Neuromuscular electrical stimulation causes excitation of the α-motoneuron, which propagates as an action potential into the muscle. A time lag between the onset of stimulation (or action potential discharge) and the development of force (or joint torque) is called electromechanical delay (EMD), reflecting not only an electrochemical process (synaptic transmission, propagation of action potential, Ca2+ release from the sarcoplasmic reticulum into the cytoplasm, and cross-bridge formation) but also a mechanical process, i.e., force transmission along the muscle fibers, aponeurosis, and tendon (6).
Recent studies have shown that EMD in electrically elicited contractions can be used for the assessment of elastic stiffness (12,13,21,38) and contractile fatigue (38) of human muscle-tendon unit in vivo. These studies have typically measured the total duration from the onset of electrical activity to the beginning of force development. The electrochemical process of EMD, however, precedes the onset of mechanical response, i.e., muscle contraction, and thus has no direct association with the elastic and contractile properties of the muscle-tendon unit. When one attempts to extract useful information from the measurement of EMD, two distinct processes, one before and one after the onset of muscle contraction, should be taken into consideration separately.
To our knowledge, there is currently no criterion standard approach for detecting the onset of muscle contraction. Although EMG has been widely used for determining the onset of electrical activity of muscle, it provides no direct information about the mechanical behavior of the muscle-tendon unit. To determine the onset of muscle contraction, we measured the mechanical vibration of the skin surface over the contracting muscle, called the surface mechanomyogram (27), with a high-sensitivity accelerometer (3,26). The acceleration of skin surface during electrically elicited muscle contraction has a frequency of up to 390 Hz (3), which is much higher than those of muscle force and motion signals. Given a sufficiently high sampling rate, the acceleration signal is therefore suitable for detecting the onset of electrically elicited muscle contraction that probably begins within a few milliseconds after the stimulation (5,15,25).
One factor that has been considered to influence the mechanical process of EMD is the joint angle reflecting the length of the muscle-tendon unit (10,23). Muraoka et al. (23) published an elegant ultrasonographic study showing that the EMD of medial gastrocnemius muscle was dependent on the ankle joint angle and increased with decreasing the tendon strain. They argued that the presence of slack (i.e., negative value of the tendon strain) at short muscle-tendon length would prolong the time for the mechanical force transmission, implying that the electrochemical process preceding the onset of muscle contraction was unaffected by the muscle-tendon length. However, as with most researchers, they measured only the total duration of EMD. It remains unknown whether the length change of the muscle-tendon unit in vivo affects the electrochemical process of EMD, whereas in vitro studies provided evidence that the muscle fiber length influenced the sensitivity of contractile proteins to Ca2+ (2,9), an important factor in the excitation-contraction coupling mechanism.
The purpose of this study was to determine the changes in the contribution of electrochemical and mechanical processes to EMD of the biceps brachii muscle over a wide range of elbow joint angles. For this purpose, the onset of muscle contraction and the beginning of muscle force development were independently determined by using the acceleration and force signals, respectively. The study hypothesis was that the electrochemical and mechanical processes of EMD were influenced differently by the changes in joint angle, reflecting different physiological mechanisms.
Ten healthy male volunteers participated in this study. Their mean (±SD) age, height, and body mass were 23.8 ± 3.6 yr, 173.9 ± 4.8 cm, and 67.3 ± 8.6 kg, respectively. All subjects were fully informed of the experimental procedure and purpose of this study, which conformed to the Declaration of Helsinki and were approved by the Ethics Committee for Human Experiments, University of Tokyo. Written informed consent was obtained from each subject before participation.
