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442 IEEE JOURNAL OF BIOMEDICAL AND HEALTH INFORMATICS, VOL. 17, NO.

2, MARCH 2013

Effect of Cadence Regulation on Muscle Activation


Patterns During Robot-Assisted Gait: A Dynamic
Simulation Study
Shahid Hussain, Sheng Q. Xie, Senior Member, IEEE, and Prashant K. Jamwal

Abstract—Cadence or stride frequency is an important param- also influences muscle coordination and the muscle activity gen-
eter being controlled in gait training of neurologically impaired erally increases with an increase in cadence [17]–[19].
subjects. The aim of this study was to examine the effects of ca- Several robotic orthoses [20]–[24] have been developed for
dence variation on muscle activation patterns during robot-assisted
unimpaired gait using dynamic simulations. A 2-D musculoskele- gait training of neurologically impaired subjects. These robotic
tal model of human gait was developed considering eight major orthoses kinematically constrain subject’s limbs; therefore the
muscle groups along with an existing ground contact force model. behavior of resulting gait dynamics and muscle activation pat-
A 2-D model of a robotic orthosis was also developed that provides terns is unclear [25]–[27]. Unfortunately, a limited number of
actuation to the hip, knee, and ankle joints in the sagittal plane to studies analyzing the effects of cadence regulation on mus-
guide subject’s limbs on reference trajectories. A custom inverse
dynamics algorithm was used along with a quadratic minimization cle activation patterns during robot-assisted gait training have
algorithm to obtain a feasible set of muscle activation patterns. been reported in literature. Electromyographic (EMG) activ-
Predicted patterns of muscle activations during slow, natural, and ity of healthy subjects has been recorded with no BWS during
fast cadence were compared and the mean muscle activations were LOKOMAT-assisted treadmill training at different gait speeds.
found to be increasing with an increase in cadence. The proposed No significant statistical difference in the magnitude of EMG
dynamic simulation provides important insight into the muscle ac-
tivation variations with change in cadence during robot-assisted has been reported for these variable speeds [25]. On the other
gait and provides the basis for investigating the influence of ca- hand, a similar study has been conducted with the LOKOMAT at
dence regulation on neuromuscular parameters of interest during different stride frequencies with variable BWS, which presents
robot-assisted gait. significant variance in the magnitude of EMG activity [26]. Ap-
Index Terms—Cadence, dynamic simulation, gait training, mus- parently, the question of how the robot-assisted gait training at
cle activation patterns, robotic orthosis. different cadence affects muscle activations still remains largely
unanswered. As has been stated earlier that cadence regula-
tion is important with regards to gait rehabilitation process; this
I. INTRODUCTION study is an attempt to investigate the effects of cadence regula-
tion on muscle activation patterns during the robot-assisted gait
EUROLOGIC injuries such as stroke and spinal cord in-
N juries cause muscle function impairments [1]–[3], spas-
ticity [4], [5], and produce changes in passive joint proper-
training.
Dynamic simulation of human gait is a useful tool for deter-
mining aspects of muscle functions and coordination patterns
ties [6]. The survivors have lower limb impairment and gait that are otherwise difficult or impossible to measure noninva-
disorders such as decreased endurance [7], reduced cadence or sively [28]–[34]. Dynamic simulations have been developed to
stride frequency [8], and asymmetric gait [9]. Body weight sup- analyze the effects of cadence regulation on muscle activations
ported (BWS) physical therapy has been used for more than during unassisted normal and impaired gait [19], [35], [36].
two decades for gait rehabilitation of these subjects [10], [11] However, results from dynamical simulations of robot-assisted
and has shown significant functional improvements [12], [13]. gait at variable cadence would be more appropriate in devising
Cadence or stride frequency has been identified as a key factor better gait rehabilitation protocols. Unfortunately, to the best
for the effectiveness of gait training on functional improvements knowledge of authors, no extant work on such studies is avail-
following a neurologic injury [14]–[16]. Variation of cadence able in the literature and the proposed work is a step toward
addressing this research question.
The objective of this study was to investigate the effects
of cadence regulation on muscle activation patterns during
Manuscript received April 26, 2012; revised August 7, 2012; accepted
October 22, 2012. Date of publication October 26, 2012; date of current version robot-assisted unimpaired gait. A dynamic simulation of robot-
March 8, 2013. This work was supported by the Auckland Medical Research assisted gait was produced to evaluate the muscle activation pat-
Council of New Zealand through the project titled “Intelligent robot assisted terns at slow, natural, and fast cadence. A 2-D musculoskeletal
gait rehabilitation” (project number: 3700987).
The authors are with the Department of Mechanical Engineering, The Univer- model of human gait was developed along with a 2-D model of
sity of Auckland, Auckland 1010, New Zealand (e-mail: shus045@aucklanduni. robotic orthosis. These models were used along with a custom
ac.nz; s.xie@aucklanduni.ac.nz; pjam025@aucklanduni.ac.nz). inverse-dynamics algorithm [27], [37] and a quadratic mini-
Color versions of one or more of the figures in this paper are available online
at http://ieeexplore.ieee.org. mization algorithm [38] to identify muscle activation patterns
Digital Object Identifier 10.1109/TITB.2012.2226596 at variable cadence, during robot-assisted gait. The information

2168-2194/$31.00 © 2012 IEEE


HUSSAIN et al.: EFFECT OF CADENCE REGULATION ON MUSCLE ACTIVATION PATTERNS DURING ROBOT-ASSISTED GAIT 443

Fig. 1. (a) Major muscle groups used in the musculoskeletal model. (b) Robotic orthosis leg model to guide subject’s limbs on reference trajectories (side view).

