JOURNAL OF NEUROTRAUMA

Volume 23, Number 3/4, 2006

© Mary Ann Liebert, Inc.
Pp. 571–585

Physical Determinants, Emerging Concepts, and Training

Approaches in Gait of Individuals with Spinal Cord Injury

HUGUES BARBEAU,1 SYLVIE NADEAU,2 and CHRISTIANE GARNEAU2

ABSTRACT

The aim of this review is to examine the physical determinants for functional walking as well as the
efficacy of gait rehabilitation after spinal cord injury (SCI) in humans. The results indicate several
important physical determinants in gait. Examples are provided of different interventions that pro-
duce beneficial effects on outcome measures of gait such as gait speed, stride length, walking en-
durance, motor recovery, and gait quality. These findings need to be considered in current SCI re-
habilitation practices, but the efficacy of certain interventions remains unclear. Well-designed
clinical trials are needed to provide evidence of the role of physical determinants in the develop-
ment of new concepts and principles in locomotor recovery after SCI. This review focuses on rele-
vant literature, and informs rehabilitation specialists and basic scientists about the physical deter-
minants and factors to consider for optimization of gait training in individuals with incomplete SCI.

Key words: determinants; emerging rehabilitation concepts; spinal cord injured subjects; treatment ap-
proaches; walking

INTRODUCTION and life expectancy have been noticed. Life expectancy

of this population has changed. Nowadays, after a SCI

I N NORTH AMERICA, spinal cord injury (SCI) occurs

yearly in 10,000–12,000 individuals, and currently
about 250,000 individuals live with such an injury
(Nobunaga et al., 1999). The data suggest that about 1000
Canadians sustain SCI every year, and about 25,000 in-
dividuals cope with its consequences. While in the past,
over 60% of individuals who had traumatic SCI were un-
der 30 years old, recent information shows that the mean
age at injury in adult population has increased to 39 years
old, with 17% of the victims sustaining SCI being over
55. Men remain predominant, at 89% (Noreau et al.,
2004). Other important trends in the severity of injury
occurring at age 20, the life expectancy currently ranges
from 37 to 44 years in individuals with severe injury (De-
Vivo et al., 1999; ASIA A–C, Table 1). Thus, a subject
with SCI will live with limitations for a longer period
than before, with great impact on societal costs and care-
giver burdens. Due to advances in trauma care, only 41%
of new SCI are complete ASIA A lesions, compared with
60% or more in the past (Noreau et al., 2004). Approxi-
mately two-thirds of the individuals with incomplete
spinal cord injury (ISCI) lesion will have functional sen-
sory-motor recovery caudal to the injury (Stover et al.,
1995).

1School of Physical and Occupational Therapy, McGill University, Montreal, Quebec, and Jewish Rehabilitation Hospital,
Laval, Quebec, Research Site of Centre de Recherche Interdisciplinaire en Réadaptation (CRIR), and 2École de Réadaptation,
Faculté de Médecine, Université de Montréal et Laboratoire de Pathokinésiologie et d’Analyse des Activités Fonctionnelles,
CRIR, Institut de Réadaptation de Montréal, Montreal, Quebec, Canada.

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 BARBEAU ET AL.

TABLE 1. NEUROLOGICAL CLASSIFICATION OF INJURY PROPOSED BY THE AMERICAN SPINAL INJURY ASSOCIATION (ASIA)

ASIA grade Description

ASIA A Complete: No motor or sensory function is preserved in the sacral segments S4–S5.
ASIA B Incomplete: Sensory but no motor function is preserved below the neurological level
and includes the sacral segments S4–S5.
ASIA C Incomplete: Motor function is preserved below the neurological level and the
majority of key muscles below the neurological level have a motor score
3
(grade 0–2).
ASIA D Same as C but at least half of the key muscles below the neurological level have a
muscle grade 3.
ASIA E Normal: Sensory and motor function are normal.

From Marino et al. (2003).

