Clinical Biomechanics 16 (2001) 793±805

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A dynamical model of locomotion in spastic hemiplegic

cerebral palsy: in¯uence of walking speed
Sergio T. Fonseca a,*, Kenneth G. Holt b,c, Elliot Saltzman b,c,d, Linda Fetters b
a
Departamento de Fisioterapia, Universidade Federal de Minas Gerais, Av. Ant^ onio Carlos 6627,
Unidade Administrativa II, 3° andar, 270-010, Belo Horizonte, MG, Brazil
b
Department of Physical Therapy, Sargent College of Health and Rehabilitation Sciences, Boston University,
635 Commonwealth Ave., Boston, MA 02215, USA
c
Center for the Ecological Study of Perception and Action, University of Connecticut, Storrs, CT, USA
d
Haskins Laboratories, New Haven, CT, USA
Received 5 June 2001; accepted 6 July 2001

Abstract
Objective. The objective of this study was to assess the capability of an escapement-driven inverted pendulum with springs and
damping model to estimate the e€ects of impairments (e.g. spasticity, muscle weakness) on the dynamics and patterns of locomotion
of children with spastic cerebral palsy.
Methods. Kinematic data of six children with spastic hemiplegic cerebral palsy and six matched, typically developing children
were collected at ®ve di€erent self-selected overground walking speeds (`very slow' to `very fast'). Changes in forcing, sti€ness and
gravitational potentials were estimated during the stance phase of each leg according to the model's equation of motion.
Results. Signi®cantly greater sti€ness and decreased forcing was observed in the more a€ected limbs of children with spastic
hemiplegic cerebral palsy and compared to typically developing peers. The forcing term of the non-a€ected limb was greater than
that of the matched typically developing children.
Conclusions. Results support the claim that disabled individuals with losses in dynamic resources (sti€ness, muscle forcing ca-
pability) exploit and develop the remaining resources in their adapted gait patterns. It was suggested that clinical interventions
aimed at normalizing a gait pattern may be contraindicated, and that rehabilitation might be more e€ective if focused at the level of
dynamics.

Relevance
Pattern formation is seen as an optimal solution based on the individuals' action capabilities and dynamic properties under
environmental and task demands. This perspective could lead to the development of interventions that address these dynamic
variables with the objective of improving the functional capabilities of children with cerebral palsy. Ó 2001 Elsevier Science Ltd. All
rights reserved.

Keywords: Cerebral palsy; Locomotion; Oscillatory models; Dynamical systems

1. Introduction energy is conserved through exchanges between kinetic

Models of locomotion have been used to describe the
dynamics involved in activities such as walking and
running [1,2]. Walking dynamics have been described as
pendular with exchanges between gravitational potential
and kinetic energy [3,5]. On the other hand, running has
been described as a mass-spring system [5], in which
*
Corresponding author.
E-mail address: sfonseca@metalink.com.br (S.T. Fonseca).
0268-0033/01/$ - see front matter Ó 2001 Elsevier Science Ltd. All rights reserved.
PII: S 0 2 6 8 - 0 0 3 3 ( 0 1 ) 0 0 0 6 7 - 5
and elastic potential energies [3]. The individual with the
appropriate dynamic action capabilities (muscle
strength, body and segment masses and lengths, and
elastic soft tissue properties) can use them to become a
walker (pendulum) or runner (spring). Walking and
running are examples of how di€erent movement pat-
terns are utilized that take advantage of di€erent dy-
namic action capabilities to conserve energy during
locomotion [4].
We have begun a line of research into the dynamics of
locomotion for children with cerebral palsy (CP). It is
794 S.T. Fonseca et al. / Clinical Biomechanics 16 (2001) 793±805
our premise that the changes in dynamic action capa-
bilities that occur as a result of upper motor neuron
disease lead to predictable changes in movement pat-
terns. The patterns are both a direct re¯ection of the
available resources and adaptations that facilitate the
use of those resources. Features of spastic cerebral palsy
include increased co-contraction [6], hyperactive stretch
re¯exes [7], decreased muscle contractility [8], and in-
creased tendon to muscle length within a muscle [9]. The
di€erences due to the neurological impairment are sug-
gestive of a sti€er system, that might be potentially
better capable of conserving elastic energy. Weakness
and poor timing of muscle concentric contractions [10]
may result in a system that is capable of producing only
limited muscle power [11]. Movement patterns of chil-
dren with CP may be a re¯ection of strategies that ex-
ploit the changed dynamic action capabilities. For
example, during walking raising the center of mass
higher and dropping the body weight from an increased
height onto a plantar ¯exed foot would present a bio-
mechanically advantageous means to increase the load-
ing torque on a sti€ gastrocnemius-soleus muscle±
tendon complex. The leg could then rebound in the
manner of a pogo stick. Thus, the running pattern often
used to describe CP gait [12] would facilitate elastic
energy return just as it does in a typical running pattern
[4,5]. This interpretation would suggest that gait pat-
terns adopted by individuals with cerebral palsy are not
limitations but adaptations to the changed dynamics.
To investigate the proposed changes in the dynamic
action capabilities of children with spastic hemiplegic
CP a model is needed that captures the muscular con-
tractile forces that are generated during gait. It should
also capture the energy conservation that is accom-
plished by exchanges between potential and kinetic en-
ergy due to gravitational, elastic and inertial forces, and
any losses of energy due to less than perfect energy ex-
changes during locomotion. Our previous work has
shown promising results on modeling locomotion.
However, the study was limited only to the analysis of
the sti€ness of children with CP during locomotion at a
constant speed under varying stride frequencies [13]. The
purpose of the present study was to assess the capability
of a forced, inverted pendulum with springs and dam-
ping model to estimate expected di€erences in the
complete dynamics of locomotion (force, sti€ness, the
gravitational e€ect and their relative contributions) at
di€erent speeds in children with spastic hemiplegic CP
and to relate them to observed kinematic patterns. As
emphasized by Bernstein [14], the analysis of the dy-
namic reactive forces arising from the movement is es-
sential to the understanding of co-ordination.
Bernstein's perspective suggests that movements are not
completely determined by e€ector processes, but also by
the internal and external forces acting on the individual.
In this spirit, the present study examined the possibility
that the observed gait patterns in CP are alternative
functional solutions to the dynamic demands of con-
tinued locomotion.
2. Modeling locomotion as an autonomous inverted
pendulum system
Several investigators have applied the concept of
pendular motion to describe walking [1,15]. Walking has
been successfully modeled as a regular pendulum-spring
to predict the preferred locomotor frequency of typically
developing adults and quadrupeds [16,17]. Recently, an
escapement-driven, inverted pendulum with springs
model (EDIPS) with viscous damping was developed to
account for the dynamics of the stance phase [18]. The
following Newtonian equation of motion describes the
behavior of the model in which spring and damping
forces act horizontally, at a distance b from the origin,
and escapement forces act horizontally at a distance L
from the origin
mL2 hd ˆ Fd …hu ; h_u †L cos hu ch_u …b cos hu †
2
kb sin hu b cos hu mLg sin hd ; …1†
where hd is the angular displacement from downward
vertical, hu the angular displacement from upward ver-
tical, hu ˆ hd p, h_d ; hd the angular velocity and accel-
eration, m the mass of the system, L the equivalent
distance from the axis of rotation to the center of mass
of the body, k the system sti€ness, c the viscous dam-
ping, b the distance from the insertion of the spring and
damping forces to the axis of rotation (ankle), g the
acceleration due to gravity, and mL2 hd is the net inertial
moment of the system, mLg sin hd the restoring torque
due to gravity, kb sin hu cos hu the restoring torque due to
the elastic properties of the tissues, Fd …hu ; h_u †L cos hu the
escapement (state-dependent forcing), and ch_d b cos hu is
the moment due to damping (see Fig. 1).
Due to the presence of a dissipative term represented
by the moment due to damping, a forcing moment
acting on the center of mass is necessary to maintain the
oscillation. This state-dependent forcing behavior re-
sembles that of the escapement mechanism of a pendu-
lum clock, where a periodic input of energy is applied to
the system at an appropriate phase of the oscillation
[19]. Thus, in such an autonomous system, the instant of
energy input is uniquely determined by the motion of
the system. However, we need to estimate kb2 in order to
estimate, in turn, the escapement's forcing moment that
is applied during the phase from onset of push-o€ to the
end of toe-o€.
In normal walking, most of the power generated
during each cycle is produced during the push-o€ phase
of walking [11]. In this escapement system, as in normal
gait, the energy is assumed to be applied by the impul-
 S.T. Fonseca et al. / Clinical Biomechanics 16 (2001) 793±805 795

