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Human Performance Laboratory, Faculty of Kinesiology, University of Calgary, Calgary, Alberta, Canada T2N 1N4
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ABSTRACT |
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During walking and running, the human body reacts to its external environment. One such response is to the impact forces that occur at heel strike. This study tested previous speculation that the levels of muscle activity in the lower extremities are adjusted in response to the loading rate of the impact forces. A pendulum apparatus was used to deliver repetitive impacts to the heels of 20 subjects. Impact forces were of similar magnitude to those experienced during running, but the loading rate was varied by 13% using different materials in the subjects' shoes. Myoelectric patterns were measured in the tibialis anterior, medial gastrocnemius, vastus medialis, and biceps femoris muscles. Wavelet analysis was used to resolve intensity of the myoelectric patterns into time and frequency space. Substantial and significant differences in the myoelectric activity occurred between the impact conditions for the 50 ms before and the 50 ms after impact, reaching 3 ms in timing, 16% in wavelet number, and 154% in the intensity of the muscle activity.
electromyogram; wavelet; impact force; time-frequency analysis
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INTRODUCTION |
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DURING WALKING AND RUNNING, the human body reacts to input from its external environment. One such input is the ground reaction force, which occurs during the ground contact phase of each stride. One possible reaction is the modification of the muscle activity patterns in response to that force. The lower extremity muscles are used for many different tasks during each stride, including the control of skeletal position, joint stiffness, vibrations of the soft tissue packages, stability during ground contact, and propulsion for the movement task. It has been speculated that there is a requirement for the muscles to control and, thus, minimize soft tissue vibrations during locomotion (25) and, thus, that there will be a change in muscle activity patterns in response to different vibration loadings on the lower extremity.
Impact forces in heel-toe walking and running are forces resulting from the collision of the heel with the ground, reaching their maximum (the impact peak) earlier than 50 ms after first contact (25). The rate at which the impact peak is reached is termed the loading rate and is a correlate of the major frequency of the impact peak. Impact forces have frequency contents in the range 10-20 Hz and should be expected to produce vibrations of the soft tissues of the body. However, observations suggest that impact-related vibrations are minimal in the muscular soft tissues of the lower extremities during walking and running. One possible mechanism to reduce soft tissue vibrations is to ensure that the resonant frequencies of the soft tissues are distinct from the frequency of the impact force and that vibrations within the soft tissues are strongly damped. The frequency and damping coefficients of vibrations in the soft tissues of the lower extremities are increased by increases in muscle force production and muscle shortening velocity (34). The natural vibration frequencies of the triceps surae, quadriceps, and tibialis anterior tissues are in the range 10-50 Hz, depending on the levels of muscle activity (34). Therefore, it should be expected that if the frequency of the impact force is close to the natural frequency of the soft tissues, then additional muscle activity will be used to minimize possible vibrations. Muscle activity has been shown to respond to frequencies of applied continuous vibrations in the medial head of the triceps brachii in the arm during isometric tests (7). However, changes in the myoelectric patterns of the lower extremities that may occur in response to the different impact conditions experienced during walking and running have not yet been demonstrated.
To test whether the body reacts to the loading rate of the impact force by modifying muscle activity, an experiment must be performed that can alter the loading rates of the impact force. The magnitude of the impact force typically increases with the running velocity (8, 12, 26); however, the magnitude of the impact force remains relatively insensitive to changes in cushioning from the shoe or ground. However, the shoe cushioning does change the loading rate (a correlate of frequency) of the impact force (8, 16, 17, 19, 26). Thus, changing the material properties of the shoe provides a tool by which the loading rate of the impact force can be experimentally manipulated.
To isolate the changes in muscle activity due to the ground impact from the muscle activity that is required for joint movement, an experimental procedure must be used that can minimize the myoelectric activity required for joint movement. One such approach is to use a human pendulum apparatus (17, 18). Use of this apparatus involves the subject lying supine on a bed with the leg supported by a harness. The pendulum motion causes the heel to impact with a wall, and thus impacts are generated without requiring the joints to move. The cyclical swinging of the subject on the pendulum results in a series of impact forces that mimic those found during running.
