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Somatosensory and Motor Research, 2012, 1–13, Early Online

ORIGINAL ARTICLE

Biomechanical and neurophysiological mechanisms related to postural


control and efficiency of movement: A review

ANDREIA S. P. SOUSA1,2, AUGUSTA SILVA1, & JOÃO MANUEL R. S. TAVARES3


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1
Escola Superior da Tecnologia de Saúde do Instituto Politécnico do Porto, Área Cientı́fica de Fisioterapia, Centro de
Estudos de Movimento e Actividade Humana, Vila Nova de Gaia, Portugal, 2Faculdade de Engenharia, Universidade
do Porto, Porto, Portugal, and 3Instituto de Engenharia Mecânica e Gestão Industrial, Departamento de Engenharia
Mecânica, Faculdade de Engenharia, Universidade do Porto, Porto, Portugal

(Received 27 July 2012; accepted 15 August 2012)

Abstract
Understanding postural control requires considering various mechanisms underlying a person’s ability to stand, to walk, and
to interact with the environment safely and efficiently. The purpose of this paper is to summarize the functional relation
between biomechanical and neurophysiological perspectives related to postural control in both standing and walking based
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on movement efficiency. Evidence related to the biomechanical and neurophysiological mechanisms is explored as well as
the role of proprioceptive input on postural and movement control.

Keywords: Postural stability, proprioceptive input, compensatory postural adjustments, standing, walking, gait

Introduction maintain a steady, erect stance; remodeling of stance


in preparation for a voluntary movement; shaping of
Postural control has been defined as the control of
the body for display purposes, as in dance; mainte-
the body’s position in space for the purposes of
nance of balance, as on the gymnast’s beam; or
balance and orientation (Massion 1998; Shumway-
conservation of energy in a demanding task (Kandel
Cook and Woolacott 2000, 2007; Horak 2006).
et al. 2000; Shumway-Cook and Woolacott 2007).
Postural orientation involves the active control of Biomechanically, a postural control position is
body alignment and tonus in relation to gravity, base achieved when the CoM is within the base of support
of support, environment, and internal references and is aligned with the center of pressure (CoP)
(Winter et al. 1990; Massion 1998; Kandel et al. (Winter 1995). Any external or internal perturbation
2000; Lundy-Ekman 2002; Horak 2006; Raine et al. that changes the projection of the CoM to the limits
2009). Postural equilibrium involves the coordina- of the base of support, and the alignment between
tion of sensorimotor strategies to stabilize the body’s CoM and CoP, may lead to postural challenge. The
center of mass (CoM) during both self-initiated and ability to maintain the body’s CoM within a specific
externally triggered disturbances in postural stability boundary is dictated by the efficiency of the individ-
(Horak 2006). Postural stability has been defined as ual’s balance mechanisms (Raine et al. 2009) related
the ability to control the CoM in relation to the base to anticipatory postural adjustments (APA), trig-
of support (Shumway-Cook and Woolacott 2000, gered by feedforward mechanisms prior to the
2007). The weight of each component, that is, of perturbation (Belen’kii et al. 1967; Massion 1992;
orientation and stability, varies according to the task Aruin and Latash 1995; Schepens and Drew 2004;
and the environment. Indeed, the postural control Li and Aruin 2007), as well as to compensatory
system adjusts its goal under different circumstances, postural adjustments (CPA) that are initiated by
such as longitudinal alignment of the whole body to sensory feedback signals (Park et al. 2004;

Correspondence: J. M. R. S. Tavares, Instituto de Engenharia Mecânica e Gestão Industrial, Departamento de Engenharia Mecânica, Faculdade de
Engenharia, Universidade do Porto, Rua Dr Roberto Frias, s/n, 4200-465 Porto, Portugal. E-mail: tavares@fe.up.pt
ISSN 0899–0220 print/ISSN 1369–1651 online ß 2012 Informa Healthcare Ltd.
DOI: 10.3109/08990220.2012.725680
2 A. S. P. Sousa et al.