A schematic of the experimental setup used in this study is shown in Figure 1. The subject rested supine on a comfortable bed with his right arm attached to a custom-designed ergometer, shoulder abducted 90°, and forearm fully supinated. The ergometer was designed to measure the force produced by the elbow flexors at a wide range of elbow joint angles. A force transducer (LUR-A-100NSA1; Kyowa Electronic Instruments, Tokyo, Japan) incorporated in the ergometer was connected to an arm cuff attached to the wrist. The acceleration signal was obtained using a miniature, high-sensitivity uniaxial accelerometer with dimensions of 3.6 × 3.6 × 9 mm and a mass of 0.4 g (A3-10; SSK, Tokyo, Japan) secured on the belly of the biceps brachii muscle (at 60% of the upper arm length, i.e., the distance from the acromion process of the scapula and the lateral epicondyle of the humerus) with double-sided adhesive tape.
An electric stimulator (SEN-7203; Nihon Kohden, Tokyo, Japan) with a stimulus-isolation unit (SS-2185; Nihon Kohden) delivered a 0.5-ms rectangular pulse through two Ag-AgCl surface electrodes with a diameter of 10 mm. The stimulating electrodes were placed on the belly of the short head of the biceps brachii muscle with a 35-mm interelectrode distance, thereby activating only a target muscle (7,23,25). Supramaximal stimulation of the biceps brachii muscle, however, may activate antagonist the triceps brachii muscle because of "stimulus cross talk" (1). Moreover, our preliminary experiment showed that the supramaximal stimulation of the biceps brachii muscle also activated the median nerve innervating most of the wrist flexor muscles. Therefore, we used a submaximal stimulation, the intensity of which was just above the motor threshold of the biceps brachii muscle. The absence of stimulus cross talk was checked with an accelerometer (of the same type as used for detecting the onset of biceps brachii muscle contraction, see Figs. 1 and 2A) placed on the anterior aspect of the forearm (flexor carpi radialis muscle), as well as by careful visual inspection and palpation. In addition, we adopted a paired-pulse (12-ms interval) instead of a single-pulse stimulation to improve the visibility of contractile motion and signal-time curves without increasing the stimulus intensity.
For each subject, elbow joint angles at which the stimulation was applied were 40°, 50°, 60°, 70°, 80°, 90°, 100°, 110°, 120°, and 130° of elbow flexion (0° represents full extension). At each joint angle, the stimulation was repeated at least six times with an interval of 6 s, during which the acceleration and force signals amplified with an amplifier (6M84; NEC San-ei, Tokyo, Japan) were simultaneously recorded at 10 kHz by using a data acquisition system (PowerLab/16SP; ADInstruments, Bella Vista, Australia). To assess repeatability of the measurement, the subject underwent two experimental sessions, with a 10-min rest in between. The order of elbow joint angle in the first session was sequential from 130° to 40° of elbow flexion, whereas that in the second session was randomized.
After removing high-frequency noise of acceleration and force signals by using a zero-lag, digital low-pass filter with cutoff frequencies of 1 kHz and 400 Hz, respectively, four stimulation records at each joint angle were manually selected after visual inspection (Fig. 2A). These records were ensemble averaged from 100 ms before the stimulation onset indicated by an electrical output of the stimulus-isolation unit. The 100-ms data before the stimulation onset were used as the baseline.
The onsets of muscle contraction (determined by the accelerometer) and elbow flexion force development (determined by the force transducer) were defined as the respective first points where the signal exceeded the mean baseline value by two SD, which has been commonly used for detecting the onset of electrical and mechanical activities of muscle contraction (e.g., Mora et al.  and Taylor et al. ), for at least 10 consecutive data points. As shown in Figure 2B, we determined three time-delay parameters, the delay between the onset of stimulation and the onset of muscle contraction (T ec), the delay between the onset of stimulation and the onset of force development (EMD), and the difference between T ec and EMD (Tm). In this study, the reference point of EMD was the onset of stimulation rather than the onset of action potential discharge because the time taken for the propagation of action potential along the motor nerve was negligibly short when the stimulation was applied to the muscle belly (25).