natural frequency of oscillation …x0 † of this system is

solely determined by its inertial and sti€ness character-
istics (spring and gravity). Rearranging Eq. (3) to cal-
culate the linearized natural frequency of the system's
oscillation we obtain
 2  2 
Fd …hu ; h_u †  cb _ kb mLg
ˆ hu ‡ hu ‡ hu ; …4†
mL mL2 mL2
where the natural frequency of oscillation …x0 † is
 2 
kb mLg
x20 ˆ : …5†
mL2
Applying the relationship between cycle period and
frequency of oscillation, the linearized natural period of
this inverted pendulum system can be de®ned as
 1=2
2p mL2
s0 ˆ ˆ 2p : …6†
x0 kb2 mLg
An important characteristic of the model's clock-like
behavior is that the system depends on a balance be-
tween the receipt and losses of energy, with the ampli-
tude of oscillation being proportional to the energy
input to the system [20]. In terms of locomotion, such a
model would predict, roughly, that the amplitude of
Fig. 1. Schematic representation of the escapement driven, damped,
inverted pendulum with spring model. m ± mass of the system, L ±
oscillation (or stride length) is directly proportional to
pendulum equivalent length, k ± spring sti€ness, c ± viscous damping, b the magnitude of forcing and inversely proportional to
± distance from the attached spring/damper to the axis of rotation, the amount of damping present, while the frequency of
Fd …h; h_ escapement, phase-dependent forcing. Inset shows the de®ni- oscillation is close to the system's linearized natural
tion for hu and hd . frequency.
An autonomous escapement driven oscillator will
sive leg when the support leg is close to vertical. Thus, show a fundamental frequency in its power spectrum
during this push-o€ phase the center of mass (inverted that can be taken to approximate the system's natural
pendulum) travels through a small angular range. Since frequency. If the mass and length of the pendulum are
at this point the amplitude of oscillation is small, the known, Eq. (6) can be rearranged to allow the calcula-
equation for the push-o€ phase can be simpli®ed tion of the systems' sti€ness
through a linear approximation about its equilibrium !
2 mL2
point at p and Eq. (1) can be rewritten as kb ˆ 2
‡ mLg: …7†
…s0 =2p†
mL2 hd ˆ Fd …hu ; h_u †L cb2 h_u kb2 …hd p† ‡ mLg…hd p†:
…2†
Considering that hu ˆ …hd p†, h_u ˆ h_d , hu ˆ hd , Eq. (2) 3. Model application to ordered and disordered movement
becomes
We use the EDIPS model to compare the dynamics of
mL2 hu ˆ Fd …hu ; h_u †L cb2 h_u kb2 hu ‡ mLghu : …3†
the involved and non-involved limbs of children with CP
(The maximum angular excursions from vertical during and non-impaired matched peers. In the model (Eq. (3)),
push-o€ were 18.5° (very fast speed), and 11.2° (slowest the mass of the pendulum …m† represents the mass of the
speed). We used the larger of the excursion values child and the length of the pendulum …L† represents the
(18.5°) to provide the most conservative estimate of the distance from the axis of rotation of the stance leg
approximation errors due to linearization. For the ap- (ankle) to the center of oscillation of the body. The mass
proximated terms in Eq. (1), these errors were 2% and length of the pendulum under the in¯uence of the
…sin hd  …hd p††, 5% …cos hu  1†, 11% …cos 2hu gravitational acceleration impart a gravitational mo-
 1†, 7% …sin qu cos qu  …qd p††.) ment …mLg† to the oscillating pendulum. The viscoelastic
In this inverted pendulum, the gravitational and properties of the connective tissues and muscles, as
elastic moments …mLghu ; kb2 hu † display opposite actions well as the increased sti€ness provided by co-contrac-
as they transfer moments from one to another. The tion, are represented by a spring of a given sti€ness
796 S.T. Fonseca et al. / Clinical Biomechanics 16 (2001) 793±805