Following SCI, limitations in sensory-motor activities
such as walking and posture are among the most severe
perturbations and are associated with a disturbance of the
reflex activity (development of spasticity) and the in-
ability or difficulty to recruit muscles below the lesion.
The recovery of sensory-motor activity, balance, resid-
ual muscle strength, and development of compensatory
strategies will therefore be determining factors in achiev-
ing a high level of functional independence. Although
one of the most common goals in these patients is the re-
covery of walking, only a few will be able to retrieve a
normal level of function. At discharge from rehabilita-
tion, 39% of the SCI individuals have an ASIA D score
(Noreau et al., 2004). These individuals plus those hav-
ing an ASIA C score have the best prognostic for the de-
velopment of independent gait. This paper will focus on
this group of persons, beginning with a review of the lit-
erature associated with the locomotor capacities and the
physical determinants in gait, and ending with the prin-
ciples and approaches of gait training.
LOCOMOTOR RECOVERY AFTER
A SPINAL CORD INJURY
The most important goal for an individual after an
acute SCI is often the recovery of safe and effective rec-
iprocal gait. A recent Quebec province study with 139
SCI individuals has shown the severity of the lesion be-
ing divided as ASIA A, B, C, and D, in respectively
50%, 16%, 11%, and 24% during acute care (Noreau et
al., 2004). According to the descriptive population sta-
tistics done in 1996 and 1997 with 4 American and 2
Canadian rehabilitation facilities, there is 15% of the
ISCI patients classified as ASIA B at time of admission
for rehabilitation that will reach a functional indepen-
dence measure (FIM; Table 2) walking score equal or
better than 5 at discharge, while 40% of ASIA C and
75% of ASIA D will do so. Even a few individual clas-
sified ASIA A within 1 to 4 weeks post injury recover
walking (Dobkin et al., 2003). Burns et al (1997) stud-
ied 105 ASIA C and D tetraplegia subjects 72 h post
accident. They have shown that 80% of patients with an
ASIA C walked, albeit abnormally, at discharge,
whereas this percentage increases until 100% for those
who were classified ASIA D. For the patients with an
ASIA C score, there is an age effect, with percentage
reaching 91% and 42%, respectively for those under and
over 50 years old. Considering that subjects in any
ASIA groups during acute care could potentially re-
trieve some locomotor function, efforts directed to max-
imize walking capabilities, reduce energy cost and de-
viations of gait are mandatory.
PHYSICAL DETERMINANTS OF GAIT
It is known that normal gait requires several capabili-
ties including strength, sufficient range of motion, coor-
dination, aerobic capacity, proprioception and sensation
of the lower limbs, as well as adequate balance, posture,
vision and planning of movements (Brown et al., 1995;
Prince et al., 1997) (Fig. 1). Some of these factors have
already been recognized as important determinants of gait
performance. A determinant of normal gait has been pre-
viously defined as a basic factor that allows one indi-
vidual to walk normally, navigate safely and efficiently
in such a way that when the factor becomes insufficient,
it prevents the subject from walking normally (Nadeau
et al., 2001; Barbeau, 2003). Regarding the patient pop-
ulation analyzed, the relative importance of the determi-
nants in gait function will vary in accordance with the
clinical status of the patient. As example, in geriatric pop-
ulation all determinants might need to be considered
whereas in orthopedic population, specific determinants
such as range of motion and strength of the lower limb

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 GAIT OF INDIVIDUALS WITH SPINAL CORD INJURY
TABLE 2. FUNCTIONAL INDEPENDENCE MEASURES (FIM)
No helper
7 Complete independence
6 Modified independence
5 Exception (household ambulation)
Helper
5 Supervision
4 Minimal contact assistance
3 Moderate assistance
2 Maximal assistance
1 Total assistance
From Center for Functional Assessment Research (1993).
will probably be more important to consider than others
in the rehabilitation process.
From a literature review of gait studies in subjects with
SCI grade C and D, it is expected that the most impor-
tant determinants are muscle strength, muscle tone, mus-
cle coordination, range of motion, proprioception and
sensation, as well as balance and posture (Fig. 2). The
majority of determinants will be more or less predicted
by the neurological level and the lesion severity (Burns
et al., 1997; Noreau et al., 2004) as evaluated by the ASIA
impairment scale. Other studies point out that the level
of independence in gait in ISCI might be affected by the
FIG. 1. Main determinants of normal gait.
Walking score
Subject walks a minimum of 50 m in a reasonable time and
safely without assistive devices. Does not use a wheelchair.
Subject walks a minimum of 50 m but uses an assistive device
(such as orthosis, cane or walker); takes more than reasonable
time or there are safety considerations.
Subject walks a minimum of 17 m independently with or
without a device. Takes more than reasonable time, or there are
safety considerations.
Subject requires supervision to go a minimum of 50 m.
Subject performs 75% or more of locomotion effort to go a
minimum of 50 m.
Subject performs 50–74% of locomotion effort to go a
minimum of 50 m.
Subject performs 25–49% of locomotion effort to go a
minimum of 17 m. Requires assistance of one person only.
Subject performs less than 25% of locomotion effort, or requires
assistance of two persons, or does not walk a minimum of 17 m.
patient’s physical condition (Waters et al., 1989), his/her
medical conditions (Subbarao, 1991), age (Burns et al.,
1997), and the medication used to reduce spasticity (Bar-
beau et al., 1999b).
The relative contribution of each determinant men-
tioned in Figure 2 for recovery of walking is still un-
known. As example, the results of a sagittal gait analy-
sis of one typical ISCI subject assessed at 3 and 12
months after the lesion, is compared to normal kinematic
(angles) and kinetic (moments) profiles obtained at self-
selected speed (Fig. 3). The results of the clinical tests
are also presented on the bottom of Figure 3. Walking
speed increased slightly from 3 to 12 months whereas the
gait parameters showed important changes during this pe-
riod. Particularly, the hip and ankle angles and the net
joint moments (internal moments) approach normal val-
ues, whereas the knee flexion pattern associated with the
high knee extensor moment was significantly reduced
and the profiles tended towards normality (Fig. 3, ar-
rows). These improvements were associated with clini-
cal gain in balance, in lower muscle strength and reduc-
tion of muscle tone. All these improvements might
explain changes in the gait pattern. However, at 12
months, the clinical results revealed normal scores for the
lower extremity motor score (LEMS), FIM, balance and
sensation (only muscle tone was still slightly increased),
whereas the walking speed and the associated gait pro-
files remained abnormal. It is believed that a further as-
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 BARBEAU ET AL.