Alexandrov et al. 2005). The process of generation of 1996; Mazzaro et al. 2005; Segers 2006;
APA is likely to be affected by expected magnitude Arechavaleta et al. 2008). The CPG designs spinal
(Aruin and Latash 1996; Bouisset et al. 2000) and networks that can generate patterns of rhythmic
direction (Aruin and Almeida 1997; Santos and activity in the absence of external feedback or
Aruin 2008) of the perturbation, voluntary action supraspinal control. However, these spinal networks
associated with the perturbation (Arruin 2003; are modulated by peripheral input and supraspinal
Shiratori and Aruin 2007), postural task and body control (Armstrong 1986; Rossignol et al. 2006).
configuration (van der Fits et al. 1998; Arruin 2003). The present study aims to review the biomechan-
In conditions of high instability demands, the central ical and neurophysiological mechanisms related to
nervous system (CNS) may suppress APA as a postural control in both standing and walking based
protection against their possible destabilizing effects on movement efficiency. In the following sections,
(Arruin et al. 1998). In fact, a relation between APA
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the neural mechanisms, the role of afferent informa-


and CPA has been demonstrated (Santos et al. tion, and biomechanical aspects will be considered to
2009), suggesting the existence of an optimal utili- upright standing and human gait.
zation of APA in postural control. The CPA response
depends not only on the APA, but also on the
direction and magnitude of the perturbation, the Postural and movement control
base of support dimension (Horak and Nashner Neural mechanisms
1986; Henry et al. 1998; Dimitrova et al. 2004; Jones
et al. 2008), and on the involvement in a secondary Upright standing. The upright stance of the human
task (Bateni et al. 2004). is an unstable position (Peterka and Loughlin 2004).
The main sensory systems involved in postural Postural sway reflects noise and regulatory activity of
control are proprioception, the vestibular system and the several control loops involved in maintenance of
vision, and their afferent pathways within the CNS balance, which requires that the CoM never deviates
(Day and Cole 2002; Shumway-Cook and Woolacott beyond the support area. The control of the appro-
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2007). Afferent and efferent pathways involve the priate level of neuromuscular activity to produce
spinal cord, the brain stem, the cerebellum, the rapid postural control strategies involves medial
midbrain, and the sensorimotor cortex. All of these descending systems (Raine et al. 2009). The role of
contribute to the development of an internal repre- these systems is fundamental to the organization of
sentation of body posture that is continuously postural tone appropriately according to environ-
updated based on multisensory feedback and is ment demands, gravity, and base of support. The
used to forward commands to control body position vestibular system action is related to postural tone
in space (Massion 1994; Mergner and Rosemeier adjustments to body weight support (Matsuyama and
1998). This provides a basis for all interactions Drew 2000). This system plays a major role in the
involving perception and action with respect to the antigravity function (Latash 1998; Siegel and Sapru
external world and is likely to be partly genetically 2011) as it is responsible, through the lateral
determined and partially acquired through ongoing vestibulospinal tract, for the activation of ipsilateral
experiential learning. It is therefore, adaptable and extensor motor neurons and their associated gamma
vulnerable, is dependent on the ongoing information motor neurons (Rothwell 1994; Latash 1998; Siegel
that it receives (Meadows and Williams 2009), and is and Sapru 2011). The reticular formation has an
related to human movement variability, allowing for important role on APA production (Schepens and
adjustable functional behavior (Van Emmerik and Drew 2004) as it receives afferent input from all the
Van Wegen 2000). sensory systems and also from the pre-motor cortex
The neural process involved in stability organiza- and supplementary motor area (Brodal 1981;
tion and body orientation in space is necessary Rothwell 1994; Kiernan 2005). The possible role of
practically for all dynamic motor actions (Massion the cortex in postural control has been discussed and
1998). Specifically, the control of balance during gait relevance has been given to the role of pre-motor
and while changing from one posture to another cortex (Massion 1992) and supplementary motor
requires a complex control of a moving body CoM area in the control of APA production (Jacobs et al.
that is not within the base of foot support (Winter 2009).
et al. 1993). In fact, human gait is influenced by a
multifactorial interaction that results from neural and
mechanical organization, including musculoskeletal Human gait. Appropriate mechanisms for control-
dynamics, a central pattern generator (CPG), based ling muscle tone are essential to maintain stable
on a genetically determined spinal circuit, and postural and locomotor synergies in bipedal gait
peripheral and supraspinal inputs (McCollum et al. performance. The dependency between postural
1995; Borghese et al. 1996; Horak and Macpherson control and movement may be justified by the
Postural control and efficiency of movement 3

