1Rehabilitation Research and
Development Center (153), Veterans Affairs Palo Alto Health Care
System, Palo Alto, California 94304;
2Department of Mechanical
Engineering,
Ting, Lena H.,
Steven A. Kautz,
David A. Brown, and
Felix E. Zajac.
Phase reversal of biomechanical functions and muscle activity in
backward pedaling. Computer simulations of pedaling have shown
that a wide range of pedaling tasks can be performed if each limb has
the capability of executing six biomechanical functions, which are
arranged into three pairs of alternating antagonistic functions. An
Ext/Flex pair accelerates the limb into extension or flexion, a
Plant/Dorsi pair accelerates the foot into plantarflexion or
dorsiflexion, and an Ant/Post pair accelerates the foot anteriorly or
posteriorly relative to the pelvis. Because each biomechanical function
(i.e., Ext, Flex, Plant, Dorsi, Ant, or Post) contributes to crank
propulsion during a specific region in the cycle, phasing of a muscle
is hypothesized to be a consequence of its ability to contribute to one
or more of the biomechanical functions. Analysis of electromyogram
(EMG) patterns has shown that this biomechanical framework assists in
the interpretation of muscle activity in healthy and hemiparetic
subjects during forward pedaling. Simulations show that backward
pedaling can be produced with a phase shift of 180° in the Ant/Post
pair. No phase shifts in the Ext/Flex and Plant/Dorsi pairs are then
necessary. To further test whether this simple yet biomechanically
viable strategy may be used by the nervous system, EMGs from 7 muscles
in 16 subjects were measured during backward as well as forward
pedaling. As predicted, phasing in vastus medialis (VM), tibialis
anterior (TA), medial gastrocnemius (MG), and soleus (SL) were
unaffected by pedaling direction, with VM and SL contributing to Ext,
MG to Plant, and TA to Dorsi. In contrast, phasing in biceps femoris
(BF) and semimembranosus (SM) were affected by pedaling direction, as
predicted, compatible with their contribution to the directionally
sensitive Post function. Phasing of rectus femoris (RF) was also
affected by pedaling direction; however, its ability to contribute to
the directionally sensitive Ant function may only be expressed in
forward pedaling. RF also contributed significantly to the
directionally insensitive Ext function in both forward and backward
pedaling. Other muscles also appear to have contributed to more than
one function, which was especially evident in backward pedaling (i.e.,
BF, SM, MG, and TA to Flex). We conclude that the phasing of only the
Ant and Post biomechanical functions are directionally sensitive. Further, we suggest that task-dependent modulation of the expression of
the functions in the motor output provides this biomechanics-based neural control scheme with the capability to execute a variety of lower
limb tasks, including walking.
Backward locomotion provides an
opportunity to test the adaptability of pattern generators in the
control of locomotion (e.g., Ashley-Ross and Lauder
1997 Computer simulations can be used to test whether a motor activity
pattern can generate backward locomotion. Simulations of walking are,
however, difficult to achieve because of the instability associated
with bipedal balance and weightbearing (Yamaguchi and Zajac
1990 Simulations of pedaling offer insight into muscle coordination
(Fregly and Zajac 1996 Simulations capable of reproducing kinematics, kinetics, and muscle
excitations in maximum-speed startup forward pedaling showed that
muscles must execute six biomechanical functions (Raasch et al.
1997
ABSTRACT
Top
Abstract
Introduction
Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Methods
Results
Discussion
References
; Duysens et al. 1996
), although neural control mechanisms are best elucidated with an understanding of the
biomechanics of forward and backward locomotion (Zernicke and
Smith 1996
). Grillner (1981)
suggested that backward walking in
the cat could be produced by a phase shift in activation of unit burst
generators controlling flexion and extension of knee and hip muscles.
Studies of backward walking in humans and cats have shown, however,
that the reconfiguration of the motor pattern proposed by Grillner
(1981)
has limitations (Buford and Smith 1990
;
Pratt et al. 1996
; Vilensky et al. 1987
).
