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Why and how are posture and movement coordinated?

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DOI: 10.1016/S0079-6123(03)43002-1 · Source: PubMed

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Progress in Brain Research, Vol. 143
ISSN 0079-6123
Copyright ß 2004 Elsevier BV. All rights reserved

CHAPTER 2

Why and how are posture and movement

coordinated?

Jean Massion1,*, Alexei Alexandrov2 and Alexander Frolov2

1
Laboratoire Parole et Langage, Universite´ de Provence, 13621 Aix-en-Provence, France
2
Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Science, Moscow 117865, Russia

Abstract: In most motor acts, posture and movement must be coordinated in order to achieve the goal of the task. The
focus of this chapter is on why and how this coordination takes place. First, the nature of posture is discussed. Two of
its general functions are recognized; an antigravity role, and a role in interfacing the body with its environment such
that perception and action can ensue. Next addressed is how posture is controlled centrally. Two models are presented
and evaluated; a genetic and a hierarchical one. The latter has two levels; internal representation and execution. Finally,
we consider how central control processes might achieve an effective coordination between posture and movement. Is a
single central control process responsible for both movement and its associated posture? Alternatively, is there a dual
coordinated control system: one for movement, and the other for posture? We provide evidence for the latter, in the
form of a biomechanical analysis that features the use of eigenmovement approach.

Introduction understand why and how this coordination occurs, it

During the execution of voluntary movements, many
aspects of the same task are coordinated and
performed simultaneously. Gaze orientation (toward
a target) results from the parallel control of eye and
head movements (Bizzi et al., 1977). Coordination
between posture and limb movement is another
example seen in daily life. Often, two goals must be
achieved at the same time. There is need for an
accurate performance of a goal-directed movement
on the one hand, and the maintenance of equilibrium
and an appropriate posture, or set of postures, on the
other (for review, Massion, 1992, 1994, 1998; Horak
and Macpherson, 1996). Similarly, the elaboration of
a locomotor gait requires coordination between a
postural function (support of the body segments
against gravity; forward acceleration of the center of
mass, CM) and the rhythmic movements of loco-
motion (Mori, 1989; Mori et al., 1999). In order to
*Corresponding author: Tel.: þ 33-4-4257-1228;
Fax: þ 33-4-4257-1228; E-mail: jean.massion@lpl.univ-aix.fr
is important to precisely define posture and explore
how it differs from movement.
A simple, coarse-grain definition is that posture
(also called ‘attitude’) is the body segments’ config-
uration at any given time (Thomas, 1940). This
definition is purely descriptive and it does not refer
to the many functions subserved by posture. To this
end, several approaches have been proposed in the
literature. One refers to stance as a genetically
determined reference posture, with characteristics
which are species dependent. This view was cham-
pioned in the classical works of Sherrington (1906),
Magnus (1924) and Rademaker (1931). They all
emphasized that the body’s orientation with respect to
gravity was determined by a group of reflexes that sets
the body segments’ collective orientation and stabi-
lizes this orientation against external disturbances.
A second approach is related to the concept of
support. Kuypers (1981) proposed it on the basis of
anatomical and functional considerations. In this
concept, axial and proximal body segments, and their
corresponding musculature, serve as a support for the

13
DOI: 10.1016/S0079-6123(03)43002-1
14
distal musculature, such as the hands for reaching
and grasping. This view was actually proposed
previously by Hess (1943). He made a distinction
between the ‘eiresmatic’ (supporting function) aspect
of a motor act and the ‘teleokinetic’ (goal-directed
movement) aspect. Hess proposed that missing the
goal resulted from the lack of appropriate support for
the movement (see Stuart et al., Chapter 1). More
recently, Bouisset et al. (1992) proposed a modified
version of the support concept, ‘posturo-kinetic
capacity’. It involves the capacity of the supporting
segments to assist the ongoing movement in terms of
their speed and forcefulness.
A third approach is to distinguish relatively sharply
between posture and movement. Its proponents argue
that the maintenance of a posture means that the
position of one or several body segments are fixed with
respect to other segments (also termed ‘joint fixation’)
or with respect to space (i.e., the external environ-
ment). This position is stabilized against external
disturbances. In contrast, ‘movement’ to these work-
ers means a change of posture (or position), i.e., the
initial posture is destabilized to achieve a new
position, which is reached through a trajectory (see
also S. Mori et al., Chapter 33). Feldman’s (1966)
equilibrium point hypothesis (for an introductory
review: Latash, 1993) is in line with this view.
Posture has two primary functions
It is clear that the current definitions of posture are
multiple, each resulting in different experimental and
theoretical approaches. One way to identify a
unifying model is to ask the question ‘‘what are the
underlying postural functions common to these
different views?’’. From this perspective, two primary
functions emerge: antigravity control, which requires
the buildup against gravity of the body segments’
collective, overall configuration, and the interface
between perception and action (i.e., controlling the
relationship between the external world and the
body).
Antigravity control
Two related processes accomplish antigravity con-
trol. First, the various segments of the kinematic
chain from feet to head should be able to support the
body’s weight against gravity forces and resulting
ground reaction forces. In addition, the kinematic
chain should be able to provide a dynamic support to
the moving segments when they are involved in a
goal-directed action.
The second process is equilibrium control. It
ensures that under static conditions, the center of
pressure and the projection of the center of gravity
(CG) should remain inside the support surface (i.e.,
the support’s contact with the environment).
Interface between perception and action
Each body segment position can be defined with
respect to the other body segments. An egocentric
reference frame is used to calculate each body
segment’s position with respect to the axis of a
given reference segment, such as the trunk or head.
When a target is moving in external space, its
position can be coded into a coordinate system
external to the body (allocentric reference frame). The
latter usually uses the vertical gravity axis as a
reference (Berthoz, 1991; Paillard, 1991). In order to
match the egocentric reference frame to the external
world, the orientation of the trunk or head (the
referent in the egocentric system) is calculated with
respect to the vertical gravity axis (the referent for the
external world). This calculation is based primarily
on a set of sensors: the otoliths, and body gravi-
ceptors (in the soles of the feet and pelvis, possibly
also muscle Golgi tendon organs), which monitor the
gravity axis (Horak and Macpherson, 1996; Massion,
1998). The known orientation of the head and/or
trunk with respect to the gravity axis can then be
utilized both for the calculation of the other body
segments’ orientation with respect to the external
world, and the external target’s position with respect
to the body (Assaiante and Amblard, 1993;
Mouchnino et al., 1993; Pozzo et al., 1995). The
reference is for the perception of body’s movements
with respect to the environment and the control of
balance. Body segment orientation with respect to the
vertical axis also serves as a reference frame for
calculation of a target’s position in space and
the trajectories required to reach this target (Wise
et al., 1991).