…kb2 †. A viscous element (damping) is included to rep- The advantage of the inverted hybrid pendulum
resent the energy lost in each cycle. Finally, a forcing model is that it includes the major dynamic elements for
moment represents the muscular actions that periodi- locomotion. This allows the model to be used for
cally generate an accelerating moment on the center of walking, running or to be applied to describe the types
mass during push-o€. of gait seen in children with CP. Because the equation
In normal walking, two thirds of the total power can be satis®ed in a number of ways, di€erent gaits may
generated during each stride is provided by the ankle be produced by varying the elements' contribution (e.g.
extensors at the push-o€ phase of walking [11]. There- increased sti€ness).
fore, most of the periodically applied forcing moment is
generated at this phase in the cycle. The resulting net
inertial moment …mL2 h† summed during this propulsive 4. Model predictions
phase re¯ects the contribution of all elements in Eq. (3)
including the forcing moment and restorative torques. The dynamics of walking in children with CP have
Because kb2 can be calculated from Eq. (7) and mLg can been described as having running-like characteristics.
be estimated from anthropometric measures, the kine- Increased re¯ex activity, co-contraction, and changes
matic measures of angular acceleration of the center of in the mechanical properties of connective and mus-
mass can be used to calculate the net inertial moment. cular tissues would be expected to result in greater
This procedure allows the estimation of the forcing sti€ness and help provide the exchange between elastic
moment according to the following equation: and kinetic energies that characterizes this motion.
Because the elastic restoring torque …kb2 † of the model
X
n X
n X
n X
n X
n
Fd L ˆ mL2 hu ‡ cb2 h_u ‡ kb2 hu ‡ mLghu ; is a global measure of the system's sti€ness, this
iˆ1 iˆ1 iˆ1 iˆ1 iˆ1 variable should capture the increased sti€ness of the
…8† a€ected limb during the stance phase. Obusek et al.
[21] demonstrated a linear scaling between the gravi-
where n is the total number of sample periods between tational and the elastic restoring torque during leg
the beginning of plantar ¯exion (start of push-o€ phase) swing. As weight was added to the legs of adult sub-
and toe-o€ (end of push-o€ phase). jects, the measured leg sti€ness increased proportion-
If it is assumed that the damping coecient (cb2 ) ally. To avoid the e€ect of anthropometric di€erences
remains constant for a given subject, changes in the among children, a sti€ness to gravitational component
damping moment over time will be dependent only on ratio …kb2 =mLg†, instead of kb2 should provide a
the changes in angular velocity of the system. Dividing measure that can better di€erentiate relative sti€ness of
Eq. (8) by the summed angular velocity during the same children of di€erent masses and lengths. Increased
time period will produce a constant to be added to the sti€ness to gravitational component ratios are expected
forcing moment, according to the following: in the a€ected side of children with hemiplegic CP
Pn Pn Pn Pn compared to non-a€ected side and typically developing
2 2
iˆ1 Fd L 2 iˆ1 mL hu ‡ iˆ1 kb hu ‡ iˆ1 mLghu children (Prediction 1).
Pn _ cb ˆ Pn _ :
hu
iˆ1 hu iˆ1 Characteristics of children with CP are poor power
…9† production of the gastrocnemius-soleus, and increased
resistance to passive motion of the limbs. The ratio be-
In any analysis aimed to assess the same individual for tween forcing and sti€ness, is predicted to be lower in
di€erent conditions, we further assume the damping the a€ected leg compared to the non-a€ected leg of
term …cb2 † to remain constant across conditions. Al- functionally limited children and compared to typically
though the values obtained for forcing moment are not developing individuals (Prediction 2).
actual values, they represent a true proportional esti- Walking speed is a multiple of frequency and stride
mate of forcing for those conditions. Thus, a propor- length. Increases in speed are due to linear increases in
tional estimate of normalized forcing can be obtained stride length and stride frequency [18]. Sti€ness is asso-
for each individual as follows: ciated with stride frequency and stride length or ampli-
Pn Pn Pn Pn tude is associated with forcing magnitude. Since children
2 2
Fd L iˆ1 mL hu ‡ iˆ1 kb hu ‡ iˆ1 mLghu with CP have a limited capability of forcing, increases in
Piˆ1 / P :
n
h_u
iˆ1
n
h_u iˆ1
speed would be achieved largely through increases in
…10† frequency (sti€ness). Therefore, the rate of change (re-
gression slope) of sti€ness in relation to walking speed is
While Eq. (9) allows an estimation of the overall gen- predicted to be higher on the a€ected side of these
erative and dissipative forces, Eq. (10) can be used to children than on the non-a€ected side or typically de-
assess the ability of a given subject to generate forcing veloping children (Prediction 3). In addition, the limited
moment as the speed of walking increases. forcing capability in children with CP should manifest in
 S.T. Fonseca et al. / Clinical Biomechanics 16 (2001) 793±805 797

the rate of change of forcing moment in relation to
speed of walking. In this case, the slope of a linear re-
gression between forcing and speed in the a€ected leg of
functionally limited children is predicted to be closer to
a ¯at line as compared to typically developing individ-
uals and to the healthy leg of children with CP (Pre-
diction 4).
height. The children's characteristics are presented in
Table 1.
The participants were recruited from schools, clinics
and hospitals in the Boston area. All children were paid
for their participation in this study. Prior to participa-
tion in this study, children, parents or guardians signed
a consent form in accordance with the policies of Boston
University Institutional Review Board.

5. Methods
5.1. Subjects
Nine children with spastic hemiplegic CP and seven
typically developing children participated in this study.
Two children with CP were excluded from the study for
inability to complete all speed conditions. In addition,
one child with CP and one typically developing child
were excluded due to technical problems during data
collection. In the ®nal analysis, three male and three
female children participated in each group. Children's
age ranged from 8 to 15 years old.
Selection criteria for typically developing children
included no prior history of cardiovascular, neurological
or orthopedic disease. Selection criteria for children with
CP included a physician diagnosis of spastic hemiplegia
with no history of cardiovascular disease and no surgery
in the past 24 months. In addition, these participants
were capable of independent walking without crutches,
walkers or braces. In the functionally limited group,
three hemiplegic children had greater left side involve-
ment and three had greater right side involvement.
Groups were matched for age, gender, body weight and
5.2. Instrumentation
Three-dimensional (3D) kinematic data were col-
lected with an Optotrak 3020 System (Northern Digital,
Waterloo, Ont., Canada) with two banks of position
sensors. Each sensor consisted of a three camera bank
and was connected in series with the other sensor and to
an IBM compatible computer through the Optotrak
System Control Unit.
Commercially available force sensing resistors (In-
terlink Electronics, Camarillo, CA, USA) linked in se-
ries and ®tted within a custom-made shoe insole served
as foot switches. The switches were linked to an elec-
trical circuit [22] that produced 3.5 V when the switches
were fully loaded by the children's weight. The voltage
output of the circuit was fed to the Optotrak Analog to
Digital Unit (ODAU) and synchronized with kinematic
data to provide event identi®cation. Data were recorded
at the rate of 100 Hz.
Pairs of photoelectric cells were placed 2 m apart
before the beginning of the viewing volume. A digital
timer connected to the photoelectric cells provided the
participants' walking speed.

