Beruflich Dokumente
Kultur Dokumente
191205, 2003
Abstract
We recorded basic gait features and associated patterns of leg muscle activity, occurring during continuous body progression when
humans walked along a curved trajectory, in order to gain insight into the nervous mechanisms underlying the control of the asymmetric
movements of the two legs. The same rhythm was propagated to both legs, in spite of inner and outer strides diverging in
length(P < 0.001). There was a phase lag in limb displacement between the inner and outer leg of 7% of the total cycle duration
(P 0.0001). Swing velocity was greater for outer than inner foot (P < 0.001). The duration of the stance phase diminished and
increased in the outer and inner leg (P < 0.01), respectively, and was associated with trunk leaning toward the inside of the path. Muscle
activity was not dramatically altered during curved walking. The amplitude of soleus burst during stance increased in the outer
(P < 0.05) and decreased in the inner leg (P < 0.05), without changes in timing. Tibialis anterior activity increased in both legs during the
swing phase (P < 0.05); it was advanced on the outer and delayed on the inner side (P < 0.01; 2% of the cycle). The peroneus longus
burst decreased in both legs, but more in the inner than the outer leg, and lasted longer in the inner leg at the onset of swing. Closing the
eyes did not affect the gait pattern and muscle activity during turning. The command to walk along a curved path may exploit the basic
mechanisms of the spinal locomotor generator, thereby limiting the computational cost of turning.
Introduction
Walking is a common motor behaviour of everyday life. It consists of
cyclic events ultimately produced by central pattern-generating networks (CPGs) located within the spinal cord (Grillner, 1981; Pearson,
1993; Rossignol, 1996; Burke, 2001). Interestingly, when isolated,
these circuits may remain functional and may still be able to produce
the basic motor pattern for walking in humans (Bussel et al., 1996;
Dimitrijevic et al., 1998; de Leon et al., 2001). Human walking, which
is often directed by a behavioural goal and normally occurs under
different visual and spatial constraints, must imply the modulation of
basic pattern-generating networks in order to fit the requirement of
ongoing navigation. Nevertheless, although the walking process is
devoted to steering the body through space and sometimes through
circuitous pathways, it is relatively unknown how gait features and
patterns of muscular activity are modified to adapt body movements to
planned trajectories.
In the companion paper, we described several basic features of the
organization of body movements when locomotion was executed along
a curved path. Stereotyped spatial and temporal patterns of head, trunk
and foot displacements were identified, the movements of which often
preceded changes in locomotor direction (heading), and conditioned
the amplitude of the subsequent turn. Our analysis provided a general
framework upon which to pursue the study of the motor implementation of the neural command to produce an appropriate trajectory
(Berthoz & Viaud-Delmon, 1999).
doi:10.1046/j.1460-9568.2003.02737.x
Turning imposes mechanical constraints inherent to the displacement along a curved path, as for example the different stride lengths of
inner and outer limbs, resultant torques and the production of centripetal forces necessary to maintain the dynamic body equilibrium
(see companion paper). Progression along the curve was also accompanied by head rotation in space and head yaw with respect to heading
direction (Grasso et al., 1996; Grasso et al., 1998a; Grasso et al.,
1998b; Hollands et al., 2001; Glasauer et al., 2002), both producing
asymmetrical vestibular and neck inputs (Gdowski & McCrea, 1999,
2000), presumably mirrored in the pattern of propulsive muscle action.
These constraints must require substantial adaptive changes in CNS
activity for the production of turning behaviour which, in turn, would
possibly transform the symmetrical spatio-temporal pattern issued
from the CPG into an asymmetrical configuration. Displacement of
the body centre of mass toward the inner foot also occurs, frequently
associated with a sustained roll inclination of the trunk directed to the
interior of the curve (see also Patla et al., 1999; Hollands et al., 2001;
Vallis et al., 2001). Consequently, this asymmetric displacement of
body masses provokes the loading of the inner foot whereas, at the
same time, the outer leg is unloaded. Such re-distribution of force
might induce changes in the pattern of the muscular action (Duysens &
Pearson, 1980; Stephens & Yang, 1999; Fouad et al., 2001), and
certainly induces changes in the turn-related sensory feedback (Dietz
et al., 2001). The central command would therefore take into account
such deliberate readjustment in the reciprocal orientation of the body
segments.