Synthesis of the two roles
Antigravity control and interface between perception
and action are closely related to the execution of
movement. For example, when raising a leg laterally,
equilibrium is maintained by shifting the CG toward
the supporting leg (Mouchnino et al., 1992). This is a
form of antigravity control. During the same task, it
can be shown that the orientation of body segments
with respect to space, which serves as an interface
between perception and action, is also preserved. In
untrained subjects, the head axis remains vertical
throughout the movement, whereas the trunk is
inclined toward the supporting leg. In expert dancers,
however, the trunk axis also remains vertical.
Mouchnino et al. (1992, 1993) have shown that the
trunk axis serves as a reference frame for the
calculation of leg angle (egocentric reference frame).
While the trunk axis remains vertical throughout the
movements of an elite dancer, the calculation of leg
angle relative to the trunk (egocentric coordinates)
becomes equivalent to the calculation of leg angle
relative to the vertical gravity axis. The latter is the
reference axis for the external space coordinating
system. Thus, for the expert dancer, keeping the trunk
axis vertical throughout the task clearly simplifies the
calculation of leg position in space.
Central organization and control of posture
Each species has its own genetic patrimony, which
provides throughout fetal development, birth and
ontogeny a central and reflex organization support-
ing basic behaviors, which are critical for survival.
There is consensus that posture and locomotion are
examples of such basic, genetically determined behav-
iors. There has been much controversy these past
three decades, however, concerning the relative contri-
bution of genetic versus learned networks to the central
organization and control of posture (Prochazka
et al., 2000; Grillner and Wallén, Chapter 1).
Genetic model of posture
Three main functions are identified in the genetic
model of posture: the body segments’ orientation
with respect to gravity, their support against gravity
and the adaptation of posture to ongoing movement.
15
These three functions are closely related to the
primary ones of antigravity control and interface
between perception and action.
Body orientation with respect to gravity
In mammals, with a body which is segmented into
head, trunk and leg sections, the otoliths and vision
provide sensory input for controlling the head’s
orientation with respect to gravity. The investigations
on righting reflexes described by Rademaker (1931)
illustrate this claim. Note that a cat falling from an
upside-down initial posture first reorients the head
along the horizontal plane, then the body along the
head plane, and finally, the legs adopt a vertical
position that makes the animal ready for landing.
There are also a series of reflexes aimed at stabilizing
the segmental orientation with respect to gravity. For
example, Vestibulo-collic reflexes stabilize head
orientation in all manners of movements. Other
reflexes help orient the foot with respect to the support
(e.g., placing reactions) or the leg with respect to the
gravity axis (hopping reactions).
Antigravity function
There is need to support the body segments against
the contact forces exerted by gravity forces acting
upon individual segments and the body as a whole.
Postural muscle tone (i.e., the level of EMG activity
in antigravity muscles) is a key means of meeting this
need. It depends in large part on operation of the
myotatic (stretch reflex) loop, predominantly in
antigravity extensor muscles. Such muscle activity is
exaggerated in decerebrate animals, which exhibit the
well known, albeit mistermed, ‘decerebrate rigidity’
(i.e., it is really a form of spasticity). These postural
reactions, which occur in the presence of an external
perturbation of stance, are determined, in part, by
both genetic endowment and learning throughout
ontogeny (Forssberg, 1999).
Adaptation of the body’s segments to ongoing
movement
Genetic patrimony is also fundamentally concerned
with the coordination between posture and
16
movement. The distribution of tone throughout the
body’s musculature depends on the orientation of the
head in space and in relation to the trunk, as achieved
in part by labyrinthine and neck reflexes. Note also
the role of lumbar reflexes, which are concerned with
the orientation of the trunk with respect to the pelvis
(Tokizane et al., 1951). These latter reflexes adapt
tone in muscles supplying the upper and lower
segments to the ongoing movement.
In summary, the genetic model of posture proposes
that its purpose is to support the body against
gravity, preserve balance, orient the body with
respect to gravity and also adapt the body’s segments
to the ongoing movement.
Limitations of the genetic model
There are several challenges to the idea that the
genetic model of posture can be the sole basis for the
central organization and control of posture. Two key
issues concern the flexibility of postural reactions,
and anticipatory postural adjustments, of which the
latter ones are involved in the coordination between
posture and movement (see also F. Mori et al.,
S. Mori et al., and Takakusaki et al., Chapters 19, 33
and 23 of this volume).
Flexibility of postural reactions
Postural reactions induced by external disturbances
are now known to be remarkably flexible (for review,
Macpherson, 1991; Horak and Macpherson, 1996).
For example, when a balance disturbance occurs
while standing, the leg muscles are the main ones
involved in the correction. If the subject simulta-
neously grasps a support with the hands, however,
the postural reaction will mainly involve the arm
muscles (Nashner and McCollum, 1985). Thus, the
postural reactions to the same stimulus depend, in
terms of their spatial distribution, on external
constraints, such as the conditions of support. This
marked flexibility is, however, a feature of proprio-
ceptive reflex organization (Forssberg et al., 1975;
Stuart, 2002). Segmental reflexes are both task and
context dependent, and under a higher level of
control for selecting appropriate reflex actions (gate
and gain control).
Anticipatory postural adjustments
Analysis of the coordination between posture and
movement argues against a purely genetically based
reflex organization of posture. During the perfor-
mance of most voluntary movements, the primary
functions of posture must be preserved in order to
accomplish the goal in an accurate fashion. Preserving
equilibrium is a necessary condition for an accurate
performance and preserving the orientation of the
body’s segments with respect to gravity are essential
because they provide a reference value for planning the
trajectory of the movement toward its goal. In
addition, the supporting function of the kinematic
chain from the ground to the moving body segments
has to be preserved during the dynamic conditions of
movement execution.
The coordination between posture and movement
must accommodate a major problem. The perfor-
mance of a movement is a source of disturbance of
posture for two reasons. First, it changes the body’s
geometry and, as a consequence, the CG’s position
with respect to the support surface (often the ground).
Second, the movement is initiated by internal muscle
forces, which are associated with reaction forces
acting on the supporting segments and the ground.
The resulting dynamic interactions between body
segments must be accommodated. Otherwise, there
would be a deviation from the planned trajectory and
misreaching would occur. This is prevented by
anticipatory postural adjustments. These were first
described by Belenkiy et al. (1967) for an arm-raising
task and they have since been observed in a wide
variety of voluntary movements (for review, Massion,
1992; Horak and Macpherson, 1996; see also
Bouisset and Zattara, 1987). Figure 1 models how
anticipatory adjustments correct in advance for
perturbations of posture and equilibrium that are
associated with the execution of movement.
Anticipation involves prediction of a forthcoming
perturbation. It implies that due to the effect of
repeated experience and learning on adaptive central
neural networks, memorized models are developed in
the central nervous system (CNS) and used during the
performance of a task. Such models accommodate the
external world, the body’s biomechanical character-
istics and their interactions. This idea of a memorized
representation (or model) was first proposed for the