obtained from this simulation is important for proper elucida- (iliopsoas, IP), and Rectus Femoris (RF). The muscle attach-
tion of clinical studies involving robotic gait training orthoses, ment parameters were determined according to anatomical data
and to develop a better understanding of the effects of cadence reported in [39]. All the muscles were modeled as mass-less
regulation on muscle function. wires. The GCF was modeled as nonlinear viscoelastic spring
damper arrangement. The spring damper arrangement was po-
II. METHODOLOGY sitioned vertically at the heel and toe of each foot [40] and was
characterized according to the relation
A. Musculoskeletal Gait Model
A 2-D musculoskeletal model was developed for simulation Fz = az 3 (1 − bż) (2)
purpose. The body segments included in the model were trunk,
where z and ż were the vertical deformation and rate of vertical
thigh, shank, and foot. Trunk was included as a single rigid
deformation of heel and toe, respectively. The values of a and b
body to account for the upper extremity inertial parameters. The
were 0.25 × 109 N/m3 and 1.0 s/m, respectively [40].
segments were connected with revolute joints and the gait was
considered as purely sagittal [see Fig. 1(a)]. The model was
developed for a subject 1.78-m tall and weighing 77.9 Kg ac- B. Robotic Orthosis Model and Control
cording to the segment lengths and inertial parameters reported 1) Model: The purpose of a robotic orthosis in this study
in [39]. The dynamical equation of motion [32] was derived by was to guide subject’s limbs on reference trajectories. Each leg
Newton–Euler Principle and is given by of the robotic orthosis weighing 9.8 Kg was modeled as a double
    pendulum [41] with an additional shoe section [see Fig. 1(b)].
M1 (θ) θ̈ + C1 θ, θ̇ + G1 (θ) + R (θ) F M + F θ, θ̇ = 0 The robotic orthosis has revolute joints at hip, knee, and ankle
(1) to provide motion in sagittal plane. The orthosis joints were
where θ, θ̇, and θ̈ are vectors of generalized position, velocity, modeled to be in perfect alignment with musculoskeletal model
and acceleration, respectively. M1 (θ) is the system mass matrix, joints. The dynamics of robotic orthosis is given by
C1 is a vector of centrifugal and Coriolis torques, and G1 is  
the vector of gravitational torques. F M is a vector of muscle M2 (θ) θ̈ + C2 θ, θ̇ + G2 (θ) = Trob (3)
activations, R (θ) is the matrix of muscle moment arms, and
F (θ, θ̇) is a vector of ground contact force (GCF). where M2 (θ) is the orthosis mass matrix, C2 is a vector of
Eight major muscle groups of each leg were selected for sim- orthosis centrifugal and Coriolis torques; G2 is a vector of or-
ulation purpose in this study [see Fig. 1(a)]: soleus (SOL), gas- thosis gravitational torques. Trob is the vector of torque applied
trocnemius (GAS), tibialis anterior (TA), hamstrings (HAM), by robotic orthosis. The orthosis joint friction torques was not
vasti (VAS), gluteus maximus (GLU), uniarticular hip flexors modeled.
444 IEEE JOURNAL OF BIOMEDICAL AND HEALTH INFORMATICS, VOL. 17, NO. 2, MARCH 2013

The mass matrices, centrifugal, Coriolis, and gravitational 3) Inverse Dynamics: The kinematic parameters were com-
torques from musculoskeletal, and orthosis model ((1), (3)) were bined with all the forces and torques acting on the subject as
combined to form an integrated dynamic model of the system shown in (4) into a custom inverse dynamic model. This model
and is represented by was used to calculate the joint torques that the subject was gen-
    erating during the gait cycle (GC), as well as the torques induced
M (θ) θ̈ + C θ, θ̇ + G (θ) + F θ, θ̇ − Trob by the robotic orthosis on the subject’s joints. This method has
also been used for LOKOMAT in [27] and [37].
= R (θ) F M = Tj (4)
where M , C, and G are the combined terms for robotic orthosis C. Optimization
and subject. The maximum joint ranges of motion were kept
under anatomical constraints by the orthosis torques. Tj is the Joint motions in the human body are achieved by the antago-
human joint torque vector. The integrated dynamic model in nistic activation of group of skeletal muscles. Fundamentally to
(4) was formed such that the robot applied torques Trob were actuate a joint, coordinated action of tension and compression
subtracted from the other matrices in order to calculate the activations in the muscles is required. However, the skeletal
human joint torque vector Tj . The robotic orthosis torques at muscles are flexible and cannot provide compressive forces.
hip, knee, and ankle joint was produced by the antagonistic Owing to this limitation, joint motions with requisite torques
actuation of pneumatic muscle actuators (PMA) [see Fig. 1(b)]. are required to be realized by the application of positive ac-
For the purpose of this study, a three element dynamic model tivation vector. Interestingly, our musculoskeletal system has
of PMA developed by Reynolds et al. in [42] was used and is redundant number of muscles acting at the joints and, hence,
given by the null space solution of the muscle activations gets extra de-
grees of freedom that could be used efficiently to get positive
Mi ẍ + B (P ) ẋ + K (P ) x = Fce (P ) − Mg (5) muscle activations [46]. Due to redundant actuation, it is pos-
sible to obtain vectors of muscle activations comprising only
where x, ẋ, ẍ, are the amount of PMA contraction, contraction
tension forces to realize required torques at joints. Therefore,
velocity, and acceleration, respectively. Fce is the effective force
objective of the present optimization is to find a unique positive
provided by the contractile element, and K and B are spring
muscle activation vector from redundant solution space.
and damping coefficients, respectively. All these coefficients are
In previous research in the literature, it has been hypothe-
functions of pressure P . Mi is the inertial load and Mg is the
sized that the skeletal muscles follow optimality principle that
load due to the weight of the system. Readers are guided to [42]
further means that the muscles are activated in a manner so that
for the further details of the three element model of PMA.
minimum energy is consumed [31], [46]. Consequently, in most
2) Control: To guide the subject’s limbs on reference tra-
of the earlier works, the norm of muscle stresses/activations
jectories, a trajectory tracking controller (position controller)
has been minimized under the constraints that the activations
was implemented. Reference joint angle trajectories for slow
so obtained are able to provide required torque and lie within
(80 ± 6 steps/min), natural (105 ± 6 steps/min), and fast (120
given bounds [46], [47]. Nevertheless, in this study a different
± 6 steps/min) cadence reported by Winter in [43] were used.
approach was carried out wherein norm of the error in the target
An error was measured between the reference trajectory θref ,
torques (required torques) and the actual torques produced by
and the measured trajectory θ. The reference trajectory and the
our optimized activation solution has been minimized. Quadratic
measured trajectory were numerically differentiated to find joint
minimization algorithm was used to optimize muscle activations
velocities. A proportional derivative (PD) feedback controller
while constraining it between two bounds [38]. Since the muscle
generates the torque necessary to guide the subject’s limbs on
activation vector was required to be positive, the lower bound
these reference trajectories. The controller was implemented in
was kept at zero. Upper bound values of the muscle activations
joint space and is represented by
(fm ax ), on the other hand, were proportional to the physiologi-
Trob = [KP + KD s] . (θref − θ) (6) cal cross-sectional area (PCSA) and were calculated separately
for individual muscle using (7). The optimization problem was
where KP and KD are the proportional and derivative controller formulated as below
gains, respectively, and s is referred to as the Laplace operator
[44]. The proportional and derivative gains for each joint were Minimize norm (R × F M − Tj ) (7)
obtained manually. The process included first increasing the ⎡ ⎤
proportional gains stepwise and then derivative gains of each n1 f1
joint to minimize the trajectory tracking error while holding ⎢n f ⎥
⎢ 2 2⎥
the feedback gains at all other joints to zero. The KP and KD M ⎢ ⎥
where F = ⎢ n3 f3 ⎥
gains used for the hip, knee, and ankle joints are 25 and 4, ⎢ ⎥
⎣ | ⎦
31 and 2, 3 and 0.5, respectively. The advanced assist-as-needed
[21] or patient-cooperative [45] gait training strategies were not ni fi
included in the present simulation study. A similar method of subject to 0 ≤ F M ≤ fm ax
operating the LOKOMAT in pure position control mode for
studying muscle activations has also been used in [25]–[27]. where fm ax = .ni .
HUSSAIN et al.: EFFECT OF CADENCE REGULATION ON MUSCLE ACTIVATION PATTERNS DURING ROBOT-ASSISTED GAIT 445

