Muscle activation and force production are dependent on the type of contraction and the velocity of movement. For a given external load, concentric actions generate greater motor unit activity compared with eccentric actions; however, greater maximal forces can be produced with eccentric actions (19). Increasing the speed of concentric actions has been associated with greater electromyographic (EMG) activity and increased metabolic demand compared to slower speeds (15). In contrast, studies have identified that EMG activity during eccentric exercise does not vary with speed of contraction (7,15,16). These findings imply that the increase in force producing capacity during fast eccentric actions is primarily the result of the viscoelastic properties of the series and parallel components of muscle and not necessarily the result of increased motor unit recruitment.
The structure and physiology of a muscle also can influence recruitment patterns, which suggests agonists may respond to various loading conditions nonhomogeneously. For example, increasing speed of the eccentric component of exercise has been advocated to facilitate fast twitch muscle fiber recruitment (i.e., plyometrics) (12,13,14), whereas slow eccentric activation is believed to preferentially recruit slow twitch stabilizing muscles (21,22). In addition, fusiform muscles are typically two-joint muscles and are recruited during phasic contractions, whereas multi-pennate muscles are usually one-joint muscles and are recruited during tonic (stabilizing) contractions (27). To date, there have been no controlled studies looking at the effects of various speeds of eccentric activation on agonist muscles that vary structurally and physiologically. To gain insight into eccentric activation patterns in various muscles, a method assessing cumulative effects of several repetitions of resistive exercise would appear to be necessary.
Recently, magnetic resonance imaging (MRI) has been used to assess cumulative muscle activity by comparing pre- and post-exercise signal intensity (4,5,8,9–11,20,24). Among the causes of MRI signal intensity changes are T2 relaxation times, which are highly influenced by the muscle’s water content (6,10). Fluid exchange between vasculature and extracellular space decreases during muscle contraction and increases immediately after contraction (4,26). It is this postcontraction fluid exchange that is captured by MRI signal intensity. MRI signal intensity increases with both exercise intensity and duration, and is greater with dynamic exercise compared to static exercise (23). Adams et al. (1) reported that the transverse relaxation time (T2) was correlated with EMG activity of both concentric and eccentric actions during elbow flexion under varying loads.
An advantage of assessing muscle activation using MRI compared with EMG is that axial plane imaging allows simultaneous visualization of signal intensities between adjacent muscles (25). In addition, the signal inconsistencies of EMG resulting from electrode placement, subcutaneous fat, skin resistance, and contamination of signal because of “muscle crosstalk” can be avoided. Furthermore, MRI allows for cumulative assessment of an exercise session by comparing the pre- and post-exercise signal intensity, whereas EMG is representative of muscle activity only while the muscle is active.
Given the ability to assess muscle recruitment patterns using MRI, the purpose of this study was to compare signal intensity changes in the primary elbow flexors (biceps brachii and brachialis) while performing two isotonic exercise protocols varying in the velocity of the eccentric component. As a result of predominantly fast twitch fiber composition and its fusiform structure, we hypothesized that the biceps brachii would be recruited more than the brachialis during the fast eccentric protocol. Conversely, we hypothesized that the brachialis would be more active during the slow exercise protocol. Information gained from this study will provide insight into muscle activation specificity and assist in optimal exercise prescription.
METHODS
Subjects.
Twelve healthy adult males participated in this study. The average age, weight, and height of the subjects was 28.8 ± 6.1 yr, 70.2 ± 8.5 kg, and 181.4 ± 8.9 cm, respectively. Subjects were excluded from this study if they had an orthopedic or neurologic disorder, which precluded them from completing the exercise protocol. In addition, subjects were excluded if there were precautions and contraindications for MRI (i.e., cardiac pacemaker, central aneurysm clips, cardiac valve replacement, metal pins, metal prosthesis, removable dentures, or nerve stimulators) (25). At the time the study was conducted, all subjects were participating in regular strength training, which included free-weight exercises. Before participation, all subjects provided written informed consent according to a protocol approved by the Institutional Review Board and Health Research Association of the University of Southern California.
Exercise protocols.
Subjects performed two isotonic exercise protocols (elbow flexion), which were randomly assigned to each arm. The protocols were similar with respect to workload and total time of exercise (144 s) but varied in time of the eccentric component (see Table 1). The workload for both protocols was set at 60% of each subject’s one repetition maximum (1RM), which was established 3–4 d before the study. For the fast protocol, the eccentric component was 2 s in duration, whereas the eccentric component for the slow protocol was 10 s in duration. To ensure that the total time for both protocols was similar, the first protocol consisted of three sets of 12 repetitions (N = 36), whereas the slow protocol consisted of three sets of four repetitions (N = 12) (Table 1). The rest time between sets was 1 min. The selection of time, repetition, and sets was chosen to mimic common workout regimens.
