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Gait & Posture 26 (2007) 482488

www.elsevier.com/locate/gaitpost

Runner-up of the Joint ESMAC and GCMAS (JEGM) 2006 Award

An exploration of the function of the triceps surae during normal


gait using functional electrical stimulation
Caroline Stewart a,*, Neil Postans a, Michael H. Schwartz b,c,
Adam Rozumalski b, Andrew Roberts a
a
Orthotic Research and Locomotor Assessment Unit, Robert Jones and Agnes Hunt Orthopaedic Hospital, Oswestry, Shropshire SY10 7AG, UK
b
Gillette Childrens Specialty Healthcare, Center for Gait and Motion Analysis, 200 East University Avenue, St. Paul, MN 55101, USA
c
University of Minnesota, Minneapolis, USA
Received 14 June 2006; received in revised form 29 November 2006; accepted 5 December 2006

This paper was selected for publication in Gait and Posture from the presentations at the Joint ESMAC and GCMAS 2006 meeting by a
Scientific Committee representing both Societies and chaired by Professor Maria Grazia Benedetti.

Abstract

Gastrocnemius and soleus have a common tendon and both are active during stance phase, where they are thought to arrest and control
tibial advance. Soleus is associated with the production of an extending moment at the knee. The two-joint gastrocnemius, which crosses the
knee joint, will have an additional contribution to the knee flexors.
Recent work using induced acceleration analysis (IAA) has demonstrated distinct differences between the actions of gastrocnemius and
soleus. This study aims to use gait analysis to provide in vivo examination of these theoretical predictions.
Functional electrical stimulation (FES) was chosen to provide a perturbation in muscle force, a close physical analogue to the theoretical
predictions of IAA. Five adult male subjects, with no gait problems, participated. Each had gastrocnemius and soleus stimulated at three
different timings during normal gait, while 3D gait data were collected. The order of testing was randomised and unstimulated trials were
randomly interspersed to act as a control.
The results show very different actions for soleus (ankle plantarflexing/knee extending) and gastrocnemius (ankle dorsiflexing/knee
flexing) in stance phase. The counterintuitive nature of the action of gastrocnemius suggests that further clinical and biomechanical
investigation into this muscles function is required. The actions of both muscles at the knee confirm published IAA predictions. In vivo
evidence such as this gives greater confidence when using model predictions. The approach adopted in this study could eventually be extended
to other muscles and patient populations.
# 2006 Elsevier B.V. All rights reserved.

Keywords: Normal gait; Gastrocnemius; Soleus; Functional electrical stimulation

1. Introduction moment arms at the talocrural joint. Both muscles also cross
the subtalar joint where the moment arms are small and
The triceps surae comprises the two calf muscles. posture dependent [1]. Only gastrocnemius crosses the knee
Gastrocnemius, having medial and lateral heads, originates joint, where it has a flexing moment arm.
from the femur and inserts into the calcaneus through the Based on their similar anatomy the calf muscles are
Achilles tendon. Soleus shares this common insertion point generally thought to have similar functions, particularly at the
but has its origin on the tibia and interosseus membrane. The ankle. Active testing on the examination couch produces a
anatomical paths of these muscles give them plantar flexing predictable plantarflexion response. Clinically, passive ankle
dorsiflexion range increases when gastrocnemius is relaxed
* Corresponding author. Tel.: +44 1691 404666; fax: +44 1691 404058.
by knee flexion, especially when this muscle is pathologically
E-mail address: Caroline.Stewart@rjah.nhs.u (C. Stewart). contracted (Silverskiold test). During dynamic activity,

0966-6362/$ see front matter # 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.gaitpost.2006.12.001
C. Stewart et al. / Gait & Posture 26 (2007) 482488 483