However, deep modifications of motor and sensory processing, with
respect to the well-oiled operations occurring during straight-ahead
locomotion, might pose a challenge to the efficiency of the spinal cord
centres and of the locomotor apparatus during turning (Alexander,
1989). The CNS must optimize its organization to maximally exploit
the locomotor direction change during one gait cycle was calculated as
the difference in heading between two successive heel strikes of one leg.
Subsequently, the co-ordinates of the different markers were converted
in the body-centred reference frame, whose X axis matched the heading
direction, through co-ordinate transformation. Following this, angles of
trunk, foot and limb axis segments were computed.
Determination of gait events
The stride cycle was considered the interval between two successive
heel strikes of one leg. In this paper we considered for further analysis
only gait cycles whose heading change was >408. Indeed, when
subjects walked along curved paths, heading change was generally
>408, whereas smaller angles corresponded to the transition from
straight to curved trajectories. Selected cycles were then expected to
provide more consistent information concerning turn-related gait
organization (in some figures, cycles associated with intermediate
heading changes are also included, and additions are indicated). Onsets
of swing phases were based on rates of change of foot vertical
translations. A threshold of foot clearance was set at 10% of maximal
peak velocity of foot vertical displacement during the swing phase.
Gait parameters
Gait cycle duration was taken as the time interval between two
successive heel strikes of one leg. Stance and swing duration was
computed and converted to percentages of total cycle duration. For
each leg, stride length was measured as the linear translation of the
malleolus between two successive heel strikes. The body displacement
was also computed as the length of the body mid-point path during the
entire time-interval of the cycle:
Body path=cycle
n1 q
X
xi1 xi 2 yi1 yi 2 zi1 zi 2
i1
where n is the number of acquired frames during the gait cycle. The
average velocity of body displacement was computed as the body path
length divided by the duration of the gait cycle. As turning affected the
walking speed (see companion paper), a speed-independent index
(Sekiya & Nagasaki, 1998) was used in order to assess the relationship
between gait parameters across the two walking directions and left and
right legs. A walking ratio was computed as the stride length divided by
the step frequency.
Limb displacements
Inter-limb coordination was calculated as the phase difference (DF)
between angular displacements of left and right limb axes:
DF 360 Dt=T
Data processing
Kinematic sampling and EMG data recordings were synchronized at
rates of 100 and 1000 Hz, respectively. Data from each trial were
ensemble-averaged after time interpolation over individual gait cycles
to fit a normalized 1000-point time base.
Elaboration of kinematics data
Co-ordinate frames
Co-ordinate frames that describe body motion while moving through
space were defined in a hierarchical manner as described by Imai et al.
(2001). The primary co-ordinate frame was the space-fixed reference
frame of the video system (XS, YS, ZS). Instantaneous heading direction
was defined as the angle of the instantaneous linear velocity vector of the
body mid-point (see the companion paper for details) in the horizontal
plane with respect to the space-fixed reference frame. The amplitude of
where T is the duration of the inner (right) limb cycle and Dt is the
difference between the time at which the outer (left) limb reaches its
angular peak (heel strike) and the time halfway between the two
successive angular peaks (heel strikes) of the inner limb (see inset of
Fig. 4). Given this definition, if the left and right limbs move 1808 out
of phase, DF would be equal to zero. In turn, when DF is positive,
contralateral heel strike occurred beyond half of the cycle, thus
indicating a phase lag of the outer with respect to the inner limb.
Mean velocity of limb endpoint displacements were evaluated as
average velocities of malleolus displacements during the swing phase.
Elaboration of EMG data
Temporal EMG features
Onsets and ends of EMG burst activity were established at the points at
which muscle activity was, respectively, greater or less than mean
2003 Federation of European Neuroscience Societies, European Journal of Neuroscience, 18, 191205
Results
The analysis of the results has been deliberately focused here on the
spatio-temporal gait and muscular events occurring after the completion of the transition between straight-ahead and turning, i.e. when the
turning behaviour had reached a plateau (see Materials and methods).
A total of 337 and 428 gait cycles where analysed during straightahead and turning, respectively. Subjects were similarly represented,
because each contributed a mean of 56 7 and 71 17 cycles for the
straight and curved paths, respectively, to the analysis.
Gait features
Spatial and temporal features of the gait pattern of all subjects across
all trials during both straight-ahead walking (SA) and turning (TU),
both with eyes open (EO) and blindfolded (BF), are detailed in
Fig. 1AC.