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Table 1: Exercise protocol parameters.
MRI.
MRI was performed using a 1.5T MRI system (General Electric Medical Systems, Milwaukee, WI). Transaxial images of the arm were obtained using a fast inversion recovery pulse sequence at a repetition time (TR) of 2500 ms, echo time (TE) of 90 ms, and inversion time (TI) of 140 ms. The transaxial slice thickness was 1.5 cm with a field of view (FOV) of 20 × 20 cm and imaging matrix of 256 × 192. Total imaging time was 2 min.
Procedures.
Before performing each exercise protocol, baseline muscle signal intensities were established. Subjects were positioned supine with two 5-inch circular coils arranged as a dual array on both sides of the extended upper arm. A small glass vial containing iodine was taped perpendicular to the lateral aspect of the arm, two-thirds the distance from the acromion to the lateral epicondyle of the humerus. This marker referenced the slice used for signal analysis. A second marker, a 4-inch vial containing saline was placed in the center of the coil, parallel to the arm, to serve as a signal intensity reference.
After the initial MRI assessment on one arm, subjects performed the randomly assigned exercise protocol. Biceps curls were performed while each subject was standing with his back supported against a wall. The time of each repetition was monitored by one of the investigators using a stopwatch. Upon completion of the exercise protocol, the subjects quickly assessed their perceived exertion using the modified rate of perceived exertion (RPE) scale (2). MRI assessment (using procedures described for the initial scan) was repeated immediately after the exercise protocol.
The elapsed time before starting the second protocol on the opposite arm was approximately 15 min. The exact MRI and exercise procedures (as described above) were utilized. After testing, subjects were asked to report any delayed onset muscle soreness (DOMS) in either arm, 24 and 48 h after testing.
Data analysis.
The image representing the cross-section of the upper arm, two-thirds the distance from the acromion to the lateral epicondyle of the humerus, was displayed on the MRI console. A circular cursor that measured 150 mm2 was used to assess the signal intensity at the region-of-interest (ROI). Because the tissues shown in the MRI image are not homogeneous, cursor placement was carefully focused on the muscle of interest while avoiding fat, fascia, and vessels. The signal intensity was evaluated within a representative ROI for the biceps brachii and brachialis using the imager software (GE System). The same investigator analyzed all MRI data.
A unique feature of the GE system software is that image contrast is maximized to ensure that various tissues can be differentiated. This “auto-scaling” function can influence signal intensity substantially so that an obvious increase in signal intensity (postexercise) could be measured as being less than preexercise. This would occur if a structure in the field of view (i.e., blood vessel) demonstrated very high signal intensity.
To control for the auto-scaling feature of the GE system software, all signal intensities were normalized to the maximal signal intensity present at the analyzed slice. The overall change in signal intensity was assessed using the following equation:MATHwhere N = muscle signal intensity/maximal signal intensity. The maximal signal intensity from each image was typically associate with a blood vessel, or the saline or iodine external markers.
Statistical analysis.
To compare signal intensity between the biceps brachii and brachialis across both exercise protocols, a 2 × 2 ANOVA (muscle × protocol) with repeated measures was used. Main effects were reported; however, if a significant interaction was found, post hoc analyses were performed. The level of perceived exertion was compared between protocols using a two-tailed t-test. DOMS was reported descriptively as the percentage of subjects reporting soreness in comparison to all subjects.
An alpha level of 0.05 was used for all analyses. Minitab (Minitab, Inc., State College, PA) statistical software was used for all analyses.
RESULTS
Both exercise protocols implemented in this study successfully activated biceps brachii and brachialis in all subjects (Fig. 1). There was no significant difference in signal intensity between the two protocols when collapsed across both muscles (no protocol effect). Similarly, there was no difference in signal intensity between the biceps and brachialis when collapsed across protocols (no muscle effect). There was however, a significant muscle × protocol interaction, indicating that the biceps brachii and brachialis signal intensities were not consistent across both protocols (Table 2). Post hoc analyses revealed that the biceps brachii had a significantly higher signal intensity change after the fast exercise protocol compared with the brachialis (P < 0.05), whereas the brachialis had a significantly higher signal intensity change after the slow exercise protocol (P < 0.05) (Fig. 2).
