REVIEW ARTICLES

Locomotor Training in Neurorehabilitation:

Emerging Rehabilitation Concepts
Hugues Barbeau

ince the publication of the review of treadmill

training in Neurorehabilitation & Neural
Repair published in 1999, several new clinical
studies have been presented on locomotor training
as a rehabilitation approach for stroke and spinal
cord injured subjects. In the series of expert commentaries,1 different authors expressed a spectrum
of views on this new rehabilitation strategy (see
also Dobkin2). The potentials and limitations on
such approaches of the recovery of stroke, spinal
cordinjured subjects, and other neurological populations were discussed.
The goal of this article is to present the newest
evidence that locomotor training is one of the evidence-based clinical approaches that will be used
in the 21st century to enhance recovery of posture
and locomotion in stroke, spinal cord injury subjects and in many other neurological conditions.
The training strategies include modern approaches
of motor learning such as task specificity training of
walking and balance in both feed-forward and
feedback modes.
Figure 1 (left side) illustrates a comprehensive
schematic of several important factors necessary to
achieve functional recovery. Several new
approaches from animal studies, predevelopment
studies, and phase I to phase III clinical trials have
been developed in the last 2 decades, such as locomotor training on treadmill and on the ground
using body weight support (BWS), functional electrical stimulation (FES), and pharmacological
From the School of Physical and Occupational Therapy, McGill
University, Montral, Qubec, and Posture and Locomotion
Research Center, Jewish Rehabilitation Hospital, Chomedey,
Laval, Qubec.
Address correspondence and reprint requests to Hugues
Barbeau, Professor, School of Physical and Occupational
Therapy, McGill University, 3630 Promenade-Sir-WilliamOsler, Montral, Qubec, H3G 1Y5, Canada. E-mail: hugues.
barbeau@mcgill.ca.
Barbeau H. Locomotor training in neurorehabilitation: emerging
rehabilitation concepts. Neurorehabil Neural Repair 2003;17:
311.
DOI: 10.1177/0888439002250442

approaches and their combination to enhanced

recovery in the neurological population particularly stroke and spinal cord injury (SCI) subjects.
These individual approaches have shown great
potential and are different in the process of validation in the rehabilitation setting. Recent reviews
summarize those findings.3-6
Stroke and SCI subjects can adapt, to a certain
limit, the functional prerequisite of posture and
walking, such as speed, slope, obstacles, including
stairs, walking aids, energy consumption, and
attentional and navigational demands (Figure 1,
right column).7 Understanding the strategy that SCI
and stroke subjects use can contribute to the development of concepts and principles that can be
included in rehabilitation.
Figure 1 also illustrates how treatment approaches affect such prerequisites7 necessary to achieve
functional recovery. From Figure 1 (lower panel),
several important concepts for rehabilitation have
emerged and will be presented in the following
section.

SPECIFICITY OF THE TASK

From distinct fundamental studies, locomotor training on the treadmill and/or overground and balance are considered specific tasks.8 For example,
animals with complete transections of the spinal
cord that were trained to walk or stand attained a
very different level of performance. The animals
that were trained to walk achieved a faster speed
than animals that were trained only to stand.
Likewise, animals that were trained to stand performed better standing than animals trained to
walk.9 That could probably explain why neurological patients who have been trained with conventional rehabilitation approaches, such as passive
bracing, would show a decrease in muscle tone but
no change in walking speed. In humans with
stroke or spinal cord injury, it has been demonstrated that locomotor training in different forms

Copyright 2003 The American Society of Neurorehabilitation

H. Barbeau

Figure 1. A model of recovery of walking following spinal cord injury. The model could be applied to other neurological conditions such as stroke. In the left panel, treatment approaches, such as pharmacological, locomotor training,
and their combinations, can enhance the functional recovery of walking, suggesting that plastic changes occur during
the subacute stage, as well as several years after spinal cord injury. In the right panel, several important prerequisites to
achieve adaptation, walking, and navigation are illustrated. In the bottom panel, proposed emerging rehabilitation concepts from animal and human studies are illustrated. (Modified from Ref no. 7.)