Fig. 1. Schematic representation of the integrated control of
posture and movement. Note the need for a postural control
system that integrates interactions between postural reactions
and anticipatory adjustments. The execution of a movement
provokes a perturbation of posture (internal perturbation),
which is compensated for by a postural reaction. This occurs
with a delay, however. It is comprised of the time for the
perturbation to be detected plus that for transmission through
the corrective pathway(s). In contrast, anticipatory postural
adjustments correct in advance for the forthcoming perturba-
tion. Adaptive neural networks, whose development requires
learning, control this anticipatory process.
whole somatic system by Bernstein on the basis of his
analysis of motor learning (for the evolution of his
ideas, see his posthumous 1967 volume). The idea was
further extended into the postural domain by Clément
et al. (1984), Gurfinkel et al. (1988) and Gurfinkel and
Levik (1991). It has also appeared in the area of
oculomotor control, where it was initially termed
‘internal models’ (see Robinson, 1986).
The genetic model of posture cannot account for
the important role of anticipation in helping achieve
an appropriate coordination between posture and
movement. The key reason is that such anticipation is
based on learning.
It thus appears that in addition to the genetic model
of posture, which nonetheless remains valid for many
basic postural controls, a higher level of postural
organization is present. It makes use of experience and
learning, and provides a finely tuned adaptation of
postural functions to the movement needs of daily life.
Hierarchical model of posture
The flexibility of postural reactions, and anticipa-
tory postural adjustments associated with voluntary
17
movements, are much better accounted for by a
hierarchical model of posture. This approach is
derived from an analogous model of movement
organization proposed initially by Bernstein. (The
evolution of this idea, too, is presented in
Bernstein’s 1967 volume.) It includes both inborn
genetically endowed reactions (Gurfinkel and Shik,
1973) and those built up by learning (Clément et al.,
1984; Gurfinkel et al., 1988; Gurfinkel and Levik,
1991). This model proposes that two types of CNS
processing are required for the control of posture.
A higher-order one accomplishes an internal repre-
sentation of body posture (the so called ‘body
schema’). In parallel, lower-order control brings
about the kinematics and force (kinetics), which are
required for implementing postural functions as a
necessary aspect of the task. In reality, this proposal
is not basically different from the body schema
model proposed by Head (1920) on neurological
grounds, or the concept of internal representations
(or models) required for the organization of
movements (Wise et al., 1991; Wolpert et al., 1995,
1998). For example, in an arm target-reaching task,
one may identify a set of control processes, which
depend on representational mechanisms, such as the
coding of target position in head and trunk
coordinates, the coding of hand position in trunk
coordinates and planning the desired trajectory. All
three processes require internal models. For the
execution of an arm-reach trajectory, both static
and dynamic models, and direct and inverse models,
are used for implementing the command in terms
of muscle force (Wise et al., 1991; Wolpert et al.,
1998).
Higher-order processing of body representation
Higher-order processing has been shown in experi-
ments that made use of artificial or biased sensory
inputs. These have included a visual-moving scene
(Dichgans et al., 1972; Lestienne et al., 1977),
galvanic stimulation of the labyrinth (Lund and
Broberg, 1983; Gurfinkel et al., 1988; Hlavacka et al.,
1995) and tendon vibration (the latter stimulus
activates largely muscle sensory Ia axons; Roll and
Roll, 1988; Roll et al., 1993, 1998). These studies
showed that the internal CNS representation of the
18
body’s posture (or body schema) includes at least
three components. First is body kinematics, i.e., the
kinematic chain from feet to head. These make use of
muscle proprioceptive Ia afferent input and/or an
efferent copy of the motor command. The latter