Further, although joint power (Winter et al. 1989
) and
limb kinematics (Thorstensson 1986
; Vilensky et
al. 1987
; Winter et al. 1989
) are essentially reversed in time during backward walking, electromyogram (EMG) activity
is not reversed in all muscles (Duysens et al. 1996
; Thorstensson 1986
; Winter et al. 1989
).
However, it is unknown whether a strict reversal of muscle activity
patterns or a phase shift in activation of knee and hip muscles
(Grillner 1981
) is biomechanically sufficient to produce
backward walking. Thus whether differences observed experimentally
arise from neural adaptations to fulfill task biomechanics or from
fundamental differences underlying neurophysiological control cannot be
ascertained.
). These instabilities are absent in pedaling, thus providing a rhythmic locomotor task that can be simulated and analyzed
in isolation of the postural task (Kautz and Brown 1998
; Neptune et al. 1997
; Raasch et al. 1997
).
Pedaling is also an ideal experimental locomotor paradigm because
cadence, speed, limb phasing, limb excursion, and workload can be kept
similar. Further, because many muscle coordination patterns can
successfully produce forward pedaling (Raasch 1996
),
task biomechanics do not overly constrain the set of feasible control
strategies. Thus insight into neural control of locomotion is possible.
; Raasch et al.
1997
) by revealing muscle contributions to joint torques and
accelerations not possible from kinematic, kinetic, and EMG
observations alone. For example, the hamstrings (HAMS) do not
accelerate the knee into flexion to prevent knee hyperextension as the
limb approaches full extension (cf. Gregor et al. 1985
;
van Ingen Schenau 1990
), but rather the knee is
accelerated into extension and the crank is accelerated as well
(Andrews 1987
; Carlsoo and Molbech 1966
;
Raasch et al. 1997
). The reason the knee is not
accelerated into flexion is that the hip extensor torque produced by
HAMS acts to accelerate the knee, as well as the hip, into extension.
Although the knee flexor torque produced by HAMS does indeed act to
accelerate the knee into flexion, the effect of the hip extensor torque
dominates. In fact, soleus (SL) is the muscle that prevents knee
hyperextension in pedaling (Raasch et al. 1997
). Muscles
(or joint torques) can accelerate joints or body segments to which they
do not attach or span because of joint reaction forces arising from
the multijoint dynamical properties of the body, which are task and
body-position dependent (Zajac and Gordon 1989
). Such
insight can be gained from forward simulations, which show the
spatiotemporal contributions of joint torques (or muscle forces) to
task execution, rather than from calculation of joint torques from
external measurements, which are incapable of showing directly such
contributions. Specifically, knowledge of pedaling biomechanics
revealed through simulations was critical to the elucidation of the
basic biomechanical functions in pedaling (Raasch et al.
1997
).
). The functions are performed in different regions of the
crank cycle and can be organized into three pairs of alternating antagonistic functions to form a basis for a control strategy capable
of producing a myriad of pedaling tasks (Fig.
1) (Raasch 1996
;
Raasch et al. 1997
). Ting (1998)
reformulated the six
functions to be applicable to walking as well as pedaling (Fig.
1B). The Ext-Flex biomechanical function pair is defined by
its contribution to the acceleration of the foot (or foot contact point
with the environment), either away from (Ext) or toward the pelvis
(Flex). Thus a muscle, which acts to accelerate the foot away from the pelvis, even if the leg is flexing, contributes to the Ext function (e.g., a muscle performing an eccentric contraction whose force acts to
decelerate ongoing leg flexion). The Ant-Post pair is defined by its
contribution to the acceleration of the foot with respect to the pelvis
in the anterior (Ant) and posterior (Post) directions, respectively
(Fig. 1B), orthogonal to that produced by the Ext-Flex
functions. The Plant-Dorsi pair is defined by its contribution to an
acceleration tending to either plantarflex (Plant) or dorsiflex (Dorsi)
the foot.
View larger version (30K):
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Fig. 1.