connection between the cortex and the reticular motor learning (Wichmann and DeLong 1996;
formation. Actually, muscle tone and the locomotor Mackay-Lyons 2002). The midbrain locomotor
system can be controlled, in parallel, by a combined region activates the ‘‘muscle tone excitatory system’’
input to the brain stem of net inhibition from the and ‘‘rhythm generating system’’ (Takakusaki et al.
basal ganglia and net excitation from the motor 2004). Although not being relevant in gait, the motor
cortex (Takakusaki et al. 2004). Specifically, an cortex is involved in the modification of CPG activity
important neuronal circuit that allows the coexis- in unstable surfaces or when gait needs a visual
tence of postural adjustments and execution of orientation. The degree of supraspinal and spinal
movement is the cortico-ponto-cerebellar pathway, influences in movement generation is determined by
which allows the connection of the cortex with the context (Mackay-Lyons 2002). The main structures
nucleus of the brain stem and cerebellum (Ito 2006). involved in postural control in both standing and
With this circuit, the postural control can be orga- walking are represented in Figure 1.
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nized ipsilaterally to the activated side with respect to


the control of movement in the contralateral side.
The role of afferent information
This relationship between movement and postural
control through the activation of ventro-medial and Upright standing. The ability to reweight sensory
dorso-lateral systems, as well as the importance of information depending on the context is important to
the coactivation mechanism between the two lower maintain stability when a person moves from one
limbs (Dietz et al. 2002) to keep the body CoM over context to another (Peterka 2002). For instance,
the feet (Dietz et al. 1989, 1992), justify the study of while vestibular information may not be a large
mechanisms that occur in both sides of the body in contributor for the control of upright stance (Winter
relation to a unilateral movement like gait initiation et al. 1998) and for triggering or coordinating muscle
as well as in relation to the gait cycle. activation patterns associated with ankle strategy
Basic structures involved in the control of locomo- (Horak et al. 1990), it is likely to play a crucial role
tion and postural muscle tone are located in the during moments of increased postural instability
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midbrain (Takakusaki et al. 2004). Some circum- (Fitzpatrick et al. 1994). As in normal conditions,
scribed regions have been identified as relevant in proprioceptive information assumes more relevance
activating and controlling the intensity of spinal than other sources; in this paper focus has been given
locomotor CPG operation, maintaining equilibrium to the role of proprioceptive information, Figure 2.
during locomotion, adapting limb movement to It is well known that the mechanoreceptors (i.e.,
external conditions, and coordinating locomotion to specialized sensorial receptors responsible for trans-
other motor acts (Armstrong 1986; Jordan 1986; duction of mechanic events into neural signs (Grigg
Orlovsky 1991). Among the main supraspinal centers 1994)) accounting for proprioceptive information are
involved are the sensorimotor cortex and the supple- primarily founded on muscles, tendons, ligaments,
mentary motor area (Mackay-Lyons 2002; Miyai et al. and capsule (Johansson et al. 1991; Jami 1992;
2002; Kapreli et al. 2006), the cerebellum, the basal Hogersvorst and Brand 1998). Receptors located in
ganglia (Garcia-Rill 1986; Mackay-Lyons 2002), the the deeper skin tissue and fascia are traditionally
midbrain locomotor region (Kandel et al. 2000; associated with touch receptors, being categorized as
Mileykovskiy et al. 2000), and the spinal cord (Dietz additional sources (Macefield et al. 1990; Grigg
et al. 1992). The sensorimotor cortex is involved in 1994; Edin and Johansson 1995). Support has been
the preparation for and execution of movement given to the role of the Golgi tendon organs in
(Nelson 1996). The cerebellum receives copies of providing afferent input from ‘‘gravity-dependent’’
CPG output to motoneurons via ventral spinocer- receptors required to indicate the projection of the
ebellar tract and spinoreticularcerebellar pathways, as body’s CoM within the base of support (Dietz et al.
well as information about the activity of the peripheral 1992; Dietz 1996, 1998; Dietz and Colombo 1996).
motor apparatus via the dorsal spinocerebellar tract In addition, the small magnitudes of sway observed
(Orlovsky 1991). Based on these, they influence during quiet standing may be enough to alter muscle
motoneurons indirectly via vestibulospinal, rubrosp- lengths, resulting in changes of Ia afferent input onto
inal, reticulospinal, and corticospinal pathways the motoneuron pool of the lower limbs. Recent
(Orlovsky 1991). The cerebellum’s main role may studies by Loram et al. (2005b) have suggested this
be the timing of muscle activation, ‘‘fine-tuning’’ the possibility, whereby muscle length changes in the
output by adapting each step (Lansner and Ekeberg gastrocnemius and soleus muscles during quiet
1994). Nevertheless, both the cerebellum and the standing have been detected within the range at
basal ganglia seem to play an important role in timing which muscle spindles are sensitive to movement
of sequential muscle activation, with the basal ganglia (Proske et al. 2000). Support has been given to the
operating at the level of planning, initiation, execu- role of medium latency responses from group II
tion, and termination of motor programs as well as during standing (Schieppati et al. 1995; Corna et al.
4 A. S. P. Sousa et al.
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Figure 1. A conceptual schematic diagram illustrating the main structures involved in postural control in both standing and
walking.
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1996; Nardone et al. 1996). Indeed, there is evidence been considered the source of muscle proprioceptive
that muscle spindle type II fibers play a more relevant information signaling changes in body position
role than group Ia fibers in the control of bipedal (Fitzpatrick et al. 1992b; Loram and Lakie 2002a;
stance (Marchand-Pauvert et al. 2005) as only Loram et al. 2005b). These muscles act predomi-
medium latency responses have a stabilizing effect nantly as active agonists and, because the foot is
during perturbations of stance, and also because constrained on the ground, they prevent forward
these fibers are more influenced by the ‘‘postural set’’ toppling of the body, whose center of gravity is
(Nardone et al. 1990). Findings obtained by maintained in front of the ankle joint (Fitzpatrick
Nardone et al. (1996), demonstrate the existence of et al. 1992a; Maki and Ostrovski 1993; Loram and
crossed neural pathways fed by these fibers, which Lakie 2002a; Lakie et al. 2003; Loram et al. 2005a).
explains the bilateral electromyographic responses to The problem with muscle spindles as position
unilateral perturbations during standing. This find- sensors is that they are able to generate impulses in
ing is supported by Dietz (1996), as this author response to muscle length changes as well as from
argues that a complex bilateral coordination of leg fusimotor activity (Proske 2006). According to Di
muscle activation (mediated by a spinal mechanism Giulio et al. (2009), the best proprioceptive infor-
(Dietz and Berger 1984)) is needed for upright mation may come from un-modulated muscles
postural control during locomotion. crossing the joint in parallel with the active agonist.
All the receptors mentioned above, and the corre- In fact, earlier studies stated that, depending upon
sponding afferent input, may allow a modulation of the stance conditions, muscle stretch does not
postural activity in relation to muscle length and necessarily result in a compensatory stretch reflex
tension variation, but only a combination of afferent response but instead results in an antagonistic
inputs can provide the necessary information to muscle activation (Hansen et al. 1988; Gollhofer
control body equilibrium (Dietz 1996). The role of et al. 1989). Based on this, it has been argued that
proprioceptive information from ankle muscles has reciprocal patterns of muscle activation are typically
been highlighted in various studies (Fitzpatrick et al. involved in postural control (Latash 1993; Di Giulio
1992a, 1994; Gatev et al. 1999; Loram et al. 2005a). et al. 2009). Neurophysiologically, reciprocal inhibi-
Some authors go further, arguing that normal sub- tion is mediated, at least in part, by a dysinaptic
jects can stand in a stable manner when receptors of circuit in the spinal cord that is subject to several
the ankle muscles are the only source of information supraspinal as well as segmental modulator mecha-
about postural sway (Fitzpatrick et al. 1992a, 1994). nisms (Jankowska 1992) and varies according to the
The soleus and the gastrocnemius have traditionally way in which antagonist muscles are activated
Postural control and efficiency of movement 5
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Figure 2. Representation of the most important proprioceptive receptors and afferences and their role in standing and stance
phase of gait (a). There are also represented important networks related to proprioceptive information (b). Dotted lines in (b)
represent efferent pathways and solid lines represent afferent pathways.