however, the roles of the gastrocnemius and soleus become induced accelerations at the knee at midstance. Neptune et al.
more complex. EMG data show that both muscles are active in [14] showed that, while soleus accelerated the joint into
stance, with soleus turning on before gastrocnemius. The extension, gastrocnemius had the opposite effect.
delay between the reported onsets of the two muscles varies The implementation of IAA models is mechanically
between studies [2,3]. Various authors have described the correct, but the practical application and significance of IAA
effects of this activity at the knee and ankle. techniques has been questioned. Chen [15] points to
The general consensus is that soleus, assisted later by differences in results and interpretation between studies.
gastrocnemius, restrains the forward progression of the tibia This study treats IAA as a perturbation analysis. IAA can be
over the talus in second rocker, hence reducing dorsiflexion viewed as predicting the accelerations, which would result
[35]. The effect at the knee is more complex. Gage [6] uses from an incremental change in muscle force. As yet no
the term plantarflexion/knee extension couple to describe experiments have been carried out to demonstrate a direct
the action of soleus in advancing the ground reaction force link between the predictions of the models and the response
and producing a knee extending moment. Exaggeration of of a real person in the laboratory. If confirmatory evidence
this mechanism is proposed as a possible cause of knee could be provided then IAA models could be used with
hyperextension in pathological gait [7]. Gage [6] reports a greater confidence. What is required is a technique for
relatively late onset for gastrocnemius in stance and does not producing a physical perturbation in muscle force to
associate the muscle with a knee extension mechanism in compare with the theoretical predictions of IAA.
normal gait. For gastrocnemius which, unlike soleus, crosses Functional electrical stimulation (FES) uses low level
the knee joint, the flexing moment arm is likely to mitigate electrical currents to induce muscle contractions. The
any similar coupling which might occur. stimulus is supplied via skin mounted electrodes, usually
Studies have been carried out looking at patients with calf placed over the belly of the muscle or the nerve that supplies
muscle deficiency [8] and also normal subjects after tibial it. FES is a convenient intervention in that it can be applied
nerve blocks [8,9]. The aim was to understand the normal randomly, with almost instantaneous but short-lived effects.
function of the muscles and the effects of nerve blocks are Increasing the force produced by a muscle with FES gives an
particularly interesting. Simon et al. and Sutherland et al. indication of the dynamic function of that particular muscle
both highlight the restraint of tibial advancement during under specific kinematic conditions. The use of FES in this
second rocker and question the appropriateness of assigning way is similar in concept to the earlier work carried out using
a propulsive action to the muscles. There are, however, two nerve blocks, with the difference that FES seeks to augment
main limitations with the work. Firstly, the block affects rather than reduce muscle forces. FES has, however, two
several muscles and it is impossible to separate out the main advantages. It is possible to target stimulation to
individual contributions of gastrocnemius and soleus. gastrocnemius and soleus separately and its rapid action,
Secondly, it is likely that compensation mechanisms will which can be switched on and off, minimises the
be seen, even in the very early period after the block has development of compensations.
taken effect. This study aims to use FES to clarify the dynamic
During walking the musculoskeletal system forms a function of the calf muscles during normal gait, increasing
dynamic, linked chain of segments. In this situation, a our understanding of the biomechanical action of the
muscle does not only affect the joints it crosses. Each muscle muscles. If the results confirm the reports of recent IAA
has the potential to affect the whole kinetic chain, which can simulation work then researchers will be able to have much
produce counterintuitive effects. Computer simulation greater confidence in the predictive power of these models.
techniques are being developed to predict these whole
mechanism effects. Forward dynamics [10] allows theore-
tical movement patterns to be generated from muscle force 2. Subjects
inputs. Induced acceleration analysis (IAA) provides a
simpler, more stable, approach which gives information Five adult male subjects consented to take part in the
about dynamic function in terms of the potential of a joint study. (Ethical approval was obtained from the local
moment [11] or muscle force [12] to accelerate the joints and research ethics committee.) Subjects had an average age
segments of the musculoskeletal system. of 38 years (2256), height of 180 cm (176183) and weight
Recent work using forward dynamics/IAA techniques has of 87 kg (67101). No subject had any pathology affecting
yielded some surprising results for the calf muscles [13,14]. their walking and this was confirmed through the normal gait
These simulations have been used to analyse the contribution data collected.
of the muscles to support (vertical acceleration), propulsion
(acceleration in the direction of progression) and the initiation
of swing phase. Both studies emphasise the importance of 3. Methods
looking at the individual components of the calf muscle
separately and both revealed clear differences between the Testing was only carried out on one lower limb, selected
actions of gastrocnemius and soleus. An example of this is the at random. One subject specifically requested that his left leg
484 C. Stewart et al. / Gait & Posture 26 (2007) 482488