Table 1
Group characteristics

Child ID Group A€ected/corresponding Sex Age (yr) Height (m) Weight (kg)
to a€ected

02 Cerebral palsy Left leg F 8 1.44 29.5

03 Cerebral palsy Right leg F 15 1.63 64.0
04 Cerebral palsy Right leg M 9 1.30 28.2
06 Cerebral palsy Right leg M 13 1.56 38.4
07 Cerebral palsy Left leg M 8 1.26 28.8
08 Cerebral palsy Left leg F 10 1.53 35.4
1N Typically developing Left leg F 10 1.32 25.8
2N Typically developing Right leg F 12 1.5 46.5
3N Typically developing Right leg M 12 1.52 44.7
4N Typically developing Left leg F 11 1.51 45.7
5N Typically developing Right leg M 9 1.34 24.0
7N Typically developing Left leg M 10 1.44 39.5
Cerebral palsy Mean 10.5 1.45 37.38
SD 2.80 0.14 13.66
Typically developing Mean 10.67 1.44 37.70
SD 1.20 0.09 10.23
*
Not signi®cantly di€erent from typically developing group.
798 S.T. Fonseca et al. / Clinical Biomechanics 16 (2001) 793±805
5.3. Protocol
Infrared light emitting diodes were placed bilaterally
on the head (zygomatic process), shoulder (acromion
process), hip (greater trochanter), knee (lateral condyle),
ankle (lateral malleolus) and foot (5th metatarsal head)
of the children. Anthropometric measures of foot,
shank, thigh and total leg length were taken using the
markers as reference for landmarks' location. Body
mass and body height were measured using a balance
scale with an adjustable ruler. Participants were asked to
walk with the foot switches for 1 min to assure proper
®tting and comfort.
Children walked overground at their comfortable
speed on a 20 m walkway. The preferred, or comfortable
walking speed was the one which the child consistently
selected on three consecutive trials. Following the de-
termination of the preferred speed, the child was asked
to walk at speeds described as fast, very fast (fastest),
slow and very slow (slowest). The actual speed was
measured by the photoelectric cells and the information
was used to normalize the data for speed di€erences and
to give feedback to the children during the experiment.
Each child walked on the walkway at his/her pre-
ferred speed and at each of the four non-preferred
speeds for at least 10 successful trials per condition. A
successful trial was de®ned by capture of a full stride
(two successive heel strikes of the same leg). The se-
quence of walking speeds was randomized during the
experiment. Kinematic data were collected for each trial.
5.4. Data reduction
Raw kinematic data were converted into 3D data by
means of the Optotrak system software using the cali-
bration results for analysis. Data were ®ltered with a
second order Butterworth ®lter with a cut-o€ frequency
of 6 Hz [23]. The swinging arm tended to block the hip
marker during the slow walking conditions. A cubic
spline interpolation was applied up to a maximum of 30
missing hip frames. The procedure was validated against
known values of actual trials before its use and dem-
onstrated a mean error of 1.4 mm and a maximum error
of 5.0 mm in the Y dimension. X and Z dimensions
presented mean errors of 0.7 and 0.5 mm, respectively.
Trials with more than 30 missing hip frames were not
included in the analyses.
Heel strike and toe-o€ were automatically identi®ed
from the analog data. The program located the frames
in which an abrupt change in voltage occurred at foot
loading (heel strike) and unloading (toe-o€). This pro-
cedure generated independent ®les for left and right
sides containing position information about both sides.
The edited 3D data ®les were sequentially concatenated
according to the speed condition. This produced a cy-
clical sequence of strides that were used for analyses.
3D linear displacement, velocity and acceleration of
each marker and center of mass were calculated. An-
gular displacement, velocity and acceleration were cal-
culated for ankle, knee and hip for both legs. Location
of the center of mass of the body for each frame was
estimated. This calculation was based on an eight-seg-
ment model with 2 feet, 2 shanks, 2 thighs, head and
neck, and trunk. Anthropometric estimates for children
were used for the calculation of the body's center of
mass [24]. Angular data were also calculated for a vector
formed by the body's center of mass and ankle marker,
and another vector corresponding to the vertical.
The inverted pendulum equivalent length …L† was
calculated according to the method described by Holt et
al. [16] and Kugler and Turvey [17]. However, instead of
calculating the equivalent pendulum length for the leg
system, the inverted model analysis considered the
whole body. The calculations applied an eight-segment
model with 2 feet, 2 shanks, 2 thighs, head and neck, and
trunk. The individual segments' mass, center of mass
location and moments of inertia was calculated based on
anthropometric data from Jensen [24], and the masses of
the arms were added to the trunk. The total mass of the
system …m† was calculated as total body mass minus the
mass of the stance foot. Stride, step and stance period
were measured from kinematic data. Walking speed was
calculated as the product of stride length and stride
frequency. A custom program was used to calculate the
total angular excursion of the center of mass about the
ankle joint from the vertical during the push-o€.
The procedure for calculation of the dynamic pa-
rameters of the inverted pendulum system followed that
outlined above. Calculations of sti€ness (kb2 ) were based
on Eq. (8). In order to allow comparisons between sides,
kb2 was measured using the observed step period as half
natural period. The gravitational restoring torque …mLg†
was obtained through the anthropometric measure-
ments, by multiplying the equivalent pendulum length
…L† by the system's mass …m† and the gravitational
constant …g†.
Normalized forcing moment was calculated from Eq.
(11) using kinematic data for center of mass angular
displacement, velocity and acceleration. The net mo-
