements, which are one of the
main sources of posture and balance disturbance. Antici-
patory adjustments can also be observed, however, when
imposed disturbance is recurrent, as in the case of hu-
man stance on a sinusoidally translating platform. The
anticipatory adjustments which are then observed serve
to orient the body so as to minimize the effects of grav-
itoinertial forces. When the frequency of the platform
translation is changed, the feedforward mode is replaced
by a feedback mode of control for a few oscillations
and the feedforward control then reappears [74’]. This
anticipatory postural control is impaired in Parkinsonian
patients [75].
Anticipatory postural adjustments before the disturbance
of a single joint position caused by the voluntary move-
ment of another segment have been described. For ex-
ample, when a subject is tapping with a hammer on the
radial muscle of his other forearm, there is a silent period
in the muscle response pattern before the actual me-
chanical impact. This inhibition may minimize impact
effect on forearm posture by reducing muscle stiffness
in advance of the disturbance [76]. The mechanisms re-
sponsible for anticipatory postural adjustments have been
investigated. In a bimanual load lifting task, where one
arm was supporting the load and the other voluntary
lifting the load, anticipatory postural adjustments were
observed in the postural arm (see [77]). Interestingly,
the sarne adjustments were observed in a patient with
forearm-afferent deprivation, indicating that these ad-
justments result from feedforward control. The limb
afferents are necessary, however, for new anticipatory
postural adjustrnent when unloading the postural fore-
arm is triggered by new movement [78].
Anticipatory postural adjustments aimed at maintaining
balance have been observed with upper trunk move-
ments (see [77]). These adjustments are impaired in
cerebellar anterior lobe patients; the main deficit involves
a lack of feedforward activation in the thigh muscles at
the onset of the movement [79]. Respiratory oscillations
can also lead to balance disturbance. As the respiratory
oscillation estimated from the center of pressure sway
path recorded from a force platform is larger in sitting
than in standing subjects, anticipatory control seems to
be more efficient when standing than when sitting [80].
The last specific type of postural adjustment occurs with
movements involving the legs, such as gait initiation,
standing on tip toe or the heels and lifting or raising
a leg. With motor acts of this kind, the movement is
preceded by postural changes that shift the CG toward a
new position compatible with equilibrium maintenance
during the leg movement. These types ofpostural adjust-
ments are impaired in patients with hemiparesis. When
asked to lift a leg, they are not able to use the paralyzed
limb to exert the appropriate horizontal ground reaction
forces needed to move the CG toward the supporting
leg [81]. When asked to stand on tip toe, the temporal
sequence is disturbed on both sides [82]. Standing on
tip toe is also markedly impaired in anterior lobe cere-
bellar patients [83] and Parkinsonian [84]. The scaling of
the amplitude and duration of the preparatory postural
phase is abnormal in cerebellar patient (low amplitude,
prolonged duration) and the temporal relationship be-
tween the postural and movement phase is lost.
Age-related changes
Ontogenesis
Successive steps have been described during the devel-
opment of posture: postural control of the head, postural
control of the trunk, sitting position, standing and loco-
motion. The emergence of these various stages depends
on the evolutional state of several systems, such as the
musculo-skeletal system, the sensori-motor system, the
level of motivation and of behavioral development, and
the internal and environmental constraints [85].

Both the visual and somatosensory systems are crucial for
stabilization of head, trunk and whole body posture, but
vision is effective earlier than the somatosensory system.
At each stage in postural development, moving visual in-
formation contributes to maintaining posture and equi-
librium. It has been established that vision and optic
flow influence spontaneous head oscillation as early as
2 to 3 days after birth, and head posture as early as
5 months of age [86]. A response to optic flow oc-
curs with a supported standing posture as early as 5
months of age and increases considerably later on. The
somatosensory system is mainly involved in reactions to
support disturbances. Head stabilization is observed from
3 to 4 months of age and head-trunk stabilization in sit-
ting posture at 5 months [87]. Hirschfeld and Forssberg
[88*] have observed that in sitting children who undergo
a forward horizontal balance disturbance, the EMG
pattern is roughly comparable to the adult one [55*],
since the activation of the front muscles induced by
backward trunk imposed displacement is similar to what
occurs in adults, although this is not so in the case of the
back muscles. These authors suggested that two levels of
control might exist: basic one present in children, and
that which develops in adults as the result of learning.