Figure 1: Representative axial fast inversion recovery MRI of mid-arm at pre- and post-fast isotonic exercise protocol.
Table 2: Summary of analysis of variance for change in muscle (biceps brachii and brachialis) signal intensity during two exercise protocols (fast and slow).
Figure 2: Mean increase in signal intensity of biceps brachii (BB) and brachialis (B) during the fast and slow exercise protocols.
There was a significant difference in the RPE between the two protocols. On average, the RPE for the fast protocol was 8.3 ± 2.1 and 5.4 ± 1.5 for the slow protocol. Similarly, 7 of the 12 subjects (58%) reported DOMS in the arm that performed the fast exercise, whereas none of the subjects reported DOMS in the arm that performed the slow exercise protocol.
DISCUSSION
The results of this study found that there were no significant differences in overall flexor muscle activity (biceps brachii and brachialis combined) between the fast and slow protocols. There was, however, a significant muscle and protocol interaction indicating that individual muscle activity varied depending on the protocol. During the fast protocol, the change in signal intensity of the biceps brachii increased 1.7 times and the change in signal intensity of the brachialis increased by 0.9. In contrast, during the slow protocol, there was a significantly greater increase in activity of the brachialis, which increased 1.5 times, compared with the 0.8 signal intensity increase of the biceps brachii.
The varied muscle activation between the two protocols may be explained on the basis of anatomic and physiologic differences between the two muscles. From an anatomical standpoint, it is logical that the biceps would be more active during the fast protocol since this muscle is capable of large amounts of shortening and quick movements as a result of its two-joint fusiform structure (27). In contrast, the brachialis is a single joint, multipennate muscle and is more likely to contribute to slow movement and joint stabilization. From a physiological perspective, the biceps brachii is comprised of predominantly fast twitch muscle fibers (57.7% Type II), which also explains why this muscle was more active during fast protocol. The fiber type of the brachialis has never been reported; however, evidence exists suggesting that this muscle may contain less Type II fibers than the biceps (17).
Apart from the varied muscle recruitment patterns, there were subjective differences between the two protocols. On the average, the isotonic exercise with the slower eccentric component was perceived as 35% less strenuous and did not produce DOMS despite the longer eccentric activation time. These findings suggest that it might be beneficial to decrease the velocity of the eccentric component of isotonic exercise, and by doing so, avoid DOMS and improve compliance to the exercise program.
The results of this study would appear to have implications with respect to exercise prescription for fitness and rehabilitation (3). If the goal of an exercise is to recruit muscles capable of explosive movement, it would appear that fast eccentric loading should be implemented. In contrast, recruitment of joint stabilizers would appear to require slow eccentric loading. Slower exercise speeds, especially those associated with eccentric activity, are often implemented in early stages of rehabilitation (18). A slower eccentric speed should allow for more conscious movement reeducation and less rapid loading of the tendon and the musculotendinous junction, thereby decreasing the potentially injurious effects of repetitive movement. This premise is supporting the finding that the slow protocol did not elicit DOMS.
In the current investigation, the use of MRI was found to be sensitive enough to quantify muscle activation patterns between protocols. EMG, whether surface or wire, would permit only selected insight into the muscle’s activity in real time. Furthermore, EMG assesses electrical activity from muscle fibers that are nearest to the recording electrode. Therefore, the use of MRI may provide a better means for a global assessment of changes occurring in muscles and muscle groups as a result of exercise. Previous EMG studies have shown no difference in muscle recruitment patterns when the speed of eccentric contraction was varied (15), suggesting that MRI may be a more sensitive measure to explore this phenomenon.
A limitation of this study was the fact that the exercise protocols were not specific to one type of contraction but included both concentric and eccentric actions. Although we attempted to control for the confounding effects of the concentric components by maintaining a constant velocity between the two protocols, further studies may consider only eccentric actions. In addition, care must be made in generalizing the results of this study to the entire population as only young male adults were studied. Whether or not the results presented in this study would be evident in different populations remains to be seen.
SUMMARY
The results of this study found that the biceps was preferentially recruited during the fast eccentric isotonic protocol, whereas the brachialis was preferentially recruited during the slow eccentric isotonic protocol. These findings appear to be related to the structural and physiological differences between the two muscles. These findings appear to have implications with respect to exercise prescriptions for specific muscles.
Address for correspondence: Kornelia Kulig, Ph.D., P.T., Department of Biokinesiology and Physical Therapy, University of Southern California, 1540 E. Alcazar Street, CHP-155, Los Angeles, CA 90033; E-mail [email protected]
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