sessment of the determinants, using measures much more

FIG. 2. Determinants that affect gait in persons with spinal
cord injury (SCI; black color). The ellipse includes factors that
reduced the impact of affected determinants.
relevant for higher gait performers such as dynamic mus-
cle testing will need to be used to assess properly the fac-
tors that limit the gait performance of this subject.
Moreover, in ISCI, factors such as the ability to use
assistive devices, orthoses (Waters et al., 1989) and, par-
ticularly the use of compensations need also to be con-
sidered to better infer of their walking capacity. These
factors have the potential to reduce the impact of affected
determinants in subjects with SCI. Nadeau et al. (2001)
and others (Winter, 1980; Danion et al., 1995) consid-
ered that a compensation is present when additional body
systems are recruited or used. It includes an idea of ad-
ditional efforts or recruitment or an overuse of a system
to compensate for an underuse of another in a given task

FIG. 3. The results of a sagittal gait analysis of one typical ISCI subject, assessed at 3 (dotted lines) and 12 months (thin lines)
after the lesion, are compared to normal (thick lines) kinematic (angles) and kinetic (moments) profiles obtained at self-selected
speed (1.26  0.19 m/s). Extension and plantarflexion have a positive sigh in graphs (a), (d), and (e) and a negative sign in graphs
(b), (c), and (f). Results of the clinical tests are presented in the table at the bottom of the figure.