mainly concerns the position of the eyes in their
respective orbits (Roll et al., 1998). Second are the
body segments’ mass and inertia, which are derived
from sensory inputs not yet clearly identified. Finally,
there are the positions of the body’s individual
segments and their weight, both with respect to the
external world. The vertical axis related to the gravity
vector is assessed by sensory inputs from multiple
sources, including vestibular graviceptors, body
graviceptors (pelvis—Mittelstaedt, 1998; plantar
sole—Kavounoudias et al., 1998, 1999) and Golgi
tendon organ receptors in extensor muscles (Dietz
et al., 1989, 1992). In addition, visual input provides
information about the vertical axis (Dichgans et al.,
1972; Lestienne et al., 1977; Dijkstra et al., 1994).
Finally, haptic (tactile) contacts of the hands on
external supports, like a wall or a cane in contact
with the ground, serve to adjust the body’s posture
relative to the external support (Jeka and Lackner,
1995).
According to Mergner and Rosemeier (1998), the
representation of the body segments’ positions with
respect to space is accomplished in two ways. A top-
down one uses the head as a reference frame with
respect to space. The position of the various body
segments can then be calculated with respect to the
head. A bottom-up representation uses the basis
of support as a reference frame. This serves mainly
to calculate the CG position with respect to the
ground.
Evidence for this internal representation of the
proprioceptive kinematic chain is illustrated by
experiments which noted the effects of vibration of
the biceps’ tendon when a human subject was holding
the nose or skull with a hand (recall that biceps
vibration stimulates Ia biceps afferents, thereby
mimicking his muscle’s stretch during arm extension).
Surprisingly, the resulting illusory perception is an
elongation of either a finger or the skull (Lackner,
1988). This finding shows that Ia afferent input is
processed by the CNS in such manner as to provide
the most likely interpretation according to the
subject’s previous experience.
Lower-order implementation of posture
The higher-order component of the hierarchical
model of posture is rather stable even when the
constraints are drastically changed. This occurs, for
example, when the subject is subjected to micro-
gravity conditions (Gurfinkel et al., 1993a,b; Massion
et al., 1998). In contrast, the lower-order control of
implementation (kinematics and kinetics) is quite
flexible and adaptable to the constraints.
Experiments performed in microgravity have
illustrated this initially surprising claim (Vernazza-
Martin et al., 2000; Baroni et al., 2001). For example,
the performance of trunk bending in normogravity is
characterized by opposite movements of upper and
lower body segments. These minimize a shift of the
CM’s horizontal position with respect to the feet, and
thereby preserve equilibrium during the movement.
In a short-term exposure to microgravity, such as a
parabolic flight, the kinematics of axial movements
during trunk bending is preserved just as well as in
normogravity. Similarly, the close covariation
between ankle, knee and hip joint movements is
retained (Vernazza-Martin et al., 2000). Also, the
CM’s displacement during movement is minimized in
microgravity to the same extent as in normogravity
(Massion et al., 1997; Baroni et al., 2001). All these
findings suggest that in normogravity, a movement is
planned kinematically on the basis of the internal
representation of body kinematics (higher-order
processing). This representation is well preserved in
microgravity. In contrast, the EMG patterns of the
limbs’ musculature, which correspond to the imple-
mentation of kinematic synergies, are markedly
changed in microgravity. This shows that muscle
forces adapt to new constraints in order to maintain
an invariant kinematic synergy.
Summary on models of posture
Both the genetic and hierarchical models of posture
make use of several identical mechanisms for
achieving postural control. These include: (1) joint
stiffness, which restricts the body’s deviation from the
desired position while standing; (2) postural reac-
tions, synergies and strategies, which reduce the
effect of postural and balance disturbances; and