In this study, we use such a pendulum technique to investigate the response of muscle activity in the leg to different impact forces. To vary the loading rate of the impact forces experienced by each subject, the viscoelastic properties of their shoe midsoles were experimentally manipulated. This study tested the hypothesis that muscle activity patterns in the lower extremities change in response to the different impact loading rates that occur at ground impact.
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METHODS |
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Approach to the problem. A pendulum apparatus was used to apply repeatable impacts to the heel. Subjects lay supine on a bed, which was cyclically swung so that the right heel impacted a wall-mounted force plate. The amplitude of each swing was set so that the impact forces were similar to those experienced during walking and running. A harness supported the leg so that muscle activity was not required for joint movement of the lower extremity. The frequency component of the impact force was modified by changing the midsole properties of the subjects' shoes, with a soft shoe giving a lower-frequency component than a hard shoe. Muscle activity patterns in the lower extremities were measured by electromyography (EMG) from the tibialis anterior, medial gastrocnemius, vastus medialis, and biceps femoris muscles. The myoelectric signals were resolved into components in intensity, time, and frequency to determine which features of the signals changed between the shoe interventions. The data were used to test the hypothesis that the muscle activity required to stiffen the leg for impact differs between the two impact conditions produced by the shoes.
Subjects. Twenty men (76.4 ± 1.7 kg body mass, 33.3 ± 2.6 yr old) who regularly ran or exercised participated in the study. They gave their informed consent in accordance with the University of Calgary Medical Bioethics policy on research using human subjects.
Pendulum apparatus.
A human pendulum apparatus was constructed (Fig.
1), adapted from that described by
Lafortune and Lake (18). The pendulum was made from a
canvas bed strapped around a polyvinyl chloride frame, and it was able
to swing freely via polyvinyl chloride rods attached to the corners.
The subject lay supine on the bed, with leg suspension straps around
the ankle and knee maintaining the right knee at a flexion angle of
20°. In this manner, the lower leg was held parallel to the ground,
and the hip flexion angle was 20°.
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Wavelet analysis of EMG. Wavelet analysis (33) was used to resolve simultaneously the intensities of the EMG signals in time and frequency space. The analysis yields an intensity that closely approximates the power of the EMG signal. The procedure to obtain the intensity from the measured EMG signal consisted of the following three steps: 1) compute the wavelet-transformed EMG signal using a filter bank of wavelets that include intensity and damping factors, 2) compute the intensity of the wavelet-transformed signal by adding its square and the square of its time derivative divided by the center frequency, and 3) apply a Gauss filter to the wavelet-transformed signal.
In step 1, a filter bank of eight wavelets was used. Each wavelet was well defined in time and frequency space, and its integral over time was 0. The set of wavelets was nearly biorthogonal and was produced by nonlinear scaling. The scaling was adjusted to obtain a physiologically acceptable time resolution at all frequencies considering the uncertainty principle. Center frequency, bandwidth, and the time resolution are indicated in Table 1.
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Definitions.
A wavelet domain was defined as the time series of intensity resolved
for one wavelet only. The frequency bands for each wavelet domain are
shown in Table 1. Intensities at frequencies <10 Hz typically contain
movement artifacts, and so data from wavelet domain 0 were
ignored. An intensity ij,k was calculated for
each sample point j and wavelet domain k. Time
tj is the time of sample j, and
wavelet wk is the wavelet number for wavelet
domain k. The global intensity (Ij)
gives the power in the myoelectric signal at each sampling point and
was defined as the sum of the intensities over wavelet domains
1-7 for each tj
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50
tj < 0 ms) and postimpact (0
tj < 50 ms) windows, respectively. For each
shoe condition and for each subject, the means of
Mi, Mt, and
Mw for the 30 impacts are
i,
t, and
w,
respectively. The intensity values for
i
were normalized so that the maximum of
i,imp for the elastic shoe
condition had a value of 1.