(Lavoie et al. 1997). Synergies between antagonist detail in the temporal pattern of the muscle activation
muscles include simple patterns of reciprocal activa- sequence (Pearson 1993; Ivanenko et al. 2006), (2)
tion, co-contractions, and complex triphasic activa- the reinforcement of ongoing motor activity, parti-
tion patterns (Lavoie et al. 1997). There is evidence cularly that involving load-bearing muscles, such as
that the strength of dysinaptic inhibition is reduced the extensor muscles during the stance phase of gait
during co-contraction of antagonist muscles com- (Pearson 1993; Stephens and Yang 1996; Sinkjær
pared with reciprocal activation (Nielsen and et al. 2000), and (3) the control of transition from
Kagamihara 1992). Another source of proprioceptive one phase of movement to another (Pearson 1993;
information may come from the cutaneous afferents Lacquaniti et al. 1999). Swing is initiated when the
of the feet as there is a large distribution of cutaneous leg is extended (stretching the flexor muscles) and
receptors at various locations on the sole of the foot unloaded (reduced force in extensor muscles sensed
(Kennedy and Inglis 2002). It has been suggested by the Golgi tendon organ of the extensor muscles)
that this source of proprioceptive information con- (Zehr and Duysens 2004). Consequently, gait cycles
tributes to both the coding and spatial representation depend on the afferent input from peripheral recep-
of body posture during standing (Roll et al. 2002), tors as the muscle force production at a given level of
and that the architecture and physiology of the foot motor unit recruitment can change according to
appear to contribute to the task of bipedal postural length (velocity) and tension variations (Frigo et al.
control with great sensitivity (Wright et al. 2012). 1996).
The monosynaptic excitation of spinal motoneu-
rons from the large diameter group Ia afferent fibers
Human gait. During gait, afferent feedback adapts related to a short latency response (Matthews 1991)
dynamically, through a reciprocal relationship, the has been demonstrated when an expected stretch of
response of the CPG to environmental requirements the ankle extensors is imposed during gait (Yang
and assumes multiple roles in regulating the produc- et al. 1991; Sinkjaer et al. 1996). In addition, a phasic
tion of motor patterns, such as: (1) the production of modulation of Ia input has also been demonstrated
6 A. S. P. Sousa et al.