(3) anticipatory postural adjustments, which are
associated with movement performance in order to
preserve the body segments’ orientation and equili-
brium, and provide appropriate postural support for
an accurate movement performance. Despite these
similarities, the genetic model alone cannot explain
the flexibility of postural reactions and anticipatory
postural adjustments. The hierarchical model of
posture, with its higher-order processing of the body
schema and lower-order processing of implementa-
tion, is far more appropriate for accommodating the
experimental findings in the domain of posture and
posturo-kinetic coordination. It is not exclusive of
the genetic model, however, because it uses many
genetically prewired circuits for accomplishing
postural tasks.
Integrated CNS control of posture and movement
In daily life, postural control is most intimately
associated with the execution of movements (reaching
and grasping tasks, locomotion, etc.). As such, it is
one key aspect of the overall control of motor tasks,
which usually involve both postures and movements.
A major difficulty in postural control, especially in
humans, concerns the ‘multijoint kinematic chain’
from the feet to the head. It includes body segments
with quite different mass and inertia, which are linked
by muscles with their own idiosyncratic viscoelastic
characteristics. Their totality (for the whole body) is
responsible for the production of force and kine-
matics. For example, Eng et al. (1992) showed that
for an arm-reaching task, each single joint movement
involves dynamic interactions with the other seg-
ments of the kinematic chain, and this becomes a
source of postural disturbance. In the human, the
relatively high level of the CG’s position, and the
narrow support surface for the feet, are other sources
of instability, which further confound postural
control during the execution of movement.
It bears emphasis that the multijoint chain from
the feet to the head is not specific to posture.
Movement of segments of this chain accompanies all
manner of bodily movements during daily life, e.g.,
trunk bending forwards and backwards. As such, the
control of axial movement involves issues not
basically different from those for other multijoint
19
movements, such as arm-reaching ones. The unique
feature of posture in the execution of any movement
involves the need to control balance and/or the
body’s segmental orientation during the motor act.
Thus, two primary problems of postural control in a
given movement task require resolution. The first is
how to simplify control by reducing the number of
degrees of freedom (Bernstein, 1967). The second
problem is how to counteract the disturbing effects of
movement performance on posture in terms of body
segment orientation and equilibrium. It is interesting
to see how far the various hypotheses proposed for
movement control can accommodate the above two
requirements. Three such concepts are presented and
evaluated below, using the guidelines that (1) internal
representations of body kinematics and dynamics
provide a basis for planning movement trajectory
(internal ‘direct’ model), and (2) during the execution
of movement, dynamic interactions between seg-
ments perturb the movement’s trajectory and the
body’s equilibrium.
‘Referent posture’
An early 20th century concept in motor control was
that EMG patterns were sufficient to reveal the
characteristics of a CNS-operated central pattern
generator (Brown, 1911; see also Pearson’s present
Chapter 12). This concept was first put into question
by Wachholder (1928). He introduced the idea that
the neural pattern also depended on the biomecha-
nical characteristics of the segment to be moved.
These include inertia, weight and the dynamic
characteristics of the task, such as velocity.
Similarly, Weiss (1961) insisted on the fact that the
EMG pattern of individual muscles in a given goal-
oriented task varied from trial to trial without
changes in the characteristics of the overall perfor-
mance. He introduced the concept that the perfor-
mance resulted from the action of the whole system
involved in the task (for review, Paillard, 1960;
Wiesendanger, 1997; Sternad and Corcos, 2001). The
lamba model of motor control was proposed by
Feldman (for its history, see Feldman and Levin,
1995). This idea is in keeping with Bernstein’s (1967)
views on the need for a systemic approach. Feldman
has argued that EMG patterns are not directly
20
programmed by a central controller, rather, they
emerge from the interaction between the central
command and pattern-generating signals, reflex
signals and the biomechanical system’s components.
Furthermore, central control must also accommodate
the biomechanical system’s interactions with the
environment (see also Hasan and Enoka, 1985;
Latash, 1993).
The concept of a ‘referent posture’ (Feldman et al.,
1999) is related to Feldman’s lamba model. (The
equilibrium point hypothesis or alpha model, which
is based on other premises, also proposes that the
final posture is programmed by the CNS; see Bizzi
et al., 1992.) Feldman’s referent posture is based on
the idea that the CNS controls the joints’ positions by
adjusting the spring-like properties of the muscles.
These are determined, in part, by the muscles’
‘threshold’ for their own myotatic reflex. This spring-
like adjustment results in an equilibrium position of
the joints being reached, thereby defining a final
position of the limb. A movement results from a
change in the equilibrium position of the joints,
which also produces a new referent postural
configuration. The actual body configuration differs
from that of the referent one, however, due to the
action of external forces, such as gravity.
Feldman’s concept is attractive due to its relative
simplicity. A single control process results in
achieving both the movement trajectory and pre-
serving postural functions. There is thus a reduction
of the controlled degrees of freedom. The main
controversy about this concept concerns the control
of dynamic interactions between the body’s segments,
which disturb movement trajectory, posture and
equilibrium. For example, is muscle stiffness along
the kinematic chain able on its own to efficiently
minimize the disturbing effect on the joints’ move-
ments on the dynamic interactions between body
segments? This question is central to evaluation of
Feldman’s ideas (Gomi and Kawato, 1996, 1997).
Direct and inverse dynamics
Direct and inverse dynamic models of the control of
posture and movement are based on the assumption
that the CNS has used learning to create an internal
model of the dynamics of the motor system. The
direct dynamic model is used to assess on-line the
dynamic state of the body’s biomechanical system.
The inverse dynamic model represents the central
command which takes into account all of the
dynamic properties of the system required to perform
a given task. These concepts have been used by
several authors (Kawato et al., 1987; Atkeson, 1989;
Miall et al., 1993; Wolpert et al., 1995).
Gomi and Kawato (1996, 1997) claim that
Feldman’s equilibrium point model cannot account
for dynamical interactions between segments. Thus, it
fails to describe the accurate performance of a goal-
directed task. They have opined that a direct dynamic
model and/or an inverse dynamic control is more
likely, i.e., one which emphasizes that the CNS has
a control system for dynamic interactions between
body segments during the accurate performance of
a task. In keeping with Ito (1984), they have proposed
that the cerebellum plays a critical role in building
and storing the direct and/or inverse models
appropriate for each motor task (cf. Wolpert et al.,
1998).
In summary, direct and inverse dynamic models
account for both balance control and movement
performance by the use of a single central control
system.
Concept of dual, coordinated control
The above two concepts feature motor actions being
controlled as a whole, i.e., no specific separate control
processes for posture and movement. The third
concept in vogue is that two independent, yet
coordinated, control processes are used for the
execution of motor acts. One is for the prime
(focal) movement, and the other for the associated
postural movement (in terms of equilibrium pre-
servation and appropriate orientations of the body
segments). The suggestion that any movement
comprises these two components was first claimed
in the works of Hess (1943) and Belenkiy et al. (1967).
More recently, Cordo and Nashner (1982) proposed
that the same repertoire of synergies could be utilized
for both reactive and anticipatory postural adjust-
ments associated with a voluntary movement. They
demonstrated that the postural component often
started earlier than the prime one in order to

