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Laboratory of Sports Sciences, Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo 153-8902, Japan
Submitted 23 July 2002 ; accepted in final form 23 February 2003
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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near-infrared spectroscopy; electromyogram; synergistic muscles
It has been reported that intramuscular pressure is linearly related to contraction intensity during knee extension (25, 32, 37, 38), elbow flexion (25), and plantar flexion (3, 25). Intramuscular pressure has mostly been compared with the total force of synergistic muscles when muscle activation is assumed to be relatively constant. Through the observation of electromyogram (EMG), however, an unusual pattern of muscle activation has often been demonstrated when sustained contraction at low-level intensity is prolonged for >30 min; the individual synergistic muscles are not continuously activated, but rather they alternate between periods of activity and silence (19, 29, 30, 37, 40). This unique pattern of muscle activation has been called "alternate muscle activity of synergistic muscles" (19, 40). Enoka and Stuart (12) suggested that alternate muscle activity would be effective for minimizing muscle fatigue. This has been reported in a variety of muscle groups, including knee extensors (19, 37), plantar flexors (35, 40), and elbow flexors (29, 30). Recently, we examined the changes in EMG activity of the quadriceps muscle during low-level sustained contractions (2.5–10% of MVC) (19). During the sustained force matching task at 2.5 or 5% of MVC in total knee extension force, alternating muscle activity of knee extensors increased the amplitude of EMG in the rectus femoris muscle, which reached 15–20% of that seen during MVC. Based on a previous study that found an impedance of blood supply to the knee extensors during contraction at 15% of MVC (38), it is possible therefore that intramuscular pressure of the individual muscles of the synergists fluctuates because of the effects of the alternate muscle activity and that the fluctuations in intramuscular pressure affect the local circulation. Indeed, one study (37) has demonstrated fluctuations in the intramuscular pressure of rectus femoris and vastus lateralis muscle during sustained contractions at 5% of MVC. However, in their study, Sjøgaard et al. reported constant blood flow to the femoral vein, and local blood circulation in the individual heads of knee extensors was not examined. Hence, the effects of alternate muscle activity on the local circulation in the individual muscles remain as yet unknown. We hypothesized that, even during low-level contraction below 10% of MVC, blood circulation is locally altered because of the effects of alternate muscle activity.
Invasive measurement of blood flow in the femoral vein has been commonly employed to examine the blood circulation during knee extension (13, 37, 38). The blood flow so measured cannot distinguish the local circulation among individual muscles, but it indicates the average value for several muscles. With near-infrared spectroscopy (NIRS), however, one can measure total Hb content in the capillary bed of individual muscles (7, 21), including the knee extensor muscles (4, 15, 24, 34). Thus the local circulation in the individual knee extensor synergists can be examined by using NIRS.
To test the above-mentioned hypothesis, local circulation in individual muscles was examined by NIRS during alternate muscle activity of knee extensor synergists. We predicted that fluctuations in the blood circulation of individual muscles are correlated with alternate muscle activity.
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METHODS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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Recording techniques. The basic setup for the knee extension procedure was the same as that described elsewhere (18, 19). Each subject was required to perform a static unilateral knee extension exercise in a seated position with the hip and knee joint angles of 100 and 90° flexed (full extension = 0 deg), respectively. The subject's upper body was firmly fixed on a chair by a seat belt. The force of isometric contraction of the knee extensors was measured by a strain-gauge force transducer that was coupled with a strain amplifier and attached by a strap to the subject's ankle. The force was displayed on a storage oscilloscope in front of the subject to provide visual feedback regarding the produced force and target. Surface EMG from skin surface over the rectus femoris (RF), vastus lateralis (VL), and vastus medialis (VM) muscles was recorded by using Ag-AgCl electrodes with a diameter of 5 mm and an interelectrode distance of 20 mm. After careful abrasion of the skin, the electrodes were placed over the muscle belly of the respective muscles. The reference electrode for the EMG was placed on the iliac crest. The electrodes were connected to a preamplifier and a differential amplifier having a bandwidth of 5 Hz to 1 kHz (model 1253A, NEC Medical Systems, Tokyo, Japan). All electric signals were stored with a sampling frequency of 1 kHz on the hard disk of a personal computer using a 12-bit analog-to-digital converter (Lab-PC+, National Instruments, Austin, TX).