by changes in the magnitude of H-reflex over the the body, causing it to accelerate further away from
course of the gait cycle, with the greatest attenuation the upright position. Corrective torque must be
occurring during flexion (Yang and Whelan 1993; generated to counter the destabilizing torque due to
Schneider et al. 2000). This modulation is consistent gravity. This process of continuous small body
with the fact that the maximum soleus length occurs deviations countered by corrective torques creates a
during the foot off, when maximum plantar flexion of pattern known as spontaneous sway. The mecha-
the foot occurs, which is coincident with its maxi- nisms underlying spontaneous sway are not fully
mum force production (Orendurff et al. 2005). The understood, and controversy remains regarding the
modulation of the H-reflex is a reflection of: (1) the organization of sensory and motor systems contrib-
background excitability of the motoneuron pool, (2) uting to the spontaneous sway. Numerous authors
the modulation associated with the activation of the have suggested that active feedback control mecha-
antagonist muscle, and (3) presynaptic inhibition of nisms contribute to the maintenance of upright
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the primary afferents (Yang and Whelan 1993) that stance (Johanson and Magnusson 1991; Peterka
seems to be related partially to Ia afferents from the and Benolken 1995; Fitzpatrick et al. 1996; van der
hip and knee extensor muscles (Brooke et al. 1997). Kooij et al. 2001; Peterka and Loughlin 2004).
Medium latency response from group II has been Recent studies have shown that a model based
demonstrated during gait (Dietz et al. 1985) and primarily on a feedback mechanism with 150–
some authors argue that this group is more important 200 ms of delay can account for postural control
to feedback in the stance phase than group Ia during a broad variety of perturbations (Peterka and
(Sinkjær et al. 2000; Grey et al. 2001, 2002; Benolken 1995; Peterka 2002; Peterka and Loughlin
Nielsen and Sinkjaer 2002). Earlier studies have 2004) and can yield a spontaneous sway pattern that
suggested that strong central effects of group II resembles normal (Peterka 2000) or pathological
muscle afferents are mediated via a complex neural spontaneous sway (Parkinson’s disease (Maurer et al.
pathway influenced by supraspinal input and periph- 2003)). However, the relevance of feedback mecha-
eral input during walking (Dietz et al. 1987; Yang nisms for postural control is still debated. Some
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et al. 1991). Specifically, there is evidence for the role authors concluded from their experiments that cor-
of vestibulo- and reticulospinal pathways (Davies and rective torque originating from feedback control is
Edgley 1994) that supports the hypothesis that the insufficient for stabilizing the body (Fitzpatrick et al.
facilitation of the relevant lumbar propriospinal 1996). Others suggested additional sources for cor-
neurons by descending tract neurons would be rective torque, like prediction (Morasso et al. 1999;
stronger over group II during maintenance of posture van der Kooij et al. 2001), or have proposed more
than during voluntary contractions (Marchand- complex concepts (Collins and De Luca 1993;
Pauvert et al. 2005). In addition, the role of group Baratto et al. 2002; Loram and Lakie 2002b).
Ib load-sensitive afferences related to a medium Postural sway has been viewed as a result of a
latency response has been reported to contribute to correlated random-walk process (Collins and De
the regulation stance phase of gait (Stephens and Luca 1993), a result of computational noise (Kiemel
Yang 1999) associated with a disynaptic Ib reflex et al. 2002), and/or a moving reference point
reversal (Stephens and Yang 1996). Findings (Zatsiorsky and Duarte 1999). The possible impor-
reported in Grey et al. (2007) suggest that tendon tance of the postural sway as a reflection of a
organ feedback via an excitatory group Ib pathway hypothetical search process within the system of
contributes to the late stance phase enhancement of postural stabilization has been emphasized (Riley
the soleus muscle activity. The combination of the et al. 1997; Mochizuki et al. 2006).
different afferent inputs plays an important role on From a functional point of view, the control of
gait dynamics related to the ipsilateral limb but also human upright posture stability is commonly viewed
on the contralateral limb, as it has been demon- as a continuous stabilization process of a multilink
strated that unilateral leg displacement during gait inverted pendulum, where the main controlled
evokes a bilateral response pattern, with a similar parameter is the CoM position within the limits of
onset on both sides (Dietz and Berger 1984). From a the supporting base (Maurer and Peterka 2005).
functional point of view, this interlimb coordination This aspect has been described as biomechanical
is necessary to keep the body’s CoM over the feet constraints that determine patterns of postural coor-
(Dietz 1996). dination (Buchanan and Horak 2003). In stance, the
limits of stability, that is, the area over which
individuals can move their CoM and maintain
Biomechanical aspects
equilibrium without changing the base of support,
Upright standing. Upright stance is associated with is shaped like a cone (McCollum and Leen 1989).
small deviations from an upright body position, Thus, equilibrium is not a particular position but a
which results in a gravity-induced torque acting on space determined by the size of the support base and
Postural control and efficiency of movement 7