Statistics. The significance of the muscle responses was tested with analyses of variance (ANOVAs). Separate balanced-design ANOVAs were used for each muscle and each time window (Minitab). The dependent variables used for these tests were Mt, Mw, and Mi. Subject number, shoe condition, and a "subject × shoe condition" interaction term were used as factors in the ANOVA. Each ANOVA contained data from both shoe conditions, all 20 subjects, and all 30 trials.
Differences in
i,
t, and
w were
calculated between the elastic and viscous shoe conditions for each subject. The ranges of these differences are represented by their RMS value.
Muscle fatigue during the experiment can result in a reduction in the
frequency content of the EMG (5). If the frequency content
of the EMG was systematically changed with the fatigue state, then the
order in which the interventions were presented would be related to
w. The effect of muscle fatigue and the order in
which the interventions were presented were tested in the following
way. The differences in
w,pre and
w,imp between the shoe conditions were scored as +1
or
1 if the elastic condition was higher or lower than the viscous
condition, respectively. These scored values were then ranked by
whether the subject was presented with the elastic or the viscous shoe
condition first. If fatigue had a significant effect on the results,
then it would be expected that the subjects who tested the elastic shoe
condition first would have a score of 1, and if they tested the viscous shoe first, then the score would be
1. The distribution of these ordered scores was tested with a nonparametric runs test (Minitab) to
determine whether there was a significant effect of muscle fatigue on
the myoelectric response.
Values are means ± SE. The range of differences in values was
indicated by their RMS value. Significance was tested at a confidence level of
= 0.05. Power analyses (29) showed that
in all cases the power of the ANOVA tests was >99%.
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RESULTS |
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Typical force and EMG for the vastus medialis muscle that resulted
from one heel strike are shown in Fig. 2,
A and B. The square of the EMG and the global EMG
intensity are shown in Fig. 2C. The intensity became visible
75 ms before impact. In the 50-ms preactivation phase, the EMG
intensity was contained almost exclusively in the summed intensity from
wavelet domains 3 and 4 (Fig. 2E). During the 50-ms postimpact period, additional activity could be
observed in wavelet domains 1 and 2 (Fig.
2D).
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Individual EMG responses.
The EMG intensities for the vastus medialis muscle for one subject are
shown in Fig. 3. In wavelet domains
1-4 the EMG intensity had increased beyond the background
levels by 50 ms before heel strike. In this example, the intensity was
generally the same between the two shoe conditions for the
preactivation and postimpact periods for all wavelets. The main
exception was at wavelet 2 for the 50-ms preactivation
period. Here the total intensity was 243% greater for the viscous than
for the elastic shoe condition, a difference that was significant.
There were 160 different combinations of 20 subjects, 4 muscles, and 2 shoe conditions. The ratio of the SE to the mean intensity was
calculated for the maximum intensity in the postimpact period for each
of these combinations. These ratios had a range of 19%, as shown by
their RMS value.
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i,pre and
i,imp is shown on a
subject-by-subject basis for both shoe conditions in Fig.
5. These data showed differences in
intensity between the shoe conditions. The ratios of the mean preactivation intensities to the postimpact intensities across all
subjects were 96, 48, 44, and 73% for the tibialis anterior, medial
gastrocnemius, vastus medialis, and biceps femoris muscles, respectively. There was a decrease from
w,pre to
w,imp, as shown for the biceps femoris muscle in
Fig. 6. This decrease was calculated for
139 of the 160 subject-muscle-shoe combinations tested, and
2 analysis showed this decrease to be significantly
different from random.
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Range of individual EMG responses.