Fig. 3. Hip, knee, and ankle joint angles of the subject with respect to %GC
during slow, natural, and fast cadence.

ysis purpose. All the simulations were performed by imple-


menting appropriate models in Matlab-Simulink R2009b, us-
ing fourth-order Runge–Kutta algorithm (The MathWorks, Inc:
Fig. 2. Stick diagram of the simulated robot-assisted locomotion (traced every Natick, Ma, USA). The frame rate of simulation was set at
10% of GC): (a) Slow cadence. (b) Natural cadence. (c) Fast cadence. 100 Hz. Data from the right GC were formatted for presentation
purpose.
F M is the vector of muscle activations (f1 , f2 , . . . , fi )
wherein multipliers n1 , n2 , . . . , ni were used to account for III. RESULTS
the muscle PCSA. It was assumed that the muscle endurance The lower extremity sagittal plane joint angles, joint torques,
is proportional to its PCSA [47]. The muscle PCSA reported GCF, and muscle activation patterns were monitored during the
by Friederich et al. were used in this study [48]. Where  is a simulations.
constant of proportionality and is given by  = 0.7 × 106 N/m2
according to [47]. A. Gait Dynamics
1) Perturbation Analysis: Subsequently, a perturbation anal-
1) Kinematics: Fig. 2(a)–(c) shows the stick diagrams of the
ysis was carried out to analyze the sensitivity of the skeletal
simulated locomotion at slow, natural, and fast cadence as a per-
muscle activation solution vector for changes in joint torques.
centage of GC. The tracked sagittal plane joint angle trajectories
In this analysis, 200 perturbations ranging between −5% and
θ for hip, knee, and ankle at three different cadences as a per-
+5% (magnitude of joint torque values) were applied to the
centage of GC are shown in Fig. 3 with mean values recorded in
natural hip joint torque and their effect on the optimization ap-
Table I. The robotic orthosis generated appropriate joint torques
proach, providing the muscle activation vector, was observed
to guide the subject’s limbs on the reference trajectories. A PD
and analyzed.
controller was selected to minimize the deviations from desired
trajectory by developing corrective torques. The maximum hip
D. Simulation joint angles during slow, natural, and fast cadence were 19◦ , 22◦ ,
Dynamic simulations of robot-assisted gait at variable ca- and 21o , respectively, and occurred during the terminal swing
dence were performed. Initial conditions of the simulation had phase (88% GC) (see Fig. 3). For knee joint the maximum an-
the model in quite standing posture. Initial step was performed gles for slow, natural, and fast cadence were 63◦ , 65◦ , and 67◦ ,
by the right foot. The duration of the simulation was set to respectively, and occurred during the initial swing phase (72%
complete eight GC. First step from initial standing posture was GC) (see Fig. 3). For ankle joint the maximum plantar flexion
eliminated and the remaining seven GC were utilized for anal- during slow, natural, and fast cadence was 18◦ , 19◦ , and 20◦ ,
446 IEEE JOURNAL OF BIOMEDICAL AND HEALTH INFORMATICS, VOL. 17, NO. 2, MARCH 2013