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 GAIT OF INDIVIDUALS WITH SPINAL CORD INJURY
or sub-task of gait. For example, Winter (1980) reported
that in order to support their body weight, subjects with
knee impairments can compensate for decreased exten-
sor moment at the knee by an increased or a prolonga-
tion of the hip extensor moment. Nadeau et al. (1999b)
showed that after a stroke, some individuals with weak
plantarflexors were able to walk at reasonable speed by
using their hip flexors. Such compensations have also
been identified in transfemoral amputees (Winter and
Sienko, 1988; Czerniecki et al., 1996) and in patients with
diabetes mellitus (Mueller et al., 1994). It is believed that
a decrease energy generation produced by the plan-
tarflexors during gait is compensated by elevating the
contribution of the hip flexors. The compensatory strate-
gies are used by patients to produce the most functional
gait within the limits of their neural defects. It is not re-
ally known why a subject decide or not to use a com-
pensation to perform better and whether the compensa-
tion is an autonomous effect or that it can be acquired by
experience (i.e., a learning effect of the nervous systems
involved). However, as mentioned previously by Nadeau
et al. (2001), the decision is probably unconsciously
based on self-optimization criteria such as minimization
of the physiological energy, maximization of the me-
chanical energy conservation, preservation of bilateral
symmetry, reduction of amount of loading in the skele-
ton and pain reduction that aim to minimize the “costs”
to the system (Mizrahi, 1984; Jeng et al. 1996) might be
taken in account. The determinants and the compensa-
tion strategies have not been rigorously assessed in per-
sons with ISCI able to walk independently and future
studies aiming to improve the understanding of gait prob-
lems in this group of subjects will need to consider these
aspects. The next sections will present some studies that
have provided evidences to the identification of determi-
nants of gait performance in ISCI population (Fig. 2).
Muscle Strength Impairments in the Lower Limbs
Many researchers have found high correlations be-
tween muscle strength and speed of gait (Perry et al.,
1993; Bohannon et al., 1996; Powers et al., 1996; Nadeau
et al., 1999a). It is known that walking puts a high de-
mand on the torque-producing capabilities of the muscu-
lar system (Hussey and Stauffer, 1973; Crowinshield et
al., 1978; Winter 1984; Bassey et al., 1988), and thus
muscle strength of the lower limbs might be expected to
be an important determinant of locomotor capacity. As
mentioned by Kim et al. (2004), muscle strengthening is
a principal intervention following ISCI to improve func-
tional abilities such as walking. In individuals with SCI,
differences in gait performance parameters were ac-
counted for by the severity of lower extremity paralysis
575
(Waters et al., 1993, 1994). Moreover, in Waters et al.
(1993), improvement in gait velocity parallels improve-
ment in strength. A study from Hussey and Stauffer
(1973) proposed that patients, able to walk in their com-
munity (walking velocity  0.94 m/sec), had pelvic con-
trol with fair hip flexor strength and fair extensor strength
in at least one knee, so that no more than one knee-an-
kle-foot orthosis (KAFO) was required.
This idea of finding key muscles in ISCI gait has been
further investigated in a recent study of Kim et al. (2004).
This group of researchers has tried to identify the mus-
cle groups that most closely relate to walking perfor-
mance in ISCI subjects able to walk. They assessed mus-
cle strength in 22 subjects with ISCI 1-year post-injury
using manual muscle test (MMT: grade 0–5) (Kendall et
al., 1993). They found that, in particular, hip flexors, hip
extensors and hip abductor strength showed the strongest
correlations with gait capacity. In general, a less affected
side showed higher level of correlations than a more af-
fected side. The hip muscles have been shown to be im-
portant key muscles in gait in other groups of patients
(Bohannon 1986; Nadeau et al., 1999b; Weiss et al.,
2000). However, in subjects having weakness post-
stroke, in general, higher gait/muscle strength correla-
tions were found on the most-affected side affected side
(Bohannon, 1986). Moreover, Kim et al. (2004) failed to
find a strong association for the knee extensor muscle
strength while several previous studies have revealed that
the strength of this muscle group was among the best pre-
dictor of gait speed (Nakamura et al., 1985; Waters et al.,
1993; Powers et al., 1996; Rantanen et al., 1998). They
suggested that when a score of 3/5, representing that anti-
gravity knee extensor strength was achieved, additional
knee extensor strength did not appear to further contribute
to an increase in walking performance. This might indi-
cate that the knee extensor strength was not the weakest
element of the chain in those subjects and further mus-
cle strength will not help to improve or compensate for
the weakest elements. However, more objective methods,
like the use of hand-held dynamometer, will need to be
used to confirm the role of the knee muscle strength in
determining gait capacity for score equal or higher to 3
in subjects with ISCI.
Although muscle strength of the lower limbs in ISCI
has been assessed only qualitatively using clinical scores
such as the ambulatory motor index (AMI), the ASIA
LEMS and MMT, there seems to be enough evidence to
support muscle strength in gait as a major determinant of
gait ability in persons with ISCI. The contribution of one
or many muscle groups might be less or more important
according to the portrait of muscle weaknesses in those
subjects. The impact of using assistive devices for gait
needs also to be considered since they reduced the level
 BARBEAU ET AL.
of preservation of lower extremity muscle strength re-
quired to walk. Waters et al. (1993) have shown that per-
sons with incomplete tetraplegia having various degrees
of upper extremity paralysis are often less capable of us-
ing extremity assistive devices than incomplete paraple-
gia having normal upper extremity functions. These in-
dividuals also tended to require relatively greater
preservation of lower extremity muscle strength to walk
than typical subjects with impairments restricted to the
trunk and lower limbs. Further research will need to pro-
vide additional evidences by analyzing the effect of spe-
cific muscle strengthening of the expected key muscle
groups and examine their impacts on gait performance.
Moreover, the strength of the trunk muscles which has
not been specifically examined, will need also to be con-
sidered, especially in subjects with ISCI who might pre-
sent varied strength impairments.
Muscle Tone Impairment and Spasticity Level
Impairment to muscle tone is probably another impor-
tant determinant in ISCI subjects able to walk indepen-
dently. In contrast to individuals with stroke, in whom
the level of spasticity (hyperactivity of the stretch reflex)
on the paretic lower limb is generally not significantly
associated with gait speed, hypertonicity might have
more impact on gait performance in ISCI subjects. Some-
times observed with co-activation and alteration of tim-
ing and amplitude of muscle activity (motor dyscoordi-
nation), spasticity is a frequent impairment in ISCI, since
one third of those having a ASIA D severity had received
antispastic treatment within a year of injury (Barbeau et
al., 1999b). Spastic paretic ISCI subjects presented
greater hip flexion during stance than normal subjects.
They made foot contact with the knee in a flexed posi-
tion, and for some the knee remained flexed throughout
the stance phase. This last finding was observed, at 3
months, in one typical subject (Fig. 3). At that time, his
Ashworth scale score (Ashworth, 1964) was of 4/5 which
indicates a considerable increase of the resistance to a
passive movement. The study of Krawetz and Nance
(1996) corroborates this idea. They assessed the level of
spasticity using the pendulum test (Brown et al., 1988)
and the Ashworth scale in 27 ISCI subjects able to am-
bulate independently for 10 m with or without aids. In
their study, individuals with thoracic SCI were the most
spastic and manifested the greatest deviations in kine-
matic gait parameters. Particularly knee excursion and
knee angular velocity parameters were significantly cor-
related with spasticity measures. All these findings con-
firm a role of muscle tone impairment in the determina-
tion of gait performance in ISCI. However, as noted
by Krawetz and Nance (1996), adequately measuring
576
changes associated with antispasticity treatment will help
to clarify the role of spasticity as a determinant of gait
in ISCI.
Range of Motion Impairment
The role of reduced range of motion (ROM) as a de-
terminant of gait has not been studied precisely in ISCI
individuals. The real impact of this factor might be dif-
ficult to assess in this group of individuals since they have
other impairments (spasticity, co-activation) that affect
their gait performance and even decrease their ROM. The
gait capacity, in general, is decreased in persons pre-
senting reduced ROM (Mattsson and Brostrom 1990;
Messier et al., 1992; Cerny et al., 1994; Shimada 1996).
Reduced joint mobility decreases the angular excursion
and reduces concomitantly the available time for accel-
eration or deceleration. This decreases the mechanical
power that can be produced in gait because power is the
product of moment and joint angular velocity. Consider-
ing that gait speed is dependent on the power generated
or absorbed at each joint, it is understandable that ROM
has an important influence on gait. Moreover, ISCI per-
sons with reduced ROM will need to increase their ef-
fort to walk since moment of force is partially dependant
on body configuration. Reduced ROM in extension will
impact more on the stance phase parameters whereas re-
duced ROM in flexion will be more cumbersome during
the swing phase of gait. However, decrease ROM in spe-
cific joints and directions can have beneficial influence
in gait. For example, there is some evidence that an equi-
nus contracture at the ankle that reduces the magnitude
in dorsiflexion can be used to substitute for weak calf
muscles and help to stabilise the knee during the stance
phase of gait (Siegler et al., 1984; Perry et al., 1993;
Nadeau et al., 1997). Further studies will need to clarify
the role of ROM as a determinant of gait in ISCI.
Posture Impairment during Walking
Lower limb motions generally did not show consistent
patterns of postural adaptation in ISCI subjects (Leroux
et al., 1999). Rather, a spectrum of postural adaptation
was found and ranged from a near normal to an adapta-
tion involving mainly the hip joint. Increasing the tread-
mill slope from 0 to 15 degrees induced a gradual in-
crease in hip and knee flexion and in ankle dorsiflexion
from late swing through the stance phase in healthy sub-
jects. The vertical displacement of the greater trochanter
is quite stable across the different grades for healthy con-
trols but not for ISCI subjects. This hip hiking was used
to compensate for the decrease of dorsiflexion during the
swing phase. Increasing the static slope from 0 to 15 de-
grees also induced a gradual increase in the amplitude of
 GAIT OF INDIVIDUALS WITH SPINAL CORD INJURY