At 9 months of age, the classical distal-proximal EMG
pattern present in adults subjects to platform disturbances
is present in standing children. It is preceded by a stage
where only the ankle joint muscles are activated and
standing without support is not possible [89,90]. The
vestibular contribution to postural reactions has turned
out to be apparently less important than the somatosen-
sory one early in life, but further investigations will be
necessary to elucidate this point.
Special attention has been paid to equilibrium control
during locomotion. As soon as locomotion starts, stabi-
lization of the hip in the frontal plane with respect to
space is observed [91*,92]. After two months of walk-
ing experience, stabilization of the shoulders improves.
This suggest that a hip-centered temporal organization of
balance control occurs while walking. Long-term mat-
uration of locomotor balance has also been investigated.
During the first stage (3-6 years), the head is stabilized
on the trunk whenever constraints makes equilibrium
difficult. By 7-8 years, the head is also stabilized in space
during locomotion when facing equilibrium constraints.
Adults use similar stabilization of the head in the frontal
plane while walking on a narrow support (see [85]).
Does the head stabilization in space depend on visual in-
puts or is it based on vestibular cues? Although peripheral
vision and movement visual cues play an important part
in balance control, especially in young children, head
stabilization in space does not depend to any great ex-
tent on visual cues and may therefore mostly depend on
vestibular cues [20]. Head stabilization in space in chil-
dren as in adults [93] is a basis for ‘top-down’ postural
control on basis of visual and vestibular cues.
Postural control system Massion 883
Ageing
The balance deficits that occur with ageing have been
extensively studied over recent years. Authors of three
recent papers [94-961 have emphasized the multiple
sources of balance deficits in the elderly and the need
to adopt a systemic approach. For example, sensory
receptors deteriorate with ageing. Sensory deprivation
or sensory conflicts have more drastic effects on balance
in the elderly than in younger subjects [97]. Mechanical
properties of the tendons and muscles are also affected
in terms of their force and elasticity. Postural responses
are delayed and weaker with more co-activation in the
elderly [98]. Ability to adapt changing external perturba-
tions such as shifting from a translation to a rotational dis-
turbance is impaired. Postural responses associated with
voluntary movements are also impaired (increased laten-
ties, excessive co-contractions, etc.) [99]. Furthermore,
the attentional demands of postural tasks are increased
in the elderly [loo]. Generally speaking, the impairment
of balance that develops in the elderly results from the
degradation of multiple systems that participate, either
directly or indirectly, in the task of balance control.
Conclusions
The overall picture of postural organization that emerges
horn recent investigations is a long way off the picture
of classical postural reflexes presented by the Sherring-
tonian School. While the old description of these re-
flexes is still valid and their analysis is still a useful means
of experimentation and neurological evaluation, the en-
phasis now is on the flexibility of postural control and its
adaptability to different contexts.
Such flexibility is reflected in the multisensory integra-
tion which is involved in postural orientation and sta-
bilization. The multisensory aspect of postural control
was first pointed out as early phylogenetically as in the
lamprey [lOl*], but its ability to adapt to context and
task is characteristic of higher vertebrates. This explains
the large range of compensatory possibilities available in
the case of selective sensory deficits, and also the fact that
a given sensory input can induce various perceptions or
postural reactions, depending on the reference frame se-
lected and the external constraints such as gravity This
flexibility is under the control of the internal representa-
tion of the body or postural body scheme, which remains
quite stable under changing conditions.
Postural reactions show a similar degree of flexibility.
Some invariant aspects of postural reactions, such as
strategies and synergies, appear to be less fixed than
was first thought to be the case, and change depend-
ing on the constraints. The external constraints, as well
as the biomechanical properties of the body segments,
impose choice of control. One of the main criteria for
the emergence of a postural pattern after training is that
884 Neural control
it should be as economical as possible in terms of en-
ergy consumption. This does not mean that the brain is
merely a passive player in the game. Its role is to utilize
passive forces to organize the most suitable spatiotempo-
ral pattern in order to carry out a task. It plays a crucial
role in coordinating postural tasks with various aspects of
the ongoing action. The coordination between posture,
equilibrium and movement is certainly one of the main
functions of the postural control system.
Acknowledgements
The author wish to thank S Zakarian for the very efficient
help in the preparation of this review paper, and F Horak and
J Macpherson for their critical reading of the manuscript. The
CNES (Centre National d’etudes Spatiales) is acknowledged for
its support.
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