During straight-ahead locomotion, cycle duration and stride length
were unchanged between left and right limbs (ANOVA, side effect,
P > 0.8 for all parameters) regardless of visual condition (vision effect,
P > 0.7). Duration of cycles was close to 1 s (on the average
1.11 0.02 s). Stride length slightly decreased (5.5%) when walking
blindfolded (vision effect, F1,5 9.9, P < 0.05). A significant effect
was found in the walking ratio (length/frequency) (see Materials and
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2003 Federation of European Neuroscience Societies, European Journal of Neuroscience, 18, 191205
Fig. 1. (A) Mean duration (upper histogram) and mean stride length (lower histogram) of gait cycles performed when walking along straight or curved paths,
with eyes open (EO) or blindfolded (BF). (B) Mean values of the walking ratio (stride length divided by step frequency). The drop in the stride length of the
right (inner) leg during turning is responsible for the decrease of its walking ratio. (C) Mean velocity (left) and mean path length (right) of the body mid-point.
Mean values from gait cycles of both legs have been averaged because the body motion features is side-independent. Velocity and length of body displacements
were smaller during curved compared to straight-ahead walking. Horizontal lines with an asterisk join conditions between which significant differences
( P < 0.01) were found.
produced during two successive heel strikes of each limb during the
gait cycle. The cluster located around the zero heading change
corresponds to straight-ahead walking. Here, the difference between
the stride length and the body path length is negative because the
body mid-point covers more distance than the foot during the time
interval of the cycle (the body mid-point moves up and down, and
right and left, during normal straight-ahead walking, while stride
length is the spatial distance between two successive heel strikes).
The data point pertaining to curved walking corresponds to the
upper and lower clusters for left and right limb, respectively. Intermediate points connecting straight- and turning-related clusters
correspond to gait cycles executed during turning but at the initial
part of the curve, when the heading change is less pronounced. The
increase in distance shown for the left limb does not result from a true
increase in stride length but depends upon the decreased distance
travelled by the body mid-point during curved cycles. In turn, the
distance travelled by the body mid-point decreases because of a shift of
the body toward the inner foot. The top right diagram attempts to
provide a graphic explanation of this phenomenon. The two feet cover
imaginary paths, their distance depending on the tightness of the
trajectory curvature; the body path (grey dashed line) tends to approach
the inner foot path, thereby loading and unloading the inner and outer
foot, respectively.
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Fig. 2. Relationship between stride length and mean body velocity during (A) straight-ahead and (B) curved-gait cycles of the left (open circles) and right (filled
circles) leg. Data from all subjects and trials pooled. Mean values of (C) slope and (D) intercept of individual length-to-speed relationships, independently computed
according to the direction of walking and side of the body. Change in direction did not modify slopes of speed-to-length relationships but affected the intercept
( P < 0.01): increases in body velocity were accompanied by increases in stride length of a constant proportion under all conditions. However, at each velocity, stride
length was significantly shorter for the inner than the outer leg during curved walking.
limb, given the longer path to be travelled with respect to the inner
limb. A further aspect of the asymmetry in the characteristics of right
and left limb displacement was the different velocity of their respective
swing phases. This is shown in the plot of Fig. 4D, where velocity of
the foot swing is depicted for right and left feet as a function of the
velocity of body progression along the curve. Indeed, the intercept of
the best-fit line differed (ANOVA/ANCOVA, P < 0.0001) between the two
limbs, whereas the slope did not (t-test, P > 0.2). An example of the
larger velocity of the outer foot is shown in the Fig. 4E, where two
velocity traces are superimposed for the right (black lines) and left foot
(grey lines) during two successive swing phases taken from the centre
part of the adjacent walking trial (in which the positions of the two
malleoli are drawn every 30 ms).
EMG patterns during turning
Spatial and temporal patterns of thigh and leg muscle EMGs were little
changed between straight-ahead and curved walking for both limbs.
Typical averaged traces from one subject during EO are shown in
Fig. 5. Traces have been normalized in duration on the basis of the
cycle duration and in amplitude with respect to the EMG during
sustained maximum voluntary contraction of the corresponding mus-
2003 Federation of European Neuroscience Societies, European Journal of Neuroscience, 18, 191205
Fig. 3. (A) Typical displacement of the body mid-point during the progression
along straight or curved paths. Foot prints (the segment joining the malleolus
and the foot) of the left and right leg during the stance phases are indicated. On
the right, imaginary paths along which the body and the legs progress are
represented (see text); the direction of travel is from bottom up and clockwise.
