Reviews

Whole-Body Responses: Neural Control

and Implications for Rehabilitation
and Fall Prevention

The Neuroscientist
Volume 15 Number 1
February 2009 36-46
2009 Sage Publications
10.1177/1073858408322674
http://nro.sagepub.com
hosted at
http://online.sagepub.com

Daniel S. Marigold and John E. Misiaszek

Humans are one of the unique species that utilize bipedal gait to
ambulate in our environment. Despite this fact, coordination of the
arms with the legs and the rest of body is essential for many daily
activities. As such, whole-body responses have emerged as the preferred strategy following perturbations to balance during both standing and walking. Complex neural circuitry may allow for this
coordination through the use of propriospinal pathways linking lumbar and cervical pattern generators in the spinal cord, with supraspinal centers altering this control depending on the context of the

he nervous system must obtain and integrate sensory

information from the visual, vestibular, and somatosensory systems to coordinate the limbs and trunk for safe
locomotion. Fundamental to maintaining upright posture during locomotion is the control of the bodys center of mass within
a moving base of support: a concept known as dynamic stability
(Patla 2003). This task is not trivial because the center of mass
is only within the base of support for ~20% of a stride (Winter
2005). Although most individuals make the task of walking look
relatively simple, those with impairments of the nervous and/or
musculoskeletal systems demonstrate the challenge of this
everyday movement.
Any perturbation during locomotion demonstrates the
complex yet highly coordinated response of the nervous system to prevent the occurrence of a fall. Whole-body responses
following perturbations to balance have emerged as the preferred strategy. Most locomoting animals utilize quadrupedal
control: We are one of the unique species that relies on
bipedal control to ambulate in the environment. Nonetheless,
we often require coordination of the arms and legs to perform
everyday tasks. For instance, pushing open a door to enter or
exit a building, carrying a laundry basket down a flight of
stairs to the basement, and serving drinks from a tray all
require varying degrees of coordination between the upper
and lower limbs.
This review will first highlight the whole-body responses
seen following perturbations during locomotion. Second, the

From the Dpartement de Physiologie, Universit de Montral, Montral, Qubec,

Canada (DSM); and Centre for Neuroscience and Department of Occupational
Therapy, University of Alberta, Edmonton, Alberta, Canada (JEM).
D. Marigolds work was supported by the Canadian Institutes of Health Research
(CIHR). J. Misiaszeks work was supported by the Natural Sciences and
Engineering Research Council, Alberta Heritage Foundation for Medical
Research and CIHR. The authors thank C. Gauthier for help with illustrations.
Address correspondence to: Daniel S. Marigold, School of Kinesiology, Simon
Fraser University, 8888 University Drive, Burnaby, British Columbia, Canada
V5A 1S6; e-mail: daniel_marigold@sfu.ca.

situation. Based on these findings, we argue that whole-body reactions may be exploited for rehabilitation purposes. Preliminary
results have indicated training programs designed to elicit wholebody responses are effective in reducing falls and improving functional mobility in older adults with and without neurological
impairment.
Keywords: locomotion; interlimb coordination; perturbation; wholebody reactions; rehabilitation

potential neural mechanisms behind this whole-body coordination will be discussed. This section is not meant as a thorough review of the neural mechanisms and the reader is
referred to recent reviews on this topic (Dietz 2002; Zehr and
Duysens 2004). Finally, how this knowledge can facilitate
rehabilitation of individuals with locomotor deficits due to
neuromuscular impairment and improve on fall prevention
techniques for older adults will be illustrated.

Whole-Body Responses
Recent research has begun to elucidate the reactions to perturbations to balance during locomotion including slips
(Bhatt and others 2006; Marigold and Patla 2002; Marigold
and others 2003; Oates and others 2005; Tang and others
1998; You and others 2001), trips (Eng and others 1994;
Pijnappels and others 2004, 2005a, 2005b; Roos and others
2008; Schillings and others 2000), and from other challenging terrain (MacLellan and Patla 2006; Marigold and Patla
2005, 2008; Menz and others 2003; Thies and others 2005).
Common to these reactions appears to be the rapid and functional whole-body responses geared to ensure dynamic stability is preserved. The following section describes the nature of
these responses.
There is a considerable body of research that has focused
on the bilateral coordination of the lower limbs in responding to
a perturbation. For example, Berger and others (1984) demonstrated that stumbles induced by accelerating or decelerating a
treadmill belt resulted in short-latency (70 msec) bilateral
responses in muscles at the ankle joints. Tang and others (1998)
reported similar responses with stumbles induced by a simulated
slip of the walking surface demonstrating that corrective
responses to balance disturbances involved bilateral responses in
muscles throughout the legs. Bilateral responses throughout the
leg musculature have also been shown when unexpectedly stepping to a lower support surface (see Fig. 1): Individuals react