be tested, due to a previous but currently asymptomatic


injury on the right, and this was accommodated. The result
of this process was that one subject had his right leg tested
(Subject 1) and the rest their left.
One pair of self adhesive FES electrodes (Nidd Valley
Medical) was placed over the belly of the lateral gastro-
cnemius muscle. The active electrode (cathode) was placed
proximally with the indifferent electrode placed directly
below. A second pair of electrodes was placed over the soleus
muscle, below the distal end of the gastrocnemius. The active
electrode was again placed proximally. The positions of the
electrodes were based on Baker et al. [16]; however, the exact
positioning had to be dictated by palpation of each individual
subject. This was done with the subject lying prone on the
examination couch. The final position was chosen to give
strong plantarflexion for each muscle, with no noticeable
(palpable) contraction of gastrocnemius when soleus was
stimulated and vice versa. The positions of the electrodes in
one subject are illustrated in Fig. 1.
An Odstock two channel stimulator (Department of
Medical Physics, Salisbury District Hospital) was used. The
stimulator could be controlled by foot switches to provide
several different stimulation algorithms. The stimulation
waveform comprised asymmetric biphasic pulses (fre-
quency 40 Hz, maximum current amplitude 70 mA). The
pulse width was adjusted to elicit as strong a contraction as
possible while remaining comfortable enough for the subject
to walk naturally.
Two foot switches were used to control the onset and
cessation of stimulation. One switch was placed under the
heel and one under the first metatarsal head on the tested
limb. As the subjects walked barefoot the foot switches were
secured using double sided tape.
A Vicon 612 system was used for the data collection, in
combination with a single Kistler force platform. A full body
marker set (PluginGait, Vicon) was used for each subject and
an initial set of data was collected to include six clean strikes
on the force platform for the tested limb. All data were
collected at a comfortable, self-selected walking speed.
Two muscles were tested, gastrocnemius and soleus, with
three stimulation patterns (1: initial contact to foot flat, 2:
foot flat to toe off, 3: heel off to toe off) giving six test
combinations. Randomisation was used to determine which Fig. 1. Typical positions of FES electrodes.
muscle was tested first and also the order of data collection
for each timing interval. of the Vicon system, allowing the exact timing to be
Data were collected in the same fashion for each of the measured and checked. The sampling rates used were 60 Hz
six test conditions. Each trial was randomly assigned as a for camera data and 1080 Hz for analogue and force plate
stimulated or non-stimulated walk to prevent any voluntary data.
compensation or anticipation. For the stimulated walks the The data were processed using Vicon standard software
FES was only used for a single gait cycle, the one over the (Workstation/PluginGait, Polygon). The first five good trials
force platform. The application of the FES was controlled were used for subsequent analysis. A good trial was one
by the foot switches, in combination with a remote, where continuous data were available for at least one
manually operated switch. Data collection continued until complete gait cycle starting with left and right initial
at least six clean force plate strikes were obtained for the contacts, where any gaps in the marker trajectories were
stimulated and unstimulated conditions. The stimulus small (less than 10 frames) and force plate strikes were
signal was recorded through one of the analogue channels clean.
C. Stewart et al. / Gait & Posture 26 (2007) 482488 485

4. Results Fig. 2 gives a set of data from one of the subjects (Subject
4). This subject illustrates the general trends most clearly. In
Each subject was able to tolerate a strong contraction every graph the mean of the stimulated curve lies outside the
in both gastrocnemius and soleus. A hand held dynam- range of 1 standard deviation for part of the gait cycle.
ometer was used to estimate the moment production in Because force produces acceleration, rather than displace-
each case and the magnitudes were in the order of ment, there will be a time delay before peak displacement is
510 Nm. observed. Effects, which occur much later in the gait cycle,
Unsurprisingly during gait the most marked effects were however, particularly in swing phase, may be compensa-
seen for the second stimulation interval (foot flat to toe off), tions, as the subject will have had sufficient time to make
where the FES burst duration was the longest. The changes volitional alterations to their gait pattern. The direct effects
observed in the sagittal plane were also greater than those in of the stimulation perturbations are likely to peak around
the coronal or transverse planes. As a result only sagittal midstance and may be interpreted as the dynamic action of
plane data for the lower limb during for the second the muscle. During third rocker the force in the calf muscles
stimulation interval will be presented here. is very high. It is, therefore, less likely that a significant