(B) Relationship between the heading change and the difference between stride
length and path travelled by the body during one cycle. In this representation,
the displacement of each leg is referred to the body-centred reference frame.
The more the body rotates, the larger the discrepancy between the stride length
of inner and outer legs. The cycles during the straight-ahead walking correspond
to the data points around 08. Those of the transition from straight to curved paths
have been added to provide clarity to the figure, and roughly correspond to data
points between 10 and 408 of heading change.
cle (see Materials and methods). The shape of the muscular activation
pattern during straight-ahead walking is not fundamentally modified
by walking along a curved path. The soleus muscles of both legs
showed a full-blown burst during the stance phase of gait. The tibialis
anterior muscles exhibited a double-peak burst at the onset of swing,
which lasted up to the first third of the subsequent stance phase. The
rectus femoris traces were almost superimposed on the second peak of
the tibialis burst. However, small but systematic changes occurred
between inner and outer limbs in both amplitude of EMG bursts and
their relative phases (temporal lag). The first of these changes was an
increase in the amplitude of the soleus burst during the stance phase in
the left leg and a decrease in the same burst in the right leg. Secondly,
during turning, there was an opposite phase shift in the tibialis EMG
burst between left and right legs. The left was anticipated and the right
was delayed with respect to the same burst in the same leg during the
straight-ahead condition. The activity of the peroneus muscle was
recorded in three subjects only. Nonetheless, its turn-related changes
were consistent across individuals and trials. The amplitude of the
peroneus burst generally decreased during curved walking in both legs.
However, such decreases were weak in the outer leg, but a sizeable
drop in the EMG activity was observed in the inner leg. In addition, the
burst of the right peroneus was delayed during the turn with respect to
the same burst observed during straight-ahead walking (see below).
The results of the analysis made on all subjects and trials is
summarized in Fig. 6. The histograms of Fig. 6A and B depict mean
values of normalized EMG activity separated by side, visual and
walking conditions. The normalization was made based on the homonymous burst during straight-ahead walking (data from EO and BF
pooled). Mean values for the soleus burst during stance and for the
tibialis anterior burst during swing are reported in Fig. 6A and B,
respectively. The statistical analysis showed a consistent difference in
EMG activity between left (8.1%; post hoc test, P 0.05) and right
(11.1%; P < 0.05) soleus muscles during turning with respect to
straight-ahead walking (side direction effect, F1,5 11.5, P < 0.05).
Post hoc comparisons also revealed that the activity increased on the
left side but decreased on the right side (P < 0.05 for left vs. right EMG
comparisons). However, there was a general increase in the tibialis
anterior burst in both legs during turning with respect to straight-ahead
(on the average, 16.3% and 12.7% for left and right legs, respectively;
direction effect, F1,5 7, P < 0.05). The visual conditions are not
further detailed in the figure, because in no walking condition did lack
of vision modify the EMG features compared to walking EO.
The schematic diagram of Fig. 6C summarizes the main temporal
and amplitude characteristics of bursts of rectus femoris, tibialis and
soleus muscles in the two limbs, during both straight-ahead and curved
walking conditions. Onsets and ends of the boxes are the average
onsets ( SD) and ends ( SD) of muscle EMGs computed from all
subjects and EO trials. The height of the boxes corresponds to the mean
EMG amplitude ( SD) normalized with respect to straight-ahead. In
this figure, the two components of the tibialis anterior burst have been
analysed and drawn as two separate but adjacent boxes. This segregation of the two bursts of the tibialis allowed detecting a further feature
of its activity, namely a turn-specific increase (side direction effect,
F1,5 9, P < 0.05) of the first component of the right muscle compared
to the activation during straight-ahead progression (SATU post hoc
comparison for the right limb, P < 0.05). The timing characteristics of
the bursts of the various muscles can be more fully appreciated in this
representation. First, there was little variability of burst onsets and ends
for all subjects and trials, as testified by the short horizontal error bars.
Second, there was a strong consistency in the respective timing
between left limb and right limb, except for the tibialis anterior.
Indeed, the onset of the first component of the tibialis anterior burst
was slightly but significantly advanced for the left limb and delayed for
the right limb during turning with respect to the straight-ahead
conditions.