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Whole-Body Responses During Locomotion / Marigold, Misiaszek

Figure 1. Unexpected down (UD) versus unexpected level walking

(UL). Top panel shows average ipsilateral medial gastrocnemius
(MGi) activity of the UD and UL conditions of a single subject. The
remainder of the panels show the average muscle activity of all subjects with the UL trials subtracted from the UD trials, where each bin
represents a period of 10 msec and error bars represent standard
deviation. Dotted line shows moment of actual heel contact (AHC)
of UD trials. Bin amplitudes with a statistically significant difference
from 0 (P  .05) are marked by gray bars on the x axis. Onset latencies of responses (L) are indicated by arrows. EHC  expected heel
contact; MGc  contralateral medial gastrocnemius; TAi and TAc 
ipsilateral and contralateral tibialis anterior, respectively; RFi and
RFc  ipsilateral and contralateral rectus femoris, respectively; BFi
and BFc  ipsilateral and contralateral biceps femoris. Figure from
van der Linden and others (2007); used with permission.

with ankle plantar flexion and knee extension of the lead limb
and knee flexion of the trailing limb (van der Linden and others
2007). As shown in this figure, muscle activity in the ipsilateral
medial gastrocnemius (MGi) muscle and contralateral tibialis
anterior (TAc) and biceps femoris (BFc) muscles were activated
prior to actual heel contact in the unexpected down (UD) condition, where the support surface was 5 cm lower than expected.
This muscle synergy in the bilateral lower limbs was responsible
for the changes in ankle and knee angles mentioned above.
However, responses to balance disturbances are not restricted to
the lower limbs during locomotion. Rather, whole-body responses
are frequently observed. Indeed, Tang and others (1998) reported
responses in muscles of the torso associated with the responses
observed in the leg muscles.
Arguably, the most compelling evidence that responses
involve the whole body is the fact that the arms are elicited in

37

conjunction with the coordinated lower limb reactions.

Arm responses are observed following slips (Dietz and
others 2001; Marigold and Patla 2002; Marigold and others
2003; Oates and others 2005; Tang and others 1998; You and others 2001), trips (Mori and others 2001, 2006; Roos and others
2008), and perturbations to the torso (Misiaszek and others
2000; Misiaszek 2003; Misiaszek and Krauss 2005) during
walking. For example, following a slip both arms are moved
upward and forward in conjunction with a lowering (i.e., hip
and knee extension) of the unperturbed lower limb. This is
illustrated in Figure 2, which shows muscle activity from
bilateral deltoid muscles and vertical arm trajectory traces
from one subject. Large muscle responses are followed by
large vertical movements of the arms. The duration of the
upward arm movements are in excess of 500 msec before
returning to their natural arm swing trajectories.
Monkeys trained to walk bipedally also demonstrate
whole-body reactions when tripped by failure to clear an
obstacle during locomotion on a treadmill (Mori and others
2001, 2006). Specifically, the Japanese monkey, M. Fuscata,
rapidly flexes both lower limbs to lower the bodys center of
mass for increased stability and then raises its arms to help
restore its posture (Mori and others 2001, 2006). In humans,
arm movements directed forward and upward are seen following a trip, with the largest arm movement occurring in the arm
contralateral to the recovery limb (Roos and others 2008).
Interestingly, the arm elevation strategy is evoked despite the
perturbations occurring at completely different segments of the
body, and the timing of the arm muscle activation is such that it
occurs simultaneously with the reactions of the rest of the body.
Figure 3 shows muscle activity and kinematic data from a single
subject during a waist-pull perturbation at heel strike during
treadmill locomotion. A large muscle response can be seen in
both the tibialis anterior muscle of the lower limb and the biceps
brachii muscle of the upper limb at approximately 65 to 75 msec
following the perturbation (Misiaszek 2003). Changes in ankle,
knee, and elbow angle are seen following these responses.
The importance of arm movements in the response following a perturbation is reflected by their role in maintaining
stability. For example, arm movements act to dissipate forward center of mass momentum induced by stopping on a
slippery surface (Oates and others 2005) and reduce forward
angular momentum following a trip during locomotion (Roos
and others 2008). Furthermore, Marigold and colleagues
(Marigold and Patla 2002; Marigold and others 2003) have
argued that the forward arm elevation strategy evoked in
response to a slip during locomotion serves to counteract the
backward falling center of mass. This may also be the reason
for the arm movements observed during pulls to the waist
while walking (Misiaszek 2003). In addition, arm responses
may serve a protective role. Specifically, the arms can be used
to reduce hip fractures resulting from a fall by absorbing
force at the point of impact (Feldman and Robinovitch 2007;
Robinovitch and others 2005). Alternatively, arm movements
may be directed to nearby handrails for grasping to maintain
balance. This may be the case, for example, when one slips
while walking down a flight a stairs. Indeed, Maki and
McIlroy (Maki and McIlroy 1997, 2006; McIlroy and Maki
1995) have continually demonstrated arm reactions for reaching and grasping following perturbations to standing balance.
Hemiparesis of the upper limb due to stroke may limit the ability