Biomechanical functions derived from simulations (Raasch
1996 ; Raasch et al. 1997
) capable of producing a
variety of forward and backward pedaling tasks. A:
phasing of the 6 biomechanical functions in forward and backward
pedaling. The functions are arranged into 3 pairs (Ext-Flex,
Dorsi-Plant, and Ant-Post), with each pair consisting of 2 antagonistic
functions (e.g., Ext function and Flex function). Backward pedaling can
be produced with a phase shift of 180° in the Ant-Post pair.
B: Ext-Flex pair is defined by its contribution to the
acceleration of the foot (or foot contact point with the environment),
either away from the pelvis (Ext) or toward the pelvis (Flex); Ant-Post
pair by its contribution to the acceleration of the foot with respect
to the pelvis in the anterior (Ant) and posterior (Post) directions,
orthogonal to that produced by the Ext-Flex pair; and Plant-Dorsi pair
by its contribution to an acceleration tending to either plantarflex
(Plant) or dorsiflex (Dorsi) the foot.
This theoretical framework of biomechanical functions was used to
analyze kinematic, kinetic, and EMG data observed in forward pedaling
in healthy and neurological impaired individuals. Some muscles in
healthy adult subjects pedaling at different cadences were found to
contribute to one function, such as vastus medialis to Ext,
gastrocnemius to Plant, hamstrings to Post, and tibialis anterior to
Dorsi. Other muscles were found to contribute to two functions, such as
rectus femoris to Ant and Ext and SL to Ext and Plant (Neptune
et al. 1997). Analysis of muscle activity of pedaling
hemiparetic individuals compared with healthy age-matched controls
(elderly adults) showed that impaired ability to produce work and
propel the crank is related to prolonged activity in muscles
contributing to Ext function and to improper phasing in muscles
contributing to Ant and Post functions (Kautz and Brown 1998
).
On the basis of pedaling simulations (Raasch 1996),
phasing of four of the biomechanical functions (Ext, Flex, Dorsi, and Plant) or muscles contributing to the execution of the functions is
proposed to be pedaling-direction invariant with respect to limb
extension and flexion (Fig. 1A). Phasing of the other two functions (Ant and Post) are proposed to reverse in backward pedaling because they are related to anterior or posterior motion of the limb,
which occur at the opposite limb extension/flexion transitions in
backward pedaling. This study was to test whether a simple biomechanics-based control scheme of alternating muscle function pairs
is sufficient to explain EMG phase shifts in backward pedaling. Because
only a phase reversal of Ant and Post functions is theoretically sufficient to satisfy the biomechanical requirements of backward pedaling, only rectus femoris (RF) and HAMS were hypothesized to change phasing (cf. vastus medialis, gastrocnemius, tibialis anterior, and SL).
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METHODS |
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Experimental setup
Sixteen healthy subjects [8 male, 8 female; age = 24 ± 7 (mean ± SD) years; height = 1.74 ± 0.10 m; weight = 70 ± 9 kg] participated in the study. Experienced cyclists who had ridden >50 miles per week were excluded. This study was approved by the Institutional Review Board (Medical Committee for the Protection of Human Subjects in Research) at Stanford University. Each subject signed a consent form before participation.
Subjects pedaled a bicycle ergometer, modified to provide the same
frictional workload (120 J/cycle) in both the forward and backward
directions (Fig. 2A). Subjects
were seated during all trials, with a restraining belt to minimize
pelvic motion. Subjects grasped handlebars that allowed them to sit
upright with a forward lean of about 10° from the vertical,
consistent with trunk angles typically encountered during walking
(Pozzo et al. 1990). Cleated cycling shoes provided a
rigid connection between the feet and the pedals.
|
The force at each pedal spindle was measured with a pedal dynamometer
(Newmiller et al. 1988). Optical encoders measured crank and pedal angles. Surface EMGs were collected bilaterally from vastus
medialis (VM), RF, biceps femoris (BF), semimembranosus (SM), tibialis
anterior (TA), medial gastrocnemius (MG), and SL. All data were sampled
at 1,000 Hz (similar to those of Ting et al. 1998
).