The consistency of this delay is further evident in the distribution
histograms of Fig. 7. These histograms report the distribution of the
soleus end and of the tibialis onset during the straight-ahead and
curved walking tasks, separately for left and right limbs. The interval
distribution of the end latencies of the soleus is centred around the end
of the stance phase (57% of the cycle). The onset of the tibialis is
delayed by a further 7.5% of the cycle. In addition, the width of the
distribution curve appears to be somewhat larger for the tibialis with
respect to the soleus (see range in the abscissas), regardless of the
walking condition. During turning, the soleus burst end was unaffected
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Fig. 4. (A) Mean duration ( SD) of the stance phase as a percentage of the gait cycle according to walking direction and body side. During turning, the stance
duration increased and decreased in inner and outer legs, respectively ( P < 0.01). (B) Relationship between the relative duration of the stance phase and mean trunk
roll, for all gait cycles under all conditions (except for side) pooled. The decrease in stance duration of the left (outer) leg during turning was associated with a
significant leaning of the trunk toward the interior, and vice versa for the right leg. (C) Distribution of the phase lags of the left with respect to the right leg. The
distribution shifted toward positive values during curved walking, indicating that the inner limb led with respect to the outer. The method of calculation of the phase
lag based on limb axis angular displacements of both legs is indicated in the right inset. (D). The relationship between mean malleolus velocity during the swing phase
and mean body velocity is shown. The velocity of the foot is systematically larger in the outer limb than in the inner limb owing to the larger distance to be covered by
the outer foot during the swing phase. (E) An example of the time course of the velocity of the malleolus of both legs is depicted. A simple illustration of the sidespecific modulation of the limb velocity during the turn is revealed by the representation at the centre of the panel. The instantaneous position of the malleolus of both
inner and outer leg is displayed every 30 ms. The body mid-point trajectory is also shown. Note the increasing distance between two successive positions of the outer
foot in the central part of the swing phase.
whereas the distribution of tibialis onset of left and right limbs shifted
in opposite directions (side direction effect, F1,5 32, P < 0.005).
The mean values of these changes are reported in the middle inset of
the same figure. (SATU post hoc comparison, P < 0.01 for left and
right legs). An analysis of the temporal coupling of subsequent
activations of the soleus and tibialis anterior was made according to
the trajectory type. However, we found no strong correlation between
the end of the soleus burst and the onset of the tibialis burst, regardless
of the side (r 0.05, ns; r 0.16, P < 0.05 for the left and right limb,
respectively), the trajectory followed (r 0.11, P < 0.05; r 0.05, ns
for straight and curved path, respectively), or within left and/or right
limbs during turning (r 0.08, ns; r 0.11, ns for the left and right
limb, respectively).
A general comparison of the effects of turning across left and right
soleus, tibialis anterior and peroneus longus muscles is given in Fig. 8.
Traces were obtained by averaging all signals from all subjects during
2003 Federation of European Neuroscience Societies, European Journal of Neuroscience, 18, 191205
Fig. 5. Representative EMG activity of thigh and leg muscles for left and right limb during straight-ahead and curved walking. Traces were obtained by averaging
time-normalized EMG traces for all trials of one subject walking in the eyes-open condition. EMG amplitude has been normalized in terms of maximal voluntary
contraction, and is expressed as a percentage of that activity. The time course of the ankle angle is traced at the bottom of the figure. Although the general spatial and
temporal patterns of muscle activity were not radically different between the two walking paths, the progression along the curve was accompanied by subtle limbspecific modifications in muscle activity (see text).
turning and normalizing them with respect to the mean activation during
straight-ahead walking, each limb individually processed. Figure 8
summarizes EMG changes in timing and amplitude between the corresponding muscles of inner and outer limbs during the progression along
the curved path. The shape of the envelopes, reflecting the activation
profile of muscles, was basically unchanged, as indicated by the very
high value obtained by cross-correlating the two profiles. No phase
shift was observed between right and left soleus muscles. However,
a difference was found in the timing of tibialis and peroneus
muscle bursts. The waveform profiles of the left leg led those of the
right leg by 11 and 40 ms, corresponding to temporal delays of 1.02 and
3.6% of the cycle duration, for the tibialis and peroneus muscles,
respectively.