minimize the perturbation of equilibrium caused by
the expected prime movement component (Cordo
and Nashner, 1982). Bouisset and Zattara (1987)
have argued that these anticipatory postural adjust-
ments are preprogrammed and integral parts of the
central motor program for the movement in question.
This concept of a dual-coordinated control for
posture and movement has been questioned in several
studies. Some of them have involved an analysis of
trunk bending. In this task, the movement involves
motion of the upper trunk. Such motion imposes a
large dynamic perturbation between body segments
along the kinematic chain from the ground to the
head. The task requires a precise coordination
between movement and posture. The size of the
base of support is limited by the relatively small
length of the feet, and the CM is located at a
relatively large distance above the support. On the
other hand, decomposition of trunk bending into its
prime movement and postural components is not so
evident as in the case of an arm-reaching task. Trunk
bending is accompanied by opposite movements of
the lower segments (Babinski, 1899; Oddsson and
Thorstensson, 1986; Crenna et al., 1987; Pedotti et al.,
1989). The identification of a postural versus move-
ment component cannot be made on the basis of
movement kinematics. The motions of the various
joints along the kinematic chain (hip, knee, ankle) are
too highly synchronized. This suggests that a single
central control system is responsible for all of the
kinematics (Alexandrov et al., 1998). As a result, a
different approach becomes necessary, like the one
presented in the next section.
The eigenmovement approach
The main difficulty in the control of a multijoint
mechanical system, such as the human body, is the
dynamical interaction between its different segments.
The movement of any one segment influences the
movement of all the other segments of the kinematic
chain. As a result, the control of a given single
segment cannot be performed without simultaneous
control of the neighboring ones. For such multijoint
systems, however, a set of dynamically independent
multijoint movements (multijoint motion units) can
be described by using the eigenmovement approach.
21
The eigenmovements represent movements along the
eigenvectors of the motion equation. Each eigenvec-
tor defines a set of ratios between the relevant joint
angles and joint torques. The number of eigenvectors
is equal to the number of degrees of freedom in the
multijoint system. For example, for the three joints
primarily involved in a trunk-bending task (hip, knee,
ankle), there are three degrees of freedom. Three
eigenvectors define for each joint a given set of ratios
between the three joints’ angles and their correspond-
ing torques. An eigenmovement is a unique movement
in which the ratios between the changes in joint angle
are fixed and, simultaneously, the changes in joint
torque are fixed. Since in each eigenmovement, all
joint angular changes are synchronized, all angular
changes in each eigenmovement can be described by
the time course of a single eigenmovement’s ‘kine-
matic amplitude’. Similarly, all joint torques changes
can be described by the time course of a single
eigenmovement’s ‘dynamic amplitude’. The relation-
ship between kinematic and dynamic amplitudes of
an individual eigenmovement is described by the
simple motion equation of an inverted pendulum
with its individual inertia. Any given multijoint
movement can be represented as a superimposition of
the eigenmovements of the relevant joints. Due to the
eigenmovements’ dynamical independence from each
other, and due to the simplicity of their motion
equations, the eigenmovement approach is a standard
and useful method for the analysis of the dynamics
of any multijoint system, be it living or inanimate.
Recently, we applied this method to the investigation
of human trunk bending in the sagittal plane
(Alexandrov et al., 2001a,b). For this, a three-joint
(hip, knee, ankle) biomechanical model of the human
body was used.
The fixed ratios between joint angles and their
corresponding joint torques, and the inertia in each
eigenmovement, are determined by the structure of
the multijoint chain (from feet to head in the present
case) and by the inertia of its segments. Figure 2
represents the ratios between joint angles (stick