Practice protocol
Subjects were trained so that they could maintain a constant
cadence of 60 rpm without feedback. First, subjects pedaled forward in
two 60-s trials, using a metronome for the first 30 and 20 s,
respectively. Subjects then pedaled backward in five 60-s trials, using
a metronome for the first 40, 30, 20, 10, and 10 s of each trial,
respectively. Subjects were given 1 min rest between each trial.
By the end of the practice session most subjects were able to pedal
smoothly and consistently, maintaining a constant cadence between 55 and 65 rpm. A few subjects did not perform consistently and were given
additional practice time. Smoothness was determined by the absence of
freewheeling, a decoupling of the crank from the flywheel load that
occurs when the crank decelerates relative to the flywheel
(Fregly 1993; Raasch 1996
).
Experimental protocol
Data were collected in four 40-s trials, two forward and two backward pedaling trials, presented in random order. Subjects used a metronome in the first 10 s, and data were collected in the last 15 s of each trial. Subjects were instructed to maintain a constant cadence and to pedal "smoothly and consistently."
Kinematic and kinetic data processing
Pedal force, crank angle, and pedal angle were downsampled to 200 Hz and low-pass filtered (10 Hz, zero-lag Butterworth filter). For each pedal, crank torque, which is the component of the force that accelerates the crank multiplied by crank arm length, was calculated from the pedal force and the pedal and crank angles. Kinematic variables were referenced to crank angle, with a reflected coordinate system for backward pedaling (Fig. 3A). By defining 0° as the position of the crank parallel to the seatpost when the leg is most flexed (pedal closest to the pelvis) and defining positive crank angle in the direction of motion in both forward and backward pedaling, crank angles between 0 and 180° always correspond to limb extension (pedal moving away from the pelvis) and crank angles between 180 and 360° to limb flexion (pedal moving toward the pelvis). Data from each trial were ensemble averaged over 10 complete crank revolutions (~10 s).
|
To compare forward and backward crank torque generation, the amount of work done by each leg was calculated during limb extension and flexion. The work done in any region of the cycle is proportional to the average crank torque during that phase. The work done during extension was found by integrating the crank torque over 0 and 180° and work during limb flexion by integrating over 180 and 360°. Total workload was found by integrating the crank torque from both legs over the entire crank cycle (0-360°). Work values were compared with two-way analysis of variance (ANOVA) with subject and pedaling direction as factors.
EMG data processing
To characterize the EMG profiles of each muscle, integrated EMG (iEMG) was calculated in 16 crank phase intervals of 22.5° over the entire crank cycle (Fig. 3A). Intervals 1-8 correspond to limb extension, and 9-16 to limb flexion. Total iEMG activity was found by summing the iEMG activity over the entire crank cycle (i.e., 16 intervals). Sixteen intervals were found to be adequate to represent changes in EMG yet sparse enough to allow for meaningful comparisons. For each trial, the iEMG profiles were ensemble averaged over 10 crank cycles. For each muscle and subject, an average iEMG profile for each pedaling direction was found by averaging each of the two forward or two backward pedaling trials. Left and right legs were analyzed independently.
To compare the phasing of iEMG profiles in forward and backward
pedaling without regard to iEMG amplitude, each iEMG profile was
normalized by the total iEMG value for that trial. The Pearson product-moment correlation (r) was then calculated at all 16 possible phase shifts between the forward and backward pedaling profile for each muscle and subject
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(1) |
The phase shift, Tmax, corresponding with the maximum correlation coefficient, rmax, identifies the phase relation at which the forward and backward iEMG profiles are most similar. The coefficient of determination, rmax2, represents the percentage of signal energy distribution common to both signals at the phase shift Tmax, i.e., the degree to which the backward pedaling iEMG profile could be explained by the forward iEMG profile shifted by Tmax. The phase shifts found in this manner can be used to determine whether muscle timing in backward and forward pedaling are similar or different. Only shifts of greater than one bin, or 22.5°, are meaningful.