Discussion
This investigation was an attempt to understand whether and to what
extent the central nervous system modifies its output, or part of it, in
order to produce a continuous curvilinear locomotion. Emphasis has
been put upon the analysis and comparison of straight-ahead with
curved walking.
Gait features
Frequency
Walking along the circular path, either with vision (EO) or blindfolded
(BF), produced no major changes in stepping frequency, thus indicat-
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Fig. 6. Mean values of EMG activity during straight-ahead and turning gait cycles in the soleus (A, stance phase) and tibialis muscle (B, swing phase) of both legs.
Mean values have been normalized with reference to the mean value of EMG activity during the progression along the straight path (EO and BF, respectively), for each
limb and gait phase independently ( P < 0.05). (C) Schematic illustration of EMG patterns of left and right leg muscles during straight-ahead and curved walking. For
each box, the left ( SD) and right ( SD) extremities indicate the onset and end of EMG bursts, respectively. The amplitude of the EMG activity is indicated by the
height ( SD) of the box, which is normalized to the SA value. Data were obtained by averaging mean values of all subjects. Changes in the temporal occurrence of the
EMG burst onset are indicated by a line connecting the conditions for which a significant difference (asterisk) was found. Significant changes in amplitude during
turning compared to straight-ahead walking are indicated by an asterisk ( P < 0.05).
ing that the transition from a straight to a curved path did not imply a
reorganization of rhythm production, or that the basal rhythm is
adapted to both conditions. There was also no difference in duration
of the right and left cycles during turning. The CNS would indeed
generate a strongly coupled locomotor pattern, during straight-ahead
locomotion as much as during locomotion along a curved path. It
is of interest that crayfish strongly modulate the frequency of each
locomotor limb while they progress along curved path (Domenici et al.,
1998), suggesting that temporal coupling across effectors is
not a systematic rule of turning but rather an exception of biped
walking.
The same rhythm was propagated to both legs, in spite of the
obvious but nontrivial consideration that the length of right and left
2003 Federation of European Neuroscience Societies, European Journal of Neuroscience, 18, 191205
Fig. 7. Distribution of the ends of soleus EMG burst and onsets of the first burst of tibialis anterior in the left (upper panel) and right (lower panel) leg, separated
according to the direction of walking. No difference occurred in the end of the soleus burst, regardless of side and trajectory conditions (compare upper and lower
graphs of the left panel). With respect to straight-ahead walking, the distribution of tibialis anterior burst onsets measured during turning was shifted toward lower and
higher values on the left and right leg, respectively. Limb-specific mean changes ( SD) in the occurrence of the onset of tibialis anterior burst is indicated in the inset
histogram. Significant differences are indicated as in Fig. 3.
legs matched the difference in radius of virtual circles along which the
feet moved.
Changes in temporal and spatial features of leg movements were
mirrored in the synthetic measure of gait provided by the walking ratio,
a velocity-independent index of walking pattern (Sekiya & Nagasaki,
1998). This measure confirmed that commands to produce outer leg
forward progression were the same under both straight-ahead and
curved walking. The behaviour of the inner leg was different in
amplitude of progression but not so in cadence. It is easy to conclude
that the CPG distributes its commands to the two legs with the same
frequency, which does not impede the two legs advancing at different
velocities. Others have shown that the two CPGs are normally strongly
entrained (Riek & Carson, 2001) and produce synchronous output to
the two sides of the body (Guadagnoli et al., 2000). Therefore, during
curved walking the CPG would need to distribute a differently
patterned command to the two sides, in a manner appropriate to
perform turning.
Intrinsic temporal features of gait
Not only were spatial features of inner and outer leg movements
different during turning, but also some key temporal features of the gait
pattern were changed, yet within the cadre of the unchanged frequency.
The duration of the stance phase of gait diminished and increased in
outer and inner legs, respectively. This discrepancy in the temporal
sequences of gait events of the inner and outer legs provoked a
phase lag between the overall limb displacements, which corresponds
to
7% of the total cycle duration. Changes in the phase relationship
of this entity between the two limbs have been observed during
straight-ahead walking in toddlers, and it has been suggested that
they are connected to gait instability (Clark, 1995). Conversely, we
show here that this phase lag is a necessary condition to produce body
rotation.