could be more powerful than conventional treatment using more traditional concepts.10,11 In fact,
the above results contrast markedly with rehabilitation approaches that focus on decreasing spasticity
or are nonspecific. For example, several studies12-15
found a decrease in spasticity when the spastic
ankle was fixed in dorsiflexion by tilting table, casting or ankle-foot orthosis, but no change in the
walking velocity and performance in cerebralpalsied children could be observed. It is not surprising to find that nonspecific rehabilitation
approaches such as passive stretching,13-15
acupuncture, transcutaneous electrical nerve stimulation (TENS),16 or general home exercise17 have no
beneficial effects on functional locomotor outcomes, as indicated by recent multicenter randomized clinical trials. The same observations have
been made with recovery of balance during walking. Dickstein et al.18 observed an improvement in
balance during standing when stroke subjects had
been trained to shift weight onto the hemiparetic
side. However, this improvement did not transfer to
walking, again suggesting the importance of task
specificity.
4

IMPORTANCE AND APPROPRIATENESS

OF SENSORY INPUTS
From animal and human studies, locomotor training does not consist only of putting the spinal animal or the SCI and stroke subjects on a treadmill.
Appropriate sensory inputs such as loading the
maximum weight that the animal is able to support
without losing balance, facilitating proper trunk
posture and hip extension, and proper loadingunloading are essential to maximizing functional
recovery. The same strategies have been applied in
SCI and stroke subjects.19,20
The important role of sensory inputs has been
shown in several animal studies. First, Forssberg
et al.21 provided evidence indicating that afferent
inputs during hip extension are very important in
resetting and entraining the locomotor rhythm (see
Rossignol for comprehensive review22). Second,
the modulation of reflexes has been shown to be
task and phase specific in intact and spinalized cats
as well as in human subjects. For example,
mechanical or electrical stimulation of the paw or
of the cutaneous nerve during the flexor activity
Neurorehabilitation and Neural Repair 17(1); 2003

Locomotor Training in Neurorehabilitation: Emerging Rehabilitation Concepts

produced an increase in ipsilateral flexor activities

as well as the contralateral extensor activity, but
when the stimulus was delivered during the ipsilateral extensor activity, it increased extensor activity.22 Third, animal studies suggested that appropriate loading (loading and unloading) is very important.23
In fact, there is increasing evidence that during
locomotion, afferent inputs from ankle extensors
lead to autogenic excitation rather than inhibition.23
The mechanism of the effect was still unclear, but
recent animal studies strongly support the role of
modulation of extensor load receptors probably
arising from Golgi tendon organs.23 This represents
a newly discovered function for these receptors in
the regulation of different phases of walking. In the
spinal cordinjured population, appropriate loading during the support phase can enhance the
extensor activity as well as increase the vertical
force during support phase and also trigger swing
phase in the contralateral limb24-26 and can be
incorporated in the locomotor training strategy.
The benefit of locomotor training using BWS may
depend partly on the degree of body unloading
during walking, but this needs further investigation.
In recent studies, Bouyer et al.27 denervated bilaterally the foot of the cat by surgical section of all
the cutaneous nerves of the foot below the ankle.
Although animals displayed a significant deficit
when required to walk on a horizontal ladder or on
a slippery surface, they could recover treadmill
locomotion within a few days. At that stage, it is
nearly impossible to detect a locomotor deficit by
kinematic analysis, although some changes in flexor muscle discharges are present and persist.
However, after spinalization, the cat could not
place its feet on the belt. This suggests that
although the animal may have the ability to compensate for the missing cutaneous information by
other sensory cues (such as proprioceptive), the
spinal cord must be intact for the animal to walk
properly with plantar foot contact.
Sensory inputs may be necessary to stimulate the
locomotor pattern not only for specific controls
(step length, foot placement) but also as an important sensory input provided during the sensory
process in the recovery process following a CNS
insult.

CHALLENGING POSTURE
AND WALKING ADAPTATION
Incorporating walking speed and posture demands
into locomotor interventions is essential to increase
Neurorehabilitation and Neural Repair 17(1); 2003