the limitations on joint range, muscle strength, and activity, muscle torque, ground reaction forces,
sensory information available to detect limits. The kinematics, and metabolic energy costs have been
CNS has an internal representation of this cone of assessed and quantified. This data set requires an
stability that it uses to determine how to move to interpretation and organization of the fundamental
maintain equilibrium (Horak 2006). Gatev et al. principles that elucidate the mechanisms of gait.
(1999) reported a signiEcant correlation between Several models have been suggested to describe
spontaneous body sway and the activity of the human gait mechanisms (Saunders et al. 1953;
gastrocnemius muscle. They also found that gastroc- Cavagna and Margaria 1966; Cavagna and Kaneko
nemius activity preceded temporally CoM displace- 1977; Waters and Mulroy 1999; Donelan et al.
ment, suggesting a central program of control of the 2002b; Kuo et al. 2005, 2007). The six determinants
ankle joint stiffness working to predict the loading of gait theory (Saunders et al. 1953), based on the
pattern. More recent studies proposed that the actual premise that vertical and horizontal CoM displace-
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postural control system during quiet standing adopts ments are energetically costly, propose a set of
a control strategy that relies notably on velocity kinematic features that help to reduce CoM dis-
information of CoM and that such a controller can placement. However, there is evidence that some
modulate muscle activity in an anticipatory manner determinants have a non-significant role on the CoM
without using feedforward mechanisms (Masani vertical displacement and that there is higher meta-
et al. 2003). According to this view, velocity feedback bolic expenditure when subjects voluntary reduce
can play a signiEcant role in anticipating body vertical displacement of CoM (for review, see Kuo
position changes because it carries information et al. 2007). The inverted pendulum model proposes
about the subsequent state of the body, that is, a that most of the work during gait is performed by a
change in CoM velocity indicates the direction and passive mechanism of exchange of gravitational
intensity with which the current CoM displacement potential and kinetic energies (60–70%) (Cavagna
will be changed in the following time instant. It has et al. 1977; Griffin et al. 2003). However, this model
been hypothesized that the integration of proprio- cannot reproduce the existence of two peaks in the
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ceptive and plantar cutaneous sensations would play vertical ground reaction force (Pandy 2003; Zajac
a signiEcant role in the velocity feedback mechanism et al. 2003) and does not account for the costs which
(Masani et al. 2003). Another biomechanical con- are not considered responsible for work, like isomet-
straint is related to frequency of postural sway ric force stabilization and body weight support (Kuo
(Nashner et al. 1989), as when postural sway is et al. 2005). The difference in the percentage of
lower than 0.5 Hz, the body can be compared to a energy recovery in relation to an ideal inverted
simple inverted pendulum (McCollum and Leen pendulum has been related mostly to the double
1989), and when it is higher than this value, the body support phase (McGeer 1990). Indeed, a low
can be compared to a double inverted pendulum percentage of energy recovery has been demon-
with the fulcrum at the hip level (Yang et al. 1990). strated in the double support phase (Geyer et al.
2006) related to the interruption of the energy-
conserving motion of single support by an inelastic
Human gait. The coordination between posture collision of the swing leg with the ground, leading to
and movement involves the dynamic control of the changes in velocities of the legs and the CoM (Kuo
CoM in the base of support (Stapley et al. 1999). et al. 2007). This energy loss can be reduced by 75%
Consequently, to access the simplified concept of through the application of a propulsion impulse in
locomotion it is necessary to consider the behavior of the trailing leg immediately before collision of the
the CoM during gait cycles. The trajectory described leading leg (Kuo 2002). Simulations suggest that
by the CoM in the plan of progression is a sinusoidal the ankle plantar flexor (soleus, gastrocnemius) and
curve that moves vertically twice during one cycle the uni- and biarticular hip extensors (gluteus max-
and laterally in the horizontal plan, and that is similar imus, hamstrings) dominate work output over the
in form to that found in the vertical displacement gait cycle (Neptune et al. 2004). These muscles,
(Norkin and Levangie 1992; Gard et al. 2004). Peak- being active in the late stance and in the beginning of
to-peak amplitude is described as being about stance, are therefore restoring energy to the body
4–5 cm for adults at freely chosen speed and has near double support (Zajac et al. 2003).
been used to estimate exchanges of mechanical Ankle plantar flexors are the primary contributors
energy, efficiency, work, and to describe the sym- for forward progression and vertical support (Kepple
metry as an indicator of the quality of gait (for more et al. 1997), before midstance, they hinder progres-
information, see Gard et al. 2004). sion (Neptune et al. 2001) and during midstance,
The human gait results from a complex interaction they maintain body support and the forward motion
of muscle forces, joint movements, and neural of the trunk and leg, which is consistent with
commands. Variables, including electromyographic inverted-pendulum-like ballistic walking as the
8 A. S. P. Sousa et al.