ment of inertia about the ankle joint …mL2 h† was calcu-
lated as the integrated system's angular acceleration
from the beginning of the ankle extension to toe-o€
multiplied by the pendulum mass …m† and the square of
the pendulum equivalent length …L†. The gravitational
and elastic restoring torques were also multiplied by the
integrated angular displacement of the center of mass
during the same period. Finally, the forcing moment was
normalized by the integrated angular velocity. A custom
program was used to identify the frame in which the
ankle joint started to plantar ¯ex and then integrated the
center of mass angular displacement, velocity and ac-
celeration about the ankle opposite to that being ana-
 S.T. Fonseca et al. / Clinical Biomechanics 16 (2001) 793±805
lyzed, until the push-o€ was reached. This period cor-
responds to the phase of concentric muscular activation
of the gastrocnemius muscle during push-o€ and de®nes
when the forcing moment is applied to the system. The
program solved the forcing moment for each stride and
the mean value for each speed condition was used for
analysis. Considering all conditions analyzed, the max-
imum number of frames included as the forcing phase
was 32 and the minimum was 8.
5.5. Statistical analysis
Fast Fourier Transform (F F T ) analyses were con-
ducted to determine the spectral power distribution of
the angular displacement of the child's center of mass.
This procedure veri®ed the condition of harmonicity of
the system.
Analyses of Variance (A N O V A ) with one between-
subject e€ect (groups) and two within-subject e€ect (leg
and speed condition) were used to compare the following
dependent variables: (1) speed, (2) elastic to gravitational
restoring torque ratio and (3) normalized forcing mo-
ment to sti€ness ratio between children with CP and
typically developing individuals during the stance phase
of walking. This statistical procedure allowed the testing
of the main e€ects group and leg for each condition, as
well as interaction e€ects. Pre-planned focussed contrasts
were performed to locate signi®cant di€erences accord-
ing to proposed hypothesis. The level of signi®cance was
set at P 6 0:1 for all comparisons. This signi®cance level
is appropriate for small sample studies by protecting
against type I error and yet facilitating the process of
®nding true group di€erences [25]. Bonferroni correction
for multiple comparisons in terms of speed conditions
was applied to contrast results. The procedure changed
the signi®cance level from 0.1 to 0.02.
General linear models were used to test di€erences in
slopes of normalized forcing moment, and elastic re-
storing torque by speed of walking between children
with CP and typically developing children.
Linear regression analyses were used to test the as-
sociation between the child's speed (independent vari-
able) and measures of normalized forcing moment and
sti€ness (dependent variables).
6. Results
The following abbreviations are used throughout the
results section: a€ected leg of functionally limited chil-
dren (CPA), non-a€ected leg of functionally limited
children (CPNA); leg corresponding to the a€ected
(matched) control leg of typically developing children
(TDCA), and leg corresponding to the non-a€ected
(matched) leg of typically developing children
(TDCNA).
799
In all conditions the mean angular excursion of the
center of mass about the ankle joint from the vertical
during the push-o€ was small. The minimum angular
excursion from the vertical was 11.2° at the very slow
speed condition of CPA and the maximum excursion
was 18.5° at the very fast condition of TDCA.The
maximum angular excursion of the center of mass from
the vertical around the ankle joint of 18.5° supported the
use of the linear approximation of the equation of mo-
tion. FFT analysis performed on the angular displace-
ment of the center of mass time series indicated that
most of the observed power was concentrated at the
walking frequency. Considering the total spectral power
as 100%, the percentage of the power found at the stride
frequency relative to the total power was calculated. It
was found that the individual percentage of the total
power at the stride frequency ranged from 89.9% to
100%. Mean results for percentage of total power at the
stride frequency varied from 93.6% at the very slow
speed (CPNA) to 97.95% at the very fast speed
(TDCNA). A second smaller peak was found for most
of the children. This ®nding suggests that a source of
energy is tapped every half cycle, consistent with an
escapement due to push-o€ of each foot. The percentage
of total power for this second peak varied from 2.05%
(very fast) to 5.98% (very slow). A representative sample
of the F F T plots is illustrated in Fig. 2.
6.1. Speed comparisons
There was a signi®cant di€erence between groups for
speed (F …1; 50† ˆ 6:59, P ˆ 0:0133) and for group by
condition interaction (F …4; 50† ˆ 2:58, P ˆ 0:049). Fo-
cussed contrast analysis demonstrated that typically
developing children …CPA ‡ CPNA† walked signi®-
cantly faster than functionally limited ones
…TDCA ‡ TDCNA† at fast and very fast speed condi-
tions F …1† ˆ 133:64, P < 0001 and F …1† ˆ 715:50,
P < 0001, respectively). Fig. 3 depicts mean and stan-
dard error for all groups and conditions.
Since sti€ness …kb2 † has been demonstrated to vary
according to the walking speed [34], all measures in-
cluding sti€ness were normalized with respect to speed
for all subsequent analyses focussing on group com-
parisons.
For speed normalized ratio kb2 =mLg, k 
kb2 =speed
k ˆ : …11†
mLg
6.2. Sti€ness to gravitational component comparison, k 
(Prediction 1)
Analysis showed that children with CP presented
signi®cantly higher k  on their a€ected side than on the
non-a€ected side in all speed conditions …P < 0:001†.
800 S.T. Fonseca et al. / Clinical Biomechanics 16 (2001) 793±805