Fig. 2. Sagittal plane kinematic data for Subject 4 for stimulation of gastrocnemius (left hand column) and soleus (right hand column). The band between the
dotted lines represents the interspersed unstimulated trials (1 standard deviation). The dark line is the mean of the stimulated trials.
486 C. Stewart et al. / Gait & Posture 26 (2007) 482488

Fig. 3. The differences between the means of the five stimulated trials and the interspersed five unstimulated trials for Subject 4. The differences are scaled by
the standard deviation of the unstimulated trials. The horizontal axis gives the percentage of the gait cycle (0100%). Knee flexion and ankle dorsiflexion are
positive.

change in kinematics will result from the augmentation of directly related to the normal step-to-step variation. Fig. 3
force produced by the addition of FES. illustrates the resulting curves for knee and ankle kinematics
For each point in the gait cycle 10 data points were of Subject 4, with the y-axis in standard deviations and the
available, 5 from the stimulated trials and 5 from the duration of the stimulation indicated.
unstimulated trials. The difference between the means of the The upper graph shows the effect at the knee.
stimulated and unstimulated trials was then calculated. This Gastrocnemius stimulation leads to a positive change
was then scaled by dividing by the standard deviation of the (greater flexion) and soleus stimulation to a negative change
five unstimulated points. The effect of this is to make the (greater extension). The lower graph shows the effect at the
measured change independent of the measurement units and ankle. Again, gastrocnemius stimulation leads to a positive

Fig. 4. Action of gastrocnemius and soleus during second rocker for all five subjects. A point is marked on the graph when the mean of five stimulated traces
differed from the mean of five interspersed unstimulated traces by at least 2 standard deviations.
C. Stewart et al. / Gait & Posture 26 (2007) 482488 487