TABLE I
MEAN KINEMATIC AND KINETIC MEASURES

Fig. 4. Vertical GCF normalized to system mass for slow, natural, and fast
cadence with respect to %GC.
Fig. 5. Torques (N·m/kg) at hip, knee, and ankle joint during slow, natural,
and fast cadence.
respectively, and occurred during initial swing phase (66% GC)
(see Fig. 3). The maximum trajectory tracking error for hip,
knee, and ankle joint at all three cadences was always within
±4◦ across the GC. GC at three cadences (see Fig. 5). The observable difference in
2) Kinetics: The vertical GCF normalized to the total mass magnitude of ankle joint torques at three cadences was during
of the system is shown in Fig. 4. The GCF model did not pro- the terminal stance and preswing phases. During the terminal
duce the familiar double hump pattern although the weight- stance phase the magnitude of ankle joint torques at slow and
acceptance hump is more pronounced as compared to the sec- natural cadence was greater as compared to fast cadence. During
ond hump. This may had happened due to the external push the preswing phase the magnitude of ankle joint torque becomes
off provided by the robotic orthosis. The magnitude of GCF greater at fast cadence as compared to slow and natural cadence.
increased with the increase of cadence (see Table I) while the There was no observable difference in the magnitude of ankle
weight acceptance hump appeared approximately at the same joint torques during the swing phase at all three cadences.
time for all three cadences. 3) Robot Induced Torques: The torques induced by the
The sagittal plane limb joint torques for slow, natural, and fast robotic orthosis at the sagittal plane hip, knee, and ankle joints
cadence in terms of %GC are shown in Fig. 5 with mean absolute of the subject at three cadences throughout the GC are shown in
values provided in Table I. For all three cadences, hip joint Fig. 6. At the hip joint the robotic orthosis-induced torque has
torques follow quite similar pattern throughout the GC, with same patterns at all three cadences but higher magnitude torques
an increase in magnitude with increasing cadence. Although at slow and natural cadence were induced as compared to fast
the increase in hip joint torque from slow to natural cadence cadence during the loading and initial swing phases (see Fig. 6).
was small, the increase in joint torque at fast cadence torque The magnitude of induced hip torques at slow, natural, and fast
was more significant particularly, during the terminal stance cadence was quite similar during the rest of stance, initial, and
and preswing phases (40–60% GC) (see Fig. 5). For knee joint terminal swing phases. At the knee sagittal plane joint the robot
the torque patterns were quite similar throughout the GC at all orthosis induced torques also followed the same pattern at all
three cadences with an increase in magnitude from slow to fast three cadences (see Fig. 6). The magnitude of torque induced at
cadence. The most significant difference in knee joint torques knee joint increased during loading and terminal swing phases
at three cadences was during the loading and midstance phases at slow and natural cadence as compared to fast cadence while
(5–20% GC), during which the torque magnitude at fast cadence during rest of the GC the magnitude of torques remained ap-
becomes twice as compared to the torque at natural cadence (see proximately same at all three cadences. For ankle joint, the robot
Fig. 5). There was no considerable difference in magnitude of induced torques also followed the same pattern and there was no
knee joint torques during swing phase at all three cadences. The considerable difference among the magnitude of these torques
ankle joint torques follow similar pattern during the complete at all three cadences (see Fig. 6).
HUSSAIN et al.: EFFECT OF CADENCE REGULATION ON MUSCLE ACTIVATION PATTERNS DURING ROBOT-ASSISTED GAIT 447

same during the major phase of GC except during the loading


and terminal swing phases during which the magnitude at fast
cadence was greater than the magnitude at slow and natural ca-
dence. The mean activations of the muscle for the complete GC
are shown in Fig. 8. The mean activations of HAM, RF, GLU,
IP, SOL, and TA increased with cadence. However, the cadence
variation had no significant effect on the mean activations of
VAS and GAS.
1) Perturbation Analysis: The results of perturbation anal-
ysis are illustrated in [see Fig. 9(a) and (b)]. Muscle activa-
tions obtained by inducing perturbation in the joint torques [see
Fig. 9(a)] are displayed. Apparently, variations in the muscle
activations [see Fig. 9(b)] were of the same order as of the per-
turbations. Further, as the perturbed activation values changed
around the nominal activation values, the optimization method
was robust against perturbations in the joint torque values. An-
other important inference drawn from these illustrations was
that, since there were no extreme variations observed in the per-
turbed activation vector, the optimization method was able to
provide a unique solution of muscle activations for given joint
torques.