Mean values of
t,
i, and
w differed
between the elastic and viscous shoe conditions for the preactivation and postimpact periods (Fig. 9). The
direction of the response varied for all measures of EMG activity
examined, with some subjects showing greater values for the elastic
shoe condition and others showing greater values for the viscous shoe
condition. The smallest RMS range for the differences in response
occurred in the preactivation phase for the tibialis anterior muscle,
with RMS values of 5% of
w,pre for the shift in
wavelet number, 26% of
i,pre for the shift in intensity, and 1.4 ms for
t,pre (Fig. 9). The largest
RMS ranges for the difference in response occurred in the postimpact
phase for the medial gastrocnemius muscle, with RMS values of 16% of
w,imp for the shift in wavelet number and 154% of
i,imp for the shift in
intensity. The largest RMS range for a change in timing between the
responses was 3.0 ms for
t,imp for the biceps femoris
muscle (Fig. 9).
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Significance of EMG responses.
The significance of the differences between Mi,
Mw, and Mt between subjects, shoes,
and subject × shoe condition was analyzed using ANOVA,
and the results are shown in Table 2. Significant differences occurred between the subjects for
Mt, Mw, and
Mi of the EMG response, and these differences were ubiquitous for all four muscles tested. The shoe condition produced significant differences in the EMG response in half of the
tests (Table 2), and these differences occurred during the preactivation and postimpact phases of the EMG signal for
Mt, Mw, and
Mi. The magnitude of the changes in
response is shown in Table 3. Significant
effects of the subject × shoe condition interaction term were
observed for Mw for all 8 tests, and significant
differences were observed for 12 of the 16 tests of this interaction
for Mt and Mi of the EMG response. The results from this interaction term show significant differences in the way in which the subjects reacted to the two shoe
conditions for Mt, Mw, and
Mi.
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Ground reaction forces.
There were significant differences in the maximum impact force
(Fmax), the time to reach this maximum (
t),
and the mean rate of force increase (Fmax/
t)
to this maximum between the two shoe conditions (ANOVA for 1,200 subject-muscle-shoe trial combinations). Changing from the elastic to
the viscous shoe condition resulted in a 4.1% decrease in
Fmax, a 10% increase in
t, and a 12.6% decrease in Fmax/
t (Table
4).
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DISCUSSION |
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An earlier experiment using a pendulum device delivered impacts to a subject with a fully extended leg, and the impact forces were shown to have magnitudes and loading rates that matched those reported for running (18). In this study, the knee was held at a flexion angle of 20° to more closely resemble the leg posture at heel strike during walking and running. A 20° knee flexion results in a reduction in the magnitude of the impact force. The magnitude and loading rate of the impact force have been measured for running speeds between 3 and 5 m/s (23), and extrapolation of these data shows that the impact forces experienced during this present pendulum study (Table 4) had magnitudes corresponding to a 2.5 m/s run and loading rates corresponding to a 1.1 m/s walk. This experiment therefore demonstrated that muscle activity patterns were different when the loading rate of the impact force was varied and when those impact forces were within the physiological range experienced during walking and running. To isolate the muscle activity patterns that occurred in response to the impact force from those required for a complete walking or running motion, the experiments were conducted on a pendulum with the lower extremity positions constrained. The supine position of the subjects could affect perceptual and proprioceptive processes that occur during impact, and this is the trade-off that must be made to obtain the pendulum-generated impact results. The impact forces with the elastic shoe had substantially higher loading rates than those with the viscous shoe. The different impact forces experienced with the two shoe conditions resulted in clear differences in the intensity patterns resolved by this functional EMG analysis.