To estimate the local circulation of individual synergists, the present study utilized NIRS (NIRO-300, Hamamatsu Photonics, Hamamatsu, Japan) equipped with dual-channel near-infrared laser diodes. The NIRS probes were firmly placed on each muscle belly of the RF and VL near the EMG electrodes. We focused on the RF and VL muscles, because we have already found that alternate muscle activity emerges between RF and either VL or VM but not between VL and VM (19). The light was generated by four laser diodes operating at 775, 810, 850, and 905 nm. The detector in the NIRS probe was separated from the light source by 40 mm. The penetration depth of NIRS corresponds to 
20 mm because penetration depth has been reported to equal to half the distance between the light source and the detector (9, 16). The absorption of light at the different wavelengths was analyzed according to the modified Beer's law, and the changes in oxygenated Hb and Hb were quantified. The sum of known wavelengths is susceptible to the changes in the total Hb (change in oxygenated Hb + change in deoxygenated Hb), which reflects the changes in blood volume under the NIRS probe (6). The algorithm requires the actual pathlength of the light between the light source and detector, but because of the technical inability to measure the pathlength in human muscles, blood volume is expressed in units that involve the pathlength factor. The blood volume assessed by the NIRS is different from the blood flow, but it can be used as an index of the local blood circulation because a good correlation has been reported between the data measured by NIRS and blood flow measured by plethysmography (10, 11). The details of this technique and principle of this instrument have been described elsewhere (39). NIRS signals were continuously stored on a personal computer connected via a RS-232C cable with a sampling frequency of 1 Hz.
Experimental protocol. The MVC for knee extension was the largest force of three trials that could be sustained for at least 2 s. After a sufficient rest period, at least for 10 min after completion of the MVC measurement, the subject performed a sustained knee extension for 60 min at a level corresponding to 2.5% of MVC. Immediately after sustained contraction, the MVC measurement was performed. The target force production in the present study was lower than that employed in the previous study (37) because the alternate muscle activity clearly emerged when the force level decreased from 5.0 to 2.5% of MVC (19).
Data analysis. The EMG signals were full-wave rectified and integrated over 1 s to yield integrated EMG (iEMG). The torque at the knee joint was calculated on the basis of the measured force multiplied by the length of the leg. The iEMG was expressed relatively as a percentage of the corresponding value during MVC [%iEMGmax].
Maximal value, mean value, SD, and coefficient of variation of iEMG sequences in the individual muscle heads were calculated for 60 min of sustained contraction (3,600 sample points). iEMG immediately after the onset of sustained contraction was also calculated over 10 s as an unfatigued value. For the blood volume fluctuation, the range and SD of sequences were calculated.
To evaluate the extent of correlation and the time relation between the iEMG and blood volume sequences of each muscle, we calculated the normalized cross-correlation function (CCF) between the two time series. Before this calculation, the two time series were low-pass filtered (cutoff frequency = 0.01 Hz) by using a fourth-order Butterworth filter employing a zero phase lag (45) to eliminate the high-frequency component. Data for a 20-min period in the early (between the 10th and the 30th min) and later stage (between the 40th and the 60th min) of the sustained contraction were selected for analysis. When the iEMG and blood volume series are written as x(t) and y(t) (t = time), respectively, the normalized CCF [Rxy(
)] was calculated as
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is time lag. The actual calculation was performed in discrete form using a 1,024 points fast Fourier transform calculation. Thus it should be noted that the CCF was for a time window of 1,024 s and that the time resolution of CCF was determined as 2 s. The peak value was used to evaluate the similarity of the two time series, and the time lag was used to evaluate the temporal relation between them.
Furthermore, we paid special attention to the responses of the blood volume around the two epochs at which alternate muscle activity emerged (Fig. 1); the epoch at which the iEMG of RF abruptly increased with the decrease in the iEMG of VL and VM (case I in Fig. 1), and the epoch at which the iEMG of RF dramatically decreased with an increase in the iEMG of VL and VM (case II in Fig. 1). The alternate muscle activities that involved case I and case II were extracted in the following way. For each case, a data set for the 240-s period that included the most abrupt change of RF in the center was selected by visual inspection (Fig. 1). We used the abrupt change in RF as a reference because the changes in the iEMG of RF are more distinct than those of VL or VM. iEMGdiff/dt was then given as a result of the time derivative of the low-pass filtered iEMG of RF (Fig. 1, bottom). The extracted data were aligned to the positive and negative peaks of the iEMGdiff/dt of RF for case I and case II, respectively. Blood volume at each epoch was expressed as the differences from the reference value (change in blood volume) in which the iEMG of the RF abruptly changed (Fig. 1, dashed lines). Thereafter, iEMG and blood volume were averaged for every 5-s period. All the data are presented as means ± SE.