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The Neuroscientist / Vol. 15, No. 1, February 2009

Figure 2. Whole-body responses evoked by a slippery surface during walking (A). Vertical displacement of a position marker on the unperturbed ankle (B), right arm (D), and left arm (F) showing a lowering response of the unperturbed lower limb and a bilateral elevation of the
arms. Bold red lines represents slip trial and the dashed blue and gray shaded region represents mean and two standard deviations of the control walking trials. The large muscle response generated in the right (C) and left deltoid (E) to elicit the arm elevation reactions following a slip
trial (bold red lines represents slip trial and blue lines represent the mean control walking trials) are also shown. Time zero represents foot
contact on the slippery surface. Modified from Marigold and others (2003); used with permission.

of the central nervous system to elicit these protective responses.

Given the prevalence of falls in persons with stroke (Harris and
others 2005), neurorehabilitation would benefit from training
whole-body movements to either compensate for this impairment or to restore the neural connections necessary for rapid
arm movements following a loss of balance.
Trunk control is essential to the maintenance of upright
posture following perturbations to balance. Indeed, increased
trunk pitch (Owings and others 2001) and the inability to
reduce angular momentum (Pijnappels and others 2005b)
can lead to a fall when tripped. Thus, in conjunction with
arm and leg responses, the musculature surrounding the
trunk may be part of the whole-body response. Several findings of increased hip extensor muscle activity (i.e., biceps
femoris and/or gluteal muscles) in the support limb following
a trip have led many to suggest that trunk control is achieved

by a hip extensor moment (Eng and others 1994; Pijnappels

and others 2005a; Schillings and others 2000). However,
eccentric activity of the erector spinae muscles may also contribute to trunk stability as demonstrated by Marigold and
Patla (2005) when individuals step onto an unexpected compliant surface. Erector spinae and abdominal muscle activity
is also seen following a slip perturbation (Marigold and Patla
2002; Marigold and others 2003; Oates and others 2005;
Tang and others 1998).
What has become apparent over recent years is that
whole-body responses depend on the context of the situation.
Restricting arm movements during waist-pull perturbations
while walking on a treadmill leads to increased lower limb
muscle activation to accommodate the lack of arm responses
following the perturbation (Misiaszek and Krauss 2005).
Conversely, when subjects hold a stable rail the compensatory

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Whole-Body Responses During Locomotion / Marigold, Misiaszek

Figure 3. Responses in arm and leg muscles evoked by a pull to waist

occur at a comparable latency, but prior to deviations in the ongoing
joint motion or head acceleration. The green traces in each pair are the
average of 10 perturbation trials from one subject delivered at heel
strike. The blue traces are the average of 40 control steps. The dashed
vertical line indicates the onset of the perturbation. The response
onset latencies and the time to a deviation in the mechanical traces are
indicated by the times displayed on the figure. TA  tibialis anterior;
BB  biceps brachii; BW  body weight. Positive deflections in the
head accelerometer trace indicate a backward acceleration of the head.
From Misiaszek (2003); used with permission.

responses in the legs are dramatically suppressed or even abolished (Misiaszek and Krauss 2004), despite that corrective
responses in the legs would presumably have been a reasonable
choice. Thus, the actions of the arms in this context replaced
the corrective actions of the legs, presumably to allow the legs
to carry on the task of locomotion unhindered. Similarly,
Rietdyk and Patla (1998) have demonstrated that the recovery
response is modulated based on the amount of support available while being tripped. Muscle activity is altered depending
on whether the individual is tripped while holding a rail during
locomotion or not. Furthermore, knowledge of an upcoming
slippery surface can lead to drastic reductions in muscle activity, elimination of an arm reaction, decreases in lower limb
loading, and stepping with a flatter foot onto the unstable surface (Heiden and others 2006; Marigold and Patla 2002).
These findings indicate that cognitive factors can play a large
role in shaping the response following a perturbation. This also
suggests that strategies for fall prevention techniques may
exploit this cognitive influence by training individuals through
education (Bhatt and Pai 2008).