electromyographic (EMG) activity of all muscles in a
healthy subject (gastronemii medialis activity increased
3.5 times the control value during push-off of level walk-
ing). In the ISCI subject, the amplitude of EMG activity
of thigh muscles (vastus lateralis and medial hamstring)
also increased during uphill walking, although to a lesser
extent than in normal subjects. Further, an increase in
slope is not associated with an increase in the amplitude
of EMG activity. For the tibialis anterior, the modulation
ranges from near normal to a complete absence of in-
creased activity during inclined walking. The absence of
increase in the level of activation of gastronemii medi-
alis likely results in a weak push off and compensatory
mechanisms from proximal segments might be used to
adapt to uphill walking. In fact, when comparing the ISCI
subjects with the healthy matched controls, they always
showed a greater forward inclination of both trunk and
pelvis during level and inclined walking (Leroux et al.,
2002). A more pronounced forward inclination was found
in ISCI subjects showing severe mobility dysfunctions as
measured by their walking speed. All the ISCI subjects
in that study seemed to adapt this anterior posture to
achieve greater stability during level and inclined walk-
ing. Results from frontal and transverse plane motions
revealed that ISCI subjects also used compensatory pos-
tural movements from trunk and pelvis to adapt to in-
clined walking However, the presence of large spectrum
of sensory and/or motor deficits and the relative small
number of subjects studied are among some limitations
of that study (Leroux et al., 2002).
EFFICACY OF TRAINING
Locomotor training has emerged as one of the evi-
dence-based clinical approaches that can be used to en-
hance recovery of posture and locomotion in stroke, ISCI
subjects and in many other neurological conditions. The
training strategies include modern task-specific ap-
proaches of motor learning such as training of walking
and balance in both feed-forward and feedback modes.
Several new approaches from animal studies, experi-
mental human studies, and phase I to phase III clinical
trials have been developed in the past two decades, such
as locomotor training on treadmill and on the ground us-
ing body weight support (BWS) (Wernig et al., 1998;
Barbeau et al., 1999a; 2001), muscle strengthening, func-
tional electrical stimulation (FES) (Wieler et al., 1999;
Ladouceur and Barbeau, 2000 a,b; Mirbagheri et al.,
2002), pharmacological approaches (Wainberg et al.,
1990; Barbeau et al., 1998; Remy-Neris et al., 1999), and
their combination (Fung et al., 1990) to enhanced recov-
ery in the neurological population particularly in ISCI
and stroke subjects. These individual approaches have
shown great potential and are different in the process of
validation in the rehabilitation setting. The findings have
been summarized in recent reviews (Barbeau et al., 1998;
Rossignol, 2000; Barbeau and Fung, 2001; Hesse et al.,
2003).
EMERGING REHABILITATION
CONCEPTS
Understanding the strategy that ISCI and stroke sub-
jects use can contribute to the development of new train-
ing concepts and principles that can be included in loco-
motor training paradigm and will be reviewed in the
following sections. This included the specificity of the
task, the importance and appropriateness of sensory in-
puts, challenging posture and walking adaptation, forced
reuse, and plasticity and permissiveness (Fig. 4).
Specificity of the Task
The importance and the specificity of training have
been shown in animal and human research studying mo-
tor performance. Similarly, fundamental studies in spinal-
ized cats have underlined the importance of training
specificity in the improvement of a task. It has been
shown that locomotor training and balance training are
in fact two different and specific tasks (Smith et al., 1982;
Barbeau and Rossignol, 1987). For instance, the maxi-
mal walking speed attained by cats trained to walk fol-
lowing spinalization is much higher than that of cats that
were only trained to stand. Such results can explain in
part why conventional rehabilitation approaches in hu-
mans with SCI or stroke is targeted towards enhancing
FIG. 4. Emerging concepts and approaches to consider in gait
training in individual with ISCI.