The length of the biceps brachii muscle-tendon unit (L) as a function of elbow joint angle (θ) was calculated from a musculoskeletal model (19,36):
where a and b are the distances between the rotational axis of the elbow joint and the insertion and origin, respectively, of the biceps brachii. In the present study, a is assumed to be 18% (19,36) of the forearm length (the distance between the styloid apophysis and the epitrochlea-epicondyle axis of the elbow), and b is assumed equal to the upper arm length.
Data are expressed as means and SD. Statistical analysis was performed with R software version 2.11.1 (http://www.r-project.org/) and Microsoft Office Excel 2007 (Microsoft, Redmond, WA). The test-retest reliability of the measurement was evaluated in terms of an intraclass correlation coefficient (ICC: type 2, 1) and a coefficient of variation. A one-way ANOVA with repeated measures was used to test whether the main effect of elbow joint angle was statistically significant. When a significant effect was found, Student's paired t-test with Bonferroni correction was performed as a post hoc analysis for multiple comparisons. Regression analysis was used to test whether the time delay for mechanical force transmission, Tm, was linearly related to the length of the muscle-tendon unit, as suggested previously in medial gastrocnemius muscle (23). P < 0.05 was considered significant.
At each joint angle, electrical stimulation of the biceps brachii elicited highly repeatable contractions with nearly identical acceleration and force traces (Fig. 2A). In addition, the test-retest reliability of the measurement with different orders of elbow joint angle was high in T ec (ICC = 0.88, 95% confidence interval = 0.83-0.92), EMD (ICC = 0.85, 95% confidence interval = 0.75-0.91), and Tm (ICC = 0.84, 95% confidence interval = 0.73-0.90). The within-subject coefficients of variation in two successive experimental sessions were 4.5% (range = 0-35%), 6.1% (range = 0.3-22%), and 8.0% (range = 0-27%) in T ec, EMD, and Tm, respectively. Accordingly, the mean values on the two experimental sessions were used for further statistical analysis.
Figure 3 shows the overall results of each time parameter determined at 10 different elbow joint angles. The one-way ANOVA revealed a significant main effect of elbow joint angle in EMD (F 9,81 = 45.7, P < 0.001) and Tm (F 9,81 = 52.3, P < 0.001) but not in T ec (F 9,81 = 0.77, P = 0.64). The post hoc analysis indicated that both EMD and Tm were significantly greater at elbow flexion positions (EMD = 100°-130°, Tm = 90°-130°) when compared with those at the most extended position in this study (40°). The values of EMD and Tm ranged from 11.3 ± 1.5 and 7.9 ± 1.6 ms, respectively, to 23.1 ± 5.5 and 19.6 ± 5.0 ms, respectively.
Figure 4 shows the relation between Tm and the muscle-tendon length of the biceps brachii normalized with its slack length (L 0), i.e., the length at which muscle-tendon unit develops passive force when being stretched. We arbitrarily assumed L 0 to be equal to the length at an elbow joint angle of 90°, at which the significant increase in Tm was first observed when compared with the most extended elbow position (Fig. 3). In fact, the relation between Tm and the muscle-tendon length was clearly biphasic, the breakpoint of which seemed close to L 0 we assumed. Therefore, only the data set below L 0 was included in the regression analysis. The data from all subjects were pooled for the regression because of the limited sample size in each individual (n = 4). The result indicated that Tm significantly increased with decreasing the muscle-tendon length (R 2 = 0.54, P < 0.001).
EMD represents a series of complex processes of converting an electrical stimulus to a mechanical response, thus being affected by several factors such as fatigue (38,39), age (12,38), contraction modality (6,14,40), muscle-tendon strain (23), myotonic dystrophy (26), and tendon harvesting (30). Previous studies have taken a variety of approach for measuring EMD and sometimes used different terminology such as force time (37) and total response time (40) to refer to the time lag between the onset of electrical activity (or electrical stimulus) and the beginning of force (or torque) development. Therefore, no consensus has emerged as to what is the most reliable approach for the assessment of EMD in human muscle contractions. In the present study, we measured EMD in electrically elicited, submaximal contractions, because 1) the electrical stimulation induced highly repeatable contractions as shown in Fig. 2A, 2) the influences of synergists and antagonists were negligible, and 3) the onset of stimulation, the reference point for EMD, could be determined without setting any arbitrary threshold.