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Statistical significance in the measurement of iEMG (%iEMGmax) and blood volume (µM · cm) sequences among synergistic muscles was tested by using a one-way ANOVA with repeated measures followed by a Tukey's post hoc test. To find significant differences in blood volume from the time at which iEMG of RF abruptly changed, blood volume data were also statistically using a repeated measurement one-way ANOVA with a Tukey's post hoc test. A paired Student's t-test was used to compare peak value of the normalized CCF in the early and the later stages. The significance level for all comparisons was set at P < 0.05.
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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A typical example of the changes in the iEMG and blood volume in the individual heads of knee extensor muscles is shown in Fig. 2. Alternate muscle activity emerged between RF and both VL and VM in all subjects. The total number of alternate muscle activities for 60 min (RF-VL: 8.5 ± 1.6, RF-VM: 8.0 ± 1.9, VL-VM: 1.0 ± 0.4) was consistent with the finding in our previous study (19). Fluctuations in iEMG and blood volume appeared to be larger in RF than in other synergists.
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Table 1 summarizes basic statistics of the iEMG and blood volume sequences in each muscle head of the knee extensors. The iEMG of each head is expressed in relative values normalized to the MVC values of each head except for coefficient of variation. This measurement revealed more pronounced changes for iEMG and blood volume in RF compared with VL or VM. The iEMG at the onset of sustained contraction is significantly higher in VL than that in the RF and the VM (P < 0.05). It is noteworthy that the iEMG in the RF is much lower than the value of 2.5% (percentage of total knee extension force relative to MVC). The average iEMG value across the three muscle heads is approximately equivalent to the contraction intensity (2.6 ± 0.1%iEMGmax). The maximal iEMG in the RF amounted to 27.6 ± 4.4%iEMGmax. This is considerably high compared with the employed contraction intensity for knee extension force (2.5% of MVC). The increase is 25 times of the iEMG in the RF at the onset of the task. On the other hand, the maximal iEMG in VL and VM was only one-half the value of RF. SD of iEMG in RF is more than twice as large as that in VL and VM (P < 0.05). Similar differences among the heads are found in coefficient of variation of iEMG, an index for fluctuations of muscle activity. The similar tendency in differences between SD and coefficient of variation of iEMG reflects no difference in the mean iEMG among the individual heads of the knee extensors. Blood volume was measured in RF and VL. Similar to the results in iEMG, the range and SD of blood volume sequence were significantly larger in RF than those in VL.
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Strength of the similarity and time lag between the iEMG and blood volume sequences in RF and VL are assessed by cross-correlation analysis over the duration of the task (Fig. 3). In the RF, the normalized CCF showed a negative peak value in the phase of 53 ± 6 and 56 ± 4 s for early and later stages, respectively. This indicates that the increase (or decrease) in iEMG occurred 50–60 s before the decrease (or increase) in blood volume (Fig. 3, top). Furthermore, the negative peak value of the normalized CCF in the later stage was -0.72 ± 0.09, which was significantly (P < 0.05) lower than that in the early stage (-0.29 ± 0.06). In contrast, a distinct sharp peak of the normalized CCF was not observed for the VL in either stage and the lowest value was approximately -0.25 (Fig. 3, bottom).
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From each subject, two epochs of dramatic changes in iEMG are randomly extracted for the duration of 240 s: one in which EMG activity switched from VL to RF (case I in Fig. 4A) and the other in which the converse occurred (case II in Fig. 4B). iEMG and blood volume are aligned to the time of abrupt change in iEMG of RF (Fig. 1, dashed lines). In both epochs, the inverse relation between iEMG and blood volume was found only in the RF with some delay but not in VL. In case I, the blood volume significantly decreased 62.5 s after iEMG started to increase. In case II, however, the increase in blood volume was followed by a decrease in iEMG with shorter time delay (27.5 s) compared with case I. In VL, the change in iEMG was small, and the blood volume was almost constant in both cases.