The longer duration of the swing or transport phase (consequence of
the shorter stance phase) allows more time for the outer leg to travel the
longer distance imposed by turning. Swing duration during turning was
longer than during straight walking, because the path travelled by the
foot was not linear during turning but bent because of the concomitant
body rotation. This explains the different vertical distance between the
lines best fitting velocity of foot swing against body progression for the
right and left foot. In other words, the difference in both stance
duration and travelling distance between left and right feet imposed
different swing velocities. In this regard, turning-related gait features
were reminiscent of those associated with the adaptation of walking on
a treadmill with split belts adjusted at different speeds. Indeed, Dietz
and collaborators (Dietz et al., 1994; Prokop et al., 1995; Zijlstra &
Dietz, 1995; Jensen et al., 1998) have shown that, under such conditions, stride length was larger on the fast side (as for the outer leg
during turning, in our case) with respect to the slow side. At the same
time, the stance duration was shortened on the fast leg whereas it
increased on the slow leg, and inversely for swing phase duration.
Concomitant with the increased duration of the stance phase of the
right, inner, leg, the trunk leant towards the interior. This was confirmed by a significant relationship between trunk roll and stance
duration. There is therefore an association between trunk leaning to the
inner side, increase of walking speed during turning (see companion
paper) and increased stance duration of the inner limb. The displacement of the trunk could contribute to the modulation of the temporal
features of the gait pattern, because loading the inner leg (and
unloading the outer leg) might produce a phase modulation through
re-afferent input from the evolving movement (see below).
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Fig. 8. Comparison of EMG envelopes of inner and outer legs, recorded during
walking along the curved trajectory. The mean profiles have been obtained by
averaging the mean traces of all subjects after normalization of their amplitude
based on muscular activity during straight-ahead cycles. The discrepancy in
leftright amplitudes is revealed by the hatched area, the pattern of which
indicates the leg for which the muscle activity increases compared to the other
leg (see legend). The quantification of the phase shift between EMG envelopes
has been obtained by cross-correlating the waveforms of the inner and outer leg.
The value of the phase lag is expressed as a percentage of the cycle and in
absolute duration, and is reported close to the corresponding traces. A positive
value means that the EMG profile of the outer leg leads that of the inner leg. The
r-value is also indicated.
EMG pattern
Subtle but consistent changes, which appear to be associated with the
above described motor behaviour, occurred in the leg muscles
The overall pattern of soleus activity was similar during turning and
straight-ahead walking. However, the amplitude of the soleus burst
decreased during stance in the inner leg (11%) and increased during
turning in the outer leg (8%). Overall, the difference between the bursts
of inner and outer legs during walking was
18%. At the same time,
left and right strides showed a discrepancy in their length (left stride
longer than right stride) of about the same amount. The precise origin
of extensor muscle modulation during walking along the curve is not
readily explained.
The relationship between EMG amplitude and stride length does not
seem to be generalisable. On the one hand, the decrease in soleus burst
amplitude during turning on the right with respect to left side can be
related to the shortening of the right stride with respect to the left. The
soleus burst of the right leg also diminished during turning with respect
to its burst during straight-ahead walking. However, in the two cases
there was no correspondence between average EMG changes and
average stride length changes. However, the left soleus increased not
only with respect to the right muscle during turning, but also with
respect to the same left soleus during straight walking. However,
during straight walking the stride length of the left leg did not change
with respect to its stride length on the curved path.
We feel that any attempt to explain these discrepancies should take
into account the fact that body orientation changes during turning. This
can create nonoptimal biomechanical conditions for the propulsive
action of the leg muscles, owing to the different spatial relationship
between the force vector produced by soleus muscle action and the
direction of the moving body. In turn, any disadvantage would be
differently shared by the two limbs. In the companion paper we
showed that foot yaw in relation to body heading was different for
the two feet during turning with respect to straight walking. In
particular, the left foot tended to approach the body trajectory while
the right foot tended to turn to the inner side of the trajectory. Within
this general trend, however, the relationship between foot positioning
and body trajectory changed during the completion of the stance phase.
At heel strike the left foot was almost aligned with heading direction
but progressively rotated with respect to body direction, thereby
diminishing the mechanical efficiency of the muscle action. This
might therefore require a stronger muscle action to support body
propulsion along the curved trajectory. Soleus activity was also larger
with respect to that recorded during straight-ahead walking,
where stride length was not different from that observed during
turning. Such an enhancement of the outer extensor muscle activity
probably contributes to the generation of the torque necessary for
producing the body turn. Moreover, because the stance phase duration
is shortened, a larger soleus activity would help create the torque for
turning.
