A JOURNAL OF NEUROLOGY
Locomotion in stroke subjects: interactions
between unaffected and affected sides
Evelyne Kloter, Markus Wirz and Volker Dietz
Spinal Cord Injury Centre, Balgrist University Hospital, Forchstrasse 340, CH-8008 Zu ¨rich, Switzerland
Correspondence to: Prof. Dr Volker Dietz,
Spinal Cord Injury Centre,
Balgrist University Hospital,
The aim of this study was to evaluate the sensorimotor interactions between unaffected and affected sides of post-stroke
subjects during locomotion. In healthy subjects, stimulation of the tibial nerve during the mid-stance phase is followed by
electromyography responses not only in the ipsilateral tibialis anterior, but also in the proximal arm muscles of both sides, with
larger amplitudes prior to swing over an obstacle compared with normal swing. In post-stroke subjects, the electromyography
responses were stronger on both sides when the tibial nerve of the unaffected leg was stimulated compared with stimulation of
the affected leg. This difference was more pronounced when stimuli were applied prior to swing over an obstacle than prior to
normal swing. This indicates an impaired processing of afferent input from the affected leg resulting in attenuated and little
task-modulated reflex responses in the arm muscles on both sides. In contrast, an afferent volley from the unaffected leg
resulted in larger electromyography responses, even in the muscles of the affected arm. Arm muscle activations were stronger
during swing over an obstacle than during normal swing, with no difference in electromyography amplitudes between the
unaffected and affected sides. It is concluded that the deficits of the affected arm are compensated for by influences from the
unaffected side. These observations indicate strong mutual influences between unaffected and affected sides during locomotion
of post-stroke subjects, which might be used to optimize rehabilitation approaches.
Keywords: stroke subjects; spinal reflexes; quadrupedal coordination; locomotion; sensorimotor deficit; spastic hemiparesis
Normal human locomotion is based on programmed activity within
spinal neuronal circuits that is under supraspinal control and adapts
to actual requirements based on multisensory feedback (Dietz,
1992). A defective reflex function is suggested to lead to impaired
stepping movements, which are associated with an increased risk of
falls and are a prominent clinical feature in patients suffering move-
ment disorders such as Parkinson’s disease or stroke (Lamontagne
et al., 2007). Modulation of homonymous (Zehr et al., 1998;
Tanabe et al., 2006; Schindler-Ivens et al., 2008) and heteronymous
(Dyer et al., 2009) spinal reflex activity is impaired in stroke subjects
and leads to abnormal inter-joint coordination (Finley et al., 2008;
Dyer et al., 2009).
Recent evidence suggests that bipedal gait involves arm move-
ments, corresponding to quadrupedal locomotion, to stabilize the
body (Dietz, 2002; Michel et al., 2008) and to keep balance
during obstacle avoidance movements (Michel et al., 2007). This
persistent quadrupedal limb coordination during locomotion is also
reflected in the behaviour of spinal reflexes (Zehr and Stein, 1999;
doi:10.1093/brain/awq370 Brain 2011: 134; 721–731 |
Received April 26, 2010. Revised October 1, 2010. Accepted November 9, 2010. Advance Access publication February 8, 2011
? The Author (2011). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved.
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Dietz et al., 2001). For example, during locomotion—but not
during stance—reflex responses to tibial nerve stimulation appear
in the proximal muscles of both arms. In addition, neuronal activity
coupling arm and leg movements is upregulated prior to swing
over an obstacle (Michel et al., 2008). Surprisingly, appropriate
activation of arm muscles is preserved during locomotion of
subjects with Parkinson’s disease, although arm movements are
attenuated (Dietz and Michel, 2008).
Arm movements are also reduced on the paretic side of stroke
subjects, which might have an influence on stepping performance.