When a muscle is activated, it takes time before the muscle force is fully developed. The time taken to reach maximum force depends on factors such as the muscle fiber type, the activation level, and the contraction dynamics but, for isometric twitches in mammalian muscle, is in the range 23-73 ms (3, 4, 10). The intensity of the myoelectric signal indicates the activation level within the muscle. The force achieved by the muscle depends on the activation level, the number and fiber type of the muscle fibers activated, the contraction dynamics, and the history of previous contractions (31). Fast- and slow-twitch muscle fibers have different intrinsic contraction properties (1), and it is typically thought that slow-twitch fibers are recruited for low-intensity activities, with a greater proportion of fast-twitch fibers being recruited as increasing force is required (6, 13). The frequency components of the myoelectric signal can indicate the muscle fiber type recruitment for any given activity, and a coefficient of frequency is given by Mw in this study. The frequency increases with the conduction velocity of the muscle fiber action potentials (20), and action potentials travel faster along larger-diameter cells (14). Fast-twitch fibers have diameters 1.2 times those of slow-twitch fibers in the vastus lateralis (9), suggesting that they should have higher-frequency components. In addition, fast-twitch muscle fibers can have faster (1.5 times) conduction velocities than slow-twitch fibers, even when they have similar diameters (27). Muscle fiber recruitment strategies can thus be determined from the EMG frequency spectra, and this has previously been demonstrated for graded muscle contractions in the cat gastrocnemius (30). The timing, activation level, and motor unit recruitment patterns leave characteristic features within the myoelectric signal. The ability to resolve time, intensity, and frequency simultaneously gives insight into how the muscles are used to accomplish a given task. Differences in the timing of activation can be seen in Figs. 4, 7, and 8; differences in the intensity of activation can be seen in Figs. 4, 5, 7, and 8; differences in the frequency of the myoelectric signal being confined to distinct wavelet domains can be seen in Figs. 2 and 3.
In this study, the myoelectric signals were resolved by wavelet analysis into their intensities in time and frequency space. The intensity represents the power within the EMG for any given time and frequency band. EMG power spectra, which are traditionally used to assess EMG frequency content, are calculated from the square of the Fourier-transformed EMG signal (21) and are thus also a measure of the power within the signal. Mw used in this study is comparable to the mean power frequency used to measure EMG contractions (32). By contrast, RMS analysis computes the amplitude, and not a power, of the signal as a function of time. The square of the RMS value is comparable to half the intensity from this wavelet analysis.
The wavelet analysis of EMG signals resulted in a variety of intensity peaks and leads to the concept of events in muscle activation. Events can be resolved over a set of wavelets and thus have their own wavelet spectrum. Events, which are separated by more than the time resolution of the wavelet, represent distinct events within the muscle activation. The example in Fig. 2, D and E, shows a muscle activation event that was localized to wavelet domains 3 and 4 and to the preactivation period. Differences in the EMG signal were thus characterized by the specific frequency band and the specific time at which they occurred. Differences that occurred in the time and the frequency content of the myoelectric signals were statistically significant (Table 2), thus justifying the use of the wavelet techniques to decompose the EMG into its components in time and frequency space. Such separation of the myoelectric signal into time and frequency components would not be possible using traditional analysis techniques such as RMS or Fourier transforms. Time-frequency decomposition is possible using windowed Fourier techniques; however, this approach is not without its difficulties (15). The time resolutions for each wavelet were chosen so that they covered physiologically relevant durations on the order of 20-40 ms. The higher-frequency wavelets progressively resolved shorter times (Table 1); however, this resulted in broader frequency bands for these wavelets because of the uncertainty principle governing signal processing (15).
Differences in the intensity patterns that resulted from the different loading rates were limited to a narrow range of wavelet domains (Figs. 2 and 3). The differences thus occurred at specific frequency bands. A net decrease in the frequency content of the EMG may occur because of recruitment of a greater proportion of slow- than fast-twitch fibers. However, a decrease in the frequency content may also be caused by the decrease in action potential conduction velocity that occurs during fatigue because of a lowering of the interstitial pH (2) and is probably due to an accumulation of metabolic by-products such as lactate within the muscle (22). Thus muscle fatigue may also appear as a shift in the EMG frequency spectrum (11). However, we have shown that fatigue was not a significant factor in these results. Therefore, it can be speculated that the change in myoelectric frequency patterns that occurs with different loading rates of the impact force is due to different patterns of muscle fiber type recruitment.