To minimize the effect of stimulus cross talk, i.e., the activation of muscles other than the target muscle, we used a submaximal paired-pulse stimulation with the intensity just above the motor threshold of the biceps brachii muscle, the resultant peak force of which was quite small, up to 7.5% of maximal voluntary elbow flexion force. Therefore, it is reasonable to assume that the stimulus cross talk was minimized. A major limitation for the use of submaximal stimuli is that the motor units activated are localized superficially and may vary with different elbow joint angles. We believe, however, that the superficial and variable activation of motor units due to submaximal electrical stimulation would not substantially affect the values of EMD because of the following reasons. First, surface electrical stimulation is considered to involve a random recruitment of motor units, activating both slow and fast motor units even at relatively low force levels (11,17). Second, because most human muscles including the biceps brachii muscle express a mosaic arrangement of slow- and fast-twitch fibers (16), the local, superficial stimulation is probably sufficient to activate both slow- and fast-twitch fibers. Third, previous studies have used various stimulus intensities (up to supramaximal intensity) for the assessment of EMD, the values of which fall within a relatively narrow range (7-30 ms) (13,14,21,23,25,35,40) when compared with those in voluntary contractions (9-130 ms) (4,6,14,30,37,40). In fact, our values of EMD (ranging between 11.3 ± 1.5 and 23.1 ± 5.5 ms) are in good agreement with these published values in electrically elicited contractions.
Although the onset of electrically elicited muscle contraction has been determined by a condenser microphone (5,15) as well as accelerometer (3,26) and more recently by ultrasonography (7,25,28), the results in the literature are inconsistent. The studies using condenser microphone and accelerometer have reported the latency between the onset of electrical stimulation (or action potential in Bolton et al.  and Orizio et al. ) and the first sign of mechanical activity to be 1-6 ms, which is similar to T ec in the present study (ranging between 3.1 ± 0.8 and 3.5 ± 0.9 ms). On the other hand, ultrasonographic studies have reported a relatively large and variable time lag (6-37 ms) between the onset of stimulation and the beginning of tissue motion, which, however, may include the time required for the force transmission from the muscle to the tissues examined, such as patella (7) and tendon (25). Part of this time lag may also be accounted for by several limitations inherent in the ultrasonographic measurement, including the internal time delay (28), the data processing for fine motion detection (7,25,28), and the limited time resolution of typically 3-10 ms (7,28). In particular, the limited time resolution seems to be critical because the synaptic transmission and the excitation-contraction coupling, important mechanisms for the electrochemical process of EMD, are completed within a few milliseconds (18,31). In fact, a recent study using very high frame rate (4 kHz) ultrasound has detected the muscle fascicle motion only 5-7 ms after the stimulation of medial gastrocnemius muscle (25). These values are much closer to our results of T ec than to those reported by the other ultrasonographic studies, although a small but measurable difference of approximately 3 ms remains unclear and merits further investigation.
To our knowledge, no study has examined whether the electrochemical process of EMD is affected by the joint angle or muscle-tendon length in vivo. Single-fiber studies have shown an increase in the sensitivity of contractile proteins to Ca2+ as sarcomere length is increased over the ascending limb and plateau of the force-length relation (2,9), at which in vivo the biceps brachii muscle is considered to operate (24). Accordingly, it is reasonable to expect that at elbow extension position, a low concentration of Ca2+ is sufficient to induce the contraction of the biceps brachii muscle, which should manifest as the shortened T ec. Contrary to our expectation, T ec was almost independent of elbow joint angle. Because the series elastic component, along which the force produced by the contractile component is transmitted, originates not only from the tendon structures but also from cross bridges within the sarcomere, it is theoretically possible that T ec measured in the present study includes the time for force transmission within the sarcomere. Nevertheless, the time required for the completion of synaptic transmission and excitation-contraction coupling (18,31) is in good agreement with T ec. We thus believe that the force transmission within the sarcomere accounts for only a small fraction of the process before the onset of muscle contraction, as discussed elsewhere (25).