synergy of these muscles in this subphase occurs with can store and recover energy in the passive elastic
minimal metabolic energy expenditure, as expected tissues in the tendon and muscles. However, this last
in ballistic-like walking (Zajac et al. 2003). energy-conserving mechanism is quite small in
Biarticular hip extensors generate forward accelera- walking (Winter and Eng 1995). The CNS has
tion during the first half of stance, while uniarticular learnt how to create motor patterns to conserve
quadriceps muscles and the uniarticular hip exten- much of the energy that was generated earlier in the
sors decelerate the body mass center and provide gait cycle. It has been estimated that of the total
body support (Neptune et al. 2004; Liu et al. 2006). energy changes of all body segments over the gait
The biarticular quadriceps muscle is a significant cycle only 33% are caused by active muscle gener-
contributor to forward progression in late stance ation and absorption, while 67% are due to the
(Neptune et al. 2004). passive transfers between segments (Pierrynowski
According to Donelan et al. (2004), lateral stabi-
Somatosens Mot Res Downloaded from informahealthcare.com by IBI Circulation - Ashley Publications Ltd on 10/29/12

et al. 1980). Considering this, it is important to


lization exacts a modest metabolic cost as walking quantify the movement also on the criterion of
requires active lateral stabilization. It has been efficiency (Fetters and Holt 1990; Sparrow and
demonstrated that the gluteus medius, although Newell 1998).
acting primarily outside the sagittal plane in walking, In biomechanical and physiological research, effi-
contributes to support and slows progression (less ciency of movement is normally defined as the ratio
than the other muscles) in the first half of stance and of the mechanical work performed and the metabolic
contributes to support in the second half (Liu et al. cost of performing the work (Stainsby et al. 1980).
2006). Additionally, it has been demonstrated that Typically, the efficiency is calculated as
the body lateral motion is partially stabilized via
medio-lateral foot placement (Kuo 1999; Donelan Mechanical work
Efficiency ð%Þ ¼  100:
et al. 2004). Energy work
Energy expenditure during walking can be char-
For personal use only.