39

Figure 4. Ensemble average electromyographic traces depicting the

responses evoked in leg and arm muscles following a sudden forward
pull (15 cm) of a set of handles being held by the subject during treadmill walking. The thick dark blue traces represent the perturbed steps
and the thin light blue trace represents undisturbed steps. The evoked
response has been shaded for highlight. Responses in the leg and arm
muscles were observed at a comparable latency, with the response in
gastrocnemius (Gast) occurring earliest at 68 o 5 msec. Perturbations
were applied 200 to 250 msec following left heel strike (LHS). The thin
vertical line indicates onset of the perturbation. The thick vertical line
indicates the onset of the response in Gast. Ham  hamstrings; Tib 
tibialis anterior; VLat  vastus lateralis; Bic  biceps brachii. From
Nashner and Forssberg (1986); used with permission.

What has not been well studied are the corrective

responses evoked during walking when the arms are actively
engaged in weight support and propulsion. Obviously, when
people crawl on all fours the arms take on a role quite different
from when people walk bipedally. It is also the case that when
people use crutches, canes, and walkers, the arms become variably engaged in weight support and propulsion (Peacock
1966). Presumably, the use of assistive devices for ambulation
following neurological injury such as stroke or among frail
older adults, for instance, will alter the strategies of the legs
and arms in balance control. For example, engaging the arms
with the use of walkers and crutches may direct the balance
strategy toward the arms and away from the legs, similar to the
holding of the handles described above (Misiaszek and Krauss
2004). Moreover, the expectation will be that a coordinated
whole-body response will be evoked when the perturbation to
balance is initiated through the arms, via the assistive device,
for example, by a slip of a crutch or the catching of a walker on
an obstacle (in essence, a trip of the walker). Indeed, Nashner
and Forssberg (1986) demonstrated clear responses in muscles
of the arms and legs at comparable latencies following sudden
displacement of a set of handles the subjects were holding during walking (Fig. 4). Similar studies when the arms are engaged

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The Neuroscientist / Vol. 15, No. 1, February 2009

Figure 5. Cutaneous reflexes evoked with electrical stimulation of the right tibial nerve are present in the left triceps brachii (Tric L) during
walking (A), but absent during standing (B) or sitting (C). The thick traces depict the average electromyographic responses to electrical
stimulation of the right tibial nerve (10 r 1 msec rectangular pulses at 200 Hz) and the thin traces depict control recordings with no stimulation. During the standing condition, the arm was swinging, mimicking the arm swing of walking. While sitting, subjects were writing so as to
engage the muscle. Traces in the right tibialis anterior (TA) indicate the effectiveness of the stimulation in eliciting a reflex in that muscle in
all three conditions. From Dietz and others (2001); used with permission from Blackwell Publishing.

in weight support and propulsion have yet to be done. It is also

not yet known to what extent the balance strategies employed
when individuals utilize mobility aids need to be learned after
initiation of their use. However, it is quite likely that optimizing
balance strategies while utilizing mobility aids will require
training with the aids themselves. There is certainly an opportunity for further research into the balance control strategies
and mechanisms employed when utilizing mobility aids to
enhance the effectiveness of these compensatory devices and
optimize safety with their usage.
Taken together, the discussion above supports the notion
that the nervous system utilizes and controls multiple body
segments to maintain balance. That whole-body responses
are part of the natural repertoire available to the central nervous system suggests that neurorehabilitation should promote
the functional recovery of the pathways coordinating the
upper and lower limbs for these responses as part of exercise
programs for people with stroke and/or incomplete spinal
cord injury. Indeed, Ferris and others (2006) have shown that
upper limb movement can enhance lower limb muscle activation during recumbent stepping and argue that neurorehabilitation should make use of the effects of arm movements
to coordinate lower limb muscle activity during therapy. The
neural circuitry involved in this coordination is just beginning
to be teased apart, and the following section attempts to shed
light on the potential mechanisms.