The preactivation period occurred before heel strike, and muscle activity within this period was the result of feedforward control mechanisms. Thus the different muscle preactivation states that occurred between the impact conditions (Table 2) must have been the consequence of the different muscle tuning requirements that were anticipated for each heel strike. The postimpact period began at heel strike and would initially be the result of feedforward mechanisms. However, toward the end of the 50-ms postimpact period, there may additionally have been some stretch reflex responses. Short-latency reflex responses have been shown to occur 41 ms after stretch in the triceps surae muscles (24) and may occur with even shorter latencies as low as 34 and 39 ms in the biceps femoris and rectus femoris, respectively (28). The majority of the postimpact period occurred before the muscle activity could have been influenced by stretch reflexes. Indeed, differences in postimpact muscle activity before the influence of stretch reflexes can be clearly seen in Figs. 2-4. Toward the end of the postimpact period, however, differences in short-latency monosynaptic reflexes may have additionally contributed to the different muscle activity patterns.
The intensity patterns were complex in time and wavelet space. The
results could be more easily submitted to statistical analysis by
reducing the intensity patterns to coefficients describing the mean
time, wavelet number, and intensity for the 50-ms time windows before
and after impact. Such mean coefficients have smaller magnitudes than
the peak values in the intensity patterns. Nonetheless, the RMS values
for the differences of the mean responses for all the subjects show
that the response of the body to the different shoe conditions can be
of substantial magnitude. A range of responses occurred across the
individuals tested, with some subjects showing an increase in
t,
w, or
i between the impact conditions, whereas
other subjects showed decreases in these parameters (Figs. 5 and 9).
Furthermore, testing between elastic and viscous midsole conditions
resulted in large differences in
t,
w, or
i for some
subjects, whereas little change was observed in others. The way in
which the muscle activation patterns respond to different loading rates
of the impact force is thus subject specific. Patterns of
i can be seen in Fig. 5; for instance,
subjects 3 and 20 showed a negligible intensity
during the preactivation period for the medial gastrocnemius, vastus
medialis, and rectus femoris muscles, while subjects 1, 8, 9, 13, 16, 18, and 19 showed some periods of preactivation
that had substantially greater intensity than the following postimpact
period. It would seem as if the individual responses to these impacts
can be grouped into distinct strategies, although the functional
significance of the strategies is not yet understood.
Some locomotor studies are challenged by the fact that muscles are used to move the limbs (to change the joint angles) and, additionally, to provide the joint stiffness required for the locomotor task. In such cases, it can be difficult to segregate these two tasks from the EMG signals. In this study, the leg motion was minimized, with the lower leg being supported in a harness. By eliminating the muscle action required to move the legs, the EMG activity recorded was mainly that necessary for minimizing soft tissue vibrations and for generating the joint stiffness required to withstand the "ground" impact. Significantly different myoelectric patterns were seen in response to the different shoe midsole conditions and, thus, the loading rate of the impact force. These changes were present in the timing, intensity, and frequency content of the EMG and occurred in the period 50 ms before impact and the period 50 ms after heel strike. If "tuning" is considered to be the alteration of the mechanical properties of the leg due to changes in muscle activity, irrespective of any motion that occurs in the joints, then the results from this study have shown that the leg is tuned differently in response to the changes in the loading rate of the impact force.
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ACKNOWLEDGEMENTS |
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We thank Darren Stefanyshyn for help during the study.
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FOOTNOTES |
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Financial support was provided by Adidas International, the Alberta Heritage Foundation for Medical Research, and the Swiss National Foundation.
Address for reprint requests and other correspondence: J. M. Wakeling, Human Performance Laboratory, Faculty of Kinesiology, University of Calgary, Calgary, AB, Canada T2N 1N4 (E-mail: wakeling{at}kin.ucalgary.ca).
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 31 December 2000; accepted in final form 10 May 2001.
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