the maximal walking speed,28 decrease energy

cost,29-31 and change walking aids.28 Training at a
comfortable speed will not challenge locomotor
performance as much as speed training. Thus, to
improve locomotor and postural adaptation, it is
important first to understand the limiting control
mechanisms and second to identify important
determinant variables that could be used to evaluate proper locomotion and posture and to incorporate them into a locomotor and posture training
strategy.
Depending on the severity of the patients
injury (Figure 2) and the time since the injury
(Figure 3), recovery of walking could be achieved
with challenging, task-specific approaches. Several
clinical trials demonstrated major improvement in
walking speed and functional recovery. In fact, the
stroke subject with a low functional level needs a
combination of BWS and treadmill training to
challenge both the posture and the walking speed
(< 0.4 m/s19,32), whereas stroke subjects with initial
walking speeds of 0.4 to 0.5 m/s and above33-35
benefit from BWS plus treadmill training and overground training to challenge both walking speed
and balance. The faster the walking speed was
challenged, the better the outcomes.34,35 Thus, challenges in walking and balance as illustrated in
Figure 1 (right side) should be a prerequisite for
fundamental changes, but challenges should also
be graded according to the severity of the patients
functional limitations. This concept contrasts very
much with training using Bobath approaches36
where no change in walking speed could be
observed. For those subjects who have no locomotor capabilities to start withwho need maximal
assistance in lower limbs at fast speeds, the use of
BWS and treadmill training would probably allow
nonambulatory people to practice a gait-like
motion repeatedly during the recovery process.37
Results from a recent NIH randomized clinical trial
on Asia B, C, and D will be available in 2003. The
recent development of different gait trainers, which
allow wheelchair-bound stroke and SCI subjects to
practice repetitive gait-like movements without
overstraining therapists, showed great potential,
but this approach is only at the beginning of the
validation process.38-40
Locomotor training with BWS may also improve
walking speed in the chronic stages of injury
(Figure 3). This has been suggested by recent
phase I clinical trials in SCI and stroke subjects, but
the magnitude of the change was smaller than that
seen in the subacute stages.3 Locomotor training
using BWS has been proposed for other neurological conditions such as Parkinsons disease and
5

Overground Walking
Speed (m/s)

H. Barbeau

Figure 2. Results from clinical trials by Kosak and Reding (2000), Visintin et al. (1998), Laufer et al. (2001), Nilsson et
al. (2002), Sullivan et al. (2002), Pohl et al. (2002), and one open clinical trial (Lennon et al. 2002), stratified by the initial walking speed. The grey shaded bands represent the comfort speed of healthy subjects. The dotted lines delineate
studies with initial speeds of below 0.5 m/s from those above 0.5 m/s.
Statistical
Treatment Group
Pre/Post Training (wks)
Difference
Kosak and Reding 200032
Visintin et al. 199819
Laufer et al. 200111
Lennon 200236
Nilsson et al. 200233
Sullivan et al. 200234
Pohl et al. 200235

BWS treadmill (n = 8)
ABAW (n = 14)
BWS treadmill (n = 43)
FWS treadmill (n = 43)

Treadmill (n = 13)
Conventional (n = 12)
BOBATH (n = 9)
BWS treadmill (n = 18)
FWS treadmill (n = 19)
Fast treadmill (n = 8)
Variable treadmill (n = 8)
Slow treadmill (n = 8)
STT treadmill (n = 20)
LTT treadmill (n = 20)
CGT treadmill (n = 20)

1.
2.
1.
2.
3.
1.
2.
1.
2.
1.
2.
1.
2.
3.
1.
2.
3.

Pre training
Post training (6W)
Pre training
Post training (6W)
Follow-up (12W)
Pre training
Post training (3W)
Pre training
Post training (17W)
Pre training
Follow-up (40W)
Pre training
Post training (4.5W)
Follow-up (8.5W)
Pre training
Post training (2W)
Post training (4W)

P < 0.039
P < 0.020
P < 0.006
P < 0.030
N/S*
N/S*
P < 0.001
P < 0.010
P < 0.001

N/S = Non-significant
* = P < 0.05
** = P < 0.005

cerebral palsy. Miyai et al.41 showed in a randomized clinical trial of 10 Parkinsons subjects that the
group undergoing locomotor training with BWS
performed significantly better that the conventional group, with the gait increasing from 0.83 to 1.00
m/s in the BWS group versus 0.83 to 0.87 m/s in
the conventional treatment group.
Figure 3 shows the same clinical trials but stratified by the time postinjury, which represents a very
important factor for functional recovery. For example, in study 11, locomotor training was initiated at
3.0 and 5.0 weeks after injury, whereas in the other
studies (Ref nos. 32, 20, 35, 36, 34), training was
initiated at 5.7, 10.4, 16, 16.5, and 104 weeks
6

postinjury, respectively. From these studies, it can

be seen that the earlier the training process is initiated on stroke subjects, the greater the functional
benefits that will result. However, significant
improvement could also be observed during the
chronic stage of recovery.34
Figure 4 shows that approaches combining locomotor training with FES clearly improved the maximal walking speed during the chronic phase of the
recovery, in which no changes are expected. Major
changes occurred in subjects having the faster initial speed (~ 1.0 m/s) but were also observed in
chronic SCI subjects having an initial speed of 0.5
m/s and even in subjects having less than 0.2 m/s.28
Neurorehabilitation and Neural Repair 17(1); 2003