Neural Mechanisms of Upper and

Lower Body Coordination
To date, there is no conclusive evidence to indicate whether
the whole-body responses evoked by balance disturbances are in
fact coordinated and integrated outputs from a common nervous
system response, or if they are coincidental responses evoked

independently by mechanical linkage of the musculoskeletal

system. However, that the corrective responses in the legs share
common features regardless of whether the locus of the disturbance is at the feet or torso would suggest that there is a coordination of the responses in the legs related to a balance
disturbance per se and not to features of the mechanical perturbation. Similarly, the responses in the arm muscles occur at
latencies comparable with responses in the leg muscles, regardless of the locus of the perturbation (Dietz and others 2001;
Misiaszek 2003). These responses often occur prior to the
mechanical disturbance to the limb. Consequently, the more
likely explanation is that these responses are integrated wholebody responses coordinated by common nervous system action.
There are a number of neural mechanisms available to
ensure appropriate coordination of the legs and arms during
balance reactions. Based on the results of studies in the cat
(Gernandt and Megirian 1961; Miller and others 1973, 1975;
Skinner and others 1980) and, more recently, in the turtle
(Samara and Currie 2008) and neonatal rat (Juvin and others
2005), it has been suggested that propriospinal pathways
provide the necessary link between the lumbrosacral and
cervical spinal segments responsible for controlling the lower
and upper limbs, respectively. In humans, interlimb reflexes
have been identified whereby electrical stimulation of the
foot (Kearney and Chan 1979) or mechanical perturbation of
the ankle (Kearney and Chan 1981) produces responses in
the muscles of the arms. Interlimb responses are also evident
during locomotion and are modulated over the step cycle suggesting that these responses are involved in coordination of
the actions of the legs and arms (Haridas and Zehr 2003).
Dietz and others (2001) identified a response that was evoked
in the muscles of the arm following electrical stimulation of
the tibial nerve during walking that was absent when subjects
were standing or sitting (Fig. 5). Electrical stimulation of the
distal tibial nerve evokes a reflex response in tibialis anterior

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Whole-Body Responses During Locomotion / Marigold, Misiaszek

that is qualitatively similar in all three tasks (walking, standing with arm swing, sitting and writing). In contrast, the
evoked response observed in the contralateral triceps brachii
is only observed when subjects were walking. Dietz (2002)
suggests that a flexible neuronal coupling between upper and
lower limbs exists and that the task of locomotion gates this
coupling such that functionally meaningful connections are
available during walking that are not present during other
tasks. Furthermore, Haridas and others (2006) demonstrated
that interlimb reflexes in the arms are modulated with changing levels of postural threat during walking, suggesting that
interlimb reflexes serve a functional link between the arms
and the legs with implications for maintaining stability. Upper
and lower limb coordination may also be part of an anticipatory strategy for a precision locomotor task such as obstacle
avoidance (Michel and others 2008). Cutaneous reflexes
evoked in arm muscles following tibial nerve stimulation were
shown to be enhanced prior to stepping over an obstacle compared with normal steps, and the rate of adaptation of contralateral arm flexor muscle reflex amplitude mimicked that of foot
clearance adaptation to repeated obstacle crossings.
These observed neural connections between the upper
and lower limbs may be exploited for neurorehabilitation of
individuals with spinal cord injury and/or stroke. For example,
cutaneous electrical stimulation can enhance arm and leg
coupling as suggested by Zehr and others (2007). Whereas
combined repetitive task-specific training with electrical
stimulation of the hand improves upper limb function in persons with chronic incomplete tetraplegia (Beekhuizen and
Field-Fote 2008), to promote recovery of upper and lower
limb coordination, repetitive whole-body training combined
with electrical stimulation of the foot (or hand), which could
access interlimb neural circuitry, may also improve upper
limb (or lower limb) function.
During locomotion, both the legs and the arms move
rhythmically in a diagonally coordinated manner. The arms
do not simply swing passively. Rather, it is argued that the
rhythmic motion of the arms requires active control that is
likely to involve a spinal central pattern generator (CPG)
such as has been long argued to be involved in the rhythmic
control of leg movements during locomotion (Wannier and
others 2001; Zehr and Duysens 2004). Propriospinal connections between the CPG networks for the arms and legs are
argued to be critical to ensuring the timing of the activity in
the two oscillators is coordinated (Dietz 2002; Zehr and
Duysens 2004). Recently, Misiaszek (2006) argued that the
rhythmic activity of the CPG for locomotion would be a convenient means by which balance reactions could be gated
over the step cycle to meet the changing functional needs of
the unique biomechanical states of the body during walking.
If so, then the communication between the upper limb and
lower limb oscillators presumably would also be important for
the appropriate scaling or weighting of the responses evoked
in both pairs of limbs following a balance disturbance.
That the whole-body responses described in the previous
section and the cutaneously evoked reflexes described above are
modulated in a context-dependent manner suggests some contribution from supraspinal (and possibly cortical) sources acting
on the lumbar and/or cervical CPGs, or the neuronal linkages
between them. Misiaszek (2006) suggested that descending
influences associated with changing environmental and task
constraints altered the weighting of the components of the