To compare overall iEMG amplitude between forward and backward pedaling, total iEMG was calculated for each muscle (left and right) in each subject. The values were analyzed with an ANOVA with subject and side (left or right, nested within subject) as blocking factors and pedaling direction as a factor.
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RESULTS |
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Subjects successfully pedaled without freewheeling at the same cadence and against the same workload in both forward and backward pedaling. The average cadences for forward and backward pedaling were not significantly different (62 ± 1 rpm, and 61 ± 2 rpm, respectively, P > 0.05). No significant difference in total workload over the cycle was found between forward and backward pedaling (forward: 130 ± 14 J, backward: 124 ± 6 J; P > 0.05).
The shape and magnitude of the crank torque trajectories from one leg
in forward and backward pedaling were also similar, exhibiting a large
peak in crank torque during limb extension, and negative torque
generation during limb flexion (e.g., Fig. 4). Furthermore, no difference in the
amount of work done during backward and forward pedaling was found
during either limb extension (forward: 73 ± 10 J, backward:
71 ± 9 J; P > 0.05) or limb flexion (forward:
8 ± 5 J, backward:
9 ± 9 J; P > 0.05).
|
EMG phase shifts
During both forward and backward pedaling, each muscle exhibited a
major burst of EMG activity once per cycle (e.g., Fig. 2, B
and C). Forward pedaling EMGs were similar to those
previously reported (e.g., Ryan and Gregor 1992).
Backward pedaling EMGs have not been previously reported. In each
muscle, the phasing of the burst of activity was consistent across all
subjects in both directions (Fig. 3B). Of the seven muscles
investigated, four exhibited the same phasing in forward and backward
pedaling (e.g., Fig. 2B). Three exhibited altered phasing
(e.g., Fig. 2C).
Phasing of activity in VM, SL, MG, and TA was the same in forward and backward pedaling, as the mean phase shift Tmax was less than one bin (i.e., <22.5°, Table 1). VM and SL were active only during limb extension (Fig. 3B). TA was active primarily at the flexion-to-extension transition and MG at the opposite transition (Fig. 3B).
|
Phasing of activity in BF, SM, and RF was different in backward and forward pedaling (Table 1). BF activity in backward pedaling was delayed 166 ± 74°. In forward pedaling peak BF activity occurred just before the extension-to-flexion transition and in backward pedaling just before the opposite (flexion-to-extension) transition (Fig. 3B). SM activity in backward pedaling was delayed 107 ± 57°. In 22 of 32 SM EMG comparisons (one EMG comparison/leg in 16 subjects), the average shift was 139 ± 32°, closer to the shift found for BF (cf. SM with BF, Fig. 3B). In the other 10 SM EMG comparisons, peak SM activity occurred at midflexion during both forward and backward pedaling (compared with only 2 records in the BF), resulting in an average shift of just 36 ± 39°. RF was active during the flexion-to-extension transition and into limb extension in forward pedaling, but in backward pedaling the burst, which occurred during limb extension, was shorter (Fig. 3B). In backward pedaling, RF was delayed by 51 ± 38° (Table 1).
EMG correlation coefficients
In each muscle, the EMG signal energy common in forward and
backward pedaling was highly significant (P < 0.01, Table 1). In VM and SL, the correlation coefficient of determination,
rmax2, was very high
(0.90 and 0.85, respectively), indicating that the signal energy
distribution was essentially identical between forward and backward
pedaling. Because the VM and SL have very distinct bursts in forward
pedaling, the same pattern characterizes their activity in backward
pedaling. In the other muscles (TA, MG, BF, SM, and RF), however, the
signal energy distribution common in forward and backward pedaling was
less (0.62 rmax2
0.77). In the worst case, TA had
rmax2 of 0.62, indicating
that 38% of the signal energy distribution was unaccounted for by a
phase shift. The unaccounted signal energy probably results from these
muscles having more than one region of activity in the crank cycle
with, usually, unequal activity in the regions. For example, it can be
seen from the ensemble iEMGs of MG in backward pedaling (Fig.