577
 BARBEAU ET AL.
stability of joints with bracing and reducing spasticity.
Studies have shown that rehabilitation of gait following
ISCI or stroke was improved when incorporating high
level of locomotor training, as compared to conventional
treatments suggesting once again that rehabilitation has
to include more training that is specific to the task (Bar-
beau, 2003). In contrast, recovery of balance during
standing has been shown in stroke subjects when trained
to shift their weight onto the hemiparetic side (Dickstein
et al., 1984). However, their balance during their walk-
ing capacity did not improve, outlining once again the
importance of task specificity. Therefore, findings show-
ing the rehabilitation approaches not specific to locomo-
tion such as passive stretching (Tremblay et al., 1990;
Brouwer et al., 2000; Crenshaw et al., 2000), acupunc-
ture, transcutaneous electrical nerve stimulation (TENS)
(Johansson et al., 2001), general home exercise (Mayo et
al., 2000) did not improve substantially functional loco-
motor outcomes, are not surprising.
Importance and Appropriateness of
Sensory Inputs
Sensory inputs play a crucial role in locomotor train-
ing following a lesion to the central nervous system
(CNS). For instance, there is strong evidence in animal
studies that suggest afferent inputs during hip extension
are involved in resetting and triggering the locomotor
rhythm (Forssberg et al., 1975; Rossignol, 1996). Addi-
tional evidence for the importance of sensory inputs is
that the modulation of reflexes is task and phase specific
in intact and spinalized cats as well as in normal and SCI
human subjects. For example, mechanical or electrical
stimulation of the paw or of the cutaneous nerve during
the flexor activity produced an increase in ipsilateral
flexor activities as well as the contralateral extensor ac-
tivity, but when the stimulus was delivered during the ip-
silateral extensor activity, it increased extensor activity
(Rossignol, 1996).
In human, electrical stimulation during the swing phase
increased the amplitude of the swing (Ladouceur and
Barbeau 2000) as well as increasing the walking speed
(Fig. 5).
Appropriate loading (loading and unloading) of hind
limbs is also a very important sensory input. This has
been possibly explained by an autogenic excitation rather
than an inhibition of afferent inputs from ankle exten-
sors. Although the mechanisms are still unclear, this ex-
citation could be due to the modulation of extensor load
receptors response likely arising from Golgi tendon or-
gans (Pearson, 1995). The importance of an appropriate
loading has also been shown in subjects with ISCI or
stroke subjects (Visintin and Barbeau, 1989; Visintin et
578
al., 1998). During walking with a BWS system, an ap-
propriate loading during the support phase enabled to en-
hance the extensor muscles activity as well as increase
the vertical force during the support phase. The FES of
the extensor muscle may also contribute to a better sup-
port phase (Fig. 5). An appropriate loading was also re-
sponsible for triggering swing phase in the contralateral
limb (Barbeau et al., 1992; Harkema et al., 1997; Wernig
et al., 1998). Therefore, the benefit of a locomotor train-
ing using BWS may depend partly on the degree of body
unloading during walking, but this needs further investi-
gation.
Sensory inputs may be necessary to shape the loco-
motor pattern not only for specific controls (step length,
foot placement) but also as an important sensory input
during the recovery process following a CNS insult.
Harkema et al. (2000) confirmed animal findings sug-
gesting that the critical issue for the recovery of gait af-
ter SCI is the ability of the spinal cord to interpret on-
going sensory input during walking in combination with
the intrinsic ability of neurons to execute oscillations in
flexor and extensor motor pools. From animal and hu-
man studies, it is clear that locomotor training cannot con-
sist only on putting the SCI and stroke subjects on a tread-
mill but depend on receiving the specific sensory input
associated with performance of a motor task (Barbeau,
2003). Appropriate sensory inputs such as (a) loading the
maximum weight on legs that the individual can bear
without losing balance, (b) avoiding (or minimize) weight
bearing on the arms and facilitating reciprocal arm swing,
(c) facilitating adequate head and trunk posture, (d)
achieving as normal as possible leg joints kinematics for
walking (such as hip and knee extension in terminal
stance), (e) promoting proper loading-unloading of limbs,
and (f) generating normal stepping velocities (0.75–1.25
m/sec) are necessary to optimize recovery (Barbeau et
al., 1999c; Harkema et al., 2000). The repetitive practice
of that task is also very important in order to optimize
the motor learning capacity of the spinal cord (Carr and
Shepherd, 1989; Visintin and Barbeau, 1994; Visintin et
al., 1998; Shepherd and Carr, 1999; Harkema et al.,
2000).
Challenging Posture and Walking Adaptation
During locomotor training, it is essential to incorpo-
rate higher demands in walking speed and posture in or-
der to increase the maximal walking speed (Ladouceur
and Barbeau, 2000b), decrease the energy demand
(Danielsson and Sunnerhagen, 2000; Ladouceur and Bar-
beau, 2000a; Macko et al. 2001), and change walking
aids (Ladouceur and Barbeau, 2000b). When training is
maintained at maximal speed, whereby both maximal
 GAIT OF INDIVIDUALS WITH SPINAL CORD INJURY