41

corrective responses. In this way, certain rules that must be followed during the task of locomotion can be integrated with the
available options for corrections. Evidence for such a role of
reweighting specific spinal circuitries by descending influences
has been demonstrated by Nielsen and colleagues (Christensen
and others 2001; Nielsen and others 1997; Petersen and others
1998) by using transcranial magnetic stimulation (TMS). First,
Nielsen and others (1997) demonstrated that during tonic voluntary contractions in a seated position, the discharge probability of tibialis anterior motor units and H-reflex amplitude
following combined electrical sural and TMS was larger than
each of the two stimuli applied separately. Second, Petersen and
others (1998) found that TMS timed to arrive during the M3
component of an ankle dorsiflexor stretch while seated resulted
in a greater reflex response of this component, which was not
observed for the M1 and M2 reflex components. Finally, during
the swing phase of walking, TMS timed to arrive during the M3
component of an ankle dorsiflexor stretch results in a greater
reflex response of this component (Christensen and others
2001). Pijnappels and others (1998) have also demonstrated
TMS facilitation of biceps femoris and tibialis anterior cutaneous reflexes evoked by electrical stimulation of the sural nerve
during the swing phase of walking. Although there is also evidence for descending influences during stance phase, it is
much weaker (Christensen and others 2001; Pijnappels and
others 1998). These influences of TMS on specific spinal circuitry provide the evidence to suggest that descending inputs
from at least the motor cortex form the basis by which reweighting or rescaling of corrective responses can occur when the task
or environmental constraints are changed, such as when the
arms are not available either because they are engaged in
another task or are limited by injury (Misiaszek and Krauss
2005). Presumably, descending commands will also determine
the specific responses available, such as the interlimb reflex
observed by Dietz and others (2001) during walking not
observed during sitting.
The implication for neurorehabilitation of a descending
influence on interlimb coordination is that by altering cortical
excitability by noninvasive techniques, it may be possible to
facilitate the recovery of the neural circuitry involved in upper
and lower limb coordination. Cortical excitability may be
altered over a short duration by transcranial direct current
stimulation (tDCS) or repetitive transcranial magnetic stimulation (rTMS) and has been argued to be an important means of
improving function following stroke (Talelli and Rothwell
2006). For instance, anodal tDCS (which increases cortical
excitability) over the arm area of the motor cortex can improve
motor function after stroke when combined with motor rehabilitation (Hummel and others 2005). Furthermore, anodal
tDCS over the leg area of the motor cortex is known to increase
excitability of the corticospinal tract projections to the tibialis
anterior muscle (Jeffrey and others 2007). Thus, whole-body
training following a bout of tDCS or rTMS to the appropriate
cortical area (e.g., primary motor cortex) may be an effective
means of improving motor function. This can be combined with
sensory stimulation via cutaneous electrical stimulation to the
hand and/or foot as discussed above.
It is tempting to speculate that the neuronal linkage
between the upper and lower limbs through propriospinal
pathways (with influence from supraspinal centers) evolved
from quadrupedal locomotion to control whole-body responses
essential for maintaining dynamic stability. In fact, Georgopoulos

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The Neuroscientist / Vol. 15, No. 1, February 2009

and Grillner (1989) have argued that reaching evolved from

the neural systems involved in precision stepping during locomotion. This neural circuitry is likely to provide the means to
coordinate protective responses in the upper body following
perturbations at the foot or torso.