However, arm swing remains synchronized with stride frequency
(Ford et al., 2007) and post-stroke subjects are able to adapt
interlimb coordination of the legs to walk at different speeds on
a split-belt treadmill (Reisman et al., 2007). Nevertheless an
abnormal coupling of upper and lower limb muscles was described
in subjects following stroke (Debaere et al., 2001; Kline et al.,
2007; Barzi and Zehr, 2008; Stephenson et al., 2010) or cervical
spinal cord lesions (Calancie et al., 1996). The disturbed inter- and
intra-limb coupling is assumed to contribute to falls in post-stroke
subjects (Marigold et al., 2004; Marigold and Eng, 2006;
Lamontagne et al., 2007; Finley et al., 2008; Divani et al.,
2009; Lamontagne and Fung, 2009).
The use of reflex testing to investigate quadrupedal coupling of
limb movements during locomotion may offer more insight into
several aspects of movement disorder in stroke subjects. First,
recording bilateral arm muscle reflex responses to unilateral tibial
nerve stimulation prior to normal and obstacle swing allows the
study of the task-modulated processing of afferent input from
the unaffected and affected legs. Second, bilateral arm muscle
activation during normal and obstacle swing allows the study of
automatic efferent control of arm movements. In healthy subjects,
this arm muscle activation follows the preceding pattern of reflex
activity (Michel et al., 2008).
In stroke subjects, it is hypothesized that arm muscle reflex
responses to leg nerve stimulation and arm muscle activation
during normal and obstacle steps are impaired on the affected
side. This is thought to be especially true when the nerve of the
spastic leg is stimulated and when the affected leg swings over the
Materials and methods
This study was approved by the Ethics Committee and conformed to
the standards set by the Declaration of Helsinki. All subjects were
informed about the experiment and gave written consent for their
Seventeen subjects with stroke were included in this study (Table 1). The
inclusion criteria were a hemiparesis due to ischaemic or haemorrhagic
stroke 6 months or longer before enrolment, age 418 years, the
ability to walk independently (Functional Ambulation Category 53)
(Holden et al., 1986) for at least 10min and cognitive function
sufficient to follow the instructions. In addition, the 10m walk test
was applied (Rossier and Wade, 2001). The clinical Fugl-Meyer test
(Fugl-Meyer et al., 1975) was used to assess the sensorimotor
deficits in the affected upper limb. Subjects with pre-existing or concomi-
tant conditions interferingwith theability towalk (e.g. totaljoint replace-
ment, severe osteoarthritis or cardiopulmonary disease) or epilepsy were
excluded. Subjects were recruited from an outpatient rehabilitation
centre and from a subject database (convenience sample).
General procedures and conditions
In order to ensure inclusion and exclusion criteria, the motor capacity
of each subject was assessed using the Functional Ambulation
Subjects walked with full vision on a split belt treadmill (Woodway,
Weil am Rhein, Germany) with both belts running simultaneously at
1.4–2.8km/h. In this range the individually most comfortable speed
was chosen. Subjects’ arms moved freely during walking. Force sensors
located under the right and left treadmill belts detected ‘heel strike’
and ‘toe off’ for both feet. Two custom-built obstacle devices were
placed on either side of the treadmill (Fig. 1A) (Erni and Dietz, 2001;
van Hedel et al., 2002). The experimental details have been described
previously (Dietz and Michel, 2008; Michel et al., 2008).
In short, the obstacle consisted of a foam stick placed 7–14cm
above the treadmill belt, according to the individual patient’s ability.
The stick was attached to the obstacle machine in such a way that it
passively fell off if the subject touched it while attempting to overstep
it. The heel strike signal randomly triggered the obstacle machine at
either the right or left side to release the obstacle. After release, the
obstacle moved at the same speed as the belt and the subjects could
step over the obstacle with either foot without changing their rhythmic
walking cadence. At the end of the treadmill, the obstacle folded up
and moved back to its starting position at the front of the treadmill.
Before the experiment, subjects adapted to walking on the treadmill
without obstacles and stimulation for ?8min. The experiment itself
lasted 25–30min including a break after ?10min of walking.
The protocol comprised 70 trials, with seven different experimental
conditions. Each condition was recorded 10 times in random order,
prior toexperimental testing.
Table 1 Clinical data of the stroke subjects included in the
Fugl-Meyer test: maximum score for upper limbs = 66.
Brain 2011: 134; 721–731E. Kloter et al.
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Locomotion in stroke subjectsBrain 2011: 134; 721–731 |
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