Movement efficiency acterized through mechanical energy estimations


(Cavagna et al. 1963; Willems et al. 1995; Saibene
The relationship between muscle activity and whole
and Minetti 2003) or metabolic energy measure-
body mechanics is too variable and complex to allow
ments (Waters and Mulroy 1999). Mechanical
direct control of the latter without an intermediate
energy is generally estimated by one of three
kinematic representation (Lacquaniti et al. 1999).
approaches: (1) analysis of energy changes of the
There is evidence that supports the idea that global
CoM in relation to the surroundings (external work)
kinematic gait is controlled (Ivanenko et al. 2004).
Kinematics is relatively invariant in various modes of and of the body segments regarding the CoM
locomotion, while the electromyographic activity (internal work) (Cavagna et al. 1963; Cavagna and
patterns to produce the required kinematic patterns Margaria 1966; Willems et al. 1995); (2) analysis of
can vary considerably (Grasso et al. 1998; Ivanenko the energy changes of moving body segments (sum of
et al. 2004). These findings suggest that neural segmental energies); or (3) measurement of muscle
circuitry can somehow specify limb kinematics, and power around the joints (net joint work) (Winter
the appropriate muscle synergies would be deter- 2005). In all mechanical energy estimations, the
mined in a subordinate and flexible manner to adapt actual amount of work performed is underestimated,
to the current mechanical constraints (Lacquaniti as additional metabolic work resulting from isometric
et al. 1999, 2002). The basic biomechanical control muscle contractions or antagonist co-contractions is
signal may exert its action through an appropriate not taken into account (Fetters and Holt 1990;
model of inverse dynamics and feedback device that Winter 2005). This problem is overcome when
determines the muscle torque necessary to achieve assessing metabolic energy, that is, by measuring
kinematic patterns (Ivanenko et al. 2004). The oxygen consumption during walking (Fetters and
significance of muscle redundancy would then be Holt 1990; Vandewalle 2004). The relation between
to allow the same movement to be carried out by metabolic cost and the mechanical work performed
means of different combinations of muscle activity by stance limb muscles to lift and accelerate the CoM
under dissimilar environmental circumstances, for during walking has been already demonstrated
instance, to cope with fatigue or changes in load (Donelan et al. 2001, 2002a) and has been consid-
(Lacquaniti et al. 1999). ered a valid predictor of walking performance
The major function of muscles in gait is to (Anderson and Pandy 2001). Metabolic energy
generate and absorb energy; such function is largely expenditure can be accessed through indirect calo-
ignored in neurophysiological research (Winter and rimetry, where oxygen consumption and/or carbon
Eng 1995). The body has the capacity of transferring dioxide production is measured and converted into
energy between segments across the joint centers and energy expenditure using formulae (Garby and
Postural control and efficiency of movement 9

Astrup 1987; Cunningham 1990) which have been triggered by standard motor action. Electroencephalogr Clin
reported as a valid method (Levine 2005). Neurophysiol 101(6):497–503.
Aruin A, Almeida G. 1997. A coactivation strategy in anticipatory
Mechanical and metabolic energy analyses allow postural adjustment in persons with Down syndrome. Motor
monitoring how the CNS takes advantage of energy- Control (2):178–197.
conserving mechanisms in order to achieve a more Baratto L, Morasso PG, Re C, Spada G. 2002. A new look at
efficient movement. posturographic analysis in the clinical context: Sway-density
versus other parameterization techniques. Motor Control
6(3):246–270.
Concluding remarks Bateni H, Zecevi A, McIlroy W, Maki B. 2004. Resolving conflicts
in task demands during balance recovery: Does holding an
Postural control has been vastly explored in the object inhibit compensatory grasping? Exp Brain Res
scientific community. However, the complexity of 157(1):49–58.
Belen’kii V, Gurfinkel’ V, Pal’tsev Y. 1967. Elements of control of
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the interrelations between neural and mechanical


voluntary movements. Biofizika 10:135–141.
aspects and the environment leads to the need to Borghese N, Bianchi L, Lacquaniti F. 1996. Kinematic
study postural control in a holistic way. In addition, determinants of human locomotion. J Physiol 494(3):863–869.
the study of postural control needs to reflect the Bouisset S, Richardson J, Zattara M. 2000. Are amplitude and
dynamic interrelation of the different components of duration of anticipatory postural adjustments identically scaled
human movement on the basis of movement effi- to focal movement parameters in humans? Neurosci Lett
278(3):153–156.
ciency. The adaptability, vulnerability, and continu-
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of clinical interest. Considering that the postural Staines WR. 1997. Sensori-sensory afferent conditioning with
control system has the capacity of reorganization for leg movement: Gain control in spinal reflex and ascending
higher movement performance, it is important to paths. Prog Neurobiol 51(4):393–421.
Buchanan J, Horak F. 2003. Voluntary control of postural
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Cavagna G, Saibene F, Margaria R. 1963. External work in


mechanisms influence other systems and are influ- walking. J Appl Physiol 18:1–9.
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