In the present study, the first sign of mechanical response to electrical stimulation was typically a small negative (inward) deflection of skin surface detected by the accelerometer on the biceps brachii, as shown in Figure 2A. This phenomenon has been previously reported and interpreted as the "transverse latency relaxation" (3,15), probably reflecting the passive elongation of muscle fibers underneath the contact sensor due to the early shortening of muscle fibers near the motor point (22). Considering the propagation velocity of the negative deflection is very high when compared with the apparent velocity of action potentials (22), we can assume that the onset of muscle contraction measured with the accelerometer represents the mechanical activity of the first activated muscle fibers. It should be acknowledged, however, that T ec in the present study may depend not only on Ca2+ sensitivity of contractile proteins but also on the distance between the accelerometer and the first activated fibers, which varies with elbow joint angles as well. To assess the confounding effect of accelerometer location on the values of T ec, future studies should use multiple accelerometers to detect the vibration of the different portions of the muscle.
The time lag between the onset of muscle contraction and the beginning of force development, Tm, corresponds to a mechanical process of EMD and is considered the time for the force transmission along the series elastic component of the muscle-tendon unit (25). Despite the interindividual variability shown in Figure 4, the regression analysis revealed that, at the muscle-tendon length below L 0, Tm significantly increased with decreasing the muscle-tendon length (R 2 = 0.54, P < 0.001). When the muscle-tendon unit was stretched beyond L 0, on the other hand, Tm seemed independent of muscle-tendon length because neither T ec nor EMD showed any length-dependent changes. Although the causes of interindividual variability of Tm remain unclear, possible explanations include differences in viscoelasticity, real slack length, and contractile properties of the biceps brachii muscle. The results are consistent with the previous observation on human medial gastrocnemius muscle (23), suggesting that the increase in EMD at short muscle-tendon length corresponds to the time required for the muscle to take up the slack within the muscle-tendon unit. Therefore, Tm measured in the present study is likely to be a function of the extent of slack and the shortening velocity of the fastest muscle fibers (because these fibers should initially take up the slack), as indicated by both in vitro (8) and in vivo (32,33) experiments.
By using a reciprocal of the regression slope of length-time relation sh own in Figure 4, we calculated the shortening velocity of the biceps brachii muscle, assuming a constant ratio of muscle fascicle and muscle-tendon lengths (14.5/32.8, adopted from Murray et al. ). The resultant value, 17.2 fascicle length per second, is in good agreement with the maximal shortening velocity of fast-twitch skeletal muscles in rats (11.9-20.6 fiber length per second ) measured at a physiological temperature (35°C). This suggests that the shortening velocity of muscle taking up the slack can be estimated from the relation between the muscle-tendon length and Tm, the value of which will represent the maximal velocity of the fastest fibers activated. Nevertheless, there should be some difference in shortening velocity between rat and human muscles because of the difference in species (20) as well as method used.
In conclusion, our results suggest that, in the human biceps brachii muscle, the prolongation of EMD at short muscle-tendon length is not attributed to the impairment of the electrochemical process of muscle contraction but to the increased slack within the muscle-tendon unit. The separation of electrochemical and mechanical process of EMD over a wide range of joint angles may provide useful physiological information on the human muscles in vivo, including excitation-contraction dynamics and intrinsic shortening velocity that can be altered in response to fatigue, exercise training, and aging.
This study was supported by a Grant-in-Aid for Scientific Research, Japan (18300217 to N.I. and 19800010 to K.S.).
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the article.
The authors thank Yukie Tomioka for her assistance with data collection and Kazunori Sasaki for his help with producing Figure 1.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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