3B) that, although the primary activity occurs at about the
same crank phase as in forward pedaling, significant signal energy also
exists throughout limb flexion. In RF, the unaccounted signal energy
probably results from the unequal burst durations in the two pedaling
directions.
EMG amplitude
The total iEMG amplitude in BF decreased by 32% during backward pedaling (P < 0.01, Table 1). However, the level of BF activity in backward pedaling compared with forward pedaling varied greatly across subjects. Some had very little BF activity during backward pedaling (8/32 had <50% total energy compared with forward pedaling), whereas a few demonstrated equivalent or higher total iEMG levels in backward pedaling (10/32 had >90% total energy compared with forward pedaling).
The only other muscles to exhibit a change in total iEMG in backward
pedaling were SL (10%, P < 0.05) and MG (
11%,
P < 0.01; Table 1). VM, TA, RF, and SM exhibited no
change in total iEMG.
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DISCUSSION |
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As hypothesized, we found phasing changes in pedaling to occur in
only those muscles (BF, SM, and RF) contributing to the execution of
the Ant and Post biomechanical functions (Neptune et al.
1997; Raasch et al. 1997
). Our contention that
the phasing of only the Ant and Post biomechanical functions are
directionally sensitive is therefore supported. However, these
biarticular muscles did not necessarily contribute to the same
function(s) in forward and backward pedaling. Also, other muscles were
found to contribute somewhat to other functions in backward pedaling,
which were not expressed in forward pedaling. It is suggested that the
ability of a muscle to contribute to more than one function, with the expression of each in the motor output under neural modulation, gives
the biomechanics-based neural control scheme flexibility and thus the
capability to execute a variety of lower limb tasks, including walking.
EMGs compared with predicted muscle excitations based on biomechanical functions
Phasing of some muscles (VM, SL, MG, and TA) were unaffected by
pedaling direction, consistent with their role being to contribute to
the execution of a directionally insensitive biomechanical function
(i.e., VM and SL to Ext; MG to Plant; TA to Dorsi; see Fig.
1A). Data from simulations and other experiments on forward pedaling are consistent with these muscles contributing to these functions (Neptune et al. 1997; Raasch
1996
). However, at higher loads or cadences, at least in
forward pedaling, SL contributes significantly also to Plant function
(Neptune et al. 1997
; Raasch et al. 1997
;
Ryan and Gregor 1992
).
Phasing of the other muscles (BF, SM, and RF) were affected by pedaling
direction, consistent with their role being to contribute to the two
directionally sensitive biomechanical functions (i.e., BF and SM to
Post; RF to Ant). The largest changes in phasing were found in BF and
SM, probably because these muscles contribute mostly to Post, although
a contribution to Flex probably occurs as well (Fig. 3). Indeed, a SM
burst during limb flexion is evident at high cadences (Neptune
et al. 1997). The smaller but still notable change in phasing
in RF is due to its shorter burst in backward pedaling, which may be
due to RF only contributing to Ext rather than to both Ext and Ant
(Fig. 3). Neptune et al. (1997)
also find RF to contribute to both Ext
and Ant in forward pedaling.
Directionally sensitive expression of the biomechanical functions in
the motor output pattern may appear not only in muscles showing large
changes in phasing (e.g., SM and RF) but also in muscles showing
invariance in phasing. For example, TA and MG may also contribute to
another biomechanical function (Flex) in addition to Dorsi and Plant
functions, respectively (Fig. 3B). The expression of Flex,
primarily in the backward direction, is consistent with the EMG signal
energy in backward pedaling being unaccounted for by a phase shift. The
ability of TA to contribute to Flex is consistent with the increase in
crank torque and TA activity seen in one-legged pedaling (Ting
et al. 1998). These task-dependent expressions of biomechanical
functions in the motor output may arise from modulation of the neural
elements responsible for the expression of the functions in the output.