Implications for Neurorehabilitation, Fall

Prevention, and Mobility Aid Design
Clearly, whole-body responses are seen following perturbations
to balance and that there appear to be the neural connections
for this coordination highlights their usefulness in maintaining
balance. Consequently, it seems reasonable to suggest that
rehabilitation of individuals with neurological impairment such
as stroke and spinal cord injury and fall prevention strategies for
those at risk may benefit from utilizing training principles
aimed at eliciting whole-body coordination. Evidence of this
notion stems from the promising results demonstrated in older
adults (Barnett and others 2003; Davis and others 2004; Fong
and Ng 2006; Gatts and Woollacott 2006, 2007; Liu-Ambrose
and others 2004, 2005; Weerdesteyn and others 2006) and
persons with chronic stroke (Marigold and others 2005). These
exercise interventions have shown that balance can be improved
and falls reduced in these populations. For example, Barnett
and others (2003) found a 40% reduction in prospective falls
following an agility-type exercise intervention.
In recent years it has become more apparent that considerable gains in neurorehabilitation are experienced through
approaches that incorporate mass practice. For example, programs of body-weight supported treadmill training (BWSTT)
for improving walking or constraint-induced movement therapy
(CIMT) for improving hand function rely on intensive programs
of repeated exposure to training of specific tasks and functions
of the affected limbs. BWSTT has been effective in improving
the speed and endurance of walking in those with spinal cord
injury, stroke, Parkinsons disease, and other motor impairments. These functional gains have been observed concomitant
with adaptations in the nervous system control of locomotion.
For example, treadmill training in spinal cord-injured individuals leads to more defined patterns of alternating bursts of extensor and flexor activity during the step cycle argued to be
achieved through plasticity of spinal interneuronal networks
(Harkema 2008). There is also the suggestion that treadmill
training is associated with changes in motor cortex maps
(Thomas and Gorassini 2005; Norton and Gorassini 2006; Yen
and others 2008), as has been observed following training of
more skilled tasks such as with CIMT (Liepert and others 2000;
Wittenberg and others 2003). The implication is that a portion
of the benefits realized with mass practice programs is achieved
through plastic adaptations of the neural control of the trained
task. These adaptations may occur along the entire neuroaxis
and multiple levels of the control system.
However, the functional gains in walking ability that have
been realized with programs like BWSTT are limited. The
improved performance in speed and endurance does not transfer to improved or more frequent ambulation in the community.
Stability and balance control remain a concern and become
limiting factors to community ambulation. The most likely
reason for this is that programs such as BWSTT lead to
highly repetitive and stereotyped movements not reflective of
the diversity of needed actions in a more natural setting.

Consequently, if training programs for walking balance control

are to be successful in improving functional ambulation in the
community, the programs are likely to require intensive programs involving a variety of challenges and incorporating
aspects of the whole-body strategies described below.
Whole-body coordination training can be elicited through
various means including the use of agility training or by walking
tasks that challenge balance. Examples of exercises that utilize
whole-body training principles are numerous, and the following
list is not meant to be exhaustive. Agility training is meant to
challenge foot-eye, hand-eye, and whole-body coordination.
Agility training exercises used in the literature include dance
movements, obstacle courses, ball games (e.g., catching/throwing
activities), and stepping movements (Barnett and others 2003;
Liu-Ambrose and others 2004, 2005; Marigold and others 2005;
Weerdesteyn and others 2006). The latter encompass many different aspects such as changes in direction, rapid stepping onto
targets, crossover and side stepping, stepping over obstacles,
tandem walking, and figure-eight walking. Additional ways of
eliciting whole-body coordination include walking while carrying
shopping bags or trays with empty cups (Weerdesteyn and others
2006), Tai Chi exercises (Fong and Ng 2006; Gatts and
Woollacott 2006, 2007), and perturbation training (Hocherman
and others 1984; Marigold and others 2005).
A recent technique for improving functional balance and
reducing falls is the use of challenging ground terrain (or multisurface terrain). Indeed, trunk control is impaired in older adults
when walking on different types of ground terrain (Marigold and
Patla 2008) and the challenges evoked by different surface characteristics can increase the risk of a fall. Weerdesteyn and others
(2006) have shown a reduced incidence of falling in older adults
following an exercise intervention designed with an obstacle
course featuring different ground surfaces (e.g., uneven and
compliant terrain) and challenges to foot placement via stepping
to irregularly spaced targets.
Interestingly, several recent studies have found exercise can
lead to faster reflexes following perturbations to balance (Fong
and Ng 2006; Gatts and Woollacott 2006; Marigold and others
2005), which may also serve to reduce falls. For instance, it has
been shown that delayed postural reflexes in paretic lower limb
muscles in persons with stroke following perturbations during
standing contribute to falling (Marigold and Eng 2006). Following
an intensive agility exercise program that involved whole-body coordination training in persons with chronic stroke, Marigold and
others (2005) demonstrated an ~28-msec shorter postural reflex
in the paretic rectus femoris muscle and a reduction of falls following standing perturbations.
Although considerable strides have been made in improving gait function in persons with incomplete spinal cord
injury, future work may also benefit from the use of wholebody training. Incorporating whole-body coordination into
the neurorehabilitation of individuals with spinal cord injury
may encourage the reestablishment of functional connections between the upper and lower limbs that may have been
compromised due to the lesion of the spinal cord. An early
study by Musselman and others (Musselman KE, Fouad K,
Misiaszek JE, Yang JF, unpublished data, 2008) has shown
that incomplete spinal cord-injured subjects who have plateaued with respect to treadmill training programs experience
further functional gains in locomotor capacity and balance
confidence from a training program that incorporated obstacles, stairs, slopes, and different ground surfaces.