diagrams) and joint torques (sizes of circles) for each
eigenmovement of our three-joint human body
model, using standard anthropometric parameters
(Winter, 1990).
In Fig. 2, the eigenmovements are termed
according to their predominant joint. For our
22
Fig. 2. Application of the eigenmovement approach to a
human trunk-bending task. Kinematic (stick diagrams) and
kinetic (circles at joints) patterns of ankle (A-), knee (K-), and
hip (H-) eigenmovements during voluntary trunk bending. The
term, ‘eigenmovement’ is defined in the text. In each
eigenmovement, the sticks’ inclinations and the sizes of circles
correspond to the ratios between the changes in joint angles and
joint torques, respectively. The values at the bottom correspond
to the normalized ratios between the three eigenmovement’s
inertias (i.e., relative to a value of 1 for the K-eigenmovement).
trunk-bending task, ankle (A-) eigenmovement
involved ankle dorsiflexion combined with knee
extension and hip flexion. Hip (H-) eigenmovement
consisted of hip flexion combined with knee and
ankle extension. Finally, knee (K-) eigenmovement
was composed of knee and hip flexion, and ankle
dorsiflexion. The inertia of the A-eigenmovement was
five times greater than that of the H-eigenmovement.
In turn, the inertia of the H-eigenmovement was 20
times greater than that of the K-eigenmovement. In
our three-joint model, any arbitrary movement in the
sagittal plane could be represented, in terms of its
kinematics and kinetics, as a superimposition of these
three eigenmovements.
We found previously that the K-eigenmovement
(again, knee and hip flexion with ankle dorsiflexion)
during human forward upper trunk bending was
negligibly small (Alexandrov et al., 2001b). Therefore,
we could decompose the task into only two (H- and
A-) of our three eigenmovements. We found that the
H-eigenmovement (hip flexion with knee and ankle
extension) was responsible for the main part of the
movement kinematics (i.e., it described more than
95% of the total angular variance at the hip, knee
and ankle). Due to the ankle extension accompanying
hip flexion, the H-eigenmovement was the main
reason for a backward shift of the CM (to about
4.5 cm), which perturbed equilibrium. The A-eigen-
movement (ankle dorsiflexion with knee extension
and hip flexion) was responsible for only 5% of total
angular variance at the hip, knee and ankle. Its
contribution to the total CM displacement was
comparable to that of the H-eigenmovement, how-
ever. The changes in ankle angle produced a forward
CM shift of about 5 cm, which compensated for the
backward CM shift caused by the H-eigenmovement.
Therefore, the A-eigenmovement was concerned
mainly with equilibrium control during the task.
The above analysis suggests that in a trunk-
bending task, the CNS uses a dual-control process;
one for bending, per se (the H-eigenmovement), and
the other for equilibrium maintenance (the A-eigen-
movement). The arguments in favor of the idea that
the A- and H-eigenmovements are controlled in the
task as entire (involving all three joints) motion
units were developed previously (Alexandrov et al.,
2001a,b).
An important aspect of the control of H- and
A-eigenmovements during trunk bending is their
relative timing. Due to the large inertia of the
A-eigenmovement (five times greater than that of
H-eigenmovement), it must start earlier and last
longer than the H-eigenmovement. Our previous
modeling experiments on forward bending on an
extremely narrow support (Alexandrov et al., 2001a)
showed that when both eigenmovements started
simultaneously, the A-eigenmovement, which pro-
duces forward acceleration of the CM, could not
compensate for the backward CM movement
associated with the H-eigenmovement. As a result,
the body experienced a fall backward.
Fig. 3 shows that during our present trunk-
bending task, the A-eigenmovement actually started
70  20 ms earlier and lasted longer (for 820  200
ms) than did the H-eigenmovement (510  80 ms).
The initial forward CM acceleration in the A-eigen-
movement was presumably produced by activ-
ation of ankle dorsiflexors. This interpretation
clarifies the functional meaning of the early EMG
(activation) pattern of tibialis anterior, which is
usually observed in trunk-bending tasks (Oddsson
and Thorstensson, 1986; Crenna et al., 1987; Pedotti
et al., 1989).