Overground Walking
Speed (m/s)

Locomotor Training in Neurorehabilitation: Emerging Rehabilitation Concepts

Time (Weeks)

This study, in addition to addressing the challenge

issues, raised the importance of intensity and duration of the treatment, since the SCI subjects were
trained on a daily basis. From the above studies,
several important questions need to be addressed
in the near future.

DURING DIFFERENT
STAGES OF RECOVERY
1. Does the combination of different locomotor training approaches, such as locomotor training using
BWS, or FES combined with medication, further
improve the recovery in the most severely affected
subjects? (Figure 2 y-axis to dotted line).
2. Could the initiation of locomotor training using
BWS and/or automated gait trainer improve substantially the walking speed and functional recovery when initiated earlier (< 5 weeks postinjury) in
stroke subjects? (Figure 3, y-axis to dotted line).
3. During the chronic stage of recovery, does the
combination of different approaches as demonstrated by Fung et al42 also improve recovery in the
most severely affected subjects?

FORCED REUSE
The use of assistive walking devices, such as parallel bars, while necessary for the expression of
locomotor behavior, can also lead to overcompenNeurorehabilitation and Neural Repair 17(1); 2003

Overground Walking
Speed (m/s)

Figure 3. Same as Figure 2, but the walking speed is stratified according to the time since the injury. Note that the xaxis is interrupted once and represents the time in weeks.

52
Time (Weeks )

Figure 4. Results of locomotor training using FES plus

treadmill training. (Modified from Ref no. 28.)
n = 5,

n = 5,

n=5

sation and limited adaptive capacity. It is important

to identify means of achieving locomotion at the
early stages of recovery with minimal compensation, such as the use of BWS, and to progressively
decrease the weight support over the training period. In addition, BWS induces a pattern of forced
reuse of the paretic leg, so that the patients cannot
7

H. Barbeau

Figure 5. A to C, The right lower limb kinematics and EMG of a spinal cord injury (SCI) subject walking on the treadmill, at a speed of 0.08 m/s, at 0% BWS (full weight bearing, FWFB with parallel bars [squares], 40% BWS with parallel
bars [triangles], and 40% BWS without parallel bars [circles]). The sagittal angular displacement patterns of a representative cycle for the hip (A), knee (B), and ankle (C) are illustrated. Note the presence of a knee flexion and ankle dorsiflexion at 40% BWS without parallel bars (circles). D, The right lower limb EMG activity for the same 3 conditions FWB
with parallel bars (1st column), 40% BWS with parallel bars (2nd column), and 40% BWS without parallel bars (3rd column). The downward arrows indicate foot-floor contact, whereas the upward arrows indicate toe-off, with the solid line
depicting stance duration and the space denoting swing duration, for both right (R) and left (L) lower limbs. A more
phasic EMG activity in VL and GM and the appearance of a burst of activity in TA during swing could also be observed
with 40% BWS without parallel bars (D). (Modified from Ref no. 44.)

compensate by using the nonparetic leg. This

approach has been in the process of validation for
upper extremities by constraint therapy, to force
the use of the arm and hand.43 This forced-use therapy is already part of the training process for lower
limb recovery in both stroke and SCI subjects, particularly for those presenting an asymmetric lower
limb pattern. As shown in Figure 4, the chronic SCI
subject walks on the treadmill holding onto parallel bars with no BWS, the SCI subject compensates
by pushing with his upper extremities and the less
affected lower limb. The resulting lower limb kinematics show an increase in ankle plantarflexion in
the left (less affected) limb (not illustrated) at the
end of stance, while swinging the right leg (more
8

affected, illustrated in Figure 5) with a minimal

amount of hip, knee, and ankle flexion. When 40%
BWS was provided, while the SCI subject walked
with parallel bars, minimal changes were noted in
the walking pattern (Figure 5A to C, squares, triangles) as the subject continued to compensate with
the upper extremities and the less affected lower
limb. However, when the SCI subject released the
parallel bars while walking at 40% BWS, a more
normal gait pattern emerged. This was characterized by an appropriate swing phase with flexion at
the hip, knee, and ankle (Figure 5A to C circles), as
well as a burst of activity of the limb muscles such
as the tibialis anterior muscle (Fig. 5D, 40% no
bars). These results suggest that although walking
Neurorehabilitation and Neural Repair 17(1); 2003