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Whole-Body Responses During Locomotion / Marigold, Misiaszek

43

Figure 6. Simplified schematic of the neural control of whole-body coordination. Common daily activities (e.g., carrying an object while walking,
pushing a stroller) and perturbations (e.g., slipping on ice, tripping) that utilize whole-body coordination are shown. Red arrows illustrate suggested
neural connections between upper and lower limb central pattern generators (CPG). Blue arrows indicate the influence of supraspinal centers on
spinal CPGs and whole-body coordination. Green arrows demonstrate spinal CPG output to upper and lower limb musculature and afferent feedback to the spinal cord. Note that the schematic should not imply that afferent feedback is derived from only muscle mechanoreceptors of the limbs.
Other sources, including cutaneous, vestibular, and visual have not been detailed for simplicity.

Mobility aids, often thought to improve balance and

mobility, have the potential to impede recovery from a perturbation. In a review of the literature, Bateni and Maki (2005)
reported that mobility aids can restrict upper and lower limb
compensatory reactions and walker and/or cane use can be a
prospective predictor of falls (Campbell and others 1989; Maki
and others 1994) or associated with falls and injuries (Campbell
and others 1981; Charron and others 1995). For example,
Bateni, Zecevic, and others (2004) investigated the response of
participants to forward and backward standing platform translations while either holding a cane, cane top, or with both
hands free. There was a dramatic reduction in the percentage
of trials in which a reaching/ grasping reaction was used when
holding the cane or cane top. Although muscle activity in the
arm was not necessarily inhibited, the amplitude was attenuated. Interestingly, Bateni, Zecevic, and others (2004) also
found that individuals tend to hold onto a cane rather than
utilize the reaching/grasping reactions observed when the hand
was free despite this choice causing a loss of balance, and they
argue the nervous system seems to give priority to the ongoing

task. Furthermore, Bateni, Heung, and others (2004) found

that collisions between the swing foot and a standard pickup
walker or cane were frequent (i.e., 60% of stepping reactions
in the walker condition) and step length was reduced when
lateral stepping reactions were evoked by medial-lateral platform translations.
Impeding arm movements following a perturbation to
gait (e.g., slip) may also have devastating consequences.
Indeed, restricting the arms causes a change in response following a perturbation during locomotion (Misiaszek and
Krauss 2005). Misiaszek and Krauss (2004) recently found
that 1) compensatory responses in the legs were suppressed
in amplitude and 2) compensatory responses in the arms
were slower when subjects held safety rails, compared with
when the arms were swinging freely. This may reflect an
increased confidence of the subjects when holding the handles, which could impair the quality of the corrective response
if the ability of the arms to contribute to a corrective response
is overestimated. This would have important implications for
the role of such corrective reactions when mobility aids are

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The Neuroscientist / Vol. 15, No. 1, February 2009

used to assist with balance maintenance. Taken together,

these findings support the notion that mobility aid design
must account for the potential negative effects of their use
and future research needs to address this issue.

Conclusions
Whole-body responses are utilized for recovering from perturbations during locomotion to maintain dynamic stability.
These responses manifest themselves as coordinated lower
limb and arm reactions as well as stabilizing muscular activity
at the torso. This interlimb coordination may be controlled
through a combination of propriospinal pathways linking
cervical and lumbar central pattern generators and supraspinal input that facilitates context-dependent responses. This is
summarized schematically in Figure 6. As illustrated in this
figure and discussed throughout this review, many daily
activities and situations require whole-body coordination.
The importance of the coordination of the arms and legs is
reflected in the modifications evoked when one of these segments is restricted (i.e., arms constrained) and by the fact
that the arms contribute to the response following a perturbation to the waist or feet during both walking and standing.
If whole-body responses are important for maintaining
dynamic stability, then fall prevention techniques and neurorehabilitation of people with locomotor deficits (e.g., stroke
and spinal cord injury) should include whole-body coordination. Agility training, Tai Chi, and the use of multisurface
terrain may all be effective in this endeavor as they each elicit
these whole-body stabilizing reactions. These techniques may
then facilitate changes in neural structures leading to meaningful improvements in motor function.

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