FIG. 5. Experimental data from two chronic SCI patients (S #1, S # 2) that illustrate the extent of locomotor recovery. The top
panel shows the progression of walking speed of a patient who first participated in the experimental trial of medication on the
walking behaviour. These trials were followed with the initiation of an FES-assisted walking training program. The FES ortho-
sis consist of the stimulation of both common peroneal nerves and is triggered by handswitches. Two points arise from this panel.
Firstly the subject was incapable of stepping independently before the first drug (clonidine). Secondly the subject remained in-
capable of overground walking during the drug study. It should be noted that the overground walking speed subsequently sur-
passed that on the treadmill, when training with FES, showing the highly nonlinear trend of the process of locomotor recovery.
The bottom panel represents the progression of maximal walking speed of a second chronic SCI patient who first participated in
a 12-week BWS training program with no changes in either his maximal overground or treadmill speed. Forty weeks after the
end of this therapeutic intervention, the walking speed had a minimal change and a program of FES-assisted walking was initi-
ated. He used a single channel of stimulation over the left common peroneal nerve triggered a flexion at the the beginning of the
swing.. As a result there was an increase in maximal walking speed over time. Concurrently, walking with different aids could
be achieved. The participant used a walker at the beginning of the training period, then started using forearm crutches after 2
weeks of FES training and was able to use two canes after 30 weeks of training (modified from Ladouceur et al. 1997).

movement of muscles and proper posture are challenged,
great clinical improvements of the locomotor perfor-
mance can be observed (Fig. 5).
Whereas conventional training has shown minimal
change in walking speed in acute SCI and stroke patients,
a series of locomotor training studies have shown promis-
ing results. The severity of injury and the time since the
injury are, of course, key factors in the recovery of walk-
ing, and well-targeted task-specific approaches during
clinical trials have led to major improvement in walking
speed and functional recovery. In stroke subjects with a
low functional level, a combination of BWS and tread-
mill training challenging both the posture and the walk-
ing speed should be used whereas in stroke subjects able
to walk at higher speeds (0.4 and above) will gain from
BWS plus treadmill training combined to overground
training that will challenge both walking speed and bal-
ance (Nilsson et al., 2001; Pohl et al., 2002; Sullivan et
al., 2002). The outcomes are in fact better when subjects
are challenged at their fastest walking speed (Pohl et al.,
2002; Sullivan et al., 2002). Challenges in walking and
balance should be a prerequisite for fundamental changes,
but these challenges should also be proportional to the
severity of the patient’s functional limitations. For sub-