Fig. 2. Representative sample of FFT on the angular displacement time series for the a€ected leg of functionally limited children, CPA (a), non-
a€ected leg of functionally limited children, CPNA (b), leg corresponding to the a€ected (matched) leg of typically developing children, TDCA (c)
and leg corresponding to the non-a€ected (matched) leg of typically developing children, TDCNA (d).

Comparisons between the a€ected side of functionally

limited children (CPA) and typically developing children
…TDCA ‡ TDCNA† also demonstrated a signi®cantly
higher mean normalized ratio for the functionally limited
group in all speed conditions …P < 0:0002†. No signi®-
cant ratio di€erence was observed on the non-a€ected
side of children with CP as compared to typically de-
veloping children …P > 0:049. Mean and standard error
for all groups and conditions are displayed in Fig. 4.

6.3. Normalized forcing function to sti€ness ratio com-

parisons (Prediction 2)

Comparisons were performed on the ratio between

the forcing and sti€ness values …Fd =kb2 †. The analysis
demonstrated that the a€ected side of functionally lim-
Fig. 3. Mean and standard error of speed for all groups according to ited children had signi®cantly lower normalized Fd =kb2
speed condition. Groups are: a€ected leg of functionally limited chil- ratio than the non-a€ected side for all conditions
dren, CPA (j), non-a€ected leg of functionally limited children,
…P < 0:01†. In addition, CPA children presented signif-
CPNA (d), leg corresponding to the a€ected (matched) leg of typically
developing children, TDCA (
) and leg corresponding to the non- icantly lower normalized ratios as compared to typically
a€ected (matched) leg of typically developing children, TDCNA (
). developing children (TDCA + TDCNA) at the very slow
 S.T. Fonseca et al. / Clinical Biomechanics 16 (2001) 793±805
Fig. 4. Mean and standard error of sti€ness …kb2 † to gravitational
component …mLg† ratio normalized by speed for all groups according
to speed condition. Groups are: a€ected leg of functionally limited
children, CPA (j), non-a€ected leg of functionally limited children,
CPNA (d), leg corresponding to the a€ected (matched) leg of typically
developing children, TDCA () and leg corresponding to the non-af-
fected (matched) leg of typically developing children, TDCNA (
). leg of typically developing children, TDCNA (
).
…P ˆ 0:018† and preferred …P ˆ 0:014† speed conditions.
No di€erence was observed at slow, fast and very fast
conditions …P > 0:089†. Comparisons between CPNA
and typically developing children …TDCA ‡ TDCNA†
demonstrated that functionally limited children pre-
sented signi®cantly lower normalized Fd =kb2 than non-
functionally limited children …P < 0:001†, except for the
very slow …P ˆ 0:482† and very fast …P ˆ 0:046† speed
condition. Fig. 5 presents mean and standard error for
all groups and conditions.
6.4. Sti€ness/speed relationship (Prediction 3)
6.4.1. Sti€ness/speed regressions
Regression analyses for each individual between
sti€ness and speed demonstrated a very strong and sig-
ni®cant linear relationship for all children. Values for R2
ranged from 0.946 to 0.999 for CPA, from 0.965 to 0.997
for TDCA, from 0.908 to 0.998 for CPNA, and from
0.968 to 0.989 for TDCNA.
6.4.2. Sti€ness/speed slope comparisons
A general linear model was used to compare the
slopes of the linear regression between sti€ness and
speed. The regression lines of the group's mean value for
each speed demonstrated a very high association be-
tween speed and sti€ness for the a€ected side of the
functionally limited group (R2 ˆ 0:994, slope ˆ 1595.25,
P ˆ 0:0001), and for the non-a€ected side of the func-
tionally limited group (R2 ˆ 0:984, slope ˆ 1503.18,
P ˆ 0:0009). Similar results were found for the side
corresponding to the a€ected side of the typically de-
veloping group (R2 ˆ 0:992, slope ˆ 1346.53,
801
Fig. 5. Mean and standard error of normalized forcing to sti€ness ratio
normalized by speed for all groups according to speed condition.
Groups are: a€ected leg of functionally limited children, CPA (j),
non-a€ected leg of functionally limited children, CPNA (d), leg cor-
responding to the a€ected (matched) leg of typically developing chil-
dren, TDCA () and leg corresponding to the non-a€ected (matched)
P ˆ 0:0003), and for the side corresponding to the non-
a€ected side of the typically developing group
(R2 ˆ 0:981, slope ˆ 1421.50, P ˆ 0:0011). The slope
comparisons demonstrated a signi®cant di€erence be-
tween CPA and TDCA (F …2; 6† ˆ 66:79, P ˆ 0:0001),
and between CPA and CPNA (F …2; 6† ˆ 43:25,
P ˆ 0:0003). No di€erence was observed between CPNA
and TDCNA (F …2; 6† ˆ 0:18, P ˆ 0:839), and between
TDCA and TDCNA (F …2; 6† ˆ 0:407, P ˆ 0:683). In
summary, the results are in agreement with Prediction 3.
Slope comparisons on the mean sti€ness values for each
group and leg indicated that the a€ected side of the
functionally limited children had signi®cantly steeper
slopes than the non-a€ected side and typically develop-
ing individuals. These results are summarized in Fig. 6.
6.5. Forcing/speed relationship (Prediction 4)
6.5.1. Forcing/speed regressions
In contrast to the sti€ness results, individual regres-
sion analysis between forcing and speed demonstrated
non-uniform results. The R2 values ranged from 0.003 to
0.443 for CPA, from 0.430 to 0.976 for CPNA, from
0.619 to 0.982 for TDCA, and from 0.007 to 0.858 for
TDCNA. For some children there was a marked drop in
forcing moment at very fast speeds. Since the very fast
speed is located at the extreme of the regression line, this
condition has a strong leverage e€ect reducing the as-
sociation between the variables. Removal of the very
fast speed produced much stronger and signi®cant re-
lationship between normalized forcing and speed for
CPNA and TDCA groups. The R2 values ranged from
0.853 to 0.976 for CPNA, and from 0.825 to 0.994 for
802 S.T. Fonseca et al. / Clinical Biomechanics 16 (2001) 793±805
Fig. 6. Scatter plot with ®tted regression lines between sti€ness and
speed. Groups are: a€ected leg of functionally limited children, CPA
(j, y ˆ 1592:0x ‡ 563:4, R2 ˆ 0:995), non-a€ected leg of functionally
limited children, CPNA (d, y ˆ 1503:2x ‡ 266:3, R2 ˆ 0:984), leg
corresponding to the a€ected (matched) leg of typically developing
children, TDCA (d, y ˆ 1346:5x ‡ 334:5, R2 ˆ 0:990), and leg corre-
sponding to the non-a€ected (matched) leg of typically developing
children, TDCNA (
, y ˆ 1421:5x ‡ 290:0, R2 ˆ 0:980).
, y ˆ 263:82x 0:87, R2 ˆ 0:69).
TDCA. For TDCNA the coecients improved for two
children and one child remained with R2 of 0.01. Ex-
cluding this child, the R2 values ranged from 0.74 to
0.89. The results for CPA were not a€ected by the re-
moval of the very fast condition except for one child.
The R2 values ranged from 0.015 to 0.653.
In summary the relationship between forcing and
speed for individual regressions was strong and signi®-
cant only after the removal of the very fast speed for the
typically developing individuals and for the non-a€ected
leg of children with spastic CP. The a€ected side of the
functionally limited children did not show a signi®cant
association between forcing and speed.
6.5.2. Forcing/speed slope comparisons