Locomotor Training in Neurorehabilitation: Emerging Rehabilitation Concepts

Figure 6. Representative video pictures at critical gait events of a chronic spinal cord injury (SCI) subject taken, respectively, during placebo evaluation (A), postmedication evaluation (B), and posttraining evaluation (C) (see text). Arrow
1, knee sag; arrow 2, no knee extension; arrow 3, minimal stride length; and arrow 4, trunk instability. (Modified from
Ref no. 42.)

aids are necessary for locomotion, some of them

could be detrimental to the gait during early training. Hence, means other than assistive walking
devices, for example, BWS, should be considered
as permissive for the locomotor training process.

PLASTICITY AND PERMISSIVENESS

Results from animal and human studies revealed
that several important factors are permissive for
walking in SCI and stroke subjects and other neurological populations. For example, in the behaving spinal cat, some drugs that replace neurotransmitters from descending systems, for example, as
noradrenergic agents, combined with locomotor
training can accelerate the recovery of walking.45
Neurorehabilitation and Neural Repair 17(1); 2003

When recovery occurred, the locomotor pattern

could be maintained even if the nonadrenergic
drugs have been removed. In chronic SCI subjects,
Clonidine could also induce limited walking.46,47
But when combined with locomotor training using
BWS, the recovery of walking was greatly
enhanced.42 Figure 6 shows an example of a chronic SCI subject who could not walk or stand; complete support of the body weight and maximal
assistance of two therapists were necessary to
move the lower limbs. After medication, the SCI
subject walked very slowly on the treadmill with
the help of some weight support, but the pattern of
walking was quite abnormal, because it was the 1st
time that the subject walked since the injury. Trunk
and lower limb abnormalities such as leaning forward, knee sag (arrow 1), no hip extension (arrow
9

H. Barbeau

2), short stride length (arrow 3), and leaning backward could be observed (arrow 4). Following locomotor training with BWS, the subject could walk
independently at full body weight on treadmill and
on ground with an increased walking speed at 0.35
m/s. Trunk alignment was improved, and the
patient also exhibited increase of hip extension, a
decrease of knee flexion in early stance and knee
sag at the end of stance, a better weight acceptance, and flatness of foot at floor contact. Thus, the
medication allowed a limited expression of locomotor pattern (permissive) as the locomotor training with BWS and shaped the locomotor pattern
and increased walking and postural performance
using appropriate sensory feedback.
Other permissive strategies, such as body weight
support and/or functional electrical stimulation,
could enhance the recovery of walking when combined with locomotor training.19,20,28,48
In conclusion, this update since the 2nd World
Congress on Neurological Rehabilitation increased
our knowledge about the potential of the locomotor training strategies in the neurological population. First, understanding the effect of new treatment approaches such as locomotor training on the
treadmill, on the ground using BWS and/or FES,
and pharmacological interventions and their combinations will lead to a more comprehensive and
integrative approach in the development of rehabilitation strategies. The time since injury and the
severity of injury are 2 very important variables that
should be taken into account when developing
new rehabilitation approaches. Second, understanding the basic mechanism of adaptation of
locomotion and posture leads to the identification
of control and determinant variables that are
important to properly evaluate and treat neurological populations. Third, emerging rehabilitation
principles based on both animals and human findings should be recognized as important concepts in
neuroplasticity that can impact motor learning and
rehabilitation. Finally, the effectiveness of such
new approaches should be demonstrated by several phase 2 and 3 multicenter randomized clinical
trials.
Within the near future, we can now envision the
integration of several other areas of basic development promoting plasticity and permissivity, such as
pharmacological manipulations, growth factors,
neuronal gene therapy, immunization, cell transplantation, and many others. Those approaches
have already shown a great potential to induce
functional recovery in animal studies.

10

Acknowledgments
Many thanks are due to Vira Rose for secretarial
support, Dr Joyce Fung for her editorial comments,
and Gevorg Chilingaryan for the figures and statistical analysis. This work was supported by the
Fonds de la Recherche en Sant de Quebec (FRSQ)
and the Jewish Rehabilitation Foundation.

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