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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Negative correlation between local circulation and muscle activity. The alternate muscle activity of the knee extensors emerged during sustained contraction at 2.5% of MVC for 60 min (Fig. 2), and this is consistent with the reports by Sjøgaard et al. (37), who employed 5% of MVC. In the present study, we focused on the local circulation of the individual synergistic muscles in relation to the alternate muscle activity. As a result, blood volume fluctuated rather than maintaining a constant value throughout the sustained contraction. Cross-correlation analysis clearly demonstrated that blood volume sequence was negatively correlated with iEMG sequence. This negative correlation indicates that iEMG increases with the decrease in blood volume or that iEMG decreases with the increase in blood volume. It was shown that, during prolonged contraction at 5% of MVC, blood flow in the femoral vein was maintained, on average (38). Closer examination of their data, however, tells us that the variation of the blood flow was progressively increased to a great extent as the exercise prolonged. On the basis of the present results, local circulation of blood may be modulated by the alternate muscle activity even during low-level sustained contraction at 2.5% of MVC.
The possibility for regional temporal hypoperfusion of the blood during low-level isometric contraction has been reviewed by Rowell (22). Although the mean intramuscular pressure seems to be well below systolic, diastolic, or mean arterial pressure during low-level contraction (32, 38), spatial distribution of intramuscular pressure is complex depending on the architecture of the muscle (muscle fiber orientation, thickness, curvature of the fibers) (31). The major effect of the intramuscular pressure during low-level contraction is thought to be venous compression, which would be expected to impede blood flow (22). In addition, impedance to flow may be caused not only by the effect of the compression on vascular radius and resistance but also by the twisting of arteries (14). The femoral venous blood flow at 15% of MVC is already reduced below the highest flow at 5% of MVC (38). Marked postcontraction hyperemia after 10–15% of MVC (38, 42) would suggest that blood flow was low because the contraction had caused a hypoperfusion relative to metabolic rate somewhere within the quadriceps muscle. In the present study, iEMG of RF reached above 20% of iEMGmax during the alternate muscle activity and close relations have been shown between EMG and intramuscular pressure during fatiguing exercise (8, 25). Thus the negative correlation between the muscle activity and blood volume of the RF may be interpreted as follows: the blood supply to the working regions fluctuated as a result of the dramatic increase or decrease in the muscle activity and consequent changes in the intramuscular pressure even during low-level sustained contraction at 2.5% of MVC.
It is of interest that a clear negative correlation between the iEMG and blood volume sequences was found in only RF but not in VL (Fig. 3). There are three major possibilities that may be related to the different results between these muscles: 1) larger changes in muscle activity, 2) higher muscle force, and 3) higher fatigability in RF.
The larger changes in muscle activity in RF were evident from the comparison of changes in iEMG and the coefficient of variation of iEMG (Table 1). The maximum change of iEMG relative to the onset value amounted to 25 times in RF, whereas it was only 3–5 times in vasti muscles. Despite the low-level contraction at 2.5% of MVC, iEMG of RF amounted to in excess of the values above 20% of iEMGmax. In contrast, iEMG was always <20% of iEMGmax in VL or VM. The coefficient of variation of iEMG, an index of the fluctuations of muscle activity, was also considerably larger in RF than that in VL or VM. These results suggest that the larger change in the muscle activity of RF than vasti muscles during sustained contraction at 2.5% of MVC alters the local circulation of the RF.
Intramuscular pressure depends on the muscle fiber force and differences in the muscle force per physiological cross sectional area (force/PCSA) of each muscle head reflect the differences in the muscle fiber force. From the previous studies on young Japanese with similar physical characteristics and MVC to the present subjects, PCSA of each muscle head can be estimated as 230–238% for VL, 154–159% for VM, and 171–185% for vastus intermedius (VI) compared with RF (1, 2). Alternate muscle activity is not observed between the VL and VM (19), and most of the VI is fused to the VL (43, 44). Hence alternate muscle activity is likely to emerge between the RF and all of the vasti muscles. On the basis of this information, compared with the force/PCSA of RF during the condition in which only the RF is active, the force/PCSA of vasti muscles (VL, VM, and VI) would be 17.2–17.7% during the condition in which only the vasti muscles are activated (even if the activity of VI is neglected, the force/PCSA of VL and VM would be 23.6–24.6% compared with RF). Thus the marked difference in the muscle fiber force between RF and other synergists may have induced heterogeneity of intramuscular pressure and thus the heterogeneity of the local circulation among the knee extensor synergists even during low-level sustained contraction.