The regression lines of the group's mean value for
each speed demonstrated a strong association between
speed and forcing for the side corresponding to a€ected
and non-a€ected of the typically developing group
(R2 ˆ 0:947, slope ˆ 422.11, P ˆ 0:039 and R2 ˆ 0:875,
slope ˆ 263.82, P ˆ 0:019, respectively). The non-af-
fected side of the functionally limited group demon-
strated only a moderate linear relationship (R2 ˆ 0:765,
slope ˆ 582.99; P ˆ 0:052). The a€ected side of the
functionally limited group also displayed a moderate
association between forcing and speed (R2 ˆ 0:698,
slope ˆ 82.303, P ˆ 0:078). The slope comparisons
demonstrated signi®cant di€erences between CPA and
TDCA (F …2; 6† ˆ 41:724, P ˆ 0:0003), between CPA
and CPNA (F …2; 6† ˆ 46:040, P ˆ 0:0002), and between
CPNA and TDCNA (F …2; 6† ˆ 17:915, P ˆ 0:003). No
di€erence was observed between TDCA and TDCNA
Fig. 7. Scatter plot with ®tted regression lines between normalized
forcing and speed. Groups are: a€ected leg of functionally limited
children, CPA (j, y ˆ 82:3x 127:5; R2 ˆ 0:69), non-a€ected leg of
functionally limited children, CPNA (d, y ˆ 582:9x 86:1, R2 ˆ 0:76),
leg corresponding to the a€ected (matched) leg of typically developing
children, TDCA (, y ˆ 422:11x 265:57, R2 ˆ 0:95), and leg corre-
sponding to the non-a€ected (matched) leg of typically developing
children, TDCNA (
(F …2; 6† ˆ 2:643, P ˆ 0:1502). In summary, the results
are in agreement with Prediction 4. Typically developing
children and CPNA had signi®cantly steeper slopes than
that observed on the a€ected side of functionally limited
children. No di€erence between sides was observed in
typically developing children. These results are pre-
sented in Fig. 7.
7. Discussion
The results supported the dynamic predictions in
children with spastic hemiplegic CP derived from the
EDIPS model and from the changes in the kinematics
and kinetics of the gait of CP reported previously in the
literature. CP are relatively sti€er and generate less ac-
tive force on the a€ected side (Prediction 1, Fig. 4). The
greater sti€ness is due to increased re¯ex gain and co-
contraction and to alterations of the connective and
muscle tissues that are characteristic of CP [6±8]. It has
been suggested that uneven structural growth of bone
and muscles in CP may result in longer bones and ten-
dons and shorter muscle bellies leading to increased re-
sistance to a passive stretch [8,9]. These anatomical/
structural changes in children with spastic CP poten-
tially provide them with an enhanced ability to store and
return elastic energy. The decreased force generation on
the a€ected side captured in the model estimates is
consistent with reports of limited power production and
poor timing in the ankle plantar ¯exors [10,11].
CP and typically developing children displayed simi-
lar preferred, slow and very slow speeds. However, in
 S.T. Fonseca et al. / Clinical Biomechanics 16 (2001) 793±805
response to the requirement to walk above preferred
speed, children with spastic CP did not achieve the
higher speeds observed in typically developing children
(Fig. 3). Nevertheless, CP were capable of increasing
speed above their preferred. Increased speed of walking
was partially achieved by an increase in sti€ness and
resulting higher frequency as indicated by the steeper
slope of the speed-sti€ness curve (Prediction 3). The
inability of the a€ected limb to increase force in response
to a required increase in speed is indicated by the min-
imal change in escapement forcing across speed condi-
tions. Because sti€ness and its potential for elastic
energy return act conservatively, they cannot compen-
sate for energy losses due to limited force production
and the resultant decrease in amplitude on the a€ected
side (Prediction 2, Fig. 5). Energy losses were compen-
sated for by an increase of force on the non-a€ected side
that was higher than that normally displayed by typi-
cally developing children (Fig. 5). The decrement in the
forcing: sti€ness ratio at the higher speeds in the non-
a€ected limb suggests that the limit on walking speed
).
may be determined by the limited capability of the non-
a€ected side to compensate by additional forcing. The
presence of a power producing mechanism provided by
the non-a€ected leg may explain why more children with
spastic hemiplegic CP are able to walk independently
than in any other type of CP [26].
The dynamic contributions to the gait cycle from
each leg of CP are also re¯ected in asymmetries in the
kinematic patterns that are not seen in TD. According
to the model, changes in force will result in changes in
amplitude or stride length, and changes in sti€ness will
result primarily in changes in stride frequency. Zarrugh
[27] demonstrated a ®xed ratio between frequency and
amplitude across di€erent speeds of walking. In the
present study, this ratio was almost constant except for a
drop at very fast condition (Fig. 8). However, the ratio
amplitude: frequency was signi®cantly lower for the af-
fected side compared to the non-a€ected and the non-
disabled children, and, for the non-a€ected side, it was
higher compared to both a€ected and non-impaired
controls. This asymmetry is re¯ective of the alternative
use of dynamic resources in each leg of the children with
CP. In the a€ected leg a greater utilization of the in-
creased sti€ness was evident, while the non-a€ected limb
used a greater proportion of its greater forcing capa-
bility. In the very fast condition, the ratio amplitude/
frequency for the non-disabled group approached that
of the a€ected leg of children with spastic CP, suggesting
that the both groups started to converge to a similar
solution, in which elastic energy return becomes an im-
portant element for locomotion.
There may be other changes in the kinematics that
might facilitate the use of the changed dynamics. One
possibility is that the non-a€ected limb is acting as an
escapement-driven pendulum that lifts and pushes for-
803
Fig. 8. Mean and standard error of step amplitude to step frequency
ratio for all groups according to speed condition. Groups are: a€ected
leg of functionally limited children, CPA (j), non-a€ected leg of
functionally limited children, CPNA (d), leg corresponding to the
a€ected (matched) leg of typically developing children, TDCA () and
leg corresponding to the non-a€ected (matched) leg of typically de-
veloping children, TDCNA (
ward the center of mass, and drops that mass onto the
a€ected limb. The a€ected limb then acts like a trans-
lational vertical spring or pogo stick. In order to test this
interpretation we are currently analyzing measures of
vertical sti€ness, landing angles, center of mass trajec-
tory and potential and kinetic energy exchanges in the
two limbs. For example, it would be predicted that
landing angle on the a€ected side would be steeper to
facilitate the use of that limb as a vertical spring, and
that the slope of the center of mass would rise more
vertically on push-o€ from the a€ected limb.
The ®ndings of this study lead to the proposal that
kinematic patterns observed in CP are adaptations to
the changes in dynamic action capabilities that result
from the upper motor neuron disease. Furthermore, CP
may actually take advantage of the altered dynamics by