579
 BARBEAU ET AL.
jects with no locomotor capabilities at the beginning of
training, or those needing maximal assistance to move
their lower limbs at fast speeds, the use of BWS and
treadmill training could allow them to repeat a gait-like
motion (Behrman and Harkema, 2000). Results from a
recent randomized clinical trial funded by the National
Institutes of Health (NIH) will address this question
(Dobkin et al., 2006). The recent development of differ-
ent gait trainers, which allow wheelchair-bound stroke
and SCI subjects to practice repetitive gait-like move-
ments without overstraining therapists, showed great po-
tential, but this approach is only at the beginning of the
validation process (Colombo et al., 2000; Hesse et al.,
2000; Volpe et al., 2000).
Locomotor training with BWS and FES also induces
improvements of the walking speed in chronic stages of
injuries to the CNS. Such improvements were shown by
Ladouceur et al. (1997) and are illustrated in Figure 5.
Comparisons of the results from different studies (Bar-
beau et al., 1998; Visintin et al., 1998; Kosak and Red-
ing, 2000; Rossignol, 2000; Lennon et al., 2002; Pohl et
al., 2002; Sullivan et al., 2002; Dobkin et al., 2006) show
that when the training process was started early on stroke
and ISCI subjects, greater functional benefits resulted
from the training. However, significant clinical im-
provement could also be observed during the chronic
stage of recovery (Sullivan et al., 2002).
The combination of locomotor training with FES dur-
ing the chronic phase of recovery significantly improve
the maximal walking speed of ISCI subjects. The changes
were described in two typical ASIA C SCI subjects with
an initial maximal speed ranging between 0 and 0.25
m/sec (Ladouceur and Barbeau, 2000b) (Fig. 5).
Forced Reuse
One advantage of using assistive walking devices in
the rehabilitation of gait in stroke or ISCI subjects is that
it allows the expression of the locomotor behavior when
possible. However, it has the disadvantage to cause over-
compensation and limit the adaptive capacity of the
locomotor behavior. Therefore, locomotion must be
achieved early in the recovery process using strategies
that minimize compensation and progressively challenge
the subjects in order to induce adaptation of the behav-
ior. For instance, the use of BWS will allow the expres-
sion of locomotion, and a progressive decrease of the
weight support over the training period will force the sub-
jects to reuse the paretic leg because they cannot com-
pensate with the non-paretic leg. Such an approach has
been tested for upper extremities by constraint therapy to
force the use of the arm and hand (Taub and Morris,
2001).
580
A forced-use therapy approach in stroke and SCI sub-
jects, especially those presenting asymmetries in their
lower limb walking pattern, has been a part of the train-
ing process for lower limb recovery. In chronic ISCI sub-
jects walked on a treadmill with no BWS and holding
onto parallel bars, the subjects clearly compensates with
his upper extremities by pushing down on the bars, and
by using mostly the less affected lower limb. Lower limb
kinematics showed that plantarflexion in the left limb
(less affected) increased at the end of stance, whereas
swinging of the right leg (more affected) was produced
with a minimal amount of hip, knee, and ankle flexion
(Barbeau, 2003). When subjects walked with BWS (40%)
and held onto the parallel bars, little changes were ob-
served in the walking pattern and compensation still oc-
curred in the upper extremities and the less affected lower
limb. Subsequently, while maintaining the BWS at 40%,
the subjects released the parallel bars and a gait pattern
closer to normal emerged, characterised by an appropri-
ate swing phase with flexion at the hip, knee, and ankle,
and better defined bursts of activity of the tibialis ante-
rior and other lower limb muscles similar in many as-
pects to the normal pattern. Based on these results, it
seems that walking aids can limit the recovery of gait
during early training, even though they are necessary for
locomotion. Therefore, strategies other than assistive
walking devices, such as BWS, should be part of a lo-
comotor training process because they are permissive for
the expression as well as the adaptation of the gait be-
havior (Barbeau, 2003).
Plasticity and Permissiveness
As it was previously seen, BWS and/or FES, can en-
hance the recovery of walking when combined with lo-
comotor training (Visintin and Barbeau, 1989; Visintin
et al., 1998; Ladouceur and Barbeau, 2000b; Barbeau et
al., 2002), and therefore are viewed as permissive strate-
gies. Also drugs can be permissive factors for the ex-
pression of the walking behaviour in SCI and stroke sub-
jects, as well as in other neurological populations.
Results from animal studies have revealed that some
drugs replacing neurotransmitters from descending sys-
tems (for example replacing noradrenaline [NA] by the no-
radrenergic agonist clonidine), when combined with loco-
motor training could promote a faster recovery of walking
(Barbeau et al., 1998). The fact that improvement of walk-
ing is maintained following termination of the drugs, in-
dicate that neural system changes have occurred in the
spinal cord caudal to the transaction. This type of plastic-
ity may possibly to to take place in human as well.
Interestingly, clonidine, for instance, has been shown
to also induce limited walking in chronic SCI subjects
 GAIT OF INDIVIDUALS WITH SPINAL CORD INJURY
(Norman et al., 1998; Remy-Neris et al., 1999). Follow-
ing partial recovery, the locomotor pattern was main-
tained even after decreasing clonidine. Ladouceur et al.
(1997) showed that when clonidine treatment was given
during locomotor training using BWS, the recovery of
walking was greatly enhanced (Fig. 5A). Chronic ISCI
subjects who could not walk or stand with full weight-
bearing were able to walk very slowly on the treadmill
with some of their weight supported, but the pattern of
walking was quite abnormal. Continued locomotor train-
ing but now with additional FES further supported inde-
pendent walking on treadmill and on ground and the
walking speed increased to a range from 0.50 m/sec (Fig.
5A) up to 0.80 m/sec (Fig. 5B). Better trunk alignment
was observed along with increased hip extension, a de-
creased knee flexion in early and mid stance at the end
of stance, a better weight acceptance, and flat position-
ing of the foot at floor contact. The medication seems to
allow a limited expression of a locomotor pattern (per-
missive), which is refined using appropriate sensory-mo-
tor training with FES (another permissive situation). This
results in an overall improvement of the walking and pos-
tural performance.
CONCLUSION
A more comprehensive and integrative approach in the
development of rehabilitation strategies will be possible
from understanding the effects of new treatment ap-
proaches. Such approaches include locomotor training on
treadmill and/or overground, use of BWS and/or FES,
and pharmacological interventions. These approaches can
be used alone or combined with others to maximize gain
in locomotor and balance performance. The development
of new rehabilitation approaches must take into account
the time since injury and the severity of injury. The iden-
tification and understanding of determinant variables that
are important to properly treat neurological populations
depends upon the understanding of the basic mechanisms
of adaptation in locomotion and posture. Findings in an-
imals and humans have led to new rehabilitation princi-
ples and should be recognized as important concepts in
neuroplasticity, which can impact motor learning and re-
habilitation. Finally, the effectiveness of such new ap-
proaches should be demonstrated by robust and well-de-
signed randomized clinical trials.
The integration of areas of basic development pro-
moting plasticity and permissivity (such as pharmaco-
logical manipulations, growth factors, neuronal gene
therapy, immunisation, cell transplantation, and many
others) have already shown a great potential to induce
functional recovery in animal studies. This integration of
581
new approaches is most likely the key for functional re-
covery of walking in humans with a neurological im-
pairment, such as individuals with SCI. Finally, the used
of spinal fMRI will eventually be able to diagnose spinal
cord damage by identifying the location and the degree
of impairment caused by injury.
ACKNOWLEDGMENTS
Many thanks to the Fonds de la Recherche en Santé
du Québec (FRSQ), the Jewish Rehabilitation Founda-
tion and La Fondation pour la Recherche sur la Moelle
Épinière. C.G. holds a research training grant, and S.N.
holds a Junior II investigator award from the FRSQ.
Many thanks to Dr. Joyce Fung for her helpful comments
on the manuscript.
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Address reprint requests to:
Dr. Hugues Barbeau
School of Physical and Occupational Therapy
McGill University
3630 Promenade-Sir-William-Osler
Montreal, Quebec, H3G 1Y5, Canada
E-mail: hugues.barbeau@mcgill.ca