IV. DISCUSSION
Fig. 6. Torques induced by the robotic orthosis at hip, knee, and ankle joints
during slow, natural, and fast cadence. The objective of this study was to investigate the effects of
cadence regulation on muscle activation patterns during robot-
assisted unimpaired gait. Dynamic simulations of robot-assisted
B. Muscle Activation Patterns gait at three different levels of cadence were performed. Analy-
Normalized activation patterns of eight major muscle groups sis of these simulations showed an overall increasing trend in the
produced during robot-assisted gait at slow, natural, and fast mean muscle activations with an increase in cadence. It should
cadence throughout the GC are illustrated in Fig. 7. These opti- be stressed that there was an increase in the activations of VAS
mized muscle activities reproduced the joint torques. Hip, knee, and GAS with walking speed (see Fig. 7), however the differ-
and ankle torques were reproduced with an RMS error of the ences were not statistically significant (see Fig. 8). Also the hip
order of 10−32 N·m/kg. For most part of the GC, the muscle extensors and ankle plantar flexors showed a phase change in
activation patterns are quite similar for all three cadences al- muscle activations with change in cadence.
though a small phase variation was observed in the activity of The muscle coordination patterns during robot-assisted gait
ankle plantar flexors (40–60% GC) and hip extensors (10–25% at variable gait speeds have also been studied earlier. A study
GC). HAM activity magnitude generally increased with an in- conducted by Hidler and Wall on healthy subjects has shown no
crease in cadence and showed a higher activity during loading significant difference in EMG patterns of LOKOMAT-assisted
and terminal swing phases at fast cadence as compared to slow gait at different walking speeds while no body weight support
and natural cadence. GLU showed similar activation patterns as has been provided [25]. Another study conducted by Klarner
of HAM although the magnitude of GLU activation patterns is et al. on healthy subjects to examine the effects of variable stride
a bit lower than the HAM activation patterns. RF activity also frequency and BWS during LOKOMAT-assisted gait has shown
increased with an increase in cadence. The most considerable a decrease in EMG intensity with an increase in stride frequency
difference in RF activity magnitude was during the loading and and BWS [26]. The results from our simulation showed an
mid stance phases during which the magnitude of muscle ac- increase in mean muscle activations with an increase in cadence
tivation at fast cadence was nearly twice as compared to the with no BWS.
magnitude at slow and natural cadence. Magnitude of IP activ- The decrease in EMG intensity reported by Klarner et al. [26]
ity at fast cadence was greater than slow and natural cadence may have resulted due to the additional bias of BWS on variable
during the midstance phase. The magnitude of IP activity during stride frequency that was not considered in this study. On the
initial swing phase was greater for slow and natural cadence as other hand, the invariance of EMG magnitude with change in
compared to fast cadence. Magnitude of GAS and SOL also walking speed reported by Hidler and Wall may have happened
remained same throughout the GC at all three cadences but a due to the narrow range of walking speeds used in this study [25].
small increase was observed during the terminal stance phase To make the difference in muscle activation magnitudes more
at fast cadence. The magnitude of VAS activity also increased pronounced at different cadences, a wider range of cadence was
at fast cadence during the midstance phase as compared to slow used in this study. The increase in mean muscle activations with
and natural cadence. The magnitude of TA activity remained an increase in cadence during robot-assisted gait (see Fig. 8) is
448 IEEE JOURNAL OF BIOMEDICAL AND HEALTH INFORMATICS, VOL. 17, NO. 2, MARCH 2013

Fig. 7. Muscle activation patterns for a GC at slow, natural, and fast cadence. Abbreviations: Hamstrings (HAM), rectus femoris (RF), gluteus maximus (GLU),
uniarticular hip flexors (iliopsoas, IP), gastrocnemius (GAS), vasti (VAS), soleus (SOL), and tibialis anterior (TA).

The findings reported by Hidler and Wall [25] showed that the
muscle activation patterns during robot-assisted gait could be
significantly different from the unassisted normal gait. There-
fore, the statistical behavior of VAS and GAS activities (see
Fig. 8) reported in this study is not surprising and needs further
investigation.
The musculoskeletal gait and robotic orthosis model devel-
oped in this study was 2-D. Future work shall involve the
musculoskeletal and robotic orthosis model with hip abduc-
tion/adduction joints to facilitate the study of frontal plane mus-
cle activation patterns. It is important to mention here that most
Fig. 8. Mean activation patterns for a GC at slow, natural, and fast cadence.
of the available robotic orthoses do not provide actuation for
hip abduction/adduction motion [20], [21]. The robotic orthosis
was also operated in trajectory tracking mode and the advanced
in accordance normal unassisted gait. During normal gait the assist-as-needed [21] or patient-cooperative [45] gait training
magnitude of muscle activations generally increases with an in- strategies were not included in the present simulation study.
crease in cadence or stride frequency [17]–[19]. However, the A similar method of operating the LOKOMAT in trajectory
mean activations of VAS and GAS (see Fig. 8) were not sig- tracking mode for studying muscle activations has also been
nificantly affected by the variation in cadence. This finding is used in [26] and [27]. BWS was not applied during the pre-
contrary to the behavior of VAS and GAS activations during sented simulations as is commonly done during robot-assisted
normal unassisted gait [17]–[19]. A possible explanation of this gait training of neurologically impaired subjects. The reason
behavior is that there is a tight correlation between the walking for not applying BWS was that the BWS has also shown to
speed and muscle activations [25], [49]. The study conducted by alter the muscle activation patterns [26], [50], [51] and we did
Hidler and Wall [25] compared the EMG patterns during unas- not want to introduce any other biases that could potentially
sisted gait and LOKOMAT-assisted gait of healthy subjects. Hi- alter the behavior exhibited by walking in the robotic orthosis
dler and Wall [25] also reported higher muscle activation in the at variable cadence. Also other than the muscle activation con-
rectus femoris, vastus lateralis, and the gluteus muscle groups straints, the physiological muscle properties were not included
during LOKOMAT-assisted gait than during unassisted normal in the musculoskeletal model because the muscle physiology
gait, while there have been often less activation in the gastrocne- has a small effect on the characteristics of static optimization
mius, adductor longus, and TA during LOKOMAT-assisted gait. solutions [31], [52].
HUSSAIN et al.: EFFECT OF CADENCE REGULATION ON MUSCLE ACTIVATION PATTERNS DURING ROBOT-ASSISTED GAIT 449

closer to the skin [54]. Due to the aforementioned reasons and


the availability of the reliable EMG data only for superficial
muscles, we could not validate the muscle activations obtained
from the dynamic simulations developed in this study with the
EMG signals recorded during robot-assisted gait.
Although only a trajectory tracking controller was imple-
mented in this study, these dynamic simulations can also be
used to study the muscle activation patterns of subjects walk-
ing in the robotic gait training orthoses during advance assist-
as-needed [21] or patient-cooperative [23], [45] gait training
strategies such as impedance control [55]. The role of advance
assist-as-needed robotic gait training strategies is still under in-
vestigation in context of motor function recovery [21].