change (greater dorsiflexion) and soleus stimulation to a The data from all five subjects demonstrate that soleus
negative change (greater plantarflexion). The direction of acts to restrain dorsiflexion after foot flat, in agreement with
the change is interpreted as the dynamic action of the the general consensus in the literature. When the muscle is
muscle. Subject 4 clearly has opposing actions at the knee stimulated dorsiflexion is decreased. This action is, however,
and ankle for gastrocnemius and soleus. The action of entirely absent in this group when gastrocnemius is
gastrocnemius as a knee flexor and ankle dorsiflexor is stimulated. In fact, four of the five subjects show the
particularly surprising. opposite effect. Gastrocnemius activity appears to promote,
A threshold of significance was set at 2 standard rather than restrain, tibial advance. This role of gastro-
deviations. An effect, which produces a change of this cnemius as a dorsiflexor is surprising, given its anatomy and
magnitude will be large. The period of interest was taken to no other evidence has been found in the literature confirming
be from foot flat to toe off and for this region the areas where this finding. Further musculoskeletal modelling work may
a 2 standard deviation change is observed are marked with a help to explain these observations, in particular IAA
solid horizontal line. simulations focusing on stance phase ankle control.
Fig. 4 gives the equivalent results, in summary, for all five At the knee opposing actions are again observed in
subjects. It shows the regions where stimulation led to a gastrocnemius and soleus. The common understanding of
change of at least 2 standard deviations, the sign of the change the plantarflexion/knee extension couple is that calf muscle
being interpreted as the dynamic action. Each point on the activity can promote knee extension in stance phase by
figure represents 2% of the gait cycle. The trends observed for advancing the ground reaction vector. Increased knee
Subject 4 can now be analysed for the whole group. extension is clearly demonstrated for soleus in three of
At the knee, all subjects showed significantly increased the subjects. Once again gastrocnemius seems to have the
knee flexion when gastrocnemius was stimulated. The time opposite action, promoting knee flexion in all subjects. Here,
taken to reach the required threshold varied but the trend is there is supporting evidence from Neptune et al.s [14]
clear. A delay is unsurprising given the time taken for the model-based study, which also reported the two muscles
resultant acceleration to produce a significant displacement. acting in opposition at the knee. It would appear that, when
Three subjects show the opposite action for soleus, with the foot is on the ground, ankle dorsiflexion and knee flexion
stimulation causing greater knee extension. Inspection of the are coupled, as are ankle plantarflexion and knee extension.
raw data for Subject 2 showed that the same trend was also In the case of gastrocnemius the effects at the knee seem to
present throughout the stimulation period; however, the dominate the apparent anatomical action at the ankle.
magnitude peaked at 1.4 standard deviations and so failed to Not all of our subjects showed the general trend described
reach the threshold. Subject 5 showed the opposite effect, at both joints and for both muscles. Two subjects failed to
with soleus stimulation leading to increased knee flexion. reach the two standard deviation threshold, Subject 2 at the
At the ankle, four subjects showed significantly increased knee for soleus stimulation and Subject 1 at the ankle for
dorsiflexion when gastrocnemius was stimulated. Again the gastrocnemius stimulation. Two standard deviations represent
time to reach the threshold varied but the trend was clear. For a high threshold and in one of these cases a clear change could
Subject 4 the threshold was achieved relatively late but, as be seen in the raw data (not presented here) at a lower level.
can be seen from Fig. 3, a lower magnitude change occurred Subjects 1 and 2 had the lowest stimulation moments, as
much earlier. Subject 1 failed to produce a change in ankle measured with the dynamometer, which may have con-
angle on gastrocnemius stimulation. Stimulation of soleus tributed to the failure to observe an effect. The stimulation
produced increased ankle plantarflexion in all subjects. magnitude does depend on individual subject tolerance levels.
From these data, an overall trend emerges, with The variability seen in Subject 5 is harder to explain. In
gastrocnemius and soleus appearing to have opposing his case soleus stimulation appeared to lead to increased
actions at the ankle and knee in second rocker. For only one knee flexion. One possibility is that the stimulation current
stimulation condition (soleus), at one joint (the knee), for was also affecting gastrocnemius. The effect at the ankle is,
one subject (Subject 5) do the results directly contradict this however, entirely consistent with the general trend for both
trend and this requires further discussion. There is also muscles. There does not seem to be a marked difference in
variability in the magnitude of the response between gait patterns between the subjects, which were consistently
subjects. within normal limits.
Overall, it is likely that the variability observed arose
from differences in the magnitude of the stimuli, the
5. Discussion electrical isolation of the muscles, the mass properties of the
limb segments, the individual musculoskeletal geometry or
The results of this study appear to show antagonistic tissue interconnections. It will be interesting to see whether
activity in gastrocnemius and soleus during stance phase of the differences between subjects are also reflected in their
normal gait. The five subjects did, however, respond individual IAA results. A larger study would be necessary to
differently to the stimulation and this variability is also explore the extent of variability within the normal
discussed below. population and the factors influencing it.
488 C. Stewart et al. / Gait & Posture 26 (2007) 482488