An inverse trend was observed for the right foot, which was placed
on the floor at a wide angle with respect to heading, and became almost
parallel to body direction at the time of toe-off. This might explain the
need for less muscle activity in the right than left soleus muscle during
turning, and in the same right soleus during turning compared to
straight walking. Two further effects of turning, liable to require
modulation in opposing senses of right soleus activity, are the smaller
2003 Federation of European Neuroscience Societies, European Journal of Neuroscience, 18, 191205
Peroneus longus
During straight-ahead walking, there was a coactivation of peroneus
and soleus muscles. Such activity was not due to crosstalk between
soleus and peroneus muscles, because it was checked that pure foot
plantar flexion did not induce activity in the peroneus (see also Hunt
et al., 2001, for straight walking). Both soleus and peroneus muscles
were active during the stance phase and their bursts were similar in
shape and timing. The peroneus assists in plantar flexion and produces
abduction and eversion of the foot, which counteracts the internal
rotation action of the triceps muscle, and helps to produce the lateral
displacement of the body weight from the actual stance foot to the next,
contralateral, foot (Hunt et al., 2001). During turning, relatively large
changes occurred in the timing and amplitude of the peroneus burst
with respect to straight-ahead. First, the amplitude of the burst
decreased in both legs, but almost two times more in the inner than
in the outer leg. This general decrease in peroneus activity may be due
in part to the decrease in the body velocity during turning. Nevertheless, side-specific modification of muscle activity rather suggests
that these changes are directly connected to the achievement of body
rotation. This would be not particularly astonishing because peroneus
action produces a medio-lateral displacement of the body in addition to
helping progression. Although peroneus muscle action ensures lateral
body equilibrium, regardless of walking conditions, its functional
implication should be different during turning than during straightahead walking.
Turning implies an opposite, asymmetric, action of the two limbs in
order to produce the force pulling the body to the ever-changing
direction of the curved trajectory. In the companion paper, we reported
that the change in heading direction is associated with a narrowing of
stance width of the left leg. More precisely, the more the body rotates
the closer the distance between the line joining two successive left
(outer) footprints and the right foot print. As a consequence, the body
need not be displaced toward the inner foot because the latter is already
positioned underneath the body weight, as also indicated by the
decrease in the distance of the right foot to the body trajectory, thereby
requiring less action of the right peroneus muscle. The peroneus of the
left side, in turn, need not increase its activity during stance, either,
because its pushing action toward the inner side of the trajectory is
enhanced by the mechanical moment created by the increased distance
between the stance foot and the position of the body. During turning,
the combined muscular action of the peroneus and of the soleus of the
outer leg is then mainly devoted to assisting body rotation.
However, at the beginning of the swing phase the peroneus burst
appears to behave in a different way in the two legs: on the right side,
there is prolonged activity and relative increase of the burst amplitude.
We suggest that it is because of the relative increase in duration of the
stance phase on the right with respect to the left side, and because of
the need for the right feet to be extra-rotated to prepare the subsequent
foot heel strike.
Rectus femoris
On average, the rectus femoris was active around the transition
between swing and stance phases. In general, its activity was of
smaller amplitude than that of the other recorded muscles. No significant difference could be found in the amplitude of the bursts of the
same muscle (left or right) between straight and curved walking. No
differences were found, either, when the two limbs were compared
during turning. This was equally true in terms of timing. Increase in
rectus femoris burst has been shown to occur during rapid complete
turning and it has been explained by the need to brake body progression and allow a quick spin turn (Hase & Stein, 1999). Absence of any
2003 Federation of European Neuroscience Societies, European Journal of Neuroscience, 18, 191205
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2003 Federation of European Neuroscience Societies, European Journal of Neuroscience, 18, 191205
Acknowlegments
This research was supported by grants from the University of Pavia, the Italian
Ministry of Health and the Fondazione Salvatore Maugeri (IRCCS). G.C. was
supported by a grant from the French Minister of Research. We are most grateful
to Dr Paul Stapley, who edited the last version of the manuscript.
Abbreviations
ANCOVA, analysis of covariance; ANOVA, analysis of variance; BF, blindfolded;
CPG, central pattern-generating network; EMG, electromyography; EO, eyes
open; SA, straight ahead; TU, turning.
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