Comparison to walking
Activity of muscles during forward and backward walking can also
be categorized into similar biomechanical functions, with some having
to change in phasing during a reversal in walking direction. Extensor
muscles (e.g., vasti and gluteus maximus) are active in stance in
forward and backward walking to produce, putatively, limb extension
(Ext function). Thus the Ext function does not change phasing in
walking, although burst durations in extensor muscles may be
directionally sensitive (Thorstensson 1986;
Winter et al. 1989
). Iliopsoas and iliacus are active
during swing in forward walking to produce limb flexion (Flex function) and alternate with extensors (Perry 1992
; Rose
and Gamble 1994
). In walking, acceleration of the limb in the
anterior and posterior directions occur at opposite limb
extension/flexion transitions compared with pedaling because of
differences in the biomechanics. For example, in forward walking the
foot is accelerated anteriorly with respect to the pelvis at the
extension-to-flexion transition, which is opposite to forward pedaling.
Thus the Ant and Post functions in walking with respect to limb
extension and flexion are opposite compared with pedaling, although as
in pedaling they reverse with direction. Consistent with RF and HAM
contributing to Ant and Post functions, respectively, they tend to be
active at the appropriate transitions in forward walking (e.g.,
Nilsson et al. 1985
; Perry 1992
;
Rose and Gamble 1994
) and tend to shift phase in
backward walking (Deursen et al. 1998
; Duysens et
al. 1996
; Thorstensson 1986
; Winter et
al. 1989
). During walking, RF typically has another burst
during stance, which corresponds with Ext (Nilsson et al. 1985
; Shiavi 1990
; Thorstensson
1986
; Winter et al. 1989
). Similar to pedaling,
the RF burst during stance (Ext function) is emphasized in backward
walking (Deursen et al. 1998
; Thorstensson
1986
; Winter et al. 1989
), although at higher
forward walking speeds and in forward running, the RF burst during
anterior transitions may increase in prominence (Nilsson et al.
1985
). In addition, reflex modulation in RF and HAMS appears to
reverse in backward walking (Duysens et al. 1996
). In
contrast to pedaling, however, phase shifts are typically seen in ankle
muscles when walking direction is reversed (Deursen et al.
1998
; Thorstensson 1986
; Winter et al.
1989
), which may be consistent with the reversal in ankle power
(Winter et al. 1989
).
Backward walking may, therefore, require a reversal in phasing of two
biomechanical function pairs (Plant/Dorsi as well as Ant/Post) instead
of just one (Ant/Post) as in pedaling, with the phasing of the Ext/Flex
pair immutable to walking direction. A control scheme for walking
composed of two main components (i.e., some biomechanical functions
that change in phasing with walking direction and others that do not)
is compatible with the finding that forward and backward walking can be
characterized by just two features of the motor output (Deursen
et al. 1998). Similarly, in salamanders, one principal feature,
correlated with muscles undergoing a phase shift, can describe the EMG
differences in forward and backward walking (Ashley-Ross and
Lauder 1997
).
Neural strategy for locomotion
The biomechanical function pairs (Ext-Flex, Ant-Post, and
Dorsi-Plant) form a basis for a control strategy of forward and backward pedaling, which may also apply to walking. Reflex modulation in pedaling (e.g., Brown and Kukulka 1993; for review
see Brooke et al. 1997
) is very similar to that in
walking (e.g., Yang and Stein 1990
) and suggests a
common neuronal basis. On the basis of the hindlimb locomotion of
decorticate cats, a similar division of the locomotor cycle into
flexion, extension, and two overlapping transition regions was
proposed, with biarticular and more distal muscles acting primarily
during the transitions (cf. Fig. 1A with Fig. 10 from
Perret and Cabelguen 1980
). The three pairs of
alternating functions are similar in concept to Grillner's (1981)
unit-burst generators or other concepts of mutually inhibitory neuronal
elements (e.g., Stein and Smith 1997
). However, the
elements in our scheme are organized by biomechanical function rather
than by muscle anatomy. Loeb (1984)
also proposed compartmentalization
of neuromuscular control based on function.