Despite the variability, a general trend emerges and it is common peroneal nerve could produce a flexor pattern, as
interesting to explore the implications of the observations observed for gastrocnemius. It is, however, very unlikely
made. Gastrocnemius and soleus, both inserting into the that sufficient current reached the nerve to have any effect
Achilles tendon, are working apparently antagonistically at and no dorsiflexion, or tension in the dorsiflexors or
two adjacent joints. It is difficult to think of another similar hamstrings was observed during testing on the couch.
example. Given that the muscles work synergistically in This study has cast new light on the role of the triceps
much of stance phase how could this action be explained? surae muscles in normal gait. Evidence is presented for
The main effect would appear to be loading of the Achilles gastrocnemius and soleus having antagonistic actions at
tendon in second rocker so it is possible to speculate that the ankle and knee, in at least some normal subjects. The role of
muscles may be storing elastic energy for release during gastrocnemius, which produced dorsiflexion in four out of
third rocker. five subjects, is particularly surprising. FES stimulation
It is difficult to draw any firm conclusions about provides a sudden perturbation in muscle force, making its
pathological mechanisms from this work using normal results suitable for direct comparison with those from
subjects. The calf muscles are, however, often associated models based on IAA. This study has provided experimental
with the pathological gait patterns and implicated in the evidence for the differing roles of gastrocnemius and soleus
development of equinus or calcaneus deformities of foot and revealed by IAA and reported in the literature.
ankle and crouch or hyperextension patterns at the knee. It is
tempting to conclude that equinus with hyperextension can
be blamed on overactivity of soleus (or weakness of
gastrocnemius) and crouch and calcaneus on overactivity of References
gastrocnemius (or weakness of soleus). Unfortunately such
[1] Klein P, Mattys S, Rooze M. Moment arm length variations of selected
simple conclusions are often comfounded by the complex muscles acting on the talocrural and subtalar joints during movement:
interaction of many factors, both primary pathology and an in vitro study. J Biomech 1996;29(1):2130.
secondary compensations. [2] Sutherland DH. An electromyographic study of the plantar flexors of
The work described here for normal subjects will need to the ankle in normal walking on the level. J Bone Joint Surg Am
be repeated for a range of different pathologies. It will be 1966;48(1):6671.
[3] Perry J. Gait analysis: normal and pathological function. Thorofare,
interesting to see what FES stimulation and IAA modelling NJ, USA: SLACK Incorporated; 1992.
reveal in patient groups with weakness, control deficits and [4] Bleck E. Orthopaedic management in cerebral palsy. Oxford: MacK-
skeletal deformities. eith Press; 1987.
The conclusions of this study need to be considered in the [5] Sutherland DH, Olshen R, Biden E, et al. The development of mature
walking. Oxford: MacKeith Press; 1988.
light of its limitations, some of which have already been
[6] Gage JR. Gait analysis in cerebral palsy. Oxford: MacKeith Press;
discussed in the context of the variability observed. When 1991.
stimulating muscles it is possible to define precisely the [7] Chambers HG, Rose J. Dynamic electromyography. In: Chambers HG,
stimulation timing and waveform. It is, however, difficult to Rose J, Gage JR, editors. The treatment of gait problems in cerebral
correlate this directly with muscle force, which develops palsy, Cambridge: MacKeith Press; 2004. p. 13445. Chapter 9.
more slowly. Ideally stimulation would produce short, [8] Simon SR, Mann RA, Hagy JL, Larsen LJ. Role of the posterior calf
muscles in normal gait. J Bone Joint Surg Am 1978;60(4):46572.
discrete, instantaneous step changes in muscle force [9] Sutherland DH, Cooper L, Daniel D. The role of the ankle plantar
allowing the effects to be assessed at precisely controlled flexors in normal walking. J Bone Joint Surg Am 1980;62(3):35463.
stages of the gait cycle. Experience from this study indicates [10] Anderson FC, Pandy MG. Dynamic optimization of human walking. J
that this is unrealistic. It is also possible that soft tissue Biomech Eng 2001;123(5):38190.
interconnections can cause attenuation of the force between [11] Kepple TM, Siegel KL, Stanhope SJ. Relative contributions of the
lower extremity joint moments to forward progression and support
origin and insertion. This is a particular risk for gastro- during gait. Gait Posture 1997;6:18.
cnemius where the electrodes were placed high to achieve [12] Schwartz M, Lakin G. The effect of tibial torsion on the dynamic
isolation. Testing on the couch provided reassurance here, as function of the soleus during gait. Gait Posture 2003;17(2):1138.
gastrocnemius stimulation produced much stronger plantar- [13] Hof AL, Otten E. Assessment of two-dimensional induced accelera-
tions from measured kinematic and kinetic data. Gait Posture 2005;22
flexion than knee flexion.
(3):1828.
The stimulation current will also cross boundaries, [14] Neptune RR, Kautz SA, Zajac FE. Contributions of the individual
affecting other adjacent muscles. Soleus, in particular, ankle plantar flexors to support, forward progression and swing
cannot be totally isolated but we feel it is unlikely that any initiation during walking. J Biomech 2001;34(11):138798.
cross-activation produced a contraction strong enough to [15] Chen G. Induced acceleration contributions to locomotion dynamics
influence the results in most cases, with the possible are not physically well defined. Gait Posture 2006;23(1):3744.
[16] Baker LL, Wederich CL, MeNeal DR, Newsam C, Waters RL.
exception of Subject 5. The different results obtained from Neuromuscular electrical stimulation: a practical clinical guide.
gastrocnemius and soleus provide some reassurance that Downey, CA: Ranchos Los Amigos Rehabilitation Centre, Ranchos
satisfactory isolation has been achieved. Stimulation of the Los Amigos Hospital; 2000.

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