V. CONCLUSION
Cadence or stride frequency is an important clinical param-
eter for the gait rehabilitation of neurologically impaired sub-
jects. The variation of cadence also affects the muscle activa-
tion patterns. The dynamic simulation developed in this study
provides detailed knowledge of effects of cadence regulation
on muscle activation patterns during robot-assisted unimpaired
gait. According to authors’ best knowledge the dynamic simu-
lations of robot-assisted gait at variable cadence have not been
reported in literature. Although the muscle coordination patterns
and gait kinematics and kinetics for different cadences during
robot-assisted gait can be measured, dynamic simulations pro-
vide a tool to quantify how individual muscle function varies
with change in cadence. The proposed dynamic simulation pro-
vides important insight into the muscle activation variations with
change in cadence during robot-assisted gait and provides the
basis for investigating the influence of cadence regulation on
various neuromuscular parameters of interest during the robot-
assisted gait training.
Fig. 9. (a) Perturbation torques at hip joint during natural cadence. Blue and
red curves show a +5% and −5% perturbation, respectively. A small window
shows the perturbation torques during 50–60% of GC. (b) Hip joint muscle
activations produced in response to the perturbations.
REFERENCES
[1] S. J. Olney and C. Richards, “Hemiparetic gait following stroke. Part I:
Characteristics,” Gait Posture, vol. 4, pp. 136–148, 1996.
[2] A. Lamontagne, C. L. Richards, and F. Malouin, “Coactivation during gait
It is problematic and difficult to validate the muscle activa- as an adaptive behavior after stroke,” J. Electromyogr. Kinesiol., vol. 10,
tion patterns with the EMG signals recorded during the robot- pp. 407–415, 2000.
assisted gait. Some of the reasons include the poor placement [3] J. M. Hidler, M. Carroll, and E. H. Federovich, “Strength and coordination
in the paretic leg of individuals following acute stroke,” IEEE Trans.
of EMG surface electrodes in conjunction with robotic ortho- Neural Syst. Rehabil. Eng., vol. 15, no. 4, pp. 526–534, Dec. 2007.
sis that may not provide the reliable EMG activities of some [4] D. M. Corcos, G. L. Gottlieb, and R. D. Penn, “Movement deficits caused
muscle groups for validation purpose. The relative movement by hyperexcitable stretch reflexes in spastic humans,” Brain, vol. 109,
pp. 1043–1058, 1986.
of the robotic orthosis joints with subject’s joints also creates a [5] I. Black, D. Nichols, M. Pelliccio, and J. Hidler, “Quantification of reflex
shift in the robotic orthosis applied torques [53] that may not activity in stroke survivors during an imposed multi-joint leg extension
present the true picture of muscle activities. The rehabilitation movement,” Exp. Brain Res., vol. 183, pp. 271–281, 2007.
[6] S. G. Chung, E. Van Rey, Z. Bai, E. J. Roth, and L. Q. Zhang, “Biome-
engineering community is working toward the development of chanic changes in passive properties of hemiplegic ankles with spastic
robotic orthosis mechanisms that have better alignment with hypertonia,” Arch. Phys. Med. Rehabil., vol. 85, pp. 1638–1646, 2004.
the subject’s joints. The available robotic gait training orthosis [7] C. M. Dean, C. L. Richards, and F. Malouin, “Walking speed over 10 me-
tres overestimates locomotor capacity after stroke,” Clin. Rehabil., vol. 15,
such as LOKOMAT do not provide actuation to the ankle joint. pp. 415–421, 2001.
Therefore, the activity of some important muscles such as biar- [8] H. P. Von Schroeder, R. D. Coutts, P. D. Lyden, E. BillingsJr., and
ticular GAS, TA, and SOL cannot be compared with the EMG V. L. Nickel, “Gait parameters following stroke: A practical assessment,”
J. Rehabil. Res. Dev., vol. 32, pp. 25–31, 1995.
signals recorded during LOKOMAT-assisted gait [25]. More- [9] S. J. Olney, M. P. Griffin, T. N. Monga, and I. D. McBride, “Work and
over, the EMG recordings of some large muscles such as vastus power in gait of stroke patients,” Arch. Phys. Med. Rehabil., vol. 72,
medialis are not reliable as they are hidden by other muscles pp. 309–314, 1991.
450 IEEE JOURNAL OF BIOMEDICAL AND HEALTH INFORMATICS, VOL. 17, NO. 2, MARCH 2013

