Download Human gait as a step in evolution

Editorial
Brain (2002), 125, 2589±2590
Human gait as a step in evolution
The nervous systems in various species do not change rapidly
in evolution. Yet the idea that human gait would be controlled
in much the same way as it is in other mammals, or indeed
even in invertebrates (Clarac et al., 2000) has met a lot of
resistance (Capaday, 2001). Nevertheless, as evidenced by
Dietz et al. in this issue of Brain (Dietz et al., 2002), we
should take this evolutionary idea seriously.
From the work on cats it is known that the rhythmic muscle
activities during gait are generated by specialized neural
circuits located in the spinal cord (the so-called central
pattern generator, CPGs for locomotion). Each limb is
controlled by such a CPG, either located in the rostral or in
the caudal spinal cord, subserving forelimb and hind limbs,
respectively (Duysens and Van de Crommert, 1998). These
CPGs are coordinated by neurones, which interconnect both
sides or which transmit information between the cervical and
lumbar spine (Dietz, 2002a, b). Each CPG is guided by
sensory feedback to facilitate the transitions between the
phases of the step cycle. Two important sources of feedback
to the CPGs have been identi®ed. First, signals about the
loading and unloading of the limb are important. During the
stance phase of gait the load signals increase extensor activity
(extensor reinforcing re¯ex) while at the same time suppressing the onset of swing. At end stance the loading
decreases and swing can be initiated (Duysens and Pearson,
1980; for review see Duysens et al., 2000). A second signal
relates to hip position (Andersson and Grillner, 1981). At end
stance the extension of the hip is a powerful cue for the
initiation of the swing phase. This cue is thought to come
from the stretch of hip ¯exor muscles at the end of the stance
phase (Hiebert et al., 1996).
Do these cues play a role in human locomotion as well? It
would be quite surprising if basic mechanisms, such as the
regulation of phase transitions during gait, were to stop with
the advent of man. Yet, it has been quite dif®cult to obtain
good evidence, especially in man with an intact nervous
system in which cortical inputs can overrule underlying re¯ex
mechanisms. So far, the strongest evidence comes from two
types of human subjects in which the spinal cord receives
relatively little cortical input, namely either from infants or
from patients with spinal cord injury (SCI).
In infants the importance of loading and hip position was
demonstrated by hip extension inducing locomotor movements (Pang and Yang, 2000) and by showing that sudden
loading of the leg can prolong the stance phase and produce a
delay in the ensuing swing phase equivalent to that observed
in the decerebrate cat (Yang et al., 1998).
ã Guarantors of Brain 2002
In SCI patients one has another chance to study what the
spinal cord can achieve in the absence of corticospinal input.
First, Dietz and his group demonstrated the importance of
load feedback for gait in these patients by showing that
manipulation of this feedback is crucial in locomotor
recovery (Dietz et al., 1994). In the present issue, the
question of hip and load feedback is raised in the context of
imposed movements in SCI patients with a complete lesion.
The paper from the Dietz laboratory on SCI (Dietz et al.,
2002) shows that a close to normal rhythmic locomotor
pattern can be elicited when a robotic device [driven gait
orthosis (DGO), see Fig. 1] is used to assist the movements in
these patients, who cannot walk independently.
When the imposed movements were restricted to the hip
(the knee and ankle being held in an extended position) a
close to normal locomotor EMG pattern could be elicited,
provided the appropriate level of body weight support was
given. In contrast, imposed movements at the ankle were
ineffective to generate these near normal patterns. The data,
although obtained so far on a limited number of patients,
provide convincing evidence for an involvement of hip and/or
load afferents in the generation of locomotor activity. A
complete separation of these two inputs was not possible
since imposed movements at 100% body unloading were
ineffective in eliciting locomotor patterns.
The DGO experiments, described in this issue, promises to
provide some new and exciting data on the issue of interlimb
coordination during gait as well. Unilateral DGO-assisted
movements did induce much less contralateral stepping
movements in SCI patients than in normal controls during
unloaded gait. The present study is the ®rst to describe such
limited coordination between the two legs in SCI patients,
thereby illustrating that coupling between CPGs is weak
when the input from supraspinal structures is reduced. This is
in line with cat data showing that interlimb coupling in spinal
cats is much weaker than in cats with intact supraspinal
control (Dietz, 2002a, b). The present type of evidence is very
timely since several recent studies on humans, mostly again
from the Dietz group, have shown that human interlimb
coordination and re¯exes during locomotor related activities
are organized much in the same way as it is in the cat (Dietz
et al., 2001; Wannier et al., 2001).
The clinical importance of the Dietz et al. (2002) study is
best illustrated by the very tool used to investigate the
experimental question. The DGO, as illustrated in Fig. 1, is
routinely used to train SCI patients on a treadmill. Dietz was
one of the ®rst neurologists to realize that gait training on a
2590
Editorial
Capaday C. Force-feedback during human walking. Trends
Neurosci 2001; 24: 10.
Clarac F, Cattaert D, Le Ray D. Central control components of a
`simple' stretch re¯ex. [Review] Trends Neurosci 2000; 23: 199±
208.
Dietz V. Do human bipeds use quadrupedal coordination? Trends
Neurosci 2002a; 25: 462.
Dietz V. Proprioception and locomotor disorders. Nat Rev Neurosci
2002b; 3: 781±90.
Dietz V, Colombo G, Jensen L. Locomotor activity in spinal man.
Lancet 1994; 344: 1260±3.
Dietz V, Fouad K, Bastiaanse CM. Neuronal coordination of arm
and leg movements during human locomotion. Eur J Neurosci 2001;
14: 1906±14.
Fig. 1 Driven gait orthosis (DGO).
treadmill could be used to recover locomotor ability in
patients with SCI (Dietz et al., 1994). The idea arose from
knowledge of cat physiology, since it was long known that
spinal cats can be successfully trained to walk on a treadmill,
provided there is enough body weight support (Duysens et al.,
2000). In addition, some passive movement assistance is
often needed and the DGO was developed for this purpose.
The present data illustrate that imposed hip extension in
combination with body weight support could be very
important in treadmill training, thereby con®rming earlier
clinical experience. In this way, the Dietz study illustrates
that insight into evolution of the nervous system can lead to
better therapy.
J. Duysens
Department of Biophysics,
University Nijmegen and SMK-research,
Nijmegen, The Netherlands
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