Fig. 3. Calculated changes in the CG’s velocity for A- and
H-eigenmovements during voluntary forward trunk bending by
a human subject. Note that a positive (upward) velocity
corresponds to forward CG displacement, and vice versa. The
thin vertical lines show the onset and offset of the CG velocity
due to the H-eigenmovement. The vertical broken lines show the
onset and offset of the CG velocity due to the A-eigenmove-
ment (threshold effect at 5% of the maximal velocity). Note
that the onset of the CG velocity changes due to the A-
eigenmovement started earlier and ended later than did that due
to the H-eigenmovement. Note also that the velocity changes
because these two eigenmovements are in an opposite direction.
Abbreviation: CG, center of gravity. See text for further
information.
The results of our eigenmovement approach
suggest that the CNS needs an internal model of
the inertia of the mentioned multijoint motion units.
It can use this model to adapt the timing of its neural
control mechanisms to the task in question, i.e.,
movement performance (trunk bending in our
experiments) and equilibrium maintenance.
Summary on eigenmovements
We believe that the eigenmovements identified by our
analysis correspond not only to purely mathematical
formalisms, but also to real components of the CNS’s
control system. First, in each eigenmovement, joint
angles and joint torques change synchronously in all
three (hip, knee, ankle) joints. In our opinion, this is
the simplest scaling procedure to be controlled by the
CNS. Second, the two goal components of the task
(i.e., movement and appropriate postures) can be
explained by each one having its own single eigen-
movemment; the H-eigenmovement for the prime
movement of bending per se, and the A-eigenmove-
ment for postural control by forward acceleration of
23
the CM and minimizing its perturbation by the prime
mover (i.e., the H-eigenmovement). Third, recall the
experiments of Horak and Nashner (1986), in which
they studied postural reactions to an external
disturbance of the erect posture. They proposed
that two strategies, hip and ankle ones, are the main
mechanisms for restoring balance control in response
to sudden perturbations. They showed that an ankle
strategy (rotation of the whole body around the ankle
joint) was of much higher inertia than a hip strategy
(rotation of the trunk around the hip). They argued
that the two strategies were task dependent, with the
ankle strategy used to compensate for small and slow
perturbations, whereas the hip strategy accommo-
dated large and fast ones.
The ankle and hip strategies of Horak and
Nashner (1986) can be identified in our A- and H-
eigenmovements. For example, in the A-eigenmove-
ment (ankle dorsiflexion with knee extension and
hip flexion), the ankle dominates, just as it does in
their ankle strategy. Similarly, the kinematic
pattern of H-eigenmovement (hip flexion with knee
and ankle extension) is close to that of their hip
strategy (see also Kuo and Zajac, 1993). Note further
that the high inertial A-eigenmovement (again like
the ankle strategy in the experiments of Horak and
Nashner) is efficient in slow CM displacements,
whereas the five times less inertial H-eigenmovement
(as in their hip strategy) is efficient when the
perturbation is fast.
In summary, our biomechanical analysis of human
trunk bending suggests that hip and ankle strate-
gies (best quantified as H- and A-eigenmovements)
represent elementary multijoint motion units of the
biomechanical system. They can be independently
controlled by the CNS to achieve different behavioral
goals within the same task (trunk bending using
H-eigenmovement control, and equilibrium main-
tenance using A-eigenmovement control). They act
conjointly to prevent a potentially forthcoming
disturbance of posture and equilibrium provoked by
the movement performance. The same motion units
are also presumed by us to operate either separately
or in conjunction with other tasks, e.g., when
initiating gait or rising on tiptoe (Crenna and Frigo,
1991); or, during low or high amplitude body
oscillations during fixating on an oscillating visual
target (Bardy et al., 1999).
24
How these two motion units are controlled by the
CNS, including their relative timing, is still an open
question. Is an internal model of the biomechanical
characteristics (mass, inertia) of each of these
multijoint motion units stored at the cerebellar
level? This would be in keeping with the direct or
inverse dynamic model of Gomi and Kawato (1996),
Gomi and Kawato (1997) and Wolpert et al. (1998).
Is the control of these multijoint motion units
compatible with the equilibrium point hypothesis
and, more specifically, with the concept of referent
posture as proposed by Feldman and Levin (1995)
and Feldman et al. (1999)? The answering of these
questions remains open in the absence of special
analytical techniques, like those of Domen et al.
(1999), or a model of the neuromuscular apparatus
similar to those developed for the human arm
(Flanagan et al., 1993; Gribble et al., 1998; Frolov
et al., 2000).
Summary and conclusions
The coordination between posture and movement
results from two parallel controls. They operate on
multijoint motion units (eigenmovements) of the
overall biomechanical system responsible for both the
movement and its associated postural adjustment(s).
An example is ankle and hip eigenmovements during
voluntary forward bending of the trunk. In this
case, a critical aspect for the coordination of the two
eigenmovements is their timing, which is a function
of their respective inertias. It is suggested that this
type of control might be a general rule for co-
ordinating posture and movement. It is likely that the
cerebellum plays a critical role in this coordination,
particularly in terms of the timing of eigen-
movements. Recall, for example, that it has long
been known that the coordination between move-
ment and posture is impaired in cerebellar patients
(Babinski, 1899).
Acknowledgments
We thank Dr. Becky Farley, The University of
Arizona, for her very effective help in reviewing an
early draft of this chapter. The work was supported
by the Russian Foundation For Basic Research
(projects 02-04-48410a and 01-04-48924a) and the
Russian Foundation of Humanity (project 00-06-
00242a).
Abbreviations
A ankle
CM center of mass
CNS central nervous system
CG center of gravity
H hip
K knee
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