[10] A. L. Behrman and S. J. Harkema, “Locomotor training after human spinal [32] F. E. Zajac, “Understanding muscle coordination of the human leg with
cord injury: A series of case studies,” Phys. Ther., vol. 80, pp. 688–700, dynamical simulations,” J. Biomech., vol. 35, pp. 1011–1018, 2002.
2000. [33] F. E. Zajac, R. R. Neptune, and S. A. Kautz, “Biomechanics and muscle
[11] S. Hesse, C. Bertelt, M. T. Jahnke, A. Schaffrin, P. Baake, M. Malezic, coordination of human walking: Part I: Introduction to concepts, power
and K. H. Mauritz, “Treadmill training with partial body weight support transfer, dynamics and simulations,” Gait Posture, vol. 16, pp. 215–232,
compared with physiotherapy in nonambulatory hemiparetic patients,” 2002.
Stroke, vol. 26, pp. 976–981, 1995. [34] F. E. Zajac, R. R. Neptune, and S. A. Kautz, “Biomechanics and mus-
[12] Y. Laufer, R. Dickstein, Y. Chefez, and E. Marcovitz, “The effect of cle coordination of human walking: Part II: Lessons from dynamical
treadmill training on the ambulation of stroke survivors in the early stages simulations and clinical implications,” Gait Posture, vol. 17, pp. 1–17,
of rehabilitation: A randomized study,” J. Rehabil. Res. Dev., vol. 38, 2003.
pp. 69–78, 2001. [35] K. J. Agarwal-Harding, M. H. Schwartz, and S. L. Delp, “Variation of
[13] I. T. Da Cunha, Jr, P. A. Lim, H. Qureshy, H. Henson, T. Monga, hamstrings lengths and velocities with walking speed,” J. Biomech.,
and E. J. Protas, “Gait outcomes after acute stroke rehabilitation with vol. 43, pp. 1522–1526, 2010.
supported treadmill ambulation training: A randomized controlled pilot [36] M. D. Fox and S. L. Delp, “Contributions of muscles and passive dynamics
study,” Arch. Phys. Med. Rehabil., vol. 83, pp. 1258–1265, 2002. to swing initiation over a range of walking speeds,” J. Biomech., vol. 43,
[14] A. Lamontagne and J. Fung, “Faster is better. Implications for speed- pp. 1450–1455, 2010.
intensive gait training after stroke,” Stroke, vol. 35, pp. 2543–8, 2004. [37] J. Hidler and N. Neckel, “Inverse-dynamics based assessment of gait using
[15] K. J. Sullivan, B. J. Knowlton, and B. H. Dobkin, “Step training with a robotic orthosis,” in Proc. IEEE 28th Annu. Int. Conf. Eng. Med. Biol.
body weight support: Effect of treadmill speed and practice paradigms Soc., 2006, vol. 1, pp. 185–188.
on poststroke locomotor recovery,” Arch. Phys. Med. Rehabil., vol. 83, [38] J. J. Moré and G. Toraldo, “Algorithms for bound constrained quadratic
pp. 683–691, 2002. programming problems,” Numerische Math., vol. 55, pp. 377–400,
[16] M. Pohl, J. Mehrholz, C. Ritschel, and S. Rückriem, “Speed-dependent 1989.
treadmill training in ambulatory hemiparetic stroke patients: A random- [39] G. T. Yamaguchi, Dynamic Modeling of Musculoskeletal Motion – A Vec-
ized controlled trial,” Stroke, vol. 33, pp. 553–558, 2002. torized Approach for Biomechanical Analysis in Three Dimensions, 1st
[17] A. L. Hof, H. Elzinga, W. Grimmius, and J. P. K. Halbertsma, “Speed ed. Norwell, MA: Kluwer Academic Publishers, 2001.
dependence of averaged EMG profiles in walking,” Gait Posture, vol. 16, [40] K. G. M. Gerritsen, A. J. Van Den Bogert, and B. M. Nigg, “Direct dy-
pp. 78–86, 2002. namics simulation of the impact phase in heel-toe running,” J. Biomech.,
[18] A. R. den Otter, A. C. H. Geurts, T. Mulder, and J. Duysens, “Speed related vol. 28, pp. 661–668, 1995.
changes in muscle activity from normal to very slow walking speeds,” Gait [41] S. Jezernik, G. Colombo, and M. Morari, “Automatic gait-pattern adap-
Posture, vol. 19, pp. 270–278, 2004. tation algorithms for rehabilitation with a 4-DOF robotic orthosis,” IEEE
[19] R. R. Neptune, K. Sasaki, and S. A. Kautz, “The effect of walking speed Trans. Robot. Autom., vol. 20, no. 3, pp. 574–582, Jun. 2004.
on muscle function and mechanical energetics,” Gait Posture, vol. 28, [42] D. B. Reynolds, D. W. Repperger, C. A. Phillips, and G. Bandry, “Model-
pp. 135–143, 2008. ing the dynamic characteristics of pneumatic muscle,” Ann. Biomed. Eng.,
[20] G. Colombo, M. Joerg, R. Schreier, and V. Dietz, “Treadmill training of vol. 31, pp. 310–317, 2003.
paraplegic patients using a robotic orthosis,” J. Rehabil. Res. Develop., [43] D. A. Winter, The Biomechanics and Motor Control of Human Gait: Nor-
vol. 37, pp. 693–700, 2000. mal, Elderly and Pathological, 2nd ed. Waterloo,, Canada: University
[21] S. K. Banala, S. H. Kim, S. K. Agrawal, and J. P. Scholz, “Robot assisted of Waterloo Press, 1991.
gait training with active leg exoskeleton (ALEX),” IEEE Trans. Neural [44] B. C. kuo and F. Golnaraghi, Automatic Control Systems, 8th ed. Hobo-
Syst. Rehabil. Eng., vol. 17, pp. 2–8, 2009. ken, NJ: Wiley, 2002.
[22] J. F. Veneman, R. Kruidhof, E. E. G. Hekman, R. Ekkelenkamp, [45] R. Riener, L. Lunenburger, S. Jezernik, M. Anderschitz, G. Colombo, and
E. H. F. Van Asseldonk, and H. Van Der Kooij, “Design and evalua- V. Dietz, “Patient-cooperative strategies for robot-aided treadmill train-
tion of the LOPES exoskeleton robot for interactive gait rehabilitation,” ing: First experimental results,” IEEE Trans. Neural Syst. Rehabil. Eng.,
IEEE Trans. Neural Syst. Rehabil. Eng., vol. 15, no. 3, pp. 379–386, Sep. vol. 13, no. 3, pp. 380–394, Sep. 2005.
2007. [46] J. Ueda, D. Ming, V. Krishnamoorthy, M. Shinohara, and T. Ogasawara,
[23] S. Hussain, S. Q. Xie, and G. Liu, “Robot assisted treadmill training: “Individual muscle control using an exoskeleton robot for muscle function
Mechanisms and training strategies,” Med. Eng. Phys., vol. 33, pp. 527– testing,” IEEE Trans. Neural Syst. Rehabil. Eng., vol. 18, no. 4, pp. 339–
533, 2011. 350, Aug. 2010.
[24] W. E. I. Daisuke Aoyagi, S. J. Harkema, D. J. Reinkensmeyer, and [47] R. D. Crowninshield and R. A. Brand, “A physiologically based criterion
J. E. Bobrow, “A robot and control algorithm that can synchronously of muscle force prediction in locomotion,” J. Biomech., vol. 14, pp. 793–
assist in naturalistic motion during body-weight-supported gait training 801, 1981.
following neurologic injury,” IEEE Trans. Neural Syst. Rehabil. Eng., [48] J. A. Friederich and R. A. Brand, “Muscle fiber architecture in the human
vol. 15, pp. 387–400, 2007. lower limb,” J. Biomech., vol. 23, pp. 91–95, 1990.
[25] J. M. Hidler and A. E. Wall, “Alterations in muscle activation patterns [49] A. L. Hof, H. Elzinga, W. Grimmius, and J. P. K. Halbertsma, “Speed
during robotic-assisted walking,” Clin. Biomech., vol. 20, pp. 184–193, dependence of averaged EMG profiles in walking,” Gait Posture, vol. 16,
2005. pp. 78–86, 2002.
[26] T. Klarner, H. K. Chan, J. M. Wakeling, and T. Lam, “Patterns of muscle [50] L. Finch, H. Barbeau, and B. Arsenault, “Influence of body weight support
coordination vary with stride frequency during weight assisted treadmill on normal human gait: Development of a gait retraining strategy,” Phys.
walking,” Gait Posture, vol. 31, pp. 360–365, 2010. Therapy, vol. 71, pp. 842–856, 1991.
[27] N. D. Neckel, N. Blonien, D. Nichols, and J. Hidler, “Abnormal joint [51] V. Dietz, R. Müller, and G. Colombo, “Locomotor activity in spinal
torque patterns exhibited by chronic stroke subjects while walking with man: Significance of afferent input from joint and load receptors,” Brain,
a prescribed physiological gait pattern,” J. NeuroEng. Rehabil., vol. 5, vol. 125, pp. 2626–2634, 2002.
2008, doi: 10.1186/1743-0003-5-19. [52] F. C. Anderson and M. G. Pandy, “Static and dynamic optimization solu-
[28] K. M. Steele, A. Seth, J. L. Hicks, M. S. Schwartz, and S. L. Delp, “Mus- tions for gait are practically equivalent,” J. Biomech., vol. 34, pp. 153–161,
cle contributions to support and progression during single-limb stance in 2001.
crouch gait,” J. Biomech., vol. 43, pp. 2099–2105, 2010. [53] A. H. A. Stienen, E. E. G. Hekman, F. C. T. van der Helm, and H. van
[29] F. C. Anderson and M. G. Pandy, “Individual muscle contributions der Kooij, “Self-aligning exoskeleton axes through decoupling of joint
to support in normal walking,” Gait Posture, vol. 17, pp. 159–169, rotations and translations,” IEEE Trans. Robot., vol. 25, no. 3, pp. 628–
2003. 633, Jun. 2009.
[30] H. Geyer and H. Herr, “A muscle-reflex model that encodes principles of [54] T. S. Bae, P. Loan, K. Choi, D. Hong, and M. S. Mun, “Estimation of
legged mechanics produces human walking dynamics and muscle activi- muscle response using three-dimensional musculoskeletal models be-
ties,” IEEE Trans. Neural Syst. Rehabil. Eng., vol. 18, no. 3, pp. 263–273, fore impact situation: A simulation study,” J. Biomech. Eng., vol. 132,
Jun. 2010. pp. 121011-1–121011-7, 2010.
[31] M. G. Pandy, “Computer modeling and simulation of human movement,” [55] N. Hogan, “Impedance control: An approach to manipulation,” J. Dyn.
Annu. Rev. Biomed. Eng., vol. 3, pp. 245–273, 2001. Syst. Meas. Control, vol. 107, pp. 1–23, 1985.
HUSSAIN et al.: EFFECT OF CADENCE REGULATION ON MUSCLE ACTIVATION PATTERNS DURING ROBOT-ASSISTED GAIT 451