During sustained low-level contraction in which EMG activity increases with time, the increase in EMG activity matches the increase in the intramuscular pressure (8, 25). The increase in EMG activity is regarded as a measure of muscle fatigue, i.e., decline in the ability of muscle of motor unit to produce force. Hence some process that occurs in concurrent with the development of muscle fatigue has been discussed as a possible cause of the increased intramuscular pressure. Accumulation of intramuscular water, which was observed during knee extension at 5% of MVC (36), was suggested other than the effect of increased motor unit activity (8). In the present study, MVC force was decreased by 15%. It is of note that RF is more susceptible to muscle fatigue compared with VL and VM (17, 33, 41). Thus it is possible that the enhanced negative relation between iEMG and blood volume of RF in the later stage is related to the development of fatigue. With these points taken into account, it is most likely that the negative correlation of normalized CCF between iEMG and blood volume observed in only the RF is attributable to the divergence of the force levels and the fatigue state among the knee extensor muscles during sustained contraction at 2.5% of MVC.
Time lag between iEMG and blood volume. In the RF muscle, the cross-correlation analysis resulted in the inverse relation between iEMG and blood volume sequences with a time lag of 50 s. This indicates that the local circulatory change generally occurs after 50 s of the fluctuations in muscle activity. To examine this time delay in more detail, the data of the two epochs of alternate muscle activity were further analyzed: data around the increase in iEMG of RF accompanied by the decline in iEMG of VL (case I) and vice versa (case II). In case I, blood volume of RF started to decrease 50–60 s after the onset of the increase in iEMG of RF. This is probably related to the slow development of muscle force in RF, which is implied by the slow development of iEMG of RF. From the presence of marked postcontraction hyperemia after 10–15% of MVC (38, 42), hypoperfusion somewhere within the quadriceps muscle is suggested to exist around this level of contraction (23). In the present study, it required 50 s for the iEMG of RF to exceed 15% of iEMGmax, on average. This amount of time may have been necessary for the muscle force and intramuscular pressure to be developed up to the level that could affect local blood circulation.
As the time proceeded with iEMG of RF maintained as high as 15–20% of iEMGmax, it is possible that muscle sympathetic nerve activity was enhanced. Responses in muscle sympathetic nerve activity depend not only intensity of exercise but also on exercise mode, and they are enhanced in accordance with the development of fatigue as well as the local sensation of fatigue (26–28). During sustained knee extension at 20% of MVC, muscle sympathetic nerve activity increased by 83% (26). Seals and Enoka (28) showed that the increase in muscle sympathetic nerve activity was related to the increase in EMG activity during sustained contraction, which was regarded as the index of fatigue. They further found that muscle sympathetic nerve activity was enhanced due to the prior fatiguing exercise and claimed the physiological link between EMG activity and muscle sympathetic nerve activity. Furthermore, increase in muscle sympathetic nerve activity is related to local sensation of fatigue during prolonged contraction (26, 27). Although it was anecdotal, subjects in the present study reported increased local sensation of fatigue in the RF when its iEMG was high. Thus it is likely that increase in muscle sympathetic nerve activity was developed when iEMG of RF was high. In case II, when iEMG of RF dropped, there was a time delay for the blood volume to increase, although the amount of time was shorter compared with the delay for the decrease in case I. If muscle sympathetic nerve activity is enhanced, the delay in case I could be related to the delayed recovery of the muscle sympathetic nerve activity.
In conclusion, local circulation in the RF is modulated by the alternate muscle activity among the knee extensor synergists even during low-level sustained contraction.
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ACKNOWLEDGMENTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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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.
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REFERENCES |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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, RF; 
, VL; 
, VM. iEMG and blood volume expressed as the differences (
) from the reference value in which iEMG of RF abruptly changed (