adopting a movement pattern that allows them to lo-
comote in spite of their impairments, and to do it in a
way that minimizes metabolic costs. Previous ®ndings
have shown that although the kinematic patterns of CP
may be quite di€erent, the metabolic costs are minimal
in these preferred gaits [28]. This hypothesis of loco-
motor function in CP is in contrast to most of the lit-
erature that describes the kinematic patterns observed in
children with CP as immature and inecient [12,29].
The interpretation is consistent with the views of Bern-
stein [14], however, who stressed the importance of
considering internal and environmental forces when in-
vestigating the emergence of co-ordinated behaviors.
Instead of considering the passive and reactive forces as
a problem for co-ordination, Bernstein understood that
movements are structured in a way as to take advantage
of these forces. He proposed that the secret of co-ordi-
804 S.T. Fonseca et al. / Clinical Biomechanics 16 (2001) 793±805
nation lies in employing active muscle forces only as a
complement to the passive and reactive ones. The ED-
IPS model captures the dynamic action capabilities
(escapement force, sti€ness) and the gravitational forces
…mLg†, and provides a way to understand the interplay
of these forces in the emergent movement patterns.
Despite the promising ®ndings of the study there are
some caveats related to the use of the EDIPS model.
Critical to estimating parameters of the model is the as-
sumption that the system is operating at a natural fre-
quency. The natural frequency assumption depends on
the presence of an escapement mechanism. In the gait
patterns of typically developing individuals the gastroc-
nemius-soleus group produces most of the power during
the push-o€ phase, thereby supporting the assumption.
This claim is further supported by the FFT that showed
power at twice the stride frequency (i.e. at the step fre-
quency) suggesting an input of energy at each leg's push-
o€. In the limited data of children with spastic hemiplegic
gait, EMG patterns show distinct bursts of activity dur-
ing the stance phase suggesting that energy is imparted to
the system in an escapement-like fashion [30].
There were also a number of unexpected ®ndings in
this study. Analysis of the forcing to sti€ness ratio
demonstrated that the a€ected limb presented signi®-
cantly lower ratios than the non-a€ected limb for all
conditions. However, comparisons between the a€ected
side and the limbs of typically developing children in-
dicated that functionally limited children only had sig-
ni®cantly lower ratios at the very slow and preferred
condition. These ®ndings suggest that children with ce-
rebral palsy utilize a greater proportion of elastic re-
storing moment relative to force production during the
push-o€ at lower speeds. The lack of the expected dif-
ferences between CPA and TD at higher speeds suggests
that typically developing children may employ greater
amounts of elastic energy when walking at faster speeds
or experience a decrease in forcing or some combina-
tion.
While the results of this study show that the model is
capable of describing a wide range of expected di€er-
ences in dynamics between limbs and groups, there are
some limitations. First, the model is abstract in the sense
that it does not capture the contribution of individual
muscle±tendon units to the overall force and sti€ness.
Nor does it capture the complexity of the double and
compound pendulums that truly re¯ect the legs and
segments that make up the locomotor unit. Neverthe-
less, as the results of this study indicate, the model, with
its limited assumptions, is capable of capturing the
global changes in the resources available for locomotion
as a function of CP. Furthermore, it suggests that the
gait patterns that are adopted are a direct re¯ection of
the changes in the global dynamics. Further experiments
and models that detail the muscular and mechanical
components of locomotion are currently being explored.
8. Clinical implications
A major accomplishment of the model is the capa-
bility to quantify sti€ness in active movement. Despite
several attempts to assess spastic hypertonia from me-
chanical or neural sources, measures of sti€ness during
functional movements have not been achieved before
[31,32]. Similar results were achieved in a previous study
that looked at the e€ect of manipulating walking fre-
quency on the behavior of children with CP [13].
However, scaling step frequency, instead of speed,
forced the children with CP to adopt a higher speed than
they normally assume. Allowing the children to self
adjust the step frequency as walking speed is increased is
a more e€ective way to examine sti€ness di€erences in all
speeds, since no linear scaling is forced in advance. The
linear relationship found between speed and sti€ness in
the current study is a natural result and not a forced
one.
In contrast to the pathophysiological view that the
altered walking pattern presented by children with CP
is a non-functional behavior, the dynamical approach
presented in this study provides an alternative per-
spective. Pattern formation is an optimal solution that
is based on the individuals' action capabilities and
dynamical properties of the system in face of envi-
ronmental and task demands. This perspective could
provide more meaningful interventions than the ones
currently focused on reducing spasticity. Techniques
directed towards providing increased forcing (power
production) through the appropriate muscle groups
and at the appropriate time in the gait cycle may be
more successful. Results on functional electrical-stim-
ulation of the gastrocnemius-soleus muscles during
walking as reported by Carmick [33,34] and Comeaux
et al. [35] demonstrated that functional electrical
stimulation (FES) of the ankle plantar ¯exors of chil-
dren with spastic diplegic CP during the stance phase
led to a gait pattern in which a normal heel strike was
achieved. We suggest that the introduction of FES
induces a change in the dynamic action capabilities
that are re¯ected in a decreased need to adapt a gait
pattern (plantar-¯exed foot) that facilitates the use of
the potential elastic energy return of sti€ muscle±ten-
dons.
Methods focusing only on the compensatory mecha-
nisms (e.g. increased sti€ness) or based on the imposi-
tion of extrinsic and non-task speci®c patterns (e.g. FES
of tibialis anterior) are not supported by the perspective
proposed in this study. We propose that approaches
focusing on changes in speci®c parameters, such as
functional muscle strength, may lead to a dynamic
reorganization of the system, and provide altered func-
tional behaviors. Therefore, the results of this study may
induce important changes in the treatment of walking
disorders in children with CP.
 S.T. Fonseca et al. / Clinical Biomechanics 16 (2001) 793±805
Acknowledgements
This work was partially supported by the Brazilian
government agency CNPq through a four year schol-
arship and by the Dudley Sargent Research Fund Grant
conferred to the ®rst author. The work was also partially
supported by a grant from the Physical Therapy
Foundation awarded to the second author.
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