Shahid Hussain received the B.Sc. degree (Hons.) Prashant K. Jamwal received the Master’s of Tech-
in mechatronics and control engineering from the nology degree from I.I.T., Roorkee, India, and the
University of Engineering and Technology, Lahore, Ph.D. degree from The University of Auckland,
Pakistan, the M.E. degree in mechanical engineering Auckland, New Zealand.
from The University of Auckland, Auckland, New He is a Research Fellow in the Department of Me-
Zealand, in 2007 and 2009, respectively, and is cur- chanical Engineering, The University of Auckland.
rently working toward the Ph.D. degree from the De- He has more than 15 years of teaching and research
partment of Mechanical Engineering, The University experience in mechatronics, medical robotics, and
of Auckland. advanced manufacturing technologies. He is the As-
He is acting as a Reviewer for many international sociate Editor of International Journal of Biomecha-
journals and conferences. His research interests in- tronics and Robotics and is acting as a Reviewer for
clude compliant actuation of rehabilitation robots, robot-assisted gait rehabili- many international journals and conferences. He has also published numerous
tation, human–robot interaction, and nonlinear control of dynamic systems. papers in refereed international journals and conferences. His research interests
include artificial intelligence, fuzzy mathematics and applications, smart sensors
and actuators, biomechatronics, biomedical robotics, evolutionary algorithms,
and multiobjective optimization.

Sheng Q. Xie (SM’11) received the Ph.D. degrees


from the Huazhong University of Science and Tech-
nology, Wuhan, China, and University of Canterbury,
Ilam, New Zealand.
He is a Chair Professor in Biomechatronics in the
University of Auckland, New Zealand. He has more
than 17 years of teaching and research experience in
mechatronics and robotics. He is the editor of two
international journals, and is an editorial board mem-
ber and scientific advisory member for many inter-
national journals and conferences. He has published
more than 200 papers in refereed international journals and conferences. His
research interests include intelligent mechatronics systems, vision techniques
and applications, smart sensors and actuators, biomechatronics, and biomedical
robotics.

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