The phasing of the biomechanical function pairs could be achieved
through three pairs of mutually inhibitory neuronal elements. However,
the neural circuitry producing the 25% phase shift between either
Ant-Post or Plant-Dorsi and Ext-Flex (Fig. 1A) may be more complex than the mutually inhibitory connections proposed by Grillner (1981) to exist among the unit burst generators (cf. schema for 25%
phase shift in swimmerets) (Skinner et al. 1997
).
Similar to the concepts of Grillner (1981)
, connections between the
biomechanical function pairs must be reconfigured, depending on the
locomotor task and direction. In forward pedaling, Ant and Dorsi are
excited concurrently (and out-of-phase with Post and Plant), suggesting possible mutually excitatory and inhibitory interconnections between these functions. In backward pedaling, these interconnections must be
opposite. The setting of the configuration of the interconnections among the biomechanical function elements is likely under supraspinal control with afferent modulation (e.g., Grillner 1981
;
Grillner and Dubuc 1988
; Rossignol et al.
1988
).
The scheme proposed, although largely maintaining opposition of
traditional antagonistic elements, allows for the flexibility in muscle
excitation often observed. Task-dependent modulation of the expression
of a function in the motor output provides a muscle with the capability
to participate in one function at times and another function at other
times. In contrast, the strict extensor-flexor groupings proposed by
Grillner (1981) cannot account for the sometimes "paradoxical"
activity of biarticular muscles classified as either extensor or flexor
according to anatomy (e.g., HAMS in pedaling) (Gregor et al.
1985
). Specifically, both biarticular muscles, e.g., RF in
human walking (Nilsson et al. 1985
), ST in cat walking (Loeb 1984
), and RF in rat locomotion (Leon et
al. 1994
), and monoarticular muscles, e.g., SL in pedaling
(Neptune et al. 1997
) and VL in rat locomotion
(Leon et al. 1994
), may have multiple bursts. In our
scheme, multiple bursts (or bursts of differing durations) are to be
expected as both biarticular and uniarticular muscles can contribute to
the execution of multiple functions. Others proposed that biarticular
muscle activity is highly mutable (Smith 1987
) and may
receive inputs from both flexor and extensor half-centers
(Perret and Cabelguen 1980
), compatible in concept with
our scheme of muscles being able to contribute to multiple functions.
Because multiarticular muscles develop torques at more than one joint,
they will tend to have multiple functions, although loading conditions
(e.g., interactions with the environment) can affect the functions of
both mono- and biarticular muscles (e.g., Zajac and Gordon
1989
). Modulation of the neural elements controlling the
expression of the functions in the motor output provides the control
scheme with the ability to execute a variety of tasks.
Conclusion
A locomotor strategy based on control of biomechanical functions derived from computer simulations of pedaling was found to be compatible with forward and backward pedaling. Each of the six functions is proposed to alternate with only one other function to form three biomechanical function pairs. This strategy predicts well the phasing of muscles during these tasks. In pedaling, a reversal in phasing of one biomechanical function pair is suggested. Because some muscles can participate in the execution of more than one biomechanical function, complex changes in the phasing of a muscle can and do occur with a change in pedaling direction. Similarities between pedaling and walking suggest that a similar strategy may be operational in both tasks.
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ACKNOWLEDGMENTS |
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We thank Dr. Christine Raasch and C. Dairaghi for help collecting and processing data.
This work was supported by National Institute of Neurological Disorders and Stroke Grant NS-17662, and the Rehabilitation R&D Service of the Department of Veterans Affairs.
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FOOTNOTES |
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Address for reprint requests: F. E. Zajac, Rehabilitation R&D Center (153), VA Palo Alto Health Care System, 3801 Miranda Ave., Palo Alto, CA 94304.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 1 May 1998; accepted in final form 22 October 1998.
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REFERENCES |
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